Shipping living donor kidneys and transplant recipient outcomes

Kidney paired donation (KPD) is an important tool to facilitate living donor kidney transplantation (LDKT). Concerns remain over prolonged cold ischemia times (CIT) associated with shipping kidneys long distances through KPD. We examined the association between CIT and delayed graft function (DGF), allograft survival, and patient survival for 1267 shipped and 205 nonshipped/internal KPD LDKTs facilitated by the National Kidney Registry in the United States from 2008 to 2015, compared to 4800 unrelated, nonshipped, non-KPD LDKTs. Shipped KPD recipients had a median CIT of 9.3 hours (range = 0.25-23.9 hours), compared to 1.0 hour for internal KPD transplants and 0.93 hours for non-KPD LDKTs. Each hour of CIT was associated with a 5% increased odds of DGF (adjusted odds ratio: 1.05, 95% confidence interval [CI], 1.02-1.09, P < .01). However, there was not a significant association between CIT and all-cause graft failure (adjusted hazard ratio [aHR]: 1.01, 95% CI: 0.98-1.04, P = .4), death-censored graft failure ( [aHR]: 1.02, 95% CI, 0.98-1.06, P = .4), or mortality (aHR 1.00, 95% CI, 0.96-1.04, P > .9). This study of KPD-facilitated LDKTs found no evidence that long CIT is a concern for reduced graft or patient survival. Studies with longer follow-up are needed to refine our understanding of the safety of shipping donor kidneys through KPD. Kidney paired donation (KPD) is an important tool to facilitate living donor kidney transplantation (LDKT). Concerns remain over prolonged cold ischemia times (CIT) associated with shipping kidneys long distances through KPD. We examined the association between CIT and delayed graft function (DGF), allograft survival, and patient survival for 1267 shipped and 205 nonshipped/internal KPD LDKTs facilitated by the National Kidney Registry in the United States from 2008 to 2015, compared to 4800 unrelated, nonshipped, non-KPD LDKTs. Shipped KPD recipients had a median CIT of 9.3 hours (range = 0.25-23.9 hours), compared to 1.0 hour for internal KPD transplants and 0.93 hours for non-KPD LDKTs. Each hour of CIT was associated with a 5% increased odds of DGF (adjusted odds ratio: 1.05, 95% confidence interval [CI], 1.02-1.09, P < .01). However, there was not a significant association between CIT and all-cause graft failure (adjusted hazard ratio [aHR]: 1.01, 95% CI: 0.98-1.04, P = .4), death-censored graft failure ( [aHR]: 1.02, 95% CI, 0.98-1.06, P = .4), or mortality (aHR 1.00, 95% CI, 0.96-1.04, P > .9). This study of KPD-facilitated LDKTs found no evidence that long CIT is a concern for reduced graft or patient survival. Studies with longer follow-up are needed to refine our understanding of the safety of shipping donor kidneys through KPD. The burden of end-stage renal disease (ESRD) is high in the United States, with approximately 98 000 patients waiting for a kidney transplant (Organ Procurement and Transport Network [OPTN] data as of May 22, 2017). Living donor kidney transplantation (LDKT) is a better alternative to waiting for a deceased donor organ when the recipient candidate has a willing and compatible donor. If the donor and candidate are incompatible, however, kidney paired donation (KPD) provides a means to exchange donors with another incompatible pair so that both candidates can undergo a compatible LDKT. Recent acceptance of the practice of KPD in the United States has given rise to national KPD registries that facilitate KPD exchanges between kidney donors and recipients separated by long distances.1Rees MA Kopke JE Pelletier RP et al.A nonsimultaneous, extended, altruistic-donor chain.N Engl J Med. 2009; 360: 1096-1101Crossref PubMed Scopus (243) Google Scholar Although these nationwide exchanges allow more incompatible pairs to participate in LDKT, the long distances between transplant centers result in prolonged cold ischemia time (CIT) for the shipped kidney. The transplant community varies in whether they support shipping living donor kidneys long distances through KPD programs adding significant CIT. Some national programs, such as in Canada or The Netherlands, never ship extirpated living donor kidneys.2de Klerk M Keizer KM Claas FH Witvliet M Haase-Kromwijk BJ Weimar W The Dutch national living donor kidney exchange program.Am J Transplant. 2005; 5: 2302-2305Abstract Full Text Full Text PDF PubMed Scopus (132) Google Scholar,3Cole EH Nickerson P Campbell P et al.The Canadian kidney paired donation program: A national program to increase living donor transplantation.Transplantation. 2015; 99: 985-990Crossref PubMed Scopus (32) Google Scholar On the other hand, the National Kidney Registry (NKR) in the United States has routinely shipped living donor kidneys since inception in 2008.4Melcher ML Leeser DB Gritsch HA et al.Chain transplantation: Initial experience of a large multicenter program.Am J Transplant. 