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Medicine Services, Landspitali University Hospital, Reykjavik, Iceland and 3Faculty of Medicine, ... ICUs of Landspitali – The National University Hospital of.
Acta Anaesthesiol Scand 2012; 56: 1291–1297 Printed in Singapore. All rights reserved

© 2012 The Authors Acta Anaesthesiologica Scandinavica © 2012 The Acta Anaesthesiologica Scandinavica Foundation ACTA ANAESTHESIOLOGICA SCANDINAVICA

doi: 10.1111/j.1399-6576.2012.02767.x

Acute kidney injury in intensive care units according to RIFLE classification: a population-based study M. I. Sigurdsson1, I. O. Vesteinsdottir1,3, K. Sigvaldason1, S. Helgadottir1, O. S. Indridason2 and G. H. Sigurdsson1,3 1 Department of Anaesthesia & Intensive Care Medicine, Landspitali University Hospital, Reykjavik, Iceland, 2Division of Nephrology, Internal Medicine Services, Landspitali University Hospital, Reykjavik, Iceland and 3Faculty of Medicine, University of Iceland, Reykjavik, Iceland

Introduction: Recent studies of the incidence of acute kidney injury (AKI) are largely based on estimated baseline serum creatinine values. The aim of this study was to more accurately determine the incidence of AKI using the RIFLE criteria for intensive care unit (ICU) patients of a whole population. Materials and methods: All adult patients admitted to the ICUs of Landspitali – The National University Hospital of Iceland in 2007 (n = 1026) were studied with meticulous search for baseline creatinine. The underlying risk factors and contributing causes for AKI were defined, and survival and ratio of end-stage renal failure evaluated. Results: A measured baseline creatinine value was found for all but two patients with AKI. The incidence of AKI according to RIFLE criteria was 21.7% [95% confidence interval (CI): 19.0– 24.1%], with 7.1% (95 CI: 5.6–8.9%), 6.8% (95 CI: 5.3–8.5%) and 7.8% (95 CI: 6.2–9.6%) in the risk, injury and failure subgroups. Using estimated baseline creatinine overestimated the incidence

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cute kidney injury (AKI) is a common and a serious problem in intensive care units (ICUs).1–3 Patients with AKI stay longer in ICUs and have higher morbidity and mortality than patients who do not have AKI.1 In addition, patients with AKI put high demands on ICU resources, increasing the cost of treatment considerably.4 Until recently, the different definitions of acute kidney failure have resulted in difficulties in comparing its incidence and severity in different centres and countries.2,5,6 In 2004, the Acute Dialysis Quality Initiative (ADQI) published the RIFLE classification using elevation in serum creatinine (SCr), decrease in estimated glomerular filtration rate and urinary output from baseline to define AKI and classify patients based on the severity of AKI.7 The immediate classification has three groups of short-term kidney injury: risk (R), injury (I) and failure (F). According to the creatinine-based classification,

of AKI by 3.5%. The sensitivity and specificity of the RIFLE criteria using estimated baseline creatinine were 76% and 95%. Renal replacement therapy was required for 17% of the AKI patients. One year survival of AKI patients was 51%, but only 2.5% of patients surviving 90 days required chronic renal replacement therapy. Conclusions: The incidence of AKI in the ICU was lower than previously published, perhaps due to overestimation of AKI using estimated baseline creatinine or bias from tertiary referrals. AKI patients have high mortality, but the survivors have a low incidence of end-stage renal failure. Accepted for publication 31 July 2012 © 2012 The Authors Acta Anaesthesiologica Scandinavica © 2012 The Acta Anaesthesiologica Scandinavica Foundation

patients in the risk subgroup have creatinine values elevated 1.5-fold from baseline, in the injury subgroup creatinine values are twofold elevated from baseline, and in the failure subgroup creatinine values are either threefold elevated or above 354 mmol/L, with an elevation of more than 44 mmol/L. In 2007, the Acute Kidney Injury Network (AKIN) published a modification of the RIFLE classification of AKI, including patients with elevation of creatinine of more than 27 mmol/L from baseline into class 1 AKI, and moving any patient requiring renal replacement therapy into stage 3 AKI.5 The RIFLE classification has been used to evaluate the incidence and outcome of AKI among several patient groups, and predicts mortality and morbidity associated with AKI.1,2,6,8 The incidence of AKI among intensive care patients according to the RIFLE or the AKIN classification has been published

