key: cord-0971710-xdrzu7ps
authors: Wang, Bin; Luo, Qing; Zhang, Weiguang; Yu, Shuai; Cheng, Xiaowei; Wang, Lanlan; Chen, Xiangmei; Chen, Yizhi
title: The Involvement of Chronic Kidney Disease and Acute Kidney Injury in Disease Severity and Mortality in Patients with COVID-19: A Meta-Analysis
date: 2020-12-22
journal: Kidney Blood Press Res
DOI: 10.1159/000512211
sha: 55a0a35a43e4b1990ecd393e64094da6a81a19fe
doc_id: 971710
cord_uid: xdrzu7ps

BACKGROUND: A meta-analysis was performed to evaluate the association of chronic kidney disease (CKD) and acute kidney injury (AKI) with the clinical prognosis of patients with coronavirus disease 2019 (COVID-19). METHODS: The PubMed, EMBASE, Cochrane Library, medRxiv, Social Science Research Network, and Research Square databases (from December 1, 2019 to May 15, 2020) were searched to identify studies that reported the associations of CKD/AKI and disease severity/mortality. Pooled odds ratios (ORs) and 95% confidence intervals (CIs) were calculated and meta-regression was performed. RESULTS: In total, 42 studies enrolling 8,932 participants were included in this meta-analysis. The quality of most included studies was moderate to high. Compared with patients without previously diagnosed CKD, those with CKD had a significantly increased risk of progressing to a severe condition (OR 2.31, 95% CI 1.64–3.24) or death (OR 5.11, 95% CI 3.36–7.77). Similarly, compared with patients without AKI, those with AKI had a significantly increased risk of progressing to a severe condition (OR 11.88, 95% CI 9.29–15.19) or death (OR 30.46, 95% CI 18.33–50.59). Compared with patients with previously diagnosed CKD, those with AKI were more likely to progress to a severe condition (pgroup < 0.001, I(2) = 98.3%) and even to death (pgroup < 0.001, I(2) = 96.5%). Age had a significant impact on the association between CKD and disease severity (p = 0.001) but had no impact on the associations between AKI and disease severity (p = 0.80), between CKD and mortality (p = 0.51), or between AKI and mortality (p = 0.86). Four important complications (cardiac injury, shock, acute respiratory distress syndrome, and liver injury) did not significantly affect the associations between CKD/AKI and disease severity/mortality, indicating that CKD/AKI may be independent clinical prognostic indicators for patients with COVID-19. CONCLUSIONS: In COVID-19 patients, CKD/AKI was associated with worse outcomes compared with those without CKD/AKI. AKI was associated with higher risks of severity and mortality than CKD.

Since December 2019, a severe pneumonia outbreak caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has spread rapidly around the world [1] . On February 11, 2020 the World Health Organization declared the name of the pandemic condition to be coronavirus disease 2019 .

In patients with severe COVID-19, the infection may rapidly progress to hypoxemia, septic shock, acute respiratory distress syndrome (ARDS), need for intensive care unit (ICU) care, and even death. Recently, several reports have revealed that comorbidities or other conditions can affect the clinical progression of patients with COVID-19 [2, 3] . Several meta-analyses have demonstrated the impact of diabetes [4] , cardiac injury [5, 6] , and chronic obstructive pulmonary disease and smoking [7] on the clinical progression of patients with COVID-19.

A meta-analysis reported that the incidence of acute kidney injury (AKI) was estimated to be 3% in hospitalized patients with COVID-19, while this incidence was increased to 19% in patients admitted to an ICU [8] . Serum creatinine levels ≥133 μmol/L were reported to be associated with disease severity in a meta-analysis (three studies enrolling 979 patients) [9] . Another meta-analysis (three studies enrolling 944 patients) reported that AKI was associated with a higher risk of mortality [10] . However, the number of studies included in these published meta-analyses was relatively small. During the past half year, numerous new studies evaluating the association of chronic kidney disease (CKD)/AKI and disease severity/ mortality have been published. Therefore, a systematic review of the accumulated evidence with the aim of providing an up-to-date assessment of the association between kidney impairment (CKD/AKI) and clinical prognosis (disease severity/mortality) in patients with COV-ID-19 is important.

