Preconditioning, organ preservation, and postconditioning to prevent ischemia-reperfusion injury to the liver

Liver Transplantation

Volumn 15, Issue 10, 2009, Pages 1172-1182

  De Rougemont, Olivier ^a   Lehmann, Kuno ^a   Clavien, Pierre Alain ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; ADENOSINE; ADENOVIRUS VECTOR; ALANINE AMINOTRANSFERASE; ALLOPURINOL; ASPARTATE AMINOTRANSFERASE; GABEXATE MESILATE; GELATINASE B; GLUTATHIONE; HEME OXYGENASE; HETASTARCH; HTK SOLUTION; LACTOBIONIC ACID; MACROGOL; MAGNESIUM SULFATE; METHYLPREDNISOLONE; NITRIC OXIDE; POTASSIUM DIHYDROGEN PHOSPHATE; PROPOFOL; PROTOPORPHYRIN COBALT; PROTOPORPHYRIN ZINC; RAFFINOSE; RECOMBINANT ERYTHROPOIETIN; SEVOFLURANE; SIMVASTATIN; SMALL INTERFERING RNA; THIOCTIC ACID; TRANSCRIPTION FACTOR NRF2; VIRUS VECTOR;

ANTIOXIDANT ACTIVITY; CLINICAL TRIAL; DISEASE MODEL; FATTY LIVER; HEPATITIS; HUMAN; ISCHEMIC PRECONDITIONING; LIVER GRAFT; LIVER GRAFT REJECTION; LIVER ISCHEMIA; LIVER PERFUSION; LIVER RESECTION; LIVER TRANSPLANTATION; NONHUMAN; ORGAN DONOR; ORGAN PRESERVATION; PATIENT CARE; PORTAL VEIN BLOOD FLOW; PRIORITY JOURNAL; REPERFUSION; REPERFUSION INJURY; REVIEW; RNA INTERFERENCE; SURGEON; VEIN OCCLUSION;

EID: 70350539112     PISSN: 15276465     EISSN: 15276473     Source Type: Journal    
DOI: 10.1002/lt.21876     Document Type: Review

References (128)

1. Clavien PA, Harvey PR, Strasberg SM. Preservation and reperfusion injuries in liver allografts. An overview and synthesis of current studies. Transplantation 1992;53:957-978.
2. Ploeg RJ, D'Alessandro AM, Knechtle SJ, Stegall MD, Pirsch JD, Hoffmann RM, et al. Risk factors for primary dysfunction after liver transplantation - a multivariate analysis. Transplantation 1993;55:807-813. (Pubitemid 23122053)
3. Varotti G, Grazi GL, Vetrone G, Ercolani G, Cescon M, Del Gaudio M, et al. Causes of early acute graft failure after liver transplantation: analysis of a 17-year single-centre experience. Clin Transplant 2005;19:492-500. (Pubitemid 40990659)
4. McKeown CM, Edwards V, Phillips MJ, Harvey PR, Petrunka CN, Strasberg SM. Sinusoidal lining cell damage: the critical injury in cold preservation of liver allografts in the rat. Transplantation 1988;46:178-191. (Pubitemid 18204028)
5. Otto G, Wolff H, David H. Preservation damage in liver transplantation: electron-microscopic findings. Transplant Proc 1984;16:1247-1248. (Pubitemid 14023569)
6. Momii S, Koga A. Time-related morphological changes in cold-stored rat livers. A comparison of Euro-Collins solution with UW solution. Transplantation 1990;50:745-750.
7. Upadhya GA, Strasberg SM. Evidence that actin disassembly is a requirement for matrix metalloproteinase secretion by sinusoidal endothelial cells during cold preservation in the rat. Hepatology 1999;30:169-176.
