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The Prevalence of Acute Kidney Injury in Patients Hospitalized With COVID-19 Infection: A Systematic Review and Meta-analysis

Open AccessPublished:December 08, 2020DOI:https://doi.org/10.1016/j.xkme.2020.11.008

      Rationale & Objective

      Coronavirus disease 2019 (COVID-19) may be associated with high rates of acute kidney injury (AKI) and kidney replacement therapy (KRT), potentially overwhelming health care resources. Our objective was to determine the pooled prevalence of AKI and KRT among hospitalized patients with COVID-19.

      Study Design

      Systematic review and meta-analysis.

      Data Sources

      MEDLINE, Embase, the Cochrane Library, and a registry of preprinted studies, published up to October 14, 2020.

      Study Selection

      Eligible studies reported the prevalence of AKI in hospitalized patients with COVID-19 according to the Kidney Disease: Improving Global Outcomes (KDIGO) definition.

      Data Extraction & Synthesis

      We extracted data on patient characteristics, the proportion of patients developing AKI and commencing KRT, important clinical outcomes (discharge from hospital, ongoing hospitalization, and death), and risk of bias.

      Outcomes & Measures

      We calculated the pooled prevalence of AKI and receipt of KRT along with 95% CIs using a random-effects model. We performed subgroup analysis based on admission to an intensive care unit (ICU).

      Results

      Of 2,711 records reviewed, we included 53 published and 1 preprint study in the analysis, which comprised 30,657 hospitalized patients with COVID-19. Data for AKI were available for 30,639 patients (n = 54 studies), and receipt of KRT, for 27,525 patients (n = 48 studies). The pooled prevalence of AKI was 28% (95% CI, 22%-34%; I2 = 99%), and the pooled prevalence of KRT was 9% (95% CI, 7%-11%; I2 = 97%). The pooled prevalence of AKI among patients admitted to the ICU was 46% (95% CI, 35%-57%; I2 = 99%), and 19% of all ICU patients with COVID-19 (95% CI, 15%-22%; I2 = 88%) commenced KRT.

      Limitations

      There was significant heterogeneity among the included studies, which remained unaccounted for in subgroup analysis.

      Conclusions

      AKI complicated the course of nearly 1 in 3 patients hospitalized with COVID-19. The risk for AKI was higher in critically ill patients, with a substantial number receiving KRT at rates higher than the general ICU population. Because COVID-19 will be a public health threat for the foreseeable future, these estimates should help guide KRT resource planning.

      Graphical abstract

      Index Words

      We conducted a meta-analysis and systematic review to determine how common acute kidney injury (AKI) and kidney replacement therapy are among hospitalized patients with coronavirus disease 2019 (COVID-19) infection. We analyzed 54 studies that reported AKI using KDIGO (Kidney Disease: Improving Global Outcomes) stages, comprising 30,657 hospitalized patients with COVID-19. We found that AKI complicated the course of nearly 1 in 3 (28%) patients hospitalized with COVID-19. The risk for AKI was higher in critically ill patients, with a substantial number receiving kidney replacement therapy at rates higher than the non-critically ill population. Because COVID-19 will be a public health threat for the foreseeable future, these estimates should help guide kidney replacement therapy resource planning.
      Acute kidney injury (AKI) is a common and serious complication of severe illness. It is associated with higher mortality, prolonged hospital stay, and cardiovascular complications.
      • Chertow G.M.
      • Burdick E.
      • Honour M.
      • Bonventre J.V.
      • Bates D.W.
      Acute kidney injury, mortality, length of stay, and costs in hospitalized patients.
      ,
      • Legrand M.
      • Rossignol P.
      Cardiovascular consequences of acute kidney injury.
      In hospitalized patients, AKI is commonly associated with other markers of disease severity such as sepsis,
      • Bagshaw S.M.
      • Uchino S.
      • Bellomo R.
      • et al.
      Septic acute kidney injury in critically ill patients: clinical characteristics and outcomes.
      hypoxemic respiratory failure leading to mechanical ventilation,
      • van den Akker J.P.C.
      • Egal M.
      • Groeneveld A.B.J.
      Invasive mechanical ventilation as a risk factor for acute kidney injury in the critically ill: a systematic review and meta-analysis.
      and hypotension requiring vasopressor support.
      • Saito S.
      • Uchino S.
      • Takinami M.
      • Uezono S.
      • Bellomo R.
      Postoperative blood pressure deficit and acute kidney injury progression in vasopressor-dependent cardiovascular surgery patients.
      Consequently, it is not surprising that AKI is also a common complication of coronavirus disease 2019 (COVID-19) infection, which in its most severe presentation leads to multisystem critical illness. Recent reports suggest that COVID-19 may also affect the kidney by direct virus-mediated injury, cytokine storm, dysregulation of complement, and hypercoagulability.
      • Batlle D.
      • Soler M.J.
      • Sparks M.A.
      • et al.
      Acute kidney injury in COVID-19: emerging evidence of a distinct pathophysiology.
      These mechanisms of injury may explain some of the high rates of AKI that have strained nephrology resources. For example, reports from New York City and New Orleans estimate that 20% to 60% of patients with COVID-19 experienced AKI and most patients in an intensive care unit (ICU) received emergent kidney replacement therapy (KRT).
      • Chan L.
      • Chaudhary K.
      • Saha A.
      • et al.
      Acute kidney injury in hospitalized patients with COVID-19. Pre-print.
      • Hirsch J.S.
      • Ng J.H.
      • Ross D.W.
      • et al.
      Acute kidney injury in patients hospitalized with COVID-19.
      • Goldfarb D.S.
      • Benstein J.A.
      • Zhdanova O.
      • et al.
      Impending shortages of kidney replacement therapy for COVID-19 patients.
      • Mohamed M.M.
      • Lukitsch I.
      • Torres-Ortiz A.E.
      • et al.
      Acute kidney injury associated with coronavirus disease 2019 in urban New Orleans.
      However, other centers, particularly in China, report much lower rates of AKI and KRT in patients hospitalized with COVID-19.
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • et al.
      Clinical characteristics of coronavirus disease 2019 in China.
      ,
      • Huang C.
      • Wang Y.
      • Li X.
      • et al.
      Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China.
      This wide variation could be due to differences in patient populations, ascertainment of AKI, geographic variation in practice patterns, and study characteristics.
      As the COVID-19 pandemic progresses, accurate estimates of AKI associated with COVID-19 will be needed to ensure sufficient KRT resources and that infection control practices are in place to safely care for hospitalized patients. Accordingly, we performed a systematic review and meta-analysis to determine the pooled prevalence of AKI and KRT in patients with COVID-19.

      Methods

      The review was conducted using Meta-analysis of Observational Studies in Epidemiology (MOOSE) guidelines and reported using Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) guidelines.
      • Stroup D.F.
      • Berlin J.A.
      • Morton S.C.
      • et al.
      Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group.
      ,
      • Liberati A.
      • Altman D.G.
      • Tetzlaff J.
      • et al.
      The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration.

      Literature Sources and Search

      With the direction of a health informatics specialist (see Item S1 for search strategy), we searched Ovid MEDLINE (1946 to October 14, 2020), Embase (1946 to October 14, 2020), and the Cochrane central register of controlled trials (2019 to October 14, 2020). We did not apply language restrictions. We reviewed the bibliographies of identified articles to locate further eligible studies. In addition, we searched the nephrology section of medRxiv (a pre-print repository of medical articles available at medrxiv.org), and the COVID-19 topic section of the website of the American Society of Nephrology for additional studies.

      Study Selection

      We included studies that reported the prevalence of AKI among hospitalized patients with COVID-19 according to Kidney Disease: Improving Global Outcomes (KDIGO) criteria.
      Kidney Disease: Improving Global Outcomes (KDIGO) Acute Kidney Injury Work Group
      KDIGO clinical practice guideline for acute kidney injury.
      We excluded case series with fewer than 20 patients, reports on patients younger than 18 years, papers in languages other than English, letters to the editor, commentaries, reviews, and editorials. We also excluded studies with missing data for AKI prevalence after contacting the senior author for clarification. When we suspected multiple reports including the same participants based on the time, location, and authors, we used the most complete publication.
      Two reviewers (ZH and SH) individually scanned titles and abstracts for initial selection. We reviewed selected articles in full and independently assessed for confirmation of eligibility. We resolved discrepancies by consensus and involvement of the other authors.

      Outcomes

      Our 2 outcomes of interest were the prevalence of AKI and KRT initiation among all study patients. We accepted the indication for KRT mentioned in each study because it is difficult to ascertain the reason for KRT from published reports.

