Abstract
Background.
Donation after circulatory death (DCD) is the major contributor to the growth in deceased organ donation in the United States. Normothermic regional perfusion (NRP) and ex situ machine perfusion (es-MP) have been vital for improving organ assessment and preservation in DCD donor organs. The procurement procedure and storage strategy for noncardiac donors were determined by liver transplant centers in the early era of machine perfusion in the United States. In this study, we analyzed the landscape of liver utilization from noncardiac DCD donors in the United States during the early era of machine perfusion.
Methods.
All adult (18 y and older) DCD donors in the United States for which the heart was not used for transplantation from October 1, 2020, to December 31, 2023, were compared using procurement technique (NRP versus super rapid recovery [SRR]) and storage strategy (ex situ machine perfusion [es-MP] versus static cold storage).
Results.
One hundred fifty-six livers were transplanted from 284 NRP donors (55% utilization) versus 2497 liver transplants from 9132 SRR donors (27% utilization). Es-MP was used in 19% (n = 30) of liver NRP cases versus 28% (n = 695) of liver SRR cases. Eight hundred fifty-one liver grafts (32%) were exposed to NRP, es-MP, or both.
Conclusions.
Given the variation in liver graft management, further research needs to be conducted on the optimal strategies for using technologies such as NRP and es-MP in liver transplantation in the United States; better data collection is necessary to support this research and additional strategies are required to increase access to machine perfusion on a national level are needed.
INTRODUCTION:
Donation after circulatory death (DCD) is driving the increase in deceased organ donation in the United States. Some of the growth in liver utilization from DCD donors can be attributed to machine perfusion technology that allows for preimplantation graft assessment and results in better recipient outcomes.1-4 In situ machine perfusion, termed normothermic regional perfusion (NRP), is a technique that delivers oxygenated blood to organs intended for transplantation by using cannulas inserted into the donor’s blood vessels connected to a modified cardiopulmonary bypass machine. Ex situ machine perfusion (es-MP) delivers either oxygenated blood or a hypothermic oxygenated solution to the organs after they have been removed from the donor and can be performed either at the donor hospital (on-site) or at the transplant center (back to base). NRP and es-MP reduce the risks of liver primary nonfunction and ischemic cholangiopathy compared with super rapid recovery (SRR) with static cold storage (SCS).2,5-7
NRP and es-MP access depend on several factors that vary among transplant centers. NRP requires transporting specialized equipment, perfusionists, and surgeons trained in NRP cannulation to the donor hospital. The equipment for NRP pumps can be designed by the perfusion team to use existing portable pumps. Because cardiac transplant centers developed the first NRP programs, access to NRP in the early US experience was limited to cardiac DCD donors. A recent study of the landscape of liver transplantation (LT) from cardiac DCD donors found that most liver grafts were exposed to at least 1 type of machine perfusion and that almost 60% of transplant centers (50/84) used a liver graft from an NRP-DCD cardiac donor versus <30% of transplant centers (24/84) that used a liver graft from an SRR donor with es-MP.8 Because noncardiac donors require abdominal transplant teams or organ procurement organizations (OPOs) to provide NRP, there is likely a different landscape in the utilization of NRP for these cases.
Although the choice of procurement technique for cardiac DCD cases is generally at the discretion of the cardiac center, the choice to use es-MP is up to the LT center. Es-MP for liver grafts is currently restricted to 2 normothermic devices in the United States: Transmedics Organ Care System (OCS) and OrganOx Metra. OCS is a full-service model that includes organ procurement, transportation, and machine perfusion management, and the perfusion begins at the donor hospitals. Metra can be transported to a donor hospital for on-site perfusion of the graft and transport to the recipient hospital, or used as a back-to-base model in which the liver graft is placed on SCS at the donor hospital and then placed on the Metra at a transplant hospital or OPO facility. In terms of access, OCS can be activated for any donor through a national system and requires a surgeon certified by Transmedics to perform the procurement and Transmedics-approved or owned transportation of the device. Metra is only available at transplant centers and OPOs that have an on-site device.
