Factors Associated With COVID-19 Disease Severity in US Children and Adolescents

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Factors Associated With COVID-19 Disease Severity in US Children and Adolescents

The COVID-19 pandemic has led to more than 40 million infections and more than 650,000 deaths in the United States alone.1 Morbidity and mortality have disproportionately affected older adults.2-4 However, acute infection and delayed effects, such as multisystem inflammatory syndrome in children (MIS-C), occur and can lead to severe complications, hospitalization, and death in pediatric patients.5,6 Due to higher clinical disease prevalence and morbidity in the adult population, we have learned much about the clinical factors associated with severe adult COVID-19 disease.5,7-9 Such clinical factors include older age, concurrent comorbidities, smoke exposure, and Black race or Hispanic ethnicity, among others.5,7-10 However, there is a paucity of data on severe COVID-19 disease in pediatric patients.5,11,12 In addition, most immunization strategies and pharmacologic treatments for COVID-19 have not been evaluated or approved for use in children.13 To guide targeted prevention and treatment strategies, there is a critical need to identify children and adolescents—who are among the most vulnerable patient populations—at high risk for severe disease.

Identifying the clinical factors associated with severe COVID-19 disease will help with prioritizing and allocating vaccines when they are approved for use in patients younger than 12 years. It also can provide insight for clinicians and families faced with decisions wherein individual risk assessment is crucial (eg, in-person schooling, other group activities). The objective of this study was to determine the clinical factors associated with severe COVID-19 among children and adolescents in the United States.

METHODS

Study Design

We conducted a multicenter retrospective cohort study of patients presenting for care at pediatric hospitals that report data to the Pediatric Health Information System (PHIS) database. The PHIS administrative database includes billing and utilization data from 45 US tertiary care hospitals affiliated with the Children’s Hospital Association (Lenexa, Kansas). Data quality and reliability are ensured through a joint validation effort between the Children’s Hospital Association and participating hospitals. Hospitals submit discharge data, including demographics, diagnoses, and procedures using International Classification of Diseases, 10th Revision (ICD-10) codes, along with daily detailed information on pharmacy, location of care, and other services.

Study Population

Patients 30 days to 18 years of age discharged from the emergency department (ED) or inpatient setting with a primary diagnosis of COVID-19 (ICD-10 codes U.071 and U.072) between April 1, 2020, and September 30, 2020, were eligible for inclusion.14 In a prior study, the positive predictive value of an ICD-10–coded diagnosis of COVID-19 among hospitalized pediatric patients was 95.5%, compared with reverse transcription polymerase reaction results or presence of MIS-C.15 The diagnostic code for COVID-19 (ICD-10-CM) also had a high sensitivity (98.0%) in the hospitalized population.16 Acknowledging the increasing practice of screening patients upon admission, and in an attempt to minimize potential misclassification, we did not include encounters with secondary diagnoses of COVID-19 in our primary analyses. Pediatric patients with surgical diagnoses and neonates who never left the hospital were also excluded.

Factors Associated With Severe COVID-19 Disease

Exposures of interest were determined a priori based on current evidence in the literature and included patient age (0-4 years, 5-11 years, and 12-18 years), sex, race and ethnicity (non-Hispanic White, non-Hispanic Black, Hispanic, Asian, other non-White race [defined as Pacific Islander, Native American, or other]), payor type, cardiovascular complex chronic conditions (CCC), neuromuscular CCC, obesity/type 2 diabetes mellitus (DM), pulmonary CCC, asthma (defined using ICD-10 codes17), and immunocompromised CCC. Race and ethnicity were included as covariates based on previous studies reporting differences in COVID-19 outcomes among racial and ethnic groups.9 The CCC covariates were defined using the pediatric CCC ICD-10 classification system version 2.18

Pediatric Complications and Conditions Associated With COVID-19

Based on current evidence and expert opinion of study members, associated diagnoses and complications co-occurring with a COVID-19 diagnosis were defined a priori and identified through ICD-10 codes (Appendix Table 1). These included acute kidney injury, acute liver injury, aseptic meningitis, asthma exacerbation, bronchiolitis, cerebral infarction, croup, encephalitis, encephalopathy, infant fever, febrile seizure, gastroenteritis/dehydration, Kawasaki disease/MIS-C, myocarditis/pericarditis, pneumonia, lung effusion or empyema, respiratory failure, sepsis, nonfebrile seizure, pancreatitis, sickle cell complications, and thrombotic complications.

Outcomes

COVID-19 severity outcomes were assessed as follows: (1) mild = ED discharge; (2) moderate = inpatient admission; (3) severe = intensive care unit (ICU) admission without mechanical ventilation, shock, or death; and (4) very severe = ICU admission with mechanical ventilation, shock, or death.19 This ordinal ranking system did not violate the proportional odds assumption. Potential reasons for admission to the ICU without mechanical ventilation, shock, or death include, but are not limited to, need for noninvasive ventilation, vital sign instability, dysrhythmias, respiratory insufficiency, or complications arising from concurrent conditions (eg, thrombotic events, need for continuous albuterol therapy). We examined several secondary, hospital-based outcomes, including associated diagnoses and complications, all-cause 30-day healthcare reutilization (ED visit or rehospitalization), length of stay (LOS), and ICU LOS.

Statistical Analysis

Demographic characteristics were summarized using frequencies and percentages for categorical variables and geometric means with SD and medians with interquartile ranges (IQR) for continuous variables, as appropriate. Factors associated with hospitalization (encompassing severity levels 2-4) vs ED discharge (severity level 1) were assessed using logistic regression. Factors associated with increasing severity among hospitalized pediatric patients (severity levels 2, 3, and 4) were assessed using ordinal logistic regression. Covariates in these analyses included race and ethnicity, age, sex, payor, cardiovascular CCC, neurologic/neuromuscular CCC, obesity/type 2 DM, pulmonary CCC, asthma, and immunocompromised CCC. Adjusted odds ratios (aOR) and corresponding 95% CI for each risk factor were generated using generalized linear mixed effects models and random intercepts for each hospital. Given the potential for diagnostic misclassification of pediatric patients with COVID-19 based on primary vs secondary diagnoses, we performed sensitivity analyses defining the study population as those with a primary diagnosis of COVID-19 and those with a secondary diagnosis of COVID-19 plus a concurrent primary diagnosis of a condition associated with COVID-19 (Appendix Table 1).

All analyses were performed using SAS version 9.4 (SAS Institute, Inc), and P < .05 was considered statistically significant. The Institutional Review Board at Vanderbilt University Medical Center determined that this study of de-identified data did not meet the criteria for human subjects research.

RESULTS

Study Population

A total of 19,976 encounters were included in the study. Of those, 15,913 (79.7%) were discharged from the ED and 4063 (20.3%) were hospitalized (Table 1). The most common race/ethnicity was Hispanic (9741, 48.8%), followed by non-Hispanic White (4217, 21.1%). Reference race/ethnicity data for the overall 2019 PHIS population can be found in Appendix Table 2.

Characteristics of Children With COVID-19 Disease Who Were Evaluated at US Children’s Hospitals, April 1, 2020, to September 30, 2020

The severity distribution among the hospitalized population was moderate (3222, 79.3%), severe (431, 11.3%), and very severe (380, 9.4%). The frequency of COVID-19 diagnoses increased late in the study period (Figure). Among those hospitalized, the median LOS for the index admission was 2 days (IQR, 1-4), while among those admitted to the ICU, the median LOS was 3 days (IQR, 2-5).

Trends in COVID-19 Diagnoses

Overall, 10.1% (n = 2020) of the study population had an all-cause repeat encounter (ie, subsequent ED encounter or hospitalization) within 30 days following the index discharge. Repeat encounters were more frequent among patients hospitalized than among those discharged from the ED (Appendix Table 3).

Prevalence of Conditions and Complications Associated With COVID-19

Overall, 3257 (16.3%) patients had one or more co-occurring diagnoses categorized as a COVID-19–associated condition or complication. The most frequent diagnoses included lower respiratory tract disease (pneumonia, lung effusion, or empyema; n = 1415, 7.1%), gastroenteritis/dehydration (n = 1068, 5.3%), respiratory failure (n = 731, 3.7%), febrile infant (n = 413, 2.1%), and nonfebrile seizure (n = 425, 2.1%). Aside from nonfebrile seizure, neurological complications were less frequent and included febrile seizure (n = 155, 0.8%), encephalopathy (n = 63, 0.3%), aseptic meningitis (n = 16, 0.1%), encephalitis (n = 11, 0.1%), and cerebral infarction (n = 6, <0.1%). Kawasaki disease and MIS-C comprised 1.7% (n = 346) of diagnoses. Thrombotic complications occurred in 0.1% (n = 13) of patients. Overall, these conditions and complications associated with COVID-19 were more frequent in hospitalized patients than in those discharged from the ED (P < .001) (Table 2).

Conditions and Complications Associated With COVID-19

Factors Associated With COVID-19 Disease Severity

Compared to pediatric patients with COVID-19 discharged from the ED, factors associated with increased odds of hospitalization included private payor insurance; obesity/type 2 DM; asthma; and cardiovascular, immunocompromised, neurologic/neuromuscular, and pulmonary CCCs (Table 3). Factors associated with decreased risk of hospitalization included Black race or Hispanic ethnicity compared with White race; female sex; and age 5 to 11 years and age 12 to 17 years (vs age 0-4 years). Among children and adolescents hospitalized with COVID-19, factors associated with greater disease severity included Black or other non-White race; age 5 to 11 years; age 12 to 17 years; obesity/type 2 DM; immunocompromised conditions; and cardiovascular, neurologic/neuromuscular, and pulmonary CCCs (Table 3).

Factors Associated With Disease Severity in Children and Adolescents With COVID-19

Sensitivity Analysis

We performed a sensitivity analysis that expanded the study population to include those with a secondary diagnosis of COVID-19 plus a diagnosis of a COVID-19–associated condition or complication. Analyses using the expanded population (N = 21,247) were similar to the primary analyses (Appendix Table 4 and Appendix Table 5).

DISCUSSION

In this large multicenter study evaluating COVID-19 disease severity in more than 19,000 patients presenting for emergency care at US pediatric hospitals, approximately 20% were hospitalized, and among those hospitalized almost a quarter required ICU care. Clinical risk factors associated with increased risk of hospitalization include private payor status and selected comorbidities (obesity/type 2 DM; asthma; and cardiovascular, pulmonary, immunocompromised, neurologic/neuromuscular CCCs), while those associated with decreased risk of hospitalization include older age, female sex, and Black race or Hispanic ethnicity. Factors associated with severe disease among hospitalized pediatric patients include Black or other non-White race, school age (≥5 years), and certain chronic conditions (cardiovascular disease, obesity/type 2 DM, neurologic or neuromuscular disease). Sixteen percent of patients had a concurrent diagnosis for a condition or complication associated with COVID-19.

While the study population (ie, children and adolescents presenting to the ED) represents a small fraction of children and adolescents in the community with SARS-CoV-2 infection, the results provide important insight into factors of severe COVID-19 in the pediatric population. A report from France suggested ventilatory or hemodynamic support or death were independently associated with older age (≥10 years), elevated C-reactive protein, and hypoxemia.12 An Italian study found that younger age (0-4 years) was associated with less severe disease, while preexisting conditions were more likely in patients with severe disease.11 A single-center case series of 50 patients (aged ≤21 years) hospitalized at a children’s hospital in New York City found respiratory failure (n = 9) was more common in children older than 1 year, patients with elevated inflammatory markers, and patients with obesity.20

Our study confirms several factors for severe COVID-19 found in these studies, including older age,11,12,20 obesity,20 and preexisting conditions.11 Our findings also expand on these reports, including identification of factors associated with hospitalization. Given the rate of 30-day re-encounters among pediatric patients with COVID-19 (10.1%), identifying risk factors for hospitalization may aid ED providers in determining optimal disposition (eg, home, hospital admission, ICU). We also identified specific comorbidities associated with more severe disease in those hospitalized with COVID-19, such as cardiovascular disease, obesity/type 2 DM, and pulmonary, neurologic, or neuromuscular conditions. We also found that asthma increased the risk for hospitalization but not more severe disease among those hospitalized. This latter finding also aligns with recent single-center studies,21,22 whereas a Turkish study of pediatric patients aged 0 to 18 years found no association between asthma and COVID-19 hospitalizations.23We also examined payor type and racial/ethnic factors in our analysis. In 2019, patients who identified as Black or Hispanic comprised 52.3% of all encounters and 40.7% of hospitalizations recorded in the PHIS database. During the same year, encounters for influenza among Black or Hispanic pediatric patients comprised 58.7% of all influenza diagnoses and 47.0% of pediatric influenza hospitalizations (Appendix Table 2). In this study, patients who identified as Black or Hispanic race represented a disproportionately large share of patients presenting to children’s hospitals (68.5%) and of those hospitalized (60.8%). Hispanic ethnicity, in particular, represented a disproportionate share of patients seeking care for COVID-19 compared to the overall PHIS population (47.7% and 27.1%, respectively). After accounting for other factors, we found Black and other non-White race—but not of Hispanic ethnicity—were independently associated with more disease severity among those hospitalized. This contrasts with findings from a recent adult study by Yehia et al,24 who found (after adjusting for other clinical factors) no significant difference in mortality between Black patients and White patients among adults hospitalized due to COVID-19. It also contrasts with a recent large population-based UK study wherein pediatric patients identifying as Asian, but not Black or mixed race or ethnicity, had an increased risk of hospital admission and admission to the ICU compared to children identifying as White. Children identifying as Black or mixed race had longer hospital admissions.25 However, as the authors of the study note, residual confounders and ascertainment bias due to differences in COVID testing may have influenced these findings.

Our findings of differences in hospitalization and disease severity among those hospitalized by race and ethnicity should be interpreted carefully. These may reflect a constellation of factors that are difficult to measure, including differences in healthcare access, inequalities in care (including hospital admission inequalities), and implicit bias—all of which may reflect structural racism. For example, it is possible that children who identify as Black or Hispanic have different access to care compared to children who identify as White, and this may affect disease severity on presentation.2 Alternatively, it is possible that White pediatric patients are more likely to be hospitalized as compared to non-White pediatric patients with similar illness severity. Our finding that pediatric patients who identify as Hispanic or Black had a lower risk of hospitalization should be also interpreted carefully, as this may reflect higher utilization of the ED for SARS-CoV-2 testing, increased use of nonemergency services among those without access to primary care, or systematic differences in provider decision-making among this segment of the population.2 Further study is needed to determine specific drivers for racial and ethnic differences in healthcare utilization in children and adolescents with COVID-19.26

Complications and co-occurring diagnoses in adults with COVID-19 are well documented.27-30 However, there is little information to date on the co-occurring diagnoses and complications associated with COVID-19 in children and adolescents. We found that complications and co-occurring conditions occurred in 16.3% of the study population, with the most frequent conditions including known complications of viral infections such as pneumonia, respiratory failure, and seizures. Acute kidney and liver injury, as well as thrombotic complications, occurred less commonly than in adults.26-29 Interestingly, neurologic complications were also uncommon compared to adult reports8,31 and less frequent than in other viral illnesses in children and adolescents. For example, neurologic complications occur in approximately 7.5% of children and adolescents hospitalized with influenza.32

Limitations of the present study include the retrospective design, as well as incomplete patient-level clinical data in the PHIS database. The PHIS database only includes children’s hospitals, which may limit the generalizability of findings to community hospitals. We also excluded newborns, and our findings may not be generalizable to this population. We only included children and adolescents with a primary diagnosis of COVID-19, which has the potential for misclassification in cases where COVID-19 was a secondary diagnosis. However, results of our sensitivity analysis, which incorporated secondary diagnoses of COVID-19, were consistent with findings from our main analyses. Our study was designed to examine associations between certain prespecified factors and COVID-19 severity among pediatric patients who visited the ED or were admitted to the hospital during the COVID-19 pandemic. Thus, our findings must be interpreted in light of these considerations and may not be generalizable outside the ED or hospital setting. For example, it could be that some segments of the population utilized ED resources for testing, whereas others avoided the ED and other healthcare settings for fear of exposure to SARS-CoV-2. We also relied on diagnosis codes to identify concurrent diagnoses, as well as mechanical ventilation in our very severe outcome cohort, which resulted in this classification for some of these diagnoses. Despite these limitations, our findings represent an important step in understanding the risk factors associated with severe clinical COVID-19 disease in pediatric patients.

Our findings may inform future research and clinical interventions. Future studies on antiviral therapies and immune modulators targeting SARS-CoV-2 infection in children and adolescents should focus on high-risk populations, such as those identified in the study, as these patients are most likely to benefit from therapeutic interventions. Similarly, vaccine-development efforts may benefit from additional evaluation in high-risk populations, some of which may have altered immune responses. Furthermore, with increasing vaccination among adults and changes in recommendations, societal mitigation efforts (eg, masking, physical distancing) will diminish. Continued vigilance and COVID-19–mitigation efforts among high-risk children, for whom vaccines are not yet available, are critical during this transition.

CONCLUSION

Among children with COVID-19 who received care at children’s hospitals and EDs, 20% were hospitalized, and, of those, 21% were admitted to the ICU. Older children and adolescent patients had a lower risk of hospitalization; however, when hospitalized, they had greater illness severity. Those with selected comorbidities (eg, cardiovascular, obesity/type 2 DM, pulmonary and neurologic or neuromuscular disease) had both increased odds of hospitalization and in-hospital illness severity. While there were observed differences in COVID-19 severity by race and ethnicity, additional research is needed to clarify the drivers of such disparities. These factors should be considered when prioritizing mitigation strategies to prevent infection (eg, remote learning, avoidance of group activities, prioritization of COVID-19 vaccine when approved for children aged <12 years).

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References

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8. Helms J, Kremer S, Merdji H, et al. Neurologic features in severe SARS-CoV-2 infection. N Engl J Med. 2020;382(23):2268-2270. https://doi.org/10.1056/nejmc2008597
9. Severe Covid GWAS Group; Ellinghaus D, Degenhardt F, Bujanda L, et al. Genomewide association study of severe Covid-19 with respiratory failure. N Engl J Med. 2020;383(16):1522-1534.
10. Kabarriti R, Brodin NP, Maron MI, et al. association of race and ethnicity with comorbidities and survival among patients with COVID-19 at an urban medical center in New York. JAMA Netw Open. 2020;3(9):e2019795. https://doi.org/10.1001/jamanetworkopen.2020.19795
11. Bellino S, Punzo O, Rota MC, et al; COVID-19 Working Group. COVID-19 disease severity risk factors for pediatric patients in Italy. Pediatrics. 2020;146(4):e2020009399. https://doi.org/10.1542/peds.2020-009399
12. Ouldali N, Yang DD, Madhi F, et al; investigator group of the PANDOR study. Factors associated with severe SARS-CoV-2 infection. Pediatrics. 2020;147(3):e2020023432. https://doi.org/10.1542/peds.2020-023432
13. Castells MC, Phillips EJ. Maintaining safety with SARS-CoV-2 vaccines. N Engl J Med. 2021;384(7):643-649. https://doi.org/10.1056/nejmra2035343
14. Antoon JW, Williams DJ, Thurm C, et al. The COVID-19 pandemic and changes in healthcare utilization for pediatric respiratory and nonrespiratory illnesses in the United States. J Hosp Med. 2021;16(5):294-297. https://doi.org/10.12788/jhm.3608
15. Blatz AM, David MZ, Otto WR, Luan X, Gerber JS. Validation of International Classification of Disease-10 code for identifying children hospitalized with coronavirus disease-2019. J Pediatric Infect Dis Soc. 2020;10(4):547-548. https://doi.org/10.1093/jpids/piaa140
16. Kadri SS, Gundrum J, Warner S, et al. Uptake and accuracy of the diagnosis code for COVID-19 among US hospitalizations. JAMA. 2020;324(24):2553-2554. https://doi.org/10.1001/jama.2020.20323
17. Kaiser SV, Rodean J, Bekmezian A, et al; Pediatric Research in Inpatient Settings (PRIS) Network. Effectiveness of pediatric asthma pathways for hospitalized children: a multicenter, national analysis. J Pediatr. 2018;197:165-171.e162. https://doi.org/10.1016/j.jpeds.2018.01.084
18. Feudtner C, Feinstein JA, Zhong W, Hall M, Dai D. Pediatric complex chronic conditions classification system version 2: updated for ICD-10 and complex medical technology dependence and transplantation. BMC Pediatr. 2014;14:199. https://doi.org/10.1186/1471-2431-14-199.
19. Williams DJ, Zhu Y, Grijalva CG, et al. Predicting severe pneumonia outcomes in children. Pediatrics. 2016;138(4):e20161019. https://doi.org/10.1542/peds.2016-1019
20. Zachariah P, Johnson CL, Halabi KC, et al. Epidemiology, clinical features, and disease severity in patients with coronavirus disease 2019 (COVID-19) in a children’s hospital in New York City, New York. JAMA Pediatr. 2020;174(10):e202430. https://doi.org/10.1001/jamapediatrics.2020.2430
21. DeBiasi RL, Song X, Delaney M, et al. Severe coronavirus disease-2019 in children and young adults in the Washington, DC, metropolitan region. J Pediatr. 2020;223:199-203.e191. https://doi.org/10.1016/j.jpeds.2020.05.007
22. Lovinsky-Desir S, Deshpande DR, De A, et al. Asthma among hospitalized patients with COVID-19 and related outcomes. J Allergy Clin Immunol. 2020;146(5):1027-1034.e1024. https://doi.org/10.1016/j.jaci.2020.07.026
23. Beken B, Ozturk GK, Aygun FD, Aydogmus C, Akar HH. Asthma and allergic diseases are not risk factors for hospitalization in children with coronavirus disease 2019. Ann Allergy Asthma Immunol. 2021;126(5):569-575. https://doi.org/10.1016/j.anai.2021.01.018
24. Yehia BR, Winegar A, Fogel R, et al. Association of race with mortality among patients hospitalized with coronavirus disease 2019 (COVID-19) at 92 US hospitals. JAMA Netw Open. 2020;3(8):e2018039. https://doi.org/10.1001/jamanetworkopen.2020.18039
25. Saatci D, Ranger TA, Garriga C, et al. Association between race and COVID-19 outcomes among 2.6 million children in England. JAMA Pediatr. 2021;e211685. https://doi.org/10.1001/jamapediatrics.2021.1685
26. Lopez L, 3rd, Hart LH, 3rd, Katz MH. Racial and ethnic health disparities related to COVID-19. JAMA. 2021;325(8):719-720. https://doi.org/10.1001/jama.2020.26443
27. Altunok ES, Alkan M, Kamat S, et al. Clinical characteristics of adult patients hospitalized with laboratory-confirmed COVID-19 pneumonia. J Infect Chemother. 2020. https://doi.org/10.1016/j.jiac.2020.10.020
28. Ali H, Daoud A, Mohamed MM, et al. Survival rate in acute kidney injury superimposed COVID-19 patients: a systematic review and meta-analysis. Ren Fail. 2020;42(1):393-397. https://doi.org/10.1080/0886022x.2020.1756323
29. Anirvan P, Bharali P, Gogoi M, Thuluvath PJ, Singh SP, Satapathy SK. Liver injury in COVID-19: the hepatic aspect of the respiratory syndrome - what we know so far. World J Hepatol. 2020;12(12):1182-1197. https://doi.org/10.4254/wjh.v12.i12.1182
30. Moschonas IC, Tselepis AD. SARS-CoV-2 infection and thrombotic complications: a narrative review. J Thromb Thrombolysis. 2021;52(1):111-123. https://doi.org/10.1007/s11239-020-02374-3
31. Lee MH, Perl DP, Nair G, et al. Microvascular injury in the brains of patients with Covid-19. N Engl J Med. 2020;384(5):481-483. https://doi.org/10.1056/nejmc2033369
32. Antoon JW, Hall M, Herndon A, et al. Prevalence, risk factors, and outcomes of influenza-associated neurological Complications in Children. J Pediatr. 2021;S0022-3476(21)00657-0. https://doi.org/10.1016/j.jpeds.2021.06.075

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1Division of Hospital Medicine, Monroe Carell Jr. Children’s Hospital at Vanderbilt and Department of Pediatrics, Vanderbilt University School of Medicine, Nashville, Tennessee; 2Department of Health Policy, Vanderbilt University Medical Center, Nashville, Tennessee; 3Children’s Hospital Association, Lenexa, Kansas; 4Children’s Minnesota Research Institute, Minneapolis, Minnesota; 5Department of Pediatrics, Medical University of South Carolina, Charleston, South Carolina; 6Department of Pediatrics, Division of Hospital Medicine, Nicklaus Children’s Hospital, Miami, Florida; 7Divisions of Hospital Medicine and Infectious Diseases, Cincinnati Children’s Hospital Medical Center & Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio; 8Center for Pediatric Clinical Effectiveness, Children’s Hospital of Philadelphia and University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania; 9Division of Infectious Diseases, Department of Pediatrics, University of Utah, Salt Lake City, Utah.

Disclosures
Dr Grijalva has received consulting fees from Pfizer, Inc, Sanofi, and Merck and Co. The other authors reported no conflicts of interest.

Funding
Drs Antoon and Kenyon received funding from the National Heart, Lung, and Blood Institute of the National Institutes of Health. Drs Williams and Grijalva received funding from the National Institute of Allergy and Infectious Diseases. Dr Grijalva received research funding from Sanofi-Pasteur, Campbell Alliance, the US Centers for Disease Control and Prevention, National Institutes of Health, US Food and Drug Administration, and the Agency for Healthcare Research and Quality. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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1Division of Hospital Medicine, Monroe Carell Jr. Children’s Hospital at Vanderbilt and Department of Pediatrics, Vanderbilt University School of Medicine, Nashville, Tennessee; 2Department of Health Policy, Vanderbilt University Medical Center, Nashville, Tennessee; 3Children’s Hospital Association, Lenexa, Kansas; 4Children’s Minnesota Research Institute, Minneapolis, Minnesota; 5Department of Pediatrics, Medical University of South Carolina, Charleston, South Carolina; 6Department of Pediatrics, Division of Hospital Medicine, Nicklaus Children’s Hospital, Miami, Florida; 7Divisions of Hospital Medicine and Infectious Diseases, Cincinnati Children’s Hospital Medical Center & Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio; 8Center for Pediatric Clinical Effectiveness, Children’s Hospital of Philadelphia and University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania; 9Division of Infectious Diseases, Department of Pediatrics, University of Utah, Salt Lake City, Utah.

