key: cord-0681899-tyihh0a2
authors: Dai, Chengzhen L; Kornilov, Sergey A; Roper, Ryan T; Cohen-Cline, Hannah; Jade, Kathleen; Smith, Brett; Heath, James R; Diaz, George; Goldman, Jason D; Magis, Andrew T; Hadlock, Jennifer J
title: Characteristics and Factors Associated with COVID-19 Infection, Hospitalization, and Mortality Across Race and Ethnicity
date: 2021-02-20
journal: Clin Infect Dis
DOI: 10.1093/cid/ciab154
sha: 82cdca39642271ea2e109b04bb95a3811229b1d1
doc_id: 681899
cord_uid: tyihh0a2

BACKGROUND: Data on the characteristics of COVID-19 patients disaggregated by race/ethnicity remain limited. We evaluated the sociodemographic and clinical characteristics of patients across racial/ethnic groups and assessed their associations with COVID-19 outcomes. METHODS: This retrospective cohort study examined 629,953 patients tested for SARS-CoV-2 in a large health system spanning California, Oregon, and Washington between March 1 and December 31, 2020. Sociodemographic and clinical characteristics were obtained from electronic health records. Odds of SARS-CoV-2 infection, COVID-19 hospitalization, and in-hospital death were assessed with multivariate logistic regression. RESULTS: 570,298 patients with known race/ethnicity were tested for SARS-CoV-2, of whom 27.8% were non-White minorities. 54,645 individuals tested positive, with minorities representing 50.1%. Hispanics represented 34.3% of infections but only 13.4% of tests. While generally younger than White patients, Hispanics had higher rates of diabetes but fewer other comorbidities. 8,536 patients were hospitalized and 1,246 died, of whom 56.1% and 54.4% were non-White, respectively. Racial/ethnic distributions of outcomes across the health system tracked with state-level statistics. Increased odds of testing positive and hospitalization were associated with all minority races/ethnicities. Hispanic patients also exhibited increased morbidity, and Hispanic race/ethnicity was associated with in-hospital mortality (OR: 1.39 [95% CI: 1.14-1.70]). CONCLUSION: Major healthcare disparities were evident, especially among Hispanics who tested positive at a higher rate, required excess hospitalization and mechanical ventilation, and had higher odds of in-hospital mortality despite younger age. Targeted, culturally-responsive interventions and equitable vaccine development and distribution are needed to address the increased risk of poorer COVID-19 outcomes among minority populations.

identified as non-Hispanic White; 11.5% as Hispanic; 6.8% as non-Hispanic Asian American; 3.6 % as non-Hispanic Black; 0.6% non-Hispanic American Indian/Alaska Native; 0.5% non-Hispanic Native Hawaiian/Pacific Islander; 5.7% non-Hispanic Other; and 8.8% Unknown. The protocol for this study was approved by the PSJH Institutional Review Board (IRB#: STUDY2020000203).

Patient demographic and clinical data were extracted from PSJH's Epic electronic health record system. Patients with a positive PCR test for SARS-CoV-2 were considered to have a confirmed SARS-CoV-2 infection. For patients who had multiple tests, only the initial positive test result was considered. Extracted demographic data included age, sex, race, ethnicity, and insurance plan. 85 patients with missing sex were excluded from the study. Missing race or ethnicity were grouped as Unknown. ZIP codes were used to identify the neighborhood-level median income, crowded housing (>1 person per room), minority population (race/ethnicity except non-Hispanic white), and limited English-proficient speakers from the US Census Bureau's American Community Survey. Clinical data include underlying medical conditions identified using ICD-10-CM codes or direct clinical measurements linked to past encounters between January 1, 2019 and the date of SARS-CoV-2 A c c e p t e d M a n u s c r i p t 7 testing. We included underlying medical conditions that have previously been associated with COVID-19. [12, 13] Charlson Comorbidity Index (CCI) was used to capture the risk from multiple comorbidities. Obesity and hypertension, which are not part of CCI, were also included. We used previously-defined diagnosis codes for components of CCI; [14] I10 for hypertension and BMI For comparison with state-level data, COVID-19 cases and deaths for California, Oregon, and Washington was obtained from the COVID Racial Data Tracker, which aggregates historical data from state agencies. [15] Data on COVID-19 hospitalization for California and Oregon was obtained from the Center for Disease Control's COVID-NET while Washington data was obtained from the COVID Racial Data Tracker. [15, 16] 