The increase in access and utilization of machine perfusion is likely influencing noncardiac DCD liver graft utilization, allocation, and distribution. Therefore, it is crucial to determine how procurement methods and storage modalities have been adopted for LT in the United States and how these different approaches can lead to improved opportunities for organ utilization, transplant efficiency, and value. This study aims to describe donor, recipient, and logistical characteristics of LT from noncardiac DCD donors by procurement method and storage modality in the early era of machine perfusion in the United States.
MATERIALS AND METHODS
Data Collection
This study was approved by the Baylor University Medical Center Institutional Review Board (No. 009-261) with a waiver of informed consent. All research was conducted in accordance with both the Declaration of Helsinki and the Istanbul Declaration. Using the United Network for Organ Sharing standard transplant analysis and research (UNOS STAR) file, donor and recipient characteristics of all adult (18 y and older) noncardiac DCD donors in which the heart was not used for transplantation were identified from October 1, 2020, to December 31, 2023. The start of the study timeframe aligned with the first reported thoracoabdominal (TA)-NRP-DCD procurement in the United States.2 The UNOS data do not have variables that identify procurement techniques: SRR or NRP. Therefore, we used a previously described technique in which donors with death to cross-clamp time of <30 min were categorized as SRR, and death to cross-clamp time ≥30 min was categorized as NRP. The reasoning for our method has been previously described.9 The utilization rate for liver grafts was calculated as the number of liver grafts transplanted divided by the number of deceased donors.
Statistical Data Analysis
Donor and recipient characteristics were compared between the SRR and NRP cohorts. Continuous variables were summarized using median and interquartile range. Categorical variables were summarized using counts and percentages. The Wilcoxon rank-sum test was used to compare continuous variables. Pearson’s chi-square test or the Fisher exact test was used to compare categorical variables. Statistical significance was defined as P value of <0.05. Kaplan-Meier survival curves were used for LT 12-mo patient survival and graft survival. Log-rank tests were used to statistically compare patient death and graft failure between the SRR and NRP groups. Statistical analyses were conducted using R version 4.3.2.
RESULTS
Cohort Validation
Figure 1 shows the frequency of occurrences of time in minutes from the declaration of death to cross-clamping. There are 2 clear frequency groupings >30 min and <30 min, indicating NRP and SRR donors.
FIGURE 1.
Histogram of the frequency of occurrences of time in minutes from death to cross-clamp showing the distinction between procurement techniques for all US noncardiac donation after circulatory death (DCD) donors from October 1, 2020, to December 31, 2023. SRR clusters <30 min, and NRP clusters >30 min. NRP, normothermic regional perfusion; SRR, super rapid recovery.
LT Donor and Recipient Characteristics and Outcomes
There were 284 NRP donors and 9132 SRR noncardiac donors identified in the study period. Table 1 shows the characteristics of the noncardiac DCD donors from which the liver was used for transplantation, as well as recipient and logistical characteristics. There was a significant difference in the utilization of liver machine perfusion between groups, with 19% of NRP cases (n = 30) using es-MP versus 31% of SRR cases (n = 782). NRP donors were older (median age 50 versus 45 y, P < 0.001) and had a higher median body mass index (29 versus 27 kg/m2, P = 0.004) than SRR donors. There were no statistically significant differences in terminal transaminases, total bilirubin, or donor gender between NRP and SRR groups. There was also no statistically significant difference in recipient median age, Model for End-stage Liver Disease score, or diagnosis of hepatocellular carcinoma. NRP LT recipients had a shorter median length of stay (7 versus 8 d, P < 0.001), shorter distance between donor and recipient hospitals (32 versus 99 miles, P < 0.001), and shorter median cold ischemia times (5.2 versus 6.6 h, P < 0.001) than SRR LT recipients.
TABLE 1.
