Abstract
Aim
The aim of this study was to investigate a possible preconditioning effect of oral diet enriched with polyunsaturated fatty acids (PUFAs) on liver ischemia/reperfusion (I/R) injuries.
Methods
Wistar male rats were fed a standard diet or polyunsaturated fatty acid-rich diet (PRD) enriched with (GII) or without (GIII) ω-3 PUFA. Rats were submitted to partial liver ischemia during 1 h and evaluated in pre- and post-I/R conditions. In pre-I/R condition, livers were collected for determination of fatty acid composition, liver mitochondrial function, malondialdehyde (MDA) content, and histological analysis. Four hours after liver reperfusion serum activities of aspartate aminotransferase (AST) and alanine aminotransferase (ALT), serum levels of tumor necrosis factor-alpha, interleukin-6, interleukin-10, and prostaglandin-E2, liver mitochondrial function, MDA content, and histology were evaluated.
Results
In the pre-I/R condition, GII and GIII groups had an increase on PUFA content and exhibited slight increased macrosteatosis and microsteatosis in the liver. After 4 h of reperfusion, PRD-fed rats showed a marked decrease on steatosis, diminished necrosis, an increase in MDA formation, and mitochondrial uncoupling. We also observed a marked decrease in plasma levels of cytokines and ALT and AST activities in post-I/R condition in PRD groups.
Conclusion
In this experimental model in the rat, PRD has a preconditioning effect protecting the liver from I/R injury and should be object of future clinical studies.
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References
Serracino-Inglott F, Habib NA, Mathie RT. Hepatic ischemia-reperfusion injury. Am J Surg. 2001; 181:160–166.
Selzner M, Clavien PA. Fatty liver in liver transplantation and surgery. Semin Liver Dis 2001; 21:105–113.
Trevisani F, Caraceni P, Simoncini M, Micati M, Domenicali M, Dazzani F, Zambruni A, Stefanelli C, Grazi G, Nardo B, Guarnieri C, Bernardi M. Evidence of oxidative imbalance in long-term liver transplant patients. Dig Liver Dis 2002; 34:279–284.
Huguet C, Addario-Chieco P, Gavelli A, Arrigo E, Harb J, Clement RR. Technique of hepatic vascular exclusion for extensive liver resection. Am J Surg 1992, 163:602–605.
Powner DJ. Factors during donor care that may affect liver transplantation outcome. Prog Transplant 2004, 14:241–247.
Montalvo-Jave EE, Escalante-Tattersfield T, Ortega-Salgado JA, Piña E, Geller DA. Factors in the pathophysiology of the liver ischemia-reperfusion injury. J Surg Res. 2008; 147:153–159.
Jassem W, Fuggle SV, Rela M, Koo DD, Heaton ND. The role of mitochondria in ischemia/reperfusion injury. Transplantation. 2002 73:493–499.
Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 1986; 74:1124–1136.
Nilsson B, Friman S, Gustafsson BI, Delbro DS. Preconditioning protects against ischemia/reperfusion injury of the liver. J Gastrointest Surg 2000; 4:44–49.
Ambros JT, Herrero-Fresneda I, Borau OG. Ischemic preconditioning in solid organ transplantation: from experimental to clinics. Transpl Int 2007; 20:219–229.
Montalvo-Jave EE, Piña E, Montalvo-Arenas C, Urrutia R, Benavente-Chenhalls L, Peña-Sanchez J, Geller DA. Role of ischemic preconditioning in liver surgery and hepatic transplantation. J Gastrointest Surg 2009; 13:2074–2083.
Janoff A. Alterations in lysosomes (intracellular enzymes) during shock: effects of preconditioning (tolerance) and protective drugs. Int Anesthesiol Clin 1964; 2:251–269.
Sack MN. Mitochondrial depolarization and the role of uncoupling proteins in ischemia tolerance. Cardiovasc Res 2006; 72:210–219.
Dirnagl U, Meisel A. Endogenous neuroprotection: mitochondria as gateways to cerebral preconditioning? Neuropharmacology 2008; 55:334–344.
Cortez-Pinto H, Zhi Lin H, Qi Yang S, Odwin Da Costa S, Diehl AM. Lipids up-regulate uncoupling protein 2 expression in rat hepatocytes. Gastroenterology 1999; 116:1184–1193.
Institute of Laboratory Animal Resources, Comission on Life Sciences, National Research Council. Guide for the care and use of laboratory animals. (1996) 7th ed. Washington (DC): National Academy Press.
Yoshizumi T, Yanaga K, Soejima Y, Maeda T, Uchiyama H, Sugimachi K. Amelioration of liver injury by ischaemic preconditioning. Br J Surg 1998; 85:1636–1640.
Figueira ER, Bacchella T, Coelho AM, Sampietre SN, Leitão RM, Machado MC. Timing-dependent protection of hypertonic saline solution administration in experimental liver ischemia/reperfusion injury. Surgery 2010; 147:415–423.
Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957; 226:497–509.
Abushufa R, Reed P, Weinkove C. Fatty acids in erythrocytes measured by isocratic HPLC. Clin Chem 1994; 40:1707–1712.
Coelho AM, Machado MC, Sampietre SN, Leite KR, Oliveira VL, Pinotti HW. Hepatic damage during acute pancreatitis in the rat. Braz J Med Biol Res 1977; 30:947–953.
Estabrook RW. Mitochondrial respiratory control and the polarographic measurement of ADP/O ratios. In: Methods in Enzymology. New York: Academic Press;1967. p.41-47.
Chance B, Williams GR. A simple and rapid assay of oxidative phosphorylation. Nature 1955; 175:1120–1121.
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951; 193:265–275.
