Optimal depth and duration of mild hypothermia in a focal model of transient cerebral ischemia: Effects on neurologic outcome, infarct size, apoptosis, and inflammation

Stroke

Volumn 29, Issue 10, 1998, Pages 2171-2180

  Maier, Carolina M ^c   Ahern, Kristine V B ^c   Cheng, Ming L ^c   Lee, Jong Eun ^a   Yenari, Midori A ^a   Steinberg, Gary K ^b  

^a STANFORD UNIVERSITY   (United States)

^b STANFORD UNIVERSITY MEDICAL CENTER   (United States)

^c NONE

Author keywords

Apoptosis; Hypothermia; Inflammation; Ischemia; Neuroprotection

Indexed keywords

DNA FRAGMENT; MYELOPEROXIDASE;

ANESTHETIC RECOVERY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN INFARCTION; BRAIN ISCHEMIA; BRAIN TEMPERATURE; CONTROLLED STUDY; INDUCED HYPOTHERMIA; INFLAMMATION; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; REPERFUSION; WARMING;

EID: 0345563285     PISSN: 00392499     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.STR.29.10.2171     Document Type: Article

References (54)

1. Baker CJ, Onesti ST, Solomon RA. Reduction by delayed hypothermia of cerebral infarction following middle cerebral artery occlusion in the rat: a time-course study. J Neurosurg. 1992;77:438-444.
2. Busto R, Dietrich WD, Globus MY-T, Valdes I, Scheinberg P, Ginsberg MD. Small differences in intraischemic brain temperature critically determine the extent of ischemic neuronal injury. J Cereb Blood Flow Metab. 1987;7:729-738.
3. Busto R, Dietrich WD, Globus MY-T, Ginsberg MD. The importance of brain temperature in cerebral ischemic injury. Stroke. 1989;20: 1113-1114.
4. Chen H, Chopp M, Welch KMA. Effect of mild hypothermia on the ischemic infarct volume after middle cerebral artery occlusion in the rat. Neurology. 1991;41:1133-1135.
5. Buchan A, Pulsinelli WA. Hypothermia but not the N-methyl-D-aspartate antagonist MK-801 attenuates neuronal damage in gerbils subjected to transient global ischemia. J Neurosci. 1990;10:311-316.
6. Ginsberg MD, Sternau LL, Globus MY-T, Dietrich WD, Busto R. Therapeutic modulation of brain temperature: relevance to ischemic brain injury. Cerebrovas Brain Metab Rev. 1992;4:189-225.
7. Edwards AD, Yue X, Squier MV, Thoresen M, Cady EB, Penrice J, Cooper CE, Wyatt JS, Reynolds EOR, Mehmet H. Specific inhibition of apoptosis after cerebral hypoxia-ischemia by moderate post-insult hypothermia. Biochem Biophys Res Comm. 1995;217:1193-1199.
8. Toyoda T, Suzuki S, Kassell NF, Lee KS. Intraischemic hypothermia attenuates neutrophil infiltration in the rat neocortex after focal ischemia-reperfusion injury. Neurosurgery. 1996;39:1200-1205.
9. Corbett D, Nurse S, Colbourne F. Hypothermic neuroprotection. A global ischemia study using 18- to 20-month-old gerbils. Stroke. 1997;28: 2238-2242.
10. Colbourne F, Corbett D. Delayed postischemic hypothermia: a six month survival study using behavioral and histological assessments of neuroprotection. J Neurosci. 1995;15:7250-7260.
11. Nurse S, Corbett D. Direct measurement of brain temperature during and after intraischemic hypothermia: correlation with behavioral, physiological, and histological endpoints. J Neurosci. 1994;14:7726-7734.
12. Green EJ, Dietrich WD, van Dijk F, Busto R, Markgraf CG, McCabe P, Ginsberg MD, Schneiderman N. Protective effects of brain hypothermia on behavior and histopathology following global cerebral ischemia in rats. Brain Res. 1992;580:197-204.
13. Yli-Hankala A, Edmonds HLJ, Jiang YD, Higham HE, Zhang PY. Outcome effects of different protective hypothermia levels during cardiac arrest in rats. Acta Anaesthesiol Scand. 1997;41:511-515.
14. Osborne K, Shigeno T, Balarsky A, Ford I, McCulloch J, Teasdale G, Graham D. Quantitative assessment of early brain damage in a rat model of focal cerebral ischemia. J Neurol Neurosurg Psych. 1987;50:402-410.
