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The Use of Donation After Circulatory Death Organs for Simultaneous Liver-kidney Transplant

To DCD or Not to DCD?

Vinson, Amanda Jean, MD1; Gala-Lopez, Boris, MD2; Tennankore, Karthik, MD1; Kiberd, Bryce, MD1

doi: 10.1097/TP.0000000000002434
Original Clinical Science—Liver
Open
SDC

Background. Because of the challenges with organ scarcity, many centers performing simultaneous liver-kidney transplant (SLKT) are opting to accept donation after circulatory death (DCD) organs as a means of facilitating earlier transplant and reducing death rates on the waitlist. It has been suggested, however, that DCD organs may have inferior graft and patient survival posttransplant compared with donation after neurologic death (DND) organs.

Methods. We created a Markov model to compare the overall outcomes of accepting a DCD SLKT now versus waiting for a DND SLKT in patients waitlisted for SLKT, stratified by base Model for End-Stage Liver Disease (MELD) score (≤20, 21–30, >30).

Results. Waiting for DND SLKT was the preferred treatment strategy for patients with a MELD score of 30 or less (incremental value of 0.54 and 0.36 quality-adjusted life years for MELD score of 20 or less and MELD score of 21 to 30 with DND versus DCD SLKT, respectively). The option to accept a DCD SLKT became the preferred choice for those with a MELD score greater than 30 (incremental value of 0.31 quality-adjusted life years for DCD versus DND SLKT). This finding was confirmed in a probabilistic sensitivity analysis and persisted when analyzing total life years obtained for accept DCD versus do not accept DCD.

Conclusions. There is a benefit to accepting DCD SLKT for patients with MELD score greater than 30. Although not accepting DCD SLKT and waiting for DND SLKT is the preferred option for patients with MELD of 30 or less, the incremental value is small.

1 Department of Medicine, Dalhousie University, Halifax, Nova Scotia., Canada.

2 Department of Surgery, Dalhousie University, Halifax, Nova Scotia, Canada.

Received 14 June 2018. Revision received 30 July 2018.

Accepted 22 August 2018.

The authors declare no funding or conflicts of interest.

All authors participated in research design. A.V. and B.K. did the initial data analysis. K.T. and B.K. provided feedback and suggestions to make the analysis more robust. A.V. wrote the initial article and B.K., B.G.L., and K.T. provided feedback and helped with constructing the figures.

Supplemental digital content (SDC) is available for this article. Direct URL citations appear in the printed text, and links to the digital files are provided in the HTML text of this article on the journal’s Web site (www.transplantjournal.com).

Correspondence: Amanda J Vinson, MD, 5082 Dickson Bldg, QEII Health Sciences Centre-VG site, 5820 University Avenue, Halifax, Nova Scotia, Canada B3H 1V9. (Amanda.vinson@nshealth.ca).

This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-No Derivatives License 4.0 (CCBY-NC-ND), where it is permissible to download and share the work provided it is properly cited. The work cannot be changed in anyway or used commercially without permission from the journal.

Organ transplant is the only treatment for end-stage liver disease (ESLD) and is the preferred treatment strategy for end-stage renal disease. Kidney failure occurs in 25% to 30% of patients with ESLD.1 Those patients with ESLD and concurrent renal insufficiency have been shown to have worse pretransplant and posttransplant outcomes than those with ESLD alone.2 The implementation of the Model for End-Stage Liver Disease (MELD) score to aid organ allocation for patients with ESLD has resulted in a dramatic increase in the proportion of liver transplant recipients undergoing simultaneous liver-kidney transplant (SLKT); from 2.5% in 2001 (before MELD allocation) to 8.2% in 2014 (after MELD allocation).3 This is explained partially by the fact that a higher MELD score indicates more severe disease, and those patients are therefore given priority for transplant. Renal status contributes to MELD and is overweighted such that those with renal insufficiency have a higher baseline MELD score irrespective of their underlying liver disease and thus, are often prioritized for liver ± simultaneous kidney transplant.4 Another factor that likely contributes to the increasing rate of SLKT includes the growing incidence of nonalcoholic steatohepatitis leading to a corresponding increase in the incidence of ESLD with concurrent renal insufficiency.5 Usual activation on the liver transplant waitlist occurs at a MELD score equal or greater than 15,6 though the minimum MELD for a patient with advanced renal disease is 20. Although a higher MELD score equates to a higher transplantation rate to facilitate organ triage for sicker individuals, it also indicates a higher death rate on the transplant waitlist. MELD scores are not static and can regress and progress over time.

