Machine perfusion in liver transplantation.
Journal
Hepatology (Baltimore, Md.)
ISSN: 1527-3350
Titre abrégé: Hepatology
Pays: United States
ID NLM: 8302946
Informations de publication
Date de publication:
11 2022
11 2022
Historique:
revised:
24
02
2022
received:
19
01
2022
accepted:
24
02
2022
pubmed:
1
5
2022
medline:
22
10
2022
entrez:
30
4
2022
Statut:
ppublish
Résumé
Although liver transplantation is a true success story, many patients still die awaiting an organ. The increasing need for liver grafts therefore remains an unsolved challenge to the transplant community. To address this, transplant donor criteria have been expanded and, for example, more liver grafts with significant steatosis or from donors with circulatory death are being used. These marginal grafts, however, carry an increased risk of graft-associated complications, such as primary nonfunction, delayed graft function, or late biliary injuries. Therefore, reliable assessment of graft viability before use is essential for further success. To achieve this, machine liver perfusion, a procedure developed more than 50 years ago but almost forgotten at the end of the last century, is again of great interest. We describe in this review the clinical most applied machine perfusion techniques, their mechanistic background, and a novel concept of combining immediate organ assessment during hypothermic oxygenated perfusion, followed by an extended phase of normothermic machine perfusion, with simultaneous ex situ treatment of the perfused liver. Such a new approach may allow the pool of usable livers to dramatically increase and improve outcomes for recipients.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1531-1549Informations de copyright
© 2022 American Association for the Study of Liver Diseases.
Références
Starzl TE, Iwatsuki S, Van Thiel DH, Carlton Gartner J, Zitelli BJ, Jeffrey Malatack J, et al. Evolution of liver-transplantation. Hepatology. 1982;2(5):614S-636S.
Trotter JF, Cárdenas A. Liver transplantation around the world. Liver Transpl. 2016;22(8):1059-61.
Pandya K, Sastry V, Panlilio MT, Yip TCF, Salimi S, West C, et al. Differential impact of extended criteria donors after brain death or circulatory death in adult liver transplantation. Liver Transpl. 2020;26(12):1603-17.
Panconesi R, Carvalho MF, Muiesan P, Dutkowski P, Schlegel A. Liver perfusion strategies: What is best and do ischemia times still matter? Curr Opin Organ Transplant. 2022. https://doi.org/10.1097/MOT.0000000000000963
Verney EB, Starling EH. On secretion by the isolated kidney. J Physiol-London. 1922;56(5):353-8.
Eichholtz F, Starling EH. The action of inorganic salts on the secretion of the isolated kidney. Proc R Soc Lond B Biol Char. 1925;98(687):93-112.
Dutkowski P, de Rougemont O, Clavien PA. Alexis Carrel: Genius, innovator and ideologist. Am J Transplant. 2008;8(10):1998-2003.
Carrel A, Lindbergh CA. The culture of whole organs. Science. 1935;81(2112):621-3.
Humphries AL Jr, Russell R, Gregory J, Carter RH, Moretz WH. Hypothermic perfusion of the canine kidney for 48 hours followed by reimplantation. Am Surg. 1964;30:748-52.
Belzer FO, Ashby BS, Dunphy JE. 24-hour and 72-hour preservation of canine kidneys. Lancet. 1967;2(7515):536-9.
Belzer FO, Ashby BS, Gulyassy PF, Powell M. Successful seventeen-hour preservation and transplantation of human-cadaver kidney. N Engl J Med. 1968;278(11):608-10.
Cooper DKC. Early clinical xenotransplantation experiences-An interview with Thomas E. Starzl, MD, PhD. Xenotransplantation. 2017;24(2):e12306.
Belzer FO, Kalayoglu M, Dalessandro AM, Pirsch JD, Sollinger HW, Hoffmann R, et al. Organ preservation: experience with University of Wisconsin solution and plans for the future. Clin Transplant. 1990;4(2):73-7.
Haque O, Yuan Q, Uygun K, Markmann JF. Evolving utilization of donation after circulatory death livers in liver transplantation: The day of DCD has come. Clin Transplant. 2021;35(3):e14211.
