key: cord-0887135-997lpw4k
authors: Fernandes, Danielle M.; Oliveira, Carlos R.; Guerguis, Sandra; Eisenberg, Ruth; Choi, Jaeun; Kim, Mimi; Abdelhemid, Ashraf; Agha, Rabia; Agarwal, Saranga; Aschner, Judy L.; Avner, Jeffrey R.; Ballance, Cathleen; Bock, Joshua; Bhavsar, Sejal M.; Campbell, Melissa; Clouser, Katharine N.; Gesner, Matthew; Goldman, David L.; Hammerschlag, Margaret R.; Hymes, Saul; Howard, Ashley; Jung, Hee-jin; Kohlhoff, Stephan; Kojaoghlanian, Tsoline; Lewis, Rachel; Nachman, Sharon; Naganathan, Srividya; Paintsil, Elijah; Pall, Harpreet; Sy, Sharlene; Wadowski, Stephen; Zirinsky, Elissa; Cabana, Michael D.; Herold, Betsy C.
title: SARS-CoV-2 Clinical Syndromes and Predictors of Disease Severity in Hospitalized Children and Youth
date: 2020-11-14
journal: J Pediatr
DOI: 10.1016/j.jpeds.2020.11.016
sha: 2c9a8aa1e65213b4dcdda4657d143b62cdcbbdd6
doc_id: 887135
cord_uid: 997lpw4k

OBJECTIVE: To characterize the demographic and clinical features of pediatric SARS-CoV-2 syndromes and identify admission variables predictive of disease severity. STUDY DESIGN: We conducted a multicenter, retrospective and prospective study of pediatric patients hospitalized with acute SARS-CoV-2 infections and multisystem inflammatory syndrome in children (MIS-C) at eight sites in New York, New Jersey, and Connecticut. RESULTS: We identified 281 hospitalized patients with SARS-CoV-2 infections and divided them into three groups based on clinical features. Overall, 143 (51%) had respiratory disease, 69 (25%) had MIS-C, and 69 (25%) had other manifestations including gastrointestinal illness or fever. Patients with MIS-C were more likely to identify as non-Hispanic black compared with patients with respiratory disease (35% versus 18%, P=.02). Seven patients (2%) died and 114 (41%) were admitted to the ICU. In multivariable analyses, obesity (OR=3.39, 95% CI:1.26-9.10, P=.02) and hypoxia on admission (OR=4.01; 95% CI:1.14-14.15; P=.03) were predictive of severe respiratory disease. Lower absolute lymphocyte count (OR=8.33 per unit decrease in 10(9) cells/L, 95% CI:2.32-33.33, P=.001) and higher C-reactive protein (OR=1.06 per unit increase in mg/dL, 95% CI:1.01-1.12, P=.017) were predictive of severe MIS-C. Race/ethnicity or socioeconomic status were not predictive of disease severity. CONCLUSIONS: We identified variables at the time of hospitalization that may help predict the development of severe SARS-CoV-2 disease manifestations in children and youth. These variables may have implications for future prognostic tools that inform hospital admission and clinical management.

life and pregnant patients were excluded. In addition, patients who were admitted to the hospital with unrelated illnesses such as trauma, scheduled chemotherapy, or psychiatric disease and were found to be incidentally positive for SARS-CoV-2 by admission PCR screening were also excluded.

We reviewed the electronic medical records for demographic, clinical, laboratory, radiographic, and hospitalization outcome data from admission to discharge. Investigators at each site used a standardized data collection form and transmitted data to a central database using a web-based data capture program hosted at Albert Einstein College of Medicine (Bronx, NY). The study was approved by each center's institutional review board, and each site was exempted from obtaining informed consent.

Respiratory COVID-19 was defined based on the World Health Organization criteria and included patients having any of the following clinical features: cough, dyspnea, tachypnea, oxygen requirement, or imaging suggestive of pneumonia. 25 Each MIS-C case was independently reviewed to ensure it met CDC criteria for MIS-C. Patients who did not meet the criteria for either respiratory COVID-19 or MIS-C were classified based on their primary reason for hospitalization. For the comparative analysis, non-respiratory, non-MIS-C SARS-CoV-2 infected hospitalized patients were broadly classified as "other." Severe disease was defined as an intensive care unit (ICU) admission ≥48 hours.

