Background The outcome of organs which have been declined for paediatric recipients is not known. This study aimed to determine the outcome of kidneys initially declined for paediatric recipients and establish renal allograft survival in kidneys that were eventually transplanted. Methods Data were obtained from the UK Transplant Registry for all donation after brain death (DBD) kidneys offered and declined to paediatric recipients (< 18 years) in the UK from 2009 to 2014. Results Eighty-two percent (503/615) of kidneys initially declined for paediatric transplantation were eventually transplanted, 7% (46/615) of kidneys went to paediatric recipients and 62% (384/615) of kidneys went to adult (kidney only) recipients. The remainder were used for multiple organ transplants. In the 46 kidneys that went to paediatric recipients, 1 and 3-year renal allograft survivals were 89% (95% CI 75.8–95.3%) and 82% (95% CI 67.1–90.6%), respectively. In the 384 kidneys given to adult kidney-only recipients, 1 and 3-year renal allograft survivals were 96% (95% CI 93.5–97.6%) and 94% (95% CI 90.7– 96.1%), respectively. Eighty-four percent of the 204 children who initially had an offer declined on their behalf were eventually transplanted and have a functioning graft at a median 3-year follow-up. Conclusions This study reports acceptable short-term renal allograft survival in kidneys that were initially declined for paediatric recipients and subsequently transplanted. Evidence-based guidelines are required to ensure that the most appropriate kidneys are selected for paediatric recipients. . . Keywords Paediatric nephrology Renal transplantation Transplant outcomes Introduction deleterious effects of long-term sub-optimal dialysis in chil- dren are even more pronounced, including additional negative Pre-emptive renal transplantation is the gold standard renal effects on growth and development. The priority for many replacement therapy for children with end-stage kidney dis- paediatric nephrologists is to perform pre-emptive, in most ease (ESKD). There is a significant body of adult data cases live-related, renal transplantation for children, but where supporting the advantages of renal transplantation over dialy- a living donor is not available, a child may be listed for a sis, including improved survival and quality of life [1–3]. The donation after brain death (DBD) and/or donation after cardiac death (DCD) kidney transplant. In the UK, paediatric patients receive the highest priority for deceased donor kidney offers (at each HLA match level), as well as receiving additional * Stephen D. Marks priority points if their HLA match is not favourable. email@example.com Transplant networks in different countries vary in their or- University College London Great Ormond Street Institute of Child gan procurement and allocation methods, but when a DBD Health, London, UK kidney is matched to a paediatric recipient, the child’s ne- phrologist and transplant surgeon make the decision whether NHS Blood and Transplant, Bristol, UK to accept this kidney for this child. This decision is a time- University Hospitals Bristol NHS Foundation Trust, Bristol, UK critical one which needs to be made quickly . Paediatric Department of Paediatric Nephrology, Great Ormond Street Hospital transplant centres in the UK have 45 min to respond to a for Children NHS Foundation Trust, Great Ormond Street, DBD kidney offer. This is a challenging decision where the London WC1N 3JH, UK 1610 Pediatr Nephrol (2018) 33:1609–1616 potential benefits of transplantation need to outweigh the of transplant. One and 3-year patient and renal allograft sur- risks. The risks in transplantation include a variety of donor vival were calculated where the kidney was eventually and recipient factors [5–7], and sometimes an offer of a kidney transplanted. Data were separately analysed for those kidneys is declined for a paediatric recipient. Whilst there are a number declined for donor reasons or inappropriate size for paediatric of possible reasons for decline, the most frequent reasons for recipients. decline are not well described in the literature. Kidneys which are declined for donor factors, such as poor Outcome in paediatric patients for whom a kidney donor health or cause of death, may not be suitable for trans- was offered and declined plantation in any recipient. Other kidneys which are declined may subsequently be offered to another recipient (adult or The outcomes for the patients for whom the kidney was of- child) and may be successfully transplanted. There are no fered and declined were examined. Children were categorised reports in the literature which systematically evaluate the out- into those who received a transplant and those who were still come in kidneys which have been declined for paediatric waiting for a transplant, and then sub-divided according to