8. Upadhya AG, Harvey RP, Howard TK, Lowell JA, Shenoy S, Strasberg SM. Evidence of a role for matrix metalloproteinases in cold preservation injury of the liver in humans and in the rat. Hepatology 1997;26:922-928. (Pubitemid 27413658)
9. Gao W, Bentley RC, Madden JF, Clavien PA. Apoptosis of sinusoidal endothelial cells is a critical mechanism of preservation injury in rat liver transplantation. Hepatology 1998;27:1652-1660. (Pubitemid 28264691)
10. Natori S, Selzner M, Valentino KL, Fritz LC, Srinivasan A, Clavien PA, et al. Apoptosis of sinusoidal endothelial cells occurs during liver preservation injury by a caspase-dependent mechanism. Transplantation 1999;68:89-96. (Pubitemid 29352837)
11. Sindram D, Kohli V, Madden JF, Clavien PA. Calpain inhibition prevents sinusoidal endothelial cell apoptosis in the cold ischemic rat liver. Transplantation 1999;68:136-140. (Pubitemid 29352844)
12. Caldwell-Kenkel JC, Thurman RG, Lemasters JJ. Selective loss of nonparenchymal cell viability after cold ischemic storage of rat livers. Transplantation 1988;45:834-837.
13. Holloway CM, Harvey PR, Strasberg SM. Viability of sinusoidal lining cells in cold-preserved rat liver allografts. Transplantation 1990;49:225-229. (Pubitemid 20051625)
14. Stolz DB, Ross MA, Ikeda A, Tomiyama K, Kaizu T, Geller DA, et al. Sinusoidal endothelial cell repopulation following ischemia/reperfusion injury in rat liver transplantation. Hepatology 2007;46:1464-1475. (Pubitemid 350155528)
15. Gujral JS, Bucci TJ, Farhood A, Jaeschke H. Mechanism of cell death during warm hepatic ischemia-reperfusion in rats: apoptosis or necrosis? Hepatology 2001;33:397-405.
16. Kohli V, Selzner M, Madden JF, Bentley RC, Clavien PA. Endothelial cell and hepatocyte deaths occur by apoptosis after ischemia-reperfusion injury in the rat liver. Transplantation 1999;67:1099-1105. (Pubitemid 29205570)
17. Ikeda T, Yanaga K, Kishikawa K, Kakizoe S, Shimada M, Sugimachi K. Ischemic injury in liver transplantation: difference in injury sites between warm and cold ischemia in rats. Hepatology 1992;16:454-461.
18. Vollmar B, Glasz J, Leiderer R, Post S, Menger MD. Hepatic microcirculatory perfusion failure is a determinant of liver dysfunction in warm ischemia-reperfusion. Am J Pathol 1994;145:1421-1431. (Pubitemid 24378496)
19. Gores GJ, Herman B, Lemasters JJ. Plasma membrane bleb formation and rupture: a common feature of hepatocellular injury. Hepatology 1990;11:690-698. (Pubitemid 20151750)
20. Palmes D, Budny TB, Stratmann U, Herbst H, Spiegel HU. Endothelin-A receptor antagonist reduces microcirculatory disturbances and transplant dysfunction after partial liver transplantation. Liver Transpl 2003;9:929-939. (Pubitemid 37098841)
21. Clavien PA, Harvey PR, Sanabria JR, Cywes R, Levy GA, Strasberg SM. Lymphocyte adherence in the reperfused rat liver: mechanisms and effects. Hepatology 1993;17:131-142. (Pubitemid 23027396)
22. Cywes R, Packham MA, Tietze L, Sanabria JR, Harvey PR, Phillips MJ, et al. Role of platelets in hepatic allograft preservation injury in the rat. Hepatology 1993;18:635-647. (Pubitemid 23259965)
23. Vollmar B, Glasz J, Post S, Menger MD. Role of microcirculatory derangements in manifestation of portal triad cross-clamping-induced hepatic reperfusion injury. J Surg Res 1996;60:49-54. (Pubitemid 26044296)
24. Clavien PA, Camargo CA Jr, Gorczynski R, Washington MK, Levy GA, Langer B, et al. Acute reactant cytokines and neutrophil adhesion after warm ischemia in cirrhotic and noncirrhotic human livers. Hepatology 1996;23:1456-1463. (Pubitemid 26181229)
25. Sindram D, Porte RJ, Hoffman MR, Bentley RC, Clavien PA. Synergism between platelets and leukocytes in inducing endothelial cell apoptosis in the cold ischemic rat liver: a Kupffer cell-mediated injury. FASEB J 2001;15:1230-1232.
26. Caldwell-Kenkel JC, Currin RT, Tanaka Y, Thurman RG, Lemasters JJ. Kupffer cell activation and endothelial cell damage after storage of rat livers: effects of reperfusion. Hepatology 1991;13:83-95.
