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Pediatric En Bloc Kidney Transplantation to Adult Recipients: More Than Suboptimal?

Bhayana, Suverta1; Kuo, Yong-Fang1; Madan, Pankaj2; Mandaym, Sreedhar2; Thomas, Philip G.3; Lappin, Jacqueline A.4; Rice, James C.5; Ishihara, Kanae6,7

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doi: 10.1097/TP.0b013e3181e641f8
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Abstract

Although there are conflicting views in the transplant community, the transplantation of small pediatric kidneys into adult recipients has become an acceptable option (1–11) as expanded criteria donor (ECD) kidneys to overcome scarcity of available kidneys (12–15). The recovery and utilization of ECD kidneys have increased (15) as the benefit has been demonstrated in the selected patient population (14, 16, 17). However, the number of kidneys recovered from the donors aged 0 to 5 years remains small in the United States (3.7% of deceased kidney in 2008 and 4.2% between January 1, 1988, and January 31, 2009) (18) despite the effort to use such kidneys from young pediatric donors by many authors (1, 7, 9, 10, 19–22). The use of small pediatric kidneys into adult recipients, transplanted as en bloc, showed similar outcomes to transplants from standard adult deceased donors, and better than kidneys from donors older than 60 years (5), in part due to a greater renal reserve (23) with excellent long-term results (24–26). However, the opinions on the use of pediatric kidneys and paired versus single kidneys from such young donors to adult recipients for transplantation are still conflicting with only retrospective study results available. Many groups have reported a benefit of use of en bloc kidney (EBK) over solitary pediatric (SP) kidneys (7, 20, 21, 27–29), whereas others argue SP kidneys to adult recipients are acceptable and better use of limited resource (2, 4, 7, 8, 30, 31).

The purpose of this study is to examine the long-term outcomes of EBK transplants from small pediatric donors (age younger than 5 years) to solitary kidney transplants from small pediatric donors (age younger than 5 years), standard adult donors (age 18–59 years), and ECD to adult recipients using United Network of Organ Sharing (UNOS)/STAR data.

MATERALS AND METHODS

We analyzed data from UNOS/STAR files on primary deceased donor kidney transplants to adult recipients from January 1, 1988, to December 31, 2006. The outcomes of EBK transplants (age younger than 5 years) were compared with solitary kidney transplants from young (age younger than 5 years), 3:1 matched standard adult donor (age 19–59 years), and 2:1 matched ECD kidney transplants, matched by age, sex, region, and year of transplant for the small pediatric kidney recipients. In this study, we defined ECD as any deceased donors older than the age of 60 years or between the age of 50 and 59 years with any of the following comorbidities: history of hypertension, a terminal serum creatinine of more than 1.5 mg/dL, proteinuria, or death resulting from a cerebrovascular accident or cardiovascular disease. Delayed graft function was defined as need for dialysis during the first week posttransplant.

The differences of donor, recipient demographic, transplant and immunologic variables, and complications across four transplant types were compared by chi-square for any categorical variables and by analysis of variance for any continuous variables. Graft survival (GS) rates at 6-, 12-, 60-, and 120-month follow-ups for each transplant type were calculated by Kaplan-Meier estimation and tested by log-rank test. A Cox regression model with transplant types as a time-dependent covariate was used to compute graft loss hazard ratios (HRs), adjusted for covariates known to be associated with graft failure by others (21, 27); age, sex, race, cold ischemic time, warm ischemic time, panel reactive antibody, human leukocyte antigen, use of pump, graft thrombosis, and dialysis first week posttransplant. The covariate-adjusted GS curves were estimated by stratified Cox model in which the types of transplants were stratified. This approach allowed the time varying hazard for different types of transplants.

The estimated glomerular filtration rate (eGFR) (mL/min/1.73 m2) (32, 33) was calculated using four variables: age, sex, race, and serum creatinine concentration (34, 35) that is known to give results similar to the six-variable equation (36, 37). The abbreviated modification of diet in renal disease (aMDRD) equation was used due to lack of variables including albumin and urine urea nitrogen in the registry database. Therefore, eGFR=aMDRD formula=186×(serum creatinine)−1.154× (age)−0.203×0.742 (for female) or ×1.212 (for African American). We did not use the reexpressed formula because the serum creatinine values were not standardized (33). The median eGFR values at 5 to 8, 11 to 14, 23 to 26, 35 to 38, 47 to 50, and 59 to 62 months of follow-up for each transplant type were reported and tested by the Kruskal-Wallis test. All analyses were performed with SAS software, version 9.1 (SAS institute, Cary, NC).