Self-reported race and ethnicity were categorized into Hispanic, non-Hispanic white, non-Hispanic black, and non-Hispanic other. Patients were categorized as obese if they had a body mass index (BMI) or weight-for-age (if < 2 years old) that was ≥ 95th percentile for age and sex. 26 Patients were considered medically complex if they had comorbidities that required J o u r n a l P r e -p r o o f 6 multiple services, were technology-dependent, were considered medically fragile (e.g., cancer), or had a severe disability (e.g., intellectual disability). 27, 28 Admission vital signs and relevant laboratory test results were described using age-adjusted standard values. 29 Study definitions are detailed in Table 2 (available at www.jpeds.com). Socioeconomic measures at the zip code level were used to generate a composite index and proxy measure of individual-level SES. The selected area-level measures were based on previously described and validated instruments using data from the American Community Survey (2014) (2015) (2016) (2017) (2018) 30 , 31 and are further described in the Table 2 . Patients were considered as low SES if they resided in a zip code that was ≥1 standard deviation below the mean area-level SES index.

Descriptive statistics were used to summarize the clinical and sociodemographic characteristics of all patients for whom data were available. The clinical syndromes were collapsed into three groups: respiratory, MIS-C, and other. Differences in the distribution of the measured variables were compared using Fisher exact and Kruskal-Wallis tests for categorical and continuous variables, respectively. Results were adjusted for multiple comparisons with Tukey test.

Multivariable logistic regression models were fit for both respiratory and MIS-C groups separately to identify patient characteristics on admission that were predictive of developing severe disease. Potential predictor variables included: clinical manifestations, BMI, comorbidities, laboratory results, insurance status, race/ethnicity, age, sex, and SES. Categories of predictor variables with sparse data were combined before inclusion in the multivariable models. Specifically, insurance status was examined as Medicare/Medicaid versus all other types of payers, and race/ethnicity was examined as Hispanic, Non-Hispanic black, and Non-J o u r n a l P r e -p r o o f 7 Hispanic white or Non-Hispanic other. Only three patients with respiratory classification and six patients with MIS-C were classified as Non-Hispanic other.

For the severity models, adjusted odds ratios (aOR) were adjusted for hospital site using a fixed-effects approach given concerns about the performance and lack of convergence of random-effects models when the number of sites (clusters) is small. 32 For the multivariable analyses, the initial model included variables with P<.25 in bivariate analyses, in addition to age and race, which were deemed a priori to be important clinically (Model 1). An additional model also was fit using a stepwise backward selection strategy in which only those variables with P<.05 were retained (Model 2). Missing data rates in the predictor variables ranged from 0% to 16% and were handled using both list-wise deletion (i.e., available data) and multiple imputation (MI) using chained equations. C-reactive protein (CRP) level was not considered for inclusion in the respiratory specific model due to a high rate of missing data (28%) and potential bias from non-random missingness because CRP likely was measured more frequently in patients with severe disease.

No sample-size calculations were performed a priori. All tests of statistical significance were two-sided, and P<.05 were defined as statistically significant. Statistical analyses were performed using both Stata (V.15, Stata Corp, Texas, USA) and SAS (V. 9.4, SAS Institute Inc, Cary, NC, USA) statistical software.

We identified 315 hospitalized pediatric patients with laboratory-confirmed SARS-CoV-2 infection or MIS-C during the peak 3-month period of the pandemic in the Tri-State area. We J o u r n a l P r e -p r o o f 8 excluded 34 patients from the final cohort for analysis because review of the medical record indicated that they were hospitalized for unrelated problems deemed unlikely to be etiologically related to SARS-CoV-2, leaving a final cohort of 281 patients ( Table 1 ). The NY hospitals were located in Brooklyn, Bronx and Suffolk counties, which were among the hardest impacted areas. Hospitalizations for respiratory disease peaked during the third week of the study period and began to decline three weeks later, as MIS-C cases began to increase (Figure 1) . Hospitalizations for other syndromes peaked during the fourth week of the pandemic and remained relatively constant throughout the study period.