transplantation. this. For those children who received a kidney transplant after The outcome for children who have a kidney transplant their declined offer, the time from first declined offer to trans- declined on their behalf is also poorly understood, and further plantation was calculated. Those children who had an initial evidence is required to help clinicians decide whether a child decline for donor health or size mismatch were analysed sep- may benefit from accepting a kidney sooner rather than arately, in order to eliminate those where the kidney decline waiting for a kidney of potentially higher quality or was purely due to recipient reasons (e.g. recipient acutely appropriateness. unwell at the time of kidney offer). This was felt to give the The primary aim of this study was to determine the out- clearest data representing organs that were declined for donor come of kidneys which were declined for paediatric recipients reasons and could be transplanted into other recipients. and establish renal allograft survival in those kidneys that were eventually transplanted. Secondary aims were to inves- Prospective study of reasons for decline of a kidney tigate the outcomes for children who had a kidney declined on for a paediatric recipient their behalf and to investigate the most common reasons for declining a kidney for a paediatric recipient. For two separate years (2011 and 2014), a prospective obser- vational study was conducted. During these years (from 1 January to 31 December in each year), the paediatric renal Materials and methods transplant centre that had declined an organ for a paediatric recipient received a supplemental data collection form to com- This study was conducted into two parts, a retrospective anal- plete which requested additional information on the reason for ysis of national data from the UK Transplant Registry and a declining the kidney for the paediatric recipient, with both prospective observational study. generic reasons for decline and the option of free text com- ments as required (examples of generic reasons included; do- Retrospective analysis of kidney and patient nor unsuitable due to cause of death, meningococcemia with outcomes after a declined kidney transplant offer < 48 h of treatment, no staff/theatre time, etc.). In addition to for a paediatric recipient the routine data held by the UK Transplant Registry on de- clined offers, donor and recipient characteristics and anthro- Data were obtained from the UK Transplant Registry for all pometrics were analysed. DBD kidneys offered and declined for paediatric recipients under 18 years of age in the UK from 1 January 2009 to 31 Statistical analysis December 2014. Data on the total number of paediatric trans- plants and the number of children on the transplant waiting list Results were analysed using summary statistics and 95% con- at 1 January of each year was also collected. fidence intervals calculated as appropriate. The Kaplan-Meier method was used to estimate univariate post-transplant patient Outcome of kidneys that were initially declined and renal allograft survival separately for all cases where the for paediatric transplantation kidney was subsequently transplanted after being declined for a paediatric patient. Death censored renal allograft survival We performed a retrospective analysis on the final outcome of was defined as time from renal transplantation to renal allo- kidneys declined on behalf of paediatric recipients during this graft failure. Patient survival was defined as time from trans- time period, categorising kidneys as not transplanted or plant to patient death censoring for patients still alive at the transplanted, and separating the latter category into the type time of analysis. Pediatr Nephrol (2018) 33:1609–1616 1611 Data were fully anonymised and ethical principles adhered to throughout the study; external ethical review was not re- quired. Statistical analyses were performed in SAS version 9.2 (SAS Institute Inc., Cary, North Carolina, USA). All statistical tests are two-tailed and a p value of < 0.05 was considered statistically significant. Results Retrospective analysis of kidney and patient outcomes after a declined kidney transplant offer for a paediatric recipient The total number of declined paediatric kidney offers per year reduced during the study as did the total number of children on the active kidney transplant waiting list (Fig. 1). Outcome of kidneys that were initially declined for paediatric transplantation Four hundred and two DBD kidney offers from 308 different donors were declined for 204 different paediatric recipients from 2009 to 2014 in the UK. Some donor kidneys were of- fered to multiple children on the waiting list as some were Fig. 2 Flow diagram showing the number of recipients, donors and declined more than once. Two hundred and four children had