Local hypothermia during early reperfusion protects skeletal muscle from ischemia-reperfusion injury

Plastic and Reconstructive Surgery

Volumn 111, Issue 1, 2003, Pages 242-250

  Mowlavi, Arian ^a,b   Neumeister, Michael W ^a   Wilhelmi, Bradon J ^a   Song, Yao Hua ^a   Suchy, Hans ^a   Russell, Robert C ^a  

^a SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; NITROBLUE TETRAZOLIUM;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; EDEMA; GRACILIS MUSCLE; HYPOTHERMIA; ISCHEMIA; MALE; MUSCLE FLAP; NEUTROPHIL CHEMOTAXIS; NONHUMAN; OXIDATION REDUCTION POTENTIAL; PRIORITY JOURNAL; RAT; REPERFUSION INJURY; SKELETAL MUSCLE; THERMAL EXPOSURE;

EID: 0037216731     PISSN: 00321052     EISSN: None     Source Type: Journal    
DOI: 10.1097/00006534-200301000-00041     Document Type: Article

References (53)

1. Beris, A. E., Soucacos, P. N., Seaber, A. V., and Urbaniak, J. R. Effects of cold ischemia on reflow patterns in the rat cremaster muscle microcirculation. Int. Angiol. 14: 248, 1995.
2. Bruelli, G. A., and Brunelli, G. R. Tissue changes at different periods of ischemia. Int. Angiol. 14: 253, 1995.
3. Yoshioka, T., Shires, G. T., and Fantini, G. A. Hypothermia relieves oxidative stress in reperfused skeletal muscle following partial ischemia. J. Surg. Res. 53: 408, 1992.
4. Siemionow, M., Romanowski, L., and Lister, G. Leukocyte-depleting effect of hypothermia on muscle flap microcirculation following ischemia-reperfusion injury. J. Hand Surg. (Am.) 18: 963, 1993.
5. Wilson, Y. T., Lepore, D. A., Riccio, M., et al. Mild hypothermia protects against ischemia-reperfusion injury in rabbit skeletal muscle. Br. J. Plast. Surg. 50: 343, 1997.
6. Yabe, Y., Ishiguro, N., Shimizu, T., et al. Morphologic and metabolic study of the effect of oxygenated perfluorochemical perfusion on amputated rabbit limbs. J. Reconstr. Microsurg. 10: 185, 1994.
7. Awerbuck, D., Luong, B., Plyley, M. J., and McKee, N. H. Skeletal muscle form and function after 4 hr ischemia-hypothermia. J. Surg. Res. 57: 480, 1994.
8. Gunnes, S., Ytrehus, K., Sorlie, D., Helgesen, K. G., and Mjos, O. D. Improved energy preservation following gentle reperfusion after hypothermic, ischemic cardioplegia in infarcted rat hearts. Eur. J. Cardiothorac. Surg. 1: 139, 1987.
9. Nagano, K., Gelman, S., Bradley, E. L., and Parks, D. Hypothermia, hepatic oxygen supply-demand, and ischemia-reperfusion injury in pigs. Am. J. Physiol. 258: G910, 1990.
10. Canevari, L., Console, A., Tendi, E. A., et al. Effect of postischemia hypothermia on the mitochondrial damage induced by ischaemia and reperfusion in the gerbil. Brain Res. 817: 241, 1999.
11. Duan, M., Li, D., and Xu, J. Effects of selective head cooling on brain cell membrane activity during post-ischemic reperfusion. Chin. Med. J. 109: 463, 1996.
12. Laptook, A, R., Corbett, R. J., Sterett, R., Burns, D. K., Garcia, D., and Tollefsbol, G. Modest hypothermia provides partial neuroprotection when used for immediate resuscitation after brain ischemia. Pediatr. Res. 42: 17, 1997.
13. Huang, F., Zhou, L., and Yang, G. The effect of extending mild hypothermia on focal cerebral ischemia and reperfusion in the rat. Neurol. Res. 20: 57, 1998.
14. Zhang, R. L., Chopp, M., Chen, H., et al. Post-ischemic (1 hour) hypothermia significantly reduces ischemic cell damage in rats subjected to 2 hours of middle cerebral artery occlusion. Stroke 24: 1235, 1993.
15. Xue, D., Huang, Z. G., Smith, K. E., and Buchan, A. M. Immediate or delayed mild hypothermia prevents focal cerebral infarction. Brain Res. 587: 66, 1992.
