Acute Kidney Injury Is Associated With Higher Morbidity and Resource Utilization in Pediatric Patients Undergoing Heart Surgery

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1 CARDIAC ANESTHESIOLOGY: The Annals of Thoracic Surgery CME Program is located online at To take the CME activity related to this article, you must have either an STS member or an individual non-member subscription to the journal. Acute Kidney Injury Is Associated With Higher Morbidity and Resource Utilization in Pediatric Patients Undergoing Heart Surgery Roland Tóth, MD, Tamás Breuer, MD, Zsuzsanna Cserép, MD, Dániel Lex, Levente Fazekas, MD, PhD, Erzsébet Sápi, MD, András Szatmári, MD, PhD, János Gál, MD, PhD, and Andrea Székely, MD, PhD School of PhD Studies, and Departments of Cardiovascular Surgery, and Anesthesiology and Intensive Therapy, Semmelweis University, Budapest; and Departments of Anesthesia and Intensive Care, and Pediatric Cardiology, Gottsegen György Hungarian Institute of Cardiology, Budapest, Hungary Background. The RIFLE (risk, injury, failure, loss, and end-stage renal disease) classification system was developed to standardize the definition of acute kidney injury (AKI) in adults. We hypothesized that AKI was associated with increased mortality and morbidity. Methods. Acute kidney injury was defined as a decrease in the amount of estimated creatinine clearance based on pediatric-modified RIFLE (prifle) criteria. Using propensity score analysis, 325 patients who had AKI were matched to 325 patients who did not have AKI from a database of 1,510 consecutive pediatric patients who underwent cardiac surgery between January 2004 and December 2008 at a single center. The association between AKI and outcome was analyzed after propensity score matching of perioperative variables. Results. Four hundred eighty-one patients (31.9%) had AKI according to the RIFLE categories. Of those 1,510, 173 (11.5%) reached prifle criteria for risk; 26 (1.7%) reached the criteria for injury; and 282 (18.7%) reached the criteria for failure. Fifty-five patients (3.6%) died. The 2 matched groups were well balanced in terms of measured perioperative variables. Mortality rate was 5.2% in the AKI and 2.5% in the matched control group (p 0.09). Occurrence of low cardiac output syndrome (p 0.002), need for dialysis (p < 0.001), and infection (p 0.03) were significantly higher, and duration of mechanical ventilation (p < 0.001) and length of intensive care unit stay (p < 0.001) were significantly longer compared with the matched control group. Conclusions. Acute kidney injury was independently associated with an increased occurrence of postoperative complications but not with mortality after pediatric cardiac surgery. (Ann Thorac Surg 2012;93: ) 2012 by The Society of Thoracic Surgeons Acute kidney injury (AKI) is one of the most common and severe complications in cardiac surgery. An AKI can be characterized as a sudden worsening in the renal function, and its manifestations alternate between a minimal change in serum creatinine and anuric renal failure [1]. While the incidence rate for renal replacement therapy (RRT) is 1.1% to 1.4% after cardiac surgery, a much higher percentage suffer renal dysfunction that does not meet the criteria for acute hemodialysis [2]. Acute kidney injury is associated with an increased complication rate, including both morbidity and mortality, and the expenditure of other resources [3]. In pediatric populations, similar findings have been described [3, 4]. The application of RIFLE ((risk, injury, failure, loss, and end-stage renal disease) classification has been validated in pediatric populations [5]. In the last decade, the relationship between AKI and aprotinin was Accepted for publication Oct 14, Address correspondence to Dr Székely, Department of Anesthesiology and Intensive Therapy, Semmelweis University, Kútvölgyi út 4, Budapest, H-1125, Hungary; szekelya@kardio.hu. investigated in congenital heart surgery populations [6, 7]. These studies found a more frequent occurrence of AKI than RRT in the same population. Although renal dysfunction and failure are known risks of pediatric cardiac surgery, accurate estimates of the incidence and relationship among AKI and other complications are lacking [8 10]. The purpose of this study was to determine the occurrence of AKI in a large retrospective cohort of pediatric patients using the validated pediatric-modified RIFLE (prifle) criteria. We aimed to determine the relationship of AKI with other complications after cardiac surgery. Material and Methods After Institutional Review Board approval (TUKEB 189/ 2008), data from a prospectively collected database of consecutive pediatric ( 18 years) patients undergoing cardiac surgery and admitted to our cardiac intensive care unit (ICU) between January 1, 2004 and December 2012 by The Society of Thoracic Surgeons /$36.00 Published by Elsevier Inc doi: /j.athoracsur

