key: cord-0742626-ub49chme
authors: Charytan, David M.; Parnia, Sam; Khatri, Minesh; Petrilli, Christopher M.; Jones, Simon; Benstein, Judith; Horwitz, Leora I.
title: Decreasing Incidence of AKI in Patients with COVID-19 critical illness in New York City
date: 2021-02-04
journal: Kidney Int Rep
DOI: 10.1016/j.ekir.2021.01.036
sha: 56bb30a37e1bbe0264afe8b6037f91117857b0bb
doc_id: 742626
cord_uid: ub49chme

INTRODUCTION: Reports from the United States suggest that acute kidney injury (AKI) frequently complicates COVID-19, but understanding of AKI risks and outcomes is incomplete. Additionally, whether kidney outcomes have evolved during the course of the pandemic is unknown. METHODS: We used electronic records to identify COVID-19 patients with and without AKI admitted to 3 New York Hospitals between March 2 and August 25, 2020. Outcomes included AKI overall and according to admission week, AKI stage, the requirement for new renal replacement therapy (RRT), mortality and recovery of kidney function. Logistic regression was utilized to assess associations of patient characteristics and outcomes. RESULTS: Out of 4732 admissions 1386 (29.3%) patients had AKI. Among those with AKI, 717 (51.7%) had Stage 1, 132 (9.5%) Stage 2, 537 (38.7%) stage 3, and 237 (17.1%) required RRT initiation. In March 536/1648 (32.5%) of patients developed AKI compared with 15/87 (17.2%) in August (P<0.001 for monthly trend) whereas RRT initiation was required in 6.9% and 0% of admission, in March and August respectively. Mortality was higher with than without AKI (51.6% vs 8.6%) and was 71.9% in individuals requiring RRT. However, most patients with AKI who survived hospitalization (77%) recovered to within 0.3 mg/dL of baseline creatinine. Among those surviving to discharge, 62% discontinued RRT. CONCLUSIONS: AKI impacts a high proportion of admitted COVID-19 patients and is associated with high mortality, particularly when RRT is required. AKI incidence appears to be decreasing over time and kidney function frequently recovers in those who survive.

Reports from the United States suggest that acute kidney injury (AKI) frequently complicates COVID-19, but understanding of AKI risks and outcomes is incomplete. Additionally, whether kidney outcomes have evolved during the course of the pandemic is unknown.

We used electronic records to identify COVID-19 patients with and without AKI admitted to 3

New York Hospitals between March 2 and August 25, 2020. Outcomes included AKI overall and according to admission week, AKI stage, the requirement for new renal replacement therapy (RRT), mortality and recovery of kidney function. Logistic regression was utilized to assess associations of patient characteristics and outcomes.

Out of 4732 admissions 1386 (29.3%) patients had AKI. Among those with AKI, 717 (51.7%) had Stage 1, 132 (9.5%) Stage 2, 537 (38.7%) stage 3, and 237 (17.1%) required RRT initiation. In March 536/1648 (32.5%) of patients developed AKI compared with 15/87 (17.2%) in August (P<0.001 for monthly trend) whereas RRT initiation was required in 6.9% and 0% of admission, in March and August respectively. Mortality was higher with than without AKI (51.6% vs 8.6%) and was 71.9% in individuals requiring RRT. However, most patients with AKI who survived hospitalization (77%) recovered to within 0.3 mg/dL of baseline creatinine. Among those surviving to discharge, 62% discontinued RRT.