kidneys involved in each stage of this study, considering kidney offers kidneys declined on their behalf, and some children had mul- declined for paediatric recipients in the UK from 2009 to 2014. The tiple kidney declines. Six hundred and fifteen kidneys were outcomes of kidneys initially declined for paediatric recipients are also shown available for transplantation from the 308 donors who were declined for paediatric transplantation. We analysed the out- come for both kidneys (where the donor had two kidneys) even kidneys went to paediatric recipients (kidney-only), 74% if only one of the kidneys was declined for paediatric trans- (457) of 615 kidneys went to adult recipients (62% kidney- only and 10% simultaneous pancreas and kidney (Table 1). plantation. Therefore, the analysis of outcomes for 615 kidneys exceeds the number of declined offers (402); see Fig. 2. The remaining 2% were either double kidney or another multi- Of 615 kidneys from 308 donors declined for paediatric organ transplant involving a kidney; the numbers in this group recipients during the 6 years of the study, 7% (46) of 615 were too small to perform separate survival analysis). Fig. 1 Total number of kidney offers declined for paediatric recipients from 2009 to 2014, with the total number of transplants in children and number of children on the active kidney transplant waiting list (all values are per calendar year across the UK). Type of kidney transplants: DBD donation after brain death, DCD donation after cardiac death, LD living donor 1612 Pediatr Nephrol (2018) 33:1609–1616 Table 1 Outcome of 615 kidneys from 308 donors that were declined for paediatric recipients from 2009 to 2014 in the UK (46 paediatric kidney only transplants were from 43 donors) Outcome of organ after decline N 1-year patient survival 1-year renal allograft survival 3-year patient survival 3-year renal allograft survival for paediatric recipient % Survival 95% CI % Survival 95% CI % Survival 95% CI % Survival 95% CI Not transplanted 112 Paediatric kidney only 46 97.7 84.6 99.7 89.1 75.8 95.3 97.7 84.6 99.7 82 67.1 90.6 Adult kidney only 384 95.7 92.7 97.5 96 93.5 97.6 93.1 89.1 95.6 93.9 90.7 96.1 Adult kidney and pancreas 61 100 –– 96.7 87.5 99.2 97.9 85.8 99.7 87.4 73.5 94.3 Other 12 Patient and renal allograft survival data to 24 July 2016. ‘Other’ category includes double kidney (paediatric and adult), kidney and liver (paediatric and adult) and kidney and small bowel (adult). 4/12 kidneys went to children N number, CI confidence interval Insufficient events in each group to be able to report survival Eighteen percent (112) of 615 kidneys were not transplanted offer decline during this period and/or experienced declined (Fig. 2). offers outside of this time period. The data do not take account Of 485 kidneys from 243 donors declined due to donor of any transplants prior to the decline offer of interest. reasons or size mismatch for paediatric recipients, 79% of these kidneys were eventually transplanted and 6% (28) of Prospective study of reasons for decline of a kidney 485 went to paediatric kidney-only recipients (Table 2). for a paediatric recipient Outcome in paediatric patients for whom a kidney There were 60 and 41 kidneys declined for paediatric recipi- was offered and declined ents during the 2 years of prospective data collection (2011 and 2014, respectively). Although the absolute number of One child died while waiting for a transplant out of the 204 declines fell, the decline rate actually rose slightly from 59% children who had a kidney offer declined on their behalf dur- in 2011 to 64% in 2014. This is because the number of chil- ing the study. Eighty-four percent (171) of 204 children have dren active on the kidney transplant waiting list fell from 101 been transplanted and have a functioning graft (Fig. 3). in 2011 to 64 in 2014. One hundred percent of the additional The waiting time for a child to be transplanted after an offer supplemental data forms were returned from ten paediatric was declined for them was 0 to 1701 (median 198) days renal transplant centres in the UK. (Table 3 for all children who received a transplant and In 75% of kidney declines for paediatric recipients, donor Table 4 for those patients with initial kidney decline due to poor health or cause of death was cited as a reason for decline donor reasons or inappropriate size). These data consider the (Table 5). In order of importance, the three main donor health outcome following the patients first declined offer between or cause of death reasons for decline were as follows: (1) death 2009 and 2014. Many patients experienced more than one due to suspected meningoencephalitis without an identified Table 2 Outcome of 485 kidneys from 243 donors that were declined due to donor reasons or size mismatch for paediatric recipients from 2009 to 2014 in the UK Outcome of