Protective effect of ischemic preconditioning against intermittent warm-ischemia-induced liver injury

Journal of Surgical Research

Volumn 107, Issue 1, 2002, Pages 82-92

  Iwasaki, Yoshimi ^a   Tagaya, Nobumi ^a   Hattori, Yoshiyuki ^a   Yamaguchi, Keiichiro ^a   Kubota, Keiichi ^a  

^a DOKKYO MEDICAL UNIVERSITY   (Japan)

Author keywords

Apoptosis; Hepatic pedicle clamping (Pringle's maneuver); Intermittent ischemia; Ischemia reperfusion; Ischemic preconditioning; Necrosis; Tumor necrosis factor

Indexed keywords

AMINOTRANSFERASE; LACTIC ACID; TUMOR NECROSIS FACTOR ALPHA;

AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; HEART INFARCTION PREVENTION; HISTOPATHOLOGY; LACTATE BLOOD LEVEL; LIVER INJURY; LIVER ISCHEMIA; LIVER NECROSIS; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; REPERFUSION; SURGICAL TECHNIQUE; TREATMENT OUTCOME;

EID: 0036401208     PISSN: 00224804     EISSN: None     Source Type: Journal    
DOI: 10.1006/jsre.2002.6505     Document Type: Article

References (36)

1. Pringle, J. H. Notes on the arrest of hepatic hemorrhage due to trauma. Ann. Surg. 48: 541, 1908.
2. Belghiti, J., Noun, R., Malafosse, R., Jagot, P., Sauvanet, A., Pierangeli, F., Marty, J., and Farges, O. Continuous versus intermittent portal triad clamping for liver resection: A controlled study. Ann. Surg. 229: 369, 1999.
3. Belghiti, J., Di Carlo, I., Sauvanet, A., Uribe, M., and Fekete, F. A ten-year experience with hepatic resection in 338 patients: Evolutions in indications and of operative mortality. Eur. J. Surg. 160: 277, 1994.
4. Liu, D. L., Jeppsson, B., Hakansson, C. H., and Odselius, R. Multiple-system organ damage resulting from prolonged hepatic inflow interruption. Arch. Surg. 131: 442, 1996.
5. Hardy, K. J., Tancheroen, S., and Shulkes, A. Comparison of continuous versus intermittent ischemia-reperfusion during liver resection in an experimental model. Br. J. Surg. 82: 833, 1995.
6. Makuuchi, M., Mori, T., Gunvén, P., Yamazaki, S., and Hasegawa, H. Safety of hemihepatic vascular occlusion during resection of the liver. Surg. Gynecol. Obstet. 164: 155, 1987.
7. Murry, C. E., Jennings, R. B., and Reimer, K. A. Preconditioning with ischemia: A delay of lethal cell injury in ischemic myocardium. Circulation 74: 1124, 1986.
8. Peralta, C., Hotter, G., Closa, D., Gelpí, E., Bulbena, O., and Rosell ó-Catafau, J. Protective effect of preconditioning on the injury associated to hepatic ischemia-reperfusion in the rat: Role of nitric oxide and adenosine. Hepatology 25: 934, 1997.
9. Kume, M., Yamamoto, Y., Saad, S., Gomi, T., Kimoto, S., Shimabukuro, T., Yagi, T., Nakagami, M., Takada, Y., Morimoto, T., and Yamaoka, Y. Ischemic preconditioning of the liver in rats: Implications of heat shock protein induction to increase tolerance of ischemia-reperfusion injury. J. Lab. Clin. Med. 128: 251, 1996.
10. Peralta, C., Closa, D., Xaus, C., Gelpí, E., Roselló-Catafau, J., and Hotter, G. Hepatic preconditioning in rats is defined by a balance of adenosine and xanthine. Hepatology 28: 768, 1998.
11. Peralta, C., Fernández, L., Panés, J., Prats, N., Sans, M., Piqué, J. M., Gelpí, E., and Roselló-Catafau, J. Preconditioning protects against systemic disorders associated with hepatic ischemia-reperfusion through blockade of tumor necrosis factor-induced P-selectin up-regulation in the rat. Hepatology 33: 100, 2001.
12. Clavien, P. A., Yadav, S., Sindram, D., and Bentley, R. C. Protective effects of ischemic preconditioning for liver resection performed under inflow occlusion in humans. Ann. Surg. 232: 155, 2000.
13. Lamprecht, W., and Trautschold, I. Adenosine-5′-triphosphate: Determination with hexokinase and glucose-6-phosphate dehydrogenase. In H. U. Bergmeyer (Ed.), Methods of Enzymatic Analysis (Vol. 4), 2nd ed. New York/London: Academic Press, 1974. Pp. 2101-2110.
14. Jaworek, D., Gruber, W., and Bergmeyer, H. U. Adenosine-5′-diphosphate and adenosine-5′-monophosphate. In H. U. Bergmeyer (Ed.), Methods of Enzymatic Analysis (Vol. 4), 2nd ed. New York/London: Academic Press, 1974. Pp. 2127-2131.
15. Atkinson, D. E. The energy charge of the adenylate pool as a regulatory parameter: Interaction with feedback modifiers. Biochemistry 7: 4030, 1968.
