Journal of Critical Care 29 (2014) 432–437

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Clinical outcome of kidney transplantation from deceased donors with acute kidney injury by Acute Kidney Injury Network criteria☆ Myung Hyun Lee, MD a, b, Eun-Gyo Jeong, MD a, b, Ji Yeun Chang, MD a, b, Yaeni Kim, MD a, b, Ji-Il Kim, MD, PhD a, c, In Sung Moon, MD, PhD a, c, Bum Soon Choi, MD, PhD a, b, Cheol Whee Park, MD, PhD a, b, Chul Woo Yang, MD, PhD a, b, Yong-Soo Kim, MD, PhD a, b, Byung Ha Chung, MD, PhD a, b,⁎ a b c

Transplant Research Center, Seoul St Mary's Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea Division of Nephrology, Department of Internal Medicine, Seoul St Mary's Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea Department of Surgery, Seoul St Mary's Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea

a r t i c l e

i n f o

Keywords: Acute kidney injury Deceased donor Kidney transplantation Acute Kidney Injury Network (AKIN)

a b s t r a c t Purpose: In this study, we investigated the outcome of kidney transplantation (KT) from deceased donors with acute kidney injury (AKI), as defined by the Acute Kidney Injury Network criteria. Methods: Of 156 deceased donors, kidneys from 43 donors (27.6%) with AKI were transplanted into 57 recipients (AKI group). Another 147 recipients received kidneys from donors without AKI (non-AKI group). We compared the incidence of delayed graft function, allograft function for 1 year after KT, and long-term (5 and 10 years) graft survival rate between the 2 groups. Results: Delayed graft function developed more frequently in the AKI group than in the non-AKI group (42.1% vs 12.2%; P b .05), and allograft function—assessed by the modification of diet in renal disease equation— showed a significantly deteriorating pattern at 2 weeks and 1, 3, and 6 months after KT compared with that in the non-AKI group (P b .05 for comparisons at each time point). However, allograft function at 12 months after KT and the long-term allograft and patient survival rates did not differ between the AKI and non-AKI groups. Conclusions: In KT from deceased donors, the AKI group that received kidneys with AKI, as defined by the Acute Kidney Injury Network criteria, showed a higher delayed graft function rate and lower allograft function for 6 months after KT but no effect on allograft function 1 year after KT and on long-term allograft survival. © 2014 Elsevier Inc. All rights reserved.

1. Introduction The disparity between demand and supply of kidney allografts has accelerated the development of strategies to increase the number of kidneys for transplantation [1]. In this regard, the use of kidneys from deceased donors with acute kidney injury (AKI) has been proposed as an alternative method to increase the donor pool. However, the clinical outcome of a renal allograft from deceased donors with AKI showed contradictory results in previous studies, which is of concern to clinicians [2-5]. In addition, the definition of AKI in deceased donors has not been standardized; hence, specific guidelines on the use of kidneys from donors with AKI could not be established. In the general population, standardized classification systems for AKI that represent the whole status of the kidney have been developed and are widely used in the clinical field [6]. The Risk Injury Failure Loss End-Stage Kidney Disease (RIFLE) criteria were

developed first by the Acute Dialysis Quality Initiative group [7]. However, owing to several limitations, a modification of the RIFLE criteria, known as the Acute Kidney Injury Network (AKIN) classification system, was proposed [7,8]. These criteria have now been evaluated in a number of clinical studies of patients with AKI outside the kidney transplantation (KT) setting and have shown reliable predictability for renal outcome and patient mortality [3,6,9]. However, the previously reported standardized criteria of AKI for nontransplanted kidneys have rarely been used for potential kidney donors for the prediction of renal allograft outcome; another AKI criteria, the AKIN criteria, have not been adopted in this field [3]. Therefore, this study aimed to analyze the prevalence of AKI by the AKIN criteria in deceased donors before KT and to investigate the clinical outcome in patients who received kidneys from deceased donors with AKI based on the AKIN criteria. 2. Materials and methods