15. Swanson R, Morton M, Tsao-Wu G, Savalos R, Davidson C, Sharp F. A semiautomated method for measuring brain infarct volume. J Cereb Blood Flow Metab. 1990;10:290-293.
16. Lee JE, Kim CY, Giaccia AJ, Giffard RG. The E6 and E7 genes of human papilloma virus-type 16 protects primary astrocyte cultures from injury. Brain Res. In press.
17. Simonian NA, Getz RL, Leveque JC, Konradi C, Coyle JT. Kainic acid induces apoptosis in neurons. Neuroscience. 1996;75:1047-1055.
18. Marion DW, Penrod LE, Kelsey SF, Obrist WD, Kochanek PM, Palmer AM, Wisniewski SR, DeKoski ST. Treatment of traumatic brain injury with moderate hypothermia. N Engl J Med. 1997;336:540-546.
19. Schwab S, Spranger M, Aschoff A, Steiner T, Hacke W. Brain temperature monitoring and modulation in patients with severe MCA infarction. Neurology. 1997;48:762-767.
20. Goto Y, Kassell NF, Hiramatsu K, Soleau SW, Lee KS. Effects of intraischemic hypothermia on cerebral damage in a model of reversible focal ischemia. Neurosurgery. 1993;32:980-984.
21. Memezasa J, Smith M-L. Penumbral tissues salvaged by reperfusion following middle cerebral artery occlusion in rats. Stroke. 1992;23: 552-559.
22. Kader A, Bristman MH, Maraire N, Huh JT, Solomon RA. The effect of mild hypothermia on permanent focal ischemia in the rat. Neurosurgery. 1992;31:1056-1060.
23. Ridenour TR, Warner DS, Todd MM, MacAllister AC. Mild hypothermia reduces infarct size resulting from temporary but not permanent focal ischemia in rats. Stroke. 1992;23:733-738.
24. Karibe H, Zarow GJ, Graham SH, Weinstein PR. Mild intraischemic hypothermia reduces postischemic hyperperfusion, delayed postischemic hypoperfusion, blood-brain barrier disruption, brain edema, and neuronal damage volume after temporary focal cerebral ischemia in rats. J Cereb Blood Flow Metab. 1994;14:620-627.
25. Siesjö BK, Bengtsson F. Calcium fluxes, calcium antagonists, and calcium-related pathology in brain ischemia, hypoglycemia, and spreading-depression: a unifying hypothesis. J Cereb Blood Flow Metab. 1989; 9:127-140.
26. Berntman L, Welsh FA, Harp JR. Cerebral protective effect of low-grade hypothermia. Anesthesiology. 1981;55:495-498.
27. Kramer RS, Sanders AP, Lesage AM, Woodhall B, Sealy WC. The effect of profound hypothermia on preservation of cerebral ATP content during circulatory arrest. J Thorac Cardiovasc Surg. 1968;56:699-709.
28. Chopp M, Knight R, Tidwell CD, Helpem JA, Brown E, Welch KM. The metabolic effects of mild hypothermia on global cerebral ischemia and recirculation in the cat: comparison to normothermia and hypothermia. J Cereb Blood Flow Metab. 1989;9:141-148.
29. Busto R, Glovus MY, Dietrich WD, Marinez E, Valdes I, Ginsberg MD. Effects of mild hypothermia on ischemia-induced release of neurotransmitters and free fatty acids in rat brain. Stroke. 1989;20:904-910.
30. +2/calmodulin-dependent protein kinase II and its messenger RNA in the rat hippocampus following normo- and hypothermie ischemia. Neuroscience. 1995;68: 1003-1016.
31. 31P magnetic resonance study of the effect of temperature on ischemic brain injury. Can J Neurol Sci. 1992;19:317-325.
32. Héron A, Pollard H, Dessi F, Lasbennes F, Moreau J, Ben-Ari Y, Charriaut-Marlangue C. Regional variability in DNA fragmentation after global ischemia evidenced by combined histological and electrophoresis observations in the rat brain. J Neurochem. 1993;61:1973-1976.
33. MacManus JP, Buchan AM, Hill IE, Rasquinha I, Preston E. Global ischemia can cause DNA fragmentation indicative of apoptosis in rat brain. Neurosci Lett. 1993;164:89-92.
