Alina M. Robert, MD, Robert S. Kramer, MD, Lawrence J. Dacey, MD, David C. Charlesworth, MD, Bruce J. Leavitt, MD, Robert E. Helm, MD, Felix Hernandez, MD, Gerald L. Sardella, MD, Carmine Frumiento, MD, Donald S. Likosky, PhD, and Jeremiah R. Brown, PhD; for the Northern New England Cardiovascular Disease Study Group Internal Medicine, Dartmouth-Hitchcock Medical Center, Lebanon, New Hampshire; Cardiothoracic Surgery, Maine Medical Center, Portland, Maine; Cardiothoracic Surgery, Dartmouth-Hitchcock Medical Center, Lebanon, New Hampshire; Cardiothoracic Surgery, Catholic Medical Center, Manchester, New Hampshire; Cardiothoracic Surgery, Fletcher Allen Health Care, Burlington, Vermont; Cardiothoracic Surgery, Portsmouth Regional Hospital, Portsmouth, New Hampshire; Cardiothoracic Surgery, Eastern Maine Medical Center, Bangor, Maine; Cardiothoracic Surgery, Concord Hospital, Concord, New Hampshire; Cardiothoracic Surgery, Central Maine Medical Center, Lewiston, Maine; and Section of Cardiology, Dartmouth Institute for Health Policy and Clinical Practice, Dartmouth College, Dartmouth-Hitchcock Medical Center, Lebanon, New Hampshire
Background. Cardiac surgery-related acute kidney injury has short- and long-term impact on patients’ risk for further morbidity and mortality. Consensus statements have yielded criteria—such as the risk, injury, failure, loss, and end-stage kidney disease (RIFLE) criteria, and the Acute Kidney Injury Network (AKIN) criteria—to define the type and consequence of acute kidney injury. We sought to estimate the ability of both the RIFLE and and AKIN criteria to predict the risk of in-hospital mortality in the setting of cardiac surgery. Methods. Data were collected on 25,086 patients undergoing cardiac surgery in Northern New England from January 2001 to December 2007, excluding 339 patients on preoperative dialysis. The AKIN and RIFLE criteria were used to classify patients postoperatively, using the last preoperative and the highest postoperative serum creatinine. We compared the diagnostic properties of both criteria, and calculated the areas under the receiver operating characteristic curve.
Results. Acute kidney injury occurred in 30% of patients using the AKIN criteria and in 31% of patients using the RIFLE criteria. The areas under the receiver operating characteristic curve for in-hospital mortality estimated by AKIN and RIFLE criteria were 0.79 (95% confidence interval: 0.77 to 0.80) and 0.78 (95% confidence interval: 0.76 to 0.80), respectively (p ⴝ 0.369). Conclusions. The AKIN and RIFLE criteria are accurate early predictors of mortality. The high incidence of cardiac surgery postoperative acute kidney injury should prompt the use of either AKIN or RIFLE criteria to identify patients at risk and to stimulate institutional measures that target acute kidney injury as a quality improvement initiative.
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led to efforts to best identify and prevent renal insufficiency after cardiac surgery. In a first attempt to provide a standardized definition of acute renal failure and recommendations to assist in detecting and treating renal dysfunction in these critically ill patients, in 2004, the Acute Dialysis Quality Initiative Workgroup published the consensus RIFLE classification: it includes three stages of acute renal dysfunction, namely, risk (R), injury (I), and failure (F) based on changes from baseline in sCr, estimated glomerular filtration rate, and urine output; and the two clinical outcomes of loss (L) and end-stage kidney disease (E), based on the duration of required renal replacement therapy [4]. With the recognition that even smaller and more acute changes in sCr than those proposed by the RIFLE definition may result in adverse outcomes, the Acute Kidney Injury Network (AKIN) developed the definition and classification of AKI by introducing the AKIN
etween 5% and 30% of patients undergoing coronary artery bypass grafting (CABG) surgery may have postoperative acute kidney injury (AKI), and patients who have postoperative AKI are at increased risk for further morbidity and mortality [1–3]. The analysis by Lassnigg and colleagues [2] suggests that even a very small increase in serum creatinine (sCr), such as 0.5 mg/dL, is a predictor of poor outcomes, as it was associated with a threefold increase in 30-day mortality rate. The high incidence of postoperative AKI and its consequences of increased mortality, need for dialysis, prolonged hospital stay, and increased hospital costs have
Accepted for publication Aug 12, 2010. Address correspondence to Dr Brown, Dartmouth-Hitchcock Medical Center, Rubin 505, One Medical Center Dr, Lebanon, NH 03756; e-mail:
[email protected].