Organ scarcity remains a challenge. In an effort to expand the donor pool, centers are accepting more expanded criteria donors to facilitate transplantation of patients on the transplant waitlist. One means of expanding the donor pool is to use donation after circulatory death (DCD) organs for transplant, defined as donors with severe and irreversible brain injury who do not meet formal criteria for brain death.7 Although controversial, this has been proposed to be a viable option for liver transplantation with similar patient and graft survival compared with donation after neurologic death (DND) organs.8,9 In DCD donors, after circulation is arrested, livers are exposed to a period of reduced perfusion with the potential for subsequent posttransplant ischemic biliary complications.10 In the liver transplant alone literature, a DCD liver transplant has been associated with inferior outcomes for patients with a MELD score less than 15, but provides a survival advantage for those with a MELD score greater than 20.11 In kidney transplant, DCD organs have been associated with an increased risk of delayed graft function, but no significant long term adverse outcomes.12,13 The impact of DCD organs for SLKT has been studied less rigorously, but there is a suggestion that DCD transplants may have slightly inferior outcomes compared with DND transplants.14 It is important to realize, however, that declining DCD SLKT to wait for optimal DND organs may not be in a patient’s best interest, as death on the transplant waitlist is not negligible. Although mortality rates are strongly modified by MELD score and underlying disease severity, in 2013, 1769 patients died waiting for a liver transplant and another 1223 were removed from the waitlist after becoming too sick to be transplanted.15

Accepting a DCD SLKT now has the potential to facilitate earlier transplantation and thereby reduce waitlist mortality, especially if wait times for DND SLKT are long. However, if organ quality is inferior with worse posttransplant outcomes than DND SLKT, then accepting a DCD SLKT now instead of waiting for relatively better DND SLKT organs has the potential to reduce overall patient and graft survival. The uncertainty around regional access to DND versus DCD organs (and as such, transplant wait times), patient and graft outcomes after SLKT with DND versus DCD organs, likelihood of retransplant and the heterogeneity of the MELD score make the best option difficult to predict with confidence. The purpose of this medical decision analysis is to determine if (i) in combined liver-kidney failure requiring SLKT, overall quality-adjusted life years (QALYs) are improved by accepting a DCD donor now versus waiting for a DND donor, and (ii) at which MELD score, if any, accepting a DCD donor become the treatment strategy of choice. Given the increased mortality and poor quality of life associated with progressive liver failure and advanced MELD scores, the hypothesis is that accepting DCD SLKT organs will become more beneficial as MELD scores increase and will eventually become the dominant treatment strategy.

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MATERIALS AND METHODS

A Markov model was created to examine outcomes in a cohort of US patients with combined liver and kidney failure waitlisted for SLKT, using a 10 year time horizon with 30-day cycles and a half cycle correction. For the purposes of this study, if listed for an SLKT, liver transplant alone (LTA) was not an option and patients were restricted to those on the deceased donation waitlist, without the option for a live donor liver or kidney transplant.