27. Tsung A, Hoffman RA, Izuishi K, Critchlow ND, Nakao A, Chan MH, et al. Hepatic ischemia/reperfusion injury involves functional TLR4 signaling in nonparenchymal cells. J Immunol 2005;175:7661-7668. (Pubitemid 41713466)
28. Jaeschke H, Farhood A, Bautista AP, Spolarics Z, Spitzer JJ. Complement activates Kupffer cells and neutrophils during reperfusion after hepatic ischemia. Am J Physiol 1993;264(pt 1):G801-G809. (Pubitemid 23124784)
29. Heijnen BH, Straatsburg IH, Padilla ND, Van Mierlo GJ, Hack CE, Van Gulik TM. Inhibition of classical complement activation attenuates liver ischaemia and reperfusion injury in a rat model. Clin Exp Immunol 2006;143:15-23.
30. Jaeschke H, Farhood A. Neutrophil and Kupffer cell-induced oxidant stress and ischemia-reperfusion injury in rat liver. Am J Physiol 1991;260(pt 1):G355-G362.
31. Jaeschke H. Kupffer cell-induced oxidant stress during hepatic ischemia-reperfusion: does the controversy continue? Hepatology 1999;30:1527-1528.
32. Colletti LM, Remick DG, Burtch GD, Kunkel SL, Strieter RM, Campbell DA Jr. Role of tumor necrosis factor-alpha in the pathophysiologic alterations after hepatic ischemia/reperfusion injury in the rat. J Clin Invest 1990;85:1936-1943.
33. Decker K. Biologically active products of stimulated liver macrophages (Kupffer cells). FEBS 1990;192:245-261. (Pubitemid 20283490)
34. Bajt ML, Farhood A, Jaeschke H. Effects of CXC chemokines on neutrophil activation and sequestration in hepatic vasculature. Am J Physiol Gastrointest Liver Physiol 2001;281:G1188-G1195. (Pubitemid 33121709)
35. Zwacka RM, Zhang Y, Halldorson J, Schlossberg H, Dudus L, Engelhardt JF. CD4(+) T-lymphocytes mediate ischemia/reperfusion-induced inflammatory responses in mouse liver. J Clin Invest 1997;100:279-289. (Pubitemid 27349074)
36. Le Moine O, Louis H, Demols A, Desalle F, Demoor F, Quertinmont E, et al. Cold liver ischemia-reperfusion injury critically depends on liver T cells and is improved by donor pretreatment with interleukin 10 in mice. Hepatology 2000;31:1266-1274. (Pubitemid 30351288)
37. Green DR. Apoptotic pathways: ten minutes to dead. Cell 2005;121:671-674.
38. Yersiz H, Shaked A, Olthoff K, Imagawa D, Shackleton C, Martin P, et al. Correlation between donor age and the pattern of liver graft recovery after transplantation. Transplantation 1995;60:790-794.
39. Zaman MB, Leonard MO, Ryan EJ, Nolan NP, Hoti E, Maguire D, et al. Lower expression of Nrf2 mRNA in older donor livers: a possible contributor to increased ischemia- reperfusion injury? Transplantation 2007;84:1272-1278.
40. Ravaioli M, Grazi GL, Cescon M, Cucchetti A, Ercolani G, Fiorentino M, et al. Liver transplantations with donors aged 60 years and above: the low liver damage strategy. Transpl Int 2008;22:423-433.
41. Cescon M, Grazi GL, Cucchetti A, Ravaioli M, Ercolani G, Vivarelli M, et al. Improving the outcome of liver transplantation with very old donors with updated selection and management criteria. Liver Transpl 2008;14:672-679. (Pubitemid 351696280)
42. Anderson CD, Vachharajani N, Doyle M, Lowell JA, Wellen JR, Shenoy S, et al. Advanced donor age alone does not affect patient or graft survival after liver transplantation. J Am Coll Surg 2008;207:847-852.