34. Schmidt-Kastner R, Fliss H, Hakim AM. Subtle neuronal death in the striatum after short forebrain ischemia in rats detected by in situ endlabeling for DNA damage. Stroke. 1997;28:163-170.
35. Linnik MD, Zobrist RH, Hatfield MD. Evidence supporting a role for programmed cell death in focal cerebral ischemia in rats. Stroke. 1993; 24:2002-2008.
36. Tominaga T, Kure S, Narisawa K, Yoshimoto T. Endonuclease activation following focal ischemic injury in the rat brain. Brain Res. 1993;608:21-26.
37. Charriaut-Marlangue C, Margaill I, Plotkine M, Ben-Ari Y. Early endonuclease activation following reversible focal ischemia in the rat brain. J Cereb Blood Flow Metah. 1995;15:385-388.
38. Charriaut-Marlangue C, Margaill I, Represa A, Popovici T, Plotkine M, Ben-Ari Y. Apoptosis and necrosis after reversible focal ischemia: an in situ DNA fragmentation analysis. J Cereb Blood Flow Metab. 1996;16:186-194.
39. Du C, Hu R, Csernansky CA, Hsu CY, Choi DW. Very delayed infarction after mild focal cerebral ischemia: a role for apoptosis? J Cereb Blood Flow Metab. 1996;16:195-201.
40. Li Y, Chopp M, Jiang N, Yao F, Zaloga C. Temporal profile of in situ DNA fragmentation after transient middle cerebral artery occlusion in the rat. J Cereb Blood Flow Metab. 1995a;15:389-397.
41. Li Y, Sharov VG, Jiang N, Zaloga C, Sabbah HN, Chopp M. Ultrastructural and light microscopic evidence of apoptosis after middle cerebral artery occlusion in the rat. Am J Pathol. 1995b;146:1045-1051.
42. Hallenbeck JM. Significance of the inflammatory response in brain ischemia. Acta Neurochir [Suppl]. 1996;66:27-31.
43. del Zoppo GJ, Schmid-Schönbein GW, Copeland BR, Chang C-M. Polymorphonuclear leukocytes occlude capillaries following middle cerebral artery occlusion and reperfusion in baboons. Stroke. 1991;22:1276-1283.
44. 2 or products of activated neutrophils. Am J Med. 1991;91:89-94.
45. Kochanek PM, Hallenbeck JM. Polymorphonuclear leukocytes and monocyte/macrophages in the pathogenesis of cerebral ischemia and stroke. Stroke. 1992;23:1367-1379.
46. Garcia JH, Liu KF, Yoshida Y, Lian J, Chen S, del Zoppo GJ. Influx of leukocytes and platelets in an evolving brain infarct (Wistar rat). Am J Pathol. 1994;144:188-199.
47. Chen H, Chopp M, Bodzin G. Neutropenia reduces the volume of cerebral infarct after transient middle cerebral artery occlusion in the rat. Neurosci Res Comm. 1992;11:93-99.
48. Chen H, Chopp M, Zhang RL, Bodzin G, Chen Q, Rusche JR, Todd RFI. Anti-CD11b monoclonal antibody reduces ischemic cell damage after transient focal cerebral ischemia in rat. Ann Neurol. 1994;35:458-463.
49. Chopp M, Zhang RL, Chen H, Li Y, Jiang N, Rusche JR. Postischemic administration of an anti-Mac-1 antibody reduces ischemic cell damage after transient middle cerebral artery occlusion in rats. Stroke. 1994;25: 869-876.
50. Mori E, del Zoppo GJ, Chambers JD, Copeland BR, Arfors KE. Inhibition of polymorphonuclear leukocyte adherence suppresses no-reflow after focal cerebral ischemia in baboons. Stroke. 1992;23:712-718.
51. Xue D, Huang ZG, Smith KE, Buchan AM. Immediate or delayed mild hypothermia prevents focal cerebral infarction. Brain Res. 1992;587: 66-72.
52. Zhang ZG, Chopp M, Chen H. Duration dependent post-ischemic hypothermia alleviates cortical damage after transient middle cerebral artery occlusion in the rat. J Neurol Sci. 1993;117:240-244.
53. Dietrich WD, Busto R, Alonso O, Globus M-Y, Ginsberg MD. Intraischemic but not postischemic brain hypothermia protects chronically following global forebrain ischemia in rats. J Cereb Blood Flow Metab. 1993;13:541-549.
54. Lo EH, Steinberg GK. Effects of hypothermia on evoked potentials, magnetic resonance imaging, and blood flow in focal ischemia in rabbits. Stroke. 1992;23:889-893.