RESULTS

Donor and Recipient Characteristics

There were 19,188 adult primary kidney transplant recipients available for our study after matching for the variables (see Materials and Methods). There were 1696 EBK from donors aged younger than 5 years, 1502 solitary kidney transplants from donors aged younger than 5 years, 9594 transplants from standard adult donors aged 18 to 59 years, and 6396 ECD single kidney transplants. Donor and recipients demographics, transplant, and immunologic variables are shown in Table 1.

TABLE 1
TABLE 1:
Various donor and recipients demographics, transplant, and immunologic variables in primary deceased donor transplants in adult recipients by donor type

The EBK donors were significantly younger than SP kidney donors (age 1.7±1.2 years vs. 2.7±1.2 years, P<0.0001). The body weight of EBK donors was lower than SP kidney donors (12.5 ± 3.8 kg vs. 15.8 ± 4.8 kg, P<0.0001). The recipients of the both EBK and SP kidneys (age younger than 5 years) had lower body mass index than the recipients of kidneys from adult donors (P<0.0001). Both cold and warm ischemia times were longer in EBK than SP kidney, standard adult donor, and ECD transplants (P<0.0001). Hispanics were less likely to get EBK transplants when donors were young.

Allograft Survival

Table 2 shows GS probability estimates. All kidney transplants from pediatric donors (age younger than 5 years) had lower GS than all adult donor transplants at 6-month posttransplant (P<0.001). The GS was best for standard adult kidney transplants and worst for the SP donor transplants during the first 12 months posttransplant. The GS for EBK became comparable with standard adult kidney transplants by 60 months posttransplant and the best at the end of the study period (120 months posttransplant) (P<0.001). The adjusted HRs with 95% confidence interval (CI) for graft loss in the study population are shown in Table 3. During the first 6 months posttransplant, the risk of graft failure was highest for SP donor (HR: 1.97; CI: 1.62–2.40), followed by EBK (HR: 1.86; CI: 1.52–2.29) and ECD (HR: 1.67; CI: 1.47–1.90) kidney transplants, when compared with standard adult donors. However, 6 months posttransplant, the risk of graft failure decreased for EBK (HR: 0.74; CI: 0.61–0.89), and the risk for pediatric solitary kidney was comparable with adult standard kidney transplants. The risk of graft failure for ECD transplants became the highest after 6 months posttransplant (HR: 1.73; CI: 1.59–1.88). The adjusted GS curves are shown in Figure 1.

TABLE 2
TABLE 2:
Graft survival probability estimates for primary deceased donor transplants to adult recipients by donor type
TABLE 3
TABLE 3:
Adjusted hazard ratios for graft loss in primary deceased donor kidney transplants in adult recipients
FIGURE 1.
FIGURE 1.:
Adjusted graft survival. EBK, en bloc kidney; ECD, expanded criteria donor.

The complications after kidney transplantation in our cohort are shown in Table 4. All pediatric donor kidney transplants had higher incidence of graft thrombosis than standard adult kidney transplants. Acute rejection rates were not higher for EBK (6.0%) but were higher for SP (9.0%) and ECD transplants (8.2%) than standard adult donor transplants (6.3%; P<0.0001). The delayed graft function rates were highest for ECD kidney transplants (34.8%) and lowest for EBK (17.9%) and were similar for SP (24.4%) and standard adult donor transplants (24.2%; P<0.0001). The rate of recurrent kidney diseases was lowest in EBK (1.1%); however, these rates were not statistically different among all study cohort (P=0.2477).

TABLE 4
TABLE 4:
Complications after kidney transplantation

Allograft Function

Figure 2 shows the serial median eGFR as estimated by aMDRD equation for the cohort. The median eGFR was highest in EBK and lowest in ECD transplants throughout the study period (P<0.0001). The median eGFR of SP donor kidney transplants was similar at 6 months and became higher than the eGFR of standard adult kidney transplants by 12 months with a continuous increase until 36 months resulting in a significantly higher eGFR than standard adult kidney transplants by 60 months posttransplant (57.4 vs. 47.9 mL/min/1.73 m2) (P<0.0001). The eGFR of both EBK and pediatric donor kidney transplants increased over time, whereas the eGFR of standard adult kidney and ECD transplants decreased during the study period.