43. Mutimer DJ, Gunson B, Chen J, Berenguer J, Neuhaus P, Castaing D, et al. Impact of donor age and year of transplantation on graft and patient survival following liver transplantation for hepatitis C virus. Transplantation 2006;81:7-14. (Pubitemid 43122140)
44. Berenguer M, Prieto M, San Juan F, Rayon JM, Martinez F, Carrasco D, et al. Contribution of donor age to the recent decrease in patient survival among HCV-infected liver transplant recipients. Hepatology 2002;36:202-210. (Pubitemid 34700779)
45. Selzner M, Clavien PA. Fatty liver in liver transplantation and surgery. Semin Liver Dis 2001;21:105-113.
46. Burke A, Lucey MR. Non-alcoholic fatty liver disease, non-alcoholic steatohepatitis and orthotopic liver transplantation. Am J Transplant 2004;4:686-693. (Pubitemid 38637564)
47. Verran D, Kusyk T, Painter D, Fisher J, Koorey D, Strasser S, et al. Clinical experience gained from the use of 120 steatotic donor livers for orthotopic liver transplantation. Liver Transpl 2003;9:500-505. (Pubitemid 36621720)
48. Noujaim HM, de Ville de Goyet J, Montero EF, Ribeiro CM, Capellozzi VL, Crescentini F, et al. Expanding postmortem donor pool using steatotic liver grafts: a new look. Transplantation 2009;87:919-925.
49. 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 6-8. (Pubitemid 350179176)
50. Briceno J, Ciria R, Pleguezuelo M, de la Mata M, Muntane J, Naranjo A, et al. Impact of donor graft steatosis on overall outcome and viral recurrence after liver transplantation for hepatitis C virus cirrhosis. Liver Transpl 2009;15:37-48.
51. McCormack L, Petrowsky H, Jochum W, Furrer K, Clavien PA. Hepatic steatosis is a risk factor for postoperative complications after major hepatectomy: a matched case-control study. Ann Surg 2007;245:923-930. (Pubitemid 46809294)
52. Clavien PA, Selzner M, Rudiger HA, Graf R, Kadry Z, Rousson V, et al. A prospective randomized study in 100 consecutive patients undergoing major liver resection with versus without ischemic preconditioning. Ann Surg 2003;238:843-850; discussion 51-52 (Pubitemid 38174467)
53. Beck-Schimmer B, Breitenstein S, Urech S, De Conno E, Wittlinger M, Puhan M, et al. A randomized controlled trial on pharmacological preconditioning in liver surgery using a volatile anesthetic. Ann Surg 2008;248:909-918.
54. Saidi RF, Chang J, Verb S, Brooks S, Nalbantoglu I, Adsay V, et al. The effect of methylprednisolone on warm ischemia-reperfusion injury in the liver. Am J Surg 2007;193:345-347; discussion 7-8. (Pubitemid 46274582)
55. DeOliveira ML, Graf R, Clavien PA. Ischemic preconditioning: promises from the laboratory to patients - sustained or disillusioned? Am J Transplant 2008;8:489-491.
56. Azoulay D, Del Gaudio M, Andreani P, Ichai P, Sebag M, Adam R, et al. Effects of 10 minutes of ischemic preconditioning of the cadaveric liver on the graft's preservation and function: the ying and the yang. Ann Surg 2005;242:133-139. (Pubitemid 40917977)
57. Cescon M, Grazi GL, Grassi A, Ravaioli M, Vetrone G, Ercolani G, et al. Effect of ischemic preconditioning in whole liver transplantation from deceased donors. A pilot study. Liver Transpl 2006;12:628-635.
58. Jassem W, Fuggle SV, Cerundolo L, Heaton ND, Rela M. Ischemic preconditioning of cadaver donor livers protects allografts following transplantation. Transplantation 2006;81:169-174.
59. Amador A, Grande L, Marti J, Deulofeu R, Miquel R, Sola A, et al. Ischemic pre-conditioning in deceased donor liver transplantation: a prospective randomized clinical trial. Am J Transplant 2007;7:2180-2189. (Pubitemid 47247061)
60. Koneru B, Fisher A, He Y, Klein KM, Skurnick J, Wilson DJ, et al. Ischemic preconditioning in deceased donor liver transplantation: a prospective randomized clinical trial of safety and efficacy. Liver Transpl 2005;11:196-202. (Pubitemid 40268217)
61. Koneru B, Shareef A, Dikdan G, Desai K, Klein KM, Peng B, et al. The ischemic preconditioning paradox in deceased donor liver transplantation- evidence from a prospective randomized single blind clinical trial. Am J Transplant 2007;7:2788-2796. (Pubitemid 350045783)
62. Kim YI, Hwang YJ, Song KE, Yun YK, Lee JW, Chun BY. Hepatocyte protection by a protease inhibitor against ischemia/reperfusion injury of human liver. J Am Coll Surg 2002;195:41-50.