☆ Conflicts of interest: None. ⁎ Corresponding author. Department of Internal Medicine, Seoul St Mary's Hospital, 505 Banpo-Dong, Seocho-Ku, 137-040, Seoul, Korea. Tel.: +82 2 2258 6066; fax: +82 2 536 0323. E-mail address: [email protected] (B.H. Chung). 0883-9441/$ – see front matter © 2014 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jcrc.2013.12.016

2.1. Study population Between September 1996 and December 2012, 158 patients were pronounced brain dead in our institution. The acceptance criteria for

M.H. Lee et al. / Journal of Critical Care 29 (2014) 432–437

the use of kidneys from deceased donors in our center were (1) normal serum creatinine at baseline (b 1.2 mg/dL), (2) no medical history of chronic kidney disease, and (3) no evidence of chronic kidney disease on kidney sonography. According to these criteria, we discarded kidneys in only 2 cases and used kidneys from the remaining 156 deceased donors. Of 312 kidneys from those donors, 204 were used in our center, and another 108 were transferred to another institution for transplantation to patients. In this study, we included all 204 recipients who received kidneys from the 156 deceased donors in our center. Of those 156 donors, 43 (28%) were diagnosed with AKI as defined by the AKIN criteria: 33 (21%) with stage 1 AKI, 9 (6%) with stage 2 AKI, and only 1 (0.6%) with stage 3 AKI. Of 204 recipients, 57 (28%) underwent KT with kidneys from donors with AKI according to the AKIN classification; 44 (22%), from donors in stage 1; 12 (6%), from donors in stage 2; and 1 (0.5%), from donors in stage 3 (Fig. 1). The remaining 147 recipients were classified into the non-AKI group. This study was approved by the institutional review board of our center (KC13RISI0234), and the need for informed consent from the patients was waived because of the retrospective study design. 2.2. Clinical and biochemical data We collected the baseline data of the donors, including their age, sex, history of diabetes and hypertension, cause of death, last-day urine volume, central venous pressure, and mean arterial pressure (MAP) from the day of admission to the day of KT. In addition, we collected the baseline data of the recipients: age, sex, body mass index (BMI) (kilograms per square meter), history of diabetes and hypertension, type of dialysis, dialysis duration, previous KT number, panel-reactive antibodies (PRAs) percentage, human leukocyte antigen (HLA) mismatch number, and total ischemic time. After KT, most recipients were administered a calcineurin inhibitor such as tacrolimus (162/204, 79%) or cyclosporine (41/204, 20%); sirolimus was used in only 0.5% (1/204) of recipients. Induction therapy using basiliximab (20 mg) was administered on the day of surgery and on postoperative day 4 in all patients. 2.3. Classification of patient population according to AKIN criteria Deceased donors were classified as either the AKI or non-AKI group according to the AKIN criteria. According to the AKIN criteria, stage 1 is defined as an absolute increase in the last serum creatinine