The baseline characteristics of the overall cohort are detailed in Table 3 Among the 281 patients, 143 (51%) presented with respiratory disease, 69 (25%) with MIS-C, and 69 (25%) with one of the other acute SARS-CoV-2 related clinical syndromes or conditions. The "other" group included 32 patients with gastrointestinal symptoms, 21 febrile infants, 6 with neurologic disease, 6 with diabetic ketoacidosis, and 4 patients hospitalized for other indications listed in Table 4 (available at www.jpeds.com). Additional details on the clinical features and outcomes of patients in this "other" group are shown in Table 5 (available at www.jpeds.com).

J o u r n a l P r e -p r o o f 9 The distribution of baseline patient characteristics varied significantly between the different clinical syndromes ( Table 3) . Patients with respiratory disease were older than those with MIS-C (median age: 14 [IQR: [3] [4] [5] [6] [7] [8] [9] [10] [11] [12] [13] [14] [15] [16] [17] [18] [19] ] vs. 7 [IQR: [3] [4] [5] [6] [7] [8] [9] [10] [11] years, respectively, P<.001).

Compared with respiratory COVID-19, patients with MIS-C identified their race/ethnicity more commonly as non-Hispanic black (difference = 18%, 95%CI: 2%-33%, P=.02). Notably, the prevalence of obesity was 18% higher (95%CI: 2%-34%, P=.02) in the respiratory disease group compared with MIS-C. Similarly, the prevalence of medical complexity was 24% higher (95%CI: 10%-38%, P<.001) in the respiratory disease group compared with patients with MIS-C. Differences in other baseline characteristics by syndrome are shown in Table 6 (available at www.jpeds.com).

The most common signs and symptoms on admission are shown in Figure 2 

Nearly all patients (267/281 [95%]) recovered from their illness and were discharged home by the end of the study ( Table 9 (available at www.jpeds.com).

Overall, 40% (56/141) of patients with respiratory disease, 56% (38/68) with MIS-C, and 6% (4/69) with "other" phenotypes met our case definition of severe disease (i.e., ≥48 hours in the ICU). In multivariable analyses of the respiratory group ( 15 ), and bilateral infiltrates on chest radiograph (aOR=3.69, 95%CI: 1.46-9.32) at admission were independent predictors of severe disease (model 2); race adjusted results were similar (model 1). In the MIS-C group (Table 10) , only lower ALC (aOR=8.33 per unit decrease in 10 9 cells/L, 95%CI: 2.32-33.33) and increasing CRP (aOR=1.06 per unit increase in mg/dL, 95%CI: 1.01-1.12) at admission were independent predictors of severity (model 2). Insurance status, race/ethnicity, and SES were not significantly predictive of respiratory or MIS-C disease severity. Three patients were excluded from the analysis of disease severity (1 respiratory patient who died on the day of admission, 1 patient who was previously chronically ventilator-dependent and discharged on the same day of admission, and 1 MIS-C patient transferred to another facility on the day of admission). Results after conducting multiple imputation for missing data were similar to those estimated using available data ( Table 11; available at www.jpeds.com).

In a separate analysis, laboratory variables measured during hospitalization (as opposed to at admission) also were compared between clinical syndromes. Compared with non-severe J o u r n a l P r e -p r o o f 12 cases, both severe respiratory disease and MIS-C were significantly associated with a higher peak CRP, procalcitonin, or troponin level, and a lower nadir ALC, platelet count, or serum sodium level (Table 12 ; available at www.jpeds.com). Although 78% (45/58) of patients with MIS-C had an elevated B-type natriuretic peptide (BNP), peak BNP did not differ significantly by severity status.

This multicenter cohort study describes a spectrum of clinical manifestations of SARS-CoV-2 in children and youth admitted to hospitals that serve racially and ethnically diverse regions of NY, NJ, and CT. Although the populations served by the hospitals vary in terms of sociodemographic diversity, with several having a predominantly non-Hispanic white population, nearly all sites reported that the majority of patients with SARS-CoV-2 were Hispanic and/or black. Notably, patients with MIS-C were more likely to be Non-Hispanic black, whereas children with respiratory illness were more likely to be Hispanic. Previous MIS-C case series also have shown that black children represent a significant percentage of MIS-C cases in the US, ranging from 25-40%. 2, 3, 22 These data reinforce the notion that minorities bear a disproportionate burden of disease.

There also have been reports that communities with a high proportion of lower-income individuals are experiencing a disproportionately higher rate of COVID-19. 33, 34 Consistent with these reports, we found that 31% of patients hospitalized with SARS-CoV-2 were of low SES.