63. Aldrighetti L, Pulitano C, Arru M, Finazzi R, Catena M, Soldini L, et al. Impact of preoperative steroids administration on ischemia-reperfusion injury and systemic responses in liver surgery: a prospective randomized study. Liver Transpl 2006;12:941-949. (Pubitemid 43960370)
64. Dunschede F, Erbes K, Kircher A, Westermann S, Seifert J, Schad A, et al. Reduction of ischemia reperfusion injury after liver resection and hepatic inflow occlusion by alpha-lipoic acid in humans. World J Gastroenterol 2006;12:6812-6817. (Pubitemid 44811403)
65. Kotsch K, Ulrich F, Reutzel-Selke A, Pascher A, Faber W, Warnick P, et al. Methylprednisolone therapy in deceased donors reduces inflammation in the donor liver and improves outcome after liver transplantation: a prospective randomized controlled trial. Ann Surg 2008;248:1042-1050.
66. Bogetti D, Sankary HN, Jarzembowski TM, Manzelli A, Knight PS, Thielke J, et al. Thymoglobulin induction protects liver allografts from ischemia/reperfusion injury. Clin Transplant 2005;19:507-511. (Pubitemid 40990661)
67. Selzner N, Selzner M, Jochum W, Amann-Vesti B, Graf R, Clavien PA. Mouse livers with macrosteatosis are more susceptible to normothermic ischemic injury than those with microsteatosis. J Hepatol 2006;44:694-701.
68. Selzner M, Rudiger HA, Sindram D, Madden J, Clavien PA. Mechanisms of ischemic injury are different in the steatotic and normal rat liver. Hepatology 2000;32:1280-1288.
69. Teramoto K, Bowers JL, Kruskal JB, Clouse ME. Hepatic microcirculatory changes after reperfusion in fatty and normal liver transplantation in the rat. Transplantation 1993;56:1076-1082. (Pubitemid 23348677)
70. Seifalian AM, Chidambaram V, Rolles K, Davidson BR. In vivo demonstration of impaired microcirculation in steatotic human liver grafts. Liver Transpl Surg 1998;4:71-77.
71. El-Badry AM, Moritz W, Contaldo C, Tian Y, Graf R, Clavien PA. Prevention of reperfusion injury and microcirculatory failure in macrosteatotic mouse liver by omega-3 fatty acids. Hepatology 2007;45:855-863. (Pubitemid 46631553)
72. Rudiger HA, Clavien PA. Tumor necrosis factor alpha, but not Fas, mediates hepatocellular apoptosis in the murine ischemic liver. Gastroenterology 2002;122:202-210.
73. Moore C, Shen XD, Gao F, Busuttil RW, Coito AJ. Fibronectin- alpha4beta1 integrin interactions regulate metalloproteinase-9 expression in steatotic liver ischemia and reperfusion injury. Am J Pathol 2007;170:567-577. (Pubitemid 47339394)
74. Defamie V, Laurens M, Patrono D, Devel L, Brault A, Saint-Paul MC, et al. Matrix metalloproteinase inhibition protects rat livers from prolonged cold ischemia-warm reperfusion injury. Hepatology 2008;47:177-185. (Pubitemid 351171055)
75. Cursio R, Mari B, Louis K, Rostagno P, Saint-Paul MC, Giudicelli J, et al. Rat liver injury after normothermic ischemia is prevented by a phosphinic matrix metalloproteinase inhibitor. FASEB J 2002;16:93-95.