This meta-analysis was performed in accordance with the Meta-Analysis of Observational Studies in Epidemiology (MOOSE) method [11] . The MOOSE checklist is provided in online supplementary Table S1 (for all online suppl. material, see www.karger. com/doi/10.1159/000512211). The databases (MEDLINE, Embase, and Cochrane Library) were systematically searched for eligible published studies, with the medRxiv, Social Science Research Network, and Research Square websites searched for eligible unpublished studies from December 1, 2019 to May 15, 2020. The key words "COVID-19," "2019 novel coronavirus infection," "corona-virus disease 2019," "coronavirus," "SARS-CoV-2," "2019-nCoV," "mortality," "severe," "survival," "outcomes," "prognosis," "chronic kidney disease," "acute renal failure," "acute kidney injury," and "renal replacement therapy" were used in various combinations.

After candidate articles had been collected, further selection was conducted according to the following inclusion criteria: (1) Adult patients. (2) The numbers of patients who were diagnosed with CKD or AKI were reported or could be calculated. In the absence of explicit definitions of CKD or AKI in the included studies, patients with high serum creatinine before or on admission were considered to be diagnosed with CKD (meeting the diagnostic criteria of the Kidney Disease: Improving Global Outcomes [KDIGO] guidelines) [12] , while patients who had an increase in serum creatinine (meeting the diagnostic criteria of the KDIGO guidelines [12] ) after SARS-CoV-2 infection were considered to have AKI. The definition of AKI was the same as that in the KDIGO guidelines. Patients with both preexisting CKD before infection and an increase in serum creatinine after infection were still considered to be diagnosed with CKD, but not AKI, during data extraction and synthesis. (3) The primary outcomes were disease severity and mortality. Diagnosis of the severe cases was defined by the authors in each individual study. Most of the included studies defined severe cases as ICU admission, mechanical ventilation, or both. In the absence of an explicit definition of severe cases, the guidelines for the diagnosis and treatment of SARS-CoV-2 issued by the National Health Commission of China (sixth edition) were used [13] . In detail, severe cases were defined as patients with dyspnea, respiratory rate ≥30/min, blood oxygen saturation ≤93%, partial pressure of arterial oxygen to fraction of inspired oxygen ratio < 300, lung infiltrates > 50% within 24-48 h, or needing ICU care. (4) The patients were to be consecutively confirmed and enrolled. The studies were in the following cases: (1) reviews, editorials, conference abstracts, systematic reviews, and meta-analyses;

(2) children < 18 years old; (3) insufficient data provided to explore the associations between kidney impairment and the clinical outcomes; (4) repeated or updated reports containing or overlapping with the same group of participants.

The extracted data included publication status, study type, regions/countries, enrollment hospitals and departments, enrollment periods, numbers of patients, age, sex, complications (cardiac injury, ARDS, shock, and liver injury), and treatment strategies. Quality assessment of the studies was conducted using the Newcastle-Ottawa Scale (NOS) for all included studies [14] . Eight different domains, including selection bias (adequate case definition, representativeness of the cases, selection of controls, and definition of controls), comparability (comparability of cases and controls on the basis of the design or analysis), and exposure (ascertainment of exposure, same method of ascertainment for cases and controls, and reports of nonresponse rate) were assessed. The total scores for each included study ranged from 0 to 10 points. These scores were chosen a priori to simplify description for the present review.

Dichotomous variables were expressed as odds ratio (OR) and 95% confidence interval (CI). Heterogeneity was assessed using the Q test and quantified using the I 2 statistic [15] . The threshold p value of heterogeneity was 0.10. I 2 statistics < 25%, 25-49%, 50-75%, and > 75% were interpreted to indicate low, medium, high, and very high levels of heterogeneity, respectively. If the I 2 value was < 50%, the fixed-effect model was used. Otherwise, the random-effects model was used. For subgroup difference analysis, the I 2 value indicated the percentage of the variability in effect estimates from the different subgroups that is due to genuine subgroup differences rather than sampling error. Publication bias was explored using a funnel plot if more than 10 studies were included. Subgroup analyses were performed to evaluate whether the results differed according to the location of the studies (Wuhan city or non-Wuhan regions) and the publication status (published or unpublished). Meta-regression was performed to investigate the effects of age and complications such as cardiac injury, ARDS, shock, and liver injury on the relationship between kidney impairment and clinical prognosis. The Review Manager (version 5.3, The Cochrane Collaboration) software was used for data synthesis and publication bias. The STATA 14.0 (StataCorp, College Station, TX, USA) software was used for meta-regression. The searching and selection of the studies, data extraction and quality assessment, data synthesis, and statistical analysis were performed indepen-dently by two of the researchers (B. Wang and Q. Luo), and any discrepancies were resolved by consulting a third investigator (Y. Chen).