Liver transplant donor and recipient characteristics by recovery technique
| Characteristic | NRP (N = 156) | SRR (N = 2497) | P |
|---|---|---|---|
| Donor | |||
| Age, y, median (IQR) | 50 (37–58) | 45 (35–54) | <0.001 |
| Male sex, n (%) | 95 (61) | 1610 (64) | 0.4 |
| BMI, kg/m2, median (IQR), | 29 (25–34) | 27 (24–32) | 0.004 |
| Death to clamp time, min, median (IQR) | 107 (72–145) | 6 (4–8) | <0.001 |
| Hepatitis C positive | 12 (7.7) | 212 (8.5) | 0.7 |
| Terminal AST | 47 (29–82) | 49 (31–80) | 0.7 |
| Terminal ALT | 37 (21–70) | 38 (22–74) | 0.6 |
| Liver machine perfusion, n (%) | 0.002 | ||
| No | 118 (76) | 1642 (66) | |
| Yes | 30 (19) | 782 (31) | |
| Missing | 8 (5.1) | 73 (2.9) | |
| Recipient | |||
| Age, y | 58 (52–64) | 59 (51–65) | 0.8 |
| BMI, kg/m2, median (IQR) | 28.9 (26.2–33.5) | 28.4 (24.8–32.5) | 0.051 |
| Hepatocellular carcinoma diagnosis, n (%) | 0.068 | ||
| No | 113 (72) | 1877 (75) | |
| Yes | 37 (24) | 585 (23) | |
| Missing, n (%) | 6 (3.8) | 35 (1.4) | |
| MELD score at transplant, median (IQR) | 18 (14–23) | 19 (14–24) | 0.7 |
| Length of hospital stay, median (IQR) | 7 (5–10) | 8 (6–12) | <0.001 |
| Distance between donor and recipient hospital | 32 (8–142) | 99 (19–228) | <0.001 |
| Cold ischemia time, median (IQR) | 5.2 (4.0–6.6) | 6.6 (5.0–12.7) | <0.001 |
ALT, alanine transaminase; AST, aspartate transaminase; BMI, body mass index; IQR, interquartile range; MELD, Model for End-stage Liver Disease.
Patient and graft survival were analyzed by procurement technique (Figure 2). There was no statistically significant difference in patient survival at 1 y between NRP and SRR (96% versus 95%, P = 0.66) or in graft survival at 1 y (96% NRP versus 92% SRR, P = 0.22). Notably, graft survival in the SRR group was lower than patient survival, which was not the case with NRP, suggesting that there were more early graft losses in the SRR group.
FIGURE 2.
Comparison of 12-mo liver transplant patient survival (A) and graft survival (B) outcomes between NRP and SRR donation after circulatory death (DCD) recipients. NRP, normothermic regional perfusion; SRR, super rapid recovery.
Patient and graft survival were further compared by the combination of procurement technique and storage strategy: NRP with es-MP, NRP with SCS, SRR with es-MP, and SRR with SCS (Figure 3). There was no statistically significant difference among groups in patient or graft survival at 12 mo, and notably, the NRP with es-MP group had only 9 grafts. However, 1-y graft survival did have more separation among cohorts: 100% for NRP with es-MP, 96% for NRP with SCS, 93% for SRR with es-MP, and 91% for SRR with SCS.
FIGURE 3.
Comparison of 12-mo liver transplant patient survival (A) and graft survival (B) outcomes comparing NRP with SCS, NRP with es-MP, SRR with SCS, and SRR with es-MP procurement technique and storage strategy combinations. es-MP, ex situ machine perfusion; NRP, normothermic regional perfusion; SCS, static cold storage; SRR, super rapid recovery.
Liver Graft Utilization
Of the 9416 DCD donors in this study period for which the heart was not used for transplantation, 284 donors (3%) underwent NRP, whereas 9132 donors (97%) underwent SRR. In terms of utilization, 156 livers were transplanted from the 284 NRP donors (54.9% utilization) versus 2497 livers (27.3%) transplanted from 9132 total SRR donors (P < 0.001). Figure 4 shows the utilization rates for NRP and SRR over time. In 2020, NRP utilization was lower (14.3%) than SRR (26.2%), but there were <10 NRP donors in that cohort. In 2023, NRP utilization was 61.7% versus 32.0% for SRR, showing that there was an increase in both cohorts from 2020 but with a significantly higher utilization rate in NRP (P < 0.001). Utilization rates for es-MP could not be studied as the intention to use es-MP was not collected by UNOS.
FIGURE 4.
Plot of the annual liver utilization rates showing the distinction between procurement techniques for all US cardiac donation after circulatory death (DCD) donors from October 1, 2020, to December 31, 2023. NRP, normothermic regional perfusion; SRR, super rapid recovery.