Neuberger J. Liver transplantation in the United Kingdom. Liver Transpl. 2016;22(8):1129-35.
Lee MP, Gear AR. The effect of temperature on mitochondrial membrane-linked reactions. J Biol Chem. 1974;249(23):7541-9.
Karangwa SA, Dutkowski P, Fontes P, Friend PJ, Guarrera JV, Markmann JF, et al. Machine perfusion of donor livers for transplantation: a proposal for standardized nomenclature and reporting guidelines. Am J Transplant. 2016;16(10):2932-42.
op den Dries S, Karimian N, Sutton ME, Westerkamp AC, Nijsten MWN, Gouw ASH, Wiersema-Buist J, et al. Ex vivo normothermic machine perfusion and viability testing of discarded human donor livers. Am J Transplant. 2013;13(5):1327-35.
Liu Q, Nassar A, Buccini L, Grady P, Soliman B, Hassan A, et al. Ex situ 86-hour liver perfusion: Pushing the boundary of organ preservation. Liver Transpl. 2018;24(4):557-61.
Eshmuminov D, Becker D, Bautista Borrego L, Hefti M, Schuler MJ, Hagedorn C, et al. An integrated perfusion machine preserves injured human livers for 1 week. Nat Biotechnol. 2020;38(2):189-98.
Fondevila C, Hessheimer AJ, Ruiz A, Calatayud D, Ferrer J, Charco R, et al. Liver transplant using donors after unexpected cardiac death: Novel preservation protocol and acceptance criteria. Am J Transplant. 2007;7(7):1849-55.
Guarrera JV, Henry SD, Samstein B, Odeh-Ramadan R, Kinkhabwala M, Goldstein MJ, et al. Hypothermic machine preservation in human liver transplantation: the first clinical series. Am J Transplant. 2010;10(2):372-81.
Morito N, Obara H, Matsuno N, Enosawa S, Furukawa H. Oxygen consumption during hypothermic and subnormothermic machine perfusions of porcine liver grafts after cardiac death. J Artif Organs. 2018;21(4):450-7.
Bodewes SB, van Leeuwen OB, Thorne AM, Lascaris B, Ubbink R, Lisman T, et al. Oxygen transport during ex situ machine perfusion of donor livers using red blood cells or artificial oxygen carriers. Int J Mol Sci. 2021;22(1):235.
Dutkowski P, Polak WG, Muiesan P, Schlegel A, Verhoeven CJ, Scalera I, et al. First comparison of Hypothermic Oxygenated PErfusion versus static cold storage of human donation after cardiac death liver transplants an international-matched case analysis. Ann Surg. 2015;262(5):764-71.
Schlegel A, Kron P, De Oliveira ML, Clavien PA, Dutkowski P. Is single portal vein approach sufficient for hypothermic machine perfusion of DCD liver grafts? J Hepatol. 2016;64(1):239-41.
de Vries Y, Brüggenwirth IMA, Karangwa SA, von Meijenfeldt FA, van Leeuwen OB, Burlage LC, et al. Dual versus single oxygenated hypothermic machine perfusion of porcine livers: impact on hepatobiliary and endothelial cell injury. Transplant Direct. 2021;7(9):e741.
Schön MR, Kollmar O, Wolf S, Schrem H, Matthes M, Akkoc N, et al. Liver transplantation after organ preservation with normothermic extracorporeal perfusion. Ann Surg. 2001;233(1):114-23.
Dutkowski R, Graf R, Clavien PA. Rescue of the cold preserved rat liver by hypothermic oxygenated machine perfusion. Am J Transplant. 2006;6(5p1):903-12.
Bessems M, Doorschodt BM, Kolkert JLP, Vetelainen RL, van Vliet AK, Vreeling H, et al. Preservation of steatotic livers: a comparison between cold storage and machine perfusion preservation. Liver Transpl. 2007;13(4):497-504.
