Kidney Damage During Organ Recovery in Donation After Circulatory Death Donors: Data From UK National Transplant Database

Authors


Fabio Ausania, f.ausania@googlemail.com

Abstract

During the last 10 years, kidneys recovered/transplanted from donors after circulatory death (DCD) have significantly increased. To optimize their use, there has been an urgent need to minimize both warm and cold ischemia, which often necessitates more rapid removal. To compare the rates of kidney injury during procurement from DCD and donors after brain death (DBD) organ donors. A total of 13 260 kidney procurements were performed in the United Kingdom over a 10-year period (2000–2010). Injuries occurred in 903 procedures (7.1%). Twelve thousand three hundred seventy-two (93.3%) kidneys were recovered from DBD donors and 888 (6.7%) from DCD donors. The rates of kidney injury were significantly higher when recovered from DCD donors (11.4% vs. 6.8%, p < 0.001). Capsular, ureteric and vascular injuries were all significantly more frequent (p = 0.002, p < 0.001 and p = 0.017, respectively). Discard because of injury was more common after DCD donation (p = 0.002). Multivariate analysis demonstrated procurement injuries were significantly associated with DCD donors (p = 0.035) and increased donor age (<0.001) and donor body mass index (BMI; 0.001), donor male gender (p = 0.001) and no liver donation (0.009). We conclude that procurement from DCD donors leads to higher rates of injury to the kidney and are more likely to be discarded.

Abbreviations 
BMI

body mass index

DCD

donors after circulatory Death

DBD

donors after brain death

ICH

intracranial hemorrhage

HBD

hypoxic brain damage

NHSBT

National Health Service Blood and Transplant

RTA

road traffic accident

OTH

other

NORS

National Organ Retrieval Service

Introduction

During the last 10 years, kidneys recovered and transplanted from donors after circulatory death (DCD) have significantly increased, following a number of reports demonstrating equivalence in long-term outcome (1–3).

To optimize their use, there has been an urgent need to minimize both warm and cold ischemia, which often necessitates less dissection and more rapid removal. This combination makes kidney procurement from DCD donors a more challenging operation (4).

As reported before by Wigmore et al. in 1999 (5), injuries during kidney procurement for organ transplantation are relatively common (19%) and can result in the organ being discarded.

The aim of this study was to identify the frequency of renal injuries during organ procurement from donors within the United Kingdom and verify whether DCD donation is associated with a higher rate of damage.

Methods

Data obtained from the National Health Service Blood and Transplant (NHSBT) database on all kidneys (DBD and DCD) recovered from deceased donors within the United Kingdom and Ireland between January 2000 and February 2010 was retrospectively reviewed. As a routine, the anatomy of the recovered organ and any damage noted at recovery is documented on the HOT A NHSBT form, which the retrieving surgeon is responsible for completing. The information provided by the retrieving surgeon included: capsular injuries (stripping or tearing of the renal capsule and hematomas, ureteric injuries including inadvertently short ureters and cut renal veins and cut main or polar renal arteries. In addition, information was obtained on outcome including: kidneys used, kidneys accepted by an implanting center but not used for implant and nonacceptance by an implanting center. Reason for the kidney being discarded was also documented.

Additional donor data, including age, body mass index (BMI), cause of donor death and whether or not the liver was recovered at the same time. As described before by Wigmore et al., we classified centers into two groups according to the average number of recovery procedures done each year (less than 50 and more than 50 recovery procedures each year).

Statistical analysis

The results were analyzed using the chi-square test. For means in case of continuous numeric data, we used the independent samples t-test and the Mann–Whitney U test, respectively, for data normally and nonnormally distributed; the data were previously tested for normality by the Kolmogorov–Smirnov test. Multivariate analysis of statistically significant variables was performed using binary logistic regression. All statistical analyses were done with the statistical software package SPSS (version 17; SPSS Inc., Chicago, IL, USA).