Disclosures
Dr Grijalva has received consulting fees from Pfizer, Inc, Sanofi, and Merck and Co. The other authors reported no conflicts of interest.

Funding
Drs Antoon and Kenyon received funding from the National Heart, Lung, and Blood Institute of the National Institutes of Health. Drs Williams and Grijalva received funding from the National Institute of Allergy and Infectious Diseases. Dr Grijalva received research funding from Sanofi-Pasteur, Campbell Alliance, the US Centers for Disease Control and Prevention, National Institutes of Health, US Food and Drug Administration, and the Agency for Healthcare Research and Quality. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Author and Disclosure Information

1Division of Hospital Medicine, Monroe Carell Jr. Children’s Hospital at Vanderbilt and Department of Pediatrics, Vanderbilt University School of Medicine, Nashville, Tennessee; 2Department of Health Policy, Vanderbilt University Medical Center, Nashville, Tennessee; 3Children’s Hospital Association, Lenexa, Kansas; 4Children’s Minnesota Research Institute, Minneapolis, Minnesota; 5Department of Pediatrics, Medical University of South Carolina, Charleston, South Carolina; 6Department of Pediatrics, Division of Hospital Medicine, Nicklaus Children’s Hospital, Miami, Florida; 7Divisions of Hospital Medicine and Infectious Diseases, Cincinnati Children’s Hospital Medical Center & Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio; 8Center for Pediatric Clinical Effectiveness, Children’s Hospital of Philadelphia and University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania; 9Division of Infectious Diseases, Department of Pediatrics, University of Utah, Salt Lake City, Utah.

Disclosures
Dr Grijalva has received consulting fees from Pfizer, Inc, Sanofi, and Merck and Co. The other authors reported no conflicts of interest.

Funding
Drs Antoon and Kenyon received funding from the National Heart, Lung, and Blood Institute of the National Institutes of Health. Drs Williams and Grijalva received funding from the National Institute of Allergy and Infectious Diseases. Dr Grijalva received research funding from Sanofi-Pasteur, Campbell Alliance, the US Centers for Disease Control and Prevention, National Institutes of Health, US Food and Drug Administration, and the Agency for Healthcare Research and Quality. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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The COVID-19 pandemic has led to more than 40 million infections and more than 650,000 deaths in the United States alone.1 Morbidity and mortality have disproportionately affected older adults.2-4 However, acute infection and delayed effects, such as multisystem inflammatory syndrome in children (MIS-C), occur and can lead to severe complications, hospitalization, and death in pediatric patients.5,6 Due to higher clinical disease prevalence and morbidity in the adult population, we have learned much about the clinical factors associated with severe adult COVID-19 disease.5,7-9 Such clinical factors include older age, concurrent comorbidities, smoke exposure, and Black race or Hispanic ethnicity, among others.5,7-10 However, there is a paucity of data on severe COVID-19 disease in pediatric patients.5,11,12 In addition, most immunization strategies and pharmacologic treatments for COVID-19 have not been evaluated or approved for use in children.13 To guide targeted prevention and treatment strategies, there is a critical need to identify children and adolescents—who are among the most vulnerable patient populations—at high risk for severe disease.

Identifying the clinical factors associated with severe COVID-19 disease will help with prioritizing and allocating vaccines when they are approved for use in patients younger than 12 years. It also can provide insight for clinicians and families faced with decisions wherein individual risk assessment is crucial (eg, in-person schooling, other group activities). The objective of this study was to determine the clinical factors associated with severe COVID-19 among children and adolescents in the United States.

METHODS

Study Design

We conducted a multicenter retrospective cohort study of patients presenting for care at pediatric hospitals that report data to the Pediatric Health Information System (PHIS) database. The PHIS administrative database includes billing and utilization data from 45 US tertiary care hospitals affiliated with the Children’s Hospital Association (Lenexa, Kansas). Data quality and reliability are ensured through a joint validation effort between the Children’s Hospital Association and participating hospitals. Hospitals submit discharge data, including demographics, diagnoses, and procedures using International Classification of Diseases, 10th Revision (ICD-10) codes, along with daily detailed information on pharmacy, location of care, and other services.

Study Population

Patients 30 days to 18 years of age discharged from the emergency department (ED) or inpatient setting with a primary diagnosis of COVID-19 (ICD-10 codes U.071 and U.072) between April 1, 2020, and September 30, 2020, were eligible for inclusion.14 In a prior study, the positive predictive value of an ICD-10–coded diagnosis of COVID-19 among hospitalized pediatric patients was 95.5%, compared with reverse transcription polymerase reaction results or presence of MIS-C.15 The diagnostic code for COVID-19 (ICD-10-CM) also had a high sensitivity (98.0%) in the hospitalized population.16 Acknowledging the increasing practice of screening patients upon admission, and in an attempt to minimize potential misclassification, we did not include encounters with secondary diagnoses of COVID-19 in our primary analyses. Pediatric patients with surgical diagnoses and neonates who never left the hospital were also excluded.

Factors Associated With Severe COVID-19 Disease

Exposures of interest were determined a priori based on current evidence in the literature and included patient age (0-4 years, 5-11 years, and 12-18 years), sex, race and ethnicity (non-Hispanic White, non-Hispanic Black, Hispanic, Asian, other non-White race [defined as Pacific Islander, Native American, or other]), payor type, cardiovascular complex chronic conditions (CCC), neuromuscular CCC, obesity/type 2 diabetes mellitus (DM), pulmonary CCC, asthma (defined using ICD-10 codes17), and immunocompromised CCC. Race and ethnicity were included as covariates based on previous studies reporting differences in COVID-19 outcomes among racial and ethnic groups.9 The CCC covariates were defined using the pediatric CCC ICD-10 classification system version 2.18

Pediatric Complications and Conditions Associated With COVID-19

Based on current evidence and expert opinion of study members, associated diagnoses and complications co-occurring with a COVID-19 diagnosis were defined a priori and identified through ICD-10 codes (Appendix Table 1). These included acute kidney injury, acute liver injury, aseptic meningitis, asthma exacerbation, bronchiolitis, cerebral infarction, croup, encephalitis, encephalopathy, infant fever, febrile seizure, gastroenteritis/dehydration, Kawasaki disease/MIS-C, myocarditis/pericarditis, pneumonia, lung effusion or empyema, respiratory failure, sepsis, nonfebrile seizure, pancreatitis, sickle cell complications, and thrombotic complications.

Outcomes

COVID-19 severity outcomes were assessed as follows: (1) mild = ED discharge; (2) moderate = inpatient admission; (3) severe = intensive care unit (ICU) admission without mechanical ventilation, shock, or death; and (4) very severe = ICU admission with mechanical ventilation, shock, or death.19 This ordinal ranking system did not violate the proportional odds assumption. Potential reasons for admission to the ICU without mechanical ventilation, shock, or death include, but are not limited to, need for noninvasive ventilation, vital sign instability, dysrhythmias, respiratory insufficiency, or complications arising from concurrent conditions (eg, thrombotic events, need for continuous albuterol therapy). We examined several secondary, hospital-based outcomes, including associated diagnoses and complications, all-cause 30-day healthcare reutilization (ED visit or rehospitalization), length of stay (LOS), and ICU LOS.

Statistical Analysis

Demographic characteristics were summarized using frequencies and percentages for categorical variables and geometric means with SD and medians with interquartile ranges (IQR) for continuous variables, as appropriate. Factors associated with hospitalization (encompassing severity levels 2-4) vs ED discharge (severity level 1) were assessed using logistic regression. Factors associated with increasing severity among hospitalized pediatric patients (severity levels 2, 3, and 4) were assessed using ordinal logistic regression. Covariates in these analyses included race and ethnicity, age, sex, payor, cardiovascular CCC, neurologic/neuromuscular CCC, obesity/type 2 DM, pulmonary CCC, asthma, and immunocompromised CCC. Adjusted odds ratios (aOR) and corresponding 95% CI for each risk factor were generated using generalized linear mixed effects models and random intercepts for each hospital. Given the potential for diagnostic misclassification of pediatric patients with COVID-19 based on primary vs secondary diagnoses, we performed sensitivity analyses defining the study population as those with a primary diagnosis of COVID-19 and those with a secondary diagnosis of COVID-19 plus a concurrent primary diagnosis of a condition associated with COVID-19 (Appendix Table 1).

All analyses were performed using SAS version 9.4 (SAS Institute, Inc), and P < .05 was considered statistically significant. The Institutional Review Board at Vanderbilt University Medical Center determined that this study of de-identified data did not meet the criteria for human subjects research.

RESULTS

Study Population

A total of 19,976 encounters were included in the study. Of those, 15,913 (79.7%) were discharged from the ED and 4063 (20.3%) were hospitalized (Table 1). The most common race/ethnicity was Hispanic (9741, 48.8%), followed by non-Hispanic White (4217, 21.1%). Reference race/ethnicity data for the overall 2019 PHIS population can be found in Appendix Table 2.

Characteristics of Children With COVID-19 Disease Who Were Evaluated at US Children’s Hospitals, April 1, 2020, to September 30, 2020

The severity distribution among the hospitalized population was moderate (3222, 79.3%), severe (431, 11.3%), and very severe (380, 9.4%). The frequency of COVID-19 diagnoses increased late in the study period (Figure). Among those hospitalized, the median LOS for the index admission was 2 days (IQR, 1-4), while among those admitted to the ICU, the median LOS was 3 days (IQR, 2-5).

Trends in COVID-19 Diagnoses

Overall, 10.1% (n = 2020) of the study population had an all-cause repeat encounter (ie, subsequent ED encounter or hospitalization) within 30 days following the index discharge. Repeat encounters were more frequent among patients hospitalized than among those discharged from the ED (Appendix Table 3).

Prevalence of Conditions and Complications Associated With COVID-19

Overall, 3257 (16.3%) patients had one or more co-occurring diagnoses categorized as a COVID-19–associated condition or complication. The most frequent diagnoses included lower respiratory tract disease (pneumonia, lung effusion, or empyema; n = 1415, 7.1%), gastroenteritis/dehydration (n = 1068, 5.3%), respiratory failure (n = 731, 3.7%), febrile infant (n = 413, 2.1%), and nonfebrile seizure (n = 425, 2.1%). Aside from nonfebrile seizure, neurological complications were less frequent and included febrile seizure (n = 155, 0.8%), encephalopathy (n = 63, 0.3%), aseptic meningitis (n = 16, 0.1%), encephalitis (n = 11, 0.1%), and cerebral infarction (n = 6, <0.1%). Kawasaki disease and MIS-C comprised 1.7% (n = 346) of diagnoses. Thrombotic complications occurred in 0.1% (n = 13) of patients. Overall, these conditions and complications associated with COVID-19 were more frequent in hospitalized patients than in those discharged from the ED (P < .001) (Table 2).

Conditions and Complications Associated With COVID-19

Factors Associated With COVID-19 Disease Severity

Compared to pediatric patients with COVID-19 discharged from the ED, factors associated with increased odds of hospitalization included private payor insurance; obesity/type 2 DM; asthma; and cardiovascular, immunocompromised, neurologic/neuromuscular, and pulmonary CCCs (Table 3). Factors associated with decreased risk of hospitalization included Black race or Hispanic ethnicity compared with White race; female sex; and age 5 to 11 years and age 12 to 17 years (vs age 0-4 years). Among children and adolescents hospitalized with COVID-19, factors associated with greater disease severity included Black or other non-White race; age 5 to 11 years; age 12 to 17 years; obesity/type 2 DM; immunocompromised conditions; and cardiovascular, neurologic/neuromuscular, and pulmonary CCCs (Table 3).

Factors Associated With Disease Severity in Children and Adolescents With COVID-19

Sensitivity Analysis

We performed a sensitivity analysis that expanded the study population to include those with a secondary diagnosis of COVID-19 plus a diagnosis of a COVID-19–associated condition or complication. Analyses using the expanded population (N = 21,247) were similar to the primary analyses (Appendix Table 4 and Appendix Table 5).

DISCUSSION

In this large multicenter study evaluating COVID-19 disease severity in more than 19,000 patients presenting for emergency care at US pediatric hospitals, approximately 20% were hospitalized, and among those hospitalized almost a quarter required ICU care. Clinical risk factors associated with increased risk of hospitalization include private payor status and selected comorbidities (obesity/type 2 DM; asthma; and cardiovascular, pulmonary, immunocompromised, neurologic/neuromuscular CCCs), while those associated with decreased risk of hospitalization include older age, female sex, and Black race or Hispanic ethnicity. Factors associated with severe disease among hospitalized pediatric patients include Black or other non-White race, school age (≥5 years), and certain chronic conditions (cardiovascular disease, obesity/type 2 DM, neurologic or neuromuscular disease). Sixteen percent of patients had a concurrent diagnosis for a condition or complication associated with COVID-19.

While the study population (ie, children and adolescents presenting to the ED) represents a small fraction of children and adolescents in the community with SARS-CoV-2 infection, the results provide important insight into factors of severe COVID-19 in the pediatric population. A report from France suggested ventilatory or hemodynamic support or death were independently associated with older age (≥10 years), elevated C-reactive protein, and hypoxemia.12 An Italian study found that younger age (0-4 years) was associated with less severe disease, while preexisting conditions were more likely in patients with severe disease.11 A single-center case series of 50 patients (aged ≤21 years) hospitalized at a children’s hospital in New York City found respiratory failure (n = 9) was more common in children older than 1 year, patients with elevated inflammatory markers, and patients with obesity.20

Our study confirms several factors for severe COVID-19 found in these studies, including older age,11,12,20 obesity,20 and preexisting conditions.11 Our findings also expand on these reports, including identification of factors associated with hospitalization. Given the rate of 30-day re-encounters among pediatric patients with COVID-19 (10.1%), identifying risk factors for hospitalization may aid ED providers in determining optimal disposition (eg, home, hospital admission, ICU). We also identified specific comorbidities associated with more severe disease in those hospitalized with COVID-19, such as cardiovascular disease, obesity/type 2 DM, and pulmonary, neurologic, or neuromuscular conditions. We also found that asthma increased the risk for hospitalization but not more severe disease among those hospitalized. This latter finding also aligns with recent single-center studies,21,22 whereas a Turkish study of pediatric patients aged 0 to 18 years found no association between asthma and COVID-19 hospitalizations.23We also examined payor type and racial/ethnic factors in our analysis. In 2019, patients who identified as Black or Hispanic comprised 52.3% of all encounters and 40.7% of hospitalizations recorded in the PHIS database. During the same year, encounters for influenza among Black or Hispanic pediatric patients comprised 58.7% of all influenza diagnoses and 47.0% of pediatric influenza hospitalizations (Appendix Table 2). In this study, patients who identified as Black or Hispanic race represented a disproportionately large share of patients presenting to children’s hospitals (68.5%) and of those hospitalized (60.8%). Hispanic ethnicity, in particular, represented a disproportionate share of patients seeking care for COVID-19 compared to the overall PHIS population (47.7% and 27.1%, respectively). After accounting for other factors, we found Black and other non-White race—but not of Hispanic ethnicity—were independently associated with more disease severity among those hospitalized. This contrasts with findings from a recent adult study by Yehia et al,24 who found (after adjusting for other clinical factors) no significant difference in mortality between Black patients and White patients among adults hospitalized due to COVID-19. It also contrasts with a recent large population-based UK study wherein pediatric patients identifying as Asian, but not Black or mixed race or ethnicity, had an increased risk of hospital admission and admission to the ICU compared to children identifying as White. Children identifying as Black or mixed race had longer hospital admissions.25 However, as the authors of the study note, residual confounders and ascertainment bias due to differences in COVID testing may have influenced these findings.

Our findings of differences in hospitalization and disease severity among those hospitalized by race and ethnicity should be interpreted carefully. These may reflect a constellation of factors that are difficult to measure, including differences in healthcare access, inequalities in care (including hospital admission inequalities), and implicit bias—all of which may reflect structural racism. For example, it is possible that children who identify as Black or Hispanic have different access to care compared to children who identify as White, and this may affect disease severity on presentation.2 Alternatively, it is possible that White pediatric patients are more likely to be hospitalized as compared to non-White pediatric patients with similar illness severity. Our finding that pediatric patients who identify as Hispanic or Black had a lower risk of hospitalization should be also interpreted carefully, as this may reflect higher utilization of the ED for SARS-CoV-2 testing, increased use of nonemergency services among those without access to primary care, or systematic differences in provider decision-making among this segment of the population.2 Further study is needed to determine specific drivers for racial and ethnic differences in healthcare utilization in children and adolescents with COVID-19.26

Complications and co-occurring diagnoses in adults with COVID-19 are well documented.27-30 However, there is little information to date on the co-occurring diagnoses and complications associated with COVID-19 in children and adolescents. We found that complications and co-occurring conditions occurred in 16.3% of the study population, with the most frequent conditions including known complications of viral infections such as pneumonia, respiratory failure, and seizures. Acute kidney and liver injury, as well as thrombotic complications, occurred less commonly than in adults.26-29 Interestingly, neurologic complications were also uncommon compared to adult reports8,31 and less frequent than in other viral illnesses in children and adolescents. For example, neurologic complications occur in approximately 7.5% of children and adolescents hospitalized with influenza.32

Limitations of the present study include the retrospective design, as well as incomplete patient-level clinical data in the PHIS database. The PHIS database only includes children’s hospitals, which may limit the generalizability of findings to community hospitals. We also excluded newborns, and our findings may not be generalizable to this population. We only included children and adolescents with a primary diagnosis of COVID-19, which has the potential for misclassification in cases where COVID-19 was a secondary diagnosis. However, results of our sensitivity analysis, which incorporated secondary diagnoses of COVID-19, were consistent with findings from our main analyses. Our study was designed to examine associations between certain prespecified factors and COVID-19 severity among pediatric patients who visited the ED or were admitted to the hospital during the COVID-19 pandemic. Thus, our findings must be interpreted in light of these considerations and may not be generalizable outside the ED or hospital setting. For example, it could be that some segments of the population utilized ED resources for testing, whereas others avoided the ED and other healthcare settings for fear of exposure to SARS-CoV-2. We also relied on diagnosis codes to identify concurrent diagnoses, as well as mechanical ventilation in our very severe outcome cohort, which resulted in this classification for some of these diagnoses. Despite these limitations, our findings represent an important step in understanding the risk factors associated with severe clinical COVID-19 disease in pediatric patients.

Our findings may inform future research and clinical interventions. Future studies on antiviral therapies and immune modulators targeting SARS-CoV-2 infection in children and adolescents should focus on high-risk populations, such as those identified in the study, as these patients are most likely to benefit from therapeutic interventions. Similarly, vaccine-development efforts may benefit from additional evaluation in high-risk populations, some of which may have altered immune responses. Furthermore, with increasing vaccination among adults and changes in recommendations, societal mitigation efforts (eg, masking, physical distancing) will diminish. Continued vigilance and COVID-19–mitigation efforts among high-risk children, for whom vaccines are not yet available, are critical during this transition.

CONCLUSION

Among children with COVID-19 who received care at children’s hospitals and EDs, 20% were hospitalized, and, of those, 21% were admitted to the ICU. Older children and adolescent patients had a lower risk of hospitalization; however, when hospitalized, they had greater illness severity. Those with selected comorbidities (eg, cardiovascular, obesity/type 2 DM, pulmonary and neurologic or neuromuscular disease) had both increased odds of hospitalization and in-hospital illness severity. While there were observed differences in COVID-19 severity by race and ethnicity, additional research is needed to clarify the drivers of such disparities. These factors should be considered when prioritizing mitigation strategies to prevent infection (eg, remote learning, avoidance of group activities, prioritization of COVID-19 vaccine when approved for children aged <12 years).

The COVID-19 pandemic has led to more than 40 million infections and more than 650,000 deaths in the United States alone.1 Morbidity and mortality have disproportionately affected older adults.2-4 However, acute infection and delayed effects, such as multisystem inflammatory syndrome in children (MIS-C), occur and can lead to severe complications, hospitalization, and death in pediatric patients.5,6 Due to higher clinical disease prevalence and morbidity in the adult population, we have learned much about the clinical factors associated with severe adult COVID-19 disease.5,7-9 Such clinical factors include older age, concurrent comorbidities, smoke exposure, and Black race or Hispanic ethnicity, among others.5,7-10 However, there is a paucity of data on severe COVID-19 disease in pediatric patients.5,11,12 In addition, most immunization strategies and pharmacologic treatments for COVID-19 have not been evaluated or approved for use in children.13 To guide targeted prevention and treatment strategies, there is a critical need to identify children and adolescents—who are among the most vulnerable patient populations—at high risk for severe disease.

Identifying the clinical factors associated with severe COVID-19 disease will help with prioritizing and allocating vaccines when they are approved for use in patients younger than 12 years. It also can provide insight for clinicians and families faced with decisions wherein individual risk assessment is crucial (eg, in-person schooling, other group activities). The objective of this study was to determine the clinical factors associated with severe COVID-19 among children and adolescents in the United States.

METHODS

Study Design

We conducted a multicenter retrospective cohort study of patients presenting for care at pediatric hospitals that report data to the Pediatric Health Information System (PHIS) database. The PHIS administrative database includes billing and utilization data from 45 US tertiary care hospitals affiliated with the Children’s Hospital Association (Lenexa, Kansas). Data quality and reliability are ensured through a joint validation effort between the Children’s Hospital Association and participating hospitals. Hospitals submit discharge data, including demographics, diagnoses, and procedures using International Classification of Diseases, 10th Revision (ICD-10) codes, along with daily detailed information on pharmacy, location of care, and other services.

Study Population

Patients 30 days to 18 years of age discharged from the emergency department (ED) or inpatient setting with a primary diagnosis of COVID-19 (ICD-10 codes U.071 and U.072) between April 1, 2020, and September 30, 2020, were eligible for inclusion.14 In a prior study, the positive predictive value of an ICD-10–coded diagnosis of COVID-19 among hospitalized pediatric patients was 95.5%, compared with reverse transcription polymerase reaction results or presence of MIS-C.15 The diagnostic code for COVID-19 (ICD-10-CM) also had a high sensitivity (98.0%) in the hospitalized population.16 Acknowledging the increasing practice of screening patients upon admission, and in an attempt to minimize potential misclassification, we did not include encounters with secondary diagnoses of COVID-19 in our primary analyses. Pediatric patients with surgical diagnoses and neonates who never left the hospital were also excluded.

Factors Associated With Severe COVID-19 Disease

Exposures of interest were determined a priori based on current evidence in the literature and included patient age (0-4 years, 5-11 years, and 12-18 years), sex, race and ethnicity (non-Hispanic White, non-Hispanic Black, Hispanic, Asian, other non-White race [defined as Pacific Islander, Native American, or other]), payor type, cardiovascular complex chronic conditions (CCC), neuromuscular CCC, obesity/type 2 diabetes mellitus (DM), pulmonary CCC, asthma (defined using ICD-10 codes17), and immunocompromised CCC. Race and ethnicity were included as covariates based on previous studies reporting differences in COVID-19 outcomes among racial and ethnic groups.9 The CCC covariates were defined using the pediatric CCC ICD-10 classification system version 2.18

Pediatric Complications and Conditions Associated With COVID-19

Based on current evidence and expert opinion of study members, associated diagnoses and complications co-occurring with a COVID-19 diagnosis were defined a priori and identified through ICD-10 codes (Appendix Table 1). These included acute kidney injury, acute liver injury, aseptic meningitis, asthma exacerbation, bronchiolitis, cerebral infarction, croup, encephalitis, encephalopathy, infant fever, febrile seizure, gastroenteritis/dehydration, Kawasaki disease/MIS-C, myocarditis/pericarditis, pneumonia, lung effusion or empyema, respiratory failure, sepsis, nonfebrile seizure, pancreatitis, sickle cell complications, and thrombotic complications.

Outcomes

COVID-19 severity outcomes were assessed as follows: (1) mild = ED discharge; (2) moderate = inpatient admission; (3) severe = intensive care unit (ICU) admission without mechanical ventilation, shock, or death; and (4) very severe = ICU admission with mechanical ventilation, shock, or death.19 This ordinal ranking system did not violate the proportional odds assumption. Potential reasons for admission to the ICU without mechanical ventilation, shock, or death include, but are not limited to, need for noninvasive ventilation, vital sign instability, dysrhythmias, respiratory insufficiency, or complications arising from concurrent conditions (eg, thrombotic events, need for continuous albuterol therapy). We examined several secondary, hospital-based outcomes, including associated diagnoses and complications, all-cause 30-day healthcare reutilization (ED visit or rehospitalization), length of stay (LOS), and ICU LOS.

Statistical Analysis

Demographic characteristics were summarized using frequencies and percentages for categorical variables and geometric means with SD and medians with interquartile ranges (IQR) for continuous variables, as appropriate. Factors associated with hospitalization (encompassing severity levels 2-4) vs ED discharge (severity level 1) were assessed using logistic regression. Factors associated with increasing severity among hospitalized pediatric patients (severity levels 2, 3, and 4) were assessed using ordinal logistic regression. Covariates in these analyses included race and ethnicity, age, sex, payor, cardiovascular CCC, neurologic/neuromuscular CCC, obesity/type 2 DM, pulmonary CCC, asthma, and immunocompromised CCC. Adjusted odds ratios (aOR) and corresponding 95% CI for each risk factor were generated using generalized linear mixed effects models and random intercepts for each hospital. Given the potential for diagnostic misclassification of pediatric patients with COVID-19 based on primary vs secondary diagnoses, we performed sensitivity analyses defining the study population as those with a primary diagnosis of COVID-19 and those with a secondary diagnosis of COVID-19 plus a concurrent primary diagnosis of a condition associated with COVID-19 (Appendix Table 1).