16. Carroll, M., and Beek, O. Protection against hippocampal CA1 cell loss by post-ischemic hypothermia is dependent on delay of initiation and duration. Metab. Brain Dis. 7: 45, 1992.
17. Cornejo, C. J., Kierney, P. C., Vedder, N. B., and Winn, R. K. Mild hypothermia during reperfusion reduces injury following ischemia of the rabbit ear. Shock 9: 116, 1998.
18. Wright, J. G., Araki, C. T., Belkin, M., and Hobson, R. W. Postischemic hypothermia diminishes skeletal muscle reperfusion edema. J. Surg. Res. 47: 389, 1989.
19. Wright, J. G., Kerr, J. C., Valeri, C. R., and Hobson, R. W. Regional hypothermia protects against ischemia-reperfusion injury in isolated canine gracilis muscle. J. Trauma 28: 1026, 1988.
20. Wright, J. G., Belkin, M., and Hobson, R. W. Hypothermia and controlled reperfusion: Two non-pharmacological methods which diminish ischemia-reperfusion injury in skeletal muscle. Microcirc. Endothelium Lymphatics 5: 315, 1989.
21. Freeman, R., and King, B. Technique for the performance of the nitro-blue tetrazolium (NBT) test. J. Clin. Pathol. 25: 912, 1972.
22. Kim-Lee, M. H., Stokes, B. T., and McDonald, J. S. Procaine, lidocaine, and hypothermia inhibit calcium paradox in glial cells. Neurosurg. Anesthes. 79: 728, 1994.
23. Michenfelder, J. D., and Milde, J. H. The relationship among canine brain temperature, metabolism, and function during hypothermia. Anesthesiology 75: 130, 1991.
24. Allen, K.L., Busza, A. L., Proctor, E., et al. Controllable graded cerebral ischaemia in the gerbil: Studies of cerebral blood flow and energy metabolism by hydrogen clearance and 31PNMR spectroscopy. N.M.R. Biomed. 6: 181, 1993.
25. Berntman, L., Welsh, F. A., and Harp, J. R. Cerebral protective effect of low-grade hypothermia. Anesthesiology 55: 495, 1981.
26. Cadenas, E., Boveris, A., Ragan, C. I., and Stoppani, A. O. M. Production of superoxide radicals and hydrogen peroxide by NADH-ubiquinone reductase and ubiquinol-cytochrome c reductase from beef-heart mitochondria. Arch. Biochem. Biophys. 180: 248, 1977.
27. Globus, M. Y., Busto, R., Lin, B., et al. Detection of free radical activity during transient global ischaemia and recirculation: Effects of intraischemic brain temperature modulation. J. Neurochem. 65: 1250, 1995.
28. Karibe, H., Chen, S. F., Zarow, G. J., et al. Mild intraischemic hypothermia suppresses consumption of endogenous antioxidants after temporary focal ischemia in rats. Brain Res. 649: 12, 1994.
29. Seida, M., Wagner, H. G., Vass, K., and Klatzo, I. Effect of aminophylline on post-ischemic edema and brain damage in cats. Stroke 19: 1275, 1988.
30. Busto, R., Globus, M. Y., Dietrich, W. D., et al. Effect of mild hypothermia on ischemia-induced release of neurotransmitters and free fatty acids in rat brain. Stroke 20: 904, 1989.
31. Baker, A. J., Zornow, M. H., Grafe, M. R., et al. Hypothermia prevents ischemia-induced release of neurotransmitters and free fatty acids in rat brain. Stroke 22: 666, 1991.
32. Tamura, A., Asano, T., and Sano, K. Correlation between rCBF and histological change following temporary middle cerebral artery occlusion. Stroke 11: 487, 1980.
33. Kuroiwa, T., Shibutani, M., and Okeda, R. Nonhyperemic blood flow restoration and brain edema in experimental focal cerebral ischemia. J. Neurosurg. 70: 73, 1989.
34. Mitsui, Y., Schmelzer, J. D., Zollman, P. J., et al. Hypothermic neuroprotection of peripheral nerve of rats from ischemia-reperfusion injury: Intraischemic vs. reperfusion hypothermia. Brain Res. 827: 63, 1999.