16. Camargo, C. A. Jr., Madden, J. F., Gao, W., Selvan, R. S., and Clavien, P. A. Interleukin-6 protects liver against warm ischemia/reperfusion injury and promotes hepatocyte proliferation in the rodent. Hepatology 26: 1513, 1997.
17. Elias, D., Desruennes, E., and Lasser, P. Prolonged intermittent clamping of the portal triad during hepatectomy. Br. J. Surg. 78: 42, 1991.
18. Man, K., Fan, S. T., Ng, I. O., Lo, C. M., Liu, C. L., and Wong, J. Prospective evaluation of Pringle maneuver in hepatectomy for liver tumors by a randomized study. Ann. Surg. 226: 704, 1997.
19. Franco, D., Smadja, C., Meakins, J. L., Wu, A., Berthoux, L., and Grange, D. Improved early results of elective hepatic resection for liver tumors. One hundred consecutive hepatectomies in cirrhotic and non cirrhotic patients. Arch. Surg. 124: 1033, 1989.
20. 3 accumulation and cell killing in isolated rat hepatocytes exposed to hypoxia. Hepatology 31: 166, 2000.
21. Kohli, V., Madden, J. F., Bentley, R. C., and Clavien, P. A. Calpain mediates ischemic injury of the liver through modulation of apoptosis and necrosis. Gastroenterology 116: 168, 1999.
22. Horiuchi, T., Muraoka, R., Tabo, T., Uchinami, M., Kimura, N., and Tanigawa, N. Optimal cycles of hepatic ischemia and reperfusion for intermittent pedicle clamping during liver surgery. Arch. Surg. 130: 754, 1995.
23. Iu, S., Harvey, P. R., Makowka, L., Petrunka, C. N., Ilson, R. G., and Strasberg, S. M. Markers of allograft viability in the rat: Relationship between transplantation viability and liver function in the isolated perfused liver. Transplantation 44: 562, 1987.
24. Squadrito, F., Altavilla, D., Zingarelli, B., Ioculano, M., Calapai, G., Campo, G. M., Miceli, A., and Caputi, A. P. Tumor necrosis factor involvement in myocardial ischaemia-reperfusion injury. Eur. J. Pharmacol. 237: 223, 1993.
25. Donnahoo, K. K., Shames, B. D., Harken, A. H., and Meldrum, D. R. Review article: The role of tumor necrosis factor in renal ischemia-reperfusion injury. J. Urology 162: 196, 1999.
26. Colletti, L. M., Remick, D. G., Burtch, G. D., Kunkel, S. L., Strieter, R. M., and Campbell, D. A., Jr. Role of tumor necrosis factor-alpha in the pathophysiologic alterations after hepatic ischemia/reperfusion injury in the rat. J. Clin. Invest. 85: 1936, 1990.
27. Kimura, N., Muraoka, R., Horiuchi, T., Tabo, T., Uchinami, M., Yokomachi, J., and Doi, K. Intermittent hepatic pedicle clamping reduces liver and lung injury. J. Surg. Res. 78: 11, 1998.
28. Peralta, C., Prats, N., Xaus, C., and Gelpí, E. Protective effect of liver ischemic preconditioning on liver and lung injury by hepatic ischemia-reperfusion in the rat. Hepatology 30: 1481, 1999.
29. Essani, N. A., Bajt, M. L., Farhood, A., Vonderfecht, S. L., and Jaeschke, H. Transcriptional activation of vascular cell adhesion molecule-1 gene in vivo and its role in the pathophysiology of neutrophil-induced liver injury in murine endotoxin shock. J. Immunol. 158: 5941, 1997.
30. Rath, P. C., and Aggarwal, B. B. TNF-induced signaling in apoptosis. J. Clin. Immunol. 19: 350, 1999.
31. Zepletal, C., Maksan, S. M., Lehmann, T., Guenther, L., Fallsehr, C., Mehrabi, A., Weiss, G., Golling, M., Gebhard, M. M., Herfarth, C., and Klar, E. Ischemic preconditioning improves liver microcirculation after ischemia/reperfusion. Transplant. Proc. 31: 3260, 1999.
32. Kohli, V., Selzner, M., Madden, J. F., Bentley, R. C., and Clavien, P. A. Endothelial cell and hepatocyte deaths occur by apoptosis after ischemia-reperfusion injury in the rat liver. Transplantation 67: 1099, 1999.
33. Yadav, S. S., Sindram, D., Perry, D. K., and Clavien, P. A. Ischemic preconditioning protects the mouse liver by inhibition of apoptosis through a caspase-dependent pathway. Hepatology 30: 1223, 1999.
34. Leist, M., and Nicotera, P. The shape of cell death. Biochem. Biophys. Res. Commun. 236: 1, 1997.
35. Eguchi, Y., Shimizu, S., and Tsujimoto, Y. Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res. 57: 1835, 1997.
36. Leist, M., Single, B., Castoldi, A. F., Kuhnle, S., and Nicotera, P. Intracellular adenosine triphosphate (ATP) concentration: A switch in the decision between apoptosis and necrosis. J. Exp. Med. 185: 1481, 1997.