All analyses were performed using SAS version 9.4 (SAS Institute, Inc), and P < .05 was considered statistically significant. The Institutional Review Board at Vanderbilt University Medical Center determined that this study of de-identified data did not meet the criteria for human subjects research.

RESULTS

Study Population

A total of 19,976 encounters were included in the study. Of those, 15,913 (79.7%) were discharged from the ED and 4063 (20.3%) were hospitalized (Table 1). The most common race/ethnicity was Hispanic (9741, 48.8%), followed by non-Hispanic White (4217, 21.1%). Reference race/ethnicity data for the overall 2019 PHIS population can be found in Appendix Table 2.

Characteristics of Children With COVID-19 Disease Who Were Evaluated at US Children’s Hospitals, April 1, 2020, to September 30, 2020

The severity distribution among the hospitalized population was moderate (3222, 79.3%), severe (431, 11.3%), and very severe (380, 9.4%). The frequency of COVID-19 diagnoses increased late in the study period (Figure). Among those hospitalized, the median LOS for the index admission was 2 days (IQR, 1-4), while among those admitted to the ICU, the median LOS was 3 days (IQR, 2-5).

Trends in COVID-19 Diagnoses

Overall, 10.1% (n = 2020) of the study population had an all-cause repeat encounter (ie, subsequent ED encounter or hospitalization) within 30 days following the index discharge. Repeat encounters were more frequent among patients hospitalized than among those discharged from the ED (Appendix Table 3).

Prevalence of Conditions and Complications Associated With COVID-19

Overall, 3257 (16.3%) patients had one or more co-occurring diagnoses categorized as a COVID-19–associated condition or complication. The most frequent diagnoses included lower respiratory tract disease (pneumonia, lung effusion, or empyema; n = 1415, 7.1%), gastroenteritis/dehydration (n = 1068, 5.3%), respiratory failure (n = 731, 3.7%), febrile infant (n = 413, 2.1%), and nonfebrile seizure (n = 425, 2.1%). Aside from nonfebrile seizure, neurological complications were less frequent and included febrile seizure (n = 155, 0.8%), encephalopathy (n = 63, 0.3%), aseptic meningitis (n = 16, 0.1%), encephalitis (n = 11, 0.1%), and cerebral infarction (n = 6, <0.1%). Kawasaki disease and MIS-C comprised 1.7% (n = 346) of diagnoses. Thrombotic complications occurred in 0.1% (n = 13) of patients. Overall, these conditions and complications associated with COVID-19 were more frequent in hospitalized patients than in those discharged from the ED (P < .001) (Table 2).

Conditions and Complications Associated With COVID-19

Factors Associated With COVID-19 Disease Severity

Compared to pediatric patients with COVID-19 discharged from the ED, factors associated with increased odds of hospitalization included private payor insurance; obesity/type 2 DM; asthma; and cardiovascular, immunocompromised, neurologic/neuromuscular, and pulmonary CCCs (Table 3). Factors associated with decreased risk of hospitalization included Black race or Hispanic ethnicity compared with White race; female sex; and age 5 to 11 years and age 12 to 17 years (vs age 0-4 years). Among children and adolescents hospitalized with COVID-19, factors associated with greater disease severity included Black or other non-White race; age 5 to 11 years; age 12 to 17 years; obesity/type 2 DM; immunocompromised conditions; and cardiovascular, neurologic/neuromuscular, and pulmonary CCCs (Table 3).

Factors Associated With Disease Severity in Children and Adolescents With COVID-19

Sensitivity Analysis

We performed a sensitivity analysis that expanded the study population to include those with a secondary diagnosis of COVID-19 plus a diagnosis of a COVID-19–associated condition or complication. Analyses using the expanded population (N = 21,247) were similar to the primary analyses (Appendix Table 4 and Appendix Table 5).

DISCUSSION

In this large multicenter study evaluating COVID-19 disease severity in more than 19,000 patients presenting for emergency care at US pediatric hospitals, approximately 20% were hospitalized, and among those hospitalized almost a quarter required ICU care. Clinical risk factors associated with increased risk of hospitalization include private payor status and selected comorbidities (obesity/type 2 DM; asthma; and cardiovascular, pulmonary, immunocompromised, neurologic/neuromuscular CCCs), while those associated with decreased risk of hospitalization include older age, female sex, and Black race or Hispanic ethnicity. Factors associated with severe disease among hospitalized pediatric patients include Black or other non-White race, school age (≥5 years), and certain chronic conditions (cardiovascular disease, obesity/type 2 DM, neurologic or neuromuscular disease). Sixteen percent of patients had a concurrent diagnosis for a condition or complication associated with COVID-19.

While the study population (ie, children and adolescents presenting to the ED) represents a small fraction of children and adolescents in the community with SARS-CoV-2 infection, the results provide important insight into factors of severe COVID-19 in the pediatric population. A report from France suggested ventilatory or hemodynamic support or death were independently associated with older age (≥10 years), elevated C-reactive protein, and hypoxemia.12 An Italian study found that younger age (0-4 years) was associated with less severe disease, while preexisting conditions were more likely in patients with severe disease.11 A single-center case series of 50 patients (aged ≤21 years) hospitalized at a children’s hospital in New York City found respiratory failure (n = 9) was more common in children older than 1 year, patients with elevated inflammatory markers, and patients with obesity.20

Our study confirms several factors for severe COVID-19 found in these studies, including older age,11,12,20 obesity,20 and preexisting conditions.11 Our findings also expand on these reports, including identification of factors associated with hospitalization. Given the rate of 30-day re-encounters among pediatric patients with COVID-19 (10.1%), identifying risk factors for hospitalization may aid ED providers in determining optimal disposition (eg, home, hospital admission, ICU). We also identified specific comorbidities associated with more severe disease in those hospitalized with COVID-19, such as cardiovascular disease, obesity/type 2 DM, and pulmonary, neurologic, or neuromuscular conditions. We also found that asthma increased the risk for hospitalization but not more severe disease among those hospitalized. This latter finding also aligns with recent single-center studies,21,22 whereas a Turkish study of pediatric patients aged 0 to 18 years found no association between asthma and COVID-19 hospitalizations.23We also examined payor type and racial/ethnic factors in our analysis. In 2019, patients who identified as Black or Hispanic comprised 52.3% of all encounters and 40.7% of hospitalizations recorded in the PHIS database. During the same year, encounters for influenza among Black or Hispanic pediatric patients comprised 58.7% of all influenza diagnoses and 47.0% of pediatric influenza hospitalizations (Appendix Table 2). In this study, patients who identified as Black or Hispanic race represented a disproportionately large share of patients presenting to children’s hospitals (68.5%) and of those hospitalized (60.8%). Hispanic ethnicity, in particular, represented a disproportionate share of patients seeking care for COVID-19 compared to the overall PHIS population (47.7% and 27.1%, respectively). After accounting for other factors, we found Black and other non-White race—but not of Hispanic ethnicity—were independently associated with more disease severity among those hospitalized. This contrasts with findings from a recent adult study by Yehia et al,24 who found (after adjusting for other clinical factors) no significant difference in mortality between Black patients and White patients among adults hospitalized due to COVID-19. It also contrasts with a recent large population-based UK study wherein pediatric patients identifying as Asian, but not Black or mixed race or ethnicity, had an increased risk of hospital admission and admission to the ICU compared to children identifying as White. Children identifying as Black or mixed race had longer hospital admissions.25 However, as the authors of the study note, residual confounders and ascertainment bias due to differences in COVID testing may have influenced these findings.

Our findings of differences in hospitalization and disease severity among those hospitalized by race and ethnicity should be interpreted carefully. These may reflect a constellation of factors that are difficult to measure, including differences in healthcare access, inequalities in care (including hospital admission inequalities), and implicit bias—all of which may reflect structural racism. For example, it is possible that children who identify as Black or Hispanic have different access to care compared to children who identify as White, and this may affect disease severity on presentation.2 Alternatively, it is possible that White pediatric patients are more likely to be hospitalized as compared to non-White pediatric patients with similar illness severity. Our finding that pediatric patients who identify as Hispanic or Black had a lower risk of hospitalization should be also interpreted carefully, as this may reflect higher utilization of the ED for SARS-CoV-2 testing, increased use of nonemergency services among those without access to primary care, or systematic differences in provider decision-making among this segment of the population.2 Further study is needed to determine specific drivers for racial and ethnic differences in healthcare utilization in children and adolescents with COVID-19.26

Complications and co-occurring diagnoses in adults with COVID-19 are well documented.27-30 However, there is little information to date on the co-occurring diagnoses and complications associated with COVID-19 in children and adolescents. We found that complications and co-occurring conditions occurred in 16.3% of the study population, with the most frequent conditions including known complications of viral infections such as pneumonia, respiratory failure, and seizures. Acute kidney and liver injury, as well as thrombotic complications, occurred less commonly than in adults.26-29 Interestingly, neurologic complications were also uncommon compared to adult reports8,31 and less frequent than in other viral illnesses in children and adolescents. For example, neurologic complications occur in approximately 7.5% of children and adolescents hospitalized with influenza.32

Limitations of the present study include the retrospective design, as well as incomplete patient-level clinical data in the PHIS database. The PHIS database only includes children’s hospitals, which may limit the generalizability of findings to community hospitals. We also excluded newborns, and our findings may not be generalizable to this population. We only included children and adolescents with a primary diagnosis of COVID-19, which has the potential for misclassification in cases where COVID-19 was a secondary diagnosis. However, results of our sensitivity analysis, which incorporated secondary diagnoses of COVID-19, were consistent with findings from our main analyses. Our study was designed to examine associations between certain prespecified factors and COVID-19 severity among pediatric patients who visited the ED or were admitted to the hospital during the COVID-19 pandemic. Thus, our findings must be interpreted in light of these considerations and may not be generalizable outside the ED or hospital setting. For example, it could be that some segments of the population utilized ED resources for testing, whereas others avoided the ED and other healthcare settings for fear of exposure to SARS-CoV-2. We also relied on diagnosis codes to identify concurrent diagnoses, as well as mechanical ventilation in our very severe outcome cohort, which resulted in this classification for some of these diagnoses. Despite these limitations, our findings represent an important step in understanding the risk factors associated with severe clinical COVID-19 disease in pediatric patients.

Our findings may inform future research and clinical interventions. Future studies on antiviral therapies and immune modulators targeting SARS-CoV-2 infection in children and adolescents should focus on high-risk populations, such as those identified in the study, as these patients are most likely to benefit from therapeutic interventions. Similarly, vaccine-development efforts may benefit from additional evaluation in high-risk populations, some of which may have altered immune responses. Furthermore, with increasing vaccination among adults and changes in recommendations, societal mitigation efforts (eg, masking, physical distancing) will diminish. Continued vigilance and COVID-19–mitigation efforts among high-risk children, for whom vaccines are not yet available, are critical during this transition.

CONCLUSION

Among children with COVID-19 who received care at children’s hospitals and EDs, 20% were hospitalized, and, of those, 21% were admitted to the ICU. Older children and adolescent patients had a lower risk of hospitalization; however, when hospitalized, they had greater illness severity. Those with selected comorbidities (eg, cardiovascular, obesity/type 2 DM, pulmonary and neurologic or neuromuscular disease) had both increased odds of hospitalization and in-hospital illness severity. While there were observed differences in COVID-19 severity by race and ethnicity, additional research is needed to clarify the drivers of such disparities. These factors should be considered when prioritizing mitigation strategies to prevent infection (eg, remote learning, avoidance of group activities, prioritization of COVID-19 vaccine when approved for children aged <12 years).

References

1. Centers for Disease Control and Prevention. COVID data tracker. Accessed September 9, 2021. https://covid.cdc.gov/covid-data-tracker/#datatracker-home
2. Levy C, Basmaci R, Bensaid P, et al. Changes in reverse transcription polymerase chain reaction-positive severe acute respiratory syndrome coronavirus 2 rates in adults and children according to the epidemic stages. Pediatr Infect Dis J. 2020;39(11):e369-e372. https://doi.org/10.1097/inf.0000000000002861
3. Gudbjartsson DF, Helgason A, Jonsson H, et al. Spread of SARS-CoV-2 in the Icelandic population. N Engl J Med. 2020;382(24):2302-2315. https://doi.org/10.1056/nejmoa2006100
4. Garg S, Kim L, Whitaker M, et al. Hospitalization rates and characteristics of patients hospitalized with laboratory-confirmed coronavirus disease 2019 - COVID-NET, 14 States, March 1-30, 2020. MMWR Morb Mortal Wkly Rep. 2020;69(15):458-464. https://doi.org/10.15585/mmwr.mm6915e3
5. Castagnoli R, Votto M, Licari A, et al. Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection in children and adolescents: a systematic review. JAMA Pediatr. 2020;174(9):882-889. https://doi.org/10.1001/jamapediatrics.2020.1467
6. Feldstein LR, Rose EB, Horwitz SM, et al; Overcoming COVID-19 Investigators; CDC COVID-19 Response Team. Multisystem inflammatory syndrome in U.S. children and adolescents. N Engl J Med. 2020;383(4):334-346. https://doi.org/10.1056/nejmoa2021680
7. Magro B, Zuccaro V, Novelli L, et al. Predicting in-hospital mortality from coronavirus disease 2019: a simple validated app for clinical use. PLoS One. 2021;16(1):e0245281. https://doi.org/10.1371/journal.pone.0245281
8. Helms J, Kremer S, Merdji H, et al. Neurologic features in severe SARS-CoV-2 infection. N Engl J Med. 2020;382(23):2268-2270. https://doi.org/10.1056/nejmc2008597
9. Severe Covid GWAS Group; Ellinghaus D, Degenhardt F, Bujanda L, et al. Genomewide association study of severe Covid-19 with respiratory failure. N Engl J Med. 2020;383(16):1522-1534.
10. Kabarriti R, Brodin NP, Maron MI, et al. association of race and ethnicity with comorbidities and survival among patients with COVID-19 at an urban medical center in New York. JAMA Netw Open. 2020;3(9):e2019795. https://doi.org/10.1001/jamanetworkopen.2020.19795
11. Bellino S, Punzo O, Rota MC, et al; COVID-19 Working Group. COVID-19 disease severity risk factors for pediatric patients in Italy. Pediatrics. 2020;146(4):e2020009399. https://doi.org/10.1542/peds.2020-009399
12. Ouldali N, Yang DD, Madhi F, et al; investigator group of the PANDOR study. Factors associated with severe SARS-CoV-2 infection. Pediatrics. 2020;147(3):e2020023432. https://doi.org/10.1542/peds.2020-023432
13. Castells MC, Phillips EJ. Maintaining safety with SARS-CoV-2 vaccines. N Engl J Med. 2021;384(7):643-649. https://doi.org/10.1056/nejmra2035343
14. Antoon JW, Williams DJ, Thurm C, et al. The COVID-19 pandemic and changes in healthcare utilization for pediatric respiratory and nonrespiratory illnesses in the United States. J Hosp Med. 2021;16(5):294-297. https://doi.org/10.12788/jhm.3608
15. Blatz AM, David MZ, Otto WR, Luan X, Gerber JS. Validation of International Classification of Disease-10 code for identifying children hospitalized with coronavirus disease-2019. J Pediatric Infect Dis Soc. 2020;10(4):547-548. https://doi.org/10.1093/jpids/piaa140
16. Kadri SS, Gundrum J, Warner S, et al. Uptake and accuracy of the diagnosis code for COVID-19 among US hospitalizations. JAMA. 2020;324(24):2553-2554. https://doi.org/10.1001/jama.2020.20323
17. Kaiser SV, Rodean J, Bekmezian A, et al; Pediatric Research in Inpatient Settings (PRIS) Network. Effectiveness of pediatric asthma pathways for hospitalized children: a multicenter, national analysis. J Pediatr. 2018;197:165-171.e162. https://doi.org/10.1016/j.jpeds.2018.01.084
18. Feudtner C, Feinstein JA, Zhong W, Hall M, Dai D. Pediatric complex chronic conditions classification system version 2: updated for ICD-10 and complex medical technology dependence and transplantation. BMC Pediatr. 2014;14:199. https://doi.org/10.1186/1471-2431-14-199.
19. Williams DJ, Zhu Y, Grijalva CG, et al. Predicting severe pneumonia outcomes in children. Pediatrics. 2016;138(4):e20161019. https://doi.org/10.1542/peds.2016-1019
20. Zachariah P, Johnson CL, Halabi KC, et al. Epidemiology, clinical features, and disease severity in patients with coronavirus disease 2019 (COVID-19) in a children’s hospital in New York City, New York. JAMA Pediatr. 2020;174(10):e202430. https://doi.org/10.1001/jamapediatrics.2020.2430
21. DeBiasi RL, Song X, Delaney M, et al. Severe coronavirus disease-2019 in children and young adults in the Washington, DC, metropolitan region. J Pediatr. 2020;223:199-203.e191. https://doi.org/10.1016/j.jpeds.2020.05.007
22. Lovinsky-Desir S, Deshpande DR, De A, et al. Asthma among hospitalized patients with COVID-19 and related outcomes. J Allergy Clin Immunol. 2020;146(5):1027-1034.e1024. https://doi.org/10.1016/j.jaci.2020.07.026
23. Beken B, Ozturk GK, Aygun FD, Aydogmus C, Akar HH. Asthma and allergic diseases are not risk factors for hospitalization in children with coronavirus disease 2019. Ann Allergy Asthma Immunol. 2021;126(5):569-575. https://doi.org/10.1016/j.anai.2021.01.018
24. Yehia BR, Winegar A, Fogel R, et al. Association of race with mortality among patients hospitalized with coronavirus disease 2019 (COVID-19) at 92 US hospitals. JAMA Netw Open. 2020;3(8):e2018039. https://doi.org/10.1001/jamanetworkopen.2020.18039
25. Saatci D, Ranger TA, Garriga C, et al. Association between race and COVID-19 outcomes among 2.6 million children in England. JAMA Pediatr. 2021;e211685. https://doi.org/10.1001/jamapediatrics.2021.1685
26. Lopez L, 3rd, Hart LH, 3rd, Katz MH. Racial and ethnic health disparities related to COVID-19. JAMA. 2021;325(8):719-720. https://doi.org/10.1001/jama.2020.26443
27. Altunok ES, Alkan M, Kamat S, et al. Clinical characteristics of adult patients hospitalized with laboratory-confirmed COVID-19 pneumonia. J Infect Chemother. 2020. https://doi.org/10.1016/j.jiac.2020.10.020
28. Ali H, Daoud A, Mohamed MM, et al. Survival rate in acute kidney injury superimposed COVID-19 patients: a systematic review and meta-analysis. Ren Fail. 2020;42(1):393-397. https://doi.org/10.1080/0886022x.2020.1756323
29. Anirvan P, Bharali P, Gogoi M, Thuluvath PJ, Singh SP, Satapathy SK. Liver injury in COVID-19: the hepatic aspect of the respiratory syndrome - what we know so far. World J Hepatol. 2020;12(12):1182-1197. https://doi.org/10.4254/wjh.v12.i12.1182
30. Moschonas IC, Tselepis AD. SARS-CoV-2 infection and thrombotic complications: a narrative review. J Thromb Thrombolysis. 2021;52(1):111-123. https://doi.org/10.1007/s11239-020-02374-3
31. Lee MH, Perl DP, Nair G, et al. Microvascular injury in the brains of patients with Covid-19. N Engl J Med. 2020;384(5):481-483. https://doi.org/10.1056/nejmc2033369
32. Antoon JW, Hall M, Herndon A, et al. Prevalence, risk factors, and outcomes of influenza-associated neurological Complications in Children. J Pediatr. 2021;S0022-3476(21)00657-0. https://doi.org/10.1016/j.jpeds.2021.06.075

References

1. Centers for Disease Control and Prevention. COVID data tracker. Accessed September 9, 2021. https://covid.cdc.gov/covid-data-tracker/#datatracker-home
2. Levy C, Basmaci R, Bensaid P, et al. Changes in reverse transcription polymerase chain reaction-positive severe acute respiratory syndrome coronavirus 2 rates in adults and children according to the epidemic stages. Pediatr Infect Dis J. 2020;39(11):e369-e372. https://doi.org/10.1097/inf.0000000000002861
3. Gudbjartsson DF, Helgason A, Jonsson H, et al. Spread of SARS-CoV-2 in the Icelandic population. N Engl J Med. 2020;382(24):2302-2315. https://doi.org/10.1056/nejmoa2006100
4. Garg S, Kim L, Whitaker M, et al. Hospitalization rates and characteristics of patients hospitalized with laboratory-confirmed coronavirus disease 2019 - COVID-NET, 14 States, March 1-30, 2020. MMWR Morb Mortal Wkly Rep. 2020;69(15):458-464. https://doi.org/10.15585/mmwr.mm6915e3
5. Castagnoli R, Votto M, Licari A, et al. Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection in children and adolescents: a systematic review. JAMA Pediatr. 2020;174(9):882-889. https://doi.org/10.1001/jamapediatrics.2020.1467
6. Feldstein LR, Rose EB, Horwitz SM, et al; Overcoming COVID-19 Investigators; CDC COVID-19 Response Team. Multisystem inflammatory syndrome in U.S. children and adolescents. N Engl J Med. 2020;383(4):334-346. https://doi.org/10.1056/nejmoa2021680
7. Magro B, Zuccaro V, Novelli L, et al. Predicting in-hospital mortality from coronavirus disease 2019: a simple validated app for clinical use. PLoS One. 2021;16(1):e0245281. https://doi.org/10.1371/journal.pone.0245281
8. Helms J, Kremer S, Merdji H, et al. Neurologic features in severe SARS-CoV-2 infection. N Engl J Med. 2020;382(23):2268-2270. https://doi.org/10.1056/nejmc2008597
9. Severe Covid GWAS Group; Ellinghaus D, Degenhardt F, Bujanda L, et al. Genomewide association study of severe Covid-19 with respiratory failure. N Engl J Med. 2020;383(16):1522-1534.
10. Kabarriti R, Brodin NP, Maron MI, et al. association of race and ethnicity with comorbidities and survival among patients with COVID-19 at an urban medical center in New York. JAMA Netw Open. 2020;3(9):e2019795. https://doi.org/10.1001/jamanetworkopen.2020.19795
11. Bellino S, Punzo O, Rota MC, et al; COVID-19 Working Group. COVID-19 disease severity risk factors for pediatric patients in Italy. Pediatrics. 2020;146(4):e2020009399. https://doi.org/10.1542/peds.2020-009399
12. Ouldali N, Yang DD, Madhi F, et al; investigator group of the PANDOR study. Factors associated with severe SARS-CoV-2 infection. Pediatrics. 2020;147(3):e2020023432. https://doi.org/10.1542/peds.2020-023432
13. Castells MC, Phillips EJ. Maintaining safety with SARS-CoV-2 vaccines. N Engl J Med. 2021;384(7):643-649. https://doi.org/10.1056/nejmra2035343
14. Antoon JW, Williams DJ, Thurm C, et al. The COVID-19 pandemic and changes in healthcare utilization for pediatric respiratory and nonrespiratory illnesses in the United States. J Hosp Med. 2021;16(5):294-297. https://doi.org/10.12788/jhm.3608
15. Blatz AM, David MZ, Otto WR, Luan X, Gerber JS. Validation of International Classification of Disease-10 code for identifying children hospitalized with coronavirus disease-2019. J Pediatric Infect Dis Soc. 2020;10(4):547-548. https://doi.org/10.1093/jpids/piaa140
16. Kadri SS, Gundrum J, Warner S, et al. Uptake and accuracy of the diagnosis code for COVID-19 among US hospitalizations. JAMA. 2020;324(24):2553-2554. https://doi.org/10.1001/jama.2020.20323
17. Kaiser SV, Rodean J, Bekmezian A, et al; Pediatric Research in Inpatient Settings (PRIS) Network. Effectiveness of pediatric asthma pathways for hospitalized children: a multicenter, national analysis. J Pediatr. 2018;197:165-171.e162. https://doi.org/10.1016/j.jpeds.2018.01.084
18. Feudtner C, Feinstein JA, Zhong W, Hall M, Dai D. Pediatric complex chronic conditions classification system version 2: updated for ICD-10 and complex medical technology dependence and transplantation. BMC Pediatr. 2014;14:199. https://doi.org/10.1186/1471-2431-14-199.
19. Williams DJ, Zhu Y, Grijalva CG, et al. Predicting severe pneumonia outcomes in children. Pediatrics. 2016;138(4):e20161019. https://doi.org/10.1542/peds.2016-1019
20. Zachariah P, Johnson CL, Halabi KC, et al. Epidemiology, clinical features, and disease severity in patients with coronavirus disease 2019 (COVID-19) in a children’s hospital in New York City, New York. JAMA Pediatr. 2020;174(10):e202430. https://doi.org/10.1001/jamapediatrics.2020.2430
21. DeBiasi RL, Song X, Delaney M, et al. Severe coronavirus disease-2019 in children and young adults in the Washington, DC, metropolitan region. J Pediatr. 2020;223:199-203.e191. https://doi.org/10.1016/j.jpeds.2020.05.007
22. Lovinsky-Desir S, Deshpande DR, De A, et al. Asthma among hospitalized patients with COVID-19 and related outcomes. J Allergy Clin Immunol. 2020;146(5):1027-1034.e1024. https://doi.org/10.1016/j.jaci.2020.07.026
23. Beken B, Ozturk GK, Aygun FD, Aydogmus C, Akar HH. Asthma and allergic diseases are not risk factors for hospitalization in children with coronavirus disease 2019. Ann Allergy Asthma Immunol. 2021;126(5):569-575. https://doi.org/10.1016/j.anai.2021.01.018
24. Yehia BR, Winegar A, Fogel R, et al. Association of race with mortality among patients hospitalized with coronavirus disease 2019 (COVID-19) at 92 US hospitals. JAMA Netw Open. 2020;3(8):e2018039. https://doi.org/10.1001/jamanetworkopen.2020.18039
25. Saatci D, Ranger TA, Garriga C, et al. Association between race and COVID-19 outcomes among 2.6 million children in England. JAMA Pediatr. 2021;e211685. https://doi.org/10.1001/jamapediatrics.2021.1685
26. Lopez L, 3rd, Hart LH, 3rd, Katz MH. Racial and ethnic health disparities related to COVID-19. JAMA. 2021;325(8):719-720. https://doi.org/10.1001/jama.2020.26443
27. Altunok ES, Alkan M, Kamat S, et al. Clinical characteristics of adult patients hospitalized with laboratory-confirmed COVID-19 pneumonia. J Infect Chemother. 2020. https://doi.org/10.1016/j.jiac.2020.10.020
28. Ali H, Daoud A, Mohamed MM, et al. Survival rate in acute kidney injury superimposed COVID-19 patients: a systematic review and meta-analysis. Ren Fail. 2020;42(1):393-397. https://doi.org/10.1080/0886022x.2020.1756323
29. Anirvan P, Bharali P, Gogoi M, Thuluvath PJ, Singh SP, Satapathy SK. Liver injury in COVID-19: the hepatic aspect of the respiratory syndrome - what we know so far. World J Hepatol. 2020;12(12):1182-1197. https://doi.org/10.4254/wjh.v12.i12.1182
30. Moschonas IC, Tselepis AD. SARS-CoV-2 infection and thrombotic complications: a narrative review. J Thromb Thrombolysis. 2021;52(1):111-123. https://doi.org/10.1007/s11239-020-02374-3
31. Lee MH, Perl DP, Nair G, et al. Microvascular injury in the brains of patients with Covid-19. N Engl J Med. 2020;384(5):481-483. https://doi.org/10.1056/nejmc2033369
32. Antoon JW, Hall M, Herndon A, et al. Prevalence, risk factors, and outcomes of influenza-associated neurological Complications in Children. J Pediatr. 2021;S0022-3476(21)00657-0. https://doi.org/10.1016/j.jpeds.2021.06.075

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The COVID-19 Pandemic and Changes in Healthcare Utilization for Pediatric Respiratory and Nonrespiratory Illnesses in the United States

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The COVID-19 Pandemic and Changes in Healthcare Utilization for Pediatric Respiratory and Nonrespiratory Illnesses in the United States

In the United States, respiratory illnesses are the most common cause of emergency department (ED) visits and hospitalizations in children.1 In response to the ongoing COVID-19 pandemic, several public health interventions, including school and business closures, stay-at-home orders, and mask mandates, were implemented to limit transmission of SARS-CoV-2.2,3 Studies have shown that children can contribute to the spread of SARS-CoV-2 infections, especially within households.4-6 Recent data suggest that COVID-19, and the associated public health measures enacted to slow its spread, may have affected the transmission of other respiratory pathogens.7 Similarly, the pandemic has likely affected healthcare utilization for nonrespiratory illnesses through adoption of social distancing recommendations, suspension and delays in nonemergent elective care, avoidance of healthcare settings, and the effect of decreased respiratory disease on exacerbation of chronic illness.8 The objective of this study was to examine associations between the COVID-19 pandemic and healthcare utilization for pediatric respiratory and nonrespiratory illnesses at US pediatric hospitals.

