Journal of Surgical Research
Volume 152, Issue 1 , Pages 61-68 , March 2009

Intermittent Ischemia but Not Ischemic Preconditioning Is Effective in Restoring Bile Flow After Ischemia Reperfusion Injury in the Livers of Aged Rats

  • Marc Schiesser, M.D.

      Affiliations

    • The HPB and Liver Transplant Unit, Flinders Medical Centre and School of Medicine, Flinders University, Adelaide, South Australia, Australia
    • ,
  • Anna Wittert, M.D.

      Affiliations

    • The HPB and Liver Transplant Unit, Flinders Medical Centre and School of Medicine, Flinders University, Adelaide, South Australia, Australia
    • ,
  • Vincent B. Nieuwenhuijs, M.D., Ph.D.

      Affiliations

    • University Medical Centre, Groningen, The Netherlands
    • ,
  • Arthur Morphett, F.R.C.P.A., M.B.B.S.

      Affiliations

    • Department of Anatomical Pathology, Flinders Medical Centre and School of Medicine, Flinders University, Adelaide, South Australia, Australia
    • ,
  • Robert T.A. Padbury, F.R.A.C.S., M.B.B.S.

      Affiliations

    • The HPB and Liver Transplant Unit, Flinders Medical Centre and School of Medicine, Flinders University, Adelaide, South Australia, Australia
    • ,
  • Greg J. Barritt, Ph.D.

      Affiliations

    • Department of Medical Biochemistry, Flinders Medical Centre and School of Medicine, Flinders University, Adelaide, South Australia, Australia
    • Corresponding Author InformationTo whom correspondence and reprint requests should be addressed at Department of Medical Biochemistry, School of Medicine, Flinders University, GPO Box 2100, Adelaide SA 5001, Australia