FIGURE 2.
FIGURE 2.:
Glomerular filtration rate (GFR) by abbreviated modification of diet in renal disease (aMDRD). EBK, en bloc kidney; ECD, expanded criteria donor.

DISCUSSION

In our analysis of UNOS data from 1988 to 2006, EBK from pediatric donors (age younger than 5 years) to adult recipients had better long-term GS than SP donor kidney (age younger than 5 years), and the best long-term GS over standard adult donor and ECD kidney transplants despite higher graft loss during the first 12 months posttransplant. In addition, the allograft function of EBK transplants improved consistently over time and was the best throughout the study among our cohort, whereas the graft function of standard adult donor and ECD transplants declined over time. We demonstrate the superiority of the pediatric EBK to adult recipients over adult standard and ECD transplants using large national data that was previously shown in single-center studies.

Clinical kidney transplants using SP deceased donor kidneys were reported in the early 1960s (38), followed by increasing interest in the use of paired pediatric deceased donor kidneys as en bloc with the first case to a pediatric recipient (39) and thereafter, to adult recipients showing possible advantage of more renal reserve and technical feasibility (9, 10, 19). The various strategies have improved the outcome of EBK pediatric donor transplants, including changes in techniques (40–43), selection of the recipients and immunosuppression (6, 11, 24). Many case series have reported excellent long-term results (24, 26, 44–46), similar GS to standard adult donor kidney transplants (7, 47, 48), or similar GS to adult donor kidney transplants beyond the first 3 months despite higher rates for early graft losses in EBK when donors were young (≤12 months of age) (43).

The debate on the use of kidneys from young pediatric kidneys as single (solitary) versus en bloc lead to polarized opinions until recent analyses of UNOS data demonstrated that EBK had better GS than SP donor kidney when donors were younger than 5 years of age (21) or small (<21 kg) (7, 20), and similar GS to ideal adult donors (7).

Many single-center studies have reported the use of SP kidney transplants have comparable GS with ideal adult deceased donor kidney transplants despite of higher rate of urological complications (3) or comparable GS when donor age was older than 2 years (4, 49). Some have argued that there is no appreciable advantage achieved by using two pediatric kidneys for a single recipient because kidneys from deceased donors younger than 5 years of age, transplanted as single or en bloc, have suitable kidney function to adult recipients (2). There are also suggestions when to separate en bloc pairs into solitary allografts based on donor weight or donor kidney size to obtain comparable outcomes of SP kidney transplants to EBK (8, 30, 31, 50). Size-match-based allocation for solitary kidney transplants from pediatric donors was also suggested (51).

Others argue that the use of en bloc optimizes the long-term outcomes of transplants from donors younger than 2 years of age because GS was better in EBK than SP transplants (28). These results suggest that en bloc should remain the technique of choice for donors younger than 5 years of age because EBK showed a trend toward a lower vascular thrombosis rate but had similar long-term GS to SP donor kidney transplants (29). Moreover, GS of EBK from small pediatric donors was similar to adult live donor kidney transplants 5 years posttransplant (52).

In our study, the long-term GS of EBK was better than SP donor kidney transplants to adult recipients that is consistent with findings in studies using a large database by Dharnidharka et al. (21), Pelletier et al. (7), Kayler et al. (20), and Bresnahan et al. (27) and also in single-center studies (28, 29). However, our study also demonstrates that EBK transplants have better GS than standard adult transplants. This is not consistent with observations by most of the studies. The comparable GS of EBK with standard donor kidney transplants was reported by Pelletier et al. (7), Shapiro et al. (5), and other authors (43, 47, 48, 53), however, the superiority of EBK over standard adult kidney transplants was only reported by Maranes et al. (23), and the superiority of EBK over living donor kidney transplants was observed by Sureshkumar et al. (52).