      Data Extraction and Study Quality Assessment

      For each study, we extracted data on study characteristics (location and duration), patient characteristics (age, sex, comorbid conditions including hypertension, cardiovascular disease, chronic kidney disease, diabetes, and baseline serum creatinine value), proportion of patients developing AKI (defined according to KDIGO criteria), proportion of patients receiving KRT, proportion of patients with acute respiratory distress syndrome, proportion of patients requiring ICU admission, and important clinical outcomes (discharge from hospital, ongoing hospitalization, and death).
      Because most studies were expected to be case series, we used the National Institutes of Health Quality Assessment Tool for Case Series Studies

      National Institutes of Health (NIH). The National Institutes of Health (NIH) Quality Assessment Tool for Case Series Studies. National Institutes of Health. https://www.nhlbi.nih.gov/health-topics/study-quality-assessment-tools. Accessed December 17, 2020.

      to assess the risk of bias in included studies. This instrument incorporates 9 domains to yield an overall assessment of study quality (good, fair, or poor). We also assessed the quality of studies that were not case series using this tool.

      Statistical Analysis

      We conducted meta-analyses of proportions using arcsine transformation. We expected clinical and methodological heterogeneity between studies and so calculated pooled proportions and 95% CIs using a random-effects model. We used inverse variance to weigh each study in the pooled analysis. We assessed statistical heterogeneity using I2 values. We used a z test to compare differences between subgroups. We assessed for publication bias visually with a funnel plot. We considered P < 0.05 as statistically significant. We performed all analyses with R, version 3.6.1 (R Core team), using the metaprop command from R package meta version 4.13.
      • Balduzzi S.
      • R G.
      • Schwarzer G.
      Package ‘meta’: how to perform a meta-analysis with R: a practical tutorial.

      Subgroup Analysis

      We planned subgroup analyses across age categories, sex, comorbid conditions (chronic kidney disease, cardiovascular disease, and diabetes), and the specific clinical population (ICU vs non-ICU). We also calculated the pooled prevalence of each KDIGO AKI stage to assess the severity of AKI episodes associated with COVID-19.

      Results

      Our search strategy yielded 2,711 unique citations (Fig S1a). Of these, we excluded 830 duplicates and 1,645 citations after screening of title and abstract, leaving 236 articles for full-text review. We subsequently excluded 182 studies that did not fulfil our inclusion criteria because they consisted of studies not reporting on AKI as an outcome (N = 66); studies with incomplete data in which the author did not reply to our queries (N = 10); review articles, meta-analyses, and letters to the editor (N = 23); studies that did not use the KDIGO definition of AKI (N = 54); modelling studies (N = 5); studies comprising maintenance dialysis recipients (N = 10); and studies containing duplicate data (N = 14). This yielded 54
      • Chan L.
      • Chaudhary K.
      • Saha A.
      • et al.
      Acute kidney injury in hospitalized patients with COVID-19. Pre-print.
      ,
      • Hirsch J.S.
      • Ng J.H.
      • Ross D.W.
      • et al.
      Acute kidney injury in patients hospitalized with COVID-19.
      ,
      • Mohamed M.M.
      • Lukitsch I.
      • Torres-Ortiz A.E.
      • et al.
      Acute kidney injury associated with coronavirus disease 2019 in urban New Orleans.
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • et al.
      Clinical characteristics of coronavirus disease 2019 in China.
      • Huang C.
      • Wang Y.
      • Li X.
      • et al.
      Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China.
      ,
      • Alberici F.
      • Delbarba E.
      • Manenti C.
      • et al.
      A single center observational study of the clinical characteristics and short-term outcome of 20 kidney transplant patients admitted for SARS-CoV2 pneumonia.
      • Akalin E.
      • Azzi Y.
      • Bartash R.
      • et al.
      Covid-19 and kidney transplantation.
      • Arentz M.
      • Yim E.
      • Klaff L.
      • et al.
      Characteristics and outcomes of 21 critically ill patients with COVID-19 in Washington State.
      • Argenziano M.G.
      • Bruce S.L.
      • Slater C.L.
      • et al.
      Characterization and clinical course of 1000 patients with coronavirus disease 2019 in New York: retrospective case series.
      • Bhatraju P.K.
      • Ghassemieh B.J.
      • Nichols M.
      • et al.
      Covid-19 in critically ill patients in the Seattle region - case series.
      ,
      • Cheng Y.
      • Luo R.
      • Wang K.
      • et al.
      Kidney disease is associated with in-hospital death of patients with COVID-19.
      • Goyal P.
      • Choi J.J.
      • Pinheiro L.C.
      • et al.
      Clinical characteristics of Covid-19 in New York City.
      • Hong K.S.
      • Lee K.H.
      • Chung J.H.
      • et al.
      Clinical features and outcomes of 98 patients hospitalized with SARS-CoV-2 infection in Daegu, South Korea: a brief descriptive study.

      Li Z, Wu M, Yao J, et al. Caution on kidney dysfunctions of COVID-19 patients. Pre-print. medRxiv. 2020. https://doi.org/10.1101/2020.02.08.20021212.

      • Rubin S.
      • Orieux A.
      • Prevel R.
      • et al.
      Characterisation of acute kidney injury in critically ill patients with severe coronavirus disease-2019 (COVID-19). Pre-print.
      • Tang X.
      • Du R.
      • Wang R.
      • et al.
      Comparison of hospitalized patients with ARDS caused by COVID-19 and H1N1.
      ,
      • Yang X.
      • Yu Y.
      • Xu J.
      • et al.
      Clinical course and outcomes of critically ill patients with SARS-CoV-2 pneumonia in Wuhan, China: a single-centered, retrospective, observational study.
      • Yu Y.
      • Xu D.
      • Fu S.
      • et al.
      Patients with COVID-19 in 19 ICUs in Wuhan, China: a cross-sectional study.
      • Zheng Y.
      • Sun L.J.
      • Xu M.
      • et al.
      Clinical characteristics of 34 COVID-19 patients admitted to intensive care unit in Hangzhou, China.
      • Zhou F.
      • Yu T.
      • Du R.
      • et al.
      Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study.
      studies that included 1 preprint.

      Li Z, Wu M, Yao J, et al. Caution on kidney dysfunctions of COVID-19 patients. Pre-print. medRxiv. 2020. https://doi.org/10.1101/2020.02.08.20021212.

      Risk of Bias Assessment

      Overall, most studies were of good methodological quality (Table S1). Studies determined to be of fair quality most commonly did not report the incidence of KRT. There was no evidence of publication bias suggested by visual inspection of the funnel plot (Fig S1b).

      Study and Patient Characteristics

      Twenty-one reports were from the United States
      • Chan L.
      • Chaudhary K.
      • Saha A.
      • et al.
      Acute kidney injury in hospitalized patients with COVID-19. Pre-print.
      ,
      • Hirsch J.S.
      • Ng J.H.
      • Ross D.W.
      • et al.
      Acute kidney injury in patients hospitalized with COVID-19.
      ,
      • Mohamed M.M.
      • Lukitsch I.
      • Torres-Ortiz A.E.
      • et al.
      Acute kidney injury associated with coronavirus disease 2019 in urban New Orleans.
      ,
      • Akalin E.
      • Azzi Y.
      • Bartash R.
      • et al.
      Covid-19 and kidney transplantation.
      • Arentz M.
      • Yim E.
      • Klaff L.
      • et al.
      Characteristics and outcomes of 21 critically ill patients with COVID-19 in Washington State.
      • Argenziano M.G.
      • Bruce S.L.
      • Slater C.L.
      • et al.
      Characterization and clinical course of 1000 patients with coronavirus disease 2019 in New York: retrospective case series.
      • Bhatraju P.K.
      • Ghassemieh B.J.
      • Nichols M.
      • et al.
      Covid-19 in critically ill patients in the Seattle region - case series.
      ,
      • Goyal P.
      • Choi J.J.
      • Pinheiro L.C.
      • et al.
      Clinical characteristics of Covid-19 in New York City.
      ,
      • Chaudhry Z.S.
      • Williams J.D.
      • Vahia A.
      • et al.
      Clinical characteristics and outcomes of COVID-19 in solid organ transplant recipients: a case-control study.
      • Cummings M.J.
      • Baldwin M.R.
      • Abrams D.
      • et al.
      Epidemiology, clinical course, and outcomes of critically ill adults with COVID-19 in New York City: a prospective cohort study.
      • Ferguson J.
      • Rosser J.I.
      • Quintero O.
      • et al.
      Characteristics and outcomes of coronavirus disease patients under nonsurge conditions, Northern California, USA, March-April 2020.
      • Fisher M.
      • Neugarten J.
      • Bellin E.
      • et al.
      AKI in hospitalized patients with and without COVID-19: a comparison study.
      • Gupta S.
      • Coca S.G.
      • Chan L.
      • et al.
      AKI treated with renal replacement therapy in critically ill patients with COVID-19.
      • Imam Z.
      • Odish F.
      • Gill I.
      • et al.
      Older age and comorbidity are independent mortality predictors in a large cohort of 1305 COVID-19 patients in Michigan, United States.
      • Lee J.R.
      • Silberzweig J.
      • Akchurin O.
      • et al.
      Characteristics of acute kidney injury in hospitalized COVID-19 patients in an urban academic medical center.
      • Mukherjee V.
      • Toth A.T.
      • Fenianos M.
      • et al.
      Clinical outcomes in critically ill coronavirus disease 2019 patients: a unique New York City public hospital experience.
      • Naar L.
      • Langeveld K.
      • El Moheb M.
      • et al.
      Acute kidney injury in critically-ill patients with COVID-19: a single-center experience of 206 consecutive patients.
      • Naaraayan A.
      • Nimkar A.
      • Hasan A.
      • et al.
      Analysis of male sex as a risk factor in older adults with coronavirus disease 2019: a retrospective cohort study from the New York City metropolitan region.
      • Okoh A.K.
      • Sossou C.
      • Dangayach N.S.
      • et al.
      Coronavirus disease 19 in minority populations of Newark, New Jersey.
      • Suleyman G.
      • Fadel R.A.
      • Malette K.M.
      • et al.
      Clinical characteristics and morbidity associated with coronavirus disease 2019 in a series of patients in metropolitan Detroit.
      ; 17 were from China
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • et al.
      Clinical characteristics of coronavirus disease 2019 in China.
      ,
      • Huang C.
      • Wang Y.
      • Li X.
      • et al.
      Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China.
      ,
      • Cheng Y.
      • Luo R.
      • Wang K.
      • et al.
      Kidney disease is associated with in-hospital death of patients with COVID-19.
      ,

