Background

Understanding the distribution of organ failure before and during the COVID-19 pandemic surge can provide a deeper understanding of how the pandemic strained health care systems and affected outcomes.

Objective

To assess the distribution of organ failure in 3 New York City hospitals during the COVID-19 pandemic.

Methods

A retrospective cohort study of adult admissions across hospitals from February 1, 2020, through May 31, 2020, was conducted. The cohort was stratified into those admitted before March 17, 2020 (prepandemic) and those admitted on or after that date (SARS-CoV-2–positive and non–SARS-CoV-2). Sequential Organ Failure Assessment scores were computed every 2 hours for each admission.

Results

A total of 1 794 975 scores were computed for 20 704 admissions. Before and during the pandemic, renal failure was the most common type of organ failure at admission and respiratory failure was the most common type of hospital-onset organ failure. The SARS-CoV-2–positive group showed a 231% increase in respiratory failure compared with the prepandemic group. More than 65% of hospital-onset organ failure in the prepandemic group and 83% of hospital-onset respiratory failure in the SARS-CoV-2–positive group occurred outside intensive care units. The SARS-CoV-2–positive group showed a 341% increase in multiorgan failure compared with the prepandemic group. Compared with the prepandemic and non–SARS-CoV-2 patients, SARS-CoV-2–positive patients had significantly higher mortality for the same admission and maximum organ failure score.

Conclusion

Most hospital-onset organ failure began outside intensive care units, with a marked increase in multiorgan failure during pandemic surge conditions and greater hospital mortality for the severity of organ failure.

The COVID-19 pandemic resulted in a rapid increase in critically ill patients. Before the pandemic, the burden and distribution of organ failure had been well described within the intensive care unit (ICU) setting.1-4  However, organ failure outside of the ICU is less well studied. During the pandemic, ICU beds became scarce.5-7  The shift in the burden of organ failure (from inside to outside the ICU) and demand for hospital resources under pandemic surge conditions made it important for physicians, administrators, and policy makers to understand the development, severity, and outcomes of organ failure throughout hospitals.

At the peak of the pandemic, resources such as ICU beds and ventilators were scarce in heavily affected regions of the United States, and multiple states had ventilator allocation guidelines that based the triage of life support on the severity of organ failure, often using the Sequential Organ Failure Assessment (SOFA) score in the decision-making process.8,9  Automating calculations of SOFA scores for all patients in near-real time would be needed for such a triaging system to be useful under pandemic conditions, but this calculation system had been demonstrated only for a limited number of ICU patients in a resource-rich setting.10 

Multiple states based the triage of life support on the severity of organ failure, often using the Sequential Organ Failure Assessment (SOFA) score.

During the first wave of the COVID-19 pandemic in early 2020, we implemented an automated SOFA score calculator that tracked the development of organ failure among all adult patients across 3 hospitals. In this study, we aim to describe the frequency and location of organ failure as defined by the SOFA score and explore the associations between burden of organ failure, length of stay (LOS) in the hospital, and mortality for adult inpatients before and during the COVID-19 pandemic.

Study Design and Population

We conducted a retrospective cohort study of adult patients admitted to 3 hospitals within the Montefiore Health System in Bronx, New York. The cohort consisted of admissions of adult patients (age ≥18 years) to Montefiore Moses, Jack D. Weiler, and Wakefield Hospitals from February 1, 2020, through May 31, 2020. We excluded 50 admissions that were missing electronic data, and all admissions for patients with multiple hospitalizations were included. The admission date was used to stratify the cohort into 2 time periods. Admissions occurring before March 17, 2020—the date of the first confirmed COVID-19 case—were labeled prepandemic, and admissions that occurred on or after that date were labeled pandemic. The pandemic cohort was further stratified by SARS-CoV-2 test result into 2 groups: SARS-CoV-2–positive patients and non–SARS-CoV-2 patients. In-house reverse transcriptase polymerase chain reaction testing for SARS-CoV-2 was widely available starting March 17, 2020. Per protocol, all patients with any possible exposure, fever, respiratory or gastrointestinal symptoms, or pulmonary infiltrates were tested for SARS-CoV-2. All study hospitals share an integrated electronic health record system and comprehensive data warehouse. The study protocol was reviewed and approved by the Institutional Review Board at Albert Einstein College of Medicine. Informed consent was waived. This study followed the guidelines for Strengthening the Reporting of Observational Studies in Epidemiology.11 

Data Collection

Clinical data were obtained from Montefiore’s Enterprise Data Warehouse, an SQL database containing clinical and administrative data for all patients at the study hospitals. Baseline demographics, laboratory data, hospital interventions/assessments, and vital signs were collected (Supplemental Table 1, available online only at ajcconline.org).