2012; 12: 2429-2436Abstract Full Text Full Text PDF PubMed Scopus (49) Google Scholar Our ability to evaluate and compare these different policies on shipping kidneys and establish an evidence-based, standard approach is limited by a paucity of research. Initial preliminary studies of shipped LDKT in KPD programs have suggested minimal to no association between CIT and graft or patient outcomes; however, these studies were limited by small sample sizes and minimal follow-up times.5Treat EG Miller ET Kwan L et al.Outcomes of shipped live donor kidney transplants compared with traditional living donor kidney transplants.Transpl Int. 2014; 27: 1175-1182Crossref PubMed Scopus (13) Google Scholar,6Segev DL Veale JL Berger JC et al.Transporting live donor kidneys for kidney paired donation: Initial national results.Am J Transplant. 2011; 11: 356-360Abstract Full Text Full Text PDF PubMed Scopus (63) Google Scholar Additionally, none of these studies identified potential risk factors or predictors of poorer outcomes in shipped KPD kidneys with prolonged CIT. In a slightly different study population, a recent report of non-KPD LDKTs incurring longer CIT (maximum of 8 hours) in older donors (>50 years old) demonstrated poorer graft survival.7Krishnan AR Wong G Chapman JR et al.Prolonged ischemic time, delayed graft function, and graft and patient outcomes in live donor kidney transplant recipients.Am J Transplant. 2016; 16: 2714-2723Abstract Full Text Full Text PDF PubMed Scopus (29) Google Scholar In larger studies of deceased donor organs, there has been conflicting evidence for the association between long CIT (upwards of 24 hours) and delayed graft function (DGF), poorer allograft survival, or poorer patient survival.8Debout A Foucher Y Trebern-Launay K et al.Each additional hour of cold ischemia time significantly increases the risk of graft failure and mortality following renal transplantation.Kidney Int. 2015; 87: 343-349Abstract Full Text Full Text PDF PubMed Scopus (232) Google Scholar,9Kayler LK Srinivas TR Schold JD Influence of CIT-induced DGF on kidney transplant outcomes.Am J Transplant. 2011; 11: 2657-2664Abstract Full Text Full Text PDF PubMed Scopus (110) Google Scholar In order to address the important clinical and programmatic questions about the benefits and risks of shipping KPD kidneys, this study compares a large cohort of KPD recipients facilitated by the NKR, a large national KPD exchange program, to a national cohort of unrelated LDKTs not shipped or facilitated in a KPD exchange, which was identified from the Scientific Registry of Transplant Recipients (SRTR). This study aims to identify associations between CIT and KPD recipient DGF, allograft failure, and patient death. Additionally, we sought to identify any associated risk factors for poorer outcomes. In comparison to data used in previous studies, the unique experience of the NKR offers a larger study population and longer CIT from transcontinental shipping. The NKR is a nonprofit, 501c organization comprising 76 transplant centers within the United States participating during this study period. Details of the NKR have been previously described.5Treat EG Miller ET Kwan L et al.Outcomes of shipped live donor kidney transplants compared with traditional living donor kidney transplants.Transpl Int. 2014; 27: 1175-1182Crossref PubMed Scopus (13) Google Scholar NKR policies are available online at: http://www.kidneyregistry.org. Protocols for evaluating patients, performing the transplant procedures, and postoperative care are outlined by the NKR; however, these functions are ultimately carried out by the participating transplant centers abiding by, and in concordance with, the individual center protocols. The shipping of kidneys was performed utilizing existing organ procurement organizations methodologies in accordance with Organ Procurement and Transplantation Network (OPTN) and United Network for Organ Sharing (UNOS) standards. Cold preservation solution without pumping was used for storage of the kidneys during transport. To date, the NKR has facilitated over 2000 KPD exchanges, >80% of which involve shipping the living donor organ across the United States. KPD transplants between February 1, 2008 and November 30, 2015 were identified from the NKR registry. The NKR registry was linked to the SRTR using the UNOS donor identifier to obtain demographic and clinical variables for the recipients and donors. Any transplant that could not be linked or validated on transplant center, transplant date, ABO, and gender was excluded from the study (5%, n = 78). Additionally, as a comparison group, we included the cohort of all living unrelated non-KPD transplants identified from the SRTR that had their transplant at an NKR-participating center, during the same time period, and with short CIT (<1.33 hours, the average CIT of in-center NKR exchanges). NKR exchanges where the kidney was shipped were termed “shipped exchange,” NKR exchanges within the same center were termed “in-center exchanges,” and the additional cohort of living unrelated non-KPD transplants from SRTR were termed “other nonexchange.” In this study, CIT was defined as the hours of cold ischemia time associated with facilitating the of CIT hours and of CIT > hours were as CIT as the prolonged CIT in these was to recipient graft function was through SRTR and defined as in the We whether longer CIT was associated with increased odds of We for recipient factors of at previous and years on renal donor factors kidney donor J et al.A risk for living donor kidney J Transplant. 