J o u r n a l P r e -p r o o f Introduction SARS-CoV-2 virus is a highly infectious 1 and virulent pathogen. To our knowledge, the first peer-reviewed report focusing on AKI in COVID-19 included 116 confirmed cases from a single center in Wuhan, China. Among these patients, none of the 111 patients without chronic kidney disease (CKD) at baseline developed AKI. 3 A subsequent report including 333 patients with COVID-19 at a single hospital in China found that 75% of patients had abnormal urinalysis, 66% had proteinuria, and up to 7.5% of patients had AKI, with a plurality having stage 1 AKI. 4 A second manuscript from a tertiary care center in Wuhan reported similar findings among 701 patients, finding that proteinuria and hematuria were frequently present on admission and that 5.1% of patients experienced AKI. 5 Although these reports suggest that AKI is an infrequent component of illness, more recent reports from the United States suggest a much higher AKI incidence. In a report from the largest health system in New York, >30% of 5449 patients admitted with COVID-19 experienced AKI and 4.4% of patients required RRT. 6 Several other publications have reported even higher rates, including a manuscript reporting on 3235 patients hospitalized in New York (AKI incidence 46%, 8 .6% of all patients requiring RRT), 7 as well as smaller case series including a report from Philadelphia noting a 49% incidence of AKI with roughly 8% of AKI patients requiring RRT, 8 and a report from New Jersey finding RRT was required in 21% of minority patients. 9 These data establish AKI as a critical and frequent complication of COVID-19 disease, at least in the United States. However, it is unknown whether the rapid evolution in treatments, hospital practices, and public health measures during the initial months of the COVID pandemic has been associated with changes in the incidence of AKI. Additionally, information on the risk factors for development of AKI, the prognosis of COVD-19 associated AKI, and outcomes of RRT remain incomplete. We undertook this effort to better describe the characteristics and J o u r n a l P r e -p r o o f prognosis of COVID-19 AKI as well as temporal changes in AKI incidence in a multi-center cohort in the United States.

We included patients admitted to 3 NYU Langone Health Hospitals: Tisch Hospital in Manhattan, NYU Langone Hospital -Brooklyn in Brooklyn, and NYU Winthrop on Long Island.

The institutions span a range of models including an urban quaternary care facility, a suburban referral center, and an urban safety net institution. The cohort included all patients admitted for treatment of COVID-19 between March 1, 2020 and August 25, 2020. All patients were required to have a documented test positive for SARS-CoV-2 by real-time reverse-transcriptasepolymerase-chain-reaction (RT-PCR) assay of nasopharyngeal or oropharyngeal swab specimens during the admission or within the 2 weeks prior to the admission date. For patients admitted more than once (N=196), we included all hospitalizations. Patients with end stage renal disease on dialysis at the time of admission were excluded based on the presence of codes for "ESRD present on admission," a history of dialysis on a prior admission combined with dialysis during the index admission, and manual review of cases receiving RRT on the day of admission.

Follow-up was available through August 25, 2020. This study was approved with a waiver of informed consent and a Health Insurance Portability and Accountability Act waiver by the NYU Grossman School of Medicine Institutional Review Board (i20-00485).

J o u r n a l P r e -p r o o f We used the electronic health record (EHR, Epic Systems, Verona, WI), which contains information on inpatient and outpatient visits, to extract data on demographics, comorbidities, smoking, vital signs, comorbidities, laboratory values, and use of extracorporeal oxygenation, high flow oxygen, and mechanical ventillation. All data in the EHR was utilized to extract information including problem lists, medical history section or encounter diagnoses from prior inpatient and outpatient visits.

Our primary outcomes included AKI, the need for new RRT during the index hospitalization, and survival to discharge during the index hospitalization. Acute kidney injury was defined using the creatinine criteria as defined by Acute Kidney Injury Network (AKIN) criteria and staged accordingly: 10 Stage 1-increase of ≥0.3 mg/dL or to more than 1.5-to 2 times baseline; Stage 2-increase > 2-to ≤3 times the baseline value; Stage 3-increase >3fold from baseline or rise to ≥4.0 mg/dl with an acute increase of at least 0.5 mg/dl, or new initiation of RRT. Because urine output is inconsistently recorded for patients not admitted to the intensive care unit, we did not utilize the AKIN urine output criteria to define AKI. Where available, the most recent outpatient creatinine values within 6 months of admission were utilized to define the baseline for the definition of AKI. When no outpatient value was available within this time frame, we used the admission creatinine. A sensitivity analysis defined AKI using the minimum creatinine (while not on dialysis) during the hospitalization as the baseline for individuals without a known baseline value. We did not require that AKI-qualifying changes in creatinine be documented to occur within 7 days because the majority (76.3%) of patients with outpatient creatinine values had them drawn >7 days prior to admission, the median length of stay was 6 days, and because the first day of AKI occurred at median of 3 days and 2 days in those with and without a need for RRT. Individuals with the combination of only a single J o u r n a l P r e -p r o o f inpatient creatinine measurement, no available pre-admission creatinine, and discharge on hospital day 0 or 1 were categorized as not having acute kidney injury on the presumption that individuals with this combination were unlikely to have clinically significant kidney injury.

