HTK-N, a modified HTK solution, decreases preservation injury in a model of microsteatotic rat liver transplantation

Langenbeck's Archives of Surgery

Volumn 397, Issue 8, 2012, Pages 1323-1331

  Liu, Qinlong ^a   Bruns, Helge ^a   Schultze, Daniel ^a   Xue, Yi ^a   Zorn, Markus ^a   Flechtenmacher, Christa ^a   Straub, Beate K ^a   Rauen, Ursula ^b   Schemmer, Peter ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

Cold ischemia; Liver transplantation; Organ preservation; Preservation solution; Reperfusion injury; Steatosis

Indexed keywords

ALANINE AMINOTRANSFERASE; AMINO ACID; ASPARTATE AMINOTRANSFERASE; CASPASE 3; HTK N SOLUTION; HTK SOLUTION; INDUCIBLE NITRIC OXIDE SYNTHASE; IRON CHELATING AGENT; LACTATE DEHYDROGENASE; MYELOPEROXIDASE; N ACETYLHISTIDINE; UNCLASSIFIED DRUG; ALCOHOL; DRUG DERIVATIVE; GLUCOSE; HISTIDINE; MANNITOL; N-ACETYLHISTIDINE; POTASSIUM CHLORIDE; PRESERVATION SOLUTION; PROCAINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; COLD INJURY; CONTROLLED STUDY; ENZYME BLOOD LEVEL; FATTY LIVER; FEMALE; HISTOPATHOLOGY; LEUKOCYTE; LIVER GRAFT; LIVER INJURY; LIVER NECROSIS; LIVER PRESERVATION; LIVER PROTECTION; LIVER TRANSPLANTATION; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SURVIVAL; ANIMAL; BLOOD; CHEMISTRY; COLD; DRUG EFFECT; LIVER; MICROVASCULATURE; MORTALITY; PATHOLOGY; SPRAGUE DAWLEY RAT; SURVIVAL RATE; VASCULARIZATION;

ALANINE TRANSAMINASE; ANIMALS; ASPARTATE AMINOTRANSFERASES; COLD TEMPERATURE; ETHANOL; FATTY LIVER; FEMALE; GLUCOSE; HISTIDINE; IRON CHELATING AGENTS; L-LACTATE DEHYDROGENASE; LIVER; LIVER TRANSPLANTATION; MANNITOL; MICROVESSELS; ORGAN PRESERVATION SOLUTIONS; POTASSIUM CHLORIDE; PROCAINE; RATS; RATS, SPRAGUE-DAWLEY; SURVIVAL RATE;

EID: 84877304778     PISSN: 14352443     EISSN: 14352451     Source Type: Journal    
DOI: 10.1007/s00423-012-1022-9     Document Type: Article

References (63)