2 Ann Thorac Surg TÓTH ET AL 2012;93: AKI ASSOCIATED WITH INCREASED MORBIDITY 1985 Fig 1. Consolidated Standards of Reporting Trials statement. (eccl estimated creatinine clearance; ECMO extracorporeal membrane oxygenation; RACHS Risk Adjustment for Congenital Heart Surgery; VADs ventricular assist devices.) 31, 2008 were studied. The board waived the requirement for informed consent by the parent. During the study period, 1,767 cardiac surgeries were performed. For patients who underwent more than 1 operation during the index hospitalization, only the first operation was considered for the present analysis (Fig 1). The database collection form contains 5 sections completed consecutively by a cardiologist (preoperative and postoperative parts), anesthesiologist, surgeon, and intensivists until discharge of the patient. The cohort was matched to the Department of Biochemistry database through the use of patient identifiers and operation date. Cardiac surgical procedures were graded as class 1 6 by complexity, applying the Risk Adjustment for Congenital Heart Surgery, version 1 (RACHS) method [11]. The cumulative index of inotropic support was quantified by the modified Wernovsky score [12]. Low output syndrome was defined as hepatomegalia, oliguria, tachycardia, and, when the systolic blood pressure sank under the age-related normal value, had a base excess lower than 4 mmol/l or lactate above 2 mmol/l in 2 consecutive arterial blood samples. Pulmonary failure was defined as noninfectious, nonvascular oxygenation problems (atelectasis, pneumothorax, chylothorax, and phrenic paresis). Serious infection was defined as sepsis, deep sternal wound infection, or positive blood culture, and death was defined as in-hospital death after arrival at the ICU. All patient outcomes included in the database were determined separately by an intensivist and a cardiologist at the discharge of the patient from the hospital. Outcome Assessment The AKI was classified according to prifle categories [5]. The Schwartz formula was used to determine the estimated creatinine clearance by the following equation [13]: k height cm eccl (ml/min 1.73m 2 ) plasma creatinine mg/dl (1) where k 0.55; if 1 year, 0.45; if male and older than 13 years, 0.7. Both estimated creatinine clearance (eccl) and urine output (UO) were considered, and the patients were assigned to the appropriate prifle strata if they fulfilled either the UO or serum creatinine criteria criterion: Risk was defined as an eccl decrease of 25% or UO less than 0.5 ml kg 1 hour 1 8 hours; injury was defined as an eccl decrease of 50% or UO less than 0.5 ml kg 1 hour 1 16 hours; and failure was defined as an eccl decrease of 75%, an eccl less than 35 ml minutes m 2 or UO less than 0.3 ml kg 1 hour 1 24 hours or anuric for 24 hours. Either the eccl method or the UO method was used for stratification but they were not combined in the RIFLE classification. Renal replacement therapy was defined as a need for peritoneal or hemodialysis support. Statistical Analysis Categoric variables were summarized as frequencies and percentages. Continuous variables were expressed as means and standard deviations or medians and interquartile ranges for parametric and nonparametric variables, respectively. The unadjusted associations of the 3 thresholds of prifle with morbidities (LOS, pulmonary, neurologic, infection, mechanical ventilation greater than 72 hours, RRT, length of ICU stay) and death rates were calculated with the Wilcoxon rank sum test. Because patients with AKI and without AKI were not comparable with respect to important covariates, propensity score methods were used to match patients who had AKI to patients who had no AKI. The propensity score was constructed with multivariable logistic regression, with AKI as the binomial dependent variable and all measured covariates that could be related to AKI (20 variables) as predictor variables. The model s reliability and predictive ability were measured with the Hosmer- Lemeshow test and the c-index, respectively [14]. The propensity score derivation model was used to calculate the propensity score for each patient, and based on this score each patient who had AKI was matched to a unique control patient. A 5 1 computerized greedy matching technique was employed for this matching

3 1986 TÓTH ET AL Ann Thorac Surg AKI ASSOCIATED WITH INCREASED MORBIDITY 2012;93: process whereby cases were first matched to controls that had a propensity score that was identical in all 5 digits. Those that did not match were then matched to controls on 4 digits of the propensity score. This continued down to a 1-digit match on propensity score for those that remained unmatched. Measured covariates and outcomes in the matched group were compared between the 2 groups with paired t test or Wilcoxon signed rank test for continuous variables and McNemar test for categoric variables. The procedure yielded 325 well-matched pairs. The SPSS 16.0 statistical software (SPSS Inc Chicago, IL) was used. A p value of less than 0.05 was considered statistically significant. Results