RRT was extracted directly from the medical record. Renal recovery was defined as a decrease in creatinine to ≤0.3 mg/dL above baseline together with the absence of ongoing RRT at any time prior to discharge. Additionally, we examined an outcome of RRT discontinuation.

For this outcome, discontinuation due to futility or change in goals of care was not considered to represent discontinuation.

The following variables were extracted from the EHR: age at admission, sex, selfreported race/ethnicity, smoking status, history of hypertension, hyperlipidemia, coronary artery disease, heart failure, pulmonary disease (defined by chronic obstructive pulmonary disease or asthma), malignancy (excluding non-metastatic non-melanoma skin cancer), diabetes, CKD, and obesity (defined by most recent body mass index). We also obtained vital signs and laboratory values at admission.

Baseline variables are reported according the distribution as median (interquartile range, IQR) for continuous variables and n (%) for categorical variables, stratified by AKI stage. Binary comparisons between groups were made using chi-squared tests. We tested for a differential risk of AKI and AKI requiring RRT by calendar week of admission utilizing the Cochran-Armitage test for trend. Multivariable logistic regression models were constructed to analyze risk of J o u r n a l P r e -p r o o f developing AKI and the risk of in-hospital death with AKI compared to no AKI. Proportions of patients with each outcome according to ICU admission in those with or without AKI or with or without a new dialysis requirement were reported as n (%).

In addition, an exploratory model was utilized to analyze associations of baseline factors with in-hospital survival after starting RRT. Variables were included based on a priori clinical considerations after testing for collinearity and ensuring variance inflation factor (VIF) was>2. 11 In addition, the association of calendar week of admission with the risk of AKI was analyzed by including calendar week as a variable in final incident AKI model. Given a smaller sample size of patients receiving RRT, the model for death among patients receiving RRT included only demographic and comorbidities. Multicolllinearity was assessed using the determinant of correlation matrix using the mctest library in R. 12 All statistical analyses were conducted with R, version 3.6.3. Two-sided p values <0.05 were considered significant. No adjustments were made for multiple comparisons.

Between March 1, 2020 and August 25, 2020 we identified 4732 patients admitted with There were 1386 (29.3%) patients with AKI overall. Among those with AKI, 717 (51.7%) had Stage 1, 132 (9.5%) Stage 2, and 537 (38.7%) stage 3. New RRT was required in 237 J o u r n a l P r e -p r o o f (17.1%) of those with AKI). Among patients admitted to the ICU (N=1056), AKI incidence was even higher with 788 (74.6%) of patients having AKI and 213 (20.2%) requiring new RRT (Table   3 ). Results were similar in analyses using the nadir creatinine with an overall AKI incidence of 30.7% with RRT required in 16.3% of all AKI.

Older age, diabetes, hypertension and congestive heart failure were more common among those with AKI than those without AKI during admission (Table 1 ). There was a higher incidence of severe hypoxia (oxygen saturation <88%) at presentation in those with AKI.

Admission laboratory values ( Table 2) were substantially different in individuals with AKI, who had higher D-Dimer, IL-6, and C reactive protein levels. Among those with urinalyses, dipstick proteinuria was present in 71.1%%, hematuria in 49.5% and leukocyturia in 21.8% of patients with AKI.

Differences in oxygen saturation were more prominent in those who developed severe AKI requiring RRT and in those who developed higher stages of AKI (Supplementary Table 1 ).

In particular, hematuria and proteinuria were more frequent in those with higher AKI severity (p<0.001). Similarly, D-Dimer, IL-6 and CRP concentrations were higher in those with more severe AKI (p<0.001).