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(SCR) level by 0.3 mg/dL or higher, a 50% or higher increase in the last SCR level from the level on the day of admission, or a reduction in urine output (documented oliguria, b0.5 mL/kg per hour for N6 hours) [8]. Stage 2 is defined as an increase of more than 200% to 300% in the last SCR level from the level recorded on the day of admission or a reduction in urine output (documented oliguria, b 0.5 mL/kg per hour for N 12 hours) [8]. Stage 3 is defined as an increase of more than 300% in the last SCR level from the level recorded on the day of admission or a reduction in urine output (documented oliguria, b 0.3 mL/kg per hour for N 24 hours or anuria for 12 hours) [8]. In this study, the SCR level was measured on the day of admission to our hospital for the pronouncement of brain death. The final SCR level was measured just before organ harvesting. In all patients, the duration between the day of admission and the day of donation was within 48 hours. 2.4. Clinical outcome The primary end point of this study was the development of delayed graft function (DGF), defined as the need for dialysis during the first week after transplantation. Secondary end points included allograft function for 1 year after KT (at 3 days, 2 weeks, 1 month, 3 months, 6 months, and 1 year after KT) determined by the estimated glomerular filtration rate—assessed by the modification of diet in renal disease (MDRD) equation—and long-term patient and allograft survival rates (5- and 10-year survival). We divided the patient population into the AKI and non-AKI groups, with the AKI group subdivided into stage 1 and stage 2/3 AKI groups. We compared the allograft outcome including DGF, change of renal function for 1 year after transplantation, and allograft survival rate between the AKI and non-AKI groups and between the stage 1 AKI and stage 2/3 AKI groups. 2.5. Statistical methods Statistical analysis was performed using SPSS version 20.0 (SPSS, Inc, Chicago, IL). The comparison between the AKI and non-AKI groups was analyzed using the Student t test for numerical values and the χ 2 test for categorical data. All continuous variables were tested for normal distributions using the Shapiro-Wilk test and were expressed as the mean ± SD. Categorical variables are presented as the percentage of the number of cases. We used a nonparametric test, the Mann-Whitney U test, for comparison of allograft function (estimated glomerular filtration rate assessed by the MDRD equation) between AKIN stage 1 and 2/3. After univariate analysis of the risk factors for DGF, significant variables were analyzed by multivariate logistic regression analysis (enter method). Graft and patient survival probability was calculated using a Kaplan-Meier estimate. Differences between survivals were calculated by log-rank analysis. P b .05 was considered as statistically significant. 3. Results 3.1. Baseline characteristics of donors and recipients

Fig. 1. Division of donors into AKI and non-AKI groups and subdivision of recipients in the AKI group who received kidneys from donors with AKI into stages 1, 2, and 3 according to the AKIN classification.

Baseline characteristics and variables of donors obtained during their stay in the intensive care unit are presented in Table 1. The lastday urine volume was larger in the AKI group than in the non-AKI group, but there were no significant differences in other variables associated with AKI between the 2 groups. Furthermore, no difference in variables was noted between the stage 1 and stage 2/3 AKI groups. The recipient characteristics are shown in Table 2. Total ischemic time was significantly longer in the AKI group than in the non-AKI group. However, no significant differences in other recipient parameters, including age, sex, previous KT number, BMI, history of hypertension and diabetes, type of dialysis, PRA (total percentage of HLA class I and II), and HLA mismatch number were noted between the 2 groups.

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Table 1 Donor characteristics and AKI variables Donor

Non-AKI (n = 113)

AKI (n = 43)

P

AKIN 1 (n = 33)

AKIN 2 and 3 (n = 10)

P

Age (y) Male HTN DM Cause of death CVA Trauma Others CVP (cm H2O)a MAP (mm Hg)a Last day urine volume (mL)

41.1 ± 14.6 79 (70) 18 (16) 5 (4.4)

43.3 ± 13.8 32 (74) 8 (19) 3 (7)

.191 .26 .377 .111

45.8 ± 11.6 25 (76) 8 (24) 3 (9)

35 ± 17.5 7 (70) 0 0

.642 .819 .124 .418

27 (24) 32 (28) 54 (48) 7.6 ± 3.7 88.4 ± 14.6 4463 ± 32

6 (14) 16 (37) 21 (49) 8.4 ± 3.8 87.7 ± 18.6 3323 ± 3349

.179 .648 .455 .085 .8 .004

5 (15) 11 (33) 17 (52) 8.2 ± 4.0 90.1 ± 23.8 3243 ± 3253

1 (10) 5 (50) 4 (40) 9.0 ± 3.1 87.0 ± 24.5 3587 ± 3825

.642 .459 .665 .225 .151 .465

All values were presented as mean ± SD or n (%). HTN indicates hypertension; DM, diabetes mellitus; CVA, cerebrovascular accident; CVP, central venous pressure. a Central venous pressure and MAP: mean values during the last 12 hours before KT.