METHODS

Study Design

This is a multicenter, cross-sectional study of encounters at 44 pediatric hospitals that reported data to the Pediatric Health Information System (PHIS) database maintained by the Children’s Hospital Association (Lenexa, Kansas).

Study Population

Children 2 months to 18 years of age discharged from ED or inpatient settings with a nonsurgical diagnosis from January 1 to September 30 over a 4-year period (2017-2020) were included.

Exposure

The primary exposure was the 2020 COVID-19 pandemic time, divided into three periods: pre-COVID-19 (January-February 2020, the period prior to the pandemic in the United States), early COVID-19 (March-April 2020, coinciding with the first reported US pediatric case of COVID-19 on March 2, 2020), and COVID-19 (May-September 2020, marked by the implementation of at least two of the following containment measures in every US state: stay-at-home/shelter orders, school closures, nonessential business closures, restaurant closures, or prohibition of gatherings of more than 10 people).2

Outcomes

Respiratory illness diagnoses were classified into mutually exclusive subgroups following a prespecified hierarchy: influenza, pneumonia, croup, bronchiolitis, asthma, unspecified influenza-like illness, and “other respiratory diagnoses” (Appendix Table 1). To assess the impact of COVID-19 after its International Classification of Diseases, Tenth Revision code was established on March 25, 2020, the “other respiratory” subgroup was divided into other respiratory illnesses with and without COVID-19. Nonrespiratory illness diagnoses were defined as all diagnoses not included in the respiratory illness cohort.

Statistical Analysis

Categorical variables were summarized using frequencies and percentages and compared using chi-square tests. Continuous variables were summarized as median and interquartile range (IQR) and compared using Wilcoxon rank sum tests. Weekly observed-to-expected (O:E) ratios were calculated for each hospital by dividing the number of observed respiratory illness and nonrespiratory illness encounters in a given week in 2020 (observed) by the average number of encounters for that same week during 2017-2019 (expected). O:E ratios were then aggregated over the three COVID-19 study periods, and 95% confidence intervals were established around mean O:E ratios across individual hospitals. Outcomes were then stratified by respiratory illness subgroups, geographic region, and age. Additional details can be found in the Supplemental Methods in the Appendix.

RESULTS

Study Population

A total of 9,051,980 encounters were included in the study, 6,811,799 with nonrespiratory illnesses and 2,240,181 with respiratory illnesses. Median age was 5 years (IQR, 1-11 years), and 52.7% of the population was male (Appendix Table 2 and Appendix Table 3).

Respiratory vs Nonrespiratory Illness During the COVID-19 Pandemic

Over the study period, fewer respiratory and nonrespiratory illness encounters were observed than expected, with a larger decrease in respiratory illness encounters (Table, Appendix Table 4).

Observed-to-Expected Encounter Ratios During COVID-19 Pandemic
The initial decrease occurred between March 12 and April 9, 2020, with relative stability until a subsequent rise in encounters between May 28 and July 9. After July 9, respiratory illness encounters decreased compared with a relatively stable trend in nonrespiratory illness encounters (Figure). The O:E ratios for respiratory illnesses during the study periods were: pre-COVID-19, 1.13 (95% CI, 1.07-1.19); early COVID-19, 0.57 (95% CI, 0.54-0.60); and COVID-19, 0.38 (95% CI, 0.35-0.41). Comparatively, the O:E ratios for nonrespiratory illnesses were 1.03 (95% CI, 1.01-1.06), 0.54 (95% CI, 0.52-0.56), and 0.62 (95% CI, 0.59-0.66) over the same periods (Table, Appendix Table 4).

Respiratory and Nonrespiratory Illness at Children’s Hospitals During the COVID-19 Period

Respiratory Subgroup Analyses

The O:E ratio decreased for all respiratory subgroups over the study period (Table, Appendix Table 4). There were significant differences in specific respiratory subgroups, including asthma, bronchiolitis, croup, influenza, and pneumonia (Appendix Figure 1A). Temporal trends in respiratory encounters were consistent across hospital settings, ages, and geographic regions (Appendix Figure 1B-D). When comparing the with and without COVID-19 subgroups in the “other respiratory illnesses” cohort, other respiratory illness without COVID-19 decreased and remained lower than expected over the rest of the study period, while other respiratory illness with COVID-19 increased markedly during the summer months and declined thereafter (Appendix Figure 2).

All age groups had reductions in respiratory illness encounters during the early COVID-19 and COVID-19 periods, although the decline was less pronounced in the 12- to 17-year-old group (Appendix Figure 1B). Similarly, while all age groups experienced increases in encounters for respiratory illnesses during the summer months, only children in the 12- to 17-year-old group experienced increases beyond pre-COVID-19 levels. Importantly, this increase in respiratory encounters was largely driven by COVID-19 diagnoses (Appendix Figure 3). The trend in nonrespiratory illness encounters stratified by age is shown in Appendix Figure 4.

When patients were stratified by hospital setting, there were no differences between those hospitalized and those discharged from the ED (Appendix Figure 1C). Patterns in respiratory illnesses by geographic location were qualitatively similar until the beginning of the summer 2020, after which geographical variation became more evident (Appendix Figure 1D).

DISCUSSION

In this large, multicenter study evaluating ED visits and hospitalizations for respiratory and nonrespiratory illnesses at US pediatric hospitals during the 2020 COVID-19 pandemic, we found a significant and substantial decrease in healthcare encounters for respiratory illnesses. A rapid and marked decline in encounters for respiratory illness in a relatively short period of time (March 12-April 2) was observed across all hospitals and US regions. Declines were consistent across common respiratory illnesses. More modest, yet still substantial, declines were also observed for nonrespiratory illnesses.

There are likely multiple underlying reasons for the observed reductions. Social distancing measures almost certainly played an important role in interrupting respiratory infection transmission. Rapid reduction in influenza transmission during the early COVID-19 period has been attributed to social distancing measures,3 and influenza transmission in children decreases with school closures.9 It is also possible that some families delayed seeking care at hospitals due to COVID-19, leading to less frequent encounters but more severe illness. The similar decrease in O:E ratio for ED visits and hospitalizations, however, is inconsistent with this explanation. It is also possible that nonurgent conditions cared for in the hospital settings were diverted to other care settings. For example, during this pandemic, telehealth and telephone visits for pediatric asthma increased by 61% and 19%, respectively, while ED and outpatient visits decreased concurrently.10Similar changes in location of care may also contribute to the decline in nonrespiratory illness encounters. Decreased use of hospital resources for nonurgent care diagnoses during the pandemic would suggest that, prior to COVID-19, there was overutilization of ambulatory services at children’s hospitals. Therefore, the pandemic may be driving care to more appropriate settings.

We also found relative differences in changes in encounters for respiratory illness by age. Adolescents’ levels of respiratory healthcare use declined less and recovered at a faster rate than those of younger children, returning to pre-COVID-19 levels by the end of the study period. The reason for this age differential is likely multifaceted. Infections, such as bronchiolitis and pneumonia, are more likely to be a source of respiratory illness in younger than in older children. It is also likely that disproportionate relaxation of social distancing measures among adolescents, who are known to have a stronger pattern of social interaction, contributed to the faster rise in respiratory illness–related encounters in this age group.11 Adolescents have been reported to be more susceptible to, and more likely to transmit, SARS-CoV-2 compared to younger age groups.12 More modest, albeit similar, age-based changes were observed in encounters for nonrespiratory illnesses. It is possible that pandemic-related stressors resulted in a subsequent increase in mental health encounters among this age group.13 While the reason for this also is likely multifactorial, adolescent behavior, as well as transmission of infectious illness that can exacerbate nonrespiratory conditions, may be a factor.

Emerging evidence suggests that school-age children may play an important role in SARS-CoV-2 transmission in the community.4,14 Our finding that, compared to younger children, adolescents had significantly fewer reductions in respiratory illness encounters is concerning. These findings suggest that community-based efforts to help prevent respiratory illnesses, especially COVID-19, should focus on adolescents, who are most likely to maintain social interactions and transmit respiratory infections in the school setting and their households.

This study is limited by the inclusion of only tertiary care children’s hospitals, which may not be nationally representative, and the inability to assess the precise timing of when specific public health interventions were introduced. Moreover, previous studies suggest that social distancing behaviors may have changed even before formal recommendations were enacted.15 Future studies should investigate the local impact of state- and municipality-specific mandates on the burden of COVID-19 and other respiratory illnesses.

The COVID-19 pandemic was associated with substantial reductions in encounters for respiratory diseases, and also with more modest but still sizable reductions in encounters for nonrespiratory diseases. These reductions varied by age. Encounters among adolescents declined less and returned to previous levels faster compared with those of younger children.

ACKNOWLEDGMENT

This publication is dedicated to the memory of our coauthor, Dr. Michael Bendel-Stenzel. Dr. Bendel-Stenzel was dedicated to bettering the lives of children and advancing our knowledge of pediatrics through his research.

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References

1. Leyenaar JK, Ralston SL, Shieh MS, Pekow PS, Mangione-Smith R, Lindenauer PK. Epidemiology of pediatric hospitalizations at general hospitals and freestanding children’s hospitals in the United States. J Hosp Med. 2016;11(11):743-749. https://doi.org/10.1002/jhm.2624
2. Auger KA, Shah SS, Richardson T, et al. Association between statewide school closure and COVID-19 incidence and mortality in the US. JAMA. 2020;324(9):859-870. https://doi.org/10.1001/jama.2020.14348
3. Wiese AD, Everson J, Grijalva CG. Social distancing measures: evidence of interruption of seasonal influenza activity and early lessons of the SARS-CoV-2 pandemic. Clin Infect Dis. Published online June 20, 2020. https://doi.org/10.1093/cid/ciaa834
4. Grijalva CG, Rolfes MA, Zhu Y, et al. Transmission of SARS-COV-2 infections in households - Tennessee and Wisconsin, April-September 2020. MMWR Morb Mortal Wkly Rep. 2020;69(44):1631-1634. https://doi.org/10.15585/mmwr.mm6944e1
5. Worby CJ, Chaves SS, Wallinga J, Lipsitch M, Finelli L, Goldstein E. On the relative role of different age groups in influenza epidemics. Epidemics. 2015;13:10-16. https://doi.org/10.1016/j.epidem.2015.04.003
6. Zimmerman KO, Akinboyo IC, Brookhart MA, et al. Incidence and secondary transmission of SARS-CoV-2 infections in schools. Pediatrics. Published online January 8, 2021. https://doi.org/10.1542/peds.2020-048090
7. Hatoun J, Correa ET, Donahue SMA, Vernacchio L. Social distancing for COVID-19 and diagnoses of other infectious diseases in children. Pediatrics. 2020;146(4):e2020006460. https://doi.org/10.1542/peds.2020-006460
8. Chaiyachati BH, Agawu A, Zorc JJ, Balamuth F. Trends in pediatric emergency department utilization after institution of coronavirus disease-19 mandatory social distancing. J Pediatr. 2020;226:274-277.e1. https://doi.org/10.1016/j.jpeds.2020.07.048
9. Luca G, Kerckhove KV, Coletti P, et al. The impact of regular school closure on seasonal influenza epidemics: a data-driven spatial transmission model for Belgium. BMC Infect Dis. 2018;18(1):29. https://doi.org/10.1186/s12879-017-2934-3
10. Taquechel K, Diwadkar AR, Sayed S, et al. Pediatric asthma healthcare utilization, viral testing, and air pollution changes during the COVID-19 pandemic. J Allergy Clin Immunol Pract. 2020;8(10):3378-3387.e11. https://doi.org/10.1016/j.jaip.2020.07.057
11. Park YJ, Choe YJ, Park O, et al. Contact tracing during coronavirus disease outbreak, South Korea, 2020. Emerg Infect Dis. 2020;26(10):2465-2468. https://doi.org/10.3201/eid2610.201315
12. Davies NG, Klepac P, Liu Y, et al. Age-dependent effects in the transmission and control of COVID-19 epidemics. Nat Med. 2020;26(8):1205-1211. https://doi.org/10.1038/s41591-020-0962-9
13. Hill RM, Rufino K, Kurian S, Saxena J, Saxena K, Williams L. Suicide ideation and attempts in a pediatric emergency department before and during COVID-19. Pediatrics. Published online December 16, 2020. https://doi.org/10.1542/peds.2020-029280
14. Flasche S, Edmunds WJ. The role of schools and school-aged children in SARS-CoV-2 transmission. Lancet Infect Dis. Published online December 8, 2020. https://doi.org/10.1016/S1473-3099(20)30927-0
15. Sehra ST, George M, Wiebe DJ, Fundin S, Baker JF. Cell phone activity in categories of places and associations with growth in cases of COVID-19 in the US. JAMA Intern Med. Published online August 31, 2020. https://doi.org/10.1001/jamainternmed.2020.4288

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1Division of Hospital Medicine, Monroe Carell Jr. Children’s Hospital at Vanderbilt and Department of Pediatrics, Vanderbilt University School of Medicine, Nashville, Tennessee; 2Children’s Hospital Association, Lenexa, Kansas; 3Children’s Minnesota Research Institute, Minneapolis, Minnesota; 4Department of Pediatrics, Medical University of South Carolina, Charleston, South Carolina; 5Department of Pediatrics, Division of Hospital Medicine, Nicklaus Children’s Hospital, Miami, Florida; 6Divisions of Hospital Medicine and Infectious Diseases, Cincinnati Children’s Hospital Medical Center & Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio; 7Center for Pediatric Clinical Effectiveness, Children’s Hospital of Philadelphia and University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania; 8Division of Infectious Diseases, Department of Pediatrics, University of Utah, Salt Lake City, Utah; 9Division of Emergency Medicine, Ann and Robert H. Lurie Children’s Hospital of Chicago & Department of Pediatrics, Northwestern University Feinberg School of Medicine, Chicago, Illinois; 10Department of Health Policy, Vanderbilt University Medical Center, Nashville, Tennessee.

Disclosures

Dr Spaulding is supported by a grant from the University of Minnesota Clinical and Translational Science Institute, Children’s Minnesota, and the University of Minnesota Department of Pediatrics Child Health COVID-19 Collaborative Grant, which are paid to her institution and are outside the submitted work. Dr. Florin is supported by grants from the National Institute of Allergy and Infectious Diseases and the National Heart, Lung, and Blood Institute paid to his institution and are outside the submitted work. Dr. Grijalva reports receiving consulting fees from Pfizer, Merck, and Sanofi-Pasteur as well as grants from Campbell Alliance, the Centers for Disease Control and Prevention, National Institutes of Health, grants US Food and Drug Administration, the Agency for Health Care Research and Quality, and Sanofi, outside the submitted work. No other disclosures were reported.

Funding

Research reported in this publication was supported by the National Heart, Lung, and Blood Institute of the National Institutes of Health under Award Numbers K12 HL137943 (Dr. Antoon) and K23HL136842 (Dr. Kenyon), and National Institute of Allergy and Infectious Diseases Award Numbers K24 AI148459 (Dr. Grijalva) and R01 AI125642 (Dr. Williams). The National Institutes of Health had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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1Division of Hospital Medicine, Monroe Carell Jr. Children’s Hospital at Vanderbilt and Department of Pediatrics, Vanderbilt University School of Medicine, Nashville, Tennessee; 2Children’s Hospital Association, Lenexa, Kansas; 3Children’s Minnesota Research Institute, Minneapolis, Minnesota; 4Department of Pediatrics, Medical University of South Carolina, Charleston, South Carolina; 5Department of Pediatrics, Division of Hospital Medicine, Nicklaus Children’s Hospital, Miami, Florida; 6Divisions of Hospital Medicine and Infectious Diseases, Cincinnati Children’s Hospital Medical Center & Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio; 7Center for Pediatric Clinical Effectiveness, Children’s Hospital of Philadelphia and University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania; 8Division of Infectious Diseases, Department of Pediatrics, University of Utah, Salt Lake City, Utah; 9Division of Emergency Medicine, Ann and Robert H. Lurie Children’s Hospital of Chicago & Department of Pediatrics, Northwestern University Feinberg School of Medicine, Chicago, Illinois; 10Department of Health Policy, Vanderbilt University Medical Center, Nashville, Tennessee.

Disclosures

Dr Spaulding is supported by a grant from the University of Minnesota Clinical and Translational Science Institute, Children’s Minnesota, and the University of Minnesota Department of Pediatrics Child Health COVID-19 Collaborative Grant, which are paid to her institution and are outside the submitted work. Dr. Florin is supported by grants from the National Institute of Allergy and Infectious Diseases and the National Heart, Lung, and Blood Institute paid to his institution and are outside the submitted work. Dr. Grijalva reports receiving consulting fees from Pfizer, Merck, and Sanofi-Pasteur as well as grants from Campbell Alliance, the Centers for Disease Control and Prevention, National Institutes of Health, grants US Food and Drug Administration, the Agency for Health Care Research and Quality, and Sanofi, outside the submitted work. No other disclosures were reported.

Funding

Research reported in this publication was supported by the National Heart, Lung, and Blood Institute of the National Institutes of Health under Award Numbers K12 HL137943 (Dr. Antoon) and K23HL136842 (Dr. Kenyon), and National Institute of Allergy and Infectious Diseases Award Numbers K24 AI148459 (Dr. Grijalva) and R01 AI125642 (Dr. Williams). The National Institutes of Health had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Author and Disclosure Information

1Division of Hospital Medicine, Monroe Carell Jr. Children’s Hospital at Vanderbilt and Department of Pediatrics, Vanderbilt University School of Medicine, Nashville, Tennessee; 2Children’s Hospital Association, Lenexa, Kansas; 3Children’s Minnesota Research Institute, Minneapolis, Minnesota; 4Department of Pediatrics, Medical University of South Carolina, Charleston, South Carolina; 5Department of Pediatrics, Division of Hospital Medicine, Nicklaus Children’s Hospital, Miami, Florida; 6Divisions of Hospital Medicine and Infectious Diseases, Cincinnati Children’s Hospital Medical Center & Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio; 7Center for Pediatric Clinical Effectiveness, Children’s Hospital of Philadelphia and University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania; 8Division of Infectious Diseases, Department of Pediatrics, University of Utah, Salt Lake City, Utah; 9Division of Emergency Medicine, Ann and Robert H. Lurie Children’s Hospital of Chicago & Department of Pediatrics, Northwestern University Feinberg School of Medicine, Chicago, Illinois; 10Department of Health Policy, Vanderbilt University Medical Center, Nashville, Tennessee.

Disclosures

Dr Spaulding is supported by a grant from the University of Minnesota Clinical and Translational Science Institute, Children’s Minnesota, and the University of Minnesota Department of Pediatrics Child Health COVID-19 Collaborative Grant, which are paid to her institution and are outside the submitted work. Dr. Florin is supported by grants from the National Institute of Allergy and Infectious Diseases and the National Heart, Lung, and Blood Institute paid to his institution and are outside the submitted work. Dr. Grijalva reports receiving consulting fees from Pfizer, Merck, and Sanofi-Pasteur as well as grants from Campbell Alliance, the Centers for Disease Control and Prevention, National Institutes of Health, grants US Food and Drug Administration, the Agency for Health Care Research and Quality, and Sanofi, outside the submitted work. No other disclosures were reported.

Funding

Research reported in this publication was supported by the National Heart, Lung, and Blood Institute of the National Institutes of Health under Award Numbers K12 HL137943 (Dr. Antoon) and K23HL136842 (Dr. Kenyon), and National Institute of Allergy and Infectious Diseases Award Numbers K24 AI148459 (Dr. Grijalva) and R01 AI125642 (Dr. Williams). The National Institutes of Health had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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Related Articles

In the United States, respiratory illnesses are the most common cause of emergency department (ED) visits and hospitalizations in children.1 In response to the ongoing COVID-19 pandemic, several public health interventions, including school and business closures, stay-at-home orders, and mask mandates, were implemented to limit transmission of SARS-CoV-2.2,3 Studies have shown that children can contribute to the spread of SARS-CoV-2 infections, especially within households.4-6 Recent data suggest that COVID-19, and the associated public health measures enacted to slow its spread, may have affected the transmission of other respiratory pathogens.7 Similarly, the pandemic has likely affected healthcare utilization for nonrespiratory illnesses through adoption of social distancing recommendations, suspension and delays in nonemergent elective care, avoidance of healthcare settings, and the effect of decreased respiratory disease on exacerbation of chronic illness.8 The objective of this study was to examine associations between the COVID-19 pandemic and healthcare utilization for pediatric respiratory and nonrespiratory illnesses at US pediatric hospitals.

METHODS

Study Design

This is a multicenter, cross-sectional study of encounters at 44 pediatric hospitals that reported data to the Pediatric Health Information System (PHIS) database maintained by the Children’s Hospital Association (Lenexa, Kansas).

Study Population

Children 2 months to 18 years of age discharged from ED or inpatient settings with a nonsurgical diagnosis from January 1 to September 30 over a 4-year period (2017-2020) were included.

Exposure

The primary exposure was the 2020 COVID-19 pandemic time, divided into three periods: pre-COVID-19 (January-February 2020, the period prior to the pandemic in the United States), early COVID-19 (March-April 2020, coinciding with the first reported US pediatric case of COVID-19 on March 2, 2020), and COVID-19 (May-September 2020, marked by the implementation of at least two of the following containment measures in every US state: stay-at-home/shelter orders, school closures, nonessential business closures, restaurant closures, or prohibition of gatherings of more than 10 people).2

Outcomes

Respiratory illness diagnoses were classified into mutually exclusive subgroups following a prespecified hierarchy: influenza, pneumonia, croup, bronchiolitis, asthma, unspecified influenza-like illness, and “other respiratory diagnoses” (Appendix Table 1). To assess the impact of COVID-19 after its International Classification of Diseases, Tenth Revision code was established on March 25, 2020, the “other respiratory” subgroup was divided into other respiratory illnesses with and without COVID-19. Nonrespiratory illness diagnoses were defined as all diagnoses not included in the respiratory illness cohort.

Statistical Analysis

Categorical variables were summarized using frequencies and percentages and compared using chi-square tests. Continuous variables were summarized as median and interquartile range (IQR) and compared using Wilcoxon rank sum tests. Weekly observed-to-expected (O:E) ratios were calculated for each hospital by dividing the number of observed respiratory illness and nonrespiratory illness encounters in a given week in 2020 (observed) by the average number of encounters for that same week during 2017-2019 (expected). O:E ratios were then aggregated over the three COVID-19 study periods, and 95% confidence intervals were established around mean O:E ratios across individual hospitals. Outcomes were then stratified by respiratory illness subgroups, geographic region, and age. Additional details can be found in the Supplemental Methods in the Appendix.