Algorithm Development

We implemented the algorithm to compute SOFA scores by using a Python package (Supplemental Table 2, available online only).12  Organ systems missing data at baseline were assumed to have no preexisting dysfunction and were assigned 0 points.13  As in prior studies, the SOFA score was calculated without the neurologic component because of the sparsity of Glasgow Coma Scale data captured outside the ICUs and the difficulties of accurately scoring neurologic dysfunction for ICU patients who were sedated.14-16 

The SOFA respiratory component is the ratio of the arterial partial pressure of oxygen (Pao2) to the fraction of inspired oxygen (Fio2). In the absence of arterial blood gas measurement, the SOFA respiratory component was imputed from the oxygen saturation as measured by pulse oximetry (Spo2) and Fio2 values for patients with Spo2 no greater than 98%.17,18  For patients who were missing an arterial blood gas value for more than 24 hours and had no Spo2 measurements less than 98%, imputation was not performed, and the respiratory score was assigned a value of 0. The SOFA renal component was computed from creatinine alone because for patients outside the ICU, the quality of the urine output data was poor.

Admission SOFA scores were calculated 6 hours after hospital admission by using all available data from the previous 24 hours. Scores were recalculated every 2 hours by using the most recent 24 hours of clinical data. Components that were missing a score at baseline were assigned a value of 0; otherwise, the last observation for a component was used until a new value was available. Algorithm accuracy was iteratively improved during development by manually validating samples of 10 patients and correcting inconsistencies with the official SOFA algorithm.

Outcome Measures

Organ failure was defined as a SOFA score of at least 3 for a given organ system.3  The primary outcomes were the frequencies of admission organ failure and hospital-onset organ failure. An admission organ failure was defined as an organ system with a failing score at the time of admission. Hospital-onset organ failure was defined as an organ system that did not fail at the time of admission but did fail later during the hospitalization. Secondary outcomes were multiorgan failure, composite SOFA score, maximum SOFA score, and patient location at the onset of organ failure. Multiorgan failure was defined as 2 or more organs failing concurrently at any time during the hospitalization. Composite SOFA scores were computed at 2-hour intervals by summing scores for each of the 5 organ systems. The maximum SOFA score was the maximum value of the composite score, and the mean SOFA score was the average of all composite SOFA scores during hospitalization. Patient location was labeled ICU when the patient was assigned to a bed in an established ICU or an active ICU expansion unit.

Statistical Analysis

Descriptive statistics were used to describe clinical and demographic characteristics as well as summary measures of organ failure. Univariate analysis was performed to compare descriptive statistics and frequencies of organ failure for admissions before and during the pandemic. The χ2 test was used to test for statistical significance for categorical variables, and the t test with equal variances or the Mann Whitney U test was used to test for statistical significance for continuous variables. Spearman rank correlation (ρ) was used to measure the strength of association between continuous variables. All statistical tests were 2-sided, and a significance level of .05 was used. Results are presented as mean (SD) except when stated otherwise. Data analysis and statistical calculations were performed by using SciPy v1.6.1 at the Montefiore Health System.

The primary outcomes were the frequencies of admission organ failure and hospital-onset organ failure.

Patient Population

We studied 20 704 admissions for 17 746 unique patients; the number of hospital days for all admissions combined was 122 336. There were 9441 prepandemic admissions and 11 263 pandemic admissions. Of the 9441 prepandemic admissions, 117 admissions (1.2%) were of patients who tested positive after the test became available in house. Of the 11 263 pandemic admissions, 5552 (49.3%) tested positive for SARS-CoV-2 (Figure 1). In general, although SARS-CoV-2–positive patients were sicker and had worse outcomes than non–SARS-CoV-2 patients, the non-SARS-CoV-2 patients had higher severity of illness than did prepandemic patients. Compared with the prepandemic group, the non–SARS-CoV-2 group was younger, received less respiratory support, experienced more ICU admissions, had shorter LOS, and had higher hospital mortality (Table 1). Among patients admitted to an ICU, non–SARS-CoV-2 patients had lower mortality than prepandemic patients. The SARS-CoV-2–positive group differed significantly from the prepandemic and non–SARS-CoV-2 pandemic groups for all demographic and clinical characteristics. The SARS-CoV-2–positive group showed a 341% increase in multiorgan failure compared with the prepandemic group (16.3% vs 3.7%). The SARS-CoV-2–positive group also showed a 242% increase in use of invasive mechanical ventilation and high-flow nasal cannulas compared with the prepandemic group (30.1% vs 8.8%). Hospital mortality for patients admitted to the ICU was 46.6% in the SARS-CoV-2–positive group, 22.8% in the prepandemic group, and 14.6% in the non–SARS-CoV-2 pandemic group.