3.2. Comparison of DGF development between the AKI and non-AKI groups according to the AKIN criteria The DGF rate was significantly higher in the AKI group than in the non-AKI group (12.2% vs 42.1%; P b .05; Fig. 2A). In univariate analysis, development of AKI (as defined by the AKIN criteria) in donors and total percentage of PRA in recipients were significant risk factors for the development of DGF (Table 3). In multivariate analysis, development of AKI as defined by the AKIN criteria (odds ratio, 5.044; P = .000) and PRA percentage (odds ratio, 1.028; P = .001) were independent risk factors for the development of DGF (Table 3). No significant difference in the development of DGF was found between the stage 1 and stage 2/3 AKI groups (38.6% vs 53.8%, respectively; P = .329; Fig. 2B). 3.3. Change in allograft function between the AKI and non-AKI groups according to the AKIN criteria Allograft function assessed by the MDRD equation for 6 months after KT showed a significantly deteriorating pattern in the AKI group compared with that in the non-AKI group at each time point (9.1 ± 5.7 vs 19.4 ± 15.6, 43.7 ± 24.8 vs 58.7 ± 26.7, 53.3 ± 32.3 vs 61.3 ± 20.8, 55.0 ± 18.7 vs 61.3 ± 18.1, 56.4 ± 19.1 vs 62.1 ± 18.2 mL/min per·1.73 m 2 at 3 days, 2 weeks, 1 month, 3 months, and 6 months after KT, respectively; P b .05 for each comparison; Fig. 2C). However, allograft function at 12 months after KT did not differ between the AKI and non-AKI groups (58.9 ± 20.6 vs 63.1 ± 23.6 mL/min per 1.73 m 2; P = .209; Fig. 2C). No difference in allograft function was found between the stage 1 and stage 2/3 AKI groups for 12 months after KT (8.3 ± 4.8 vs 11.4 ± 7.5, 42.0 ± 25.3 vs 46.9 ± 18.0 vs 59.2 ± 34.5,

52.5 ± 16.8 vs 62.4 ± 24.8, 53.4 ± 18.7 vs 64.3 ± 20.2, 56.3 ± 22.3 vs 64.3 ± 16.3 in the stage 1 and stage 2/3 groups at 3 days 2 weeks, 1 month, 3 months, 6 months, and 12 months after KT, respectively; P N .05 for each comparison; Fig. 2D). 3.4. Comparison of patient and allograft survival rates between the AKI and non-AKI groups according to the AKIN criteria The long-term allograft survival rate did not differ between the AKI and non-AKI groups (Fig. 3A). The death-censored allograft survival rate was as follows: 5-year survival rate of 91% and 89% and 10-year survival rate of 91% and 82% in the AKI and non-AKI groups, respectively (P = .673). The patient survival rate was also similar between the 2 groups—the 5-year survival rate was 100% and 99%, and the 10-year survival rate was 100% and 99% in the AKI and non-AKI groups, respectively (P = .391; Fig. 3B). Development of acute rejection was not significantly different between the AKI (30%) and non-AKI (26%) groups (P = .49) and did not differ between the stage 1 and stage 2/3 AKI groups either (P = .195). 4. Discussion In the present study, we analyzed the early and long-term allograft outcomes of deceased donor kidneys with AKI, as defined by the AKIN criteria. The incidence of DGF was higher in the AKI group than in the non-AKI group, and early renal function for 6 months after KT was poorer in the AKI group than in the non-AKI group. In addition, the development of AKI as defined by the AKIN criteria was an independent risk factor for the development of DGF. However, the development of AKI was not associated with allograft function after

Table 2 Recipient characteristics Recipient

Non-AKI (n = 147)

AKI (n = 57)

P

AKIN 1 (n = 44)

AKIN 2 and 3 (n = 13)

P

Age (y) Male Retransplant BMI (kg/m2) Primary renal disease GN DM HTN Others Type of dialysis (HD)a Dialysis duration (m) PRA (%) HLA MN Total ischemic time (h)