Results

A total of 13 260 kidneys were recovered from deceased donors during January 2000 to February 2010 (Figure 1) and of these 888 (6.7%) were recovered from DCD donors.

Figure 1.

Number of kidneys recovered from January, 2000 to February, 2010 showed according to type of donor: donation after brain death (DBD) and donation after circulatory death donors (DCD).

Median donor age was 47 years (range: 0–85), median donor BMI was 25 (range: 7–69). The Distribution by donor age, sex, BMI, cause of death, concomitant liver donation and recovery unit volume is showed in Table 1.

Table 1.  Distribution of kidneys donated by donor characteristics and recovery unit volume
 TotalDBDDCDp-Value
  1. ICH = intracranial hemorrhage or thrombosis; RTA = road traffic accident or trauma; HBD = hypoxic brain damage (all causes); OTH = other or unknown.

Age years, median (range)47 (0–85)44.2 (0–85)46.89 (1–80)<0.001
Sex (%)   <0.001
 Male6912 (52.1)6378 (48.1)534 (4.0) 
 Female6346 (47.9)5992 (45.2)354 (2.7) 
 Total13 258 (100.0)12 370 (93.3)888 (6.7) 
BMI median (range)25 (7–69)25.5 (7–69)26.4 (11–60)<0.001
Cause of death (%)   <0.001
 ICH8848 (66.7)8426 (63.5)422 (3.2) 
 RTA2046 (15.4)1898 (14.3)148 (1.1) 
 HBD1136 (8.6)946 (7.1)190 (1.4) 
 OTH1230 (9.3)1102 (8.3)128 (1.0) 
 Total13 260 (100.0)12 372 (93.3)888 (6.7) 
Liver donation (%)   <0.001
 Yes11 632 (87.7)11 230 (84.7)402 (3.0) 
 No1628 (12.3)1142 (8.6)486 (3.7) 
 Total13 260 (100.0)12 372 (93.3)888 (6.7) 
Retrieval unit (%)   NS
 >50/year8562 (64,6)8002 (60.3)560 (4.2) 
 <50/year4698 (35.4)4370 (33.0)328 (2.5) 
 Total13 260 (100.0)12 372 (93.3)888 (6.7) 

Injuries occurred in 903 procedures (7.1%). Capsular, ureteric and vascular injuries occurred in 1.7%, 0.7% and 4.8% procurements, respectively. Rates of kidney injury were significantly higher when recovered from DCD donors (11.4% vs. 6.8%, p < 0.001). Capsular, ureteric and vascular injuries were significantly more frequent in kidneys from DCD donors when compared to DBD donors (p = 0.002, p < 0.001 and p = 0.017, respectively; Table 2).

Table 2.  Organ damage according to type of donor
 TotalDBD (%)DCD (%)p-Value
Capsular damage   0.002
 Yes220 (1.7)193 (1.6)27 (3.2) 
 No12 557 (98.3)11 740 (98.4)817 (96.8) 
 Total12 777 (100.0)11 933 (100)844 (100) 
Ureter damage   <0.001
 Yes90 (0.7)71 (0.6)19 (2.3) 
 No12 677 (99.3)11 856 (99.4)821 (97.7) 
 Total12 767 (100.0)11 927 (100)840 (100) 
Renal vein damage   0.243
 Yes296 (2.3)273 (2.3)23 (2.7) 
 No12 478 (97.7)11657 (97.7)821 (97.3) 
 Total12 774 (100.0)11 930 (100)844 (100) 
Renal artery damage   0.336
 Yes199 (1.6)184 (1.5)15 (1.8) 
 No12 574 (98.4)11 745 (98.5)829 (98.2) 
 Total12 773 (100.0)11 929 (100)844 (100) 
Polar artery damage   0.023
 Yes158 (1.2)140 (1.2)18 (2.1) 
 No12 610 (98.8)11 784 (98.8)826 (97.9) 
 Total12 768 (100.0)11 924 (100)844 (100) 
Vascular damage   0.017
 Yes617 (4.8)563 (4.7)54 (6.4) 
 No12 148 (95.2)11 358 (95.3)790 (93.6) 
 Total12 765 (100.0)11 921 (100)844 (100) 
Presence of at least one injury   <0.001
 Yes903 (7.1)807 (6.8)96 (11.4) 
 No11 856 (92.9)11 111 (93.2)745 (88.6) 
 Total12 759 (100.0)11 918 (100)841 (100) 

In addition Table 3, suggests that DCD donated organs are more likely to be discarded by the potential recipient center (p < 0.001) as a result of damage.