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in several studies. Ostermann and Chang studied the incidence of AKI in multiple European ICUs, and found that the incidence of the RIFLE risk, injury and failure was 17%, 11% and 8%.2 Hoste et al. similarly found that 12%, 27% and 28% of ICU patients in a tertiary academic centre fell into the risk, injury and failure RIFLE groups.1 Mandelbaum et al. applied the AKIN criteria to 19,677 patients admitted to seven ICUs in a tertiary medical centre in the United States, and found that 39%, 14% and 4% of the patients fell into AKIN risk groups 1–3.9 Two smaller prospective series have found substantial differences in the incidence of AKI, 24%10 and 66%.11 The original RIFLE classification recommends that if baseline creatinine value is unknown, a normal GFR of 75 mL/min/1.73 m2 should be assumed and the creatinine value estimated using the Modification of Diet in Renal Disease (MDRD) equation.7 This has been used in up to one half of the patient population in earlier studies of ICU patients.1,11,12 Alternatively, either the creatinine value at admission to the ICU10 or the lowest creatinine value obtained during the ICU stay9 has been used as baseline creatinine value to stage AKI. This risks overestimating the incidence of AKI in an ICU population that is likely to have elevated baseline creatinine. We sought to evaluate the incidence of AKI among ICU patients, meticulously searching for baseline creatinine levels for all patients in hospitals and healthcare centres around the country. Our hospital is the single referral centre for renal replacement therapy in Iceland and offers full ICU services. Our study is, therefore, a population-based, nationwide analysis of the incidence of AKI in the ICU.

Materials and methods The study was a retrospective analysis of all ICU admissions in 2007 at the Landspitali – The National University Hospital of Iceland (LUH). The study was approved by the hospital ethics committee and the Data Protection Authority in Iceland, and waived informed consent. The hospital has two ICUs, with an average total annual admission rate of approximately 1300 patients, serving a population of 228,203 adults in 2007. All admissions were screened and evaluated for AKI, categorising them according to the RIFLE criteria, using changes in SCr and ignoring the urine output criteria for AKI. Any patient who fell into ‘risk’, ‘injury’ or ‘failure’ category of RIFLE using changes in sCr was defined as having AKI.

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The highest creatinine value measured during the ICU stay was compared with a creatinine value from the same patient at baseline. Baseline creatinine values were found by searching the database of the clinical laboratory services at LUH, serving both the hospital and multiple primary healthcare centres. If no baseline creatinine value existed at LUH, the databases of other healthcare institutions in Iceland were searched for creatinine values obtained before the admission to the hospital. If an SCr value within a year before the admission to the ICU was available in the hospital or primary care databases, it was used as baseline value (n = 806). If there was no such information, the lowest creatinine value after discharge from the ICU was used as a baseline value (n = 4). Finally, when no reliable baseline values were obtainable, the baseline SCr value was calculated from the MDRD equation according to suggestions by the ADQI group (n = 202).7 When analysing the sensitivity, specificity, and the positive and negative predictive values of the RIFLE criteria without measured baseline creatinine, all patients without measurements of baseline creatinine were excluded from the analysis. The hospital records of all patients diagnosed with AKI in the ICU were screened for comorbidities, such as hypertension, chronic obstructive lung disease, cardiac disease, diabetes mellitus, liver disease and recently performed surgical operations. The presence of possible causative factors of AKI was also recorded from patient charts. Information on renal replacement therapy was collected and if patients surviving 90 days needed long-term renal replacement therapy. This survival was chosen to match with the ‘end-stage’ category of the RIFLE classification. We recorded the date of death and followed surviving patients to 24 October 2011.