A total of 1,724 papers were screened, and finally 42 studies with 8,932 participants were included in this meta-analysis. Eighteen of the 42 studies were published [16] [17] [18] [19] [20] [21] [22] [23] [24] [25] [26] [27] [28] [29] [30] [31] [32] [33] , and the remaining 24 studies were rapidly posted on the medRxiv, Social Science Research Network, and Research Square websites without peer review . A flow diagram outlining the literature search process is provided in Figure 1 . The characteristics of the included studies are presented in Table 1 . The median number of participants was 147 (range 16-1,000). Twelve studies used mortality as the primary outcome, 29 studies used disease severity as the primary outcome, and 1 study used both disease severity and mortality as the primary outcomes. Five studies were performed outside China (2 in the United States [16, 38] , 1 in Italy [20] , 1 in Switzerland [56] , and 1 in Saudi Arabia [40] ). The remaining 37 studies were conducted in China (22 in Wuhan City and 15 in non-Wuhan regions). In the studies conducted in China and Saudi Arabia, severe disease was defined by the National Health Commission of China criteria [13] . In the Italian study, severe disease was defined as a requirement for high-flow oxygen support. In the study conducted in Switzerland, severe disease was defined as the requirement for mechanical ventilation. For the studies conducted in the United States, severe disease was defined as the need for mechanical ventilation or ICU admission. Twenty-two of the included studies were performed in Wuhan city. Among them, 2 studies were conducted in two different departments with different enrollment periods (surgery department until December 31 [21] and respiratory department from December 26 to January 31 [52] ) in the same hospital (Wuhan Jinyintan Hospital). Two studies were conducted in two different departments with overlapping enrollment periods (respiratory department from January 1 to February 15 [53] and infectious disease department from January 16 to February 3 [30] ) in the same hospital (Seventh Hospital of Wuhan City). Three studies were conducted in three different departments with similar enrollment periods (infectious disease department from January 13 to February 12 [19] , neurology department from January 10 to February 12 [22] , and endocrinology department from January 10 to February 24 [28] ) in the same hospital (Wuhan Tongji Hospital). Four studies were conducted in three different departments with similar enrollment periods (ICU department from January 1 to January 28 [26] , ICU department until February 10 [27] , cardiology department from January 3 to February 1 [17] , and respiratory department from January 2 to February 10 [29] ) in the same hospital (Wuhan University Zhongnan Hospital). The remaining 11 studies were conducted in different hospitals.

Twenty-eight studies had NOS points ranging from 6 to 7 (13 studies scored 6 points and 15 studies scored 7 points), 14 studies had NOS points > 7 (8 studies scored 8 points and 6 studies scored 9 points), and no included study had < 6 points (online suppl. Table S2 ).

A total of 27 studies with 5,155 patients reported an association between previously diagnosed CKD and disease severity (Fig. 2A) . The overall prevalence of CKD was 3.03% (155/5,115) in all included studies. Compared with COVID-19 patients without previously diagnosed CKD, those with previously diagnosed CKD had a significantly increased risk of progressing to a severe condition (OR = 2.31, 95% CI 1.64-3.24, p < 0.001, I 2 = 13%, p heterogeneity = 0.27). Eighteen studies with 3,850 patients reported an association between AKI and disease severity ( Fig. 2A) . The overall incidence of AKI was 14.68% (565/3,850) in all included studies. Compared with CO-VID-19 patients without AKI, those with AKI had a significantly increased risk of progressing to a severe condition (OR = 11.88, 95% CI 9.29-15.19, p < 0.001, I 2 = 0%, p heterogeneity = 0.55). Subgroup analysis indicated that patients with AKI were more likely to progress to a severe condition compared with patients with previously diagnosed CKD, which was demonstrated by the significant difference between the AKI and CKD groups (AKI vs. CKD: OR = 11.88, 95% CI 9.29-15.19 vs. OR = 2.31, 95% CI 1.64-3.24; p group < 0.001, I 2 = 98.3%) (Fig. 2A) . The funnel plots indicated no publication bias for the associations of CKD/AKI with disease severity (Fig. 2B, C) .