Distribution of LTs by Procurement Technique and Storage Modality
During the study period, 99 transplant centers performed at least 1 DCD LT from a noncardiac donor. The geographic distribution of LTs by center, procurement technique, and storage modality is shown in Figure 5. Thirty-five centers (35.4%) used both NRP and SRR donors, 63 centers (63.6%) exclusively used liver grafts from SRR donors, whereas only 1 center (1.0%) exclusively used NRP donors. In terms of storage modality, 53 centers (53.5%) used a combination of es-MP and SCS, 2 (2.0%) exclusively used es-MP (1 performed 4 transplants and 1 performed 2 transplants) and 44 (44.4%) used SCS only. Table 2 shows transplant center utilization by procurement technique and storage strategy. Thirty-six centers (36.4%) used NRP, and 55 (55.6%) used es-MP for at least 1 liver graft. Table 2 also shows the liver graft management by procurement technique and storage strategy. Most grafts (1802; 67.9%) were not exposed to machine perfusion. Overall, 851 liver grafts (32.1%) were exposed to some form of machine perfusion, either NRP with SCS, SRR with es-MP, or NRP with es-MP. Only 5.9% of the total grafts (n = 156) in the study were exposed to NRP.
FIGURE 5.
Transplant center distribution of donation after circulatory death (DCD) liver grafts by procurement technique and storage modality. MP, machine perfusion; NRP, normothermic regional perfusion; SCS, static cold storage; SRR, super rapid recovery.
TABLE 2.
Distribution of liver grafts and transplant center graft utilization by the combination of procurement technique (NRP vs SRR) and storage strategy (SCS and es-MP)
| Liver graft management by procurement technique and storage strategy | ||
|---|---|---|
| Liver grafts (N = 2653) | SCS (N = 1928) | es-MP (N = 725) |
| NRP (n = 156) | 126 (4.8%) | 30 (1.1%) |
| SRR (n = 2497) | 1802 (67.9%) | 695 (26.2%) |
| Transplant center graft utilization by procurement technique and storage strategy | ||
| Transplant center (N = 99) | SCS (N = 97) | es-MP (N = 55) |
| NRP (n = 36) | 34 (34.3%) | 9 (9.1%) |
| SRR (n = 98) | 96 (97%) | 54 (54.5%) |
For liver graft management, the n is representative of each graft. For transplant center graft utilization, the n for each combination represents the utilization of that combination of technology at least once by a unique transplant center, and the percentages are calculated by the denominator of total number of transplant centers (n = 99).
es-MP, ex situ machine perfusion; NRP, normothermic regional perfusion; SCS, static cold storage; SRR, super rapid recovery
Geographic Distribution of DCD Liver Donors
Figure 6 shows the distribution of donors in each donor service area by procurement technique and storage modality for noncardiac DCD donors. Twenty-five of the 55 OPOs represented in this study had only SRR procurements, and none had only NRP procurements. The remaining 30 had both NRP and SRR procurements. Of the OPOs that had >25 DCD donors during the study period, 17 had only SRR, whereas the rest had a combination of SRR and NRP recoveries. More than half of OPOs were involved with at least 1 noncardiac NRP procurement.
FIGURE 6.
Geographic distribution of donation after circulatory death (DCD) donors in each donor service area (DSA) by procurement technique and storage modality. MP, machine perfusion; NRP, normothermic regional perfusion; SCS, static cold storage; SRR, super rapid recovery.
Allocation Logistics
Table 3 shows the numeric distribution of grafts by distance categories (≤150 nautical miles [NM], 151–250 NM, 251–500 NM, and >500 NM). A total of 1719 donors (64.8%) were located within 150 NM of the recipient transplant center, whereas 270 (10.2%) were located >500 NM away from the recipient transplant center. Figure 7 is a violin plot of the distances between donor and recipient hospitals by procurement technique and storage strategy. Notably, SRR recoveries had a wider variation in distances than NRP recoveries.
TABLE 3.