      Li Z, Wu M, Yao J, et al. Caution on kidney dysfunctions of COVID-19 patients. Pre-print. medRxiv. 2020. https://doi.org/10.1101/2020.02.08.20021212.

      ,
      • Tang X.
      • Du R.
      • Wang R.
      • et al.
      Comparison of hospitalized patients with ARDS caused by COVID-19 and H1N1.
      ,
      • Yang X.
      • Yu Y.
      • Xu J.
      • et al.
      Clinical course and outcomes of critically ill patients with SARS-CoV-2 pneumonia in Wuhan, China: a single-centered, retrospective, observational study.
      • Yu Y.
      • Xu D.
      • Fu S.
      • et al.
      Patients with COVID-19 in 19 ICUs in Wuhan, China: a cross-sectional study.
      • Zheng Y.
      • Sun L.J.
      • Xu M.
      • et al.
      Clinical characteristics of 34 COVID-19 patients admitted to intensive care unit in Hangzhou, China.
      • Zhou F.
      • Yu T.
      • Du R.
      • et al.
      Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study.
      • Chaudhry Z.S.
      • Williams J.D.
      • Vahia A.
      • et al.
      Clinical characteristics and outcomes of COVID-19 in solid organ transplant recipients: a case-control study.
      • Cummings M.J.
      • Baldwin M.R.
      • Abrams D.
      • et al.
      Epidemiology, clinical course, and outcomes of critically ill adults with COVID-19 in New York City: a prospective cohort study.
      • Ferguson J.
      • Rosser J.I.
      • Quintero O.
      • et al.
      Characteristics and outcomes of coronavirus disease patients under nonsurge conditions, Northern California, USA, March-April 2020.
      • Fisher M.
      • Neugarten J.
      • Bellin E.
      • et al.
      AKI in hospitalized patients with and without COVID-19: a comparison study.
      • Gupta S.
      • Coca S.G.
      • Chan L.
      • et al.
      AKI treated with renal replacement therapy in critically ill patients with COVID-19.
      • Imam Z.
      • Odish F.
      • Gill I.
      • et al.
      Older age and comorbidity are independent mortality predictors in a large cohort of 1305 COVID-19 patients in Michigan, United States.
      • Lee J.R.
      • Silberzweig J.
      • Akchurin O.
      • et al.
      Characteristics of acute kidney injury in hospitalized COVID-19 patients in an urban academic medical center.
      • Mukherjee V.
      • Toth A.T.
      • Fenianos M.
      • et al.
      Clinical outcomes in critically ill coronavirus disease 2019 patients: a unique New York City public hospital experience.
      • Naar L.
      • Langeveld K.
      • El Moheb M.
      • et al.
      Acute kidney injury in critically-ill patients with COVID-19: a single-center experience of 206 consecutive patients.
      • Naaraayan A.
      • Nimkar A.
      • Hasan A.
      • et al.
      Analysis of male sex as a risk factor in older adults with coronavirus disease 2019: a retrospective cohort study from the New York City metropolitan region.
      • Okoh A.K.
      • Sossou C.
      • Dangayach N.S.
      • et al.
      Coronavirus disease 19 in minority populations of Newark, New Jersey.
      • Suleyman G.
      • Fadel R.A.
      • Malette K.M.
      • et al.
      Clinical characteristics and morbidity associated with coronavirus disease 2019 in a series of patients in metropolitan Detroit.
      • Zhang G.
      • Hu C.
      • Luo L.
      • et al.
      Clinical features and short-term outcomes of 221 patients with COVID-19 in Wuhan, China.
      ,
      • Cai Q.
      • Huang D.
      • Ou P.
      • et al.
      COVID-19 in a designated infectious diseases hospital outside Hubei Province, China.
      • Liu J.
      • Zhang L.
      • Chen Y.
      • et al.
      Association of sex with clinical outcomes in COVID-19 patients: a retrospective analysis of 1190 cases.
      • Shi S.
      • Qin M.
      • Shen B.
      • et al.
      Association of cardiac injury with mortality in hospitalized patients with COVID-19 in Wuhan, China.
      • Wang J.
      • Wang Z.
      • Zhu Y.
      • et al.
      Identify the risk factors of COVID-19-related acute kidney injury: a single-center, retrospective cohort study.
      • Xia P.
      • Wen Y.
      • Duan Y.
      • et al.
      Clinicopathological features and outcomes of acute kidney injury in critically ill COVID-19 with prolonged disease course: a retrospective cohort.
      • Xu J.
      • Yang X.
      • Yang L.
      • et al.
      Clinical course and predictors of 60-day mortality in 239 critically ill patients with COVID-19: a multicenter retrospective study from Wuhan, China.
      • Qian S.-Z.
      • Hong W.-D.
      • Lingjie M.
      • Chenfeng L.
      • Zhendong F.
      • Pan J.-Y.
      Clinical characteristics and outcomes of severe and critical patients with 2019 novel coronavirus disease (COVID-19) in Wenzhou: a retrospective study.
      ; 12 were from Europe
      • Alberici F.
      • Delbarba E.
      • Manenti C.
      • et al.
      A single center observational study of the clinical characteristics and short-term outcome of 20 kidney transplant patients admitted for SARS-CoV2 pneumonia.
      ,
      • Rubin S.
      • Orieux A.
      • Prevel R.
      • et al.
      Characterisation of acute kidney injury in critically ill patients with severe coronavirus disease-2019 (COVID-19). Pre-print.
      ,
      • Azoulay E.
      • Fartoukh M.
      • Darmon M.
      • et al.
      Increased mortality in patients with severe SARS-CoV-2 infection admitted within seven days of disease onset.
      • Caillard S.
      • Anglicheau D.
      • Matignon M.
      • et al.
      An initial report from the French SOT COVID Registry suggests high mortality due to Covid-19 in recipients of kidney transplants.
      • Fava A.
      • Cucchiari D.
      • Montero N.
      • et al.
      Clinical characteristics and risk factors for severe COVID-19 in hospitalized kidney transplant recipients: a multicentric cohort study.
      • Fominskiy E.V.
      • Scandroglio A.M.
      • Monti G.
      • et al.
      Prevalence, characteristics, risk factors, and outcomes of invasively ventilated COVID-19 patients with acute kidney injury and renal replacement therapy.
      • Hoek R.A.S.
      • Manintveld O.C.
      • Betjes M.G.H.
      • et al.
      COVID-19 in solid organ transplant recipients: a single-center experience.
      • Joseph A.
      • Zafrani L.
      • Mabrouki A.
      • Azoulay E.
      • Darmon M.
      Acute kidney injury in patients with SARS-CoV-2 infection.
      • Larsson E.
      • Brattstrom O.
      • Agvald-Ohman C.
      • et al.
      Characteristics and outcomes of patients with COVID-19 admitted to ICU in a tertiary hospital in Stockholm, Sweden.
      • Lendorf M.E.
      • Boisen M.K.
      • Kristensen P.L.
      • et al.
      Characteristics and early outcomes of patients hospitalised for Covid-19 in North Zealand, Denmark.
      • Nowak B.
      • Szymanski P.
      • Pankowski I.
      • et al.
      Clinical characteristics and short-term outcomes of patients with coronavirus disease 2019: a retrospective single-center experience of a designated hospital in Poland.
      • Portoles J.
      • Marques M.
      • Lopez-Sanchez P.
      • et al.
      Chronic kidney disease and acute kidney injury in the COVID-19 Spanish outbreak.
      ; 1 each were from India,
      • Aggarwal A.
      • Shrivastava A.
      • Kumar A.
      • Ali A.
      Clinical and epidemiological features of SARS-CoV-2 patients in SARI ward of a tertiary care centre in New Delhi.
      Bahrain,
      • Taher A.
      • Alalwan A.A.
      • Naser N.
      • Alsegai O.
      • Alaradi A.
      Acute kidney injury in COVID-19 pneumonia: a single-center experience in Bahrain.
      and South Korea
      • Hong K.S.
      • Lee K.H.
      • Chung J.H.
      • et al.
      Clinical features and outcomes of 98 patients hospitalized with SARS-CoV-2 infection in Daegu, South Korea: a brief descriptive study.
      ; and 1 report
      • Cravedi P.
      • Suraj S.M.
      • Azzi Y.
      • et al.
      COVID-19 and kidney transplantation: results from the TANGO International Transplant Consortium.
      included multiple cities from the United States and Europe. The studies included 30,657 hospitalized patients, of whom 12,800 (41.8%) were women. In total, 9,650 patients (n = 40 studies) were admitted to the ICU, 15,728 patients (n = 24 studies) were admitted to a non-ICU setting, and 4,991 (n = 14 studies) patients did not have their hospital setting reported. Mean age of patients ranged between 47 and 71 years. Hypertension and diabetes mellitus were common comorbid conditions. Mean baseline serum creatinine values ranged from 0.67 to 2 mg/dL (Tables 1
      • Chan L.
      • Chaudhary K.
      • Saha A.
      • et al.
      Acute kidney injury in hospitalized patients with COVID-19. Pre-print.
      ,
      • Hirsch J.S.
      • Ng J.H.
      • Ross D.W.
      • et al.
      Acute kidney injury in patients hospitalized with COVID-19.
      ,
      • Mohamed M.M.
      • Lukitsch I.
      • Torres-Ortiz A.E.
      • et al.
      Acute kidney injury associated with coronavirus disease 2019 in urban New Orleans.
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • et al.
      Clinical characteristics of coronavirus disease 2019 in China.
      • Huang C.
      • Wang Y.
      • Li X.
      • et al.
      Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China.
      ,
      Kidney Disease: Improving Global Outcomes (KDIGO) Acute Kidney Injury Work Group
      KDIGO clinical practice guideline for acute kidney injury.
      ,
      • Alberici F.
      • Delbarba E.
      • Manenti C.
      • et al.
      A single center observational study of the clinical characteristics and short-term outcome of 20 kidney transplant patients admitted for SARS-CoV2 pneumonia.
      • Akalin E.
      • Azzi Y.
      • Bartash R.
      • et al.
      Covid-19 and kidney transplantation.
      • Arentz M.
      • Yim E.
      • Klaff L.
      • et al.
      Characteristics and outcomes of 21 critically ill patients with COVID-19 in Washington State.
      • Argenziano M.G.
      • Bruce S.L.
      • Slater C.L.
      • et al.
      Characterization and clinical course of 1000 patients with coronavirus disease 2019 in New York: retrospective case series.
      • Bhatraju P.K.
      • Ghassemieh B.J.
      • Nichols M.
      • et al.
      Covid-19 in critically ill patients in the Seattle region - case series.
      ,
      • Goyal P.
      • Choi J.J.
      • Pinheiro L.C.
      • et al.
      Clinical characteristics of Covid-19 in New York City.
      • Hong K.S.
      • Lee K.H.
      • Chung J.H.
      • et al.
      Clinical features and outcomes of 98 patients hospitalized with SARS-CoV-2 infection in Daegu, South Korea: a brief descriptive study.