46.2 ± 8.6 80 (54) 18 (12) 22.7 ± 3.3

49.2 ± 11.5 27 (49) 5 (9) 22.4 ± 2.7

.078 .286 .482 .478

50.3 ± 11.0 21(48) 4(9) 22.3 ± 2.8

45.2 ± 12.9 6(46) 1(8) 22.6 ± 2.1

.157 .92 .876 .783

70 (48) 12 (8) 34 (23) 31 (21) 94 (64) 91 ± 118 11.6 ± 34.8 3.9 ± 1.0 195 ± 103

23 (40) 8 (14) 13 (23) 13 (23) 39 (68) 101 ± 173 15.4 ± 41.2 4 ± 1.2 258 ± 149

.350 .758 .217 .789 .392 .636 .541 .553 .006

19 (43) 4 (9) 12 (27) 9 (21) 28 (64) 109 ± 194 17.2 ± 44.7 4.1 ± 1.2 249 ± 147

4 (31) 4 (31) 1 (8) 4 (31) 11 (85) 71 ± 59 9.3 ± 26.7 3.8 ± 1.4 288 ± 158

.586 .203 .154 .169 .347 .494 .564 .486 .413

All values were presented as mean ± SD or n (%). GN indicates glomerulonephritis; HD, hemodialysis; MN, mismatch number. a The rest relies on peritoneal dialysis.

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Fig. 2. Comparison of allograft outcome between AKI and non-AKI groups. A, Delayed graft function incidence in the AKI and non-AKI groups. Delayed graft function development was significantly higher in the AKI group (42.1%) than in the non-AKI group (12.2%) (P b .05). B, Delayed graft function incidence in the stage 1 and stage 2/3 AKI groups did not differ (38.6% vs 53.8%, respectively; P = .329). C, Allograft function for 6 months after KT showed a significantly deteriorating pattern in the AKI group compared with that in the non-AKI group (Pb .05). However, allograft function at 12 months after KT did not differ between the 2 groups (P N .05). All values were presented as mean ± SD. D, Allograft function for 12 months after KT was not different between the stage 1 and stage 2/3 AKI groups (P N .05). All values were presented as mean ± SD.

1 year from KT and also did not affect the long-term allograft and patient survival rates. In patients considered deceased donors, AKI commonly developed during their stay in the intensive care unit as a result of ischemic and nephrotoxic insults [4]. In this study, 27.6% of the recipients received kidneys from deceased donors with AKI, which was similar to the results (27.9%) in previous reports [10,11]. Excluding all of these donors with AKI from organ donation will result in a significant decrease in the number of transplants. However, with regard to the outcome of KT from deceased donors with AKI, a clear conclusion has not been established. First, we compared the development of DGF, which manifests as severe ischemia-reperfusion injury in the graft [12,13]. In this study, the DGF prevalence was significantly higher in the AKI group than in the non-AKI group. Kidneys with preexisting AKI before KT may be more vulnerable to ischemic injury during harvest and additional injuries such as those resulting from the use of a calcineurin inhibitor; hence, a higher DGF prevalence may occur in the AKI group. Acute kidney injury as defined by the AKIN criteria in deceased donors and a high PRA level in recipients were independent risk factors for the development of DGF in multivariate analysis. This finding is consistent with previous reports that showed that both immunologic and nonimmunologic factors are associated with DGF [12,14-16]. Short-term allograft function for 6 months after KT was also lower in the AKI group than in the nonAKI group. During the early posttransplant period, the severity of a preexisting allograft tissue injury may affect allograft function because natural repair of the renal parenchyma or tubule from AKI has not been completed; hence, this group might have inferior allograft function.

Second, we investigated whether AKI in donors affects long-term allograft function or allograft survival. We found that allograft function at 1 year after KT as well as long-term patient and allograft survival rates did not differ between the AKI and non-AKI groups. The phases of AKI in nontransplanted kidneys include initiation, repair, and recovery, and the repair process of AKI continues and peaks between 90 days and 6 months [17-23]. After this period, the long-

Table 3 Multivariate analysis for development of DGF Univariate

Multivariate

OR

95% CI

P

Donor Age DM HTN AKI (by AKIN) CVP MAP Last day urine volume Total ischemic time Cause of death (CVA)

1.005 1.703 1.096 5.336 1.061 1.004 1.00 1.002 0.640

0.981-1.030 0.421-6.889 0.438-2.741 2.595-10.972 0.964-1.168 0.975-1.034 1.00 1.000-1.005 0.296-1.383

.664 .455 .845 .000 .229 .798 .413 .1 .256

Recipient Age Male DM HTN BMI PRA (%) HLA MN

1.022 1.132 1.671 1.041 1.053 1.013 0.947

0.985-1.059 0.574-2.231 0.678-4.114 0.329-3.296 0.946-1.173 1.003-1.022 0.694-1.292

.245 .721 .264 .945 .344 .008 .73

OR

95% CI

P

5.044

2.215-11.488

.000

1.028

1.011-1.046

.001

OR indicates odds ratio; CI, confidence interval; CVA, cerebovascular accident.

