Subnormothermic machine perfusion for ex vivo preservation and recovery of the human liver for transplantation

American Journal of Transplantation

Volumn 14, Issue 6, 2014, Pages 1400-1409

  Bruinsma, B G ^a,b   Yeh, H ^a   Ozer S ^a   Martins, P N ^c   Farmer, A ^a   Wu, W ^a   Saeidi, N ^a   Op Den Dries, S ^d   Berendsen, T A ^a   Smith, R N ^a   Markmann, J F ^a   Porte, R J ^d   Yarmush, M L ^a,e   Uygun, K ^a   Izamis, M L ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

^c UMASS MEMORIAL MEDICAL CENTER   (United States)

^d UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^e RUTGERS UNIVERSITY   (United States)

Author keywords

Donation after circulatory death; liver transplantation; organ preservation; subnormothermic machine perfusion

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALANINE AMINOTRANSFERASE; ALBUMIN; BICARBONATE; BILE SALT; LACTATE DEHYDROGENASE; OXYGEN; UREA;

ADULT; AGED; ARTERY RESISTANCE; ARTICLE; BILE; BILE FLOW; CELL VIABILITY ASSAY; COLD ISCHEMIA; COMMON BILE DUCT; CRYOPRESERVATION; EX VIVO STUDY; FEMALE; GENERAL MEDICAL DEVICE; HEPATOBILIARY PARAMETERS; HUMAN; HUMAN TISSUE; ISCHEMIA; LIVER BIOPSY; LIVER CELL DAMAGE; LIVER FUNCTION; LIVER FUNCTION TEST; LIVER HISTOLOGY; LIVER PERFUSION; LIVER PRESERVATION; LIVER TRANSPLANTATION; MALE; MIDDLE AGED; ORGAN DONOR; OXYGEN CONSUMPTION; OXYGEN TENSION; PH; PORTAL VEIN; PRESERVATION AND STORAGE; PRIORITY JOURNAL; SUBNORMOTHERMIC MACHINE PERFUSION; SUBNORMOTHERMIC MACHINE PERFUSION SYSTEM; UREA CYCLE; YOUNG ADULT; FEASIBILITY STUDY; HEPATOBILIARY SYSTEM; LIVER; METABOLISM; ORGAN PRESERVATION; PATHOPHYSIOLOGY; PROCEDURES;

ADENOSINE TRIPHOSPHATE; ADULT; AGED; BILIARY TRACT; CRYOPRESERVATION; FEASIBILITY STUDIES; FEMALE; HUMANS; LIVER; LIVER TRANSPLANTATION; MALE; MIDDLE AGED; ORGAN PRESERVATION;

EID: 84901330128     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/ajt.12727     Document Type: Article

References (50)