RESULTS

Study Population

A total of 9,051,980 encounters were included in the study, 6,811,799 with nonrespiratory illnesses and 2,240,181 with respiratory illnesses. Median age was 5 years (IQR, 1-11 years), and 52.7% of the population was male (Appendix Table 2 and Appendix Table 3).

Respiratory vs Nonrespiratory Illness During the COVID-19 Pandemic

Over the study period, fewer respiratory and nonrespiratory illness encounters were observed than expected, with a larger decrease in respiratory illness encounters (Table, Appendix Table 4).

Observed-to-Expected Encounter Ratios During COVID-19 Pandemic
The initial decrease occurred between March 12 and April 9, 2020, with relative stability until a subsequent rise in encounters between May 28 and July 9. After July 9, respiratory illness encounters decreased compared with a relatively stable trend in nonrespiratory illness encounters (Figure). The O:E ratios for respiratory illnesses during the study periods were: pre-COVID-19, 1.13 (95% CI, 1.07-1.19); early COVID-19, 0.57 (95% CI, 0.54-0.60); and COVID-19, 0.38 (95% CI, 0.35-0.41). Comparatively, the O:E ratios for nonrespiratory illnesses were 1.03 (95% CI, 1.01-1.06), 0.54 (95% CI, 0.52-0.56), and 0.62 (95% CI, 0.59-0.66) over the same periods (Table, Appendix Table 4).

Respiratory and Nonrespiratory Illness at Children’s Hospitals During the COVID-19 Period

Respiratory Subgroup Analyses

The O:E ratio decreased for all respiratory subgroups over the study period (Table, Appendix Table 4). There were significant differences in specific respiratory subgroups, including asthma, bronchiolitis, croup, influenza, and pneumonia (Appendix Figure 1A). Temporal trends in respiratory encounters were consistent across hospital settings, ages, and geographic regions (Appendix Figure 1B-D). When comparing the with and without COVID-19 subgroups in the “other respiratory illnesses” cohort, other respiratory illness without COVID-19 decreased and remained lower than expected over the rest of the study period, while other respiratory illness with COVID-19 increased markedly during the summer months and declined thereafter (Appendix Figure 2).

All age groups had reductions in respiratory illness encounters during the early COVID-19 and COVID-19 periods, although the decline was less pronounced in the 12- to 17-year-old group (Appendix Figure 1B). Similarly, while all age groups experienced increases in encounters for respiratory illnesses during the summer months, only children in the 12- to 17-year-old group experienced increases beyond pre-COVID-19 levels. Importantly, this increase in respiratory encounters was largely driven by COVID-19 diagnoses (Appendix Figure 3). The trend in nonrespiratory illness encounters stratified by age is shown in Appendix Figure 4.

When patients were stratified by hospital setting, there were no differences between those hospitalized and those discharged from the ED (Appendix Figure 1C). Patterns in respiratory illnesses by geographic location were qualitatively similar until the beginning of the summer 2020, after which geographical variation became more evident (Appendix Figure 1D).

DISCUSSION

In this large, multicenter study evaluating ED visits and hospitalizations for respiratory and nonrespiratory illnesses at US pediatric hospitals during the 2020 COVID-19 pandemic, we found a significant and substantial decrease in healthcare encounters for respiratory illnesses. A rapid and marked decline in encounters for respiratory illness in a relatively short period of time (March 12-April 2) was observed across all hospitals and US regions. Declines were consistent across common respiratory illnesses. More modest, yet still substantial, declines were also observed for nonrespiratory illnesses.

There are likely multiple underlying reasons for the observed reductions. Social distancing measures almost certainly played an important role in interrupting respiratory infection transmission. Rapid reduction in influenza transmission during the early COVID-19 period has been attributed to social distancing measures,3 and influenza transmission in children decreases with school closures.9 It is also possible that some families delayed seeking care at hospitals due to COVID-19, leading to less frequent encounters but more severe illness. The similar decrease in O:E ratio for ED visits and hospitalizations, however, is inconsistent with this explanation. It is also possible that nonurgent conditions cared for in the hospital settings were diverted to other care settings. For example, during this pandemic, telehealth and telephone visits for pediatric asthma increased by 61% and 19%, respectively, while ED and outpatient visits decreased concurrently.10Similar changes in location of care may also contribute to the decline in nonrespiratory illness encounters. Decreased use of hospital resources for nonurgent care diagnoses during the pandemic would suggest that, prior to COVID-19, there was overutilization of ambulatory services at children’s hospitals. Therefore, the pandemic may be driving care to more appropriate settings.

We also found relative differences in changes in encounters for respiratory illness by age. Adolescents’ levels of respiratory healthcare use declined less and recovered at a faster rate than those of younger children, returning to pre-COVID-19 levels by the end of the study period. The reason for this age differential is likely multifaceted. Infections, such as bronchiolitis and pneumonia, are more likely to be a source of respiratory illness in younger than in older children. It is also likely that disproportionate relaxation of social distancing measures among adolescents, who are known to have a stronger pattern of social interaction, contributed to the faster rise in respiratory illness–related encounters in this age group.11 Adolescents have been reported to be more susceptible to, and more likely to transmit, SARS-CoV-2 compared to younger age groups.12 More modest, albeit similar, age-based changes were observed in encounters for nonrespiratory illnesses. It is possible that pandemic-related stressors resulted in a subsequent increase in mental health encounters among this age group.13 While the reason for this also is likely multifactorial, adolescent behavior, as well as transmission of infectious illness that can exacerbate nonrespiratory conditions, may be a factor.

Emerging evidence suggests that school-age children may play an important role in SARS-CoV-2 transmission in the community.4,14 Our finding that, compared to younger children, adolescents had significantly fewer reductions in respiratory illness encounters is concerning. These findings suggest that community-based efforts to help prevent respiratory illnesses, especially COVID-19, should focus on adolescents, who are most likely to maintain social interactions and transmit respiratory infections in the school setting and their households.

This study is limited by the inclusion of only tertiary care children’s hospitals, which may not be nationally representative, and the inability to assess the precise timing of when specific public health interventions were introduced. Moreover, previous studies suggest that social distancing behaviors may have changed even before formal recommendations were enacted.15 Future studies should investigate the local impact of state- and municipality-specific mandates on the burden of COVID-19 and other respiratory illnesses.

The COVID-19 pandemic was associated with substantial reductions in encounters for respiratory diseases, and also with more modest but still sizable reductions in encounters for nonrespiratory diseases. These reductions varied by age. Encounters among adolescents declined less and returned to previous levels faster compared with those of younger children.

ACKNOWLEDGMENT

This publication is dedicated to the memory of our coauthor, Dr. Michael Bendel-Stenzel. Dr. Bendel-Stenzel was dedicated to bettering the lives of children and advancing our knowledge of pediatrics through his research.

In the United States, respiratory illnesses are the most common cause of emergency department (ED) visits and hospitalizations in children.1 In response to the ongoing COVID-19 pandemic, several public health interventions, including school and business closures, stay-at-home orders, and mask mandates, were implemented to limit transmission of SARS-CoV-2.2,3 Studies have shown that children can contribute to the spread of SARS-CoV-2 infections, especially within households.4-6 Recent data suggest that COVID-19, and the associated public health measures enacted to slow its spread, may have affected the transmission of other respiratory pathogens.7 Similarly, the pandemic has likely affected healthcare utilization for nonrespiratory illnesses through adoption of social distancing recommendations, suspension and delays in nonemergent elective care, avoidance of healthcare settings, and the effect of decreased respiratory disease on exacerbation of chronic illness.8 The objective of this study was to examine associations between the COVID-19 pandemic and healthcare utilization for pediatric respiratory and nonrespiratory illnesses at US pediatric hospitals.

METHODS

Study Design

This is a multicenter, cross-sectional study of encounters at 44 pediatric hospitals that reported data to the Pediatric Health Information System (PHIS) database maintained by the Children’s Hospital Association (Lenexa, Kansas).

Study Population

Children 2 months to 18 years of age discharged from ED or inpatient settings with a nonsurgical diagnosis from January 1 to September 30 over a 4-year period (2017-2020) were included.

Exposure

The primary exposure was the 2020 COVID-19 pandemic time, divided into three periods: pre-COVID-19 (January-February 2020, the period prior to the pandemic in the United States), early COVID-19 (March-April 2020, coinciding with the first reported US pediatric case of COVID-19 on March 2, 2020), and COVID-19 (May-September 2020, marked by the implementation of at least two of the following containment measures in every US state: stay-at-home/shelter orders, school closures, nonessential business closures, restaurant closures, or prohibition of gatherings of more than 10 people).2

Outcomes

Respiratory illness diagnoses were classified into mutually exclusive subgroups following a prespecified hierarchy: influenza, pneumonia, croup, bronchiolitis, asthma, unspecified influenza-like illness, and “other respiratory diagnoses” (Appendix Table 1). To assess the impact of COVID-19 after its International Classification of Diseases, Tenth Revision code was established on March 25, 2020, the “other respiratory” subgroup was divided into other respiratory illnesses with and without COVID-19. Nonrespiratory illness diagnoses were defined as all diagnoses not included in the respiratory illness cohort.

Statistical Analysis

Categorical variables were summarized using frequencies and percentages and compared using chi-square tests. Continuous variables were summarized as median and interquartile range (IQR) and compared using Wilcoxon rank sum tests. Weekly observed-to-expected (O:E) ratios were calculated for each hospital by dividing the number of observed respiratory illness and nonrespiratory illness encounters in a given week in 2020 (observed) by the average number of encounters for that same week during 2017-2019 (expected). O:E ratios were then aggregated over the three COVID-19 study periods, and 95% confidence intervals were established around mean O:E ratios across individual hospitals. Outcomes were then stratified by respiratory illness subgroups, geographic region, and age. Additional details can be found in the Supplemental Methods in the Appendix.

RESULTS

Study Population

A total of 9,051,980 encounters were included in the study, 6,811,799 with nonrespiratory illnesses and 2,240,181 with respiratory illnesses. Median age was 5 years (IQR, 1-11 years), and 52.7% of the population was male (Appendix Table 2 and Appendix Table 3).

Respiratory vs Nonrespiratory Illness During the COVID-19 Pandemic

Over the study period, fewer respiratory and nonrespiratory illness encounters were observed than expected, with a larger decrease in respiratory illness encounters (Table, Appendix Table 4).

Observed-to-Expected Encounter Ratios During COVID-19 Pandemic
The initial decrease occurred between March 12 and April 9, 2020, with relative stability until a subsequent rise in encounters between May 28 and July 9. After July 9, respiratory illness encounters decreased compared with a relatively stable trend in nonrespiratory illness encounters (Figure). The O:E ratios for respiratory illnesses during the study periods were: pre-COVID-19, 1.13 (95% CI, 1.07-1.19); early COVID-19, 0.57 (95% CI, 0.54-0.60); and COVID-19, 0.38 (95% CI, 0.35-0.41). Comparatively, the O:E ratios for nonrespiratory illnesses were 1.03 (95% CI, 1.01-1.06), 0.54 (95% CI, 0.52-0.56), and 0.62 (95% CI, 0.59-0.66) over the same periods (Table, Appendix Table 4).

Respiratory and Nonrespiratory Illness at Children’s Hospitals During the COVID-19 Period

Respiratory Subgroup Analyses

The O:E ratio decreased for all respiratory subgroups over the study period (Table, Appendix Table 4). There were significant differences in specific respiratory subgroups, including asthma, bronchiolitis, croup, influenza, and pneumonia (Appendix Figure 1A). Temporal trends in respiratory encounters were consistent across hospital settings, ages, and geographic regions (Appendix Figure 1B-D). When comparing the with and without COVID-19 subgroups in the “other respiratory illnesses” cohort, other respiratory illness without COVID-19 decreased and remained lower than expected over the rest of the study period, while other respiratory illness with COVID-19 increased markedly during the summer months and declined thereafter (Appendix Figure 2).

All age groups had reductions in respiratory illness encounters during the early COVID-19 and COVID-19 periods, although the decline was less pronounced in the 12- to 17-year-old group (Appendix Figure 1B). Similarly, while all age groups experienced increases in encounters for respiratory illnesses during the summer months, only children in the 12- to 17-year-old group experienced increases beyond pre-COVID-19 levels. Importantly, this increase in respiratory encounters was largely driven by COVID-19 diagnoses (Appendix Figure 3). The trend in nonrespiratory illness encounters stratified by age is shown in Appendix Figure 4.

When patients were stratified by hospital setting, there were no differences between those hospitalized and those discharged from the ED (Appendix Figure 1C). Patterns in respiratory illnesses by geographic location were qualitatively similar until the beginning of the summer 2020, after which geographical variation became more evident (Appendix Figure 1D).

DISCUSSION

In this large, multicenter study evaluating ED visits and hospitalizations for respiratory and nonrespiratory illnesses at US pediatric hospitals during the 2020 COVID-19 pandemic, we found a significant and substantial decrease in healthcare encounters for respiratory illnesses. A rapid and marked decline in encounters for respiratory illness in a relatively short period of time (March 12-April 2) was observed across all hospitals and US regions. Declines were consistent across common respiratory illnesses. More modest, yet still substantial, declines were also observed for nonrespiratory illnesses.

There are likely multiple underlying reasons for the observed reductions. Social distancing measures almost certainly played an important role in interrupting respiratory infection transmission. Rapid reduction in influenza transmission during the early COVID-19 period has been attributed to social distancing measures,3 and influenza transmission in children decreases with school closures.9 It is also possible that some families delayed seeking care at hospitals due to COVID-19, leading to less frequent encounters but more severe illness. The similar decrease in O:E ratio for ED visits and hospitalizations, however, is inconsistent with this explanation. It is also possible that nonurgent conditions cared for in the hospital settings were diverted to other care settings. For example, during this pandemic, telehealth and telephone visits for pediatric asthma increased by 61% and 19%, respectively, while ED and outpatient visits decreased concurrently.10Similar changes in location of care may also contribute to the decline in nonrespiratory illness encounters. Decreased use of hospital resources for nonurgent care diagnoses during the pandemic would suggest that, prior to COVID-19, there was overutilization of ambulatory services at children’s hospitals. Therefore, the pandemic may be driving care to more appropriate settings.

We also found relative differences in changes in encounters for respiratory illness by age. Adolescents’ levels of respiratory healthcare use declined less and recovered at a faster rate than those of younger children, returning to pre-COVID-19 levels by the end of the study period. The reason for this age differential is likely multifaceted. Infections, such as bronchiolitis and pneumonia, are more likely to be a source of respiratory illness in younger than in older children. It is also likely that disproportionate relaxation of social distancing measures among adolescents, who are known to have a stronger pattern of social interaction, contributed to the faster rise in respiratory illness–related encounters in this age group.11 Adolescents have been reported to be more susceptible to, and more likely to transmit, SARS-CoV-2 compared to younger age groups.12 More modest, albeit similar, age-based changes were observed in encounters for nonrespiratory illnesses. It is possible that pandemic-related stressors resulted in a subsequent increase in mental health encounters among this age group.13 While the reason for this also is likely multifactorial, adolescent behavior, as well as transmission of infectious illness that can exacerbate nonrespiratory conditions, may be a factor.

Emerging evidence suggests that school-age children may play an important role in SARS-CoV-2 transmission in the community.4,14 Our finding that, compared to younger children, adolescents had significantly fewer reductions in respiratory illness encounters is concerning. These findings suggest that community-based efforts to help prevent respiratory illnesses, especially COVID-19, should focus on adolescents, who are most likely to maintain social interactions and transmit respiratory infections in the school setting and their households.

This study is limited by the inclusion of only tertiary care children’s hospitals, which may not be nationally representative, and the inability to assess the precise timing of when specific public health interventions were introduced. Moreover, previous studies suggest that social distancing behaviors may have changed even before formal recommendations were enacted.15 Future studies should investigate the local impact of state- and municipality-specific mandates on the burden of COVID-19 and other respiratory illnesses.

The COVID-19 pandemic was associated with substantial reductions in encounters for respiratory diseases, and also with more modest but still sizable reductions in encounters for nonrespiratory diseases. These reductions varied by age. Encounters among adolescents declined less and returned to previous levels faster compared with those of younger children.

ACKNOWLEDGMENT

This publication is dedicated to the memory of our coauthor, Dr. Michael Bendel-Stenzel. Dr. Bendel-Stenzel was dedicated to bettering the lives of children and advancing our knowledge of pediatrics through his research.

References

1. Leyenaar JK, Ralston SL, Shieh MS, Pekow PS, Mangione-Smith R, Lindenauer PK. Epidemiology of pediatric hospitalizations at general hospitals and freestanding children’s hospitals in the United States. J Hosp Med. 2016;11(11):743-749. https://doi.org/10.1002/jhm.2624
2. Auger KA, Shah SS, Richardson T, et al. Association between statewide school closure and COVID-19 incidence and mortality in the US. JAMA. 2020;324(9):859-870. https://doi.org/10.1001/jama.2020.14348
3. Wiese AD, Everson J, Grijalva CG. Social distancing measures: evidence of interruption of seasonal influenza activity and early lessons of the SARS-CoV-2 pandemic. Clin Infect Dis. Published online June 20, 2020. https://doi.org/10.1093/cid/ciaa834
4. Grijalva CG, Rolfes MA, Zhu Y, et al. Transmission of SARS-COV-2 infections in households - Tennessee and Wisconsin, April-September 2020. MMWR Morb Mortal Wkly Rep. 2020;69(44):1631-1634. https://doi.org/10.15585/mmwr.mm6944e1
5. Worby CJ, Chaves SS, Wallinga J, Lipsitch M, Finelli L, Goldstein E. On the relative role of different age groups in influenza epidemics. Epidemics. 2015;13:10-16. https://doi.org/10.1016/j.epidem.2015.04.003
6. Zimmerman KO, Akinboyo IC, Brookhart MA, et al. Incidence and secondary transmission of SARS-CoV-2 infections in schools. Pediatrics. Published online January 8, 2021. https://doi.org/10.1542/peds.2020-048090
7. Hatoun J, Correa ET, Donahue SMA, Vernacchio L. Social distancing for COVID-19 and diagnoses of other infectious diseases in children. Pediatrics. 2020;146(4):e2020006460. https://doi.org/10.1542/peds.2020-006460
8. Chaiyachati BH, Agawu A, Zorc JJ, Balamuth F. Trends in pediatric emergency department utilization after institution of coronavirus disease-19 mandatory social distancing. J Pediatr. 2020;226:274-277.e1. https://doi.org/10.1016/j.jpeds.2020.07.048
9. Luca G, Kerckhove KV, Coletti P, et al. The impact of regular school closure on seasonal influenza epidemics: a data-driven spatial transmission model for Belgium. BMC Infect Dis. 2018;18(1):29. https://doi.org/10.1186/s12879-017-2934-3
10. Taquechel K, Diwadkar AR, Sayed S, et al. Pediatric asthma healthcare utilization, viral testing, and air pollution changes during the COVID-19 pandemic. J Allergy Clin Immunol Pract. 2020;8(10):3378-3387.e11. https://doi.org/10.1016/j.jaip.2020.07.057
11. Park YJ, Choe YJ, Park O, et al. Contact tracing during coronavirus disease outbreak, South Korea, 2020. Emerg Infect Dis. 2020;26(10):2465-2468. https://doi.org/10.3201/eid2610.201315
12. Davies NG, Klepac P, Liu Y, et al. Age-dependent effects in the transmission and control of COVID-19 epidemics. Nat Med. 2020;26(8):1205-1211. https://doi.org/10.1038/s41591-020-0962-9
13. Hill RM, Rufino K, Kurian S, Saxena J, Saxena K, Williams L. Suicide ideation and attempts in a pediatric emergency department before and during COVID-19. Pediatrics. Published online December 16, 2020. https://doi.org/10.1542/peds.2020-029280
14. Flasche S, Edmunds WJ. The role of schools and school-aged children in SARS-CoV-2 transmission. Lancet Infect Dis. Published online December 8, 2020. https://doi.org/10.1016/S1473-3099(20)30927-0
15. Sehra ST, George M, Wiebe DJ, Fundin S, Baker JF. Cell phone activity in categories of places and associations with growth in cases of COVID-19 in the US. JAMA Intern Med. Published online August 31, 2020. https://doi.org/10.1001/jamainternmed.2020.4288

References

1. Leyenaar JK, Ralston SL, Shieh MS, Pekow PS, Mangione-Smith R, Lindenauer PK. Epidemiology of pediatric hospitalizations at general hospitals and freestanding children’s hospitals in the United States. J Hosp Med. 2016;11(11):743-749. https://doi.org/10.1002/jhm.2624
2. Auger KA, Shah SS, Richardson T, et al. Association between statewide school closure and COVID-19 incidence and mortality in the US. JAMA. 2020;324(9):859-870. https://doi.org/10.1001/jama.2020.14348
3. Wiese AD, Everson J, Grijalva CG. Social distancing measures: evidence of interruption of seasonal influenza activity and early lessons of the SARS-CoV-2 pandemic. Clin Infect Dis. Published online June 20, 2020. https://doi.org/10.1093/cid/ciaa834
4. Grijalva CG, Rolfes MA, Zhu Y, et al. Transmission of SARS-COV-2 infections in households - Tennessee and Wisconsin, April-September 2020. MMWR Morb Mortal Wkly Rep. 2020;69(44):1631-1634. https://doi.org/10.15585/mmwr.mm6944e1
5. Worby CJ, Chaves SS, Wallinga J, Lipsitch M, Finelli L, Goldstein E. On the relative role of different age groups in influenza epidemics. Epidemics. 2015;13:10-16. https://doi.org/10.1016/j.epidem.2015.04.003
6. Zimmerman KO, Akinboyo IC, Brookhart MA, et al. Incidence and secondary transmission of SARS-CoV-2 infections in schools. Pediatrics. Published online January 8, 2021. https://doi.org/10.1542/peds.2020-048090
7. Hatoun J, Correa ET, Donahue SMA, Vernacchio L. Social distancing for COVID-19 and diagnoses of other infectious diseases in children. Pediatrics. 2020;146(4):e2020006460. https://doi.org/10.1542/peds.2020-006460
8. Chaiyachati BH, Agawu A, Zorc JJ, Balamuth F. Trends in pediatric emergency department utilization after institution of coronavirus disease-19 mandatory social distancing. J Pediatr. 2020;226:274-277.e1. https://doi.org/10.1016/j.jpeds.2020.07.048
9. Luca G, Kerckhove KV, Coletti P, et al. The impact of regular school closure on seasonal influenza epidemics: a data-driven spatial transmission model for Belgium. BMC Infect Dis. 2018;18(1):29. https://doi.org/10.1186/s12879-017-2934-3
10. Taquechel K, Diwadkar AR, Sayed S, et al. Pediatric asthma healthcare utilization, viral testing, and air pollution changes during the COVID-19 pandemic. J Allergy Clin Immunol Pract. 2020;8(10):3378-3387.e11. https://doi.org/10.1016/j.jaip.2020.07.057
11. Park YJ, Choe YJ, Park O, et al. Contact tracing during coronavirus disease outbreak, South Korea, 2020. Emerg Infect Dis. 2020;26(10):2465-2468. https://doi.org/10.3201/eid2610.201315
12. Davies NG, Klepac P, Liu Y, et al. Age-dependent effects in the transmission and control of COVID-19 epidemics. Nat Med. 2020;26(8):1205-1211. https://doi.org/10.1038/s41591-020-0962-9
13. Hill RM, Rufino K, Kurian S, Saxena J, Saxena K, Williams L. Suicide ideation and attempts in a pediatric emergency department before and during COVID-19. Pediatrics. Published online December 16, 2020. https://doi.org/10.1542/peds.2020-029280
14. Flasche S, Edmunds WJ. The role of schools and school-aged children in SARS-CoV-2 transmission. Lancet Infect Dis. Published online December 8, 2020. https://doi.org/10.1016/S1473-3099(20)30927-0
15. Sehra ST, George M, Wiebe DJ, Fundin S, Baker JF. Cell phone activity in categories of places and associations with growth in cases of COVID-19 in the US. JAMA Intern Med. Published online August 31, 2020. https://doi.org/10.1001/jamainternmed.2020.4288

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Achievable Benchmarks of Care for Pediatric Readmissions

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Hospital readmission rates are a common metric for defining, evaluating, and benchmarking quality of care. The Centers for Medicare and Medicaid Services (CMS) publicly report hospital readmission rates for common adult conditions and reduces payments to hospitals with excessive readmissions.1 Recently, the focus on pediatric readmission rates has increased and the National Quality Forum (NQF) has endorsed at least two pediatric readmission-specific quality indicators which could be used by public and private payers in pay-for-performance programs aimed at institutions caring for children.2 While preventability of readmissions and their value as a marker of quality remains debated, their acceptance by the NQF and CMS has led public and private payers to propose readmission-related penalties for hospitals caring for children. 3-5

All-cause 30-day same-hospital readmission rates for pediatric conditions are half of the adult readmission rates, around 6% in most studies, compared to 12% in adults.6,7 The lower rates of pediatric readmissions makes it difficult to only use mean readmission rates to stratify hospitals into high- or low-performers and set target goals for improvement.8 While adult readmissions have been studied in depth, there are no consistent measures used to benchmark pediatric readmissions across hospital types.