Distance distribution of graft utilization by procurement technique (NRP vs SRR) and storage strategy (SCS and es-MP)
| ≤150 NM (N = 1719; 64.8%) |
151–250 NM (N = 334; 12.6%) |
251–500 NM (N = 330; 12.4%) |
>500 NM (N = 270; 10.2%) |
|
|---|---|---|---|---|
| NRP plus es-MP n = 30 (1.1%) |
23 | 2 | 5 | 0 |
| NRP plus SCS n = 126 (4.8%) |
96 | 16 | 12 | 2 |
| SRR plus es-MP n = 695 (26.2%) |
383 | 84 | 97 | 131 |
| SRR plus SCS n = 1802 (67.9%) |
1217 | 232 | 216 | 137 |
es-MP, ex situ machine perfusion; NM, nautical miles; NRP, normothermic regional perfusion; SCS, static cold storage; SRR, super rapid recovery.
FIGURE 7.
Violin plot of liver transportation distances by procurement technique for all US noncardiac donation after circulatory death (DCD) donors from October 1, 2020, to December 31, 2023. MP, machine perfusion; NRP, normothermic regional perfusion; SCS, static cold storage; SRR, super rapid recovery.
DISCUSSION
In this study, we report the outcomes, utilization, and distribution of LTs from noncardiac DCD donors, stratified by procurement technique and storage strategy. The current study found notable differences in noncardiac DCD donor characteristics between NRP and SRR cohorts in the United States. NRP donors were older with a higher body mass index than SRR donors, whereas the recipients of these grafts did not differ in age, Model for End-stage Liver Disease score, or diagnosis of hepatocellular carcinoma. Several studies on NRP-DCD LT have shown that this technique allows an increase in thresholds for donor age, functional warm ischemia time, and recipient complexity. For example, a retrospective review of NRP versus SRR LTs in Spain from 2012 to 2019 had a median NRP donor age of 59 y versus 58 y for the SRR cohort, with no differences in recipient characteristics. Despite the slightly older median age, the rates of early allograft dysfunction, biliary complications, retransplantation, and death were all lower in the NRP cohort.10 Another study from the United Kingdom, comparing SRR to NRP LTs, also had a higher median age for donors than the current study for both groups, that is, 57 y.11 In this study, there was a 51% lower risk-adjusted hazard of transplant failure in the NRP group versus SRR.11 In a single-center, observational cohort study from Italy, 1-y graft survival for NRP-DCD donors aged 75 y and older was 93.3% compared with 83.3% in an age-matched donation after brain death cohort.12 Finally, compared with a previous study by our group on cardiac DCD donors, the cohort of NRP donors in the present study is substantially older, suggesting that NRP for noncardiac donors is allowing for further expansion of the utilization of this technology for a different donor population.8
One of the more striking findings of the current study is the significant increase in liver utilization rates over time with NRP. In 2020, there were <10 noncardiac NRP DCDs, and the utilization rate was 14.3% compared with 2023, in which 121 of 196 liver grafts were used, resulting in a 61.7% utilization rate. Although SRR utilization rates have increased from 26.2% to 32.0%, they currently lag behind NRP utilization rates. However, this finding must be contextualized in that there are no data on whether donor livers were accepted for transplant, meaning that there could be a significant proportion of kidney-only DCD donors in which there was never liver utilization intent. Therefore, although the utilization rates for NRP are higher than those for SRR, the SRR rates may be higher than what we found for those cases in which there was liver utilization intent. Despite these limitations, our findings are similar to those of a UK study, which found a 63% NRP liver utilization rate versus a 34% SRR liver utilization rate.11 Moreover, a study on the utilization of liver grafts from TA-NRP donors in the United States versus SRR donors found that utilization with TA-NRP was significantly higher at 70.6% versus 24.4% with SRR.1 However, the TA-NRP cohort was very small in this study, and there was likely a selection bias toward standard DCD donors.
