1,794
Views
109
CrossRef citations to date
0
Altmetric
REVIEW ARTICLE

Liver Ischemia/Reperfusion Injury: an Overview

&
Pages 366-379 | Received 23 Dec 2013, Accepted 04 Jun 2014, Published online: 24 Jul 2014

REFERENCES

  • Saidi RF. Current status of liver transplantation. Arch Iran Med. 2012;15(12):772–776.
  • Ploeg RJ, D'Alessandro AM, Knechtle SJ, Risk factors for primary dysfunction after liver transplantation–a multivariate analysis. Transplantation. 1993;55(4):807–813.
  • Lee CT, Dunn RL, Chen BT, Impact of body mass index on radical cystectomy. J. Urol. 2004;172(4 Pt 1):1281–1285.
  • Tsukada K, Miyazaki T, Kato H, Body fat accumulation and postoperative complications after abdominal surgery. Am J Surg. 2004;70(4):347–351.
  • Serracino-Inglott F, Habib NA, Mathie RT. Hepatic ischemia-reperfusion injury. Am J Surg. 2001;181(2): 160–166.
  • Vollmar B, Glasz J, Leiderer R, Hepatic microcirculatory perfusion failure is a determinant of liver dysfunction in warm ischemia-reperfusion. Am J Pathol. 1994;145(6):1421–1431.
  • Marzi I, Takei Y, Rücker M, Endothelin-1 is involved in hepatic sinusoidal vasoconstriction after ischemia and reperfusion. Transpl Int. 1994;7(Suppl 1):S503–506.
  • Yadav SS, Howell DN, Gao W, L-selectin and ICAM-1 mediate reperfusion injury and neutrophil adhesion in the warm ischemic mouse liver. Am J Physiol. 1998;275(6 Pt 1):G1341–1352.
  • Cywes R, Packham MA, Tietze L, Role of platelets in hepatic allograft preservation injury in the rat. Hepatology. 1993;18(3):635–647.
  • Walsh KB, Toledo AH, Rivera-Chavez FA, Inflammatory mediators of liver ischemia-reperfusion injury. Exp Clin Transplant. 2009;7:78–93
  • Perry BC, Soltys D, Toledo AH, Tumor necrosis factor-α in liver ischemia/reperfusion injury. J Invest Surg. 2011;24:178–88
  • Thornton AJ, Strieter RM, Lindley I, Cytokine-induced gene expression of a neutrophil chemotactic factor/IL-8 in human hepatocytes. J Immunol. 1990;144(7):2609–2613.
  • Shito M, Wakabayashi G, Ueda M, Interleukin 1 receptor blockade reduces tumor necrosis factor production, tissue injury, and mortality after hepatic ischemia-reperfusion in the rat. Transplantation. 1997;63(1):143–148.
  • Suzuki S, Toledo-Pereyra LH. Interleukin 1 and tumor necrosis factor production as the initial stimulants of liver ischemia and reperfusion injury. J Surg Res. 1994;57(2):253–258.
  • Busuttil RW, Tanaka K. The utility of marginal donors in liver transplantation. Liver Transpl. 2003;9(7):651–663.
  • Casillas-Ramírez A, Mosbah IB, Ramalho F, Past and future approaches to ischemia-reperfusion lesion associated with liver transplantation. Life Sci. 2006;79(20):1881–1894.
  • Jaeschke H. Molecular mechanisms of hepatic ischemia-reperfusion injury and preconditioning. Am J Physiol Gastrointest Liver Physiol. 2003;284(1):G15–26.
  • Hashimoto K, Miller C. The use of marginal grafts in liver transplantation. J Hepatobiliary Pancreat Surg. 2008;15(2):92–101.
  • Ijaz S, Yang W, Winslet MC, Impairment of hepatic microcirculation in fatty liver. Microcirculation 2003;10(6):447–456.
  • Fernández L, Carrasco-Chaumel E, Serafín A, Is ischemic preconditioning a useful strategy in steatotic liver transplantation? Am J Transplant. 2004;4(6):888–899.