Hospital-Wide Organ Function

A total of 1 794 975 unique SOFA scores were computed for the cohort. The distributions of missing data used to compute SOFA scores were similar between the prepandemic and pandemic periods as well as among the 3 patient groups (Supplemental Table 3, available online only). Pandemic patients who were positive for SARS-CoV-2 were admitted with and developed organ failure more often than did non–SARS-CoV-2 patients and prepandemic patients (Table 2). Compared with the non–SARS-CoV-2 and prepandemic patients, SARS-CoV-2–positive patients had a significantly higher SOFA score on admission and a significantly higher maximum SOFA score during hospitalization. The distributions of maximum SOFA scores in the prepandemic and non–SARS-CoV-2 groups were not significantly different. However, compared with prepandemic and non–SARS-CoV-2 patients, a greater proportion of SARS-CoV-2–positive patients experienced SOFA scores of 6 or greater, indicating severe multiorgan failure (Supplemental Figure 1, available online only).

Organ Failure by System

Organ failure for a system was defined as a SOFA score of 3 or greater for that organ system. The pattern of organ failure was different for the SARS-CoV-2–positive patients than it was for the other 2 groups, both for organ failure at admission and for organ failure occurring during the hospitalization (Table 2). At admission, renal failure was the most common type of organ failure in all 3 groups. The SARS-CoV-2–positive group showed a 94% increase in renal failure compared with the prepandemic group (12.8% vs 6.6%). The second most common type of organ failure at admission was respiratory failure, and the SARS-CoV-2–positive group showed a 231% increase in respiratory failure compared with the prepandemic group (5.3% vs 1.6%). Compared with the prepandemic group, the SARS-CoV-2–positive group showed a 157% increase in cardiovascular failure (1.8% vs 0.7%) and a 57% increase in liver failure (1.1% vs 0.7%) at admission; however, the SARS-CoV-2–positive group showed a 33% decrease in coagulation failure rate at admission (0.6% vs 0.9%).

The pattern of hospital-onset organ failure for the SARS-CoV-2–positive group was also different from the patterns of the other groups. Among the types of hospital-onset organ failure, respiratory was the most common. The SARS-CoV-2–positive group showed a 289% increase in respiratory failure compared with the prepandemic group (18.3% vs 4.7%). The SARS-CoV-2–positive group showed a 325% increase in cardiovascular failure (11.9% vs 2.8%) and a 315% increase in renal failure (11.2% vs 2.7%) compared with the prepandemic group. Patterns similar to these were also seen when the SARS-CoV-2–positive group was compared with the non–SARS-CoV-2 group. No significant differences were found in the frequencies of coagulation or liver failure between the SARS-CoV-2–positive and prepandemic groups. For each of the 5 organ systems, the frequency of organ failure did not significantly differ between the non–SARS-CoV-2 and prepandemic groups.

Hospital Location During Organ Failure Events

More than 65% of new coagulation, liver, renal, and respiratory failures before the pandemic developed outside of an ICU (Supplemental Table 4, available online only). The incidence of cardiovascular, coagulation, liver, renal, and respiratory failure outside ICUs did not significantly differ between non–SARS-CoV-2 patients and prepandemic patients. Compared with the prepandemic group, the SARS-CoV-2–positive group experienced significantly more acute respiratory failure and less coagulation, liver, and renal failure outside ICUs.

Hospital Mortality and Length of Stay

Both before and during the pandemic, higher admission and maximum SOFA scores correlated with higher mortality rates (Figure 2). However, compared with the prepandemic and non–SARS-CoV-2 groups, the SARS-CoV-2–positive group had higher mortality for the same admission and maximum SOFA scores. When mortality is assessed relative to maximum SOFA score in each organ system before and during the pandemic, mortality was significantly higher for SARS-CoV-2 positive patients than for prepandemic and non–SARS-CoV-2 patients for each SOFA score (Supplemental Figure 2, available online only). Cardiovascular failure was associated with the highest mortality for all 3 groups of patients, and a score of 4 was associated with a mortality rate of greater than 60%. In SARS-CoV-2– positive patients, coagulation, liver, renal, and respiratory scores of 4 were associated with mortality rates of 52%, 74%, 48%, and 72%, respectively.