Brockmann J, Reddy S, Coussios C, Pigott D, Guirriero D, Hughes D, et al. Normothermic perfusion a new paradigm for organ preservation. Ann Surg. 2009;250(1):1-6.
de Rougemont O, Breitenstein S, Leskosek B, Weber A, Graf R, Clavien PA, et al. One hour hypothermic oxygenated perfusion (HOPE) protects nonviable liver allografts donated after cardiac death. Ann Surg. 2009;250(5):674-83.
Schlegel A, Graf R, Clavien PA, Dutkowski P. Hypothermic oxygenated perfusion (HOPE) protects from biliary injury in a rodent model of DCD liver transplantation. J Hepatol. 2013;59(5):984-91.
Liu Q, Nassar A, Farias K, Buccini L, Baldwin W, Mangino M, et al. Sanguineous normothermic machine perfusion improves hemodynamics and biliary epithelial regeneration in donation after cardiac death porcine livers. Liver Transpl. 2014;20(8):987-99.
Nasralla D, Coussios CC, Mergental H, Akhtar MZ, Butler AJ, Ceresa CDL, et al. A randomized trial of normothermic preservation in liver transplantation. Nature. 2018;557(7703):50-6.
van Rijn R, Schurink IJ, de Vries Y, van den Berg AP, Cortes Cerisuelo M, Darwish Murad S, et al. Hypothermic machine perfusion in liver transplantation-a randomized trial. N Engl J Med. 2021;384(15):1391-401.
Slankamenac K, Graf R, Barkun J, Puhan MA, Clavien PA. The comprehensive complication index: A novel continuous scale to measure surgical morbidity. Ann Surg. 2013;258(1):1-7.
Martins PN, Rizzari MD, Ghinolfi D, Jochmans I, Attia M, Jalan R, et al. Design, analysis, and pitfalls of clinical trials using ex situ liver machine perfusion: The International Liver Transplantation Society consensus guidelines. Transplantation. 2021;105(4):796-815.
Muller X, Marcon F, Sapisochin G, Marquez M, Dondero F, Rayar M, et al. Defining benchmarks in liver transplantation: a multicenter outcome analysis determining best achievable results. Ann Surg. 2018;267(3):419-25.
Granger DN, Kvietys PR. Reperfusion injury and reactive oxygen species: The evolution of a concept. Redox Biol. 2015;6:524-51.
Hirao H, Nakamura K, Kupiec-Weglinski JW. Liver ischaemia-reperfusion injury: A new understanding of the role of innate immunity. Nat Rev Gastroenterol Hepatol. 2022;19(4):239-56.
Vollmar B, Glasz J, Menger MD, Messmer K. Leukocytes contribute to hepatic ischemia-reperfusion injury via intercellular-adhesion molecule-1-mediated venular adherence. Surgery. 1995;117(2):195-200.
Sindram D, Porte RJ, Hoffman MR, Bentley RC, Clavien PA. Platelets induce sinusoidal endothelial cell apoptosis upon reperfusion of the cold ischemic rat liver. Gastroenterology. 2000;118(1):183-91.
Wu MY, Yiang GT, Liao WT, Tsai AY, Cheng YL, Cheng PW, et al. Current mechanistic concepts in ischemia and reperfusion injury. Cell Physiol Biochem. 2018;46(4):1650-67.
Hofmann J, Otarashvili G, Meszaros A, Ebner S, Weissenbacher A, Cardini B, et al. Restoring mitochondrial function while avoiding redox stress: the key to preventing ischemia/reperfusion injury in machine perfused liver grafts? Int J Mol Sci. 2020;21(9):3132.
Chouchani E, Pell V, Gaude E, Aksentijević D, Sundier S, Robb E, et al. Ischaemic accumulation of succinate controls reperfusion injury through mitochondrial ROS. Nature. 2014;515(7527):431-435.
Jiménez-Castro MB, Cornide-Petronio ME, Gracia-Sancho J, Peralta C. Inflammasome-mediated inflammation in liver ischemia-reperfusion injury. Cells. 2019;8(10):1131.
Kamo N, Ke B, Busuttil RW, Kupiec-Weglinski JW. PTEN-mediated akt/β-Catenin/foxo1 signaling regulates innate immune responses in mouse liver ischemia/reperfusion injury. Hepatology. 2013;57(1):289-98.