  • Ben Mosbah I, Alfany-Fernández I, Martel C, Endoplasmic reticulum stress inhibition protects steatotic and non-steatotic livers in partial hepatectomy under ischemia-reperfusion. Cell Death Dis. 2010;1:e52.
  • Massip-Salcedo M, Roselló-Catafau J, Prieto J, The response of the hepatocyte to ischemia. Liver Int. 2007;27(1):6–16.
  • Van Der Hoeven JA, Ter Horst GJ, Molema G, Effects of brain death and hemodynamic status on function and immunologic activation of the potential donor liver in the rat. Ann Surg. 2000;232(6):804–813.
  • Qing D-K. Prolonging warm ischemia reduces the cold preservation limits of liver grafts in swine. HBPD INT. 2006;5(4):515–520.
  • Ma Y, Wang G-D, Wu L-W, Dynamical changing patterns of histological structure and ultrastructure of liver graft undergoing warm ischemia injury from non-heart-beating donor in rats. World J Gastroenterol. 2006;12(30):4902–4905.
  • De Rougemont O, Lehmann K, Clavien P-A. Preconditioning, organ preservation, and postconditioning to prevent ischemia-reperfusion injury to the liver. Liver Transpl. 2009;15(10):1172–1182.
  • Miyagi S, Ohkohchi N, Oikawa K, Effects of anti-inflammatory cytokine agent (FR167653) and serine protease inhibitor on warm ischemia-reperfusion injury of the liver graft. Transplantation. 2004;77(10):1487–1493.
  • Yamauchi JI, Richter S, Vollmar B, Warm preflush with streptokinase improves microvascular procurement and tissue integrity in liver graft retrieval from non-heart-beating donors. Transplantation. 2000;69(9):1780–1784.
  • Oikawa K, Ohkohchi N, Sato M, The effects of the elimination of Kupffer cells in the isolated perfused liver from non-heart-beating rat. Transpl Int. 2000;13(Suppl 1):S573–579.
  • Liu Q, Bruns H, Schultze D, HTK-N, a modified HTK solution, decreases preservation injury in a model of microsteatotic rat liver transplantation. Langenbecks Arch Surg. 2012;397(8):1323–1331.
  • Phillips L, Toledo AH, Lopez-Neblina F, Nitric oxide mechanism of protection in ischemia and reperfusion injury. J Invest Surg. 2009;22:46–55.
  • Ramalho FS, Alfany-Fernandez I, Casillas-Ramirez A, Are angiotensin II receptor antagonists useful strategies in steatotic and nonsteatotic livers in conditions of partial hepatectomy under ischemia-reperfusion? J Pharmacol Exp Ther. 2009;329(1):130–140.
  • Casillas-Ramirez A, Amine-Zaouali M, Massip-Salcedo M, Inhibition of angiotensin II action protects rat steatotic livers against ischemia-reperfusion injury. Crit Care Med. 2008;36(4):1256–1266.
  • Alfany-Fernandez I, Casillas-Ramirez A, Bintanel-Morcillo M, Therapeutic targets in liver transplantation: angiotensin II in nonsteatotic grafts and angiotensin-(1–7) in steatotic grafts. Am J Transplant. 2009;9(3):439–451.
  • Liu PG, He SQ, Zhang YH, Protective effects of apocynin and allopurinol on ischemia/reperfusion-induced liver injury in mice. World J Gastroenterol. 2008;14:2832–2837
  • Vriens MR, Marinelli A, Harinck HI, The role of allopurinol in human liver ischemia/reperfusion injury: a prospective randomized clinical trial. Hepatogastroenterology. 2002;49:1069–73
  • Jansen NJ, Van Oeveren W, Van den Broek L, Inhibition by dexamethasone of the reperfusion phenomena in cardiopulmonary bypass. J Thorac Cardiovasc Surg. 1991;102(4):515–525.
  • Figueroa I, Santiago-Delpín EA. Steroid protection of the liver during experimental eschemia. Surg Gynecol Obstet. 1975;140(3):368–370.
  • Sileri P, Schena S, Fukada J, Corticosteroids enhance hepatic injury following ischemia-reperfusion. Transplant Proc. 2001;33(7–8):3712.