organ after decline N 1-year patient survival 1-year renal allograft survival 3-year patient survival 3-year renal allograft survival for paediatric recipient % Survival 95% CI % Survival 95% CI % Survival 95% CI % Survival 95% CI Not transplanted 102 Paediatric kidney only 28 96.3 76.5 99.5 82.1 62.3 92.1 96.3 76.5 99.5 78.6 58.4 89.8 Adult kidney only 308 95.1 91.5 97.2 95.7 92.7 97.5 92.2 87.9 95 93.7 90.1 96 Adult kidney and pancreas 40 100 –– 97.5 83.5 99.6 100 –– 85.9 69.2 93.9 Other 7 Patient and renal allograft survival data to 24 July 2016. ‘Other’ category includes double kidney (paediatric and adult), kidney and liver (paediatric and adult), and kidney and small bowel (adult). Two out of seven kidneys went to children N number, CI confidence interval Insufficient events in each group to be able to report survival Pediatr Nephrol (2018) 33:1609–1616 1613 Table 4 Time between declined kidney offer due to donor reasons or size mismatch from 2009 to 2014 to transplantation Donor type N Median time Range (days) to transplant (days) DBD 112 192 1–892 DCD 8 152 55–445 LD 37 186 6–1093 N number, DBD donation after brain death, DCD donation after cardiac death, LD living donor Fig. 3 Patient outcomes for children who had a kidney offer declined on Whilst the observational nature of this study does not their behalf in the UK from 2009 to 2014 (logarithmic scale) outcomes allow us to predict whether each child in this study would taken after their first decline during this period (many patients had more than one declined offer and may have had declines outside this time have benefitted from receiving the organ initially declined period) for them, the fact that 82% of 615 kidneys were eventually transplanted suggests that some of these kidneys were ap- propriate for paediatric transplantation, acknowledging dif- organism, (2) virology (hepatitis B or C) or concern over ferent risk-benefit ratios in paediatric and adult renal trans- donor substance misuse without virology results and (3) death plant recipients. A kidney that is appropriate for an adult from brain tumour without a histological diagnosis. There was recipient is not necessarily appropriate for a paediatric re- no statistically significant difference between the 2 years in cipient. The finding that 3-year renal allograft survival in any of the reasons for decline (chi-squared test). the kidneys transplanted to adult recipients is acceptable cannot necessarily be applied to paediatric recipients. However, although most children with an initial decline were eventually transplanted, this study has demonstrated Discussion that declining a kidney offer for a child in the UK extends the transplant waiting time by a further 6 months on aver- Our findings show that kidneys declined for a paediatric re- age. Whilst a child waiting an additional 6 months on an cipient can have acceptable 1 and 3-year patient and renal optimised form of renal replacement therapy (such as noc- allograft survival if eventually transplanted. Short-term renal turnal home haemodialysis) may not suffer many additional allograft outcomes are better if these organs are transplanted risks, a child on sub-optimal dialysis treatment with other into adult rather than paediatric recipients. The results also co-morbidities may suffer significant morbidity by waiting show that most children who have a kidney offer declined an additional 6 months for a transplant. Recent evidence has on their behalf will eventually be transplanted, but the median also shown that children not on dialysis at the time of trans- time to transplant is over 6 months. One child who initially plant have improved renal allograft survival compared to had a kidney declined on their behalf died whilst waiting for a those on dialysis at the time of transplant, although short transplant. There are few studies in the literature reporting periods of dialysis (< 6 months duration) did not confer any outcomes after declined kidney offers, and ours is the first to additional risk to renal allograft survival . Therefore, the systematically assess organ declines for paediatric recipients decision to refuse a kidney offer for a child must not be across a national organ allocation network. taken lightly, and better evidence is required to help clini- cians make these difficult decisions. As well as the observational nature of this study, a fur- Table 3 Time between declined kidney offer of all children from 2009 ther limitation to the conclusions we can draw from these to 2014 to transplantation results is the small number of declined organs that eventu- ally went to other paediatric recipients (46 in total). This has Donor type N Median time Range (days) to transplant (days) resulted in 1 and 3-year renal allograft survival estimates with wide confidence intervals and may in part account for DBD 129 198 0–1701 the finding