Table 3.  Outcome of donated kidneys
 Total (%)DBD (%)DCD (%)p-Value
Kidney status   <0.001
 Used12 418 (94.6)11 675 (95.3)743 (85.7) 
 Not accepted41 (0.3)38 (0.3)3 (0.3) 
 Accepted and not used664 (5.1)543 (4.4)121 (14.0) 
 Total13 123 (100)12 256 (100)867 (100.0) 
Kidneys not used for damage   0.001
 Yes112 (0.8)95 (0.8)17 (1.9) 
 Total13 259 (100)12,371 (100)888 (100) 

Univariate analysis suggests that donor age, high BMI, male gender and DCD donor type were significantly associated with a higher rate of injury. Not retrieving the liver at the donor operation was also associated with increased kidney damage (Table 4).

Table 4.  Univariate analysis: donor age, BMI and male gender, no liver donation and DCD donor type are significantly associated with organ damage
 No InjuryInjuryp-Value
Donor age (years, median)44.247.24<0.001
Donor BMI25.526.4<0.001
Kidney side (%)  0.167
 Left5853 (93.2)424 (6.8) 
 Right6003 (92.6)479 (7.4) 
 Total11 856 (92.9)903 (7.1) 
Sex  0.001
 Male6133 (92.2)518 (7.8) 
 Female5721 (93.7)385 (7.3) 
 Total11 854 (92.9)903 (7.1) 
Type of donor (%)  <0.001
 DBD11 111(93.2)807 (6.8) 
 DCD745 (88.6)96 (11.4) 
 Total11856 (92.9)903 (7.1) 
Liver donation  <0.001
 Yes10 475 (93.4)739 (6.6) 
 No1381 (89.4)164 (10.6) 
 Total11 856 (92.9)903 (7.1) 
Cause of death  0.085
 Intracranial hemorrhage or thrombosis7918 (92.9)602 (7.1) 
 Road traffic accident or trauma1841 (93.9)119 (6.1) 
 Hypoxic brain damage (all causes)1022 (92.4)83 (7.6) 
 Other or unknown1075 (91.6)99 (8.4) 
 Total11 856 (92.9)903 (7.1) 
Year  0.090
 2000–20056167 (93.3)443 (6.7) 
 2006–20105689 (92.5)460 (7.5) 
 Total11 856 (92.9)903 (7.1) 
Recovery unit volume  0.516
 >50 per year7690 (93.0)576 (7.0) 
 <50 per year4166 (92.7)327 (7.3) 
 Total11 856 (92.9)903 (7.1) 

Multivariate analysis (binary logistic regression) demonstrated procurement injuries were significantly associated with DCD donors (p = 0.035) and donor age, donor BMI, donor male gender and no liver donation (Table 5).

Table 5.  Multivariate analysis: donor age, BMI and male gender, no liver donation and DCD donor type are significantly associated with organ damage
 p-ValueOR95% CI
Donor age<0.0011.0101.005–1015
Donor BMI0.0011.2581.102–1.436
Donor male gender0.0011.2811.113–1.476
No liver donation0.0091.3181.072–1.622
DCD donor0.0351.3301.020–1.733

Discussion

In 1999, Wigmore et al. published the largest series of kidney procurement injuries. They found that only 98 of 9014 (1%) kidneys recovered were not transplanted because of damage. It was emphasized that even though injuries occurred quite often (19%), the long-term outcome of an injured kidney, when the damage is repairable, is not significantly different. In that series, kidney damage was least likely to occur when kidneys were recovered from young donors and when liver teams or centers undertaking more than 50 recoveries per year did the recovery.