76. Hamada T, Fondevila C, Busuttil RW, Coito AJ. Metalloproteinase- 9 deficiency protects against hepatic ischemia/reperfusion injury. Hepatology 2008;47:186-198. (Pubitemid 351171056)
77. Maines MD. The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol 1997;37:517-554.
78. Katori M, Busuttil RW, Kupiec-Weglinski JW. Heme oxygenase- 1 system in organ transplantation. Transplantation 2002;74:905-912. (Pubitemid 35191234)
79. Geuken E, Buis CI, Visser DS, Blokzijl H, Moshage H, Nemes B, et al. Expression of heme oxygenase-1 in human livers before transplantation correlates with graft injury and function after transplantation. Am J Transplant 2005;5:1875-1885. (Pubitemid 41039860)
80. Patel A, van de Poll MC, Greve JW, Buurman WA, Fearon KC, McNally SJ, et al. Early stress protein gene expression in a human model of ischemic preconditioning. Transplantation 2004;78:1479-1487. (Pubitemid 39552934)
81. Pachori AS, Melo LG, Hart ML, Noiseux N, Zhang L, Morello F, et al. Hypoxia-regulated therapeutic gene as a preemptive treatment strategy against ischemia/reperfusion tissue injury. Proc Natl Acad Sci U S A 2004;101:12282-12287. (Pubitemid 39145435)
82. Kato H, Amersi F, Buelow R, Melinek J, Coito AJ, Ke B, et al. Heme oxygenase-1 overexpression protects rat livers from ischemia/reperfusion injury with extended cold preservation. Am J Transplant 2001;1:121-128. (Pubitemid 33674151)
83. Lai IR, Chang KJ, Tsai HW, Chen CF. Pharmacological preconditioning with simvastatin protects liver from ischemia- reperfusion injury by heme oxygenase-1 induction. Transplantation 2008;85:732-738.
84. Schmidt R, Tritschler E, Hoetzel A, Loop T, Humar M, Halverscheid L, et al. Heme oxygenase-1 induction by the clinically used anesthetic isoflurane protects rat livers from ischemia/reperfusion injury. Ann Surg 2007;245:931-942. (Pubitemid 46809295)
85. Sepodes B, Maio R, Pinto R, Sharples E, Oliveira P, McDonald M, et al. Recombinant human erythropoietin protects the liver from hepatic ischemia-reperfusion injury in the rat. Transpl Int 2006;19:919-926. (Pubitemid 44511117)
86. Schmeding M, Neumann UP, Boas-Knoop S, Spinelli A, Neuhaus P. Erythropoietin reduces ischemia-reperfusion injury in the rat liver. Eur Surg Res 2007;39:189-197. (Pubitemid 46633182)
87. Zender L, Hutker S, Liedtke C, Tillmann HL, Zender S, Mundt B, et al. Caspase 8 small interfering RNA prevents acute liver failure in mice. Proc Natl Acad Sci U S A 2003;100:7797-7802.
88. Ke B, Shen XD, Gao F, Qiao B, Ji H, Busuttil RW, et al. Small interfering RNA targeting heme oxygenase-1 reinforces liver apoptosis induced by ischemia/reperfusion injury in mice: Ho-1 is necessary for cytoprotection. Hum Gene Ther 2009. doi://10.1089/hum.2009.049. Available at: http://www. liebertonline.com.
89. Grimm D, Streetz KL, Jopling CL, Storm TA, Pandey K, Davis CR, et al. Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature 2006;441:537-541. (Pubitemid 44050158)
90. Belzer FO, Southard JH. Principles of solid-organ preservation by cold storage. Transplantation 1988;45:673-676. (Pubitemid 18121175)
91. Meine MH, Zanotelli ML, Neumann J, Kiss G, de Jesus Grezzana T, Leipnitz I, et al. Randomized clinical assay for hepatic grafts preservation with University of Wisconsin or histidine-tryptophan-ketoglutarate solutions in liver transplantation. Transplant Proc 2006;38:1872-1875. (Pubitemid 44209349)
92. Cavallari A, Cillo U, Nardo B, Filipponi F, Gringeri E, Montalti R, et al. A multicenter pilot prospective study comparing Celsior and University of Wisconsin preserving solutions for use in liver transplantation. Liver Transpl 2003;9:814-821. (Pubitemid 36974947)
93. Garcia-Gil FA, Arenas J, Guemes A, Esteban E, Tome- Zelaya E, Lamata F, et al. Preservation of the liver graft with Celsior solution. Transplant Proc 2006;38:2385-2388. (Pubitemid 44693690)
94. Franco-Gou R, Mosbah IB, Serafin A, Abdennebi HB, Rosello-Catafau J, Peralta C. New preservation strategies for preventing liver grafts against cold ischemia reperfusion injury. J Gastroenterol Hepatol 2007;22:1120-1126. (Pubitemid 47019843)
95. Hoglen NC, Chen LS, Fisher CD, Hirakawa BP, Groessl T, Contreras PC. Characterization of IDN-6556 (3-[2-(2- tert-butyl-phenylaminooxalyl)-amino]- propionylamino]-4-oxo-5-(2,3,5,6-tetrafluoro-phenoxy)-pentanoic acid): a liver-targeted caspase inhibitor. J Pharmacol Exp Ther 2004;309:634-640.