  • Bilbao G, Contreras JL, Eckhoff DE, Reduction of ischemia-reperfusion injury of the liver by in vivo adenovirus-mediated gene transfer of the antiapoptotic Bcl-2 gene. Ann Surg. 1999;230(2):185–193.
  • Saidi RF, Chang J, Verb S, The effect of methylprednisolone on warm ischemia-reperfusion injury in the liver. Am J Surg. 2007;193(3):345–347; discussion 347–348.
  • Frankenberg MV, Forman DT, Frey W, Proteolysis but not ICAM-1 expression in fatty liver increased in tissue harvesting–role of Kupffer cells. Langenbecks Arch Chir Suppl Kongressbd. 1998;115(Suppl I):575–579.
  • Moore C, Shen X-D, Gao F, Fibronectin-alpha4beta1 integrin interactions regulate metalloproteinase-9 expression in steatotic liver ischemia and reperfusion injury. Am J Pathol. 2007;170(2):567–577.
  • Amersi F, Shen X-D, Moore C, Fibronectin-alpha 4 beta 1 integrin-mediated blockade protects genetically fat Zucker rat livers from ischemia/reperfusion injury. Am J Pathol. 2003;162(4):1229–1239.
  • Moore C, Shen XD, Fondevila C, Fibronectin-alpha4beta1 integrin interactions modulate p42/44 MAPK phosphorylation in steatotic liver cold ischemia-reperfusion injury. Transplant Proc. 2005;37(1): 432–434.
  • Koti RS, Yang W, Dashwood MR, Effect of ischemic preconditioning on hepatic microcirculation and function in a rat model of ischemia reperfusion injury. Liver Transpl. 2002;8(12):1182–1191.
  • Serafín A, Roselló-Catafau J, Prats N, Ischemic preconditioning affects interleukin release in fatty livers of rats undergoing ischemia/reperfusion. Hepatology. 2004;39(3):688–698.
  • Burke A, Lucey MR. Non-alcoholic fatty liver disease, non-alcoholic steatohepatitis and orthotopic liver transplantation. Am J Transplant. 2004;4(5):686–693.
  • Baldwin D, Chandrashekhar Y, McFalls E, Ischemic preconditioning prior to aortic cross-clamping protects high-energy phosphate levels, glucose uptake, and myocyte contractility. J Surg Res. 2002;105(2):153–159.
  • Duarte S, Shen XD, Fondevila C, Fibronectin-α4β1 interactions in hepatic cold ischemia and reperfusion injury: regulation of MMP-9 and MT1-MMP via the p38 MAPK pathway. Am J Transplant. 2012;12:2689–2699.
  • Zhai Y, Petrowsky H, Hong JC, Ischaemia-reperfusion injury in liver transplantation–from bench to bedside. Nat Rev Gastroenterol Hepatol. 2013;10:79–89.
  • Koti RS, Yang W, Dashwood MR, Effect of ischemic preconditioning on hepatic microcirculation and function in a rat model of ischemia reperfusion injury. Liver Transpl. 2002;8(12):1182–1191.
  • Lloris-Carsí JM, Cejalvo D, Toledo-Pereyra LH, Preconditioning: effect upon lesion modulation in warm liver ischemia. Transplant Proc. 1993;25:3303–3304
  • Hardy KJ, Tancheroen S, Shulkes A. Comparison of continuous versus intermittent ischaemia-reperfusion during liver resection in an experimental model. Br J Surg. 1995;82(6):833–836.
  • Isozaki H, Adam R, Gigou M, Experimental study of the protective effect of intermittent hepatic pedicle clamping in the rat. Br J Surg. 1992;79(4):310–313.
  • Horiuchi T, Muraoka R, Tabo T, Optimal cycles of hepatic ischemia and reperfusion for intermittent pedicle clamping during liver surgery. Arch Surg. 1995;130(7):754–758.
  • http://www.cdc.gov/nccdphp/dnpa/obesity/.
  • White BD, Martin RJ. Evidence for a central mechanism of obesity in the Zucker rat: role of neuropeptide Y and leptin. Proc Soc Exp Biol Med. 1997;214(3):222–232.