      Li Z, Wu M, Yao J, et al. Caution on kidney dysfunctions of COVID-19 patients. Pre-print. medRxiv. 2020. https://doi.org/10.1101/2020.02.08.20021212.

      • Rubin S.
      • Orieux A.
      • Prevel R.
      • et al.
      Characterisation of acute kidney injury in critically ill patients with severe coronavirus disease-2019 (COVID-19). Pre-print.
      • Tang X.
      • Du R.
      • Wang R.
      • et al.
      Comparison of hospitalized patients with ARDS caused by COVID-19 and H1N1.
      ,
      • Yang X.
      • Yu Y.
      • Xu J.
      • et al.
      Clinical course and outcomes of critically ill patients with SARS-CoV-2 pneumonia in Wuhan, China: a single-centered, retrospective, observational study.
      ,
      • Yu Y.
      • Xu D.
      • Fu S.
      • et al.
      Patients with COVID-19 in 19 ICUs in Wuhan, China: a cross-sectional study.
      ,
      • Zhang G.
      • Hu C.
      • Luo L.
      • et al.
      Clinical features and short-term outcomes of 221 patients with COVID-19 in Wuhan, China.
      • Cai Q.
      • Huang D.
      • Ou P.
      • et al.
      COVID-19 in a designated infectious diseases hospital outside Hubei Province, China.
      • Liu J.
      • Zhang L.
      • Chen Y.
      • et al.
      Association of sex with clinical outcomes in COVID-19 patients: a retrospective analysis of 1190 cases.
      • Shi S.
      • Qin M.
      • Shen B.
      • et al.
      Association of cardiac injury with mortality in hospitalized patients with COVID-19 in Wuhan, China.
      • Wang J.
      • Wang Z.
      • Zhu Y.
      • et al.
      Identify the risk factors of COVID-19-related acute kidney injury: a single-center, retrospective cohort study.
      • Xia P.
      • Wen Y.
      • Duan Y.
      • et al.
      Clinicopathological features and outcomes of acute kidney injury in critically ill COVID-19 with prolonged disease course: a retrospective cohort.
      • Xu J.
      • Yang X.
      • Yang L.
      • et al.
      Clinical course and predictors of 60-day mortality in 239 critically ill patients with COVID-19: a multicenter retrospective study from Wuhan, China.
      • Qian S.-Z.
      • Hong W.-D.
      • Lingjie M.
      • Chenfeng L.
      • Zhendong F.
      • Pan J.-Y.
      Clinical characteristics and outcomes of severe and critical patients with 2019 novel coronavirus disease (COVID-19) in Wenzhou: a retrospective study.
      • Azoulay E.
      • Fartoukh M.
      • Darmon M.
      • et al.
      Increased mortality in patients with severe SARS-CoV-2 infection admitted within seven days of disease onset.
      • Caillard S.
      • Anglicheau D.
      • Matignon M.
      • et al.
      An initial report from the French SOT COVID Registry suggests high mortality due to Covid-19 in recipients of kidney transplants.
      • Fava A.
      • Cucchiari D.
      • Montero N.
      • et al.
      Clinical characteristics and risk factors for severe COVID-19 in hospitalized kidney transplant recipients: a multicentric cohort study.
      • Fominskiy E.V.
      • Scandroglio A.M.
      • Monti G.
      • et al.
      Prevalence, characteristics, risk factors, and outcomes of invasively ventilated COVID-19 patients with acute kidney injury and renal replacement therapy.
      • Hoek R.A.S.
      • Manintveld O.C.
      • Betjes M.G.H.
      • et al.
      COVID-19 in solid organ transplant recipients: a single-center experience.
      • Joseph A.
      • Zafrani L.
      • Mabrouki A.
      • Azoulay E.
      • Darmon M.
      Acute kidney injury in patients with SARS-CoV-2 infection.
      • Larsson E.
      • Brattstrom O.
      • Agvald-Ohman C.
      • et al.
      Characteristics and outcomes of patients with COVID-19 admitted to ICU in a tertiary hospital in Stockholm, Sweden.
      • Lendorf M.E.
      • Boisen M.K.
      • Kristensen P.L.
      • et al.
      Characteristics and early outcomes of patients hospitalised for Covid-19 in North Zealand, Denmark.
      • Nowak B.
      • Szymanski P.
      • Pankowski I.
      • et al.
      Clinical characteristics and short-term outcomes of patients with coronavirus disease 2019: a retrospective single-center experience of a designated hospital in Poland.
      • Portoles J.
      • Marques M.
      • Lopez-Sanchez P.
      • et al.
      Chronic kidney disease and acute kidney injury in the COVID-19 Spanish outbreak.
      • Aggarwal A.
      • Shrivastava A.
      • Kumar A.
      • Ali A.
      Clinical and epidemiological features of SARS-CoV-2 patients in SARI ward of a tertiary care centre in New Delhi.
      • Taher A.
      • Alalwan A.A.
      • Naser N.
      • Alsegai O.
      • Alaradi A.
      Acute kidney injury in COVID-19 pneumonia: a single-center experience in Bahrain.
      • Cravedi P.
      • Suraj S.M.
      • Azzi Y.
      • et al.
      COVID-19 and kidney transplantation: results from the TANGO International Transplant Consortium.
      ,
      • Cheng Y.
      • Luo R.
      • Wang X.
      • et al.
      The incidence, risk factors, and prognosis of acute kidney injury in adult patients with coronavirus disease 2019.
      ,
      • Pelayo J.
      • Lo K.B.
      • Bhargav R.
      • et al.
      Clinical characteristics and outcomes of community- and hospital-acquired acute kidney injury with COVID-19 in a US inner city hospital system.
      and 2).
      Table 1Characteristics of Included Studies
      StudyCity and CountryPopulation and SettingPatient CharacteristicsComorbid DiseaseComplicationsOutcomes
      No.Age, y
      Age is reported as mean, unless italicized (median); Scr is reported as mean, unless otherwise specified or italicized (median).
      Female SexHTNCKDDMAdmission Scr, mg/dL
      Age is reported as mean, unless italicized (median); Scr is reported as mean, unless otherwise specified or italicized (median).
      AKI
      All AKI was reported according to the KDIGO AKI criteria, but not all studies reported AKI stages.15
      KRT
      Denominator is all patients included in each study.
      ARDSPatients Admitted to ICUDischarged Alive/Still in HospitalIn-Hospital Deaths
      Aggarwal et al
      • Aggarwal A.
      • Shrivastava A.
      • Kumar A.
      • Ali A.
      Clinical and epidemiological features of SARS-CoV-2 patients in SARI ward of a tertiary care centre in New Delhi.
      New Delhi, IndiaPatients with COVID-19 and severe acute respiratory illness admitted to Dr Ram Manohar Lohia hospital 4/10/20-4/30/203254.541.4%34.4%0%50%1.113 (40.6%)NRNR37.5%1%, D/C; 71%, still hospitalized28%
      Alberici et al
      • Alberici F.
      • Delbarba E.
      • Manenti C.
      • et al.
      A single center observational study of the clinical characteristics and short-term outcome of 20 kidney transplant patients admitted for SARS-CoV2 pneumonia.
      Brescia, ItalyKidney transplant recipients with COVID-19 admitted to Spedali Hospital 2/27/20-3/24/20205920%85%100%15%26 (30%)1 (5%)55%20%15%, D/C; 60%, still hospitalized25%
      Akalin et al
      • Akalin E.
      • Azzi Y.
      • Bartash R.
      • et al.
      Covid-19 and kidney transplantation.
      New York City, USATransplant recipients with COVID-19 admitted or treated as outpatients at Montefiore Medical Center 3/16/20-4/1/2036 (28 admitted)6028%94%100%69%1.4NR6 (21%)NRNR36%, D/C; 43%, still hospitalized21%