Statistical analysis Descriptive statistics were used to analyse the distribution into RIFLE categories according to age, the presence of risk factors, and probable causative factors for AKI and its treatment. Continuous variables were compared with either the Student’s t-test/ANOVA or Wilcoxon–Mann–Whitney Utest/Kruskal–Wallis test based on normality of the data and the number of compared groups. Categorical variables were compared with Chi-square, McNemar’s or Fisher’s exact test. We used multivariable linear regression to correct for age in the analysis of ICU days for the RIFLE subcategories. We used multivariable logistic regression to analyse factors associated with hospital mortality, adding all regis-

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tered variables to the original model and creating the finalised model with the stepwise backwards elimination of variables from the original model. We used Kaplan–Meier plots and the log–rank test to compare overall survival of the different AKI groups. Confidence interval (CI) around proportions was calculated using the Wilson method and the Hmisc package in R (The R Foundation, Vienna, Austria). A P-value less than 0.05 was considered statistically significant. All statistics and figure preparation was done in R, version 2.12.0 (The R Foundation, Vienna, Austria).

Results Incidence of AKI in ICU patients according to the RIFLE criteria A total of 1390 patients were admitted to intensive care at LUH during year 2007. Individuals under 18 years of age and readmissions were excluded, leaving 1026 patients in the study group. Of these, 14 patients had end-stage renal failure at admission and were excluded. Thus, 1012 patients were evaluated for AKI, and categorised into the risk, injury and

failure groups according to the RIFLE criteria. A total of 220 patients were found to have AKI, corresponding to 21.7% of all patients admitted to the ICU (95% CI: 19.2–24.4%). The average APACHE (Acute Physiology and Chronic Health Evaluation) II score of the AKI patients was 23 ⫾ 8 (median 22, range 7–48). The distribution of AKI into each subgroup of the RIFLE classification of AKI is shown in Fig. 1. The proportion of patients falling into the risk subgroup was 7.1% (95 CI: 5.6–8.9%), 6.8% (95 CI: 5.3–8.5%) for the injury group and 7.8% (95 CI: 6.2–9.6%) for the failure group. The mean age of patients without AKI was 59 ⫾ 18 years, compared with a mean age of 67 ⫾ 14 (P < 0.001, t-test), 65 ⫾ 18 (P = 0.01, t-test) and 67 ⫾ 16 (P < 0.001, t-test) years for patients within the risk, injury and failure subgroups, respectively. The proportion of ICU patients who developed AKI increased with higher age (Fig. 1, P < 0.001, Chi-square test), but the distribution into the risk, injury and failure subgroups did not change significantly with age (Fig. 1, P = 0.38, Chisquare test). The proportion of males was 61% of the study population and did not differ between patients with and without AKI.

Fig. 1. The absolute proportion of patients admitted to the intensive care unit (ICU) who met the RIFLE criteria for acute kidney injury, and the distribution into the risk, injury and failure subgroups. Shown is the subgroup distribution for all patients (All) as well as the distribution for different age groups. The numbers above each column show the number of patients in each group. The percentage value indicates the relative proportion of each RIFLE group within each age group.

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The effects of using estimated baseline creatinine on the incidence and classification of AKI Using estimated instead of measured baseline creatinine resulted in the diagnosis of AKI in 255 out of the 1012 patients, or 25.2% of all ICU patients (95 CI: 22.5–28.0%), an absolute overestimation of 3.5% and a relative overestimation of 16% (P < 0.001, McNemar’s test). The baseline creatinine level was available for 218 out of the 220 patients who developed AKI, and for 592 out of the 792 patients who did not develop AKI. Table 1 compares the RIFLE classification using the measured or estimated creatinine values. Overall, using estimated levels to diagnose AKI had a sensitivity of 76% (95% CI: 73–79%), specificity of 95% (95% CI: 94–97%), a positive predictive value of 88% (95% CI: 83–91%) and a negative predictive value of 90% (95% CI: 89–91%), compared with using measured baseline creatinine for RIFLE classification. Furthermore, using estimated baseline creatinine instead of measured baseline creatinine resulted in the correct RIFLE subgrouping for 82% of the patients (Table 1).