© 2010 by The Society of Thoracic Surgeons Published by Elsevier Inc
(Ann Thorac Surg 2010;90:1939 – 43) © 2010 by The Society of Thoracic Surgeons
0003-4975/$36.00 doi:10.1016/j.athoracsur.2010.08.018
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Cardiac Surgery-Associated Acute Kidney Injury: A Comparison of Two Consensus Criteria
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Abbreviations and Acronyms AKI ⫽ acute kidney injury AKIN ⫽ Acute Kidney Injury Network CABG ⫽ coronary artery bypass graft CI ⫽ confidence interval ICU ⫽ intensive care unit RIFLE ⫽ risk, injury, failure, loss, end-stage kidney disease ROC ⫽ receiver operating characteristic sCr ⫽ Serum creatinine
criteria in 2006. These criteria consist of stage 1, stage 2, and stage 3, which correspond to the RIFLE risk, injury, and failure stages, respectively [5]. The two classifications (Table 1) differ in that the AKIN criteria propose a period of 48 hours for detection of change in renal function and a smaller change in sCr than RIFLE criteria, with the hope of improving the sensitivity and early detection of AKI. Furthermore, the AKIN criteria do not require knowledge of a baseline sCr; rather, they consider kidney injury any acute increase in sCr that meets the criteria. The impact of these differences across the RIFLE and AKIN criteria in their prognostic utility for assessing the impact of AKI on in-hospital mortality in the setting of cardiac surgery has not yet been explored. We applied the RIFLE and AKIN criteria among 25,086 patients undergoing CABG or valve surgery in Northern New England between January 2001 and December 2007, and sought to determine which criteria (RIFLE or AKIN) provide the best prognostic power for predicting inhospital mortality.
Patients and Methods The Northern New England Cardiovascular Disease Study Group was founded in 1987 as a regional voluntary consortium capturing all of the coronary revascularizations and valve procedures in the northern New England area at eight medical centers in the states of Vermont, New Hampshire, and Maine. The group consists of clinicians, hospital administrators, and health care research personnel who seek to continuously improve the quality, safety, effectiveness, and cost of medical interventions in cardiovascular disease. The Internal Review Board at each center has approved the use of the Northern New England Cardiovascular Disease Study Group data for quality improvement and research. Patient consent was obtained as required by the center’s Internal Review Board.
Study Cohort Data were prospectively collected from 25,086 consecutive patients who underwent cardiac surgery in Northern New England from January 2001 to December 2007; 339 of the patients were excluded owing to preoperative dialysis dependency. Preoperative and postoperative sCr and death status at discharge were available for all 24,747
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patients (100%) included in the study who underwent classification by the RIFLE and AKIN criteria. The study outcome variables were development of AKI by the two criteria (RIFLE and AKIN) and in-hospital mortality.
Assessment of Renal Function Baseline sCr was defined as the last sCr value collected before surgery. The presence and type of AKI (RIFLE and AKIN) was calculated for each patient using the last preoperative and the highest postoperative sCr or new onset of acute dialysis before discharge. Patients were classified based on changes in sCr according to the RIFLE and AKIN classifications.