As shown in Table 3, Supplementary Table 2 admissions required RRT for the next 6 weeks. Subsequently, the weekly incidence of AKI requiring RRT was ≤3.6% with the exception of week 20 (4.4%) and week 29 (5.9%). . Trends were qualitatively similar in analyses using the alternative definition of AKI with peak incidence of 57.1% in the week of March 2-8 (N=4) and 40% (N=18) the week of March 9-15 and lower rates thereafter.

As shown in Figure 2 , the early decline in AKI paralleled an increase in the use of tocilizumab and corticosteroids through week 15 of 2020. However, the incidence of AKI continued to fall thereafter, despite reduced usage of these therapies. The association of admission week with risk of AKI was robust and remained significant in models adjusted for clinical risk factors and COVID-19 presentation (Table 4 ). To understand temporal trends for AKI, we analyzed patient characteristics according to the time of admission. CRP scores, age, and the proportion of patients with clinically significant hypoxia, at admission were significantly lower during later weeks of the pandemic (Table 5) .

Renal recovery back to within ≤0.3 mg/dL above baseline prior to discharge was present 

Patients with AKI were more likely to be admitted to an ICU (56.9% vs8.0% p<0.001), undergo mechanical ventilation (53.6% vs 4.0% p<0.001) or undergo extracorporeal membrane oxygenation (ECMO) (3.3% vs 0.1%, p<0.001) during admission than those without ( Table 1,   Table 6 ). Among individuals with an outcome (death or discharge), mortality was higher with than without AKI (51.6% vs 8.6%) and was 71.9% in individuals requiring RRT. Using the nadir creatinine-based definition, mortality was 50.1% and 8.4% in those with and without AKI.

Additionally, 21 patients were still admitted at the time we locked the data. Mortality was higher for individuals with AKI or AKI requiring RRT both in the setting of ICU admission and in those not admitted to an ICU during hospitalization. Patients admitted to the ICU and requiring RRT had particularly poor outcomes. Out of 211 such patients with an outcome at the time of data lock, only 50 (23.7%) patients survived to discharge. By contrast, 452 of 834 (54.2%) ICU patients not requiring RRT with outcomes survived to discharge (Table 6 . Time to event analyses of survival are provided in Supplemental Table 3 and Supplemental Figure 1 ). When analyzed according to maximal AKI stage, mortality increased across AKI stages (Supplemental Table 4 ). Following adjustment for demographics, labs and comorbid conditions the adjusted overall risk for death was more than 10-fold higher with than without AKI OR (10.22, 95% CI: Table 5 ). In contrast, week of admission was not consistently associated with mortality. In an exploratory analysis among individuals requiring RRT, we did not identify significant associations between age, race, or ethnicity. History of cancer was associated with increased mortality following RRT initiation whereas baseline CKD, coronary disease and hypertension were associated with better survival. In addition, obesity was strongly J o u r n a l P r e -p r o o f associated with the risk of death-OR 3.93 (95% CI: 1.53-10.47) for body mass index for 30-<40 vs. <25 kg/m 2 and 9.10, (95% CI: 2.36-40.68) for body mass index ≥40 vs. <25. kg/m 2 (Supplemental Table 6 ).

In adjusted analyses (Table 4) , age, male sex, baseline CKD, diabetes, heart failure, hypertension, body mass index >40kg/m 2 , and admit week were independently associated with the risk of AKI. Presenting systolic blood pressure was not independently associated with AKI risk, but AKI risk was higher in those with lower oxygen saturation and higher D-Dimer at presentation ( Figure 3 ).

We analyzed data from 4,7322 patients admitted with COVID- 19 Additionally, AKI was associated with a marked increase in the risk of in-hospital death, especially in ICU patients requiring RRT, in whom mortality exceeded 76%. Lastly, despite a J o u r n a l P r e -p r o o f high incidence of AKI, overall, we observed a marked reduction in AKI incidence over time with a rate that was 1/3 rd lower during the last 7-weeks compared with the first half of the surge.