that 1-year renal allograft survival is better in DCD 8 152 55–445 adult recipients. A possible explanation for these results is LD 41 206 6–1093 that children who eventually accept a kidney that was ini- tially declined for a paediatric recipient may be children N number, DBD donation after brain death, DCD donation after cardiac whoaredifficulttotransplantorhavebeenwaitingfora death, LD living donor 1614 Pediatr Nephrol (2018) 33:1609–1616 Table 5 Baseline data and 2011 2014 Both Years reasons for decline for all kidneys declined on behalf of paediatric Total number of declines 60 41 101 recipients in the UK from prospective audit data in 2011 and Decline rate (based on total number on waiting list) 59% 64% 61% Number of different donors 51 31 82 Number of different recipients 40 32 72 Donor age in years (median) 2–50 (38) 4–50 (40) 2–50 (40) Recipient age in years (median) 1–17 (10) 2–17 (12) 1–17 (10) Donor weight in kg (median) 14–180 16–137 (71) 14–180 (75) (75) Recipientweightinkg(median) 11–60 (20) 10–84 (32) 10–84 (26) Donor height in cm (median) 91–200 117–189 91–200 (168) (170) (170) Recipient height in cm (median) 76–178 71–171 71–178 (116) (133) (125) Reasons for decline Donor poor health or cause of death 72% 80% 75% Size mismatch 22% 15% 19% Awaiting a better offer or live transplant 5% 10% 7% Poor HLA match or positive cross match 8% 2% 6% Recipient unfit for surgery 3% 2% 3% Lack of staff to perform organ retrieval or transplant 3% 2% 3% Ischaemia time (CIT or WIT) too long or organ damage during 3% 2% 3% retrieval Other 3% 5% 4% Some declined offers had multiple reasons for the decline; the percentages shown in the table reflect the propor- tion of declines where that reason applied HLA human leukocyte antigen, CIT cold ischaemia time, WIT warm ischaemia time long time; therefore, the children that eventually get the the whole of the UK is not statistically significant, at both 1 kidney may have inferior renal allograft survival due to and 3 years. their individual recipient characteristics. When we consider the 485 kidneys declined due to donor Once the 3-year renal allograft survival data is consid- reasons or inappropriate size for paediatric recipients, only 28 ered, it appears that adult recipients can have better out- of these were eventually transplanted to other paediatric recip- comes than paediatric recipients when they get a kidney ients (Table 4). One-year renal allograft survival in this sub- that was initially declined for a paediatric recipient. We group is 82% [95% CI 62.3–92.1%]. Although this does not cannot draw firm conclusions over the reasons for this, differ significantly from the data for 955 DBD kidney trans- but the renal allograft survival estimate in our study does plants above, this is partly because the confidence intervals are not differ significantly from renal allograft survival in larg- wide due to small numbers. It is interesting to note that both 1 er cohorts of paediatric donation after brain death (DBD) and 3-year renal allograft survival is worse for paediatric re- kidney recipients. One-year renal allograft survival was cipients than adult recipients, although the number in this sub- 89% [95% CI 75.8–95.3%] for paediatric recipients, which group is small and it is difficult to draw firm conclusions. is comparable to data from the UK transplant registry for The prospective observational part of this study has en- 955 DBD kidney transplants for children where 1-year al- abled us to better understand the most common reasons for lograft survival was 93% [95% CI 91.6–94.8%; unpub- decline of a kidney offer for a paediatric recipient. Across the lished data: NHS Blood and Transplant]. Three-year renal 2 years studied, 75% of declines cited poor donor health or allograft survival in the 46 kidneys that went to paediatric cause of death as a reason for declining the organ. Nineteen recipients in our study was 82% [95% CI 67.1–90.6%], percent of declines cite an inappropriate size match between whichisalsocomparabletodatafromtheUK transplant donor and recipient as a reason for declining the organ. registry where 3-year allograft survival was 87% [95% CI The importance of good donor health is emphasised in the 84.8–89%; unpublished data: NHS Blood and Transplant]. literature [6, 9], and this is particularly the case for paediatric The difference in survival between patients in our study and recipients. Children with ESKD are likely to need multiple Pediatr Nephrol (2018) 33:1609–1616 1615 Acknowledgements This study was supported by the National Institute kidney transplants across their life, so maximising the longev- for Health Research Biomedical Research Centre at the UCL Great ity of the kidneys they receive during childhood is paramount Ormond Street Institute of Child Health and conducted on behalf and . However, there is emerging evidence from