      Arentz et al
      • Arentz M.
      • Yim E.
      • Klaff L.
      • et al.
      Characteristics and outcomes of 21 critically ill patients with COVID-19 in Washington State.
      Seattle, USAPatients with COVID-19 admitted to ICU at Evergreen Hospital 2/20/20-3/5/20217048%NR47.6%33.3%1.54 (19%)3 (14%)95%100%47.6%, still hospitalized52.4%
      Argenziano et al
      • Argenziano M.G.
      • Bruce S.L.
      • Slater C.L.
      • et al.
      Characterization and clinical course of 1000 patients with coronavirus disease 2019 in New York: retrospective case series.
      New York City, USATotal patients with COVID-19 admitted to New York Presbyterian Hospital Irving Medical Center 3/11/20-4/6/201,0006340.4%60.1%13.7%37.2%NR288
      Among 850 patients with available data.
      (33.9%)
      117 (13.8%)
      Among 850 patients with available data.
      35%
      Among 850 patients with available data.
      23.6%69.9%, D/C; 9%, still hospitalized21.1%
      Argenziano et al
      • Argenziano M.G.
      • Bruce S.L.
      • Slater C.L.
      • et al.
      Characterization and clinical course of 1000 patients with coronavirus disease 2019 in New York: retrospective case series.
      New York City, USAICU Patients with COVID-19 admitted to New York Presbyterian Hospital Irving Medical Center 3/11/20-4/6/202366233.3%66.9%11.4%42.8%NR184 (78%)
      Among 850 patients with available data.
      83 (35.2%)
      Among 850 patients with available data.
      90%
      Among 850 patients with available data.
      NRNRNR
      Argenziano et al
      • Argenziano M.G.
      • Bruce S.L.
      • Slater C.L.
      • et al.
      Characterization and clinical course of 1000 patients with coronavirus disease 2019 in New York: retrospective case series.
      New York City, USANon-ICU patients with COVID-19 admitted to New York Presbyterian Hospital Irving Medical Center 3/11/20-4/6/206146442.5%59.8%16%37.8%NR104 (16.9%)
      Among 850 patients with available data.
      34 (5.5%)
      Among 850 patients with available data.
      14%
      Among 850 patients with available data.
      NRNRNR
      Argenziano et al
      • Argenziano M.G.
      • Bruce S.L.
      • Slater C.L.
      • et al.
      Characterization and clinical course of 1000 patients with coronavirus disease 2019 in New York: retrospective case series.
      New York City, USAPatients with COVID-19 admitted to ED of New York Presbyterian Hospital Irving Medical Center 3/11/20-4/6/201505543.3%50.7%8%27%NRNRNRNRNRNRNR
      Azoulay et al
      • Azoulay E.
      • Fartoukh M.
      • Darmon M.
      • et al.
      Increased mortality in patients with severe SARS-CoV-2 infection admitted within seven days of disease onset.
      Paris, FrancePatients with COVID-19 admitted to ICU at 4 hospitals 3/11/20-4/6/203796222.9%49.6%16.9%30.1%NR195 (51.5%)74 (19.5%)NR100%34%, D/C; 27%, still hospitalized39%
      Bhatraju et al
      • Bhatraju P.K.
      • Ghassemieh B.J.
      • Nichols M.
      • et al.
      Covid-19 in critically ill patients in the Seattle region - case series.
      Seattle, USAPatients with COVID-19 admitted to ICU at 9 hospitals within Seattle region 2/24/20-3/3/20246438%NR21%58%NR6 (25%)1 (4%)75%100%21%, D/C; 29%, still hospitalized50%
      Cai et al
      • Cai Q.
      • Huang D.
      • Ou P.
      • et al.
      COVID-19 in a designated infectious diseases hospital outside Hubei Province, China.
      Shenzhen, ChinaPatients with COVID-19 admitted to Third People’s Hospital 1/11/20-2/6/2029847.551.3%15.8%NR6%0.717 (5.7%)4 (1%)NR10%89.9%, D/C; 8.1%, still hospitalized1%
      Caillard et al
      • Caillard S.
      • Anglicheau D.
      • Matignon M.
      • et al.
      An initial report from the French SOT COVID Registry suggests high mortality due to Covid-19 in recipients of kidney transplants.
      Various cities, FranceKidney transplant recipients with COVID-19 admitted to hospitals in France 3/4/20-4/21/2024361.633.3%90.1%41.3%100%2106 (43.6%)27 (11.1%)NR35%82.3%, no. D/C or still hospitalized NR17.7%
      Chan et al
      • Chan L.
      • Chaudhary K.
      • Saha A.
      • et al.
      Acute kidney injury in hospitalized patients with COVID-19. Pre-print.
      New York City, USAPatients with COVID-19 admitted to Mount Sinai Health System (5 hospitals) 2/23/20-4/15/203235; (976 ICU)66.542.3%36.9%10%24.7%0.9Total: 1,406 (43.4%); stage 1: 492 (15.2%); stage 2: 281 (8.5%); stage 3: 633 (19.7%); ICU: 553; non-ICU: 853Total: 280 (8.7%); ICU:188; non-ICU: 92NR25.2%61.7%, D/C; 14.5%, still hospitalized23.8%
      Chaudhry et al
      • Chaudhry Z.S.
      • Williams J.D.
      • Vahia A.
      • et al.
      Clinical characteristics and outcomes of COVID-19 in solid organ transplant recipients: a case-control study.
      Detroit, USATransplant recipients with COVID-19 admitted to Henry Ford Hospital 3/20/20-4/18/20356234.3%94.3%88.6%65.7%NR22 (46.8%)7 (20%)35.3%37%68.6%, D/C; 8.6%, still hospitalized22.8%
      Cheng et al
      • Cheng Y.
      • Luo R.
      • Wang X.
      • et al.
      The incidence, risk factors, and prognosis of acute kidney injury in adult patients with coronavirus disease 2019.
      Wuhan, ChinaPatients with COVID-19 admitted to Tongji Hospital 1/18/20-2/28/2013926349%36%2%17%0.8Total: 99 (7%); stage 1: 42 (3%); stage 2: 22 (2%); stage 3: 35 (3%)15 (1%)NR10NR14%
      Cravedi et al
      • Cravedi P.
      • Suraj S.M.
      • Azzi Y.
      • et al.
      COVID-19 and kidney transplantation: results from the TANGO International Transplant Consortium.
      Multiple cities in USA, Spain, ItalyKidney transplant recipients with COVID-19 admitted to 12 hospitals in USA, Italy, and Spain 3/2/20-5/15/201446234.7%95.1%100%52.1%1.574 (52.1%)NRNRNR68%, distinction NR32%
      Cummings et al
      • Cummings M.J.
      • Baldwin M.R.
      • Abrams D.
      • et al.
      Epidemiology, clinical course, and outcomes of critically ill adults with COVID-19 in New York City: a prospective cohort study.
      New York City, USAPatients with COVID-19 admitted to 2 New York Presbyterian hospitals 1/18/20-2/28/202576233%63%14%36%1.576 (30%)
      Only KRT reported.
      76 (30%)
      Only KRT reported.
      NRNR24%, D/C; 37%, still hospitalized39%
      Fava et al
      • Fava A.
      • Cucchiari D.
      • Montero N.
      • et al.
      Clinical characteristics and risk factors for severe COVID-19 in hospitalized kidney transplant recipients: a multicentric cohort study.
      Multiple cities, SpainKidney transplant recipients with COVID-19 admitted to 5 hospitals in Spain 3/4/20-4/17/2010459.742.3%86.5%100%30.8%1.8Total: 47 (45%); stage 1: 30 (29%); stage 2: 7 (6%); stage 3: 10 (10%)NR54.8%NR73.1%, distinction NR26.9%
      Ferguson et al
      • Ferguson J.
      • Rosser J.I.
      • Quintero O.
      • et al.
      Characteristics and outcomes of coronavirus disease patients under nonsurge conditions, Northern California, USA, March-April 2020.
      Palo Alto, USAPatients with COVID-19 admitted to 2 hospitals in Palo Alto (Stanford University Hospital and Valleycare) 3/13/20-4/11/2072; (21 ICU)60.447.2%34.7%12.5%27.8%0.9Total: 4 (5.6%)
      Only KRT reported.
      ; ICU: 4 (5.6%)
      Only KRT reported.
      Total: 4 (5.6%)
      Only KRT reported.