35. Weinrauch, V., Safar, P., Tisherman, S., et al. Beneficial effect of mild hypothermia and detrimental effect of deep hypothermia after cardiac arrest in dogs. Stroke 23: 1454, 1992.
36. Bergstedt, K., Hu, B. R., and Wieloch, T. Postischemic changes in protein synthesis in the rat brain: Effects of hypothermia. Exp. Brain Res. 95: 91, 1993.
37. Armstead, W. M., Mirro, R., Busija, D. W., et al. Post-ischemic generation of superoxide anion by newborn pig brain. Am. J. Physiol. 255: H401, 1988.
38. Dempsey, R. J., Combs, D. J., Maley, M. E., et al. Moderate hypothermia reduces postischemic edema development and leukotriene production. Neurosurgery 21: 177, 1987.
39. Laptook, A. R., Corbett, R. J. T., Ruley, J., et al. Quantitative relationship between brain temperature and energy utilization rate measured in vivo using 31P and 1 H magnetic resonance spectroscopy. Pediatr. Res. 38: 919, 1995.
40. Sapega, A. A., Heppenstall, R. B., Sokolow, D. P., et al. The bioenergetics of preservation in limbs before replantation. J. Bone Joint Surg. (Am.) 70: 1500, 1988.
41. Zhang, J. X., and Wolf, M. B. Effect of cold on ischemia-reperfusion induced microvascular permeability increase in cat skeletal muscle. Cryobiology 31: 94, 1994.
42. Keller, V. A., Pigott, J. D., Flint, L. M., et al. Age-related differences in response to neutrophil-mediated reperfusion injury in the neonatal piglet heart. Surgery 123: 294, 1998.
43. Lawrence, M. B., Smith, C. W., Eskin, S. G., et al. Effect of venous shear stress on CD-18 mediated neutrophil adhesion to cultured endothelium. Blood 75: 227, 1990.
44. Smith, C. W., Marlin, S. D., Rothlein, R., et al. Cooperative interactions of LFA-1 and Mac-1 with intracellular adhesion molecule-1 in facilitating adherence and transendothelial migration of human neutrophils in vitro. J. Clin. Invest. 83: 2008, 1989.
45. Furie, M. B., Tancinco, M. C., and Smith, C. W. Monoclonal antibodies to leukocyte integrins CD11a/CD18 and CD11b/CD18 or intracellular adhesion molecule-1 (ICAM-1) inhibit chemoattractant stimulated neutrophil transendothelial migration in vitro. Blood 78: 2089, 1991.
46. von Andrian, U. H., Chambers, J. D., McEvoy, L. M., et al. Two step model for leukocyte-endothelial cell interaction in inflammation: Distinct roles for LECAM-1 and the leukocyte B-integrins in vivo. Proc. Natl. Acad. Sci. U.S.A. 88: 7538, 1991.
47. Angelis, P., Scharf, S., and Christophidis, N. Effects of age on neutrophil function and its relevance to bacterial infection in the elderly. J. Clin. Lab. Immunol. 49: 33, 1997.
48. Braga, P. C., Sala, M. T., Dal Sasso, M., et al. Influence of age on oxidative bursts (chemiluminescence) of polymorphonuclear neutrophil leukocytes. Gerontology 44: 192, 1998.
49. Johnson, M., Haddix, T., Pohlman, T., et al. Hypothermia reversibly inhibits endothelial cell expression of E-selectin and tissue factor. J. Card. Surg. 10: 428, 1995.
50. Kerrigan, C. L., and Stotland, M. A. Ischemia-reperfusion injury: A review. Microsurgery 14: 165, 1993.
51. Kvietys, P. R., Perry, M. A., and Granger, D. M. Intestinal capillary exchange capacity and oxygen delivery to demand ratio. Am, J. Physiol. 245: G3651, 1983.
52. Kvietys, P. R., Harper, S. L., Korthuis, R. J., and Granger, D. N. Effects of temperature on ileal blood flow and oxygenation. Am. J. Physiol. 249: G246, 1985.
53. Jurkovich, G. J., Pitt, R. M., Curreri, P. W., and Granger, D.N. Hypothermia prevents increased capillary permeability following ischemia-reperfusion injury. J. Surg. Res. 44: 514, 1988.