During the 5-year period, 1,665 patients received operations, and in 155 (9.3%) of the cases, eccl could not be calculated. The analyzed database contained the data of 270 (17.9%) neonates, 517 (34.2%) infants, and 723 (47.9%) children. In the study population of 1,510 patients, 481 (31.9%) patients had AKI as assessed by the prifle criteria. Of those 1,510, 173 (11.5%) met the risk threshold, 26 (1.7%) met the injury threshold, and 282 (18.7%) met the failure threshold of AKI. Fifty-five patients (3.6 %) died; 4 (7.3%), 0, and 39 (70.9%) were from the risk, injury, and failure groups, respectively, and 12 patients (21.8%) had no AKI. Renal replacement therapy was needed in 96 (6.4%) patients and 8 (0.5% of the study population and 8.3% of the RRT group) patients did not meet the prifle criteria. The demographic and perioperative characteristics of the patients clustered by the prifle categories are shown in Table 1. Patients with AKI underwent more complex surgery with long cardiopulmonary bypass duration, were more likely to have cyanosis, and needed mechanical ventilation before surgery than those without renal dysfunction. Acute kidney injury patients received higher amounts of inotropic drugs and transfusions, and needed nitric oxide, steroids, and aprotinin more frequently. Patients in the failure group were younger and smaller, and one-third of them underwent acute surgery and operations with rethoracothomy. Preoperative eccl in the failure group was lower compared with the non-aki patients, while postoperative eccl and creatinine levels measured either on the first or second postoperative days were significantly lower in each group compared with the non-aki patients (data are not shown). There were no significant differences in the urine output compared with non-aki patients, except for the risk group on the day of surgery and the failure group on the second postoperative day (Fig 2). In each AKI group, the postoperative eccl was lower than the baseline level. The mortality and morbidity rates classified by prifle categories are shown in Figure 3. All 3 thresholds of AKI were associated with an increased length of mechanical ventilation and ICU stay (data are not shown). The propensity score derivation model, which included 22 variables, including the following: weight, logarithmic transformation of age, cyanosis, univentricular heart, RACHS score, previous operation, preoperative pulmonary hypertension and congestive heart failure, preoperative inotrope treatment and captopril medication, preoperative ICU stay, preoperative mechanical ventilation, cardiopulmonary bypass time, cross-clamp time, operation time, minimum nasopharyngeal temperature, deep hypothermic cardiac arrest, ultrafiltration, post-bypass inotropic score, need for nitric oxide, transfusion (ml/ kg), and use of aprotinin, was reliable (Hosmer- Lemeshow test p 0.3) and discriminative (c-index 0.94). By use of this model, 325 (of 481) AKI patients were matched to 325 control (of 1,021) non-aki patients. Table 2, shows the comparison of the measured covariates before and after propensity matching. The mean propensity scores for AKI and the non-aki groups were and 0.377, respectively (p 0.99). The propensity score of the unmatched AKI group was Table 3 contains the outcomes of the patients before and after propensity matching. Before propensity matching, AKI patients had higher mortality and morbidity compared with non-aki patients. After propensity matching, occurrence of low cardiac output syndrome, need for dialysis, and infection was higher in the AKI group. Length of mechanical ventilation and ICU stay were also longer compared with the non-aki patients. Comment We found that AKI occurs relatively frequently in the pediatric cardiac population. The incidence of postoperative complications increased with the severity of prifle categories. The prifle categorization based on urine output cannot be applied in the early postoperative period after pediatric cardiac surgery. Using propensity score methods, we successfully matched a relatively large number of patients who had AKI after pediatric cardiac surgery to a group of patients (comparable with respect to every measured covariate) who did not have AKI. We found that patients who had AKI had a higher rate of low cardiac output syndrome, dialysis, and infection than patients without AKI. Length of mechanical ventilation and ICU stay were also longer in patients in the AKI group compared with patients in the non-aki group. In cardiac populations, the pathomechanism of AKI is caused mostly by the alteration of renal blood flow, ischemia, and diminished autoregulation [15, 16]. The cardiopulmonary bypass activates the inflammatory response, and the large foreign surface and shear stress further consume the coagulation factors and damage the blood components [17]. The presence of coexisting disease, hemodynamic instability, and certain drugs such as furosemide or angiotensin convertase enzyme inhibitors, increase the likelihood of developing AKI [18]. In patients with congenital heart disease undergoing cardiac surgery, cyanosis, young age, and large volume and blood component shifts during cardiopulmonary bypass also contribute to diminished kidney function [10, 19]. The