  • Amersi F, Farmer DG, Shaw GD, P-selectin glycoprotein ligand-1 (rPSGL-Ig)-mediated blockade of CD62 selectin molecules protects rat steatotic liver grafts from ischemia/reperfusion injury. Am J Transplant. 2002;2(7):600–608.
  • Coito AJ, Buelow R, Shen X-D, Heme oxygenase-1 gene transfer inhibits inducible nitric oxide synthase expression and protects genetically fat Zucker rat livers from ischemia-reperfusion injury. Transplantation. 2002;74(1):96–102.
  • Saidi RF, Chang J, Brooks S, Ischemic preconditioning and intermittent clamping increase the tolerance of fatty liver to hepatic ischemia-reperfusion injury in the rat. Transplant Proc. 2007;39(10):3010–3014.
  • El-Badry AM, Moritz W, Contaldo C, Prevention of reperfusion injury and microcirculatory failure in macrosteatotic mouse liver by omega-3 fatty acids. Hepatology. 2007;45(4):855–863.
  • McCormack L, Dutkowski P, El-Badry AM, Liver transplantation using fatty livers: always feasible? J Hepatol. 2011;54(5):1055–1062.
  • Chavin KD, Fiorini RN, Shafizadeh S, Fatty acid synthase blockade protects steatotic livers from warm ischemia reperfusion injury and transplantation. Am J Transplant. 2004;4(9):1440–1447.
  • Net M, Valero R, Almenara R, The effect of normothermic recirculation is mediated by ischemic preconditioning in NHBD liver transplantation. Am J Transplant. 2005;5(10):2385–2392.
  • Minor T, Akbar S, Yamamoto Y. Adenosine A2 receptor stimulation protects the predamaged liver from cold preservation through activation of cyclic adenosine monophosphate-protein kinase A pathway. Liver Transpl. 2000;6(2):196–200.
  • Horstick G, Berg O, Heimann A, Application of C1-esterase inhibitor during reperfusion of ischemic myocardium: dose-related beneficial versus detrimental effects. Circulation. 2001;104(25):3125–3131.
  • Fu J, Lin G, Wu Z, Anti-apoptotic role for C1 inhibitor in ischemia/reperfusion-induced myocardial cell injury. Biochem Biophys Res Commun. 2006;349(2):504–512.
  • Hill J, Lindsay TF, Ortiz F, Soluble complement receptor type 1 ameliorates the local and remote organ injury after intestinal ischemia-reperfusion in the rat. J Immunol. 1992;149(5):1723–1728.
  • Heijnen BHM, Straatsburg IH, Padilla ND, Inhibition of classical complement activation attenuates liver ischaemia and reperfusion injury in a rat model. Clin Exp Immunol. 2006;143(1):15–23.
  • Lehmann TG, Heger M, Münch S, In vivo microscopy reveals that complement inhibition by C1-esterase inhibitor reduces ischemia/reperfusion injury in the liver. Transpl Int. 2000;13 (Suppl 1):S547–550.
  • Chan RK, Ibrahim SI, Verna N, Ischaemia-reperfusion is an event triggered by immune complexes and complement. Br J Surg. 2003;90(12):1470–1478.
  • Inderbitzin D, Beldi G, Avital I, Local and remote ischemia-reperfusion injury is mitigated in mice overexpressing human C1 inhibitor. Eur Surg Res. 2004;36(3):142–147.
  • Straatsburg IH, Boermeester MA, Wolbink GJ, Complement activation induced by ischemia-reperfusion in humans: a study in patients undergoing partial hepatectomy. J Hepatol. 2000;32(5):783–791.
  • Meyer zu Vilsendorf A, Link C, Jörns A, Preconditioning with the prostacyclin analog epoprostenol and cobra venom factor prevents reperfusion injury and hyperacute rejection in discordant liver xenotransplantation. Xenotransplantation. 2001;8(1):41–47.
  • Bergamaschini L, Gobbo G, Gatti S, Endothelial targeting with C1-inhibitor reduces complement activation in vitro and during ex vivo reperfusion of pig liver. Clin Exp Immunol. 2001;126(3):412–420.