2016; 16: Full Text Full Text PDF PubMed Scopus Google and transplant factors and of graft failure was through the Recipients were graft failure, or on November 30, We whether longer CIT was associated with an increased hazard of were on a SRTR factors included years of at disease at years of and of factors were for through graft failure was through Recipients were graft failure, for or on November 30, We whether longer CIT was associated with an increased hazard of for the same recipient and donor factors as was through Recipients were or on November 30, We whether longer CIT was associated with an increased hazard of mortality were on SRTR factors included years of at previous years of of or and of factors were for through and donor We whether CIT was associated with DGF, and mortality on whether the donor was years of or This was using an in the of CIT and donor years of in the This study was by the of as as the The NKR to the NKR to this and of the NKR data not participate in the or for this This study used data from the The SRTR data data on all and transplant recipients in the United States, by the of the and has been DL data in organ transplantation: and J Transplant. 2014; Full Text Full Text PDF PubMed Scopus Google Scholar The and of and provides to the of the and SRTR 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a to for center = of DGF were since the patient in the DGF could be data were through in a odds CI, confidence DGF, delayed graft kidney paired live donor kidney donor renal DGF was in a to for center = of DGF were since the patient in the DGF could be data were through was in shipped in in-center and in other was in shipped in in-center and in other non-KPD for between recipient and donor there was not a significant association between CIT and (adjusted hazard ratio 1.01, 95% CI, 0.98-1.04, P = Each of recipient years was associated with a hazard of Each of recipient years was associated with an increased hazard of Recipients with years of and were associated with an increased hazard of transplants and more recent of transplant were associated with hazard of In an where with data were by = CIT was not associated with increased (aHR 95% CI, P = factors for all-cause graft failure KPD and non-KPD living kidney donor transplant ischemia time at transplant at of of graft failure was in a 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were through hazard CI, confidence kidney paired live donor kidney donor renal patient survival was for shipped for in-center and for other patient survival was for shipped for in-center and for other non-KPD for between and donor there was no association found between CIT and mortality (aHR 1.00, 95% CI, 0.96-1.04, P > .9). Each of recipient at transplant years of previous and were associated with increased hazard of and more recent of transplant were associated with hazard of mortality In an where with data were by = CIT was not associated with increased mortality (aHR 1.05, 95% CI, P = factors for mortality KPD and non-KPD living kidney donor transplant ischemia time at transplant previous of of was in a with to for center = data were through hazard CI, confidence kidney paired live donor kidney donor renal in a was in a with to for center = data were through hazard CI, confidence kidney paired live donor kidney donor renal was no association between CIT and DGF with a donor years P = CIT associated with DGF with a donor years or with CI, P < was no association between CIT and = .4), = or mortality = with older donors The of shipping living donor kidneys on transplant recipient outcomes has been a In this cohort study of shipped live donor kidneys to KPD recipients in a large multicenter exchange program, hour of CIT was associated with a 5% increased odds of an a transplant recipient with a of DGF experience a of DGF with additional hour of a of DGF with additional hours of and a of DGF with additional hours of CIT. CIT was not found to be associated with graft failure or a minimal association between graft and patient outcomes and shipping living donor kidneys in a large multicenter KPD exchange to this with LDKT, in deceased donor kidney transplantation prolonged CIT has been identified as an risk for graft factors and for renal allograft PubMed Scopus Google Y A et graft risk and from a 2005; PubMed Scopus Google Scholar The of CIT-induced DGF in the studies has not graft survival, alternative or factors DGF within deceased donor organs, such as with or other which to poorer LK Srinivas TR Schold JD Influence of CIT-induced DGF on kidney transplant outcomes.Am J Transplant. 