4 Table 1. Demographic, Surgical, and Intraoperative Parameters According to prifle Categories Variable None (n 1,029) Risk (n 173) Injury (n 26) Failure (n 282) Median/N IQR/% Median/N IQR/% p Value Median/N IQR/% p Value Median/N IQR/% p Value Age (days) , , , Weight (kg) , RACHS (point) Redo Rethoracotomy Acute/urgent Preoperative factors Pulmonary hypertension Cyanosis Captopril Furosemide Inotropics/digoxin ICU stay Mechanical ventilation Intraoperative: CPB time (minutes) , Cross-clamp time (minutes) , Repeat CPB DHCA Operation time (minutes) , Blood loss (ml/kg) RBC (ml/kg) Inotropic score Ultrafiltration Aprotinin Nitric oxide Pacemaker Data are presented as number and percentage of patients or median and interquartile range (IQR) for categoric and continuous variables, respectively. For categoric variables, p values are based on a 2-sided 2 or Fischer exact test (as appropriate), comparing prifle patients to non-prifle patients. For continuous variables, p values are based on t test or Wilcoxon rank sum test. Bonferroni correction was used, and p was considered significant. CPB cardiopulmonary bypass time; DHCA deep hypothermic cardiac arrest; ICU intensive care unit; IQR interquartile range; RACHS risk-adjusted congenital heart surgery; RBC red blood cells transfusion; prifle pediatric-modified risk, injury, failure, loss, and end-stage renal disease classification system. Ann Thorac Surg TÓTH ET AL 2012;93: AKI ASSOCIATED WITH INCREASED MORBIDITY 1987

5 1988 TÓTH ET AL Ann Thorac Surg AKI ASSOCIATED WITH INCREASED MORBIDITY 2012;93: Fig 2. Urine output and pediatric modified RIFLE (prifle) categories. Columns are shown as mean of urine output expressed in ml/kg, error bars are standard deviation. Significant p values are shown above the columns. (DOS day of surgery; POD postoperative day; [R risk, I injury, and F failure, of the prifle categories.) presence of these factors could be identified in our study population who suffered from AKI. Measuring kidney function is difficult in critically ill patients. The Acute Dialysis Quality Initiative (ADQI) Working Group published the RIFLE classification, a consensus and evidence-based definition for AKI based on the changes in creatinine clearance or urine output compared with baseline [20]. The modified prifle criteria were validated in stable critically ill children [5]. Recently, the Acute Kidney Injury Network criteria, which calculates the increase in serum creatinine expressed as a ratio of the baseline value, has gained popularity because it does not require the calculation of creatinine clearance. Hence, the variation of AKI definitions causes interstudy heterogeneity [21, 22]. Therefore, homogenous classification and consensus would be essential in the definition and categorization of AKI. In our pediatric cardiac surgical population, the distribution of AKI categories was not homogenous. This discrepancy can be partly due to the failure definition of the prifle criteria; ie, the eccl less than 35 ml minute m 2 is very close to the normal value of the neonate and infant population, and small changes in eccl can cluster these patients into the failure group. However, after propensity matching the AKI group had higher morbidity compared with the non-aki group. Therefore, this eccl threshold might be interpreted as a dangerous cutoff value below which the kidney could not satisfactorily eliminate waste products. Our results also support the finding reported in adults [23] that urine output was not applicable for categorization of the pediatric cardiac surgical population. Recently, the length of ICU stay and the duration of mechanical ventilation were found to be associated with the occurrence of AKI in pediatric cardiac patients [24, 25]. Our findings show that prifle-based AKI was strongly related to postoperative complications. One explanation could be the cardiorenal syndrome described in adult patients [26]. The study design did not allow for determination between causes and consequences. Similar to a conclusion in an adult study, we must identify all modifiable factors in the development of AKI to reduce the occurrence of AKI and the associated complications [27]. Our study has limitations. First, the retrospective analysis did not allow for a search of causes and consequences. However, our proprietary hospital database has recorded prospective clinical, diagnostic, and outcome data on all pediatric ICU patients since Fig 3. Postoperative complications and pediatric modified RIFLE categories. (A) Mortality; (B) dialysis; (C) low cardiac output; (D) infection. Asterisks show p 0.05 compared to the patients without AKI. (AKI acute kidney injury; RIFLE risk, injury, failure, loss, and end-stage renal disease.)