Findings suggest that SOFA score was not an appropriate choice for a crisis standard under pandemic surge conditions.

Higher maximum SOFA scores correlated with longer hospital LOS for survivors (ρ = 0.45, P < .001). SARS-CoV-2– positive patients had longer LOS than their non–SARS-CoV-2 and prepandemic counterparts (Figure 3). This difference was most pronounced for maximum SOFA scores of 10 to 11, for which the median (IQR) LOS was 31 (19-45) days for SARS-CoV-2–positive patients but 15 (9-22) days for the prepandemic patients and 15 (10-25) days for non–SARS-CoV-2 patients.

Sensitivity Analysis

We performed a sensitivity analysis by excluding 2958 readmissions and thus limited the analysis to first admissions during the study period. We also performed sensitivity analysis by defining organ failure as a SOFA score greater than or equal to 2 and a SOFA score equal to 4 for a given organ system. The results show the same general trends in the frequency and location of organ failure and the associations between burden of organ failure, mortality, and LOS (Supplemental Tables 5 and 6, Supplemental Figures 3, 4, and 5, available online only).

In our retrospective cohort of adults admitted to large tertiary care centers across Bronx, New York, before and during the SARS-CoV-2 pandemic, we described the frequency and location of organ failure as defined by SOFA score and explored the associations between burden of organ failure, mortality, and hospital LOS. Renal failure was the most common organ failure on hospital admission among SARS-CoV-2–positive patients. However, respiratory failure was the most common hospital-onset organ failure and occurred nearly 3 times more often in SARS-CoV-2–positive patients than in prepandemic patients. Most hospital-onset organ failure in prepandemic and non–SARS-CoV-2 patients and more than 80% of hospital-onset respiratory failure in SARS-CoV-2 positive patients occurred outside ICUs. As expected, we validated the correlation of SOFA score with mortality and LOS, even when the neurologic component is omitted.2-4,12  SARS-CoV-2–positive patients experienced greater rates and severity of multi-organ failure, higher mortality, and longer LOS than did prepandemic and non–SARS-CoV-2 patients for the same maximum SOFA scores. Our study demonstrates that under surge conditions, SOFA scores led to underestimates of morbidity and mortality in SARS-CoV-2– positive patients compared with non–SARS-CoV-2 and prepandemic patients. This finding suggests that SOFA score was not an appropriate choice for a crisis standard under pandemic surge conditions.19-21 

This study advanced the field by demonstrating the feasibility of prospectively calculating SOFA scores in near-real time for the entire hospitalization period for all inpatient adults instead of isolating computation to the emergency department and ICU.1,22-25  Most hospital-onset organ failure occurred outside of the emergency department and ICU both before and during the pandemic. This finding highlights the need for critical care delivery outside of ICUs irrespective of pandemic surge conditions. Early identification and intervention for worsening organ function before ICU admission should become a priority for acute care delivery and prevention. Depending on the distribution of organ failure and resource availability of a hospital, this information can be used in prediction tools that identify patients at risk of experiencing worsening organ function with the goal of improving outcomes by nudging physicians to intervene earlier.26-29 

Because of the strong connection between SOFA scores and LOS, computing SOFA scores for all hospitalized patients can help with operational enhancements in the ICU. Leaders can use this information to forecast the need for critical care and organ support resources in times of crisis such as COVID-19 pandemic surges, when many health care systems had to increase the number of ICU beds, ventilators, and dialysis services without a clear understanding of how much they needed to augment capacity.30-32  However, we suggest using SOFA only for forecasting; caution should be taken if applying SOFA as a crisis standard to allocate resources, as it led to underestimates of morbidity and mortality in SARS-CoV-2–positive patients under surge conditions.

Respiratory failure developed more often after admission and was the most common hospital-onset organ failure for SARS-CoV-2–positive patients.