1. Jain A, Reyes J, Kashyap R, et al. Long-term survival after liver transplantation in 4,000 consecutive patients at a single center. Ann Surg 2000; 232: 490-500.
2. McCormack L, Petrowsky H, Jochum W, Mullhaupt B, Weber M, Clavien PA., Use of severely steatotic grafts in liver transplantation: A matched case-control study. Ann Surg 2007; 246: 940-946, discussion 946-948. (Pubitemid 350179176)
3. Moore DE, Feurer ID, Speroff T, et al. Impact of donor, technical, and recipient risk factors on survival and quality of life after liver transplantation. Arch Surg 2005; 140: 273-277. (Pubitemid 41001820)
4. de Vera ME, Lopez-Solis R, Dvorchik I, et al. Liver transplantation using donation after cardiac death donors: Long-term follow-up from a single center. Am J Transplant 2009; 9: 773-781.
5. de Rougemont O, Breitenstein S, Leskosek B, et al. One hour hypothermic oxygenated perfusion (HOPE) protects nonviable liver allografts donated after cardiac death. Ann Surg 2009; 250: 674-683.
6. Bessems M, Doorschodt BM, van Marle J, Vreeling H, Meijer AJ, van Gulik TM., Improved machine perfusion preservation of the non-heart-beating donor rat liver using polysol: A new machine perfusion preservation solution. Liver Transpl 2005; 11: 1379-1388. (Pubitemid 43071587)
7. Monbaliu M, Liu L, Libbrecht L, et al. Preserving morphology and evaluating quality of liver grafts by hypothermic machine perfusion, a proof of concept study using discarded human livers. Liver Transpl 2012; 18: 1495-1507.
8. 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: 984-991.
9. Guarrera JV, Henry SD, Samstein B, et al. Hypothermic machine preservation in human liver transplantation: The first clinical series. Am J Transplant 2010; 10: 372-381.
10. Dutkowski P, Schlegel A, de Oliveira M, Müllhaupt B, Clavien PA., HOPE for human liver grafts obtained from donors after cardiac death. J Hepatol 2014; 60: 765-772.
11. Xu H, Berendsen T, Kim K, et al. Excorporeal normothermic machine perfusion resuscitates pig DCD livers with extended warm ischemia. J Surg Res 2011; 43: 1484-1488.
12. Perk S, Izamis ML, Tolboom H, et al. A metabolic index of ischemic injury for perfusion-recovery of cadaveric rat livers. PLoS ONE 2011; 6: e28518.
13. Perk S, Izamis ML, Tolboom H, Uygun B, Yarmush ML, Uygun K., A fitness index for transplantation of machine-perfused cadaveric rat livers. BMC Res Notes 2012; 5: 325.
14. Op den Dries S, Karimian N, Sutton ME, et al. Ex vivo normothermic machine perfusion and viability testing of discarded human donor livers. Am J Transplant 2013; 13: 1327-1335.
15. Minor T, Efferz P, Fox M, Wohlschlaeger J, Lüer B., Controlled oxygenated rewarming of cold stored liver grafts by thermally graduated machine perfusion prior to reperfusion. Am J Transplant 2013; 13: 1450-1460.
16. Shigeta T, Matsuno N, Obara H, et al. Impact of rewarming preservation by continuous machine perfusion: Improved post-transplant recovery in pigs. Transplant Proc 2013; 45: 1684-1689.
17. Vajdová K, Graf R, Clavien PA., ATP-supplies in the cold-preserved liver: A long-neglected factor of organ viability. Hepatology 2002; 36: 1543-1552. (Pubitemid 35403546)
18. Berendsen TA, Bruinsma BG, Lee J, et al. A simplified subnormothermic machine perfusion system restores ischemically damaged liver grafts in a rat model of orthotopic liver transplantation. Transplant Res 2012; 1: 6.
19. Tolboom H, Pouw R, Uygun K, et al. A model for normothermic preservation of the rat liver. Tissue Eng 2007; 13: 2143-2151. (Pubitemid 47294009)
20. Lüer B, Koetting M, Efferz P, Minor T., Role of oxygen during hypothermic machine perfusion preservation of the liver. Transpl Int 2010; 23: 944-950.
21. Mitchell SJ, Churchill TA, Winslet MC, Fuller BJ., Energy metabolism following prolonged hepatic cold preservation: Benefits of interrupted hypoxia on the adenine nucleotide pool in rat liver. Cryobiology 1999; 39: 130-137. (Pubitemid 29526368)
22. Zhao K, Zhao GM, Wu D, et al. Cell-permeable peptide antioxidants targeted to inner mitochondrial membrane inhibit mitochondrial swelling, oxidative cell death, and reperfusion injury. J Biol Chem 2004; 279: 34682-34690. (Pubitemid 39318098)
23. McCord JM., Oxygen-derived free radicals in postischemic tissue injury. N Engl J Med 1985; 312: 159-163. (Pubitemid 15192863)
24. Reddy SP, Bhattacharjya S, Maniakin N, et al. Preservation of porcine non-heart-beating donor livers by sequential cold storage and warm perfusion. Transplantation 2004; 77: 1328-1332. (Pubitemid 38668423)