6 Ann Thorac Surg TÓTH ET AL 2012;93: AKI ASSOCIATED WITH INCREASED MORBIDITY 1989 Table 2. Group Comparison Before and After Propensity Matching Before Propensity Score Matching After Propensity Score Matching AKI (n 481) No AKI (n 1,029) AKI (n 325) Control (n 325) Variable Mean/N SD/% Mean/N SD/% p Value Mean/N SD/% Mean/N SD/% p Value Weight Age (ln) a Reoperation % % % 76 23% 0.57 RACHS Univentricular heart 45 9% 51 5% % 25 8% 0.76 Cyanosis % % % % 0.89 Preoperative ICU stay % % % 39 12% 0.99 Inotrope treatment % 51 5% % 91 28% 0.79 Mechanical ventilation 58 12% 35 3% % 24 7% 0.21 Pulm. Hypertension % % % 85 26% 0.17 Captopril 89 19% % % 81 25% 0.35 Congestive heart failure % % % 70 22% 0.77 CPB time (minutes) Cross-clamp time Operation time (minutes) T min nasopharyngeal b DHCA 34 7% 11 1% % 6 2% 0.31 Ultrafiltration 88 18% 38 4% % 22 7% 0.43 Inotropic score Nitric oxide 78 16% 26 3% % 19 6% 0.62 Transfusion (ml/kg) Aprotinin % % % 71 22% 0.77 a Age (ln) logarithmic transformation of age; b T min nasopharyngeal minimum nasopharyngeal temperature during cardiopulmonary bypass. Data are presented as number and percentage of patients or mean and standard deviation (SD) for categoric and continuous variables, respectively. AKI acute kidney injury; CPB cardiopulmonary bypass; DHCA deep hypothermic cardiac arrest; ICU intensive care unit; Pulm. pulmonary; RACHS risk-adjusted congenital heart surgery. September This was a single-center study, and the database is comprised of patients of different ages and with very heterogeneous congenital heart defects, which improves the generalizability of the study. However, our population was very similar to other study populations in terms of surgical severity scores and Table 3. Comparison of Outcomes in the Nonmatched and Matched Groups Before Propensity Score Matching After Propensity Score Matching AKI (n 481) Non-AKI (n 1,029) AKI (n 325) Non-AKI (n 325) Variable N/median %/IQR N/median %/IQR p Value N/median %/IQR N/median %/IQR p Value Mortality % % % 8 2.5% 0.09 Low cardiac output % % % % Pulmonary failure % % % % 0.63 Dialysis % 8 0.8% % 6 1.8% Infection % % % % 0.03 ICU stay (days) 6.1 ( ) 3.5 ( ) ( ) 4.1 ( ) MV (hours) 87 (32 166) 13 (7 35) (26 112) 33 (15 76) Data are presented as number and percentage of patients or median and interquartile range (IQR). AKI acute kidney injury; ICU intensive care unit; MV mechanical ventilation.

7 1990 TÓTH ET AL Ann Thorac Surg AKI ASSOCIATED WITH INCREASED MORBIDITY 2012;93: AKI rates described using various definitions. Another limitation of this study is that an appropriate match could not be identified for 32.4% of the patients who had AKI. Proteinuria was not measured quantitatively during the study period. In conclusion, we have found that measuring the change in eccl is a useful tool with which to identify patients with AKI in the postoperative period. Furthermore, AKI categorized by the prifle criteria was associated with increased morbidity after propensity score matching. Further investigations are required to determine the usefulness of the prifle criteria in the infant and neonate cardiac surgical population. References 1. Aronson S, Blumenthal R. Perioperative renal dysfunction and cardiovascular anesthesia: Concerns and controversies. J Cardiothorac Vasc Anesth 1998;12: Simmons PI, Anderson RJ. 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Circulation 2009;119: INVITED COMMENTARY The study by Tóth and colleagues [1], based on the statistical method of propensity matching in a large database of 1,500 patients, demonstrates that the category failure in the pediatric RIFLE classification (prifle) is independently associated with complications after operations for congenital heart disease. Although age and weight are surrogate markers of prifle criteria, Tóth now has shown that renal failure is an independent risk factor in addition to other well-known risks of congenital heart surgery, especially low weight, neonatal age, long 2012 by The Society of Thoracic Surgeons /$36.00 Published by Elsevier Inc doi: /j.athoracsur