Risk factors and causes of AKI Table 2 shows the frequency of known risk factors for AKI among patients within each of the RIFLE subgroups. The median number of risk factors was one (range 0–5) and did not differ between the subcategories. The most common risk factor was ischaemic heart disease followed by hypertension (Table 2). The contributing causes to the development of AKI were also evaluated within each RIFLE subgroup (Table 2). The median number of contributing causes was one (range 0–4). The most common contributing cause was cardiogenic shock, followed by respiratory failure and post-operative complications. We did not observe a statistically significant

Table 1 Classification of intensive care unit patients into the RIFLE subgroups of AKI using either measured or estimated baseline creatinine calculated from the MDRD equation. Measured creatinine Estimated creatinine

No AKI Risk Injury Failure

No AKI

Risk

Injury

Failure

533 40 18 1

21 28 19 4

5 12 31 21

1 0 6 70

AKI, acute kidney injury; MDRD, Modification of Diet in Renal Disease.

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difference in the frequency of any contributing cause of AKI between the different RIFLE subcategories. The most common type of surgery contributing to AKI was cardiac surgery. AKI following trauma was most common after motor vehicle accidents. The use of non-steroidal anti-inflammatory drugs contributed to AKI in six patients.

Treatment Out of the 220 patients with AKI, 34 (17%) received renal replacement therapy (RRT), and one out of 792 patients without AKI. There was a significant increase in the proportion of patients receiving RRT with increased severity of AKI (0.1%, 13%, 34% and < 0.1%, 0.1%, 13% and 34% for non-AKI, risk, injury and failure groups, respectively, P < 0.001). Patients who developed AKI stayed significantly longer in the ICU [median 4 (1–108) vs. 2 (0–52) days, P < 0.001, Wilcoxon–Mann–Whitney U-test], and in a multivariable linear model of the length of ICU stay, there was an increased length of stay for the risk (three additional days, P = 0.01), injury (6 days, P < 0.001) and failure (9 days, P < 0.001) groups, compared with the group that did not get AKI after

Table 2 The frequency of comorbid diseases and the contributing causes of AKI for the risk, injury and failure subgroups of the RIFLE classification. n (%) Risk factors for AKI (median, range) Decreased eGFR Ischaemic heart disease Hypertension Diabetes mellitus, type I Diabetes mellitus, type II Chronic obstructive lung disease Liver disease Cause of AKI (median, range) Post-operative Cardiogenic shock Septic shock Hypovolemic shock Respiratory failure Trauma Medication Bleeding

Risk

Injury

Failure

72 (100) 2 [0–4]

69 (100) 1 [0–5]

79 (100) 1 [0–4]

20 37 33 1 7 25

(28) (51) (46) (1) (10) (35)

10 29 25 2 6 10

(14) (42) (36) (3) (9) (14)

23 33 32 2 14 11

(29) (42) (41) (3) (18) (14)

3 1 30 33 13 5 29 6 2 3

(4) [0–3] (42) (46) (18) (7) (40) (8) (3) (4)

3 1 23 29 20 5 22 4 7 3

(4) [0–3] (33) (42) (29) (8) (32) (6) (10) (4)

2 1 24 27 25 4 27 2 8 5

(3) [0–4] (30) (34) (32) (6) (34) (3) (10) (6)

Shown is the number of patients and percentage in parenthesis, except for the absolute number of risk factors for AKI and number of contributing causes of AKI, where median and range is shown. eGFR, estimated glomerular filtration rate; AKI, acute kidney injury.

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correcting for age. The hospital stay was similar for the AKI group and non-AKI group [median 20 (1–478) vs. 17 (2–62) days, P = 0.67].