We compared the sociodemographic and clinical characteristics of patients across COVID-19 outcomes and race/ethnicity categories, defined as Hispanic; non-Hispanic Black (Black); non-Hispanic Asian American (Asian); non-Hispanic Native Hawaiian and Pacific Islander (NH/PI); non-Hispanic American Indian and Alaska Native (AI/AN); non-Hispanic white (White); and non-Hispanic other (Other), which includes multi-race/ethnicity. For COVID-19 hospitalized patients, presenting clinical characteristics were available and included clinical status on the World Health Organization (WHO) 9-point Clinical Progression Scale; [17] presenting vitals within the first 6 hours of admissions;

A c c e p t e d M a n u s c r i p t 8 and baseline laboratory test results within 24 hours of admissions. The WHO Clinical Progression Scale was developed to measure clinical illness of an COVID-19 infection and consists of the following categories: 0-uninfected; 1-ambulatory, no limitation of activity; 2-ambulatory, limitation of activity; 3-hospitalized, no oxygen therapy; 4-hospitalized, oxygen by mask or nasal prongs; 5hospitalized, non-invasive ventilation or high-flow oxygen; 6-hospitalized, intubation and mechanical ventilation; 7-hospitalized, ventilation + additional organ support; 8-death.

Associations with SARS-CoV-2 infection, COVID-19 hospitalization, and in-hospital mortality was assessed using mixed-effect logistic regression models with state and month of diagnosis nested random effect variables to account for geographic and temporal variations. For each outcome, we fitted both unadjusted univariate models and adjusted multivariate models. All multivariate models included race/ethnicity as an independent variable, with demographic factors (age; age-squared; sex), socioeconomic factors (insurance; neighborhood median income, crowded housing, limited English proficiency, and minority), and comorbidities (CCI; hypertension; obesity) as covariates. An age-squared term was included in addition to age to capture the non-linear relationship between COVID-19 outcomes and age. [18] For analyses of hospital mortality, additional covariates included presenting WHO Clinical Progression Scale score and baseline lab results. Covariates were selected based on previously identified risk factors and patterns of missingness and collinearity. Certain characteristics-BMI, insurance coverage, and baseline lab results-were not available for all patients. Alanine transaminase was excluded due to high correlation with aspartate transaminase and had higher missingness. For variables with less than 20% missingness, missing values were imputed with multiple imputation by fully conditional specification (15 imputations A c c e p t e d M a n u s c r i p t 9

A total of 629,953 patients tested for SARS-CoV-2 were included. 570,298 patients (90.5%) reported race/ethnicity, of which 72.2% were White, 13.4% were Hispanic, 5.4% were Asian, 3.8% Black, 0.9% were AI/AN, 0.6% were NH/PI, and 3.7% were Other ( Table 1 Table S1 ). The most common comorbidities were obesity (37.1%), hypertension (23.3%), diabetes (9.4%) and asthma (6.5%). The median score on the Charlson Comorbidity Index (CCI) was 1.0 (95% CI: 0.0-3.0).

54,645 patients (8.7%) of the 629,953 patients tested for SARS-CoV-2 were positive. Among the 49,081 patients with known race/ethnicity, the rate of positive test results was higher for minority patients than White patients (5.9%; Table S1 ). Hispanic and NH/PI patients had the highest rates (22.1% and 13.5%, respectively). Consequently, the racial/ethnic composition of SARS-CoV-2 infected patients were 49.9% White, 34.3% Hispanic, 5.0% Asian, 4.8% Other, 4.2% Black, 1.0% NH/PI (1.4%), and 0.9% AI/AN patients ( Table 1) .

Among all SARS-CoV-2 infected patients, the mean age was 47.8±19.2 years and 52.6% were female ( Table 1) . Compared to White patients, mean ages were lower among patients of minority race/ethnicity, except for Asians, which had a similar mean age ( Table 2) . CCI scores were also lower among minority patients. The prevalence of diabetes, however, was higher among minority patients.

A c c e p t e d M a n u s c r i p t 10 Additionally, relative to White patients, Hispanic, Black, NH/PI, and AI/AN patients had higher prevalence of obesity; Asian, Black, NH/PI, and AI/AN patients had higher prevalence of hypertension; and Black, NH/PI, and AI/AN patients had higher prevalence of both asthma and kidney disease.