1. Schemmer P, Nickkholgh A, Gerling T, Weitz J, Büchler MW, Schmidt J (2009) Rescue allocation for liver transplantation within Eurotransplant: the Heidelberg experience. Clin Transplant 23(Suppl 21):42-48. doi: 10.1111/j.1399-0012.2009.01109.x
2. Eguchi Y, Hyogo H, Ono M, Mizuta T, Ono N, Fujimoto K, Chayama K, Saibara T (2012) Prevalence and associated metabolic factors of nonalcoholic fatty liver disease in the general population from 2009 to 2010 in Japan: a multicenter large retrospective study. J Gastroenterol 47(5):586-595. doi: 10.1007/s00535-012-0533-z
3. Sirivatanauksorn Y, Taweerutchana V, Limsrichamrern S, Kositamongkol P, Mahawithitwong P, Asavakarn S, Tovikkai C, Sanphasitvong V (2012) Analysis of donor risk factors associated with graft outcomes in orthotopic liver transplantation. Transplant Proc 44(2):320-323. doi: 10.1016/j.transproceed. 2011.12.031
4. Pokorny H, Gruenberger T, Soliman T, Rockenschaub S, Langle F, Steininger R (2000) Organ survival after primary dysfunction of liver grafts in clinical orthotopic liver transplantation. Transpl Int: Off J of the Eur Soc for Organ Transplant 13(Suppl 1):S154-S157
5. Ke B, Lipshutz GS, Kupiec-Weglinski JW (2006) Gene therapy in liver ischemia and reperfusion injury. Curr Pharm Des 12(23):2969-2975 (Pubitemid 44184629)
6. Cieslak B, Lewandowski Z, Urban M, Ziarkiewicz-Wroblewska B, Krawczyk M (2009) Microvesicular liver graft steatosis as a risk factor of initial poor function in relation to suboptimal donor parameters. Transplant Proc 41(8):2985-2988. doi: 10.1016/j.transproceed.2009.08.019
7. Stegemann J, Hirner A, Rauen U, Minor T (2010) Use of a new modified HTK solution for machine preservation of marginal liver grafts. J Surg Res 160(1):155-162. doi: 10.1016/j.jss.2008.10.021
8. Wu K, Turk TR, Rauen U, Su S, Feldkamp T, de Groot H, Wiswedel I, Baba HA, Kribben A, Witzke O (2011) Prolonged cold storage using a new histidine-tryptophan-ketoglutarate-based preservation solution in isogeneic cardiac mouse grafts. Eur Hear J 32(4):509-516. doi: 10.1093/eurheartj/ehq135
9. Kerkweg U, Li T, de Groot H, Rauen U (2002) Cold-induced apoptosis of rat liver cells in University of Wisconsin solution: the central role of chelatable iron. Hepatology 35(3):560-567. doi: 10.1053/jhep.2002.31869 (Pubitemid 34183959)
10. Rauen U, Kerkweg U, de Groot H (2007) Iron-dependent vs. iron-independent cold-induced injury to cultured rat hepatocytes: a comparative study in physiological media and organ preservation solutions. Cryobiology 54(1):77-86. doi: 10.1016/j.cryobiol.2006.11.008 (Pubitemid 46282702)
11. 2 formation. FASEB J: Off Publ of the Fed of Am Soc for Exp Biol 14(13):1953-1964. doi: 10.1096/fj.00-0071com
12. Rauen U, Polzar B, Stephan H, Mannherz HG, de Groot H (1999) Cold-induced apoptosis in cultured hepatocytes and liver endothelial cells: mediation by reactive oxygen species. FASEB J: Off Publ of the Fed of Am Soc for Exp Biol 13(1):155-168 (Pubitemid 29038285)
13. Rauen U, de Groot H (2008) Inherent toxicity of organ preservation solutions to cultured hepatocytes. Cryobiology 56(1):88-92. doi: 10.1016/j.cryobiol.2007.09.003
14. Rauen U, Klempt S, de Groot H (2007) Histidine-induced injury to cultured liver cells, effects of histidine derivatives and of iron chelators. Cell Mol Life Sci: CMLS 64(2):192-205. doi: 10.1007/s00018-006-6456-1 (Pubitemid 46155699)
15. Dalal P, Romani A (2010) Adenosine triphosphate depletion by cyanide results in a Na(+)-dependent Mg(2+) extrusion from liver cells. Metab Clin Exp 59(11):1663-1671. doi: 10.1016/j.metabol.2010.03.019
16. Frank A, Rauen U, de Groot H (2000) Protection by glycine against hypoxic injury of rat hepatocytes: inhibition of ion fluxes through nonspecific leaks. J Hepatol 32(1):58-66 (Pubitemid 30039448)