The allograft function of EBK was compared with other kidney transplants by various authors. Mean serum creatinine of EBK was lowest and not only similar to adult deceased donor but also living donor kidney transplants up to 10-year follow-up (25). The significantly lower serum creatinine was seen in EBK than adult donor transplants by 6 months and stayed lower 1, 3, and 5 years posttransplant (P<0.001) (43). Serum creatinine values and calculated creatinine clearance were significantly better in EBK than all other deceased donor kidney transplants up to 3 years posttransplant (5). The eGFR calculated by Cockcroft-Gault formula was significantly higher in EBK than single pediatric kidney transplants from donor weighing less than 15 kg at 1 year posttransplant (8) and was also significantly better in EBK (mean age 20.5±1.0 months) than transplants from adult donors throughout the study (at 1–5 year posttransplant) (48). The GFR measured as inulin clearance and renal plasma flow calculated as PAH clearance after infusion of amino acid increased in EBK, whereas GFR or renal plasma flow did not increased in adult donor kidney transplants (P<0.05 and P<0.01, respectively), reflecting greater renal functional reserve in EBK (23). Kidney volume of EBK by sonograms showed threefold increase and the GFR measured by 99mtechnetium-diethylenetriaminepentaacetic acid showed fivefold increase by 6 months while resistive indices and recipient blood pressure remained at normal range in 21 EBK transplants from infants to adult recipients (54). Allograft function estimated by aMDRD formula showed significantly higher in EBK from pediatric donors than live adult donor kidney transplants up to an 8-year follow-up without significant increase in proteinuria (52). We used aMDRD in our study due to limitation of available variables but still providing a better measure of allograft function than serum creatinine values alone. Our study supports the benefit of EBK in allograft functional reserve observed by others.

Once EBK survives the early vascular complications reflected as higher rate of thrombosis, their functional capacity continues to increase rapidly over time, potentially providing the best long-term graft outcome among deceased donor transplants. This may be explained by the benefit of not only having larger total renal mass (vs. SP donor kidney transplants) but also significant increase in GRF (vs. standard adult and ECD transplants). These results are consistent with experimental findings of Larsson et al. (55) and Hayslett (56) that compensatory renal growth after unilateral nephrectomy in rats at an early age is largely dependent on the developmental stage of the kidney at the time of the nephrectomy with an inverse correlation to age and is more pronounced when nephrectomy is performed before normal nephrogenesis is complete. The use of pediatric deceased donor kidney to adult recipients was traditionally believed to cause hyperfiltration damage leading to graft loss due to the disparity between the size of the recipient and the donor (57, 58). However, there is little evidence that the rate of hyperfiltration damage is actually higher in pediatric EBK (25, 44). Moreover, the incident and the degree of proteinuria in EBK are similar to living donor kidney transplants (52). EBK optimizes the graft outcome by overcoming small renal mass in addition to a better renal compensatory ability of young pediatric kidneys, compared with kidneys from adult donors, eliminating hyperfiltration injury.

Our study showed the acute rejection rate for EBK was similar to standard kidney transplant, whereas the acute rejection rate for SP transplants was similar to ECD transplants but the highest. Although the reason for this is unclear, one possible explanation is that transplantation of a larger mass of allograft tissue may confer protection from rejection (host vs. graft reaction) in the long term, as is known to occur in the case of liver and multivisceral transplantation.

The use of kidneys from donors traditionally considered as nonideal including young pediatric donors and ECD became necessary to overcome ever-increasing shortage of available kidneys. Our study also demonstrates that solitary kidney transplants from small pediatric donors had better long-term renal function and similar GS, comparing with standard adult donors, despite the challenges of graft thrombosis and acute rejection during the early postoperative period. Transplants of SP donor kidney also have same advantage as en bloc in compensatory renal growth capacity that is better than adult donor transplants. Although transplants of EBK appear to be more beneficial than SP kidney transplants, SP kidney transplants may provide adequate outcomes when pediatric donors are older and heavier as suggested by some authors (30, 31, 50). Establishing evidence-based guidelines for selection criteria when to separate “en-bloc” kidneys into single kidneys, along with careful selection of immunosuppressive regimen and recipients, may increase available kidneys for transplants with better graft outcomes and optimize the use of small pediatric kidneys. Furthermore, an effort should be always made to increase recoveries of pediatric small kidneys overall, especially as en bloc because en bloc recovery is shown to result in higher probability of transplantation (7, 20). The organ allocation policy for kidneys from young donors may accelerate identification of suitable recipients, resulting in lower discard rates.

Our study is based on the retrospective data analysis that has a limitation. However, it includes a large number of transplants from various regions in the United States, which makes our study more valid.

In summary, using a large national data, our study demonstrates EBK transplants from young pediatric donors had the best long-term graft outcomes among deceased donor transplants to adult recipients, providing unique options for those who do not have living donors.

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Keywords:

Kidney transplantation; En bloc; Pediatric donor; GFR; UNOS; Deceased donor; Graft survival

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