Soriano FG, Liaudet L, Szabó E, Virág L, Mabley JG, Pacher P, Szabó C. Resistance to acute septic peritonitis in poly(ADP-ribose) polymerase-1-deficient mice. Shock 2002; 17:286–292.
Quireze C, Montero EF, Leitao RM, Juliano Y, Fagundes DJ, Poli-de-Figueredo LF. Ischemic preconditioning prevents apoptotic cell death and necrosis in early and intermediate phases of liver ischemia-reperfusion injury in rats. J Invest Surg 2006; 19: 229–236.
Frongillo F, Avolio AW, Nure E, Mulè A, Pepe G, Magalini SC. Quantification of degree of steatosis in extended criteria donor grafts with standardized histologic techniques: implications for graft survival. Transplant Proc 2009; 41:1268–1272.
Lang, G. and Michael, G. In: Methods of Enzymatic Analysis. New York: Academic Press. 1974
Correia SC, Santos RX, Perry G, Zhu X, Moreira PI, Smith MA. Mitochondria: the missing link between preconditioning and neuroprotection. J Alzheimers Dis 2010; 20:S475-485.
Ravati A, Ahlemeyer B, Becker A, Klumpp S, Krieglstein J. Preconditioning-induced neuroprotection is mediated by reactive oxygen species and activation of the transcription factor nuclear factor-kappaB. J Neurochem 2001; 78:909–919.
Ravati A, Ahlemeyer B, Becker A, Krieglstein J. Preconditioning-induced neuroprotection is mediated by reactive oxygen species. Brain Res 2000; 866:23–32.
Simerabet M, Robin E, Aristi I, Adamczyk S, Tavernier B, Vallet B, Bordet R, Lebuffe G. Preconditioning by an in situ administration of hydrogen peroxide: involvement of reactive oxygen species and mitochondrial ATP-dependent potassium channel in a cerebral ischemia-reperfusion model. Brain Res 2008; 1240:177–184.
Tang L, Tian F, Tao W, Cui J. Hepatocellular glycogen in alleviation of liver ischemia-reperfusion injury during partial hepatectomy. World J Surg, 2007; 31:2039–2043.
Selzner M, Selzner N, Jochum W, Graf R, Clavien PA. Increased ischemic injury in old mouse liver: an ATP-dependent mechanism. Liver Transpl 2007; 13: 382–390.
Bilzer M, Jaeschke H, Vollmar AM, Paumgartner G, Gerbes AL. Prevention of Kupffer cell-induced oxidant injury in rat liver by atrial natriuretic peptide. Am J Physiol 1999; 276:G1137-1144.
Lentsch AB, Kato A, Yoshidome H, McMasters KM, Edwards MJ. Inflammatory mechanisms and therapeutic strategies for warm hepatic ischemia/reperfusion injury. Hepatology. 2000 Aug;32(2):169–73
Wheeler M.D. Endotoxin and Kupffer cell activation in alcoholic liver disease. Alcohol Res Health 2003; 27:300–306.
Sadeghi S, Wallace FA, Calder PC. Dietary lipids modify the cytokine response to bacterial lipopolysaccharide in mice. Immunology 1999; 96:404–410.
Zhong Z, Thurman RG. A fish oil diet minimizes hepatic reperfusion injury in the low-flow, reflow liver perfusion model. Hepatology 1995; 22:929–935.
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.
Iwata K, Shimazu M, Wakabayashi G, Ohshima A, Yoshida M, Kitajima M. Intraportal perfusion of prostaglandin E1 attenuates hepatic postischaemic microcirculatory impairments in rats. J Gastroenterol Hepatol 1999; 14:634–641.
Matsuo K, Togo S, Sekido H, Morita T, Kamiyama M, Morioka D, Kubota T, Miura Y, Tanaka K, Ishikawa T, Ichikawa Y, Endo I, Goto H, Nitanda H, Okazaki Y, Hayashizaki Y, Shimada H. Pharmacologic preconditioning effects: prostaglandin E1 induces heat-shock proteins immediately after ischemia/reperfusion of the mouse liver. J Gastrointest Surg 2005; 9: 758–768.
Natori S, Fujii Y, Kurosawa H, Nakano A, Shimada H. Prostaglandin E1 protects against ischemia-reperfusion injury of the liver by inhibition of neutrophil adherence to endothelial cells. Transplantation 1997; 64:1514–1520.
Iwasaki W, Kume M, Kudo K, Uchinami H, Kikuchi I, Nakagawa Y, Yoshioka M, Yamamoto Y. Changes in the fatty acid composition of the liver with the administration of N-3 polyunsaturated fatty acids and the effects on warm ischemia/reperfusion injury in the rat liver. Shock 2010; 33:306–314.
Kim YI, Kai T, Kitano S, Ishii T, Tatsuma T, Kamada N, Sugimachi K. Hepatoprotection by a PGI2 analogue in complete warm ischemia of the pig liver. Prostanoid release from the reperfused liver. Transplantation 1994; 58: 875–879.
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The authors are indebted to the technical assistance of Nilza Molan and Alcione Lescano.
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This work was presented at the 52nd Annual Meeting of the Society for Surgery of the Alimentary Tract on May 2011, in Chicago, IL.
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Coelho, A.M.M., Machado, M.C.C., Takahashi, H.K. et al. Ischemic Preconditioning-Like Effect of Polyunsaturated Fatty Acid-Rich Diet on Hepatic Ischemia/Reperfusion Injury. J Gastrointest Surg 15, 1679–1688 (2011). https://doi.org/10.1007/s11605-011-1648-x
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DOI: https://doi.org/10.1007/s11605-011-1648-x