In the model, patients can accept a DCD SLKT now, or can decline DCD SLKT and wait for a DND SLKT. Those who accept a DCD SLKT can (i) remain well with functioning liver and kidney grafts, (ii) die or have liver graft failure, (iii) have kidney graft loss and either remain on dialysis or undergo kidney-after liver transplant (KALT), (iv) those who undergo KALT can either remain well or can lose their kidney graft. In those who do not accept DCD SLKT and instead choose to wait for DND organs, patients can (i) receive a DND SLKT transplant in which case the same above health states exist; however, in addition they can (ii) die on the transplant waitlist and/or (iii) progress/regress through MELD stages (Figure 1). Mortality and transplant rates from the literature were converted to probabilities. Because these rates are high, annual rates were converted to 30-day cycles to achieve more granular outcomes. Waitlist mortality and transplant rates, stratified by base MELD score, were obtained using data from the Scientific Registry of Transplant Recipients (Table 1).11 Patient and graft survival after SLKT were acquired from literature based on United Network for Organ Sharing data from 2002 to 2011, consisting of 3026 DND SLKT and 98 DCD SLKT recipients (the largest cohort to date), Table 1.14 In this study, there was no significant difference between DND and DCD SLKT recipient age at transplant (53.7 ± 9.8 y versus 54.2 ± 9.2 y for DND versus DCD SLKT, respectively; P = 0.64), sex (33.7% female for both DND and DCD SLKT; P = 1.0), or race (62.9% and 74.5% white for DND versus DCD SLKT, respectively; P = 0.12). However, MELD score was lower in those undergoing DCD SLKT (26.8 ± 7.5) than for those undergoing DND SLKT (29.3 ± 8.3) (P = 0.004).14

TABLE 1

TABLE 1

FIGURE 1

FIGURE 1

Overall QALYs projected for each option were calculated, stratified by base MELD score (≤20, 21–30, >30) and displayed as a cumulative incidence curve. Given literature availability, patients were stratified by the original MELD score, not the more recently introduced Na-MELD score.20,21 QALYs were discounted at an annual rate of 3%. The main outcome was the difference in QALYs between accept DCD SLKT versus do not accept DCD SLKT, assessed using a paired t test. In a secondary analysis, the total life years obtained for accept DCD SLKT and do not accept DCD SLKT were also determined. Although most events would be expected to occur before or early after SLKT (and thus would be reflected in a 10 year time horizon), we repeated the analysis for both QALYs and total life years extending the time horizon out to 20 years to confirm stability of our finding. Lastly, we calculated the median time to transplant in those who did not accept DCD and waited for DND SLKT.

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Key Assumptions

  1. The perspective was from the patient who will want to maximize their QALYs acknowledging that societal and patient perspectives may be conflicting.
  2. The annual death and/or graft loss probabilities were converted to 30-day cycles.4,14 We assumed a stable rate of death and/or graft loss in the first year, with no inclusion of a disutility state or increased risk of death immediately post-SLKT.
  3. We assumed a stable rate of death and/or graft loss (lower than the first 1 y) in the subsequent 9 years, given that the risk of death/graft loss is dramatically decreased after the first year posttransplant.
  4. Those who have liver graft failure are not retransplanted and have a health state equivalent to death.
  5. The repeat kidney transplant rate in SLKT recipients who lose their kidney graft is the same as the US national repeat transplant rate for kidney transplant alone.
  6. The rate of kidney graft loss for repeat kidney transplant is the same as for KALT.
  7. The probability of death with kidney graft failure post-SLKT is equivalent to the probability of death in combined liver-kidney organ failure patients on dialysis who undergo LTA.
  8. The same waitlist probabilities exist for MELD progression, transplantation, and death on the waitlist for SLKT as for liver transplant alone, stratified by baseline MELD score.
  9. Post-SLKT survival is independent of pretransplant MELD score and relates only to DCD versus DND organs.
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Sensitivity Analyses

  1. Two-way sensitivity analyses were performed to assess variability in 30-day transplant rates and death rates on the waitlist for those who opted to decline DCD SLKT and wait for potential DND SLKT, stratified by each base MELD category.
  2. A 1-way sensitivity analysis was used to vary the utilities for MELD of ≤20, 21–30, and >30 given heterogeneity in the MELD phenotype.
  3. Parameter uncertainty was assessed with probabilistic sensitivity analyses with beta-distributions for:
    • a.The 0- to 1-year probability of death and/or liver graft loss in DCD SLKT.
    • b.The 0- to 1-year probability of death and/or liver graft loss in DND SLKT.
    • c.The 1- to 10-year probability of death and/or liver graft loss in DCD SLKT.
    • d.The 1- to 10-year probability of death and/or liver graft loss in DND SLKT.
    • e.The 0- to 1-year probability of kidney graft loss in DCD SLKT.
    • f.The 0- to 1-year probability of kidney graft loss in DND SLKT.
    • g.The 1- to 10-year probability of kidney graft loss in DCD SLKT.
    • h.The 1- to 10-year probability of kidney graft loss in DND SLKT.
    • i.The probability of death after kidney graft failure in SLKT