We defined organ failure as a SOFA score of 3 or greater for a given organ system, and that level of severity corresponds to need for vasopressors, respiratory support, or other high-level support that is usually provided in the ICU (eg, for severe renal failure). Organ failure among SARS-CoV-2–positive patients occurred at double the rate of failure among prepandemic and non–SARS-CoV-2 pandemic patients; the higher rate of organ failure among SARS-CoV-2–positive patients exerted a significant strain on hospital systems and staff outside ICUs and may have contributed to the higher mortality rates seen among SARS-CoV-2–positive patients in heavily affected areas during the pandemic.33  Despite the frequent association of SARS-CoV-2 with respiratory failure and acute respiratory distress syndrome, we found that the most common type of organ failure at admission for SARS-CoV-2–positive patients was renal failure. This finding agrees with the results of other studies that report acute kidney injury was prevalent outside ICUs before the COVID-19 pandemic began and among patients with COVID-19: more than 20% of hospitalized patients and more than 50% of patients in the ICU experienced acute kidney injury.34,35  Acute kidney injury in patients with COVID-19 is likely to be multifactorial and have various pathogenic mechanisms. Cardiovascular comorbidity and predisposing factors such as sepsis, hypovolemia, and nephrotoxins can contribute to acute kidney injury. Furthermore, SARS-CoV-2 can affect the kidney either indirectly through endothelial dysfunction, coagulopathy, and complement activation or directly through viral tropism.34,36,37 

Respiratory failure developed more often after admission and was the most common hospital-onset organ failure for SARS-CoV-2–positive patients. Except at the upper limit of admission and maximum SOFA scores, SARS-CoV-2–positive patients experienced a larger burden of multiorgan failure with greater hospital mortality for the same burden of organ failure than did prepandemic and non–SARS-CoV-2 patients.

For non–SARS-CoV-2 patients during the pandemic, hospital admissions decreased but hospital mortality increased. Higher admission SOFA scores suggest that, to minimize their risk of SARS-CoV-2 infection, many patients without SARS-CoV-2 avoided the hospital during the pandemic unless they were very sick.38 

Limitations of near-real time SOFA calculation include data availability, which may be worse during a pandemic and thus could bias the results toward less organ failure. Even so, we saw more organ failure with greater severity during the pandemic. We were unable to automatically identify patients with chronic organ failure such as end-stage liver or renal disease because prehospitalization creatinine and bilirubin data were not always available. However, we were able to examine acute organ failure by focusing on hospital-onset organ failure that was not present at admission. Although the data used to compute SOFA scores are captured in all electronic health record systems, we recognize that computing SOFA scores in near-real time does require technical expertise that may be available only at institutions with dedicated informatics teams. Routine testing was not available immediately during the pandemic, which may have caused some patients to be misclassified with respect to SARS-CoV-2 status. However, testing became widely available 1 week after the cutoff, so the extent of possible misclassification is limited. Finally, the study was limited to 3 hospitals in the Bronx that were among the most severely affected areas in the country at the time of this study. Results may be less severe in areas with lower rates of SARS-CoV-2 cases, but our results are more informative for developing crisis standards of care by understanding what may happen under surge conditions from a natural disaster or future pandemic that strains hospital systems.

The study has several strengths. First, the cohort is from a period with a high frequency of hospital-onset organ failure due to the rapid and poignant onset of the SARS-CoV-2 pandemic in the catchment area. To our knowledge, this study is the largest one that captures the shift in the burden of organ failure across multiple hospitals from prepandemic to pandemic surge conditions. Complete hospitalization data for the cohort permitted us to compute SOFA scores from the time of admission through the time of discharge irrespective of the patient’s location in the hospital; thus, we were able to extend SOFA outside ICUs to investigate the frequency and location of new organ failure throughout the study hospitals.

Before and during the COVID-19 pandemic, respiratory and renal systems were the most common organ systems to fail, and most hospital-onset organ failure commenced outside the ICUs. The burden of multiorgan failure increased markedly during pandemic surge conditions, leading to increases in ICU admissions, invasive mechanical ventilation, hospital LOS, and mortality. SOFA scores led to underestimates of mortality in SARS-CoV-2–positive patients under pandemic surge conditions and should be applied with caution to crisis standards of care.

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Footnotes

 

FINANCIAL DISCLOSURES

The research described was supported by National Institutes of Health (NIH)/National Center for Advancing Translational Science Einstein-Montefiore CTSA grant number UL1 TR002556, Agency for Healthcare Research and Quality grant number R18HS026188, and NIH/National Heart, Lung, and Blood Institute grant number UH3HL125119. James Brogan is supported in part by an Alpha Omega Alpha Carolyn L. Kuckein Student Research Fellowship.

 

SEE ALSO

For more about scales used to assess organ failure, visit the Critical Care Nurse website, www.ccnonline.org, and read the article by Pellathy et al, “Intensive Care Unit Scoring Systems” (August 2021).

 

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