      ICU: 4 (5.6%)
      Only KRT reported.
      18%29%86.1%, D/C; 5.6%, still hospitalized8.3%
      Fisher et al
      • Fisher M.
      • Neugarten J.
      • Bellin E.
      • et al.
      AKI in hospitalized patients with and without COVID-19: a comparison study.
      New York City, USAPatients with COVID-19 admitted to 3 hospitals in Montefiore Health System 3/1/20-4/26/203,34564.446.9%NR12.2%27.1%NRTotal: 1,903 (56.9%); stage 1: 942 (49.5%); stage 2: 387 (20.3%); stage 3: 574 (30.2%)164 (4.9%)NR13.1%64%, D/C; 12.8%, still hospitalized23.2%
      Fominskliy et al
      • Fominskiy E.V.
      • Scandroglio A.M.
      • Monti G.
      • et al.
      Prevalence, characteristics, risk factors, and outcomes of invasively ventilated COVID-19 patients with acute kidney injury and renal replacement therapy.
      Milan, ItalyMechanically ventilated patients with COVID-19 admitted to ICU 2/5/20-4/20/2096NR16.7%43.8%6.3%16.6%NRTotal: 72 (75%); stage 1: 33 (34.3%); stage 2: 15 (15.6%); stage 3: 24 (25%)17 (17.7%)NR100%NR33.3%
      Guan et al
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • et al.
      Clinical characteristics of coronavirus disease 2019 in China.
      Multiple cities, ChinaPatients with COVID-19 hospitalized at 552 sites in 30 provinces in China 12/11/19-1/29/201,0994742%15%0.7%7.4%NR6 (0.5%)9 (0.8%)
      Some patients receiving KRT may have been maintenance dialysis patients, but not reported by the authors.
      3.4%5%5%, D/C; 93.6%, still hospitalized1.4%
      Gupta et al
      • Gupta S.
      • Coca S.G.
      • Chan L.
      • et al.
      AKI treated with renal replacement therapy in critically ill patients with COVID-19.
      Multiple cities, USAPatients with COVID-19 admitted to ICU 3/4/20-4/11/203,0996235.4%60.3%28.9%40%1.5637 (20.6%)
      Only KRT reported.
      637 (20.6%)
      Only KRT reported.
      NR100%NRNR
      Goyal et al
      • Goyal P.
      • Choi J.J.
      • Pinheiro L.C.
      • et al.
      Clinical characteristics of Covid-19 in New York City.
      New York City, USAPatients with COVID-19 admitted to 2 hospitals in Manhattan (Weill Cornell Medical Center and Lower Manhattan Hospital) 3/3/20-3/27/20393
      Renal outcomes reported for only 375 patients.
      62.239.4%50.1%4.6% ESKD25.2%16% ≥ 1.518 (4.8%)
      Only KRT reported.
      18 (4.8%)
      Renal outcomes reported for only 375 patients.
      NRNR66.2%, D/C; 23.6%, still hospitalized10.2%
      Hirsch et al
      • Hirsch J.S.
      • Ng J.H.
      • Ross D.W.
      • et al.
      Acute kidney injury in patients hospitalized with COVID-19.
      New York City, USAPatients with COVID-19 admitted to 13 hospitals in Northwell Medical System 3/1/20-4/5/205,449; (ICU: 1,395)6439.1%55.7%NR33%1.0Total: 1,993 (36.6%); stage 1: 927 (17%); stage 2: 447 (8.2%); stage 3: 619 (11.4%); ICU: 1,060; non-ICU: 993285 (5.2%)NR25.6%60.2%, D/C; 16.3%, still hospitalized23.5%
      Hoek et al
      • Hoek R.A.S.
      • Manintveld O.C.
      • Betjes M.G.H.
      • et al.
      COVID-19 in solid organ transplant recipients: a single-center experience.
      Multiple cities, NetherlandsSolid organ transplant recipients with COVID-19 admitted to various hospitals in Netherlands 2/27/20-4/30/202359.321.7%83%NR43%2.21 (4.3%)
      Only KRT reported.
      1 (4.3%)
      Only KRT reported.
      NRNRNR21.7%
      Hong et al
      • Hong K.S.
      • Lee K.H.
      • Chung J.H.
      • et al.
      Clinical features and outcomes of 98 patients hospitalized with SARS-CoV-2 infection in Daegu, South Korea: a brief descriptive study.
      Daegu, South KoreaPatients with COVID-19 admitted to Yeungnam University Medical Center through 3/29/20Total: 98; ICU: 135561.2%30.6%NR9.2%NR9 (9.2%); ICU: 8; non-ICU: 13 (3%); ICU: 318.4%13.2%30.6%, D/C; 58.2%, still hospitalized; 6.1%, transferred5.1%
      Huang et al
      • Huang C.
      • Wang Y.
      • Li X.
      • et al.
      Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China.
      Wuhan, ChinaPatients with COVID-19 admitted to Jin Yintan Hospital 12/16/19-1/2/20Total: 41; (ICU: 13)4927%15%NR20%10% > 1.53 (7%)
      Only KRT reported.
      ; ICU: 3
      Only KRT reported.
      3 (7%)
      Only KRT reported.
      ; ICU: 3
      Only KRT reported.
      29%32%68%, D/C; 17%, still hospitalized15%
      Imam et al
      • Imam Z.
      • Odish F.
      • Gill I.
      • et al.
      Older age and comorbidity are independent mortality predictors in a large cohort of 1305 COVID-19 patients in Michigan, United States.
      Detroit, USAPatients with COVID-19 admitted to 8 hospitals in Beaumont Health system 3/1/20-4/17/201,3056146.2%56.2%17.5%30.1%1.276 (5.8%)NRNR26.4%78.3%, D/C; 6.4%, still hospitalized15.3%
      Joseph et al
      • Joseph A.
      • Zafrani L.
      • Mabrouki A.
      • Azoulay E.
      • Darmon M.
      Acute kidney injury in patients with SARS-CoV-2 infection.
      Paris, FrancePatients with COVID-19 admitted to ICU at Hopital Saint-Louis 3/1/20-6/1/20 01005930%56%29%30%0.7Total: 81 (81%); stage 1:44 (44%); stage 2: 10 (10%); stage 3:27 (27%)13 (13%)NR100%71%, distinction NR29%
      Larsson et al
      • Larsson E.
      • Brattstrom O.
      • Agvald-Ohman C.
      • et al.
      Characteristics and outcomes of patients with COVID-19 admitted to ICU in a tertiary hospital in Stockholm, Sweden.
      Stockholm, SwedenPatients with COVID-19 admitted to ICU of Karolinsk University Hospital 3/9/20-4/20/202605920%39.6%1.5%26.2%NR59 (22.7%)
      Only KRT reported.
      59 (22.7%)
      Only KRT reported.
      NR100%31.3%, D/C; 38.4, still hospitalized30.3%
      Lee et al
      • Lee J.R.
      • Silberzweig J.
      • Akchurin O.
      • et al.
      Characteristics of acute kidney injury in hospitalized COVID-19 patients in an urban academic medical center.
      NYC, USAPatients with COVID-19 admitted to New York Presbyterian/Weill Cornell Medical center 3/1/20-4/19/201,0026648%60%14%38%0.9Total: 294 (29%); stage 1: 182 (18%); stage 2: 29 (3%); stage 3: 83 (8%)59 (6%)NR27%83%, distinction NR17%
      Lendorf et al
      • Lendorf M.E.
      • Boisen M.K.
      • Kristensen P.L.
      • et al.
      Characteristics and early outcomes of patients hospitalised for Covid-19 in North Zealand, Denmark.
      DenmarkPatients with COVID-19 admitted to North Zealand Hospital 3/1/20-5/4/20111; (20 ICU)6840%34%7%14%0.9Total: 13 (12%); ICU: 6; non-ICU: 7Total: 3 (3%); ICU: 3NR18%81%, D/C; 5%, still hospitalized14%
      Li et al