Statistical Analysis Baseline characteristics and clinical outcomes were summarized by percentages and means (⫾SD). Univariate logistic regression analysis was used to determine the association between AKI as defined by the RIFLE and AKIN criteria and in-hospital mortality. We evaluated the diagnostic properties of the RIFLE and AKIN criteria using the Hosmer-Lemeshow goodness-of-fit statistic for Table 1. Classification of Acute Kidney Injury RIFLE Classification Risk Increase in sCr by 1.5 times from baseline or GFR decrease ⬎25% Injury Increase in sCr by 2 times from baseline or GFR decrease ⬎50% Failure Increase in sCr by 3 times from baseline or sCr ⱖ4 mg/dL, or GFR decrease by 7 Loss Persistent need for renal replacement ⬎4 weeks ESKD Need for renal replacement therapy ⬎3 months AKIN Classification Stage 1 Increase in sCr by ⱖ0.3 mg/ dL or increase by 1.5 to 2 times from baseline Stage 2 Increase in sCr ⬎2 to 3 times from baseline Stage 3 Increase in sCr by ⬎3 times from baseline or absolute sCr ⱖ4 mg/dL, with acute increase of ⱖ0.5 mg/dL
Urinary output ⬍0.5 mL/kg/h for 6 hours
Urinary output ⬍0.5 mL/kg/h for 12 hours
Urinary output ⬍0.3 mL/kg/h or anuria for 12 hours
Urinary output ⬍0.5 mL/kg/h for 6 hours
Urinary output ⬍0.5 mL/kg/h for ⬎12 hours Urine output ⬍0.3 mL/ kg/hr for 24 hours or anuria for 12 hours
AKIN ⫽ Acute Kidney Injury Network; ESKD ⫽ end-stage kidney disease; GFR ⫽ glomerular filtration rate; RIFLE ⫽ risk, injury, failure, loss, end-stage kidney disease; sCr ⫽ serum creatinine.
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Table 2. Patient and Disease Characteristics % or Mean ⫾ SD
Variable Number of patients Patient comorbidities Age Female sex Body mass index Diabetes mellitus Peripheral vascular disease COPD Cardiac disease Coronary artery disease Hypertension Ejection fraction Number diseased vessels Myocardial infarction within 7 days Prior PCI Prior CABG Laboratory measures Baseline serum creatinine, mg/dL Baseline estimated GFR, [mL ⫻ min⫺1 ⫻ (1.73 m2)⫺2] ⱖ90 60–89 30–59 15–29 ⬍15 Type of surgery CABG Valve CABG/valve
24,747 66 ⫾ 11 29.2 29 ⫾ 6 31.9 24.0 12.60 87.9 71.6 53 ⫾ 14 2⫾1 18.0 26.1 5.2 1.1 ⫾ 1.0
22.2 50.7 24.8 1.9 0.4 68.9 15.6 15.5
CABG ⫽ coronary artery bypass graft surgery; COPD ⫽ chronic obstructive pulmonary disease; GFR ⫽ glomerular filtration rate; PCI ⫽ percutaneous coronary intervention.
model calibration and the area under the receiver operating characteristic (ROC) curve for discrimination. Differences between the areas under the ROC were explored using Harell’s C statistic. Stata Version 11.0 software (Stata Corp, College Station, TX) was used to conduct these analyses.
Results In general, the patient cohort was predominantly male, 71% had a history of hypertension, 88% had coronary
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artery disease, 73% had normal or near normal glomerular filtration rate, and 69% underwent CABG surgery alone (Table 2). Acute kidney injury developed in 7,391 patients (30%) using the AKIN criteria, and in 7,730 patients (31%) using the RIFLE criteria (Table 3). While the general classification was similar, the classification of the extent of injury appears to be different. Most patients with AKI were classified as stage 1 (23%) or risk (22%). Of note is that AKIN assigned more patients to stage 1 (5, 659) than RIFLE assigned to risk (5,357), and that RIFLE assigned more patients to injury (1,473) than AKIN assigned to stage 2 (852). The proportions of patients in stage 3 (880 patients) and failure (900 patients) were similar. There were 902 in-hospital deaths (3.6%). Risk of mortality increased among patients with greater degree of AKI, irrespective of criteria (Table 3). The calibration of the univariate models including AKIN stage or RIFLE stages was good, with p value of 1.0. The univariate odds ratios for in-hospital mortality by AKIN stage were as follows (no AKI as reference): AKIN stage 1, 3.17 (95% confidence interval [CI]: 2.63 to 3.82); AKIN stage 2, 12.43 (95% CI: 9.85 to 15.69); and AKIN stage 3, 43.77 (95% CI: 36.22 to 52.89). Odds ratios for in-hospital mortality by RIFLE category were as follows (no AKI as reference): risk, 2.41 (95% CI: 1.98 to 2.94); injury, 8.94 (95% CI: 7.27 to 11.00); and failure, 40.94 (95% CI: 33.95 to 49.36). There was no difference in the discriminatory power of mortality across criteria: AKIN 0.79 (95% CI: 0.77 to 0.80) and RIFLE 0.78 (95% CI: 0.76 to 0.80). The ROC comparison statistic demonstrated no statistical difference, with 2 ⫽ 0.81; p value for equality of ROC areas was 0.369 (Fig 1).