Hispanic, Black, NH/PI, and AI/NH patients were more likely to have Medicaid insurance than White and Asian patients ( Table 2 ). All minority patients were more likely than White patients to reside in neighborhoods with higher percentages of crowded housing and minorities. Hispanic, Asian, and Black patients in particular were also more likely to live in neighborhoods with a higher percentage of limited English proficient population. All minority patients were more likely to have received their tests in the emergency department than White patients.

15.6% (n=8,536) of the patients who tested positive for COVID-19 were hospitalized. 8,210 patients (96.2%) had known race/ethnicity, of which 45.7% were White, 35.3% were Hispanic, 6.5% were Asian, 4.5% were Black, 1.2% were NH/PI, 0.9% were AI/AN, and 5.9% were Other ( Table 1) . The mean age of all patients was 64.7±17.6 years and 54.5% were male. The median CCI score was 3.0 (2.0-6.0) and the most common comorbidities were obesity (42.4%), hypertension (40.2%), and diabetes (28.3%).

White patients had the highest mean age (70.5±16.2 years; Table 3 ) and median CCI score On admission, a higher percentage of Hispanic patients (11.1%) than White patients (6.7%) had a score of five or above on the WHO Clinical Progression Scale, and a higher percentage of Hispanic patients than White patients were febrile, had low oxygen saturation, and had high respiration rates.

Over the course of hospitalization, a higher percentage of Hispanic patients (18.5%) than White patients (11.1%) needed mechanical ventilation.

Throughout the pandemic, rates of positive test, hospitalization, and in-hospital mortality per 100,000 patients were on average higher for Black, Hispanic, NH/PI, and AI/AN patients than Asian and White patients (Figure 1 ). Hispanics patients, in particular, had the highest rates, especially during the June-July and November-December resurgence of COVID-19. The mean age of SARS-CoV-2 infected patients generally decreased over time while the mean age of COVID-19 hospitalized patients and patients who experienced in-hospital mortality remained relatively consistent.

The distribution of race/ethnicity among patients in this study generally reflected state-level distributions for COVID-19 outcomes ( Figure S1-3) , including for mortality in which state-level data A c c e p t e d M a n u s c r i p t 12 captured both in-hospital and out-of-hospital deaths. High proportions of Hispanics were consistently observed in both the state-wide data and the health system. The differences in racial/ethnic distributions between the health system population and the catchment population were consistent or smaller than the differences observed at the state-level (Figure S4-5 ).

Minority populations including Hispanic, Black, Asian, NH/PI and AI/AN had increased odds of SARS-CoV-2 infection compared to Whites in unadjusted and adjusted analysis ( Medicaid insurance, lack of insurance, and residence in a neighborhood with higher percentage limited English proficient individuals were also independently associated with increased odds of infection. Higher CCI score, Medicare insurance, and higher median income, however, were associated with lower odds of positive SARS-CoV-2 infection.

Minority races/ethnicities were also associated with increased odds for COVID-19 hospitalization ( Increasing age, male sex, public insurance, no insurance, higher CCI score, being underweight, having class 2 or 3 obesity, having hypertension, and residence in a neighborhood with higher rates of A c c e p t e d M a n u s c r i p t 13 limited English proficiency were also independently associated with increased odds of hospitalization.

In adjusted multivariate analysis, Hispanic race/ethnicity was significantly associated with increased odds of in-hospital mortality (1.41 [1.15 -1.71]). Other minority races/ethnicities, however, were not significantly associated ( Table 4) . Hospital mortality was also independently associated with age; class 3 obesity; public insurance; higher score on the WHO Clinical Progression Scale and CCI; and high white blood cell count, low lymphocyte, low platelet count, high AST, high blood urea nitrogen, high creatinine, and high bilirubin. Interaction analysis of race/ethnicity and age further identified disproportionately increased odds of hospital mortality among Hispanic patients as age increased previous studies, we also found a significant association between Hispanic race/ethnicity and hospital mortality and a significant interaction between Hispanic race/ethnicity and age that signifies the relationship between Hispanic race/ethnicity and hospital mortality is moderated by age. The clinical characteristics of Hispanic patients at hospital admission suggest that they are presenting with more severe illness than White patients, as Hispanic patients are more likely to be febrile, have low oxygen saturation, and high respiration rates. The higher percentage of Hispanic patients A c c e p t e d M a n u s c r i p t 15 presented with WHO Clinical Progression Scale scores of five or higher reflects a need for high-flow supplemental oxygen or mechanical ventilation. These clinical findings indicate a delay in seeking care among Hispanic patients. While this study cannot identify the causes behind the observed associations, certain social, structural or biologic determinants of health have been suggested. [3] Social and structural determinants could include occupation risk and limited access to healthcare and testing. [3] Additional studies are needed to identify the causal factors driving disparities in COVID-19. While the large size of this study's diverse cohort and its multi-state distribution are strengths of this study, there are limitations. This study was limited to a single health system and certain catchment areas within California, Oregon, and Washington. Thus, the results may be less generalizable to other regions. In particular, the racial/ethnicity composition of COVID-19 patients in our study's may 