TreeAge PRO Healthcare 2018 (TreeAge Software Inc., Williamstown, MA) was used for this medical decision analysis. First order Monte Carlo microsimulation was used to determine model heterogeneity with 10 000 trials. Uncertainty in patient and graft survival was examined using a probabilistic sensitivity analysis. In the simulation, 100 parallel head-to-head trials of 100 patients were run. The model was both internally and externally validated. Internal consistency was determined using the above sensitivity analyses and external consistency was determined by comparing median time to transplant for DND SLKT (accounting for transplant rate and death on the waitlist) to estimates based on epidemiologic data from unrelated studies. Given that this is a theoretical model that uses published population data, ethics approval was not required.

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RESULTS

The cumulative incidence curves for QALYs obtained for accept DCD and do not accept DCD are shown in Figure 2, stratified by base MELD score. Do not accept a DCD SLKT was the preferred treatment strategy for patients with a MELD score of 30 or less, resulting in an incremental value of 0.54 and 0.36 QALYs for MELD score of ≤20 and MELD score of 21–30 with DND versus DCD SLKT (Table 2). For those patients with MELD >30 however, accept a DCD SLKT became the dominant strategy with an incremental value for DCD versus DND SLKT of 0.31 QALYs (Table 2). This finding was confirmed in a probabilistic sensitivity analysis, varying parameter estimates for waitlist transplant and mortality rates, patient and liver/kidney graft survival in the first 0 to 1 years and the subsequent 1 to 10 years, and mortality in those with SLKT who lose their kidney graft (Table S1, SDC, http://links.lww.com/TP/B632). In probabilistic sensitivity analyses, the accept DCD strategy was selected 43%, 50%, and 67% of the time for MELD scores of ≤20, 21–30, and >30, respectively.

TABLE 2

TABLE 2

FIGURE 2

FIGURE 2

The same findings were confirmed when examining total life years gained from DCD versus DND SLKT instead of QALYs. Do not accept DCD was again preferred for those with a MELD ≤30 and accepting DCD was preferred when MELD score was greater than 30 (Table 2). Similar to the primary analysis, in probabilistic sensitivity analyses, the accept DCD strategy was the preferred option 39%, 49%, and 71% of the time for MELD scores of ≤20, 21–30, and >30, respectively.

Two-way sensitivity analyses are shown in Figures 3A, B, and C, varying 30-day waitlist mortality (from 0% to 50%) and transplant probability (from 0% to 50%), stratified by base MELD score. One-way sensitivity analyses are shown in Figure 4A–C, varying utilities for MELD scores of 20 or less, 21 to 30, and greater than 30.

FIGURE 3

FIGURE 3

FIGURE 4

FIGURE 4

In patients who do not accept DCD and wait for DND-SLKT, the time to greater than 95.0% of patients being transplanted or dying was 2.71, 2.05, and 0.49 years for those with MELD scores of ≤20, 21–30, and >30, respectively. The median time to transplant for these groups was approximately 240, 85, and 15 days (Figure 5). From the literature, median time to transplant is 82 days for MELD <30 and 14 days for MELD score of 30 to <40, confirming external consistency.22 For those who declined DCD and chose to wait for DND-SLKT, 22.7%, 20.9%, and 29.1% of patients with base MELD scores of ≤20, 21–30, and >30 died on the waitlist, never undergoing SLKT.