Survival and development of end-stage kidney disease The median follow-up for patients with AKI was 11.0 months (range 0–58 months), and the median follow-up for patients without AKI was 21.4 months (range 0–58 months) (P = 0.07, Wilcoxon–Mann– Whitney U-test). Overall, the ICU mortality in the period was 9%, with increased mortality for the risk (11%), injury (39%) and failure (39%) groups compared with the group that did not develop AKI (3%) (P < 0.001, Chi-square test). If calculated instead of measured baselines creatinine was used for RIFLE classification, ICU mortality would be 11%, 24% and 38% for the risk, injury and failure groups, respectively. The hospital mortality was similarly increased for the risk (26%), injury (51%) and failure (51%) groups compared with the group that did not develop AKI (9%) (P < 0.001, Chi-square test). Using calculated creatinine for RIFLE classification would result in hospital mortality of 20%, 38% and 49% for the risk, injury and failure groups, respectively. In a logistic regression model of hospital mortality in the AKI group, there were increased odds of hospital mortality for patients within the injury (odds ratio (OR) 3.73, 95% CI: 1.56–8.93, P = 0.003) and failure (OR 4.45, 95% CI: 1.88–10.54, P = 0.001) groups compared with the risk group (OR 1.00, reference), even after correcting for age (OR 1.03, 95% CI: 1.00–1.05, P = 0.02), risk factors of AKI and the contributing cause of AKI, such as cardiogenic shock (OR 3.68, 95% CI: 1.81–7.48, P = 0.002) and post-operative AKI (OR 0.31, 95% CI: 0.15–0.66, P = 0.003). Figure 2 shows the 1-year survival of the ICU patients based on their RIFLE criteria. Survival was significantly decreased in patients with AKI compared with patients without AKI (P < 0.001, log– rank test). Survival at 1 year was 84% (95% CI: 82–87%) for the group without AKI, 63% (95% CI: 53–76%) for the risk subgroup, 45% (95% CI: 35%– 58%) for the injury subgroup and 45% (95% CI: 35%–58%) for the failure subgroup of AKI, and was similar using calculated creatinine for RIFLE classification (data not shown). Only three (2.5%) out of the 119 patients who developed AKI and survived for more than 90 days required chronic renal replacement therapy for endstage kidney disease, one patient in each of the RIFLE groups.

Fig. 2. Kaplan–Meier plot of the 1-year survival of patients admitted to Icelandic intensive care units based on the RIFLE criteria for acute kidney injury (AKI). The survival of patients with AKI was significantly lower than the survival of patients without AKI (P < 0.001, log–rank test).

Discussion This is, to our knowledge, the first Scandinavian study on the incidence of AKI in ICUs serving a whole nation using the RIFLE classification. The study shows that 21.7% of all adult patients in the ICU develop some form of AKI, with an equal distribution between the RIFLE risk groups. In addition, our study underscores the importance of finding baseline creatinine values in studying the incidence of AKI. Several international studies of the incidence of AKI in ICUs using the RIFLE classification have been published recently,1,2,9–12 yielding variable results. For example, in the population described by Hoste et al., the incidence of AKI was 67%,1 and in the paper by Ostermann and Chang, the incidence was 35.8%.2 While Ostermann and Chang did not report the number of patients with baseline creatinine estimated with the MDRD equation, it was used in one half of the patients in the study by Hoste et al. Other studies have either used creatinine obtained at the admission to the ICU or the lowest creatinine measured during the ICU stay as baseline creatinine when analysing the severity of AKI.9,10 Similar to our study, all these studies are limited by the lack of data on urine output, and thus unable to apply the urine output criteria for diagnosing AKI,