In this study, a minority of liver grafts were exposed to machine perfusion, which differs from the findings of a previous study on cardiac DCD donor liver utilization in the United States where 63.2% of grafts were exposed to at least 1 type of perfusion technology. Noncardiac DCD donors require either an OPO-based NRP program or an abdominal transplant center-based NRP program.13,14 Conversely, the wider availability of normothermic machine perfusion to any transplant program, along with the mitigation of distance and cold time constraints, may explain the larger number of centers using this technology for noncardiac DCD liver grafts, especially those from further away. Moreover, the current study found that the utilization rates of SRR liver grafts were lower than those of NRP liver grafts (27.3% versus 54.9%), which differs from the cardiac donor study in which 61% of TA-NRP liver grafts were used compared with 56% of SRR liver grafts. The difference in these findings could be related to 2 factors. First, the donors in the current study may be more medically complex than those in the cardiac DCD study, as the median donor age in the current study was 50 in the NRP group and 45 in the SRR group compared with 31 in both cohorts of the cardiac DCD study. Second, some of the donors in the study would not have had the liver allocated for transplantation due to quality, a data point not available for this study. It is likely that most NRP donors in the cohort had their liver allocated for transplantation, as very few kidney-only donors underwent NRP in the early era of machine perfusion in the United States. Because we do not know which grafts were intended for transplantation at the time of withdrawal, we do not know the true utilization rate of livers with the intention to transplant in each group and suspect that there were more donors in the SRR group who did not have an intention to transplant. However, further research is needed to determine utilization rates from an intention to transplant starting point. Although our study shows a difference in the application of machine perfusion types and utilization rates for noncardiac DCD donors compared with our previous study of cardiac DCD donors, it does not provide concrete explanations for these differences, a topic that needs further investigation.
There are several limitations to this study. First, the method used to categorize NRP and SRR donors has been used in multiple studies because the procurement technique is not a variable included in the UNOS STAR file. Although we believe that this method is accurate, it could miscategorize some donors in which times are not accurately recorded or in which the death-to-cross-clamp time is >30 min in SRR recoveries. This limitation indicates an opportunity to improve data collection by adding a field for procurement technique, as we have previously recommended.8,15 Another limitation is that the accuracy of es-MP data collection may not be adequate if back-to-base es-MP is not captured in the UNOS STAR file. Again, this provides an opportunity for better data collection, specifically, not only when machine perfusion is used but also when the type of es-MP is used, as well as perfusion start and end times, so that research can be conducted on the optimal protocols for es-MP liver graft management. Finally, in terms of utilization rates, the current study could not capture whether there was an intention to use liver grafts from DCD donors or even an intention to use es-MP before procurement. Because of this, some of the donors may never have had a liver allocated, so there was never an intention to use the grafts from these donors. Further studies that start with either allocation intention or predonation liver graft acceptance should be conducted to gain a better understanding of how NRP and es-MP impact graft utilization rates.
In conclusion, this study provides a broad overview of the current state of LT and graft utilization from noncardiac DCD donors, categorized by procurement technique and storage strategy in the United States. Although the majority of DCD grafts in this study were not exposed to machine perfusion technology, we believe that this will change soon because of better outcomes associated with both NRP and es-MP DCD LT as well as expanded options. Specifically, the eventual commercial adoption of hypothermic machine perfusion in the United States will provide another option for liver assessment and storage, which could change center approaches to DCD liver graft utilization. Because of the rapidly changing nature of LT with machine perfusion, better data collection must be implemented at a national level so that the transplant community can understand how these technologies are being used, how they can be optimized, and how they can be used in complementary ways to best serve LT recipients.
Footnotes
A.W. designed the study, oversaw the analysis of the data, and provided critical revisions to the article. J.D. assisted in study design, conducted the data analysis, and assisted in drafting and revision of the article. M.S. assisted in study design, data collection and cleaning, article writing, and figure editing. J.B., S.D., S.H.L., E.M., and A.G. provided critical feedback on the article. G.R. and W.F.P. assisted in study design, data analysis, and article revisions. S.A. assisted with study design and critical feedback on the article. G.T. assisted with study design and article revisions.
A.W. is the medical director of Regional Perfusion Services. The other authors declare no conflicts of interest.
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Contributor Information
Jinyu Du, Email: jinyu.du@bswhealth.org.
Matthew Snoddy, Email: matthew.snoddy@bswhealth.org.
Johanna Bayer, Email: johanna.bayer@bswhealth.org.
Sebastian Danobeitia, Email: juan.danobeitia@bswhealth.org.
Seung Hee Lee, Email: seunghee.lee@bswhealth.org.