Early reports of COVID-19 illness from China suggested that the incidence of acute kidney injury was low, ranging from <1-7.5%. 2, 4, 5, 13 A recent meta-analysis suggested the prevalence of AKI was 17%, 14 and recent reports from the United States have consistently demonstrated even higher rates of AKI. [6] [7] [8] [9] Consistent with these reports, we observed a markedly higher incidence of overall AKI among patients admitted with COVID-19 in New York compared with reports from China, and identified a rate of severe AKI requiring RRT comparable to the highest incidence of AKI in the previous reports and higher than those seen in earlier reports from China. 4 Reasons for the stark differences in the incidence of AKI in the United States and China are uncertain. Potential explanations include differences in threshold for admission between China and the United States, differences in the race and ethnicity and underlying genetic susceptibility to COVID-related AKI in patients, as well as socio-economic conditions, differences in age, underlying comorbidities such as diabetes and pre-existing CKD, or the treatments provided for patients upon presentation. The lack of standardization in the definitions used to define AKI, the absence of baseline creatinine measurements, varying methods used to define the baseline creatinine, and the lack of data on urine output in most studies are also likely to contribute to the observed differences in incidence across published studies. In theory, differences in the pathogenesis of the most prevalent viral strains 15 between New York and China could also underlie differences in kidney injury outcomes, although there is no evidence supporting this to date. Finally, differences in RRT rates may also reflect differences in practice patterns and utilization of RRT in patients with critical illness between countries. Studies designed to assess the causal roles of risk factors, treatments, and viral strains, as well as the role of practice patterns in COVID-19 AKI are needed to better understand these phenomena.

In addition, to further refining estimates of AKI, our study extends upon the earlier studies from the United States and China in demonstrating significant temporal changes in the AKI incidence during the course of the New York surge. To our knowledge, a decrease in the incidence of COVID-related AKI over time has not been previously reported. If the decrease in AKI rate over time is generalizable, it would have important implications regarding resource allocations needed to prepare for future surges. Additionally, given the high mortality incidence in patients with COVID-associated AKI, a decrease in AKI incidence would be expected to be associated with concomitant reductions in mortality among hospitalized COVID-19 patients.

Reasons for the decreased incidence require further investigation. The decrease in AKI did not have a clear relationship to the use of steroids or tocilizumab. However, it may reflect other evolutions in clinical care over the course of the pandemic including broader use of prophylactic anti-coagulation, widespread use of proning, differential management of volume status, changes in thresholds for the use of mechanical ventilation, and changes in the availability of ICU beds. Indeed, the decrease in admission rates later in the surge is likely to have improved staffing ratios and allowed for more careful assessment of volume status.

Additionally, age and CRP levels were lower in patients admitted during later months of the pandemic whereas the proportion of patients with clinically significant hypoxia was lower. These findings suggest that patients admitted later had lower degrees of inflammation and less severe pulmonary involvement possibly reflecting lower degrees of viral exposure in patients admitted following the institution of lockdowns, widespread social distancing, and mask-wearing. The change in AKI incidence (and severity of illness/inflammation at admission) may also be partly attributable to changes in the age distribution of admitted patients. However, in multivariable models the change in AKI incidence across time was independent of age and degree of hypoxia at admission suggesting that other factors such as the quality of care are likely to be important, as well. Further investigation of the underlying explanation is warranted.

Our study also provides detailed information on the AKI development and prognosis. As in other forms of AKI, 16 pre-existing CKD, heart failure and diabetes were associated as well as older age were associated with the development of AKI. This is consistent with the possibility that patients with COVID-19 suffer from similar types of kidney injury, primarily acute tubular necrosis, as individuals with other forms of critical illness and lung-kidney cross-talk. 17 Indeed, diffuse proximal tubular injury and frank necrosis was frequently identified in renal specimen from a recently reported post-mortem series. 18 However, the high incidence of proteinuria, hematuria, leukocyturia, and the strong independent association of higher D-dimer concentration with AKI risk are consistent with important roles for additional mechanisms of kidney injury in COVID-19. The elevated D-dimer levels suggest an important role for thrombosis and microangiopathy in AKI and are consistent with observations of megakarocytosis and thrombosis observed pathologically. 18, 19 Conversely, the urinary findings suggest that collapsing glomerulopathy, 20-22 the presence of viral particles in tubular cells 18 , pigmented casts, and capillary obstruction by erythrocytes aggregates, which were also seen in the aforementioned series, may underlie an important proportion of COVID-19 AKI.