17. Fuckert O, Rauen U, De Groot H (2000) A role for sodium in hypoxic but not in hypothermic injury to hepatocytes and LLC-PK1 cells. Transplantation 70(5):723-730
18. Weinberg JM, Venkatachalam MA, Roeser NF, Nissim I (2000) Mitochondrial dysfunction during hypoxia/reoxygenation and its correction by anaerobic metabolism of citric acid cycle intermediates. Proc Natl Acad Sci U S A 97(6):2826-2831 (Pubitemid 30159256)
19. Uhlmann D, Uhlmann S, Spiegel HU (2000) Endothelin/nitric oxide balance influences hepatic ischemia-reperfusion injury. J Cardiovasc Pharmacol 36(5 Suppl 1):S212-S214
20. Wu B, Iwakiri R, Tsunada S, Utsumi H, Kojima M, Fujise T, Ootani A, Fujimoto K (2002) iNOS enhances rat intestinal apoptosis after ischemia-reperfusion. Free Radic Biol Med 33(5):649-658 (Pubitemid 35245837)
21. Yagnik GP, Takahashi Y, Tsoulfas G, Reid K, Murase N, Geller DA (2002) Blockade of the l-arginine/NO synthase pathway worsens hepatic apoptosis and liver transplant preservation injury. Hepatology 36(3):573-581. doi: 10.1053/jhep.2002.35058 (Pubitemid 34977167)
22. Stegemann J, Hirner A, Rauen U, Minor T (2009) Gaseous oxygen persufflation or oxygenated machine perfusion with Custodiol-N for long-term preservation of ischemic rat livers? Cryobiology 58(1):45-51. doi: 10.1016/j.cryobiol.2008.10.127
23. Liu Q, Bruns H, Nickkholgh A, Schemmer P (2009) Custodiol-N attenuates reperfusion injury of steatotic rat livers. In: Abstracts of the 5th ELITA-ELTR (European Society for Organ Transplantation-European Liver and Intestine Transplant Association) Winter Meeting, Are, Sweden, 19-21 March 2009. Transplant International: Official Journal of the European Society for Organ Transplantation 22 Suppl 1:1-7. doi: 10.1111/j.1432-2277.2009.00853.x
24. Enomoto N, Yamashina S, Kono H, Schemmer P, Rivera CA, Enomoto A, Nishiura T, Nishimura T, Brenner DA, Thurman RG (1999) Development of a new, simple rat model of early alcohol-induced liver injury based on sensitization of Kupffer cells. Hepatology 29(6):1680-1689. doi: 10.1002/hep.510290633 (Pubitemid 29247039)
25. Gao W, Lemasters JJ, Thurman RG (1993) Development of a new method for hepatic rearterialization in rat orthotopic liver transplantation. Reduction of liver injury and improvement of surgical outcome by arterialization. Transplantation 56(1):19-24 (Pubitemid 23220566)
26. Schemmer P, Schoonhoven R, Swenberg JA, Bunzendahl H, Thurman RG (1998) Gentle in situ liver manipulation during organ harvest decreases survival after rat liver transplantation: role of Kupffer cells. Transplantation 65(8):1015-1020 (Pubitemid 28208417)
27. Bergmeyer H (1988) Methods of enzymatic analysis. Academic Press, New York
28. Nickkholgh A, Weitz J, Encke J, Sauer P, Mehrabi A, Büchler MW, Schmidt J, Schemmer P (2007) Utilization of extended donor criteria in liver transplantation: a comprehensive review of the literature. Nephrol Dial Transplant: Off Publ of the Eur Dial and Transplant Assoc-Eur Ren Assoc 22(Suppl 8):viii29-viii36. doi: 10.1093/ndt/gfm654
29. Schemmer P, Nickkholgh A, Hinz U, Gerling T, Mehrabi A, Sauer P, Encke J, Friess H, Weitz J, Büchler MW, Schmidt J (2007) Extended donor criteria have no negative impact on early outcome after liver transplantation: a single-center multivariate analysis. Transplant Proc 39(2):529-534. doi: 10.1016/j.transproceed.2006.12.002 (Pubitemid 46386206)
30. Rauen U, de Groot H (2004) New insights into the cellular and molecular mechanisms of cold storage injury. J of Invest Med: The Off Publ of the Am Fed for Clin Res 52(5):299-309 (Pubitemid 39447360)
31. Hui AM, Kawasaki S, Makuuchi M, Nakayama J, Ikegami T, Miyagawa S (1994) Liver injury following normothermic ischemia in steatotic rat liver. Hepatology 20(5):1287-1293 (Pubitemid 24323579)
32. Zimmerman BJ, Grisham MB, Granger DN (1990) Role of oxidants in ischemia/reperfusion-induced granulocyte infiltration. Am J Physiol 258(2 Pt 1):G185-G190