FIGURE 5

FIGURE 5

Extending the time horizon out to 20 years did not change the dominant strategy for each MELD category, (Table S2, SDC, http://links.lww.com/TP/B632).

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DISCUSSION

Worldwide, the transplant waitlist continues to grow with many more recipients waiting for organs than available donors. The number of patients on the waitlist in the United States has increased by 516% since 1991, with a relatively smaller 229% increase in donors.23 A variety of strategies to mitigate the organ shortage have been adopted, including an international effort to expand the use of DCD organs. It has been proposed that increased use of DCD organs could expand the donor pool twofold to 4.5-fold.24 The concern is that DCD organs may be of inferior quality to DND organs. Although controversial, liver transplant from DCD donors has comparable outcomes with DND liver transplant,8,9,25 especially in those with higher base MELD scores.11 In kidney transplant, DCD organs have similar long term outcomes as for DND organs, despite a higher rate of delayed graft function.12 The implications of DCD SLKT have been less rigorously studied. One cohort study suggested equivalent outcomes with DCD and DND SLKT at 1 year posttransplant, however this study included only 5 DCD SLKT recipients.25 A subsequent analysis demonstrated reduced 5-year patient and graft survival with DCD versus DND SLKT (56.7% versus 68.5%; 89.4% versus 97%; 84.2% versus 93% for patient, death-censored liver, and death-censored kidney survival, respectively).14 Despite being inferior to DND SLKT, 5-year patient and graft survival for DCD SLKT remained greater than 50% suggesting this may still be a reasonable option for transplant given the challenges with organ scarcity.14 Identifying which patients if any would benefit most from accepting a DCD SLKT was the objective for this medical decision analysis.

This study demonstrated that from the patient perspective, the decision of whether to accept or decline a DCD SLKT is dependent on a patient’s underlying disease severity as indicated by their MELD score. In those with lower MELD scores (MELD ≤30), the preferred treatment strategy is to not accept DCD SLKT and instead wait for better DND SLKT organs. This likely reflects the relatively lower waitlist mortality and higher baseline health utility in this less sick population. Conversely, for those with a MELD score >30, the strategy of choice is to accept a DCD SLKT now given the much higher waitlist mortality and lower health utility for this sicker group, irrespective of their higher transplant rate. This finding was robust across a number of sensitivity analyses varying waitlist mortality and transplant rate (for SLKT and kidney alone), as well as post-SLKT patient, liver, and kidney graft survival. All sensitivity analyses were coherent with expected conclusions suggesting the model was internally consistent. Median time to transplant for those who declined DCD SLKT and waited for DND organs was similar to epidemiologic data from another study not used in model derivation,22 which suggests the model was also externally consistent, acknowledging that not all centers perform SLKT, and results may vary between centers with high and low SLKT transplant rates.26

From the patient perspective, waiting for relatively better DND SLKT organs may be beneficial for those with lower MELD scores, however this conflicts with what is best from a societal perspective. For liver transplant in the United States, DCD organs have independently been associated with a nearly fourfold increase in the odds of organ nonuse; a trend which has increased over time.27 Declining organs simply for being of DCD origin has the potential to worsen the organ shortage and will contribute to the growing transplant waitlist. From a societal perspective, the utilization of all organs with a reasonable expectation for graft survival would be the preferred approach to maximize the donor pool and facilitate more transplantation. If there is no alternative candidate, the risk of declining DCD SLKT is one less person being transplanted and removed from the transplant waitlist. There is a benefit to the individual of accepting a DCD SLKT for those with a MELD >30, but not lower. Patient’s with higher MELD scores and more advanced disease are currently prioritized for LTA/SLKT given their high waitlist mortality rates, so are likely already triaged for whichever organs first become available (DCD or DND). Thus, this issue more so applies to DCD SLKT organs when there are no recipients with MELD score greater than 30. Although from the patient perspective declining these organs would be the preferred strategy in terms of quality of life, the incremental value of waiting for a DND SLKT is small (≤0.54 QALYs over 10 y) and the societal cost of not reducing the waitlist is large. As such, DCD SLKT should still be considered in these patients if no higher risk candidates (MELD score, >30) are available.