Poverty is associated with poor health outcomes and higher rates of pediatric ICU admissions in general. 35 Importantly, however, children of lower SES in our study were not more likely to have severe outcomes following hospitalization.

J o u r n a l P r e -p r o o f 13 Several features differentiated the various SARS-CoV-2 infection phenotypes. More than half of the patients with respiratory disease (similar to COVID-19 in adults) were older than 13 years on admission. Similar to what has been reported for adults, children and youth with respiratory COVID-19 commonly had obesity, preexisting pulmonary and neurologic disease, as well as medical complexity. In contrast, patients with MIS-C often had no comorbidities, and more than half were under 7 years of age. Although patients with MIS-C often were critically ill, requiring vasopressor and immunomodulatory therapy, their hospitalization outcomes generally were excellent.

There is little evidence-based guidance available to aid clinicians in the management of children and youth with acute COVID-19 or MIS-C. Predicting clinical decompensation has important ramifications in terms of resource utilization, hospital admission, and patient management. In terms of severity, close to one third of the hospitalized patients in our cohort spent ≥ 48 hours in the ICU, and 2% (7/281) died. Patients with respiratory COVID-19 were more likely to develop severe disease if, on admission, they had either an elevated white blood cell count, hypoxia, bilateral infiltrates on chest radiograph, were of younger age, or were obese.

The association between weight and severe respiratory COVID-19 is consistent with the adult literature; however, the mechanisms of this association require further study. 36 For MIS-C, only admission laboratory values of CRP and absolute lymphocyte count were predictive of severity.

This study builds on the growing body of evidence showing that mortality in hospitalized pediatric patients is low compared with adults. 8, 9 However, it highlights that the young population is not universally spared from morbidity, and that even previously healthy children and youth can develop severe disease requiring supportive therapy. 37, 38 J o u r n a l P r e -p r o o f 14 We found a wide array of clinical manifestations in children and youth hospitalized with SARS-CoV-2. Although most of the clinical manifestations in children have also been reported in adults, the frequency of some differ considerably. For example, gastrointestinal symptoms such as abdominal pain, emesis and diarrhea, occur in less than a quarter of hospitalized adults, yet up to half of the patients in our cohort reported one of these symptoms 39 . Ocular and dermatologic findings are also rarely reported in adults yet were observed in 32% and 39% of MIS-C cases, respectively. We also found that SARS-CoV-2 can be an incidental finding in a substantial number of hospitalized pediatric patients. As testing became more accessible and routine for all hospital admissions in late March, we documented a steady rate of incidental SARS-CoV-2 infections (i.e. not plausibly etiologically related). This observation has implications for infection control policies and for monitoring community prevalence of infection.

Although data are limited, studies show that children can have high viral loads even when asymptomatic or affected with mild disease and some studies suggest that they can spread disease 40 , making it important to screen hospitalized children to both limit potential transmission and track community prevalence of the virus.

Our study has limitations. The study population included patients within the Tri-State area but did not include patients hospitalized in all of the New York City boroughs and may not be generalizable to other geographic regions. Decisions to admit to the hospital and ICU may have varied by location. To date, children have been excluded from randomized controlled trials of antiviral drugs such as remdesivir 41, 42 and there have been no controlled studies on the optimal treatment of MIS-C. Therefore, approaches to treatment, and as a consequence, the clinical outcomes of the patients in this study, may have varied across sites. 

Respiratory: any one of the following reported or documented clinical features: cough, dyspnea, tachypnea, increased oxygen requirement, or imaging suggestive of pneumonia. MIS-C: aged <21 years, with fever for more than 24 hours, laboratory markers of inflammation, multisystem organ involvement, positive of SARS-CoV-2 testing or exposure to a suspected or confirmed COVID-19 case within four weeks of symptom onset, and no plausible alternative diagnoses. Other: Patients who did not meet the criteria for either respiratory COVID-19 or MIS-C.

Patients with incidental SARS-CoV-2 included those hospitalized for psychiatric diseases (n=9), trauma (n=7), cancer treatment (n=2), gastrostomy tube malfunction (n=1), skin and soft tissue infection (n=8), urinary tract infection (n=3), bacteremia (n=2), otorrhea (n=1), and Epstein-Barr virus infection (n=1).