  • Caliezi C, Wuillemin WA, Zeerleder S, C1-Esterase inhibitor: an anti-inflammatory agent and its potential use in the treatment of diseases other than hereditary angioedema. Pharmacol Rev. 2000;52(1):91–112.
  • Suzuki S, Nakamura S, Koizumi T, The beneficial effect of a prostaglandin I2 analog on ischemic rat liver. Transplantation. 1991;52(6):979–983.
  • Davis AE 3rd, Mejia P, Lu F. Biological activities of C1 inhibitor. Mol Immunol. 2008;45(16):4057–4063.
  • Fausto N. Liver regeneration. J Hepatol. 2000;32(1 Suppl):19–31.
  • Michalopoulos GK, DeFrances MC. Liver regeneration. Science. 1997;276(5309):60–66.
  • Guo JT, Zhou H, Liu C, Apoptosis and regeneration of hepatocytes during recovery from transient hepadnavirus infections. J Virol. 2000;74(3):1495–1505.
  • Schieferdecker HL, Schlaf G, Koleva M, Induction of functional anaphylatoxin C5a receptors on hepatocytes by in vivo treatment of rats with IL-6. J Immunol. 2000;164(10):5453–5458.
  • Saidi RF, Walter O, Rajeshkumar B, Human C1-esterase inhibitor attenuates liver ischemia-reperfusion injury and promotes regeneration. J Surg Res. 2014;187:660–666.
  • Almeida-Porada G, Zanjani ED, Porada CD. Bone marrow stem cells and liver regeneration. Exp Hematol. 2010;38(7):574–580.
  • Ishikawa T, Banas A, Hagiwara K, Stem cells for hepatic regeneration: the role of adipose tissue derived mesenchymal stem cells. Curr Stem Cell Res Ther. 2010;5(2):182–189.
  • Di Bonzo LV, Ferrero I, Cravanzola C, Human mesenchymal stem cells as a two-edged sword in hepatic regenerative medicine: engraftment and hepatocyte differentiation versus profibrogenic potential. Gut. 2008;57(2):223–231.
  • Saidi RF, Walter O, Rajeshkumar B, Human adipose derived mesenchymal stem cells attenuates liver ischemia-reperfusion injury and promotes liver regeneration. American Journal of Transplantation 2013;13(S5): 413
  • Kuboki S, Sakai N, Tschöp J, Distinct contributions of CD4+ T cell subsets in hepatic ischemia/reperfusion injury. Am J Physiol Gastrointest Liver Physiol. 2009;296(5):G1054–1059.
  • Farhood A, McGuire GM, Manning AM, Intercellular adhesion molecule 1 (ICAM-1) expression and its role in neutrophil-induced ischemia-reperfusion injury in rat liver. J Leukoc Biol. 1995;57:368–374.
  • Kiuchi T, Oldhafer KJ, Schlitt HJ, Background and prognostic implications of perireperfusion tissue injuries in human liver transplants: a panel histochemical study. Transplantation 1998;66:737–747.
  • Scoazec JY, Durand F, Degott C, Expression of cytokine-dependent adhesion molecules in postreperfusion biopsy specimens of liver allografts. Gastroenterology 1994;107:1094–102.
  • Nakano H, Kuzume M, Namatame K, Efficacy of intraportal injection of anti-ICAM-1 monoclonal antibody against liver cell injury following warm ischemia in the rat. Am J Surg. 1995;170:64–66.
  • Vollmar B, Glasz J, Menger MD, Leukocytes contribute to hepatic ischemia/reperfusion injury via intercellular adhesion molecule-1-mediated venular adherence. Surgery. 1995;117:195–200.
  • Monbaliu D, Brassil J. Machine perfusion of the liver: past, present and future. Curr Opin Organ Transplant. 2010;15(2):160–166.
  • Starzl TE, Groth CG, Brettschneider L, Extended survival in 3 cases of orthotopic homotransplantation of the human liver. Surgery. 1968;63(4):549–563.
  • Vogel T, Brockmann JG, Friend PJ. Ex-vivo normothermic liver perfusion: an update. Curr Opin Organ Transplant. 2010;15(2):167–172.