96. Linton SD, Aja T, Armstrong RA, Bai X, Chen LS, Chen N, et al. First-in-class pan caspase inhibitor developed for the treatment of liver disease. J Med Chem 2005;48:6779-6782. (Pubitemid 41533098)
97. Natori S, Higuchi H, Contreras P, Gores GJ. The caspase inhibitor IDN-6556 prevents caspase activation and apoptosis in sinusoidal endothelial cells during liver preservation injury. Liver Transpl 2003;9:278-284. (Pubitemid 36322330)
98. Valentino KL, Gutierrez M, Sanchez R, Winship MJ, Shapiro DA. First clinical trial of a novel caspase inhibitor: anti-apoptotic caspase inhibitor, IDN-6556, improves liver enzymes. Int J Clin Pharmacol Ther 2003;41:441-449. (Pubitemid 37258860)
99. 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;118:183-191. (Pubitemid 30020386)
100. Baskin-Bey ES, Washburn K, Feng S, Oltersdorf T, Shapiro D, Huyghe M, et al. Clinical trial of the pan-caspase inhibitor, IDN-6556, in human liver preservation injury. Am J Transplant 2007;7:218-225. (Pubitemid 44952876)
101. Ben Mosbah I, Massip-Salcedo M, Fernandez-Monteiro I, Xaus C, Bartrons R, Boillot O, et al. Addition of adenosine monophosphate-activated protein kinase activators to University of Wisconsin solution: a way of protecting rat steatotic livers. Liver Transpl 2007;13:410-425. (Pubitemid 46444471)
102. Qing DK, Dong JH, Han BL, Chen XR. Cold preservation of pig liver grafts with warm ischemia and pentoxifylline- UW solution. Arch Med Res 2006;37:449-455.
103. Tian Y, Jochum W, Georgiev P, Moritz W, Graf R, Clavien PA. Kupffer cell-dependent TNF-alpha signaling mediates injury in the arterialized small-for-size liver transplantation in the mouse. Proc Natl Acad Sci U S A 2006;103:4598-4603.
104. Dutkowski P, de Rougemont O, Clavien PA. Machine perfusion for 'marginal' liver grafts. Am J Transplant 2008;8:917-924.
105. Schon 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;233:114-123. (Pubitemid 32042781)
106. Lee CY, Jain S, Duncan HM, Zhang JX, Jones JW Jr, Southard JH, et al. Survival transplantation of preserved non-heart-beating donor rat livers: preservation by hypothermic machine perfusion. Transplantation 2003;76:1432-1436. (Pubitemid 37467689)
107. Dutkowski P, Furrer K, Tian Y, Graf R, Clavien PA. Novel short-term hypothermic oxygenated perfusion (HOPE) system prevents injury in rat liver graft from non-heart beating donor. Ann Surg 2006;244:968-976; discussion 76-77. (Pubitemid 44808636)
108. Bessems M, Doorschodt BM, Kolkert JL, 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;13:497-504. (Pubitemid 46605850)
109. Kroemer G, Reed JC. Mitochondrial control of cell death. Nat Med 2000;6:513-519.
110. Schild L, Reinheckel T, Wiswedel I, Augustin W. Short-term impairment of energy production in isolated rat liver mitochondria by hypoxia/reoxygenation: involvement of oxidative protein modification. Biochem J 1997;328(pt 1):205-210. (Pubitemid 27499460)
111. Rouslin W. Mitochondrial complexes I, II, III, IV, and V in myocardial ischemia and autolysis. Am J Physiol 1983;244:H743-H748.