      Li Z, Wu M, Yao J, et al. Caution on kidney dysfunctions of COVID-19 patients. Pre-print. medRxiv. 2020. https://doi.org/10.1101/2020.02.08.20021212.

      Wuhan and Chongqing, ChinaPatients with COVID-19 admitted to 4 hospitals in Hubei province and Chongqing (Tongji, Pulmonary, Central and Chongqing Southwest) 1/6/20-2/21/201935751%NRNRNR0.855 (28%)7 (4%)28%NR49%, D/C; 34%, still hospitalized17%
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      Wuhan, ChinaPatients admitted with COVID-19 pneumonia to Wuhan Infectious Disease Hospital 1/31/20-2/20/201,1905746.6%26.1%2.6%12.2%151 (4.3%)NR19.2%NR86.8%, distinction NR13.2%
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      New Orleans, USAPatients with COVID-19 admitted to Ochsner Medical Center 3/1/20-3/31/20575; (ICU: 173)6545.7%73.7%29.9%48.9%1, de novo AKI; 1.6, prior CKDTotal: 161 (28%); stage 1: 30 (5%); stage 2: 25 (5%); stage 3: 106 (18%); ICU: 105; non-ICU:5689 (15%); ICU: 77; non-ICU: 1230%65%50%, D/C or still hospitalized (distinction NR)50%
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      Note: Disease severity is reported according to the classification used in each study, which is based on the classification scheme of the World Health Organization.
      Abbreviations: AKI, acute kidney injury; ARDS, acute respiratory distress syndrome; CKD, chronic kidney disease; COVID-19, coronavirus disease 2019; D/C, discharged; DM, diabetes mellitus; ED, emergency department; ESKD, end-stage kidney disease; HTN, hypertension; ICU, intensive care unit; KDIGO, Kidney Disease: Improving Global Outcomes; KRT, kidney replacement therapy; NR, not reported; Scr, admission serum creatinine [mean (median) unless otherwise specified].
      a Age is reported as mean, unless italicized (median); Scr is reported as mean, unless otherwise specified or italicized (median).
      b All AKI was reported according to the KDIGO AKI criteria, but not all studies reported AKI stages.
      Kidney Disease: Improving Global Outcomes (KDIGO) Acute Kidney Injury Work Group
      KDIGO clinical practice guideline for acute kidney injury.
      c Denominator is all patients included in each study.
      d Among 850 patients with available data.
      e Renal outcomes reported for only 375 patients.
      f Only KRT reported.
      g Some patients receiving KRT may have been maintenance dialysis patients, but not reported by the authors.
      Table 2Summary of AKI Events
      CharacteristicAKIKRT
      No. of studies5449
       Pooled prevalence (95% CI)28% (22%-34%)9% (7%-11%)
      Kidney events in patients admitted to an ICU
       Pooled prevalence (95% CI)46% (35%-57%)19% (15%-22%)
      Kidney events in patients admitted to a non-ICU setting
       Pooled prevalence (95% CI)12% (6%-19%)1% (0%-3%)
      Abbreviations: AKI, acute kidney injury; ICU, intensive care unit; KRT, kidney replacement therapy.

      Outcomes

      Data for AKI were available for 30,639 patients (n = 54 studies) and data for the receipt of KRT were available for 27,525 patients (n = 48 studies; Table 2). We were able to determine the indication for the initiation of KRT in only 3
      • Arentz M.
      • Yim E.
      • Klaff L.
      • et al.
      Characteristics and outcomes of 21 critically ill patients with COVID-19 in Washington State.
      ,
      • Goyal P.
      • Choi J.J.
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      • et al.
      Clinical characteristics of Covid-19 in New York City.
      ,
      • Cummings M.J.
      • Baldwin M.R.
      • Abrams D.
      • et al.
      Epidemiology, clinical course, and outcomes of critically ill adults with COVID-19 in New York City: a prospective cohort study.
      of the 48 studies. For the entire hospitalized population, the pooled prevalence of AKI was 28% (95% CI, 22%-34%; I2 = 99%), and the pooled prevalence of receipt of KRT was 9% (95% CI, 7%-11%; I2 = 97; Figs 1 and 2).
      Figure thumbnail gr1
      Figure 1Pooled prevalence of acute kidney injury among all patients with coronavirus disease 2019 (COVID-19) using a random-effects model.
      Figure thumbnail gr2
      Figure 2Pooled prevalence of kidney replacement therapy among all patients with coronavirus disease 2019 (COVID-19) using a random-effects model.

      Subgroup Analysis

      In subgroup analysis, data were available to report outcomes only for patients admitted to an ICU or non-ICU setting, and AKI severity.

      ICU Versus Non-ICU Setting

      Of the 9,650 patients admitted to an ICU, ascertainment of AKI and receipt of KRT were feasible for only 8,086 and 6,618 patients, respectively (n = 25 studies for AKI; n = 23 studies for KRT). The pooled prevalence of AKI and KRT for patients receiving care in an ICU was 46% (95% CI, 35%-57%; I2 = 99%) and 19% (95% CI, 15%-22%; I2 = 88%), respectively (Fig S2).
      Among the 15,728 patients who did not receive care in an ICU, the presence of AKI could be ascertained in 7,799 patients (9 studies), and the receipt of KRT, in 3,745 patients (8 studies). The pooled proportion of AKI and KRT in non-ICU patients was 12% (95% CI, 6%-19%; I2 = 98%) and 1% (95% CI, 0%-3%; I2 = 88%), respectively (Fig S3). There was a significant difference in risk for AKI and KRT between patients admitted versus those not admitted to the ICU (P < 0.001 for AKI; P < 0.001 for KRT).

      AKI Severity

      Thirteen studies (n = 6,211 patients) reported on the severity of AKI by KDIGO stage. The pooled prevalence of stage 1 AKI was 44% (95% CI, 38%-50%; I2 = 94%), stage 2 AKI was 19% (95% CI, 17%-22%; I2 = 76%), and stage 3 AKI was 34% (95% CI, 28%-40%; I2 = 94%; Fig S4).