Comment Our study compared the sensitivity and specificity of the AKIN and RIFLE classifications in assessing the presence of AKI and in predicting in-hospital mortality. We found similar rates of AKI as those previously reported by both the AKIN and RIFLE criteria. Additionally, there was no significant difference in prediction of in-hospital mortality between the two classifications. This is the largest study aimed at comparing the two classifications in cardiac surgery patients. However, we confirm in this analysis that both AKIN and RIFLE classifications provide powerful and accurate risk assessment for in-hospital mortality, especially when patients are classified into the appropriate classification rather than AKI alone.
Table 3. AKIN and RIFLE Classification of Postoperative Renal Function AKIN Classification (Total No. Patients 24,747) Stage No AKI Stage 1 AKI Stage 2 AKI Stage 3 AKI
RIFLE Classification (Total No. Patients 24, 747)
n (%)
Mortality Rate, n (%)
Stage
n (%)
Mortality Rate, n (%)
17, 356 (70.1) 5, 659 (22.9) 852 (3.4) 880 (3.6)
228 (1.3) 229 (4.1) 121 (14.2) 324 (36.8)
No AKI Risk Injury Failure
17, 017 (68.8) 5, 357 (21.7) 1,473 (5.9) 900 (3.6)
235 (1.4) 175 (3.3) 164 (11.1) 328 (36.4)
AKI ⫽ acute kidney injury;
AKIN ⫽ Acute Kidney Injury Network;
RIFLE ⫽ risk, injury, failure, loss, end-stage kidney disease.
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ADULT CARDIAC Fig 1. Receiver operating characteristic (ROC) curves for the Acute Kidney Injury Network (AKIN) classification (solid circles) and the risk, injury, failure, loss, end-stage kidney disease (RIFLE) classification (open circle) predicting all-cause in-hospital mortality. The c-statistic for each model with 95% confidence intervals is listed (p ⫽ 0.369).
The RIFLE criteria have been evaluated in prior studies in an attempt to validate its use in different clinical settings such as intensive care units (ICU), non-ICU settings, and cardiac patients. Ricci and colleagues [6] reviewed 24 studies that evaluated the RIFLE criteria since its publication, with a total of 71,000 patients (including ICU, non-ICU, and cardiac surgery patients), and reported that mortality rate was consistently and significantly higher among patients with AKI, and it increased with worsening renal function. Furthermore, Kuitunen and associates [3] evaluated the RIFLE classification in a cohort of 813 cardiac surgery patients and found that AKI as defined by the RIFLE classification was an independent predictor for 90-day mortality and prolonged hospital stay, in comparison with changes in estimated glomerular filtration rate and plasma creatinine. Both the Kuitunen and Ricci studies were in agreement that there was a stepwise increase in the relative risk for death with each AKI class from risk to failure. With the development of the revised AKI classification with the AKIN criteria, some studies have tried to compare the performance of the RIFLE and AKIN criteria in determining in-hospital mortality. A recently published analysis by Joannidis and coworkers [7] compared RIFLE and AKIN criteria in determining the development of AKI and hospital mortality in a large cohort of patients admitted to the ICU. Their findings were significant for increased observed mortality among patients who had AKI compared with expected mortality based on the severity of their illness, with higher mortality at each stage of AKI. Additionally, their analysis noted that the RIFLE criteria were more sensitive as it identified 7% more patients with AKI than did the AKIN criteria [7]. Yan and colleagues [8] compared the two classifications in a small cohort of 67 postcardiotomy patients having received extracorporeal membrane oxygenation support for as long as 48 hours, and results revealed that AKIN and RIFLE criteria performed similarly in detecting AKI and in predicting in-hospital mortality. Haase and colleagues [9] conducted a small prospective study to com-