Received 24 October 2007

References 

  1. Busuttil RW, Tanaka K. The utility of marginal donors in liver transplantation. Liver Transplant. 2003;9:651
  2. Okaya T, Blanchard J, Schuster R, et al. Age-dependent responses to hepatic ischemia/reperfusion injury. Shock. 2005;24:421
  3. Serafin A, Rosello-Catafau J, Prats N, et al. Ischemic preconditioning increases the tolerance of Fatty liver to hepatic ischemia-reperfusion injury in the rat. Am J Pathol. 2002;161:587
  4. Park Y, Hirose R, Coatney JL, et al. Ischemia-reperfusion injury is more severe in older versus young rat livers. J Surg Res. 2007;137:96
  5. Grazi GL, Ravaioli M, Zanello M, et al. Using elderly donors in liver transplantation. Transplant Proc. 2005;37:2582
  6. Madariaga JR, Marino IR, Karavias DD, et al. Long-term results after liver transplantation for primary hepatic epithelioid hemangioendothelioma. Ann Surg Oncol. 1995;2:483
  7. Ploeg RJ, D'Alessandro AM, Knechtle SJ, et al. Risk factors for primary dysfunction after liver transplantation–a multivariate analysis. Transplantation. 1993;55:807
  8. Le Couteur DG, Rivory LP, Pond SM. The effects of aging and nutritional state on hypoxia-reoxygenation injury in the perfused rat liver. Transplantation. 1994;58:531
  9. Iakova P, Awad SS, Timchenko NA. Aging reduces proliferative capacities of liver by switching pathways of C/EBPalpha growth arrest. Cell. 2003;113:495
  10. Reznick RM, Zong H, Li J, et al. Aging-associated reductions in AMP-activated protein kinase activity and mitochondrial biogenesis. Cell Metab. 2007;5:151
  11. Lesnefsky EJ, Gudz TI, Migita CT, et al. Ischemic injury to mitochondrial electron transport in the aging heart: Damage to the iron-sulfur protein subunit of electron transport complex III. Arch Biochem Biophys. 2001;385:117
  12. Sastre J, Pallardo FV, Pla R, et al. Aging of the liver: Age-associated mitochondrial damage in intact hepatocytes. Hepatology. 1996;24:1199
  13. Zhao Y, Lo CM, Liu CL, et al. Use of elderly donors (>60 years) for liver transplantation. Asian J Surg. 2004;27:114
  14. Glantzounis GK, Salacinski HJ, Yang W, et al. The contemporary role of antioxidant therapy in attenuating liver ischemia-reperfusion injury: A review. [see comment] Liver Transplant. 2005;11:1031
  15. Massip-Salcedo M, Rosello-Catafau J, Prieto J, et al. The response of the hepatocyte to ischemia. Liver Int. 2007;27:6
  16. Nieuwenhuijs VB, De Bruijn MT, Padbury RT, et al. Hepatic ischemia-reperfusion injury: roles of Ca2+ and other intracellular mediators of impaired bile flow and hepatocyte damage. Dig Dis Sci. 2006;51:1087
  17. Nieuwenhuijs VB, De Bruijn MT, Schiesser M, et al. Ischemic preconditioning and intermittent ischemia preserve bile flow in a rat model of ischemia reperfusion injury. Dig Dis Sci. 2007;52:1159
  18. Jourdan M, Vaubourdolle M, Cynober L, et al. Effect of aging on liver functions-an experimental study in a perfused rat liver model. Exp Gerontol. 2004;39:1341
  19. Accatino L, Pizarro M, Solis N, et al. Bile secretory function after warm hepatic ischemia-reperfusion injury in the rat. Liver Transplant. 2003;9:1199
  20. Koeppel TA, Trauner M, Mennone A, et al. Role of glutathione in hepatic bile formation during reperfusion after cold ischemia of the rat liver. J Hepatol. 1998;28:812
  21. Stadtman ER. Protein oxidation and aging. Science. 1992;257:1220
  22. Hasselgren PO, Fornander J, Jagenburg R, et al. Effects of live ischemia on hepatic protein synthesis in vitro and in vivo. Acta Physiol Scand. 1982;114:143
  23. Bowers BA, Branum GD, Rotolo FS, et al. Bile flow—an index of ischemic injury. J Surg Res. 1987;42:565
  24. Kamiike W, Burdelski M, Steinhoff G, et al. Adenine nucleotide metabolism and its relation to organ viability in human liver transplantation. Transplantation. 1988;45:138
  25. Sumimoto K, Inagaki K, Yamada K, et al. Reliable indices for the determination of viability of grafted liver immediately after orthotopic transplantation (Bile flow rate and cellular adenosine triphosphate level). Transplantation. 1988;46:506
  26. Selzner M, Selzner N, Jochum W, et al. Increased ischemic injury in old mouse liver: An ATP dependent mechanism. Liver Transplant. 2007;13:382
  27. Clavien PA, Selzner M, Rudiger HA, et al. A prospective randomized study in 100 consecutive patients undergoing major liver resection with versus without ischemic preconditioning. Ann Surg. 2003;238:843;discussion 851
  28. Petrowsky H, McCormack L, Trujillo M, et al. A prospective, randomized, controlled trial comparing intermittent portal triad clamping versus ischemic preconditioning with continuous clamping for major liver resection. Ann Surg. 2006;244:921;discussion 928
  29. Kerem M, Bedirli A, Ofluoglu E, et al. Ischemic preconditioning improves liver regeneration by sustaining energy metabolism after partial hepatectomy under ischemia in rats. Liver Int. 2006;26:994
  30. Niemann CU, Hirose R, Liu T, et al. Ischemic preconditioning improves energy state and transplantation survival in obese Zucker rat livers. Anesth Analges. 2005;101:1577
  31. Tang L-J, Tian F-Z, Tao W, et al. Hepatocellular glycogen in alleviation of liver ischemia reperfusion injury during partial hepatectomy. World J Surg. 2007;31:2039
  32. Selzner N, Rudiger H, Graf R, et al. Protective strategies against ischemic injury of the liver. Gastroenterology. 2003;125:917
  33. Burtis CA, Ashwood ER. In: Tietz textbook of clinical chemistry. Philadelphia: W.B. Saunders; 1999;p. 641
  34. Rudiger HA, Kang KJ, Sindram D, et al. Comparison of ischemic preconditioning and intermittent and continuous inflow occlusion in the murine liver. Ann Surg. 2002;235:400
  35. Smyrniotis V, Theodoraki K, Arkadopoulos N, et al. Ischemic preconditioning versus intermittent vascular occlusion in liver resections performed under selective vascular exclusion: A prospective randomized study. Am J Surg. 2006;192:669
  36. Vajdova K, Heinrich S, Tian Y, et al. Ischemic preconditioning and intermittent clamping improve murine hepatic microcirculation and Kupffer cell function after ischemic injury. Liver Transplant. 2004;10:520
  37. Berrevoet F, Schafer T, Vollmar B, et al. Ischemic preconditioning: enough evidence to support clinical application in liver surgery and transplantation?. Acta Chir Belg. 2003;103:485
  38. Furrer K, Deoliveira ML, Graf R, et al. Improving outcome in patients undergoing liver surgery. Liver Int. 2007;27:26
  39. Gomez D, Homer-Vanniasinkam S, Graham AM, et al. Role of ischaemic preconditioning in liver regeneration following major liver resection and transplantation. World J Gastroenterol. 2007;13:657
  40. Nuzzo G, Giuliante F, Vellone M, et al. Pedicle clamping with ischemic preconditioning in liver resection. Liver Transplant. 2004;10:S53
  41. Padbury RT. European survey on the application of vascular clamping in liver surgery: Editorial comment. Dig Surg. 2007;24:434
  42. van der Bilt JD, Livestro DP, Borren A, et al. European survey on the application of vascular clamping in liver surgery. Dig Surg. 2007;24:423
  43. Smyrniotis V, Farantos C, Kostopanagiotou G, et al. Vascular control during hepatectomy: Review of methods and results. World J Surg. 2005;29:1384
  44. van der Bilt JD, Kranenburg O, Nijkamp MW, et al. Ischemia/reperfusion accelerates the outgrowth of hepatic micrometastases in a highly standardized murine model. Hepatology. 2005;42:165

PII: S0022-4804(08)00008-5

doi: 10.1016/j.jss.2008.01.007

Journal of Surgical Research
Volume 152, Issue 1 , Pages 61-68 , March 2009

Article Tools

* Image Usage & Resolution