Previous definitions for severe disease include any admission to the intensive care unit, need for supplemental oxygen or invasive mechanical ventilation and, for MIS-C, vasopressor support. 1,3, 5 We defined severe disease as ≥ 48 hours in the ICU. With the exception of 1 patient who was transferred on the day of admission, 1 patient who was chronically ventilator-dependent and discharged on hospital day one, and 1 patient who died on the day of admission, this definition included all children who were ventilated during hospitalization and/or required vasopressors. There were 16 patients (6%) who were admitted to the ICU for <48 hours and none of these required mechanical ventilation or vasopressors.

Two or more of the following: Any one of the following: multiple comorbidities that require multiple services, technology-dependence, medical fragility (e.g., cancer, congenital heart disease), or severe disability (e.g., intellectual disability). COVID-19 exposure Given the high incidence of COVID-19 infection in the Tri-State area during the study period, all patients who met criteria for MIS-C were considered exposed.

Defined as having subjective fever or measured temperature of ≥38.0 degrees Celsius by any method Hypoxia

Defined as oxygen saturation <90% Tachypnea for age

Refers to a presenting respiratory rate (RR) per minute above the 95 th percentile for age 45 

Using data from the American Community Survey (2014-2018), we calculated a socioeconomic score index based on patient home addresses as previously described and validated. 31 The index includes data from each patient's home zip code using census-derived zip code tabulation areas and combines six variables to form a SES score for each geographic area. The variables are the percentage of 1) adults with less than a high school education; 2) families with income below the federal poverty level; 3) households receiving public assistance; 4) female-headed households with children; 5) male unemployment; and 6) median household income. These measures were standardized to a mean of 0 and a standard deviation of 1, with positive values associated with a higher socioeconomic status. The variables were then summed and re-standardized to a mean of 0 and a standard deviation of 1.

Data are presented as n/total (%) for categorical measures and median (IQR) for continuous measures. Pairwise comparison between groups are shown in Table 6 . Continuous variables are compared using ANOVA or Kruskal-Wallis based on normality test, categorical variables are compared using Fisher's exact tests. a See definitions in Table 2 . Table 2 b Hospital length of stay excluding patients who were transferred to another facility c ICU length of stay excluding patients who did not spend time in ICU J o u r n a l P r e -p r o o f J o u r n a l P r e -p r o o f Table 9 . Narrative of Deaths year-old male with intermittent asthma, asthma, seizure disorder, developmental delay, and a gastrostomy tube, was admitted with a 3-day history of fever, cough, wheezing, dyspnea, and increased seizure frequency. He was started on high-flow nasal cannula, but by the first hospital day, he required intubation for mechanical ventilation. He was noted to have co-infection with Rhinovirus as well as SARS-CoV-2. He received methylprednisolone on admission and was on a steroid taper throughout this hospitalization. A 10-day course of Remdesivir and a single dose of Anakinra were also given. He developed line-associated Enterococcus faecalis bacteremia and was also noted to have a right femoral deep-vein-thrombosis for which he received antibiotics and anticoagulation, respectively. He died on hospital day 58. An 11-year-old-male with metastatic osteosarcoma on palliative chemotherapy with baseline nasal-cannula oxygen requirement presented with dyspnea and cough of 1-day duration. He was immediately intubated and mechanically ventilated for respiratory failure per the family's request. Care was withdrawn approximately 1 week later, and the patient died from respiratory failure due to a combination of lung metastases and SARS-CoV-2 infection. A 3-month-old female with pulmonary hypertension, large atrial septum defect, and a moderate patent ductus arteriosus was admitted with a 1-day history of cough, fever, and dyspnea. She was initially started on nasal-cannula; however, soon after admission, she developed tachypnea and desaturations and was subsequently intubated for mechanical ventilation. She received a 10-day course of Remdesivir as well as intravenous immunoglobulin. She developed acute kidney injury, thrombocytopenia, and line-associated Enterococcus faecalis bacteremia. She remained mechanically ventilated and died on hospital day 30. An 18-year-old female with morbid obesity, hypertension, and intermittent asthma presented with 8-day history of cough, fever, and dyspnea. She was immediately intubated and mechanically ventilated in the intensive care unit. She had evidence of acute kidney injury and acute respiratory distress syndrome. She was started on hydroxychloroquine and azithromycin, but these were discontinued after two days. She received a five-day course of methylprednisolone and a single dose of tocilizumab. However, she remained mechanically ventilated and died on hospital day 38.