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pare the RIFLE and AKIN criteria in their performance for detection of AKI and prediction of in-hospital mortality. They enrolled 282 patients who underwent CABG, singlevalve surgery, combined CABG and valve surgery, and thoracic aortic surgery. In their analysis, a similar percentage of patients developed AKI by both the RIFLE and AKIN criteria assessment. Furthermore, both sets of criteria demonstrated similar performance in predicting in-hospital mortality, with sCr being the strongest predictor and urinary output the weakest predictor of in-hospital mortality [9]. A large retrospective study of ICU patients in Australia also found no statistical difference in the predictive ability of RIFLE criteria versus AKIN criteria for in-hospital mortality among critically ill patients or among patients with septic shock [10]. Lopes and associates [11], in a similar retrospective study of ICU patients, noted no significant difference in detection of AKI or predicting in-hospital mortality between AKIN criteria and RIFLE criteria, although AKIN criteria detected more patients with AKI and staged more patients under stage 1 AKI [11]. Our study extends findings of prior studies by supporting that both RIFLE criteria and AKIN criteria are equivalent predictors of in-hospital mortality. The advantages of the AKIN criteria are that it does not require a baseline creatinine, as two sCr values within 48 hours would suffice to detect a change in renal function and development of AKI; it does not require measurement of urinary output, as those measurements are clinically known to be inaccurate; and it simplifies the classification of AKI with three stages. There are limitations to consider in our analysis. We did not use urine output to aid in classifying patients’ renal function. Accurate documentation of preoperative and postoperative urine output has not been uniformly demonstrated across different clinical setting and facilities, including those collecting data for the Northern New England Cardiovascular Disease Study Group database. Moreover, many patients, if stable, are not monitored in the ICU in the preoperative period; thus, urine output is not closely measured. As we did not want to compromise the accuracy of our analysis, we have only used changes in sCr to stage patients using both the RIFLE criteria and the AKIN criteria. Additionally, the AKIN criteria [5] require changes in serum creatinine or urine output, but not both, as do the previous RIFLE criteria [4]. These criteria were evaluated by the AKIN executive committee and found not to reduce the performance of the diagnostic measure owing to lack of consistent urine output measurement in the clinical setting [5]. Furthermore, Barrantes and colleagues [12] and Mehta [13] validated the diagnostic ability of sCr over urine output, demonstrating the predictability of AKI on mortality using only sCr (AKIN definition) with odds ratio of 3.7 (95% CI: 2.3 to 6.2), whereas oliguria was 3.0 (95% CI: 1.8 to 5.1). In conclusion, the RIFLE criteria and the AKIN criteria were developed in attempt to improve detection of and care for patients who experienced an acute decrease in renal function after cardiac surgery. Based on our analysis, both AKIN and RIFLE criteria are accurate early predictors of in-hospital mortality. The high incidence of AKI associated with cardiac surgery should prompt the
use of either AKIN criteria or RIFLE criteria in the early postoperative period to identify patients at increased risk and to stimulate institutional measures that target AKI as a quality improvement initiative. This project was supported by grant number K01 HS018443 (Dr Brown) from the Agency for Healthcare Research and Quality. The content is solely the responsibility of the authors and does not necessarily represent the official views of the Agency for Healthcare Research and Quality.
References 1. Karkouti K, Wijeysundera DN, Yau TM, et al. Acute kidney injury after cardiac surgery: focus on modifiable risk factors. Circulation 2009;119:495–502. 2. Lassnigg A, Schmidlin D, Mouhieddine M, et al. Minimal changes of serum creatinine predict prognosis in patients after cardiothoracic surgery: a prospective cohort study. J Am Soc Nephrol 2004;15:1597– 605. 3. Kuitunen A, Vento A, Suojaranta-Ylinen R, Pettila V. Acute renal failure after cardiac surgery: evaluation of the RIFLE classification. Ann Thorac Surg 2006;81:542– 6. 4. Bellomo R, Ronco C, Kellum JA, Mehta RL, Palevsky P, for the Acute Dialysis Quality Initiative workgroup. Acute renal failure— definition, outcome measures, animal models, fluid therapy and information technology needs: the second international consensus conference of the Acute Dialysis Quality Initiative (ADQI) group. Crit Care 2004;8:R204 –12.