Subgroup analyses indicated that the publication status did not significantly affect the associations between CKD/ AKI and disease severity (CKD: published vs. unpublished studies: OR = 6.53, 95% CI 3.02-14.11 vs. OR = 12.74, 95% CI 9.82-16.52, p subgroup = 0.11, I 2 = 61.5%) (online suppl. Fig. S1A, S1B) . Similarly, subgroup analyses revealed that the geographic region did not significantly affect the associations of CKD/AKI with disease severity (CKD: Wuhan City vs. non-Wuhan regions: OR = 2.40, 95% CI 1.43-4.01 vs. OR = 2.23, 95% CI 1.41-3.51, p subgroup = 0.83, I 2 = 0%; AKI: OR = 11.67, 95% CI 6.90-19.73 vs. OR = 11.95, 95% CI 9.06-15.77, p subgroup = 0.94, I 2 = 0%) (online suppl. Fig. S2A, S2B) . Neither the publication status nor the geographic region had an influence on the associations of CKD/AKI with disease severity.

Eleven studies with 2,140 participants reported an association between previously diagnosed CKD and disease mortality (Fig. 3A) . The overall prevalence of CKD was 6.73% (144/2,140) in all included studies. Compared with COVID-19 patients without previously diagnosed CKD, those with previously diagnosed CKD had a significantly increased risk of death (OR = 5.11, 95% CI 3.36-7.77, p < 0.001, I 2 = 0%, p heterogeneity = 0.68). Six studies with 1,220 patients reported an association between AKI and disease mortality. The incidence of AKI was 13.28% (162/1,220) in all included studies. Compared with COVID-19 patients without AKI, those with AKI had a significantly increased risk of death, with medium heterogeneity (OR = 30.46, 95% CI 18.33-50.59, p < 0.001, I 2 = 42%, p heterogeneity = 0.12) (Fig. 3A ). Subgroup analysis indicated that patients with AKI were more likely to die than patients with previously diagnosed CKD, which was demonstrated by the significant difference between the AKI and CKD groups (AKI vs. CKD: OR = 30.46, 95% CI 18.33-50.59 vs. OR = 5.11, 95% CI 3.36-7.77, p group < 0.001, I 2 = 96.5%) (Fig. 3A) . The funnel plot indicated no publication bias for the associations of CKD with disease mortality (Fig. 3B) . Publication bias was not explored for the association of AKI and mortality because the number of included studies was < 10.

Subgroup analysis indicated that the publication status did not significantly affect the association between CKD and disease mortality (published vs. unpublished studies: OR = 4.77, 95% CI 1.93-11.77 vs. OR = 5.21, 95% CI 3.25-8.36, p subgroup = 0.87, I 2 = 0%) (online suppl. Fig. S3A ). However, subgroup analysis revealed that the publication status had a significant impact on the association of AKI with disease mortality (published vs. unpublished studies: OR = 86. 13 Fig. S3B ). The subgroup analyses to explore the impact of geographic region on the association of CKD/AKI with disease mortality were not performed because all the included studies were conducted in Wuhan City.

Meta-regression analysis indicated that age had a significant impact on the association between CKD and disease severity (p = 0.001) (Fig. 4A) . However, meta-regression analyses indicated that age did not significantly affect the associations between AKI and disease severity (p = 0.80) (Fig. 4B) , between CKD and mortality (p = 0.51) (Fig. 4C) , or between AKI and mortality (p = 0.86) (Fig. 4D ). Metaregression analyses indicated that four important complications (cardiac injury, shock, ARDS, and liver injury) did not significantly affect the associations between CKD/AKI and disease severity/mortality ( Table 2 ).

We provide an up-to-date analysis of the evidence regarding the associations of CKD/AKI with clinical prognosis in patients with COVID-19 (42 studies with 8,932 patients). We demonstrated that COVID-19 patients with previously diagnosed CKD or AKI had significantly increased risks of progression to a severe condition and even death. Compared with patients with previously diagnosed CKD before SARS-CoV-2 infection, patients with AKI after SARS-CoV-2 infection were more likely to progress to a severe condition or death.