adult litera- with the support of the NHS Blood and Transplant Paediatric Subgroup ture that suggests that inferior but acceptable transplant out- of the Kidney Advisory Group. comes can be achieved with ‘marginal’ or ‘extended-criteria’ Funding Salary funding for MM was provided by the UK National donors [6, 9]. Whilst this does not permit automatic extension Institute of Health Research (NIHR) as an Academic Clinical Fellow. of this evidence to paediatric recipients, when the negative All other authors are supported by their institutions. impact of other forms of renal replacement therapy such as dialysis is considered , it may be prudent to consider wid- Compliance with ethical standards ening the criteria of potential organ acceptance for paediatric recipients. We are already seeing increased utilisation of do- The clinical and research activities being reported are consistent with the nation after DCD kidney transplants in both adults and chil- Principles of the Declaration of Istanbul as outlined in the ‘Declaration of Istanbul on Organ Trafficking and Transplant Tourism’. All NHS Blood dren with good outcomes to date [12, 13], so there may be a and Transplant data protection and ethical principles were followed. case for extending the criteria for organ acceptance for paedi- atric recipients. Conflict of interest The authors declare that they have no conflicts of The issue of size mismatch is a controversial one in paedi- interest. atric renal transplantation. Whilst the potential surgical and Open Access This article is distributed under the terms of the Creative haemodynamic problems of large kidneys for small recipients Commons Attribution 4.0 International License (http:// are well documented , there are reports of similar renal creativecommons.org/licenses/by/4.0/), which permits unrestricted use, allograft outcomes to size-matched grafts  and these con- distribution, and reproduction in any medium, provided you give appro- cerns must be balanced against the well-recognised risks of priate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. staying on dialysis in such young patients . This is even more so the case in this situation, where a size mismatch is also likely to occur for any potential living-related donor, and may also prevent this type of transplantation occurring. Size mismatch is not listed as a contraindication in the NHS Blood References and Transplant guideline (2013) outlining reasons for decline of kidneys for paediatric recipients . This is generally a 1. Wolfe RA, Ashby VB, Milford EL, Ojo AO, Ettenger RE, Agodoa decision made at a local level by the recipient’s individual LY, Held PJ, Port FK (1999) Comparison of mortality in all patients nephrologist and transplant surgeon, where size mismatch on dialysis, patients on dialysis awaiting transplantation, and recip- may eventually be a factor which results in a decision to de- ients of a first cadaveric transplant. N Engl J Med 341:1725–1730 cline by the operating surgeon. 2. Ojo AO, Hanson JA, Meier-Kriesche H, Okechukwu CN, Wolfe RA, Leichtman AB, Agodoa LY, Kaplan B, Port FK (2001) Although this part of our study helps us to understand the Survival in recipients of marginal cadaveric donor kidneys com- commonest reasons for decline of a kidney offer for a pae- pared with other recipients and wait-listed transplant candidates. J diatric recipient, further study is required to help clarify Am Soc Nephrol 12:589–597 these factors and to provide evidence for guideline devel- 3. McDonald SP, Russ GR (2002) Survival of recipients of cadaveric kidney transplants compared with those receiving dialysis treatment opment. In particular, detailed analysis of which donor in Australia and New Zealand. Nephrol Dial Transplant 17:2212– health issues preclude transplant and the specifics of size mismatch (e.g. kidney too big or small) will help to evaluate 4. Chaudhuri A, James G, Grimm P (2015) Whether or not to accept a these factors further. deceased donor kidney offer for a pediatric patient. Pediatr Nephrol In conclusion, this study demonstrates that most kidneys 30:1529–1536 5. Watson AR, Hayes WN, Vondrak K, Ariceta G, Schmitt CP, Ekim initially declined for paediatric transplantation can be success- M, Fischbach M, Edefonti A, Shroff R, Holta T, Zurowska A, Klaus fully transplanted into both adult and paediatric recipients, G, Bakkaloglu S, Stefanidis CJ, Stefanidos C, Van de Walle J with acceptable 1 and 3-year patient and renal allograft sur- (2013) Factors influencing choice of renal replacement therapy in vival (although there may be an advantage for adult renal European paediatric nephrology units. Pediatr Nephrol 28:2361– transplant recipients). 6. 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Pediatric Nephrology – Springer Journals
Published: May 28, 2018
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