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5. Mehta RL, Kellum JA, Shah SV, et al. Acute Kidney Injury Network: report of an initiative to improve outcomes in acute kidney injury. Crit Care 2007;11:R31. 6. Ricci Z, Cruz D, Ronco C. The RIFLE criteria and mortality in acute kidney injury: a systematic review. Kidney Int 2008;73: 538 – 46. 7. Joannidis M, Metnitz B, Bauer P, et al. Acute kidney injury in critically ill patients classified by AKIN versus RIFLE using the SAPS 3 database. Intens Care Med 2009;35:1692–702. 8. Yan X, Jia S, Meng X, et al. Acute kidney injury in adult postcardiotomy patients with extracorporeal membrane oxygenation: evaluation of the RIFLE classification and the acute kidney injury network criteria. Eur J Cardiothorac Surg 2010;37:334–8. 9. Haase M, Bellomo R, Matalanis G, Calzavacca P, Dragun D, Haase-Fielitz A. A comparison of the RIFLE and Acute Kidney Injury Network classifications for cardiac surgeryassociated acute kidney injury: a prospective cohort study. J Thorac Cardiovasc Surg 2009;138:1370 – 6. 10. Bagshaw SM, George C, Bellomo R, for the ANZICS Database Management Committe. A comparison of the RIFLE and AKIN criteria for acute kidney injury in critically ill patients. Nephrol Dial Transplant 2008;23:1569 –74. 11. Lopes JA, Fernandes P, Jorge S, et al. Acute kidney injury in intensive care unit patients: a comparison between the RIFLE and the acute kidney injury network classifications. Crit Care 2008;12:R110. 12. Barrantes F, Tian J, Vazquez R, Amoateng-Adjepong Y, Manthous CA. Acute kidney injury criteria predict outcomes of critically ill patients. Crit Care Med 2008;36:1397– 403. 13. Mehta RL. From acute renal failure to acute kidney injury: emerging concepts. Crit Care Med 2008;36:1641–2.
INVITED COMMENTARY Robert and colleagues [1] present a comparison of the two major consensus criteria to evaluate acute kidney injury using a large prospective cohort. The largest to date, with 24,747 patients, this study is timely and relevant for the evaluation of patients after cardiac surgery. Until the development of these major consensus criteria, there was little diagnostic clarity on the complex disorder of acute kidney injury. The acute kidney injury network (AKIN) and risk injury failure loss end stage renal disease (RIFLE) criteria are used to define the spectrum of this disorder, with the initial stage (R in RIFLE and stage 1 in AKIN) representing risk of kidney injury. The injury and failure stages (or stage 2 and 3) represent true injury to the kidneys, and perhaps should be combined. Although this study confirms the use of the AKIN and RIFLE criteria as accurate predictors of in-hospital mortality, it would be of interest if they had provided additional outcome criteria, such as numbers of patients requiring renal replacement therapy in both the short-term and long-term, length of intensive care unit and hospital stay, and long-term mortality. Reporting of positive and negative predictive values and likelihood ratios would also have been valuable. Robert and colleagues [1] limited categorization by only using changes in serum creatinine rather than including urine output criteria. We believe this is appropriate in the cardiac surgery population, as manipulation of urine output with diuretics is standard and this would make it a less reliable indicator of renal function. Some clinicians have suggested that the change in serum creatinine of 0.3 mg/dL (required by the AKIN criteria for categorization of stage 1) is too small, but in the postcar© 2010 by The Society of Thoracic Surgeons Published by Elsevier Inc
diopulmonary bypass population, creatinine typically decreases initially, so even this small increase from the preoperative baseline in the immediate postoperative period likely represents a real change in kidney function. Serum creatinine remains a sensitive and relevant marker for declining kidney function. New biomarkers such as neutrophil gelatinase associated lipocalin and kidney injury molecule-1 are currently being validated and will hopefully provide us with a clearer determination of injury and prognosis. The area under the receiver operating characteristic curves in this study (0.79, 0.78) show that although the AKIN and RIFLE criteria provide accurate prediction of kidney injury and mortality in postcardiac surgery patients, we have significant room to improve in this important disease state. Nicole Guinn, MD Andrew D. Shaw, MD, FCCM Department of Anesthesiology Duke University Medical Center 508 Fulton St Durham, NC 27705 e-mail:
[email protected]
Reference 1. Robert AM, Kramer RS, Dacey LJ, et al. Cardiac surgeryassociated acute kidney injury: a comparison of two consensus criteria. Ann Thorac Surg 2010;90:1939 – 43. 0003-4975/$36.00 doi:10.1016/j.athoracsur.2010.09.014
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