As expected, individuals with AKI had worse survival compared to patients without AKI even after adjusting for comorbidities and severity of presentation. Our data suggests that COVID-19 AKI has a particularly poor prognosis compared to other forms of AKI-mortality for admitted patients with AKI was 38% among non-ICU patients and 61% among those admitted to an ICU-comparable to the mortality generally reported for pre-COVID cohorts of ICU patients requiring RRT. 23 Furthermore, the combination of ICU admission and requirement for RRT was fatal in nearly three quarters of cases suggesting that RRT may not change survival in an important proportion of cases. Identifying individuals unlikely to benefit from RRT may be important given concerns that have been raised about the ability of health systems to provide RRT to all COVID-19 AKI patients, 24 J o u r n a l P r e -p r o o f Although mortality was high in individuals with AKI in the setting of COVID-19, recovery of renal function was relatively common among survivors. Recovery to baseline was observed in 80% of patients and RRT was discontinued in 80% of discharged survivors. Data on renal recovery after RRT is sparse. Kidney function recovery amongst survivors was 57% in a preprint manuscript. 7 Discontinuation of RRT amongst survivors was not reported, but approximately 30% of patients requiring RRT had stage ≤2 Stage 2 AKI at the time of discharge or death in this series. Similarly, Gupta et al reported that 28.7% of patients requiring RRT were able to discontinue dialysis. 25 Additionally, our estimates of mortality as well as kidney recovery following AKI in COVID-19 are likely to be more precise than prior reports since the vast majority of individuals in our study (99.6%) had a final disposition compared to prior reports in which ≥20% of patients with AKI were still admitted at the time of data lock, 6, 7 Although our cohort was large and included patients admitted to three hospitals, several limitations should be acknowledged. Baseline creatinine was not available in the majority of patients. Although results were consistent in analyses using a nadir creatinine to define the baseline in those without prior values, we cannot rule out some misclassification. Individuals with no prior baseline creatinine and only a single inpatient measurement who were discharged on hospital day 0 or 1 were classified as no AKI. We believe that individuals with apparent AKI or high severity of illness would be unlikely to be discharged so rapidly and that their elimination would have excluded the least sick individuals and resulted in biased, non-generalizable estimates. We cannot rule out the possibility of misclassification of early AKI in some of these individuals, but qualitative impact on our findings is unlikely. We were unable to assess the underlying causes of AKI or distinguish tubular necrosis from "pre-renal" or other causes of kidney injury, or assess duration of symptoms prior to presentation. Our findings may reflect the unique makeup of included patients and hospitals and should be generalized cautiously.

Whether evolving practice patterns will impact AKI incidence or survival is uncertain, but our findings are best interpreted within the context of a newly-defined disease entity for which J o u r n a l P r e -p r o o f treatments and understanding are rapidly evolving. Lastly, a recent outpatient measurement of serum creatinine was not available in all patients. It is reassuring that results were similar when we used the admission creatinine or nadir creatinine as the baseline, but some misclassification could have occurred.

In summary, among patients admitted with COVID-19 in NY, AKI impacted 31% of all admissions with RRT required in 21% of critically ill patients and was associated with poor survival particularly amongst ICU patients requiring RRT. Kidney injury was transient with independence from RRT and recovery to or near baseline kidney function in the majority of survivors. Lastly, the incidence of COVID-associated AKI appears to be decreasing. Our findings suggest that AKI is an important but potentially preventable complication of COVID-19

and suggest an urgent need to improve understanding of the underlying mechanisms, develop risk-stratification tools, and develop therapies for AKI.

This work was funded in part by the Kenneth C. Griffin Charitable Fund. * Among patients who did not die or were not discharged to hospice **Among patients who did not die or were not discharged to hospice J o u r n a l P r e -p r o o f The N is provided within each row for laboratory tests not done on all patients 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 N=4729. Two patients were not included due to missing data on oxygen saturation and one due to missing information on systolic blood pressure. OR-odds ratio. CI-confidence interval. Data are presented as n (%) or median (25 th , 75 th percentile). SOFA-Sequential Organ Failure Assessment Score. Higher scores indicated greater severity of illness. CRP-C reactive protein. * 

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