Given the emphasis placed on readmissions, it is essential to understand patterns in pediatric readmission rates to determine optimal and achievable targets for improvement. Achievable Benchmarks of Care (ABCs) are one approach to understanding readmission rates and have an advantage over using mean or medians in performance improvement as they can stratify performance for conditions with low readmission rates and low volumes.9 When creating benchmarks, it is important that hospitals performance is evaluated among peer hospitals with similar patient populations, not just a cumulative average from all hospital types which may punish hospitals with a more complex patient case mix.10 The goal of this study was to calculate the readmission rates and the ABCs for common pediatric diagnoses by hospital type to identify priority conditions for quality improvement efforts using a previously published methodology.11-13

 

 

METHODS

Data Source

We conducted a retrospective analysis of patients less than 18 years of age in the Healthcare Utilization Project 2014 Nationwide Readmissions Database (NRD). The NRD includes public hospitals; academic medical centers; and specialty hospitals in obstetrics and gynecology, otolaryngology, orthopedics, and cancer; and pediatric, public, and academic medical hospitals. Excluded are long-term care facilities such as rehabilitation, long-term acute care, psychiatric, alcoholism, and chemical dependency hospitals. The readmissions data contains information from hospitals grouped by region, population census, and teaching status.14 Three hospital type classifications used in this study were metropolitan teaching hospitals, metropolitan nonteaching hospitals, and nonmetropolitan hospitals. These three hospital type classifications follow the reporting format in the NRD.

Study Population

Patients less than 18 years old were included if they were discharged from January 1, 2014 through November 30, 2014 and had a readmission to the index hospital within 30 days. We limited inclusion to discharges through November 30 so we could identify patients with a 30-day readmission as patient identifiers do not link across years in the NRD.

Exposure

We included 30-day, all-cause, same-hospital readmissions to the index acute care hospital, excluding labor and delivery, normal newborn care, chemotherapy, transfers, and mortalities. Intrahospital discharge and admissions within the same hospital system were not defined as a readmission, but rather as a “same-day event.”15 For example, institutions with inpatient mental health facilities, medical unit discharges and admission to the mental health unit were not identified as a readmission in this dataset.

Outcome

For each hospital type, we measured same-hospital, all-cause, 30-day readmission rates and achievable benchmark of care for the 17 most commonly readmitted pediatric discharge diagnoses. To identify the target readmission diagnoses and all-cause, 30-day readmissions based on their index hospitalizations, All-Patient Refined Diagnosis-Related Groups (APR-DRG), version 25 (3M Health Information Systems, Salt Lake City, Utah) were ordered by frequency for each hospital type. The 20 most common APR-DRGs were the same across all hospital types. The authors then evaluated these 20 APR-DRGs for clinical consistency of included diagnoses identified by the International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9-CM) codes within each APR-DRG. Three diagnosis-related groups were excluded from the analysis (major hematologic/immunologic disease except for sickle cell, other anemia and disorders of blood and blood forming organs, and other digestive system diagnoses) due to the heterogeneity of the diagnoses identified by the ICD-9-CM codes within each APR-DRG. We refer to each APR-DRG as a “diagnosis” throughout the article.

Analysis

The demographic characteristics of the patients seen at the three hospital types were summarized using frequencies and percentages. Reports were generated for patient age, gender, payer source, patient residence, median household income, patient complexity, and discharge disposition. Patient complexity was defined using complex chronic condition (CCC) and the number of chronic conditions (CCI).16,17 As previously defined in the literature, a complex chronic condition is “any medical condition that can be reasonably expected to last at least 12 months (unless death intervenes) and to involve either several different organ systems or one organ system severely enough to require specialty pediatric care and probably some period of hospitalization in a tertiary care center.”16 Whereas, the Agency for Healthcare Research and Quality’s Chronic Condition Indicator (CCI) defines single, non-CCCs (eg, allergic rhinitis).17

 

 

For each diagnosis, we calculated the mean readmission rate for hospitals in each hospital type category. We then calculated an ABC for each diagnosis in each hospital type using a four-step process.13,18 First, to control for hospitals with small sample sizes, we adjusted all readmission rates using an adjusted performance fraction ([numerator+1]/[denominator +2]), where the numerator is the number of all-cause 30-day readmissions and the denominator is the number of discharges for the selected diagnosis. Then the hospitals were ordered from lowest (best performing) to highest (worst performing) using the adjusted readmission rate. Third, the number of discharges from the best performing hospital to the worst performing hospital was summed until at least 10% of the total discharges had been accounted for. Finally, we computed the ABC as the average of these best performing hospitals. We only report ABCs for which at least three hospitals were included as best performers in the calculation.13

To evaluate hospital performance on ABCs for each diagnosis, we identified the percent of hospitals in each setting that were outliers. We defined an outlier as any hospital whose 95% confidence interval for their readmission rate for a given diagnosis did not contain the ABC for their hospital type. All the statistical analyses were performed using SAS version 9.3 (SAS Institute, Inc, Cary, North Carolina).

This project was reviewed by the Cincinnati Children’s Hospital Medical Center Institutional Review Board and determined to be nonhuman subjects research.

RESULTS

Hospital-Type Demographics

The 690,949 discharges from 1,664 hospitals were categorized into 525 metropolitan teaching (550,039 discharges, 79.6% of discharges), 552 metropolitan nonteaching (97,207 discharges, 14% of discharges), and 587 nonmetropolitan hospitals (43,703 discharges, 6.3% of discharges; Table 1). There were significant differences in the patient composition among the three hospital settings. Nonmetropolitan hospitals had a larger percentage of younger patients (aged 0-4 years, P < .001), prominence of first and second quartile median household income, and fewer medically complex patients (48.3% No CCC/No CCI versus 25.5% metropolitan teaching and 33.7% nonteaching, P < .001). Disposition home was over 96% in all three hospital types; however, the metropolitan teaching had a greater percentage of patients discharged to home health versus metropolitan nonteaching and nonmetropolitan hospitals (2.3% versus 0.5%; P < .001).

Readmission Rates

The 17 most common diagnoses based on the number of all-cause 30-day same-hospital readmissions, were categorized into two surgical, seven acute/infectious, four chronic, and four mental health diagnoses (Table 2). Readmission rates varied based on diagnosis and hospital type (Table 2). Overall, mean readmission rates were low, especially in acute respiratory tract related diseases. For chronic diseases, asthma readmissions were consistently low in all three hospital types, whereas sickle cell disease had the highest readmission rate in all three hospital types.

Achievable Benchmarks of Care by Hospital Type

The diagnoses for which ABC could be calculated across all three hospital types included appendectomy and four acute conditions (bronchiolitis, pneumonia, nonbacterial gastroenteritis, and kidney/urinary tract infections). For these conditions, metropolitan teaching hospitals had a more significant percentage of outlier hospitals compared to metropolitan nonteaching and nonmetropolitan hospitals. The percent of outlier hospitals varied by diagnosis and hospital type (Figure).

 

 

Metropolitan Teaching

The readmission ABC was calculated for all 17 diagnoses (Table 2). The ABC ranged from 0.4% in acute kidney and urinary tract infection to 7.0% in sickle cell anemia crisis. Bipolar disorder, major depressive disorders and other psychoses, and sickle cell disease (SCD) had the highest percent of outlier hospitals whose mean readmission rates confidence interval did not contain the ABC; tonsil and adenoid procedures and viral illness had the lowest.1

Metropolitan Nonteaching

The ABC was calculated for 13 of the 17 diagnoses because ABCs were not calculated when there were fewer than three best practicing hospitals. This was the case for tonsil and adenoid procedures, diabetes, seizures, and depression except for major depressive disorder (Table 2). Seven of the 13 diagnoses had an ABC of 0.0%: viral illness, infections of the upper respiratory tract, bronchiolitis, gastroenteritis, hypovolemia and electrolyte disorders, asthma, and childhood behavioral disorders. Like the findings at the metropolitan teaching hospitals, ABCs were lowest for surgical and acute conditions while bipolar disorder, major depressive disorders and other psychoses, and SCD had the highest percent of outlier hospitals with readmission rates beyond the 95% confidence interval of their hospital type’s ABC.

Nonmetropolitan

There was a sufficient number of best practicing hospitals to calculate the ABC for six of the 17 diagnoses (Table 2). For conditions where readmission ABCs could be calculated, they were low: 0.0% for appendectomy, bronchiolitis, gastroenteritis, and seizure; 0.3% for pneumonia; and 1.3% in kidney and urinary tract disorders. None of the conditions with the highest ABCs in other hospital settings (bipolar disease, sickle cell anemia crisis, and major depressive disorders and other psychoses) could be calculated in this setting. Seizure-related readmissions exhibited the most outlier hospitals yet were less than 5%.1

DISCUSSION

Among a nationally representative sample of different hospital types that deliver care to children, we report the mean readmission rates and ABCs for 30-day all-cause, same-hospital readmissions for the most commonly readmitted pediatric diagnoses based on hospital type. Previous studies have shown patient variables such as race, ethnicity, and insurance type influencing readmission rates.19,20 However, hospital type has also been associated with a higher risk of readmission due to the varying complexity of patients at different hospital types.21,22 Our analyses provide hospital-type specific national estimates of pediatric readmission ABCs for medical and surgical conditions, many less than 1%. While commonly encountered pediatric conditions like asthma and bronchiolitis had low mean readmission rates and ABCs across all hospital types, the mean rates and ABCs for SCD and mental health disorders were much higher with more hospitals performing far from the ABCs.

Diagnoses with a larger percentage of outlier hospitals may represent a national opportunity to improve care for children. Conditions such as SCD and mental illnesses have the highest percentage of hospitals whose readmission rates fall outside of the ABCs in both metropolitan teaching and metropolitan nonteaching hospitals. Hospital performance on SCD and mental health disorders may not reflect deficits in hospital quality or poor adherence to evidence-based best practices, but rather the complex interplay of factors on various levels from government policy and insurance plans, to patient and family resources, to access and availability of medical and mental health specific care. Most importantly, these diseases may represent a significant opportunity for quality improvementin hospitals across the United States.

Sickle cell disease is predominantly a disease among African-Americans, a demographic risk factor for decreased access to care and limited patient and family resources.23-26 In previous studies evaluating the disparity in readmission rates for Black children with asthma, socioeconomic variables explained 53% of the observed disparity and readmission rates were inversely related to the childhood opportunity index of the patient’s census tract and positively related with geographic social risk.27,28 Likewise, with SCD affecting a specific demographic and being a chronic disease, best practice policies need to account for the child’s medical needs and include the patient and family resources to ensure access to care and enhanced case management for chronic disease if we aim to improve performance among the outlier hospitals.

Similarly, barriers to care for children with mental illnesses in the United States need attention.29,30 While there is a paucity of data on the prevalence of mental health disorders in children, one national report estimates that one in 10 American adolescents have depression.29,31 The American Academy of Pediatrics has developed a policy statement on mental health competencies and a mental health tool-kit for primary care pediatricians; however, no such guidelines or policy statements exist for hospitalized patients with acute or chronic psychiatric conditions.32,33 Moreover, hospitals are increasingly facing “boarding” of children with acute psychiatric illness in inpatient units and emergency departments.34 The American Medical Association and the American College of Emergency Physicians have expressed concerns regarding the boarding of children with acute psychiatric illness because nonpsychiatric hospitals do not have adequate resources to evaluate, manage, and place these children who deserve appropriate facilities for further management. Coordinated case management and “bundled” discharge planning in other chronic illnesses have shown benefit in cost reduction and readmission.35-37 Evidence-based practices around pediatric readmissions in other diagnoses should be explored as possible interventions in these conditions.38

There are several limitations to this study. Our data is limited to one calendar year; therefore, admissions in January do not account for potential readmissions from December of the previous year, as patient identifiers do not link across years in the NRD. We also limited our evaluation to the conventional 30-day readmission window, but recent publications may indicate that readmission windows with different timelines could be a more accurate reflection of medically preventable readmissions versus a reflection of social determinants of health leading to readmissions.24 Newborn index admissions were not an allowable index admission; therefore, we may be underreporting readmissions in the neonatal age group. We also chose to include all-cause readmissions, a conventional method to evaluate readmission within an institution, but which may not reflect the quality of care delivered in the index admission. For example, an asthmatic discharged after an acute exacerbation readmitted for dehydration secondary to gastroenteritis may not reflect a lack of quality in asthma inpatient care. Readmissions were limited to the same hospital; therefore, this study cannot account for readmissions at other institutions, which may cause us to underestimate readmission rates. However, end-users of our findings most likely have access only to their own institution’s data. The inclusion of observation status admissions in the database varies from state to state; therefore, this percent of admissions in the database is unknown.

The use of the ABC methodology has some inherent limitations. One hospital with a significant volume diagnosis and low readmission rate within a hospital type may prohibit the reporting of an ABC if less than three hospitals composed the total of the ‘best performing’ hospitals. This was a significant limitation leading to the exclusion of many ABCs in nonmetropolitan institutions. The limitation of calculating and reporting an ABC then prohibits the calculation of outlier hospitals within a hospital type for a given diagnosis. However, when the ABCs are not available, we do provide the mean readmission rate for the diagnosis within the hospital type. While the hospital groupings by population and teaching status for ABCs provide meaningful comparisons for within each hospital setting, it should be noted that there may be vast differences among hospitals within each type (eg, tertiary children’s hospitals compared to teaching hospitals with a pediatric floor in the metropolitan teaching hospital category).39,40

As healthcare moves from a fee-for-service model to a population-health centered, value-based model, reduction in readmission rates will be more than a quality measure and will have potential financial implications.41 In the Medicare fee-for-service patients, the Hospital Readmission Reduction Program (HRRP) penalize hospitals with excess readmissions for acute myocardial infarction, heart failure, and pneumonia. The hospitals subject to penalties in the HRRP had greater reduction in readmission rates in the targeted, and even nontargeted conditions, compared with hospitals not subject to penalties.42 Similarly, we believe that our data on low readmission rates and ABCs for conditions such as asthma, bronchiolitis, and appendicitis could represent decades of quality improvement work for the most common pediatric conditions among hospitalized children. Sickle cell disease and mental health problems remain as outliers and merit further attention. To move to a true population-health model, hospitals will need to explore outlier conditions including evaluating patient-level readmission patterns across institutions. This moves readmission from a hospital quality measure to a patient-centric quality measure, and perhaps will provide value to the patient and the healthcare system alike.

 

 

CONCLUSIONS

The readmission ABCs for the most commonly readmitted pediatric diagnoses are low, regardless of the hospital setting. The highest pediatric readmission rates in SCD, bipolar disorders, and major depressive disorder were lower than the most common adult readmission diagnoses. However, mental health conditions and SCD remain as outliers for pediatric readmissions, burden hospital systems, and perhaps warrant national-level attention. The ABCs stratified by hospital type in this study facilitate comparisons and identify opportunities for population-level interventions to meaningfully improve patient care.

Disclosures

The authors have nothing to disclose.

 

References

1. Medicare. 30-day death and readmission measures data. https://www.medicare.gov/hospitalcompare/Data/30-day-measures.html. Accessed October 24, 2017.
2. National Quality Forum. Performance Measures; 2016 https://www.quality fourm.org/Measuring_Performance/Endorsed_Performance_Measures_Maintenance.aspx. Accessed October 24, 2017.
3. Auger KA, Simon TD, Cooperberg D, et al. Summary of STARNet: seamless transitions and (re)admissions network. Pediatrics. 2015;135(1):164-175. https://doi.org/10.1542/peds.2014-1887.
4. Toomey SL, Peltz A, Loren S, et al. Potentially preventable 30-day hospital readmissions at a children’s hospital. Pediatrics. 2016;138(2):e20154182-e20154182. https://doi.org/10.1542/peds.2015-4182.
5. Halfon P, Eggli Y, Prêtre-Rohrbach I, et al. Validation of the potentially avoidable hospital readmission rate as a routine indicator of the quality of hospital care. Med Care. 2006;44(11):972-981. https://doi.org/10.1097/01.mlr.0000228002.43688.c2.
6. Gay JC, Agrawal R, Auger KA, et al. Rates and impact of potentially preventable readmissions at children’s hospitals. J Pediatr. 2015;166(3):613-619. https://doi.org/10.1016/j.jpeds.2014.10.052.
7. Berry JG, Gay JC, Joynt Maddox KJ, et al. Age trends in 30 day hospital readmissions: US national retrospective analysis. BMJ. 2018;360:k497. https://doi.org/10.1136/bmj.k497.
8. Bardach NS, Vittinghoff E, Asteria-Penaloza R, et al. Measuring hospital quality using pediatric readmission and revisit rates. Pediatrics. 2013;132(3):429-436. https://doi.org/10.1542/peds.2012-3527d.
9. Berry JG, Toomey SL, Zaslavsky AM, et al. Pediatric readmission prevalence and variability across hospitals. JAMA. 2013;309(4):372-380. https://doi.org/10.1001/jama.2012.188351.
10. Gohil SK, Datta R, Cao C, et al. Impact of hospital population case-mix, including poverty, on hospital all-cause and infection-related 30-day readmission rates. Clin Infect Dis. 2015;61(8):1235-1243. https://doi.org/10.1093/cid/civ539.
11. Parikh K, Hall M, Mittal V, et al. Establishing benchmarks for the hospitalized care of children with asthma, bronchiolitis, and pneumonia. Pediatrics. 2014;134(3):555-562. https://doi.org/10.1542/peds.2014-1052.
12. Reyes M, Paulus E, Hronek C, et al. Choosing wisely campaign: report card and achievable benchmarks of care for children’s hospitals. Hosp Pediatr. 2017;7(11):633-641. https://doi.org/10.1542/hpeds.2017-0029.
13. Kiefe CI, Weissman NW, Allison JJ, et al. Identifying achievable benchmarks of care: concepts and methodology. Int J Qual Health Care. 1998;10(5):443-447. https://doi.org/10.1093/intqhc/10.5.443.
14. Agency for Healthcare Research and Quality. Nationwide Readmissions Database Availability of Data Elements. . https://www.hcup-us.ahrq.gov/partner/MOARef/HCUPdata_elements.pdf. Accessed 2018 Jun 6
15. Healthcare Cost and Utilization Project. HCUP NRD description of data elements. Agency Healthc Res Qual. https://www.hcup-us.ahrq.gov/db/vars/samedayevent/nrdnote.jsp. Accessed 2018 Jun 6; 2015.
16. Feudtner C, Feinstein JA, Zhong W, Hall M, Dai D. Pediatric complex chronic conditions classification system version 2: updated for ICD-10 and complex medical technology dependence and transplantation. BMC Pediatr. 2014;14:199. https://doi.org/10.1186/1471-2431-14-199.
17. Agency for Healthcare Research and Quality. HCUP chronic condition indicator. Healthc Cost Util Proj. https://www.hcup-us.ahrq.gov/toolssoftware/chronic/chronic.jsp. Accessed 2016 Apr 26; 2009.
18. Weissman NW, Allison JJ, Kiefe CI, et al. Achievable benchmarks of care: the ABCs of benchmarking. J Eval Clin Pract. 1999;5(3):269-281. https://doi.org/10.1046/j.1365-2753.1999.00203.x.
19. Joynt KE, Orav EJ, Jha AK. Thirty-day readmission rates for medicare beneficiaries by race and site of care. JAMA. 2011;305(7):675-681. https://doi.org/10.1001/jama.2011.123.
20. Kenyon CC, Melvin PR, Chiang VW, et al. Rehospitalization for childhood asthma: timing, variation, and opportunities for intervention. J Pediatr. 2014;164(2):300-305. https://doi.org/10.1016/j.jpeds.2013.10.003.
21. Sobota A, Graham DA, Neufeld EJ, Heeney MM. Thirty-day readmission rates following hospitalization for pediatric sickle cell crisis at freestanding children’s hospitals: risk factors and hospital variation. Pediatr Blood Cancer. 2012;58(1):61-65. https://doi.org/10.1002/pbc.23221.
22. Berry JG, Hall DE, Kuo DZ, et al. Hospital utilization and characteristics of patients experiencing recurrent readmissions within children’s hospitals. JAMA. 2011;305(7):682-690. https://doi.org/10.1001/jama.2011.122.
23. Ginde AA, Espinola JA, Camargo CA. Improved overall trends but persistent racial disparities in emergency department visits for acute asthma, 1993-2005. J Allergy Clin Immunol. 2008;122(2):313-318. https://doi.org/10.1016/j.jaci.2008.04.024.
24. Parikh K, Berry J, Hall M, et al. Racial and ethnic differences in pediatric readmissions for common chronic conditions. J Pediatr. 2017;186. https://doi.org/10.1016/j.jpeds.2017.03.046.
25. Chen BK, Hibbert J, Cheng X, Bennett K. Travel distance and sociodemographic correlates of potentially avoidable emergency department visits in California, 2006-2010: an observational study. Int J Equity Health. 2015;14(1):30. https://doi.org/10.1186/s12939-015-0158-y.
26. Ray KN, Chari AV, Engberg J, et al. Disparities in time spent seeking medical care in the United States. JAMA Intern Med. 2015;175(12):175(12):1983-1986. https://doi.org/10.1001/jamainternmed.2015.4468.
27. Beck AF, Huang B, Wheeler K, et al. The child opportunity index and disparities in pediatric asthma hospitalizations across one Ohio metropolitan area. J Pediatr. 2011-2013;190:200-206. https://doi.org/10.1016/j.jpeds.2017.08.007.
28. Beck AF, Simmons JM, Huang B, Kahn RS. Geomedicine: area-based socioeconomic measures for assessing the risk of hospital reutilization among children admitted for asthma. Am J Public Health. 2012;102(12):2308-2314. https://doi.org/10.2105/AJPH.2012.300806.
29. Avenevoli S, Swendsen J, He JP, Burstein M, Merikangas KR. Major depression in the national comorbidity survey-adolescent supplement: prevalence, correlates, and treatment. J Am Acad Child Adolesc Psychiatry. 2015;54(1):37-44.e2. https://doi.org/10.1016/j.jaac.2014.10.010.
30. Feng JY, Toomey SL, Zaslavsky AM, Nakamura MM, Schuster MA. Readmission after pediatric mental health admissions. Pediatrics. 2017;140(6):e20171571. https://doi.org/10.1542/peds.2017-1571.
31. Merikangas KR, He JP, Burstein M, et al. Lifetime prevalence of mental disorders in U.S. adolescents: results from the National comorbidity Survey Replication-Adolescent Supplement (NCS-A). J Am Acad Child Adolesc Psychiatry. 2010;49(10):980-989. https://doi.org/10.1016/j.jaac.2010.05.017.
32. Cheung AH, Zuckerbrot RA, Jensen PS, et al. Guidelines for adolescent depression in primary care (GLAD-PC): Part II. Treatment and ongoing management. Pediatrics. 2018;141(3):e20174082. https://doi.org/10.1542/peds.2017-4082.
33. Zuckerbrot RA, Cheung A, Jensen PS, et al. Guidelines for adolescent depression in primary care (GLAD-PC): Part I. Practice preparation, identification, assessment, and initial management. Pediatrics. 2018;141(3):e20174081. https://doi.org/10.1542/peds.2017-4081.
34. Dolan MA, Fein JA, Committee on Pediatric Emergency Medicine. Pediatric and adolescent mental health emergencies in the emergency Medical Services system. Pediatrics. 2011;127(5):e1356-e1366. https://doi.org/10.1542/peds.2011-0522.
35. Collaborative Healthcare Strategies. Hospital Guide to Reducing Medicaid Readmissions. Rockville, MD: 2014. https://www.ahrq.gov/sites/default/files/publications/files/medreadmissions.pdf. Accessed 2017 Oct 11.
36. Hilbert K, Payne R, Wooton S. Children’s Hospitals’ Solutions for Patient Safety. Readmissions Bundle Tools. Cincinnati, OH; 2014.
37. Nuckols TK, Keeler E, Morton S, et al. Economic evaluation of quality improvement interventions designed to prevent hospital readmission: a systematic review and meta-analysis. JAMA Intern Med. 2017;177(7):975-985. https://doi.org/10.1001/jamainternmed.2017.1136.
38. Berry JG, Blaine K, Rogers J, et al. A framework of pediatric hospital discharge care informed by legislation, research, and practice. JAMA Pediatr. 2014;168(10):955-962. https://doi.org/10.1001/jamapediatrics.2014.891.
39. Chen HF, Carlson E, Popoola T, Suzuki S. The impact of rurality on 30-day preventable readmission, illness severity, and risk of mortality for heart failure Medicare home health beneficiaries. J Rural Health. 2016;32(2):176-187. https://doi.org/10.1111/jrh.12142.
40. Khan A, Nakamura MM, Zaslavsky AM, et al. Same-hospital readmission rates as a measure of pediatric quality of care. JAMA Pediatr. 2015;169(10):905-912. https://doi.org/10.1001/jamapediatrics.2015.1129.
41. Share DA, Campbell DA, Birkmeyer N, et al. How a regional collaborative of hospitals and physicians in Michigan cut costs and improved the quality of care. Health Aff. 2011;30(4):636-645. https://doi.org/10.1377/hlthaff.2010.0526.
42. Desai NR, Ross JS, Kwon JY, et al. Association between hospital penalty status under the hospital readmission reduction program and readmission rates for target and nontarget conditions. JAMA. 2016;316(24):2647-2656. https://doi.org/10.1001/jama.2016.18533.

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Hospital readmission rates are a common metric for defining, evaluating, and benchmarking quality of care. The Centers for Medicare and Medicaid Services (CMS) publicly report hospital readmission rates for common adult conditions and reduces payments to hospitals with excessive readmissions.1 Recently, the focus on pediatric readmission rates has increased and the National Quality Forum (NQF) has endorsed at least two pediatric readmission-specific quality indicators which could be used by public and private payers in pay-for-performance programs aimed at institutions caring for children.2 While preventability of readmissions and their value as a marker of quality remains debated, their acceptance by the NQF and CMS has led public and private payers to propose readmission-related penalties for hospitals caring for children. 3-5

All-cause 30-day same-hospital readmission rates for pediatric conditions are half of the adult readmission rates, around 6% in most studies, compared to 12% in adults.6,7 The lower rates of pediatric readmissions makes it difficult to only use mean readmission rates to stratify hospitals into high- or low-performers and set target goals for improvement.8 While adult readmissions have been studied in depth, there are no consistent measures used to benchmark pediatric readmissions across hospital types.