During the last 10 years, there has been a significant increase in the number of DCD donors. This has been as a result of published data from a number of centers suggesting that the outcome of kidneys transplanted from DCD donors is comparable to DBD's outcome (6–8) . Virtually, all centers in the United Kingdom are now accepting kidneys recovered from DCD donors and the numbers are increasing year on year; in November 2011, 697 kidneys were recovered from DCD donors and 567 kidneys were transplanted and the numbers are still increasing year on year (9–10) with some centers successfully exploring longer agonal-phase times (11).

Although, our study demonstrated a higher rate of damage in the DCD procurements overall; damage was reported in 11.4% of the cases (as opposed to the 19% reported in 1999), showing that a significant effort has been made in the last 10 years to improve the training in organ procurement; new measures have been recommended by the UK Transplant Task Force in 2008 and only dedicated teams are now responsible for the organ procurement procedures (12). In addition, the number of kidneys discarded because of damage was lower overall (0.8% vs. 1%), although higher in the DCD population (1.9%): it is difficult to establish whether concurrent concerns such as poor perfusion and ischemic time played a role in discarding the organs. In fact, the stronger association was with ureteric and polar artery injuries, which rarely make the organ unusable. Further data analysis will be able to ascertain whether the increased damage, seen with DCD kidney procurement, has an impact on postoperative complications and graft survival, although there are many other factors which can account for graft loss not just renal damage (e.g. acute rejection, vascular thrombosis, prolonged ischemia and recurrent disease).

The other factors found to be significantly associated with an increased rate of injury were already known: such as donor age, possibly associated with more calcified vessels and "kidney only" procurement, perhaps suggesting that access was not as good, and less technical expertise present at the procedure when the liver is not removed.

This audit predates National Organ Retrieval System (NORS; April, 2010) and at that time 28 centers were involved in the kidney procurement. We did not find any difference in terms of injuries related to number of organs procured per year, using as a cut-off value 50 procedures per year as reported before by the Scottish Liver Transplant Centre.

Both male pelvis and high BMI are associated with a narrower surgical exposure and with a more challenging cold dissection and unsurprisingly there was a strong association of these factors with damage.

It is important to note that we did not include any damage reported by the recipient centers, because robust data was not readily available and sometimes not interpretable. Clearly identifying bench-work related injuries, was not possible but could be important as additional dissection can sometimes reveal other injuries. In addition, we decided not to include damage to the "renal artery aortic patch" because this injury now rarely results in the organ being discarded, largely because of the increasing expertise gained with living donation renal transplantation.

Other clinical factors such as the presence of bowel contamination (which seems to be more frequent in DCD donors) and the subjective assessment of "poor organ perfusion" made by the retrieving surgeon possibly may also contribute to the organ being discarded. It is intuitive that an injured DCD kidney is more likely to be discarded than a similarly injured DBD kidney: in fact, not just the injury leads to discard, but a combination of injury plus other DCD factors such as warm ischemic time, donor agonic time and flush characteristics. Unfortunately, this was not possible to accurately assess and we believe this data should be collected in the future.

In conclusion, DCD donation is associated with a significantly increased incidence of procurement related kidney damage, especially with regard to ureteric and polar artery injuries. The awareness of this issue should lead to an optimization of procurement techniques to improve the quality of this increasingly important resource for renal transplantation.

Author Contributions

Fabio Ausania performed study, analyzed data and wrote the paper; Steven White wrote the paper; Phil Pocock collected and analyzed data; Derek Manas wrote the paper.

Disclosure

The authors of this manuscript declare that the manuscript was not prepared in any part by a commercial organization and it was not funded in any part by a commercial organization, including educational grants.

The authors of this manuscript have no conflicts of interest to disclose as described by the American Journal of Transplantation.

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