33. Bruns H, Watanpour I, Gebhard MM, Flechtenmacher C, Galli U, Schulze-Bergkamen H, Zorn M, Büchler MW, Schemmer P (2011) Glycine and taurine equally prevent fatty livers from Kupffer cell-dependent injury: an in vivo microscopy study. Microcirculation 18(3):205-213. doi: 10.1111/j.1549-8719. 2010.00078.x
34. Schemmer P, Enomoto N, Bradford BU, Bunzendahl H, Raleigh JA, Lemasters JJ, Thurman RG (2001) Activated Kupffer cells cause a hypermetabolic state after gentle in situ manipulation of liver in rats. Am J Physiol Gastrointest Liver Physiol 280(6):G1076-G1082
35. Wheeler MD, Ikejema K, Enomoto N, Stacklewitz RF, Seabra V, Zhong Z, Yin M, Schemmer P, Rose ML, Rusyn I, Bradford B, Thurman RG (1999) Glycine: a new anti-inflammatory immunonutrient. Cell Mol Life Sci: CMLS 56(9-10):843-856
36. Szabo G, Bala S (2010) Alcoholic liver disease and the gut-liver axis. World J Gastroenterol: WJG 16(11):1321-1329
37. Enomoto N, Ikejima K, Bradford B, Rivera C, Kono H, Brenner DA, Thurman RG (1998) Alcohol causes both tolerance and sensitization of rat Kupffer cells via mechanisms dependent on endotoxin. Gastroenterology 115(2):443-451 (Pubitemid 28363437)
38. DeCarli LM, Lieber CS (1967) Fatty liver in the rat after prolonged intake of ethanol with a nutritionally adequate new liquid diet. J Nutr 91(3):331-336
39. Lieber CS, Jones DP, Decarli LM (1965) Effects of prolonged ethanol intake: production of fatty liver despite adequate diets. J Clin Investig 44:1009-1021. doi: 10.1172/JCI105200
40. Lieber CS, Spritz N, DeCarli LM (1969) Fatty liver produced by dietary deficiencies: its pathogenesis and potentiation by ethanol. J of Lipid Res 10(3):283-287
41. Devlin J, Dunne JB, Sherwood RA, Chambers SM, Tan KC, Peters TJ, Williams R (1995) Relationship between early liver graft viability and enzyme activities in effluent preservation solution. Transplantation 60(7):627-631
42. + overload in the rat. Hepatology 26(1):107-112. doi: 10.1002/hep.510260114 (Pubitemid 27280313)
43. Arkadopoulos N, Nastos C, Kalimeris K, Economou E, Theodoraki K, Kouskouni E, Pafiti A, Kostopanagiotou G, Smyrniotis V (2010) Iron chelation for amelioration of liver ischemia-reperfusion injury. Hemoglobin 34(3):265-277. doi: 10.3109/03630269.2010.484766
44. Hoffmann K, Büchler MW, Schemmer P (2011) Supplementation of amino acids to prevent reperfusion injury after liver surgery and transplantation - where do we stand today? Clin Nutr 30(2):143-147. doi: 10.1016/j.clnu.2010.09. 006
45. Schemmer P, Schoonhoven R, Swenberg JA, Bunzendahl H, Raleigh JA, Lemasters JJ, Thurman RG (1999) Gentle organ manipulation during harvest as a key determinant of survival of fatty livers after transplantation in the rat. Transplant Int: Off J of the Eur Soc for Organ Transplant 12(5):351-359 (Pubitemid 29502005)
46. Enomoto N, Ikejima K, Yamashina S, Enomoto A, Nishiura T, Nishimura T, Brenner DA, Schemmer P, Bradford BU, Rivera CA, Zhong Z, Thurman RG (2000) Kupffer cell-derived prostaglandin E(2) is involved in alcohol-induced fat accumulation in rat liver. Am J Physiol Gastrointest Liver Physiol 279(1):G100-G106
47. Yadav SS, Howell DN, Gao W, Steeber DA, Harland RC, Clavien PA (1998) l-selectin and ICAM-1 mediate reperfusion injury and neutrophil adhesion in the warm ischemic mouse liver. Am J Physiol 275(6 Pt 1):G1341-G1352
48. Andrades M, Ritter C, de Oliveira MR, Streck EL, Fonseca Moreira JC, Dal-Pizzol F (2011) Antioxidant treatment reverses organ failure in rat model of sepsis: role of antioxidant enzymes imbalance, neutrophil infiltration, and oxidative stress. J Surg Res 167(2):e307-e313. doi: 10.1016/j.jss.2009.08.005
49. Burch JB, Svendsen E, Siegel PD, Wagner SE, von Essen S, Keefe T, Mehaffy J, Martinez AS, Bradford M, Baker L, Cranmer B, Saito R, Tessari J, Linda P, Andersen C, Christensen O, Koehncke N, Reynolds SJ (2010) Endotoxin exposure and inflammation markers among agricultural workers in Colorado and Nebraska. J Toxic Environ Health A 73(1):5-22. doi: 10.1080/15287390903248604