Since the outbreak of the COVID-19 epidemic, several meta-analyses concerning kidney impairment and clinical prognosis have been published. Ng et al. [8] reported that the overall risk of AKI in hospitalized patients was 3% and that this risk increased to 19% when patients were admitted to an ICU. Zheng et al. [9] found that serum creatinine could impact the risk of progression of COVID-19. Ali et al. [10] revealed that severe AKI was associated with a higher risk of mortality (relative risk = 3.08, 95% CI 1.54-6.19). Potere et al. [58] reported that the incidence of AKI was 6% in hospitalized patients. Lim et al. [59] demonstrated that AKI was associated with increased mortality, severe condition, and the need for ICU care. In our study, we demonstrated that not only previously diagnosed CKD but also AKI significantly affected the disease severity and mortality of COVID-19. We also found that AKI was associated with a more severe condition and a higher risk of mortality than CKD. Four major complications (cardiac injury, ARDS, shock, and liver injury) did not participate substantially in the associations between CKD/AKI and clinical prognoses, indicating that kidney impairment may be an independent clinical prognostic indicator for these patients.

The reason why COVID-19 patients with CKD comorbidity exhibited an increased risk of progression to a severe condition or death has not been fully elucidated to date. Plausible explanations are as follows: (1) Patients with CKD have a proinflammatory milieu and functional defects in innate and adaptive immune cell populations [60] . In a community-based cohort of nearly 10,000 adult individuals, reduced glomerular filtration rate and elevated albumin-creatinine ratios were associated with a higher risk of hospitalization, with infection and subsequent mortality [61] . (2) Patients with CKD have a high risk of upper respiratory tract infection and pneumonia [62, 63] , which may become important concurrent infections with SARS-CoV-2. (3) CKD frequently coexists with comorbidities, especially diabetes and cardiovascular disease, which are also known to be associated with worse outcomes in patients with COVID-19 [9] . (4) CKD prevalence rises with age, and the burden of COVID-19 morbidity and mortality is heavily concentrated in older age groups. An important limitation of the present study is that we were unable to determine the extent to which age and comorbidities independently contribute to poor outcomes in patients with CKD.

AKI is a syndrome of abrupt loss of kidney function that is strongly associated with increased mortality and morbidity in several conditions [64] . There is a high incidence of AKI in patients with COVID-19, especially in the cohort with severe disease [46, 49, 65] . The following reasons have been postulated to explain why an increased incidence of AKI occurs after SARS-CoV-2 infection: (1) The severity of the disease may be associated with an increase in the initial renal viral load or severe systemic inflammation, or both. SARS-CoV-2 can penetrate cells via two receptors -angiotensin-converting enzyme 2 (ACE2) and transmembrane protease, serine 2 (TMPRSS2) [66] -, and ACE2 is highly expressed in proximal tubular epithelial cells and in podocytes. Nine of 26 autopsied Chinese patients with AKI after SARS-CoV-2 infection had diffuse proximal tubular injury, with some frank necrosis and no glomerular injury [67] . (2) The fever, vomiting, diarrhea, and shock often observed with SARS-CoV-2 infection can cause kidney hypoperfusion. These reasons may cooperatively contribute to an increased risk of AKI. Additionally, COVID-19 patients with severe conditions also have complications involving various organ dysfunctions, which may in turn lead to AKI.

This meta-analysis has several limitations: (1) Twentytwo of the included studies were from Wuhan, China, and although it is unlikely that the same patients were included in multiple studies, the low heterogeneity in the outcome of our study may be attributable to the fact that these patients from the same region with similar genetic background were infected by the same strain of SARS-CoV-2 virus in similar periods. This may limit generalizability, although subgroup analysis showed that the association with CKD/AKI and disease severity was consistent between studies from China and outside China.

(2) Half of the included studies were posted on academic websites and were not peer-reviewed, and subgroup analysis demonstrated that the impact of AKI on the mortality in published studies was significantly higher than that in unpublished studies. This significant subgroup difference indicated the existence of publication bias. (3) The comparability of the baseline characteristics between the two groups (severe/nonsevere, survivors/deaths) was not well matched in a majority of studies, indicating that residual confounding is likely.

In conclusion, not only previously diagnosed CKD before SARS-CoV-2 infection, but also AKI after SARS-CoV-2 infection were associated with disease severity and mortality. AKI had a higher risk of disease progression and death compared with CKD.

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