25. Ferrigno A, Rizzo V, Boncompagni E, et al. Machine perfusion at 20°C reduces preservation damage to livers from non-heart beating donors. Cryobiology 2011; 62: 152-158.
26. Lanir A, Jenkins RL, Caldwell C, Lee RG, Khettry U, Clouse ME., Hepatic transplantation survival: Correlation with adenine nucleotide level in donor liver. Hepatology 1988; 8: 471-475.
27. Kamiike W, Burdelski M, Steinhoff G, Ringe B, Lauchart W, Pichlmayr R., Adenine nucleotide metabolism and its relation to organ viability in human liver transplantation. Transplantation 1988; 45: 138-143. (Pubitemid 18084626)
28. Usta OB, He X, Kim Y, et al. Supercooling as a viable non-freezing cell preservation method of rat hepatocytes. PLoS ONE 2013; 8: e69334.
29. Berendsen TA, Izamis ML, Xu H, et al. Hepatocyte viability and adenosine triphosphate content decrease linearly over time during conventional cold storage of rat liver grafts. Transplant Proc 2011; 43: 1484-1488.
30. Bruinsma BG, Berendsen TA, Izamis ML, Yarmush ML, Uygun K., Determination and extension of the limits to static cold storage using subnormothermic machine perfusion. Int J Artif Organs 2013; 36: 775-780.
31. Minor T, Tolba R, Neumann S, Schulz S, Sitzia M., Fibrinolysis in organ procurement for transplantation after cardiocirculatory compromise. Thromb Haemost 2003; 90: 361-362. (Pubitemid 36992513)
32. Koetting M, Minor T., Donation after cardiac death: Dynamic graft reconditioning during or after ischemic preservation ? Artif Organs 2011; 35: 565-571.
33. St Peter SD, Imber CJ, Lopez I, Hughes D, Friend PJ., Extended preservation of non-heart-beating donor livers with normothermic machine perfusion. Br J Surg 2002; 89: 609-616. (Pubitemid 34415612)
34. Butler AJ, Rees MA, Wight DGD, et al. Successful extracorporeal porcine liver perfusion for 72 hr. Transplantation 2002; 73: 1212-1218. (Pubitemid 34454265)
35. Bessems M, Doorschodt BM, Dinant S, de Graaf W, van Gulik TM., Machine perfusion preservation of the pig liver using a new preservation solution, polysol. Transplant Proc 2006; 38: 1238-1242.
36. Reddy S, Greenwood J, Maniakin N, et al. Non-heart-beating donor porcine livers: The adverse effect of cooling. Liver Transpl 2005; 11: 35-38. (Pubitemid 40124440)
37. van der Plaats A, Maathuis MH, 'T Hart NA, et al. The Groningen hypothermic liver perfusion pump: Functional evaluation of a new machine perfusion system. Ann Biomed Eng 2006; 34: 1924-1934. (Pubitemid 44770845)
38. Miyagi S, Iwane T, Akamatsu Y, Nakamura A, Sato A, Satomi S., The significance of preserving the energy status and microcirculation in liver grafts from non-heart-beating donor. Cell Transplant 2008; 17: 173-178. (Pubitemid 351551393)
39. Friend PJ, Imber C, St Peter S, Lopez I, Butler AJ, Rees MA., Normothermic perfusion of the isolated liver. Transplant Proc 2001; 33: 3436-3438. (Pubitemid 34042639)
40. Vajdová K, Smreková R, Mislanová C, Kukan M, Lutterová M., Cold-preservation-induced sensitivity of rat hepatocyte function to rewarming injury and its prevention by short-term reperfusion. Hepatology 2000; 32: 289-296. (Pubitemid 30614661)
41. Wojcicki M, Milkiewicz P, Silva M., Biliary tract complications after liver transplantation: A review. Dig Surg 2008; 25: 245-257.
42. Geuken E, Visser D, Kuipers F, et al. Rapid increase of bile salt secretion is associated with bile duct injury after human liver transplantation. J Hepatol 2004; 41: 1017-1025. (Pubitemid 39575670)
43. Buis CI, Geuken E, Visser DS, et al. Altered bile composition after liver transplantation is associated with the development of nonanastomotic biliary strictures. J Hepatol 2009; 50: 69-79.
44. Hertl M, Harvey PR, Swanson PE, et al. Evidence of preservation injury to bile ducts by bile salts in the pig and its prevention by infusions of hydrophilic bile salts. Hepatology 1995; 21: 1130-1137.
45. Imber CJ, St Peter SD, de Cenarruzabeitia IL, et al. Optimisation of bile production during normothermic preservation of porcine livers. Am J Transplant 2002; 2: 593-599. (Pubitemid 36306850)
46. 2+. Liver Transpl 2008; 14: 494-503. (Pubitemid 351524405)
47. +/- mice. Hepatology 2006; 43: 1022-1031. (Pubitemid 43724627)
48. 3- umbrella constitutes a protective mechanism against bile acid-induced injury in human cholangiocytes. Hepatology 2012; 55: 173-183.
49. Brockmann J, Reddy S, Coussios C, et al. Normothermic perfusion: A new paradigm for organ preservation. Ann Surg 2009; 250: 1-6.
50. Tolboom H, Izamis ML, Sharma N, et al. Subnormothermic machine perfusion at both 20°C and 30°C recovers ischemic rat livers for successful transplantation. J Surg Res 2011; 175: 149-156.