  • Imber CJ, St Peter SD, Lopez de Cenarruzabeitia I, Advantages of normothermic perfusion over cold storage in liver preservation. Transplantation. 2002;73(5):701–709.
  • Reddy S, Greenwood J, Maniakin N, Non-heart-beating donor porcine livers: the adverse effect of cooling. Liver Transpl. 2005;11(1):35–38.
  • Schön MR, Kollmar O, Wolf S, Liver transplantation after organ preservation with normothermic extracorporeal perfusion. Ann Surg. 2001;233(1):114–123.
  • García-Valdecasas JC, Fondevila C. In-vivo normothermic recirculation: an update. Curr Opin Organ Transplant. 2010;15(2):173–176.
  • Valero R, García-Valdecasas JC, Net M, L-arginine reduces liver and biliary tract damage after liver transplantation from non-heart-beating donor pigs. Transplantation. 2000;70(5):730–737.
  • Lee CY, Jain S, Duncan HM, Survival transplantation of preserved non-heart-beating donor rat livers: preservation by hypothermic machine perfusion. Transplantation. 2003;76(10):1432–1436.
  • Dutkowski P, Furrer K, Tian Y, Novel short-term hypothermic oxygenated perfusion (HOPE) system prevents injury in rat liver graft from non-heart beating donor. Ann Surg. 2006;244(6):968–976; discussion 976–977.
  • Bessems M, Doorschodt BM, Van Marle J, Improved machine perfusion preservation of the non-heart-beating donor rat liver using Polysol: a new machine perfusion preservation solution. Liver Transpl. 2005;11(11):1379–1388.
  • Rojas A, Chen L, Bartlett RH, Assessment of liver function during extracorporeal membrane oxygenation in the non-heart beating donor swine. Transplant Proc. 2004;36(5):1268–1270.
  • Wang C-C, Wang S-H, Lin C-C, Liver transplantation from an uncontrolled non-heart-beating donor maintained on extracorporeal membrane oxygenation. Transplant Proc. 2005;37(10):4331–4333.
  • Vekemans K, Liu Q, Brassil J, Influence of flow and addition of oxygen during porcine liver hypothermic machine perfusion. Transplant Proc. 2007;39(8):2647–2651.
  • Pringle JH. V. Notes on the arrest of hepatic hemorrhage due to trauma. Ann Surg. 1908;48(4):541–549.
  • Belghiti J, Noun R, Zante E, Portal triad clamping or hepatic vascular exclusion for major liver resection. A controlled study. Ann Surg. 1996;224(2):155–161.
  • Man K, Fan ST, Ng IO, Prospective evaluation of Pringle maneuver in hepatectomy for liver tumors by a randomized study. Ann Surg. 1997;226(6):704–711; discussion 711–713.
  • Terblanche J, Krige JE, Bornman PC. Simplified hepatic resection with the use of prolonged vascular inflow occlusion. Arch Surg. 1991;126(3):298–301.
  • Cunningham JD, Fong Y, Shriver C, One hundred consecutive hepatic resections. Blood loss, transfusion, and operative technique. Arch Surg. 1994;129(10): 1050–1056.
  • Bismuth H, Castaing D, Garden OJ. Major hepatic resection under total vascular exclusion. Ann Surg. 1989;210(1):13–19.
  • Belghiti J, Noun R, Malafosse R, Continuous versus intermittent portal triad clamping for liver resection: a controlled study. Ann Surg. 1999;229(3):369–375.
  • Makuuchi M, Mori T, Gunvén P, Safety of hemihepatic vascular occlusion during resection of the liver. Surg Gynecol Obstet. 1987;164(2):155–158.
  • Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation. 1986;74(5):1124–1136.
  • Peralta C, Closa D, Hotter G, Liver ischemic preconditioning is mediated by the inhibitory action of nitric oxide on endothelin. Biochem Biophys Res Commun. 1996;229(1):264–270.
  • Hardy KJ, McClure DN, Subwongcharoen S. Ischaemic preconditioning of the liver: a preliminary study. Aust N Z J Surg. 1996;66(10):707–710.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.