Li J, Zhao J, Xu M, Li M, Wang B, Qu X, et al. Blocking GSDMD processing in innate immune cells but not in hepatocytes protects hepatic ischemia-reperfusion injury. Cell Death Dis. 2020;11(4):244.
Katsargyris A, Klonaris C, Alexandrou A, Giakoustidis AE, Vasileiou I, Theocharis S. Toll like receptors in liver ischemia reperfusion injury: a novel target for therapeutic modulation? Expert Opin Ther Targets. 2009;13(4):427-42.
Bekki Y, Myers B, Wang R, Smith N, Zerillo J, Rocha C, et al. Postreperfusion syndrome in liver transplantation: Outcomes, predictors, and application for recipient selection. Clin Transplant. 2022;36(4):e14587.
Hilmi I, Horton CN, Planinsic RM, Sakai T, Nicolau-Raducu R, Damian D, et al. The impact of postreperfusion syndrome on short-term patient and liver allograft outcome in patients undergoing orthotopic liver transplantation. Liver Transpl. 2008;14(4):504-8.
Ito T, Naini BV, Markovic D, Aziz A, Younan S, Lu M, et al. Ischemia-reperfusion injury and its relationship with early allograft dysfunction in liver transplant patients. Am J Transplant. 2021;21(2):614-25.
Buis CI, Hoekstra H, Verdonk RC, Porte RJ. Causes and consequences of ischemic-type biliary lesions after liver transplantation. J Hepatobiliary Pancreatic Surg. 2006;13(6):517-24.
Muller X, Schlegel A, Kron P, Eshmuminov D, Würdinger M, Meierhofer D, et al. Novel real-time prediction of liver graft function during hypothermic oxygenated machine perfusion before liver transplantation. Ann Surg. 2019;270(5):783-90.
Mueller M, Hefti M, Eshmuminov D, Schuler MJ, Sousa Da Silva RX, Petrowsky H, et al. Long-term normothermic machine preservation of partial livers: first experience with 21 human hemi-livers. Ann Surg. 2021;274(5):836-42.
Vries Y, Matton APM, Nijsten MWN, Werner MJM, Berg AP, Boer MT, et al. Pretransplant sequential hypo- and normothermic machine perfusion of suboptimal livers donated after circulatory death using a hemoglobin-based oxygen carrier perfusion solution. Am J Transplant. 2019;19(4):1202-11.
Michalopoulos GK. Hepatostat: Liver regeneration and normal liver tissue maintenance. Hepatology. 2017;65(4):1384-92.
Bruggenwirth IMA, Martins PN. RNA interference therapeutics in organ transplantation: The dawn of a new era. Am J Transplant. 2020;20(4):931-41.
Ogrodnik M, Miwa S, Tchkonia T, Tiniakos D, Wilson CL, Lahat A, et al. Cellular senescence drives age-dependent hepatic steatosis. Nat Communications. 2017;8(1):15691.
Nagrath D, Xu H, Tanimura Y, Zuo R, Berthiaume F, Avila M, et al. Metabolic preconditioning of donor organs: Defatting fatty livers by normothermic perfusion ex vivo. Metab Eng. 2009;11(4-5):274-83.
Bioulac-Sage P, Balabaud C, Ferrell L. Lipopeliosis revisited: Should we keep the term? Am J Surg Pathol. 2002;26(1):134-5.
Sampaziotis F, Muraro D, Tysoe OC, Sawiak S, Beach TE, Godfrey EM, et al. Cholangiocyte organoids can repair bile ducts after transplantation in the human liver. Science. 2021;371(6531):839-46.
Verstegen MMA, Willemse J, van den Hoek S, Kremers GJ, Luider TM, van Huizen NA, et al. Decellularization of whole human liver grafts using controlled perfusion for transplantable organ bioscaffolds. Stem Cells Dev. 2017;26(18):1304-15.
McCormack L, Petrowsky H, Jochum W, Furrer K, Clavien P-A. Hepatic Steatosis Is a Risk Factor for Postoperative Complications After Major Hepatectomy. Annals of Surgery. 2007;245(6):923-930.