112. Arduini A, Mezzetti A, Porreca E, Lapenna D, DeJulia J, Marzio L, et al. Effect of ischemia and reperfusion on antioxidant enzymes and mitochondrial inner membrane proteins in perfused rat heart. Biochim Biophys Acta 1988;970:113-121. (Pubitemid 18154407)
113. Kurokawa T, Kobayashi H, Nonami T, Harada A, Nakao A, Takagi H. Mitochondrial glutathione redox and energy producing function during liver ischemia and reperfusion. J Surg Res 1996;66:1-5. (Pubitemid 27009367)
114. Dutkowski P, Krug A, Krysiak M, Dunschede F, Seifert JK, Junginger T. Detection of mitochondrial electron chain carrier redox status by transhepatic light intensity during rat liver reperfusion. Cryobiology 2003;47:125-142. (Pubitemid 37315806)
115. Hasegawa T, Ito Y, Wijeweera J, Liu J, Malle E, Farhood A, et al. Reduced inflammatory response and increased microcirculatory disturbances during hepatic ischemia-reperfusion injury in steatotic livers of ob/ob mice. Am J Physiol Gastrointest Liver Physiol 2007;292:G1385-G1395. (Pubitemid 47084668)
116. Lang JD Jr, Teng X, Chumley P, Crawford JH, Isbell TS, Chacko BK, et al. Inhaled NO accelerates restoration of liver function in adults following orthotopic liver transplantation. J Clin Invest 2007;117:2583-2591. (Pubitemid 47494359)
117. Clemens MG. Nitric oxide in liver injury. Hepatology 1999;30:1-5.
118. Shah V, Haddad FG, Garcia-Cardena G, Frangos JA, Mennone A, Groszmann RJ, et al. Liver sinusoidal endothelial cells are responsible for nitric oxide modulation of resistance in the hepatic sinusoids. J Clin Invest 1997;100:2923-2930. (Pubitemid 28007564)
119. Hur GM, Ryu YS, Yun HY, Jeon BH, Kim YM, Seok JH, et al. Hepatic ischemia/reperfusion in rats induces iNOS gene transcription by activation of NF-kappaB. Biochem Biophys Res Commun 1999;261:917-922.
120. Bogdan C. Nitric oxide and the immune response. Nat Immunol 2001;2:907-916.
121. Takei Y, Marzi I, Gao WS, Gores GJ, Lemasters JJ, Thurman RG. Leukocyte adhesion and cell death following orthotopic liver transplantation in the rat. Transplantation 1991;51:959-965.
122. Nakano H, Nagasaki H, Barama A, Boudjema K, Jaeck D, Kumada K, et al. The effects of N-acetylcysteine and anti-intercellular adhesion molecule-1 monoclonal antibody against ischemia-reperfusion injury of the rat steatotic liver produced by a choline-methionine-deficient diet. Hepatology 1997;26:670-678. (Pubitemid 27392359)
123. Tacchini L, Cairo G, De Ponti C, Massip M, Rosello- Catafau J, Peralta C. Up regulation of IL-6 by ischemic preconditioning in normal and fatty rat livers: association with reduction of oxidative stress. Free Radic Res 2006;40:1206-1217. (Pubitemid 44490161)
124. Massip-Salcedo M, Zaouali MA, Padrissa-Altes S, Casillas- Ramirez A, Rodes J, Rosello-Catafau J, et al. Activation of peroxisome proliferator- activated receptor-alpha inhibits the injurious effects of adiponectin in rat steatotic liver undergoing ischemia-reperfusion. Hepatology 2008;47:461-472. (Pubitemid 351280714)
125. Lehmann TG, Wheeler MD, Froh M, Schwabe RF, Bunzendahl H, Samulski RJ, et al. Effects of three superoxide dismutase genes delivered with an adenovirus on graft function after transplantation of fatty livers in the rat. Transplantation 2003;76:28-37. (Pubitemid 36877111)
126. Nocito A, Dahm F, Jochum W, Jang JH, Georgiev P, Bader M, et al. Serotonin mediates oxidative stress and mitochondrial toxicity in a murine model of nonalcoholic steatohepatitis. Gastroenterology 2007;133:608-618. (Pubitemid 47187345)
127. Nocito A, Georgiev P, Dahm F, Jochum W, Bader M, Graf R, et al. Platelets and platelet-derived serotonin promote tissue repair after normothermic hepatic ischemia in mice. Hepatology 2007;45:369-376. (Pubitemid 46374593)
128. Lesurtel M, Graf R, Aleil B, Walther DJ, Tian Y, Jochum W, et al. Platelet-derived serotonin mediates liver regeneration. Science 2006;312:104-107.