Eric Martinez, Email: eric.martinez1@bswhealth.org.
Amar Gupta, Email: amar.gupta@bswhealth.org.
William F Parker, Email: william.parker@bsd.uchicago.edu.
Sumeet Asrani, Email: sumeet.asrani@bswhealth.org.
Giuliano Testa, Email: giuliano.testa@bswhealth.org.
REFERENCES
- 1.Bekki Y, Croome KP, Myers B, et al. Normothermic regional perfusion can improve both utilization and outcomes in DCD liver, kidney, and pancreas transplantation. Transplant Direct. 2023;9:e1450. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Brubaker AL, Sellers MT, Abt PL, et al. US liver transplant outcomes after normothermic regional perfusion vs standard super rapid recovery. JAMA Surg. 2024;159:677. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Chapman WC, Barbas AS, D’Alessandro AM, et al. Normothermic machine perfusion of donor livers for transplantation in the United States: a randomized controlled trial. Ann Surg. 2023;278:e912–e921. [DOI] [PubMed] [Google Scholar]
- 4.Mergental H, Laing RW, Kirkham AJ, et al. Transplantation of discarded livers following viability testing with normothermic machine perfusion. Nat Commun. 2020;11:2939. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Eden J, Bruggenwirth IMA, Berlakovich G, et al. Long-term outcomes after hypothermic oxygenated machine perfusion and transplantation of 1,202 donor livers in a real-world setting (HOPE-REAL study). J Hepatol. 2025;82:97–106. [DOI] [PubMed] [Google Scholar]
- 6.Hessheimer AJ, Riquelme F, Fundora-Suarez Y, et al. Normothermic perfusion and outcomes after liver transplantation. Transplant Rev (Orlando). 2019;33:200–208. [DOI] [PubMed] [Google Scholar]
- 7.Markmann JF, Abouljoud MS, Ghobrial RM, et al. Impact of portable normothermic blood-based machine perfusion on outcomes of liver transplant: the OCS Liver PROTECT randomized clinical trial. JAMA Surg. 2022;157:189–198. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Wall A, Snoddy M, Du J, et al. The current landscape of in situ and ex situ machine perfusion utilization for liver grafts from cardiac donation after circulatory death donors in the US. Am J Transplant. 2024;25:574. [DOI] [PubMed] [Google Scholar]
- 9.Wall A, Rosenzweig M, McKenna GJ, et al. Six-month abdominal transplant recipient outcomes from donation after circulatory death heart donors: a retrospective analysis by procurement technique. Am J Transplant. 2023;23:987–995. [DOI] [PubMed] [Google Scholar]
- 10.Hessheimer AJ, de la Rosa G, Gastaca M, et al. Abdominal normothermic regional perfusion in controlled donation after circulatory determination of death liver transplantation: outcomes and risk factors for graft loss. Am J Transplant. 2022;22:1169–1181. [DOI] [PubMed] [Google Scholar]
- 11.Oniscu GC, Mehew J, Butler AJ, et al. Improved organ utilization and better transplant outcomes with in situ normothermic regional perfusion in controlled donation after circulatory death. Transplantation. 2023;107:438–448. [DOI] [PubMed] [Google Scholar]
- 12.Fallani G, Stocco A, Siniscalchi A, et al. Beyond the concepts of elder and marginal in DCD liver transplantation: a prospective observational matched-cohort study in the Italian clinical setting. Transpl Int. 2023;36:11697. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Croome KP, Brown TE, Mabrey RL, et al. Development of a portable abdominal normothermic regional perfusion (A-NRP) program in the United States. Liver Transpl. 2023;29:1282–1291. [DOI] [PubMed] [Google Scholar]
- 14.Wall A, Arunachalam P, Martinez E, et al. Stepwise development and expansion of an abdominal normothermic regional perfusion program for donation after circulatory determination of death organ procurement. Clin Transplant. 2024;38:e15297. [DOI] [PubMed] [Google Scholar]
- 15.Wisel SA, Steggerda JA, Brubaker AL, et al. Keep the engine running: maintaining transplant registry utility in liver transplant. Am J Transplant. 2024;25:447. [DOI] [PubMed] [Google Scholar]