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likely because this may be even more difficult to ascertain than baseline creatinine values. Using urine output values increases the sensitivity of the RIFLE criteria, but at the same time, a decrease in the mortality rate of each RIFLE subgroup is observed,13 indicating that the patients added by using the urine output values might have a less severe kidney injury. Assuming a normal creatinine value in the ICU population of elderly patients suffering from multiple comorbidities might overestimate the absolute incidence of AKI and incorrectly classify the severity of AKI. Using creatinine at admission to ICU or the lowest creatinine measured during the ICU stay might similarly underestimate the true incidence of AKI. This was recently demonstrated in a subset of patients admitted to two ICUs, comparing available baseline creatinine measurement with estimated baseline creatinine according to the MDRD equation, resulting in the overestimation of the incidence of AKI using the RIFLE criteria by 11%.14 Similarly, Bagshaw et al. found that excluding patients with suspected chronic kidney disease substantially improved the correlation between measured and estimated baseline creatinine, and called for improved methods to estimate baseline creatinine.15 The performance of the MDRD equation to establish baseline creatinine has been found to both overand underestimate the frequency of mild cases of AKI.16,17 In one such study, using the estimated baseline creatinine from the MDRD equation compared with measured creatinine correctly RIFLE-classified only 25% of cases in a mixed-case ICU.17 This was improved to 63% by only considering the injury and failure groups.17 This highlights the core strength of our study. We meticulously searched and obtained a reliable baseline creatinine measurement for the majority of the patients admitted to our ICUs, including a measured baseline value for all but two patients who developed AKI. Our results, therefore, are likely to represent the true incidence of AKI. It should be kept in mind, however, that baseline creatinine values were selected from up to 1 year prior to admission, potentially limiting their ability to represent the true baseline status. Patients with AKI required significant ICU resources. A total of 17% of AKI patients were treated with RRT. In comparison, 12% and 8% of the AKI populations described by Ostermann and Chang et al. and Hoste et al. received such treatment.1,2 This might suggest that the patients in our study had more severe disease, or simply be a result

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of differences in medical practice between countries and centres. Both ICU and hospital mortality was four times higher in the patients who developed AKI compared with the patients without AKI. Hospital mortality for patients with AKI in our population was higher than the mortality rate published by Hoste et al,1 similar to the one published by Ostermann and Chang2 but lower than the 74% mortality in the failure group reported by Medve et al.10 This variability might be due to different case mix in these populations, differences in hospital discharge criteria (such as the availability of long-term nursing and rehabilitation facilities) or over/underestimation of the true incidence of AKI. It might also represent the practice in Icelandic ICUs generally accepting the majority of admission requests regardless of overall prognosis, but suggesting an early limitation of therapy if initial therapy is not successful and the overall prognosis is considered poor. The 1-year survival was significantly reduced for the patients with AKI compared with the patients without AKI, but only three (2.5%) required longterm renal replacement therapy in the almost 3 years of follow-up. This is lower than the observed 8% of all patients surviving AKI until hospital discharge and requiring chronic renal replacement in three tertiary care ICUs in the United States.18 The difference might be due to the fact that we have a mixed nationwide, population-based cohort and not solely serving the most severely ill patients as some tertiary referral ICUs. The main limitation of this study is that it was a retrospective, single-centre study in only two ICUs with a limited number of patients in a small population. It was not designed to examine the total incidence of AKI in Icelandic hospitals but rather the incidence of AKI in the ICUs. The inherent differences in ICU admission indications and variable availability of non-ICU treatment of acutely ill patients can decrease the ability to generalise from our results to other ICU cohorts.

Conclusions In this first nationwide study, the incidence of AKI in ICUs determined by the RIFLE criteria was 21.7%, which is considerably lower than in two previously published European studies. The incidence would be 3.5% higher if estimated creatinine was only used. In our extended long-term follow-up, 49% of the patients with AKI had died 1 year after discharge compared with 17% of the ICU patients without

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AKI. However, only a small number of patients surviving AKI developed end-stage renal failure. Conflicts of interest: None of the authors have any conflicts of interest to report. Funding: None.

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Address: Gisli H. Sigurdsson Department of Anaesthesia & Intensive Care Medicine Landspitali University Hospital Hringbraut, IS 101 Reykjavik Iceland e-mail: [email protected]

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