This study has limitations. It was assumed patients with liver graft loss would not be retransplanted and as such, both death and liver graft failure were treated as a composite outcome with a utility of 0. While retransplantation is the only viable option for liver graft failure, it has been associated with a high mortality rate (1 y patient survival of 45% for 2nd transplants and 1 year survival 24% for 3rd transplants)28 and the benefit of retransplantation has been proposed to be limited to certain healthier subgroups.29 Despite this, repeat liver transplant occurs in 5% to 19% of all liver transplants30,31 and could be considered in a more complex future model. Inclusion of an option for repeat liver transplant would have favored the accept DCD arm given the reduced graft survival rates observed with DCD SLKT. We also assumed that those waiting for SLKT could not undergo LTA, although it is known that about 12% of the population with combined liver-kidney failure will actually undergo LTA.1 The indications for SLKT versus LTA in patients with varying degrees of renal insufficiency are not well established, but most centers are striving to achieve SLKT in appropriate candidates as a way of increasing donor tolerogenicity and improving kidney graft survival compared with KALT.32 Parameter uncertainty for posttransplant outcomes was addressed in multiple sensitivity analyses. It should be noted that patients with ESLD and advanced kidney disease generally have a MELD score of 20 or greater; however, patients with MELD score <20 may still undergo SLKT.33 Based on available literature regarding both health states and transition probabilities, we chose to stratify our model by MELD score, not Na-MELD. Although Na-MELD has been shown to have better predictive accuracy for 90-day mortality than the original MELD score, the difference between the 2 is small and of uncertain significance (c-statistic 0.883 for Na-MELD and 0.868 for MELD) with 93% crossover between the 2 scores.20 Additionally, an Na-MELD based LTA/SLKT allocation system was only adopted in the United States in 2016 and thus was not in use during the 2002 to 2011 period from which our transition probabilities were derived.34 Thus, given the available literature we felt that use of the MELD score was clinically appropriate, however, to confirm stability of our results, we did explore a range of health states and transition probabilities for each base MELD score (encompassing corresponding Na-MELD); none of which altered our result. Results based on Na-MELD score would not be expected to significantly differ from those presented here, however this may be an area for future study. It has been suggested that given the heterogeneic phenotype of the MELD score, MELD score in and of itself may not correlate well with quality of life (QOL).35 Ascites and encephalopathy have been associated with worse QOL, but the presence of these decompensations is not well captured by the MELD scoring system and therefore, there may be uncertainty around the utilities assigned for each base MELD category.35 This issue was addressed using a 1-way sensitivity analysis varying the utilities for each MELD category assessed, and could potentially be explored in a future analysis that incorporates the baseline Child-Pugh score in addition to MELD. We did not have data available to examine more granular cut-points for baseline MELD scores. Our study demonstrates that the transition point where not accepting and accepting a DCD SLKT lies somewhere between a MELD score of 21–30 and MELD score >30, but we did not have the data available to determine the exact threshold where this decision changes. Lastly, it is important to acknowledge that while this model was designed to explore patient QOL related to DND versus DCD SLKT, it does not consider other patient factors that may motivate a patient to accept the first available organ; for example, medical expenses or lost wages while on medical leave. Extrinsic patient motivators for accepting an organ with a shorter wait time would be expected to favor acceptance of DCD organs.

In summary, patients with a MELD score of ≤30 benefit from waiting for a DND SLKT given their relatively low waitlist mortality. In patients with a MELD score >30, however, accepting a DCD SLKT is the preferred treatment strategy given the reduced QOL and high mortality on the SLKT waitlist. Declining a DCD SLKT may not be the strategy of choice from a societal perspective, however, as it has the potential to result in higher organ discard rates and longer transplant waitlists. For lower MELD scores, the societal and individual perspectives regarding DCD SLKT are conflicting; however, it should be noted that the incremental value of declining DCD SLKT in patients with lower MELD scores is small, whereas the societal risk may be large.

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