A 20-year-old male with a medical history of intermittent asthma was admitted with respiratory distress. He had been ill for 21 days prior to hospital presentation with fever, cough, wheezing, myalgia, dyspnea, vomiting, fatigue, and neck swelling. He was immediately intubated and mechanically ventilated after arriving at the intensive care unit. He had evidence of thrombocytopenia, acute respiratory distress syndrome, and acute kidney injury. He received empiric antibiotic therapy, methylprednisolone, and convalescent plasma but died on hospital day 2.

A 5-month-old male with no medical history was admitted after he was found to be unresponsive and limp while at home. No proceeding symptoms or known exposure to COVID-19 was reported. On hospital presentation, he was immediately intubated and started on mechanical ventilation as well as epinephrine, norepinephrine, and vasopressin. In addition to the SARS-CoV-2 infection, he was found to have parainfluenza infection. He received empiric antibiotic therapy with Ceftriaxone and Vancomycin. Five days into his hospitalization, he developed severe thrombocytopenia and acute kidney injury. At that time, he was started on a 6-day course of hydroxychloroquine. One week into his hospitalization, he was noted to have a Staphylococcus epidermidis lineassociated bacteremia as well as Stenotrophomonas maltophilia pneumonia. Despite these interventions, he remained mechanically ventilated. He was given convalescent plasma on hospital day 29. He died shortly after a 31-day hospitalization. A 10-year-old male with a medical history of intermittent asthma was admitted with fever, cough, wheezing, and dyspnea for seven days prior to presentation. The patient was noted to be in significant respiratory distress with hypoxia. He was admitted to the intensive care unit with ARDS and was mechanically ventilated and had L sided chest tube placement. He had evidence of acute kidney injury with elevated creatinine. He received methylprednisolone and empiric antibiotic therapy with Ceftaroline. He died on hospital day two due to respiratory distress.

J o u r n a l P r e -p r o o f Low SES a (reference ≥ -1) 0.78 (0.23, 2.62) 0.69 P values for OR (odds ratio) and aOR (adjusted OR) estimated using logistic regression. All estimates are adjusted for site with fixed effects. Excluded 2 Respiratory cases (one who was chronically ventilator-dependent and discharged on hospital day one, and one who died on the day of admission) and 1 MIS-C case (transferred on the day of admission). Model 1 includes variables with P<.25 in bivariate analysis, age and race. Model 2 includes only variables with P<.05 using stepwise backward selection strategy. CRP level excluded in multivariable Respiratory models because 28% missing and data not missing at random. Bilateral infiltrates on radiograph not included in multivariable MIS-C due to limited number of MIS-C patients with this condition (N=7). a See definitions in Table 2 For Respiratory illness, excluded 2 Respiratory cases (one who was chronically ventilator-dependent and discharged on hospital day one, and one who died on the day of admission). Multiple imputation model included outcome, all predictor variables listed in Table  10 and hospital site. Results based on 40 imputed data sets. For MIS-C, excluded 1 MIS-C case (transferred on the day of admission). Multiple imputation model included outcome, all predictor variables listed in Table 10 and hospital site. Results based on 40 imputed data sets. Model 1 includes variables with P<.25 in bivariate analysis, age and race. Model 2 had nearly complete data (2 missing values) so multiple imputation not performed. a See definitions in Table 2 J o u r n a l P r e -p r o o f Data are presented as median (IQR) for continuous measures, and n/total (%) for categorical measures. *Continuous variables are compared using Wilcoxon rank-sum, categorical variables are compared using Fisher's exact tests; Severity analysis excluded 1 MIS-C case (transferred on the day of admission) and 2 Respiratory cases (one who was chronically ventilator-dependent and discharged on hospital day one, and one who died on the day of admission). a See definitions in Table 2 . 

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COVID-19) at a Tertiary Care Medical Center

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We thank each of the COVID-19 treatment teams and healthcare providers at the sites involved in the care of patients with COVID-19 for their work and dedication to patient care.

J o u r n a l P r e -p r o o f