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Although the DGF rate was higher in the AKI group, the long-term outcome in the AKI group was not inferior compared with the non-AKI group. This finding is not consistent with some studies that have found that DGF is associated with an increased risk of a long-term outcome such as graft failure or mortality [25,26]. Interestingly, DGF associated with donors with AKI in KT does not have a detrimental effect on medium-term graft survival, but DGF occurring in non-AKI standard criteria donor kidneys has a significant effect and decreases 3-year graft survival [11]. However, further investigation may be required to clarify this issue. This study has some limitations. First, this was a retrospective study. A prospective controlled study may be required to clearly indicate the impact of AKI, as defined by the AKIN criteria, on allograft outcome in deceased donors. Second, the AKIN criteria impose time constraints of 48 hours, which may limit the use of these criteria in potential deceased donors. According to guidelines for the management of deceased donors in Korea, when a patient is suspected as brain dead and the patient's family agrees with deceased donor organ transplantation, the patient should be transferred to an appointed institution for the pronouncement of brain death. After admission to an appointed institution such as our hospital, all of the processes including pronouncement of brain death and organ harvesting usually are completed within 48 hours. Therefore, in all patients, at least in this study, the final SCR level before KT on the day of donation was measured within 48 hours of the baseline SCR level measurement on the day of admission. In conclusion, in deceased donor KT, the definition of AKI using the AKIN criteria in donors is useful to predict DGF development after transplantation and graft function for 6 months after KT. However, the long-term allograft outcome from deceased donors with AKI was not inferior to that from donors without AKI; hence, the development of AKI, as defined by the AKIN criteria, in potential donors could not be considered an exclusion criterion for kidney donation.

Acknowledgment

Fig. 3. Patient and allograft survival between AKI and non-AKI groups. A, The deathcensored allograft survival rate between the AKI and non-AKI groups did not differ significantly between the 2 groups (log rank = 0.673). B, The patient survival rate between the AKI and non-AKI groups was also similar between the 2 groups (log rank = 0.391).

term outcome of the kidney would not be influenced by AKI, which could also apply to the outcome of allografts from donors with AKI. We found that the AKI group showed poorer early outcomes such as a higher DGF rate and lower allograft function for 6 months after KT than the non-AKI group, which corresponds to inferior initiation and repair phases of the AKI group as described previously. However, allograft function at 1 year after KT and long-term survival did not differ between the AKI and non-AKI groups, which suggest that preexisting AKI may not affect the long-term outcome of the allograft kidney after completion of the repair process. It is well known that the AKI stage is an important determinant of renal outcome in nontransplanted kidneys [17,24]. However, the clinical outcomes of the kidney allograft including DGF development, change of allograft function, and allograft survival rate were not significantly different between the stage 1 and stage 2/3 groups in this study. In contrast to the nontransplanted kidney, the kidney allograft essentially received additional ischemic insult during the transplant procedures, and many other factors may affect graft outcome; hence, it is possible that the severity of a baseline kidney injury may have less impact in a transplanted kidney than in a nontransplanted kidney. However, because of the limited number of stage 2/3 recipients, no clear conclusion can be drawn from this study.

This research was supported by Seoul St Mary's Hospital Clinical Medicine Research Program for 2013 through the Catholic University of Korea.

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Clinical outcome of kidney transplantation from deceased donors with acute kidney injury by Acute Kidney Injury Network criteria.

In this study, we investigated the outcome of kidney transplantation (KT) from deceased donors with acute kidney injury (AKI), as defined by the Acute...
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