Given the emphasis placed on readmissions, it is essential to understand patterns in pediatric readmission rates to determine optimal and achievable targets for improvement. Achievable Benchmarks of Care (ABCs) are one approach to understanding readmission rates and have an advantage over using mean or medians in performance improvement as they can stratify performance for conditions with low readmission rates and low volumes.9 When creating benchmarks, it is important that hospitals performance is evaluated among peer hospitals with similar patient populations, not just a cumulative average from all hospital types which may punish hospitals with a more complex patient case mix.10 The goal of this study was to calculate the readmission rates and the ABCs for common pediatric diagnoses by hospital type to identify priority conditions for quality improvement efforts using a previously published methodology.11-13

 

 

METHODS

Data Source

We conducted a retrospective analysis of patients less than 18 years of age in the Healthcare Utilization Project 2014 Nationwide Readmissions Database (NRD). The NRD includes public hospitals; academic medical centers; and specialty hospitals in obstetrics and gynecology, otolaryngology, orthopedics, and cancer; and pediatric, public, and academic medical hospitals. Excluded are long-term care facilities such as rehabilitation, long-term acute care, psychiatric, alcoholism, and chemical dependency hospitals. The readmissions data contains information from hospitals grouped by region, population census, and teaching status.14 Three hospital type classifications used in this study were metropolitan teaching hospitals, metropolitan nonteaching hospitals, and nonmetropolitan hospitals. These three hospital type classifications follow the reporting format in the NRD.

Study Population

Patients less than 18 years old were included if they were discharged from January 1, 2014 through November 30, 2014 and had a readmission to the index hospital within 30 days. We limited inclusion to discharges through November 30 so we could identify patients with a 30-day readmission as patient identifiers do not link across years in the NRD.

Exposure

We included 30-day, all-cause, same-hospital readmissions to the index acute care hospital, excluding labor and delivery, normal newborn care, chemotherapy, transfers, and mortalities. Intrahospital discharge and admissions within the same hospital system were not defined as a readmission, but rather as a “same-day event.”15 For example, institutions with inpatient mental health facilities, medical unit discharges and admission to the mental health unit were not identified as a readmission in this dataset.

Outcome

For each hospital type, we measured same-hospital, all-cause, 30-day readmission rates and achievable benchmark of care for the 17 most commonly readmitted pediatric discharge diagnoses. To identify the target readmission diagnoses and all-cause, 30-day readmissions based on their index hospitalizations, All-Patient Refined Diagnosis-Related Groups (APR-DRG), version 25 (3M Health Information Systems, Salt Lake City, Utah) were ordered by frequency for each hospital type. The 20 most common APR-DRGs were the same across all hospital types. The authors then evaluated these 20 APR-DRGs for clinical consistency of included diagnoses identified by the International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9-CM) codes within each APR-DRG. Three diagnosis-related groups were excluded from the analysis (major hematologic/immunologic disease except for sickle cell, other anemia and disorders of blood and blood forming organs, and other digestive system diagnoses) due to the heterogeneity of the diagnoses identified by the ICD-9-CM codes within each APR-DRG. We refer to each APR-DRG as a “diagnosis” throughout the article.

Analysis

The demographic characteristics of the patients seen at the three hospital types were summarized using frequencies and percentages. Reports were generated for patient age, gender, payer source, patient residence, median household income, patient complexity, and discharge disposition. Patient complexity was defined using complex chronic condition (CCC) and the number of chronic conditions (CCI).16,17 As previously defined in the literature, a complex chronic condition is “any medical condition that can be reasonably expected to last at least 12 months (unless death intervenes) and to involve either several different organ systems or one organ system severely enough to require specialty pediatric care and probably some period of hospitalization in a tertiary care center.”16 Whereas, the Agency for Healthcare Research and Quality’s Chronic Condition Indicator (CCI) defines single, non-CCCs (eg, allergic rhinitis).17

 

 

For each diagnosis, we calculated the mean readmission rate for hospitals in each hospital type category. We then calculated an ABC for each diagnosis in each hospital type using a four-step process.13,18 First, to control for hospitals with small sample sizes, we adjusted all readmission rates using an adjusted performance fraction ([numerator+1]/[denominator +2]), where the numerator is the number of all-cause 30-day readmissions and the denominator is the number of discharges for the selected diagnosis. Then the hospitals were ordered from lowest (best performing) to highest (worst performing) using the adjusted readmission rate. Third, the number of discharges from the best performing hospital to the worst performing hospital was summed until at least 10% of the total discharges had been accounted for. Finally, we computed the ABC as the average of these best performing hospitals. We only report ABCs for which at least three hospitals were included as best performers in the calculation.13

To evaluate hospital performance on ABCs for each diagnosis, we identified the percent of hospitals in each setting that were outliers. We defined an outlier as any hospital whose 95% confidence interval for their readmission rate for a given diagnosis did not contain the ABC for their hospital type. All the statistical analyses were performed using SAS version 9.3 (SAS Institute, Inc, Cary, North Carolina).

This project was reviewed by the Cincinnati Children’s Hospital Medical Center Institutional Review Board and determined to be nonhuman subjects research.

RESULTS

Hospital-Type Demographics

The 690,949 discharges from 1,664 hospitals were categorized into 525 metropolitan teaching (550,039 discharges, 79.6% of discharges), 552 metropolitan nonteaching (97,207 discharges, 14% of discharges), and 587 nonmetropolitan hospitals (43,703 discharges, 6.3% of discharges; Table 1). There were significant differences in the patient composition among the three hospital settings. Nonmetropolitan hospitals had a larger percentage of younger patients (aged 0-4 years, P < .001), prominence of first and second quartile median household income, and fewer medically complex patients (48.3% No CCC/No CCI versus 25.5% metropolitan teaching and 33.7% nonteaching, P < .001). Disposition home was over 96% in all three hospital types; however, the metropolitan teaching had a greater percentage of patients discharged to home health versus metropolitan nonteaching and nonmetropolitan hospitals (2.3% versus 0.5%; P < .001).

Readmission Rates

The 17 most common diagnoses based on the number of all-cause 30-day same-hospital readmissions, were categorized into two surgical, seven acute/infectious, four chronic, and four mental health diagnoses (Table 2). Readmission rates varied based on diagnosis and hospital type (Table 2). Overall, mean readmission rates were low, especially in acute respiratory tract related diseases. For chronic diseases, asthma readmissions were consistently low in all three hospital types, whereas sickle cell disease had the highest readmission rate in all three hospital types.

Achievable Benchmarks of Care by Hospital Type

The diagnoses for which ABC could be calculated across all three hospital types included appendectomy and four acute conditions (bronchiolitis, pneumonia, nonbacterial gastroenteritis, and kidney/urinary tract infections). For these conditions, metropolitan teaching hospitals had a more significant percentage of outlier hospitals compared to metropolitan nonteaching and nonmetropolitan hospitals. The percent of outlier hospitals varied by diagnosis and hospital type (Figure).

 

 

Metropolitan Teaching

The readmission ABC was calculated for all 17 diagnoses (Table 2). The ABC ranged from 0.4% in acute kidney and urinary tract infection to 7.0% in sickle cell anemia crisis. Bipolar disorder, major depressive disorders and other psychoses, and sickle cell disease (SCD) had the highest percent of outlier hospitals whose mean readmission rates confidence interval did not contain the ABC; tonsil and adenoid procedures and viral illness had the lowest.1

Metropolitan Nonteaching

The ABC was calculated for 13 of the 17 diagnoses because ABCs were not calculated when there were fewer than three best practicing hospitals. This was the case for tonsil and adenoid procedures, diabetes, seizures, and depression except for major depressive disorder (Table 2). Seven of the 13 diagnoses had an ABC of 0.0%: viral illness, infections of the upper respiratory tract, bronchiolitis, gastroenteritis, hypovolemia and electrolyte disorders, asthma, and childhood behavioral disorders. Like the findings at the metropolitan teaching hospitals, ABCs were lowest for surgical and acute conditions while bipolar disorder, major depressive disorders and other psychoses, and SCD had the highest percent of outlier hospitals with readmission rates beyond the 95% confidence interval of their hospital type’s ABC.

Nonmetropolitan

There was a sufficient number of best practicing hospitals to calculate the ABC for six of the 17 diagnoses (Table 2). For conditions where readmission ABCs could be calculated, they were low: 0.0% for appendectomy, bronchiolitis, gastroenteritis, and seizure; 0.3% for pneumonia; and 1.3% in kidney and urinary tract disorders. None of the conditions with the highest ABCs in other hospital settings (bipolar disease, sickle cell anemia crisis, and major depressive disorders and other psychoses) could be calculated in this setting. Seizure-related readmissions exhibited the most outlier hospitals yet were less than 5%.1

DISCUSSION

Among a nationally representative sample of different hospital types that deliver care to children, we report the mean readmission rates and ABCs for 30-day all-cause, same-hospital readmissions for the most commonly readmitted pediatric diagnoses based on hospital type. Previous studies have shown patient variables such as race, ethnicity, and insurance type influencing readmission rates.19,20 However, hospital type has also been associated with a higher risk of readmission due to the varying complexity of patients at different hospital types.21,22 Our analyses provide hospital-type specific national estimates of pediatric readmission ABCs for medical and surgical conditions, many less than 1%. While commonly encountered pediatric conditions like asthma and bronchiolitis had low mean readmission rates and ABCs across all hospital types, the mean rates and ABCs for SCD and mental health disorders were much higher with more hospitals performing far from the ABCs.

Diagnoses with a larger percentage of outlier hospitals may represent a national opportunity to improve care for children. Conditions such as SCD and mental illnesses have the highest percentage of hospitals whose readmission rates fall outside of the ABCs in both metropolitan teaching and metropolitan nonteaching hospitals. Hospital performance on SCD and mental health disorders may not reflect deficits in hospital quality or poor adherence to evidence-based best practices, but rather the complex interplay of factors on various levels from government policy and insurance plans, to patient and family resources, to access and availability of medical and mental health specific care. Most importantly, these diseases may represent a significant opportunity for quality improvementin hospitals across the United States.

Sickle cell disease is predominantly a disease among African-Americans, a demographic risk factor for decreased access to care and limited patient and family resources.23-26 In previous studies evaluating the disparity in readmission rates for Black children with asthma, socioeconomic variables explained 53% of the observed disparity and readmission rates were inversely related to the childhood opportunity index of the patient’s census tract and positively related with geographic social risk.27,28 Likewise, with SCD affecting a specific demographic and being a chronic disease, best practice policies need to account for the child’s medical needs and include the patient and family resources to ensure access to care and enhanced case management for chronic disease if we aim to improve performance among the outlier hospitals.

Similarly, barriers to care for children with mental illnesses in the United States need attention.29,30 While there is a paucity of data on the prevalence of mental health disorders in children, one national report estimates that one in 10 American adolescents have depression.29,31 The American Academy of Pediatrics has developed a policy statement on mental health competencies and a mental health tool-kit for primary care pediatricians; however, no such guidelines or policy statements exist for hospitalized patients with acute or chronic psychiatric conditions.32,33 Moreover, hospitals are increasingly facing “boarding” of children with acute psychiatric illness in inpatient units and emergency departments.34 The American Medical Association and the American College of Emergency Physicians have expressed concerns regarding the boarding of children with acute psychiatric illness because nonpsychiatric hospitals do not have adequate resources to evaluate, manage, and place these children who deserve appropriate facilities for further management. Coordinated case management and “bundled” discharge planning in other chronic illnesses have shown benefit in cost reduction and readmission.35-37 Evidence-based practices around pediatric readmissions in other diagnoses should be explored as possible interventions in these conditions.38

There are several limitations to this study. Our data is limited to one calendar year; therefore, admissions in January do not account for potential readmissions from December of the previous year, as patient identifiers do not link across years in the NRD. We also limited our evaluation to the conventional 30-day readmission window, but recent publications may indicate that readmission windows with different timelines could be a more accurate reflection of medically preventable readmissions versus a reflection of social determinants of health leading to readmissions.24 Newborn index admissions were not an allowable index admission; therefore, we may be underreporting readmissions in the neonatal age group. We also chose to include all-cause readmissions, a conventional method to evaluate readmission within an institution, but which may not reflect the quality of care delivered in the index admission. For example, an asthmatic discharged after an acute exacerbation readmitted for dehydration secondary to gastroenteritis may not reflect a lack of quality in asthma inpatient care. Readmissions were limited to the same hospital; therefore, this study cannot account for readmissions at other institutions, which may cause us to underestimate readmission rates. However, end-users of our findings most likely have access only to their own institution’s data. The inclusion of observation status admissions in the database varies from state to state; therefore, this percent of admissions in the database is unknown.

The use of the ABC methodology has some inherent limitations. One hospital with a significant volume diagnosis and low readmission rate within a hospital type may prohibit the reporting of an ABC if less than three hospitals composed the total of the ‘best performing’ hospitals. This was a significant limitation leading to the exclusion of many ABCs in nonmetropolitan institutions. The limitation of calculating and reporting an ABC then prohibits the calculation of outlier hospitals within a hospital type for a given diagnosis. However, when the ABCs are not available, we do provide the mean readmission rate for the diagnosis within the hospital type. While the hospital groupings by population and teaching status for ABCs provide meaningful comparisons for within each hospital setting, it should be noted that there may be vast differences among hospitals within each type (eg, tertiary children’s hospitals compared to teaching hospitals with a pediatric floor in the metropolitan teaching hospital category).39,40

As healthcare moves from a fee-for-service model to a population-health centered, value-based model, reduction in readmission rates will be more than a quality measure and will have potential financial implications.41 In the Medicare fee-for-service patients, the Hospital Readmission Reduction Program (HRRP) penalize hospitals with excess readmissions for acute myocardial infarction, heart failure, and pneumonia. The hospitals subject to penalties in the HRRP had greater reduction in readmission rates in the targeted, and even nontargeted conditions, compared with hospitals not subject to penalties.42 Similarly, we believe that our data on low readmission rates and ABCs for conditions such as asthma, bronchiolitis, and appendicitis could represent decades of quality improvement work for the most common pediatric conditions among hospitalized children. Sickle cell disease and mental health problems remain as outliers and merit further attention. To move to a true population-health model, hospitals will need to explore outlier conditions including evaluating patient-level readmission patterns across institutions. This moves readmission from a hospital quality measure to a patient-centric quality measure, and perhaps will provide value to the patient and the healthcare system alike.

 

 

CONCLUSIONS

The readmission ABCs for the most commonly readmitted pediatric diagnoses are low, regardless of the hospital setting. The highest pediatric readmission rates in SCD, bipolar disorders, and major depressive disorder were lower than the most common adult readmission diagnoses. However, mental health conditions and SCD remain as outliers for pediatric readmissions, burden hospital systems, and perhaps warrant national-level attention. The ABCs stratified by hospital type in this study facilitate comparisons and identify opportunities for population-level interventions to meaningfully improve patient care.

Disclosures

The authors have nothing to disclose.

 

Hospital readmission rates are a common metric for defining, evaluating, and benchmarking quality of care. The Centers for Medicare and Medicaid Services (CMS) publicly report hospital readmission rates for common adult conditions and reduces payments to hospitals with excessive readmissions.1 Recently, the focus on pediatric readmission rates has increased and the National Quality Forum (NQF) has endorsed at least two pediatric readmission-specific quality indicators which could be used by public and private payers in pay-for-performance programs aimed at institutions caring for children.2 While preventability of readmissions and their value as a marker of quality remains debated, their acceptance by the NQF and CMS has led public and private payers to propose readmission-related penalties for hospitals caring for children. 3-5

All-cause 30-day same-hospital readmission rates for pediatric conditions are half of the adult readmission rates, around 6% in most studies, compared to 12% in adults.6,7 The lower rates of pediatric readmissions makes it difficult to only use mean readmission rates to stratify hospitals into high- or low-performers and set target goals for improvement.8 While adult readmissions have been studied in depth, there are no consistent measures used to benchmark pediatric readmissions across hospital types.

Given the emphasis placed on readmissions, it is essential to understand patterns in pediatric readmission rates to determine optimal and achievable targets for improvement. Achievable Benchmarks of Care (ABCs) are one approach to understanding readmission rates and have an advantage over using mean or medians in performance improvement as they can stratify performance for conditions with low readmission rates and low volumes.9 When creating benchmarks, it is important that hospitals performance is evaluated among peer hospitals with similar patient populations, not just a cumulative average from all hospital types which may punish hospitals with a more complex patient case mix.10 The goal of this study was to calculate the readmission rates and the ABCs for common pediatric diagnoses by hospital type to identify priority conditions for quality improvement efforts using a previously published methodology.11-13

 

 

METHODS

Data Source

We conducted a retrospective analysis of patients less than 18 years of age in the Healthcare Utilization Project 2014 Nationwide Readmissions Database (NRD). The NRD includes public hospitals; academic medical centers; and specialty hospitals in obstetrics and gynecology, otolaryngology, orthopedics, and cancer; and pediatric, public, and academic medical hospitals. Excluded are long-term care facilities such as rehabilitation, long-term acute care, psychiatric, alcoholism, and chemical dependency hospitals. The readmissions data contains information from hospitals grouped by region, population census, and teaching status.14 Three hospital type classifications used in this study were metropolitan teaching hospitals, metropolitan nonteaching hospitals, and nonmetropolitan hospitals. These three hospital type classifications follow the reporting format in the NRD.

Study Population

Patients less than 18 years old were included if they were discharged from January 1, 2014 through November 30, 2014 and had a readmission to the index hospital within 30 days. We limited inclusion to discharges through November 30 so we could identify patients with a 30-day readmission as patient identifiers do not link across years in the NRD.

Exposure

We included 30-day, all-cause, same-hospital readmissions to the index acute care hospital, excluding labor and delivery, normal newborn care, chemotherapy, transfers, and mortalities. Intrahospital discharge and admissions within the same hospital system were not defined as a readmission, but rather as a “same-day event.”15 For example, institutions with inpatient mental health facilities, medical unit discharges and admission to the mental health unit were not identified as a readmission in this dataset.

Outcome

For each hospital type, we measured same-hospital, all-cause, 30-day readmission rates and achievable benchmark of care for the 17 most commonly readmitted pediatric discharge diagnoses. To identify the target readmission diagnoses and all-cause, 30-day readmissions based on their index hospitalizations, All-Patient Refined Diagnosis-Related Groups (APR-DRG), version 25 (3M Health Information Systems, Salt Lake City, Utah) were ordered by frequency for each hospital type. The 20 most common APR-DRGs were the same across all hospital types. The authors then evaluated these 20 APR-DRGs for clinical consistency of included diagnoses identified by the International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9-CM) codes within each APR-DRG. Three diagnosis-related groups were excluded from the analysis (major hematologic/immunologic disease except for sickle cell, other anemia and disorders of blood and blood forming organs, and other digestive system diagnoses) due to the heterogeneity of the diagnoses identified by the ICD-9-CM codes within each APR-DRG. We refer to each APR-DRG as a “diagnosis” throughout the article.

Analysis

The demographic characteristics of the patients seen at the three hospital types were summarized using frequencies and percentages. Reports were generated for patient age, gender, payer source, patient residence, median household income, patient complexity, and discharge disposition. Patient complexity was defined using complex chronic condition (CCC) and the number of chronic conditions (CCI).16,17 As previously defined in the literature, a complex chronic condition is “any medical condition that can be reasonably expected to last at least 12 months (unless death intervenes) and to involve either several different organ systems or one organ system severely enough to require specialty pediatric care and probably some period of hospitalization in a tertiary care center.”16 Whereas, the Agency for Healthcare Research and Quality’s Chronic Condition Indicator (CCI) defines single, non-CCCs (eg, allergic rhinitis).17

 

 

For each diagnosis, we calculated the mean readmission rate for hospitals in each hospital type category. We then calculated an ABC for each diagnosis in each hospital type using a four-step process.13,18 First, to control for hospitals with small sample sizes, we adjusted all readmission rates using an adjusted performance fraction ([numerator+1]/[denominator +2]), where the numerator is the number of all-cause 30-day readmissions and the denominator is the number of discharges for the selected diagnosis. Then the hospitals were ordered from lowest (best performing) to highest (worst performing) using the adjusted readmission rate. Third, the number of discharges from the best performing hospital to the worst performing hospital was summed until at least 10% of the total discharges had been accounted for. Finally, we computed the ABC as the average of these best performing hospitals. We only report ABCs for which at least three hospitals were included as best performers in the calculation.13

To evaluate hospital performance on ABCs for each diagnosis, we identified the percent of hospitals in each setting that were outliers. We defined an outlier as any hospital whose 95% confidence interval for their readmission rate for a given diagnosis did not contain the ABC for their hospital type. All the statistical analyses were performed using SAS version 9.3 (SAS Institute, Inc, Cary, North Carolina).

This project was reviewed by the Cincinnati Children’s Hospital Medical Center Institutional Review Board and determined to be nonhuman subjects research.

RESULTS

Hospital-Type Demographics

The 690,949 discharges from 1,664 hospitals were categorized into 525 metropolitan teaching (550,039 discharges, 79.6% of discharges), 552 metropolitan nonteaching (97,207 discharges, 14% of discharges), and 587 nonmetropolitan hospitals (43,703 discharges, 6.3% of discharges; Table 1). There were significant differences in the patient composition among the three hospital settings. Nonmetropolitan hospitals had a larger percentage of younger patients (aged 0-4 years, P < .001), prominence of first and second quartile median household income, and fewer medically complex patients (48.3% No CCC/No CCI versus 25.5% metropolitan teaching and 33.7% nonteaching, P < .001). Disposition home was over 96% in all three hospital types; however, the metropolitan teaching had a greater percentage of patients discharged to home health versus metropolitan nonteaching and nonmetropolitan hospitals (2.3% versus 0.5%; P < .001).

Readmission Rates

The 17 most common diagnoses based on the number of all-cause 30-day same-hospital readmissions, were categorized into two surgical, seven acute/infectious, four chronic, and four mental health diagnoses (Table 2). Readmission rates varied based on diagnosis and hospital type (Table 2). Overall, mean readmission rates were low, especially in acute respiratory tract related diseases. For chronic diseases, asthma readmissions were consistently low in all three hospital types, whereas sickle cell disease had the highest readmission rate in all three hospital types.

Achievable Benchmarks of Care by Hospital Type

The diagnoses for which ABC could be calculated across all three hospital types included appendectomy and four acute conditions (bronchiolitis, pneumonia, nonbacterial gastroenteritis, and kidney/urinary tract infections). For these conditions, metropolitan teaching hospitals had a more significant percentage of outlier hospitals compared to metropolitan nonteaching and nonmetropolitan hospitals. The percent of outlier hospitals varied by diagnosis and hospital type (Figure).

 

 

Metropolitan Teaching

The readmission ABC was calculated for all 17 diagnoses (Table 2). The ABC ranged from 0.4% in acute kidney and urinary tract infection to 7.0% in sickle cell anemia crisis. Bipolar disorder, major depressive disorders and other psychoses, and sickle cell disease (SCD) had the highest percent of outlier hospitals whose mean readmission rates confidence interval did not contain the ABC; tonsil and adenoid procedures and viral illness had the lowest.1

Metropolitan Nonteaching

The ABC was calculated for 13 of the 17 diagnoses because ABCs were not calculated when there were fewer than three best practicing hospitals. This was the case for tonsil and adenoid procedures, diabetes, seizures, and depression except for major depressive disorder (Table 2). Seven of the 13 diagnoses had an ABC of 0.0%: viral illness, infections of the upper respiratory tract, bronchiolitis, gastroenteritis, hypovolemia and electrolyte disorders, asthma, and childhood behavioral disorders. Like the findings at the metropolitan teaching hospitals, ABCs were lowest for surgical and acute conditions while bipolar disorder, major depressive disorders and other psychoses, and SCD had the highest percent of outlier hospitals with readmission rates beyond the 95% confidence interval of their hospital type’s ABC.

Nonmetropolitan

There was a sufficient number of best practicing hospitals to calculate the ABC for six of the 17 diagnoses (Table 2). For conditions where readmission ABCs could be calculated, they were low: 0.0% for appendectomy, bronchiolitis, gastroenteritis, and seizure; 0.3% for pneumonia; and 1.3% in kidney and urinary tract disorders. None of the conditions with the highest ABCs in other hospital settings (bipolar disease, sickle cell anemia crisis, and major depressive disorders and other psychoses) could be calculated in this setting. Seizure-related readmissions exhibited the most outlier hospitals yet were less than 5%.1

DISCUSSION

Among a nationally representative sample of different hospital types that deliver care to children, we report the mean readmission rates and ABCs for 30-day all-cause, same-hospital readmissions for the most commonly readmitted pediatric diagnoses based on hospital type. Previous studies have shown patient variables such as race, ethnicity, and insurance type influencing readmission rates.19,20 However, hospital type has also been associated with a higher risk of readmission due to the varying complexity of patients at different hospital types.21,22 Our analyses provide hospital-type specific national estimates of pediatric readmission ABCs for medical and surgical conditions, many less than 1%. While commonly encountered pediatric conditions like asthma and bronchiolitis had low mean readmission rates and ABCs across all hospital types, the mean rates and ABCs for SCD and mental health disorders were much higher with more hospitals performing far from the ABCs.

Diagnoses with a larger percentage of outlier hospitals may represent a national opportunity to improve care for children. Conditions such as SCD and mental illnesses have the highest percentage of hospitals whose readmission rates fall outside of the ABCs in both metropolitan teaching and metropolitan nonteaching hospitals. Hospital performance on SCD and mental health disorders may not reflect deficits in hospital quality or poor adherence to evidence-based best practices, but rather the complex interplay of factors on various levels from government policy and insurance plans, to patient and family resources, to access and availability of medical and mental health specific care. Most importantly, these diseases may represent a significant opportunity for quality improvementin hospitals across the United States.