No funders had a role in designing the study; collecting, analyzing, or interpreting the data; or preparing, reviewing, or approving the manuscript for submission/publication. M a n u s c r i p t 22 M a n u s c r i p t 23 A c c e p t e d M a n u s c r i p t M a n u s c r i p t M a n u s c r i p t 

Left column represents patients who have tested positive for SARS-CoV-2 infection; middle column represents patients who have been hospitalized for COVID-19; and right column represents COVID-19

hospitalized patients who experienced in-hospital death. The first row of each column represents the rolling 7-day mean count of patients for the event; the second row represents the rolling 7-day mean age of patients; and the third row represents the 7-day mean rate of event per 100,000 patients. Rate per 100,000 patients were calculated out of total patients under care since 2019 for each race/ethnicity.

A c c e p t e d M a n u s c r i p t 32 Figure 1 

CDC. COVID-19 Hospitalization and Death by Race/Ethnicity. 2020. Available at

Disparities in Incidence of COVID-19 Among Underrepresented Racial/Ethnic Groups in Counties Identified as Hotspots During

COVID-19 and Racial/Ethnic Disparities

Ethnic and racial disparities in COVID-19-related deaths: counting the trees, hiding the forest

Racial Disparities in COVID-19: Key Findings from Available Data and Analysis -Issue Brief

Racial/ethnic differences in multimorbidity development and chronic disease accumulation for middle-aged adults

Communities of Color at Higher Risk for Health and Economic Challenges due to COVID-19

Associations Between Built Environment, Neighborhood Socioeconomic Status, and SARS-CoV-2 Infection Among Pregnant Women

Individuals with obesity and COVID-19: A global perspective on the epidemiology and biological relationships

Count Native Hawaiian And Pacific Islanders In COVID-19 Data-It's An OMB Mandate

Asian Americans Facing High COVID-19 Case Fatality

Comorbidity and its impact on 1590 patients with COVID-19 in China: a nationwide analysis

Charlson Comorbidity Index Score and Risk of Severe Outcome and Death in Danish COVID-19 Patients

Coding algorithms for defining comorbidities in ICD-9-CM and ICD-10 administrative data

COVID-19)-Associated Hospitalization Surveillance Network (COVID-NET)

COVID-19 Therapeutic Trial Synopsis. Available at

Characteristics of and Important Lessons From the Coronavirus Disease 2019 (COVID-19) Outbreak in China: Summary of a Report of 72 314 Cases From the Chinese Center for Disease Control and Prevention

COVID-19 disparities: An urgent call for race reporting and representation in clinical research

Hospitalization and Mortality among Black Patients and White Patients with Covid-19

Association of Race With Mortality Among Patients Hospitalized With Coronavirus Disease 2019 (COVID-19) at 92 US Hospitals

Class 2 Obesity 52

5%) 2,894 (5.3%) 574 (6.7%)

6%) 2,897 (5.3%) 1,469 (17.2%) Liver disease 19,772 (3.1%) 1,353 (2.5%) 345 (4.0%) Cancer

1%) 12,842 (52.5%) 1,181 (50.2%) 2,737 (49.2%) Male

8%) 538 (22.9%) 1,322 (23.8%) Other outpatient 4,165 (24.7%) 564 (27.3%)

1%) 85 (26.1%) 2,891

) 106 (19.9%) 21 (21.4%) 12 (15.6%) 749 (20.0%) 74 (15.3%) 37 (11.3%) Liver disease 97/2

Oxygen saturation < 94% 1

3%) 97/317 (30.6%)

4%) 640/3,668 (17.4%) 83/471 (17.6%)

) on the WHO Clinical Progression Scale, as defined as: WHO Score 3 -hospitalized, no oxygen therapy; WHO Score 4 -hospitalized, oxygen by mask or nasal prongs; WHO Score 5 -hospitalized, non-invasive ventilation or high-flow oxygen

A c c e p t e d M a n u s c r i p t A c c e p t e d M a n u s c r i p t