2011; 11: 2657-2664Abstract Full Text Full Text PDF PubMed Scopus (110) Google Scholar to deceased donor organs, prolonged cold storage in living donation to be associated with of however, this small increase in DGF not to be associated with graft or patient outcomes in this this study was not to as an of allograft to graft and patient survival, our are to in the study by et which was to address outcomes and to for other factors the donor LK Srinivas TR Schold JD Influence of CIT-induced DGF on kidney transplant outcomes.Am J Transplant. 2011; 11: 2657-2664Abstract Full Text Full Text PDF PubMed Scopus (110) Google Scholar large studies have found no significant associations between CIT and deceased donor allograft K kidney donation by of living donor Transplant. PubMed Scopus Google Scholar transplant centers be of the small increase in risk for DGF that with increased shipping times demonstrated by this study, and that risk their for the with more risk such as additional time on important of in this additional of the of the DGF of and et graft function and kidney transplant PubMed Scopus Google Scholar of DGF associated with shipping kidneys could transplant centers whether or not the small risk of DGF associated with long shipping times is to Although recent studies poorer allograft outcomes with prolonged CIT in living donor recipients not participating in exchange programs, we no association between CIT and allograft or patient survival in our shipped KPD et found that recipients of kidneys from donors CIT of hours was associated with an increased odds of death-censored and all-cause graft AR Wong G Chapman JR et al.Prolonged ischemic time, delayed graft function, and graft and patient outcomes in live donor kidney transplant recipients.Am J Transplant. 2016; 16: 2714-2723Abstract Full Text Full Text PDF PubMed Scopus (29) Google Scholar We found no evidence that DGF, graft failure, or mortality by donors years and conflicting be by in the study study and of CIT In the study, the kidneys were not and they excluded exchange transplants with CIT > 8 hours, and Although that study had longer follow-up their CIT was 8 hours, the median CIT of hours and a of hours in this previous studies of living donor exchange programs and shipping kidneys in the United States were limited by small sample sizes and report to this study in to DGF and graft and patient EG Miller ET Kwan L et al.Outcomes of shipped live donor kidney transplants compared with traditional living donor kidney transplants.Transpl Int. 2014; 27: 1175-1182Crossref PubMed Scopus (13) Google Scholar,6Segev DL Veale JL Berger JC et al.Transporting live donor kidneys for kidney paired donation: Initial national results.Am J Transplant. 2011; 11: 356-360Abstract Full Text Full Text PDF PubMed Scopus (63) Google Scholar from previous studies outcomes of LDKT found risk factors that were to our for DGF, and patient MA A risk for delayed graft function in the of deceased donor renal J Transplant. Full Text Full Text PDF PubMed Scopus Google time on as the risk for renal transplant a paired donor kidney PubMed Scopus Google of the or of on the survival of renal transplants from living Engl J Med. PubMed Scopus Google Scholar of older living donors is in clinical and from older donors have been to have outcomes in LDKT remain better deceased donor MA et al.Outcomes in kidney transplant recipients from older living 2015; 99: PubMed Scopus Google Scholar In DGF 5% are with donors the of which is the recent DGF of for LDKT in the SRTR Registry of Transplant of and and of Scholar On the other hand, donor which poorer graft survival in this study, that prolonged CIT other factors as these and other risk factors for poorer outcomes in LDKT, between and prolonged cold storage can be a in for for exchange outcomes. 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The practice of shipping living donor kidneys in KPD exchange programs increases CIT in kidney This study demonstrated increased odds of DGF for KPD recipients of shipped kidneys, no associations between CIT and graft or patient survival. support the practice of shipping living donor in to increase living donor be with the that the outcomes of shipping kidneys are not This study and evidence the of cold time and shipping for KPD programs, of the of living donor kidneys in the transplant This was in by and the National of and the and The is the of the and not the or policies of the of and of or organizations by the The are for and these the are of the and not of the or is by from the National of and and Kidney The data have been by the as the for the Scientific Registry of Transplant Recipients (SRTR). The and of these data are the of the and in no be as an of or by the SRTR or the The of this have no of to as by the of

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