      Discussion

      In this systematic review and meta-analysis of 54 studies, we found that AKI occurred in ∼30% of patients hospitalized with COVID-19. AKI complicated the course of >45% of patients requiring ICU care, and 1 in 5 patients admitted to the ICU received KRT. Because COVID-19 is expected to remain a public health threat for the foreseeable future and disease surges are anticipated, our data provide important information for clinicians caring for hospitalized patients and administrators who need to marshal KRT resources.
      A previous worldwide meta-analysis of 154 studies using KDIGO AKI criteria in patients without COVID-19 reported a pooled incidence rate of 21.6% (95% CI, 19.3%-24.1%), which increased to 31.7% (95% CI, 28.6%-35.0%) in a critical care setting.
      • Hoste E.A.
      • Bagshaw S.M.
      • Bellomo R.
      • et al.
      Epidemiology of acute kidney injury in critically ill patients: the multinational AKI-EPI study.
      Approximately 10% of patients with AKI received KRT (2% of all patients). In other prospective studies of critically ill patients, between 15% and 30% of patients with AKI received KRT (5%-15% of all patients).
      • Bouchard J.
      • Acharya A.
      • Cerda J.
      • et al.
      A prospective international multicenter study of AKI in the intensive care unit.
      • Hoste E.A.
      • Bagshaw S.M.
      • Bellomo R.
      • et al.
      Epidemiology of acute kidney injury in critically ill patients: the multinational AKI-EPI study.
      • Prescott G.J.
      • Metcalfe W.
      • Baharani J.
      • et al.
      A prospective national study of acute renal failure treated with RRT: incidence, aetiology and outcomes.
      Therefore, our reported overall AKI prevalence of 28% in hospitalized patients with COVID-19 is consistent with this prior work, but the rate of AKI in critically ill patients is higher. We also identified more use of KRT in COVID-19–associated AKI. These findings are driven primarily by data from the United States and Europe because most of the studies from China reported less overall AKI and use of KRT, which has been described previously in patients without COVID-19.
      • Susantitaphong P.
      • Cruz D.N.
      • Cerda J.
      • et al.
      World incidence of AKI: a meta-analysis.
      ,
      • Bouchard J.
      • Acharya A.
      • Cerda J.
      • et al.
      A prospective international multicenter study of AKI in the intensive care unit.
      ,
      • Yang L.
      • Xing G.
      • Wang L.
      • et al.
      Acute kidney injury in China: a cross-sectional survey.
      These differences could be explained in part by underrecognition of AKI stemming from differences in the frequency of kidney function measurement, as well as KRT resource limitations and practice pattern variation in the initiation of KRT among different centers.
      • Mehta R.L.
      • Burdmann E.A.
      • Cerda J.
      • et al.
      Recognition and management of acute kidney injury in the International Society of Nephrology 0by25 Global Snapshot: a multinational cross-sectional study.
      These data suggest that COVID-19–associated AKI contributes to a more severe AKI phenotype, and higher rates of KRT should spur further investigation into the mechanisms underlying this complication. Commonly cited hypotheses include a hypercoagulable state and direct viral invasion related to angiotensin-converting enzyme 2 expression on the proximal tubule,
      • Batlle D.
      • Soler M.J.
      • Sparks M.A.
      • et al.
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      ,
      • Ye M.
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      • William J.
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      • Cokic I.
      • Batlle D.
      Glomerular localization and expression of angiotensin-converting enzyme 2 and angiotensin-converting enzyme: implications for albuminuria in diabetes.
      ,
      • Farkash E.A.
      • Wilson A.M.
      • Jentzen J.M.
      Ultrastructural evidence for direct renal infection with SARS-CoV-2.
      supported by small autopsy studies that demonstrated severe proximal tubule injury, peritubular erythrocyte aggregation, glomerular fibrin thrombi, and even collapsing glomerulopathy in a subset of patients.
      • Su H.
      • Yang M.
      • Wan C.
      • et al.
      Renal histopathological analysis of 26 postmortem findings of patients with COVID-19 in China.
      ,
      • Diao B.
      • Wang C.
      • Wang R.
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      Notably, pigment casts were present in these reports, suggesting some degree of inflammation and acute tubular necrosis, which is a common cause of AKI in patients with multiorgan failure that is compounded by intravascular volume depletion and mechanical ventilation.
      • Darmon M.
      • Clec’h C.
      • Adrie C.
      • et al.
      Acute respiratory distress syndrome and risk of AKI among critically ill patients.
      Our data also give health care providers and administrators estimates of KRT capacity needed in future COVID-19 surges. This planning involves considering human resources (ie, nurses), equipment availability (ie, KRT machines and reverse osmosis devices), disposables (ie, filters, dialysate, and anticoagulation), and protocol development for other acute dialysis modalities (ie, sustained low efficiency dialysis and/or acute peritoneal dialysis) in case continuous kidney replacement therapy resources become overwhelmed.
      • Goldfarb D.S.
      • Benstein J.A.
      • Zhdanova O.
      • et al.
      Impending shortages of kidney replacement therapy for COVID-19 patients.
      ,
      • Burgner A.
      • Ikizler T.A.
      • Dwyer J.P.
      COVID-19 and the inpatient dialysis unit.
      ,
      • El Shamy O.
      • Patel N.
      • Abdelbaset M.H.
      • et al.
      Acute start peritoneal dialysis during the COVID-19 pandemic: outcomes and experiences.
      In patients with AKI who survive their COVID-19, there will be increased risks for rehospitalization, recurrent AKI, cardiovascular complications, and death that mostly occur within the first year after hospitalization.
      • Silver S.A.
      • Siew E.D.
      Follow-up care in acute kidney injury: lost in transition.
      Current after-care programs for survivors of COVID-19 focus mainly on respiratory and mental health, and the high rates of AKI reported here suggest that kidney monitoring should also be incorporated.
      The strengths of our systematic review include the use of a comprehensive search strategy that incorporated pre-prints and careful identification of duplicate studies. Some of the studies still temporally overlapped in setting and location, and we included only the most complete reports to avoid double counting. We also ascertained all AKI episodes according to KDIGO criteria.
      This study has some limitations. First, there was significant heterogeneity among the included studies that remained unaccounted for in subgroup analysis. Factors that may have contributed to heterogeneity included baseline kidney function ascertainment, hospital setting, and hospital policies. For example, AKI could be underreported in hospitals with less frequent kidney function measurement, and criteria for hospital/ICU admission and KRT initiation are determined locally.
      In addition, most studies only reported the presence of AKI based on KDIGO criteria (ie, yes/no) and few provided data on the severity of AKI by KDIGO stage. However, we estimated the point prevalence of each KDIGO AKI stage among studies reporting these data, as well as the use of KRT, which is a marker of severe AKI. Second, detailed information on the subset of patients who received KRT, including modality and prescription used, was limited; therefore, the optimal method of KRT delivery remains an important knowledge gap. Third, data for kidney recovery and mortality were incomplete, with many patients still hospitalized and the follow-up time too short to properly assess these outcomes. Fourth, we may have slightly overestimated KRT rates by virtue of some patients receiving KRT for end-stage kidney disease. Last, although our study included more than 30,000 patients from 54 studies, our estimates could be affected by the exclusion of 130 studies that did not report on AKI or in which KDIGO criteria were not used.
      Our systematic review and meta-analysis provides health care providers and administrators with updated and comprehensive information on the epidemiology of AKI and KRT in hospitalized patients with COVID-19. Approximately 50% of critically ill patients may experience AKI, with almost 20% of all critically ill patients receiving KRT. These data identify targets to guide adequate capacity planning in the face of future COVID-19 surges. Given the prominence of AKI and KRT in hospitalized patients with COVID-19, further work is also needed to better characterize COVID-19–associated AKI and kidney-specific treatments. Future reports should provide detailed data on AKI severity, triggers for KRT, pathology (when performed), and information on the KRT prescription (ie, modality, anticoagulation, and ultrafiltration), as well as data for mortality and kidney recovery.

      Article Information

      Authors’ Full Names and Academic Degrees

      Samuel A. Silver, MD, MSc, William Beaubien-Souligny, MD, Prakesh S. Shah, MD, MSc, Shai Harel, MD, MS, Daniel Blum, MD, Teruko Kishibe, MISt, Alejandro Meraz-Munoz, MD, Ron Wald, MDCM, MPH, and Ziv Harel, MD, MSc.

      Authors’ Contributions

      Study concept and design: RW, ZH; Acquisition, analysis, or interpretation of data: all authors; study supervision: RW, ZH. SAS and WB-S contributed equally. RW and ZH contributed equally. All authors approved the final version of the submitted manuscript. Each author contributed important intellectual content during manuscript drafting or revision and accepts accountability for the overall work by ensuring that questions pertaining to the accuracy or integrity of any portion of the work are appropriately investigated and resolved.

      Support

      Dr Silver is supported by a Kidney Research Scientist Core Education and National Training (KRESCENT) Program New Investigator Award (co-funded by the Kidney Foundation of Canada , Canadian Society of Nephrology , and Canadian Institutes of Health Research ). Dr Beaubien-Souligny is supported by the Fonds de Recherche du Québec - Santé ( FRQS ).

      Financial Disclosure

      All authors have completed the ICMJE uniform disclosure form at www.icmje.org/coi_disclosure.pdf and declare: Dr Silver has received speaking fees from Baxter Canada. Dr Wald has received unrestricted research funding and speaker fees from Baxter. The remaining authors declare that they have no relevant financial interests.

      Peer Review

      Received July 31, 2020. Evaluated by 2 external peer reviewers, with direct editorial input from the Editor-in-Chief. Accepted in revised form November 15, 2020.

      Supplementary Material

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