Sickle cell disease is predominantly a disease among African-Americans, a demographic risk factor for decreased access to care and limited patient and family resources.23-26 In previous studies evaluating the disparity in readmission rates for Black children with asthma, socioeconomic variables explained 53% of the observed disparity and readmission rates were inversely related to the childhood opportunity index of the patient’s census tract and positively related with geographic social risk.27,28 Likewise, with SCD affecting a specific demographic and being a chronic disease, best practice policies need to account for the child’s medical needs and include the patient and family resources to ensure access to care and enhanced case management for chronic disease if we aim to improve performance among the outlier hospitals.

Similarly, barriers to care for children with mental illnesses in the United States need attention.29,30 While there is a paucity of data on the prevalence of mental health disorders in children, one national report estimates that one in 10 American adolescents have depression.29,31 The American Academy of Pediatrics has developed a policy statement on mental health competencies and a mental health tool-kit for primary care pediatricians; however, no such guidelines or policy statements exist for hospitalized patients with acute or chronic psychiatric conditions.32,33 Moreover, hospitals are increasingly facing “boarding” of children with acute psychiatric illness in inpatient units and emergency departments.34 The American Medical Association and the American College of Emergency Physicians have expressed concerns regarding the boarding of children with acute psychiatric illness because nonpsychiatric hospitals do not have adequate resources to evaluate, manage, and place these children who deserve appropriate facilities for further management. Coordinated case management and “bundled” discharge planning in other chronic illnesses have shown benefit in cost reduction and readmission.35-37 Evidence-based practices around pediatric readmissions in other diagnoses should be explored as possible interventions in these conditions.38

There are several limitations to this study. Our data is limited to one calendar year; therefore, admissions in January do not account for potential readmissions from December of the previous year, as patient identifiers do not link across years in the NRD. We also limited our evaluation to the conventional 30-day readmission window, but recent publications may indicate that readmission windows with different timelines could be a more accurate reflection of medically preventable readmissions versus a reflection of social determinants of health leading to readmissions.24 Newborn index admissions were not an allowable index admission; therefore, we may be underreporting readmissions in the neonatal age group. We also chose to include all-cause readmissions, a conventional method to evaluate readmission within an institution, but which may not reflect the quality of care delivered in the index admission. For example, an asthmatic discharged after an acute exacerbation readmitted for dehydration secondary to gastroenteritis may not reflect a lack of quality in asthma inpatient care. Readmissions were limited to the same hospital; therefore, this study cannot account for readmissions at other institutions, which may cause us to underestimate readmission rates. However, end-users of our findings most likely have access only to their own institution’s data. The inclusion of observation status admissions in the database varies from state to state; therefore, this percent of admissions in the database is unknown.

The use of the ABC methodology has some inherent limitations. One hospital with a significant volume diagnosis and low readmission rate within a hospital type may prohibit the reporting of an ABC if less than three hospitals composed the total of the ‘best performing’ hospitals. This was a significant limitation leading to the exclusion of many ABCs in nonmetropolitan institutions. The limitation of calculating and reporting an ABC then prohibits the calculation of outlier hospitals within a hospital type for a given diagnosis. However, when the ABCs are not available, we do provide the mean readmission rate for the diagnosis within the hospital type. While the hospital groupings by population and teaching status for ABCs provide meaningful comparisons for within each hospital setting, it should be noted that there may be vast differences among hospitals within each type (eg, tertiary children’s hospitals compared to teaching hospitals with a pediatric floor in the metropolitan teaching hospital category).39,40

As healthcare moves from a fee-for-service model to a population-health centered, value-based model, reduction in readmission rates will be more than a quality measure and will have potential financial implications.41 In the Medicare fee-for-service patients, the Hospital Readmission Reduction Program (HRRP) penalize hospitals with excess readmissions for acute myocardial infarction, heart failure, and pneumonia. The hospitals subject to penalties in the HRRP had greater reduction in readmission rates in the targeted, and even nontargeted conditions, compared with hospitals not subject to penalties.42 Similarly, we believe that our data on low readmission rates and ABCs for conditions such as asthma, bronchiolitis, and appendicitis could represent decades of quality improvement work for the most common pediatric conditions among hospitalized children. Sickle cell disease and mental health problems remain as outliers and merit further attention. To move to a true population-health model, hospitals will need to explore outlier conditions including evaluating patient-level readmission patterns across institutions. This moves readmission from a hospital quality measure to a patient-centric quality measure, and perhaps will provide value to the patient and the healthcare system alike.

 

 

CONCLUSIONS

The readmission ABCs for the most commonly readmitted pediatric diagnoses are low, regardless of the hospital setting. The highest pediatric readmission rates in SCD, bipolar disorders, and major depressive disorder were lower than the most common adult readmission diagnoses. However, mental health conditions and SCD remain as outliers for pediatric readmissions, burden hospital systems, and perhaps warrant national-level attention. The ABCs stratified by hospital type in this study facilitate comparisons and identify opportunities for population-level interventions to meaningfully improve patient care.

Disclosures

The authors have nothing to disclose.

 

References

1. Medicare. 30-day death and readmission measures data. https://www.medicare.gov/hospitalcompare/Data/30-day-measures.html. Accessed October 24, 2017.
2. National Quality Forum. Performance Measures; 2016 https://www.quality fourm.org/Measuring_Performance/Endorsed_Performance_Measures_Maintenance.aspx. Accessed October 24, 2017.
3. Auger KA, Simon TD, Cooperberg D, et al. Summary of STARNet: seamless transitions and (re)admissions network. Pediatrics. 2015;135(1):164-175. https://doi.org/10.1542/peds.2014-1887.
4. Toomey SL, Peltz A, Loren S, et al. Potentially preventable 30-day hospital readmissions at a children’s hospital. Pediatrics. 2016;138(2):e20154182-e20154182. https://doi.org/10.1542/peds.2015-4182.
5. Halfon P, Eggli Y, Prêtre-Rohrbach I, et al. Validation of the potentially avoidable hospital readmission rate as a routine indicator of the quality of hospital care. Med Care. 2006;44(11):972-981. https://doi.org/10.1097/01.mlr.0000228002.43688.c2.
6. Gay JC, Agrawal R, Auger KA, et al. Rates and impact of potentially preventable readmissions at children’s hospitals. J Pediatr. 2015;166(3):613-619. https://doi.org/10.1016/j.jpeds.2014.10.052.
7. Berry JG, Gay JC, Joynt Maddox KJ, et al. Age trends in 30 day hospital readmissions: US national retrospective analysis. BMJ. 2018;360:k497. https://doi.org/10.1136/bmj.k497.
8. Bardach NS, Vittinghoff E, Asteria-Penaloza R, et al. Measuring hospital quality using pediatric readmission and revisit rates. Pediatrics. 2013;132(3):429-436. https://doi.org/10.1542/peds.2012-3527d.
9. Berry JG, Toomey SL, Zaslavsky AM, et al. Pediatric readmission prevalence and variability across hospitals. JAMA. 2013;309(4):372-380. https://doi.org/10.1001/jama.2012.188351.
10. Gohil SK, Datta R, Cao C, et al. Impact of hospital population case-mix, including poverty, on hospital all-cause and infection-related 30-day readmission rates. Clin Infect Dis. 2015;61(8):1235-1243. https://doi.org/10.1093/cid/civ539.
11. Parikh K, Hall M, Mittal V, et al. Establishing benchmarks for the hospitalized care of children with asthma, bronchiolitis, and pneumonia. Pediatrics. 2014;134(3):555-562. https://doi.org/10.1542/peds.2014-1052.
12. Reyes M, Paulus E, Hronek C, et al. Choosing wisely campaign: report card and achievable benchmarks of care for children’s hospitals. Hosp Pediatr. 2017;7(11):633-641. https://doi.org/10.1542/hpeds.2017-0029.
13. Kiefe CI, Weissman NW, Allison JJ, et al. Identifying achievable benchmarks of care: concepts and methodology. Int J Qual Health Care. 1998;10(5):443-447. https://doi.org/10.1093/intqhc/10.5.443.
14. Agency for Healthcare Research and Quality. Nationwide Readmissions Database Availability of Data Elements. . https://www.hcup-us.ahrq.gov/partner/MOARef/HCUPdata_elements.pdf. Accessed 2018 Jun 6
15. Healthcare Cost and Utilization Project. HCUP NRD description of data elements. Agency Healthc Res Qual. https://www.hcup-us.ahrq.gov/db/vars/samedayevent/nrdnote.jsp. Accessed 2018 Jun 6; 2015.
16. Feudtner C, Feinstein JA, Zhong W, Hall M, Dai D. Pediatric complex chronic conditions classification system version 2: updated for ICD-10 and complex medical technology dependence and transplantation. BMC Pediatr. 2014;14:199. https://doi.org/10.1186/1471-2431-14-199.
17. Agency for Healthcare Research and Quality. HCUP chronic condition indicator. Healthc Cost Util Proj. https://www.hcup-us.ahrq.gov/toolssoftware/chronic/chronic.jsp. Accessed 2016 Apr 26; 2009.
18. Weissman NW, Allison JJ, Kiefe CI, et al. Achievable benchmarks of care: the ABCs of benchmarking. J Eval Clin Pract. 1999;5(3):269-281. https://doi.org/10.1046/j.1365-2753.1999.00203.x.
19. Joynt KE, Orav EJ, Jha AK. Thirty-day readmission rates for medicare beneficiaries by race and site of care. JAMA. 2011;305(7):675-681. https://doi.org/10.1001/jama.2011.123.
20. Kenyon CC, Melvin PR, Chiang VW, et al. Rehospitalization for childhood asthma: timing, variation, and opportunities for intervention. J Pediatr. 2014;164(2):300-305. https://doi.org/10.1016/j.jpeds.2013.10.003.
21. Sobota A, Graham DA, Neufeld EJ, Heeney MM. Thirty-day readmission rates following hospitalization for pediatric sickle cell crisis at freestanding children’s hospitals: risk factors and hospital variation. Pediatr Blood Cancer. 2012;58(1):61-65. https://doi.org/10.1002/pbc.23221.
22. Berry JG, Hall DE, Kuo DZ, et al. Hospital utilization and characteristics of patients experiencing recurrent readmissions within children’s hospitals. JAMA. 2011;305(7):682-690. https://doi.org/10.1001/jama.2011.122.
23. Ginde AA, Espinola JA, Camargo CA. Improved overall trends but persistent racial disparities in emergency department visits for acute asthma, 1993-2005. J Allergy Clin Immunol. 2008;122(2):313-318. https://doi.org/10.1016/j.jaci.2008.04.024.
24. Parikh K, Berry J, Hall M, et al. Racial and ethnic differences in pediatric readmissions for common chronic conditions. J Pediatr. 2017;186. https://doi.org/10.1016/j.jpeds.2017.03.046.
25. Chen BK, Hibbert J, Cheng X, Bennett K. Travel distance and sociodemographic correlates of potentially avoidable emergency department visits in California, 2006-2010: an observational study. Int J Equity Health. 2015;14(1):30. https://doi.org/10.1186/s12939-015-0158-y.
26. Ray KN, Chari AV, Engberg J, et al. Disparities in time spent seeking medical care in the United States. JAMA Intern Med. 2015;175(12):175(12):1983-1986. https://doi.org/10.1001/jamainternmed.2015.4468.
27. Beck AF, Huang B, Wheeler K, et al. The child opportunity index and disparities in pediatric asthma hospitalizations across one Ohio metropolitan area. J Pediatr. 2011-2013;190:200-206. https://doi.org/10.1016/j.jpeds.2017.08.007.
28. Beck AF, Simmons JM, Huang B, Kahn RS. Geomedicine: area-based socioeconomic measures for assessing the risk of hospital reutilization among children admitted for asthma. Am J Public Health. 2012;102(12):2308-2314. https://doi.org/10.2105/AJPH.2012.300806.
29. Avenevoli S, Swendsen J, He JP, Burstein M, Merikangas KR. Major depression in the national comorbidity survey-adolescent supplement: prevalence, correlates, and treatment. J Am Acad Child Adolesc Psychiatry. 2015;54(1):37-44.e2. https://doi.org/10.1016/j.jaac.2014.10.010.
30. Feng JY, Toomey SL, Zaslavsky AM, Nakamura MM, Schuster MA. Readmission after pediatric mental health admissions. Pediatrics. 2017;140(6):e20171571. https://doi.org/10.1542/peds.2017-1571.
31. Merikangas KR, He JP, Burstein M, et al. Lifetime prevalence of mental disorders in U.S. adolescents: results from the National comorbidity Survey Replication-Adolescent Supplement (NCS-A). J Am Acad Child Adolesc Psychiatry. 2010;49(10):980-989. https://doi.org/10.1016/j.jaac.2010.05.017.
32. Cheung AH, Zuckerbrot RA, Jensen PS, et al. Guidelines for adolescent depression in primary care (GLAD-PC): Part II. Treatment and ongoing management. Pediatrics. 2018;141(3):e20174082. https://doi.org/10.1542/peds.2017-4082.
33. Zuckerbrot RA, Cheung A, Jensen PS, et al. Guidelines for adolescent depression in primary care (GLAD-PC): Part I. Practice preparation, identification, assessment, and initial management. Pediatrics. 2018;141(3):e20174081. https://doi.org/10.1542/peds.2017-4081.
34. Dolan MA, Fein JA, Committee on Pediatric Emergency Medicine. Pediatric and adolescent mental health emergencies in the emergency Medical Services system. Pediatrics. 2011;127(5):e1356-e1366. https://doi.org/10.1542/peds.2011-0522.
35. Collaborative Healthcare Strategies. Hospital Guide to Reducing Medicaid Readmissions. Rockville, MD: 2014. https://www.ahrq.gov/sites/default/files/publications/files/medreadmissions.pdf. Accessed 2017 Oct 11.
36. Hilbert K, Payne R, Wooton S. Children’s Hospitals’ Solutions for Patient Safety. Readmissions Bundle Tools. Cincinnati, OH; 2014.
37. Nuckols TK, Keeler E, Morton S, et al. Economic evaluation of quality improvement interventions designed to prevent hospital readmission: a systematic review and meta-analysis. JAMA Intern Med. 2017;177(7):975-985. https://doi.org/10.1001/jamainternmed.2017.1136.
38. Berry JG, Blaine K, Rogers J, et al. A framework of pediatric hospital discharge care informed by legislation, research, and practice. JAMA Pediatr. 2014;168(10):955-962. https://doi.org/10.1001/jamapediatrics.2014.891.
39. Chen HF, Carlson E, Popoola T, Suzuki S. The impact of rurality on 30-day preventable readmission, illness severity, and risk of mortality for heart failure Medicare home health beneficiaries. J Rural Health. 2016;32(2):176-187. https://doi.org/10.1111/jrh.12142.
40. Khan A, Nakamura MM, Zaslavsky AM, et al. Same-hospital readmission rates as a measure of pediatric quality of care. JAMA Pediatr. 2015;169(10):905-912. https://doi.org/10.1001/jamapediatrics.2015.1129.
41. Share DA, Campbell DA, Birkmeyer N, et al. How a regional collaborative of hospitals and physicians in Michigan cut costs and improved the quality of care. Health Aff. 2011;30(4):636-645. https://doi.org/10.1377/hlthaff.2010.0526.
42. Desai NR, Ross JS, Kwon JY, et al. Association between hospital penalty status under the hospital readmission reduction program and readmission rates for target and nontarget conditions. JAMA. 2016;316(24):2647-2656. https://doi.org/10.1001/jama.2016.18533.

References

1. Medicare. 30-day death and readmission measures data. https://www.medicare.gov/hospitalcompare/Data/30-day-measures.html. Accessed October 24, 2017.
2. National Quality Forum. Performance Measures; 2016 https://www.quality fourm.org/Measuring_Performance/Endorsed_Performance_Measures_Maintenance.aspx. Accessed October 24, 2017.
3. Auger KA, Simon TD, Cooperberg D, et al. Summary of STARNet: seamless transitions and (re)admissions network. Pediatrics. 2015;135(1):164-175. https://doi.org/10.1542/peds.2014-1887.
4. Toomey SL, Peltz A, Loren S, et al. Potentially preventable 30-day hospital readmissions at a children’s hospital. Pediatrics. 2016;138(2):e20154182-e20154182. https://doi.org/10.1542/peds.2015-4182.
5. Halfon P, Eggli Y, Prêtre-Rohrbach I, et al. Validation of the potentially avoidable hospital readmission rate as a routine indicator of the quality of hospital care. Med Care. 2006;44(11):972-981. https://doi.org/10.1097/01.mlr.0000228002.43688.c2.
6. Gay JC, Agrawal R, Auger KA, et al. Rates and impact of potentially preventable readmissions at children’s hospitals. J Pediatr. 2015;166(3):613-619. https://doi.org/10.1016/j.jpeds.2014.10.052.
7. Berry JG, Gay JC, Joynt Maddox KJ, et al. Age trends in 30 day hospital readmissions: US national retrospective analysis. BMJ. 2018;360:k497. https://doi.org/10.1136/bmj.k497.
8. Bardach NS, Vittinghoff E, Asteria-Penaloza R, et al. Measuring hospital quality using pediatric readmission and revisit rates. Pediatrics. 2013;132(3):429-436. https://doi.org/10.1542/peds.2012-3527d.
9. Berry JG, Toomey SL, Zaslavsky AM, et al. Pediatric readmission prevalence and variability across hospitals. JAMA. 2013;309(4):372-380. https://doi.org/10.1001/jama.2012.188351.
10. Gohil SK, Datta R, Cao C, et al. Impact of hospital population case-mix, including poverty, on hospital all-cause and infection-related 30-day readmission rates. Clin Infect Dis. 2015;61(8):1235-1243. https://doi.org/10.1093/cid/civ539.
11. Parikh K, Hall M, Mittal V, et al. Establishing benchmarks for the hospitalized care of children with asthma, bronchiolitis, and pneumonia. Pediatrics. 2014;134(3):555-562. https://doi.org/10.1542/peds.2014-1052.
12. Reyes M, Paulus E, Hronek C, et al. Choosing wisely campaign: report card and achievable benchmarks of care for children’s hospitals. Hosp Pediatr. 2017;7(11):633-641. https://doi.org/10.1542/hpeds.2017-0029.
13. Kiefe CI, Weissman NW, Allison JJ, et al. Identifying achievable benchmarks of care: concepts and methodology. Int J Qual Health Care. 1998;10(5):443-447. https://doi.org/10.1093/intqhc/10.5.443.
14. Agency for Healthcare Research and Quality. Nationwide Readmissions Database Availability of Data Elements. . https://www.hcup-us.ahrq.gov/partner/MOARef/HCUPdata_elements.pdf. Accessed 2018 Jun 6
15. Healthcare Cost and Utilization Project. HCUP NRD description of data elements. Agency Healthc Res Qual. https://www.hcup-us.ahrq.gov/db/vars/samedayevent/nrdnote.jsp. Accessed 2018 Jun 6; 2015.
16. Feudtner C, Feinstein JA, Zhong W, Hall M, Dai D. Pediatric complex chronic conditions classification system version 2: updated for ICD-10 and complex medical technology dependence and transplantation. BMC Pediatr. 2014;14:199. https://doi.org/10.1186/1471-2431-14-199.
17. Agency for Healthcare Research and Quality. HCUP chronic condition indicator. Healthc Cost Util Proj. https://www.hcup-us.ahrq.gov/toolssoftware/chronic/chronic.jsp. Accessed 2016 Apr 26; 2009.
18. Weissman NW, Allison JJ, Kiefe CI, et al. Achievable benchmarks of care: the ABCs of benchmarking. J Eval Clin Pract. 1999;5(3):269-281. https://doi.org/10.1046/j.1365-2753.1999.00203.x.
19. Joynt KE, Orav EJ, Jha AK. Thirty-day readmission rates for medicare beneficiaries by race and site of care. JAMA. 2011;305(7):675-681. https://doi.org/10.1001/jama.2011.123.
20. Kenyon CC, Melvin PR, Chiang VW, et al. Rehospitalization for childhood asthma: timing, variation, and opportunities for intervention. J Pediatr. 2014;164(2):300-305. https://doi.org/10.1016/j.jpeds.2013.10.003.
21. Sobota A, Graham DA, Neufeld EJ, Heeney MM. Thirty-day readmission rates following hospitalization for pediatric sickle cell crisis at freestanding children’s hospitals: risk factors and hospital variation. Pediatr Blood Cancer. 2012;58(1):61-65. https://doi.org/10.1002/pbc.23221.
22. Berry JG, Hall DE, Kuo DZ, et al. Hospital utilization and characteristics of patients experiencing recurrent readmissions within children’s hospitals. JAMA. 2011;305(7):682-690. https://doi.org/10.1001/jama.2011.122.
23. Ginde AA, Espinola JA, Camargo CA. Improved overall trends but persistent racial disparities in emergency department visits for acute asthma, 1993-2005. J Allergy Clin Immunol. 2008;122(2):313-318. https://doi.org/10.1016/j.jaci.2008.04.024.
24. Parikh K, Berry J, Hall M, et al. Racial and ethnic differences in pediatric readmissions for common chronic conditions. J Pediatr. 2017;186. https://doi.org/10.1016/j.jpeds.2017.03.046.
25. Chen BK, Hibbert J, Cheng X, Bennett K. Travel distance and sociodemographic correlates of potentially avoidable emergency department visits in California, 2006-2010: an observational study. Int J Equity Health. 2015;14(1):30. https://doi.org/10.1186/s12939-015-0158-y.
26. Ray KN, Chari AV, Engberg J, et al. Disparities in time spent seeking medical care in the United States. JAMA Intern Med. 2015;175(12):175(12):1983-1986. https://doi.org/10.1001/jamainternmed.2015.4468.
27. Beck AF, Huang B, Wheeler K, et al. The child opportunity index and disparities in pediatric asthma hospitalizations across one Ohio metropolitan area. J Pediatr. 2011-2013;190:200-206. https://doi.org/10.1016/j.jpeds.2017.08.007.
28. Beck AF, Simmons JM, Huang B, Kahn RS. Geomedicine: area-based socioeconomic measures for assessing the risk of hospital reutilization among children admitted for asthma. Am J Public Health. 2012;102(12):2308-2314. https://doi.org/10.2105/AJPH.2012.300806.
29. Avenevoli S, Swendsen J, He JP, Burstein M, Merikangas KR. Major depression in the national comorbidity survey-adolescent supplement: prevalence, correlates, and treatment. J Am Acad Child Adolesc Psychiatry. 2015;54(1):37-44.e2. https://doi.org/10.1016/j.jaac.2014.10.010.
30. Feng JY, Toomey SL, Zaslavsky AM, Nakamura MM, Schuster MA. Readmission after pediatric mental health admissions. Pediatrics. 2017;140(6):e20171571. https://doi.org/10.1542/peds.2017-1571.
31. Merikangas KR, He JP, Burstein M, et al. Lifetime prevalence of mental disorders in U.S. adolescents: results from the National comorbidity Survey Replication-Adolescent Supplement (NCS-A). J Am Acad Child Adolesc Psychiatry. 2010;49(10):980-989. https://doi.org/10.1016/j.jaac.2010.05.017.
32. Cheung AH, Zuckerbrot RA, Jensen PS, et al. Guidelines for adolescent depression in primary care (GLAD-PC): Part II. Treatment and ongoing management. Pediatrics. 2018;141(3):e20174082. https://doi.org/10.1542/peds.2017-4082.
33. Zuckerbrot RA, Cheung A, Jensen PS, et al. Guidelines for adolescent depression in primary care (GLAD-PC): Part I. Practice preparation, identification, assessment, and initial management. Pediatrics. 2018;141(3):e20174081. https://doi.org/10.1542/peds.2017-4081.
34. Dolan MA, Fein JA, Committee on Pediatric Emergency Medicine. Pediatric and adolescent mental health emergencies in the emergency Medical Services system. Pediatrics. 2011;127(5):e1356-e1366. https://doi.org/10.1542/peds.2011-0522.
35. Collaborative Healthcare Strategies. Hospital Guide to Reducing Medicaid Readmissions. Rockville, MD: 2014. https://www.ahrq.gov/sites/default/files/publications/files/medreadmissions.pdf. Accessed 2017 Oct 11.
36. Hilbert K, Payne R, Wooton S. Children’s Hospitals’ Solutions for Patient Safety. Readmissions Bundle Tools. Cincinnati, OH; 2014.
37. Nuckols TK, Keeler E, Morton S, et al. Economic evaluation of quality improvement interventions designed to prevent hospital readmission: a systematic review and meta-analysis. JAMA Intern Med. 2017;177(7):975-985. https://doi.org/10.1001/jamainternmed.2017.1136.
38. Berry JG, Blaine K, Rogers J, et al. A framework of pediatric hospital discharge care informed by legislation, research, and practice. JAMA Pediatr. 2014;168(10):955-962. https://doi.org/10.1001/jamapediatrics.2014.891.
39. Chen HF, Carlson E, Popoola T, Suzuki S. The impact of rurality on 30-day preventable readmission, illness severity, and risk of mortality for heart failure Medicare home health beneficiaries. J Rural Health. 2016;32(2):176-187. https://doi.org/10.1111/jrh.12142.
40. Khan A, Nakamura MM, Zaslavsky AM, et al. Same-hospital readmission rates as a measure of pediatric quality of care. JAMA Pediatr. 2015;169(10):905-912. https://doi.org/10.1001/jamapediatrics.2015.1129.
41. Share DA, Campbell DA, Birkmeyer N, et al. How a regional collaborative of hospitals and physicians in Michigan cut costs and improved the quality of care. Health Aff. 2011;30(4):636-645. https://doi.org/10.1377/hlthaff.2010.0526.
42. Desai NR, Ross JS, Kwon JY, et al. Association between hospital penalty status under the hospital readmission reduction program and readmission rates for target and nontarget conditions. JAMA. 2016;316(24):2647-2656. https://doi.org/10.1001/jama.2016.18533.

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Journal of Hospital Medicine 14(9)
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Journal of Hospital Medicine 14(9)
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534-540. Published online first May 10, 2019
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