50. Yoshida M, Sasaki M, Nakabayashi I, Akashi M, Tomiyasu T, Yoshikawa N, Kojima T, Ohno N, Yamada M (2009) Two types of myeloperoxidase-antineutrophil cytoplasmic autoantibodies with a high affinity and a low affinity in small vessel vasculitis. Clin Exp Rheumatol 27(1 Suppl 52):S28-S32
51. Palmes D, Minin E, Budny T, Uhlmann D, Armann B, Stratmann U, Herbst H, Spiegel HU (2005) The endothelin/nitric oxide balance determines small-for-size liver injury after reduced-size rat liver transplantation. Virchows Arch: an Int J of Pathol 447(4):731-741. doi: 10.1007/s00428-005-0006-3 (Pubitemid 41571189)
52. Uhlmann D, Armann B, Gaebel G, Ludwig S, Hess J, Pietsch UC, Escher E, Fiedler M, Tannapfel A, Hauss J, Witzigmann H (2003) Endothelin A receptor blockade reduces hepatic ischemia/reperfusion injury after warm ischemia in a pig model. J of Gastrointest Surg: Off J of the Soc for Surg of the Aliment Tract 7(3):331-339 (Pubitemid 36875771)
53. Bahde R, Palmes D, Gemsa O, Minin E, Stratmann U, de Groot H, Rauen U, Spiegel HU (2008) Attenuated cold storage injury of rat livers using a modified HTK solution. J Surg Res 146(1):49-56. doi: 10.1016/j.jss.2007.08.011
54. + homeostasis as a critical step in the development of irreversible hepatocyte injury after adenosine triphosphate depletion. Hepatology 21(4):1089-1098
55. Carini R, De Cesaris MG, Splendore R, Bagnati M, Albano E (2000) Ischemic preconditioning reduces Na(+) accumulation and cell killing in isolated rat hepatocytes exposed to hypoxia. Hepatology 31(1):166-172. doi: 10.1002/hep.510310125 (Pubitemid 30033703)
56. Schemmer P, Golling M, Kraus T, Mayatepek E, Herfarth C, Klar E (2001) Glycine reduces reperfusion injury in human liver transplantation: our first patients. Transplant Proc 33(7-8):3750-3752 (Pubitemid 34042764)
57. Atahan E, Ergun Y, Kurutas EB, Alici T (2010) Protective effect of zinc aspartate on long-term ischemia-reperfusion injury in rat skeletal muscle. Biol Trace Elem Res 137(2):206-215. doi: 10.1007/s12011-009-8568-6
58. Natori S, Selzner M, Valentino KL, Fritz LC, Srinivasan A, Clavien PA, Gores GJ (1999) Apoptosis of sinusoidal endothelial cells occurs during liver preservation injury by a caspase-dependent mechanism. Transplantation 68(1):89-96 (Pubitemid 29352837)
59. Rentsch M, Beham A, Iesalnieks I, Mirwald T, Anthuber M, Jauch KW (2001) Impact of prolonged cold ischemia and reperfusion on apoptosis, activation of caspase 3, and expression of bax after liver transplantation in the rat. Transplant Proc 33(1-2):850-851 (Pubitemid 32237653)
60. Zhang Y, Dong Y, Wu X, Lu Y, Xu Z, Knapp A, Yue Y, Xu T, Xie Z (2010) The mitochondrial pathway of anesthetic isoflurane-induced apoptosis. J Biol Chem 285(6):4025-4037. doi: 10.1074/jbc.M109.065664
61. Abu-Amara M, Yang SY, Seifalian A, Davidson B, Fuller B (2012) The nitric oxide pathway - evidence and mechanisms for protection against liver ischaemia reperfusion injury. Liver Int: Off J of the Int Assoc for the Study of the Liver 32(4):531-543. doi: 10.1111/j.1478-3231.2012.02755.x
62. Koeppel TA, Mihaljevic N, Kraenzlin B, Loehr M, Jesenofsky R, Post S, Palma P (2007) Enhanced iNOS gene expression in the steatotic rat liver after normothermic ischemia. Eur Sur Res Europaische Chirurgische Forsch Rech Chirurgicales Europeennes 39(5):303-311. doi: 10.1159/000104401 (Pubitemid 47294442)
63. Kaizu T, Ikeda A, Nakao A, Takahashi Y, Tsung A, Kohmoto J, Toyokawa H, Shao L, Bucher BT, Tomiyama K, Nalesnik MA, Murase N, Geller DA (2006) Donor graft adenoviral iNOS gene transfer ameliorates rat liver transplant preservation injury and improves survival. Hepatology 43(3):464-473. doi: 10.1002/hep.21067