Metabolic downregulation: A key to successful neuroprotection?

Stroke

Volumn 39, Issue 10, 2008, Pages 2910-2917

  Yenari, Midori ^a,e   Kitagawa, Kazuo ^b   Lyden, Patrick ^c   Perez Pinzon, Miguel ^d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^e SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Cerebral ischemia; Hypothermia; Ischemic tolerance

Indexed keywords

ALTEPLASE; FIBRINOLYTIC AGENT; GLUTAMIC ACID;

APOPTOSIS; BLOOD BRAIN BARRIER; BRAIN BLOOD FLOW; BRAIN DISEASE; BRAIN METABOLISM; CLINICAL RESEARCH; CLINICAL TRIAL; DOWN REGULATION; GENE CONTROL; HEART ARREST; HUMAN; INDUCED HYPOTHERMIA; INFLAMMATION; ISCHEMIC PRECONDITIONING; METABOLIC REGULATION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; STROKE; SYSTEMATIC REVIEW; TISSUE METABOLISM; TRANSIENT ISCHEMIC ATTACK; ANIMAL; BRAIN; BRAIN CIRCULATION; CRYOANESTHESIA; METABOLISM; METHODOLOGY; NERVE DEGENERATION; PHYSIOLOGY;

ANIMALS; BRAIN; CEREBROVASCULAR CIRCULATION; CLINICAL TRIALS AS TOPIC; DOWN-REGULATION; HUMANS; HYPOTHERMIA, INDUCED; ISCHEMIC PRECONDITIONING; NERVE DEGENERATION; STROKE;

EID: 54049103618     PISSN: 00392499     EISSN: None     Source Type: Journal    
DOI: 10.1161/STROKEAHA.108.514471     Document Type: Review

References (102)

1. Lyden P, Krieger DW, Yenari MA, Dietrich WD. Therapeutic hypothermia for acute stroke. Int J Stroke. 2006;1:9-19.
2. Krieger DW, Yenari MA. Therapeutic hypothermia for acute ischemic stroke: What do laboratory studies teach us? Stroke. 2004;35:1482-1489.
3. Erecinska M, Thoresen M, Silver IA. Effects of hypothermia on energy metabolism in mammalian central nervous system. J Cereb Blood Flow Metab. 2003;23:513-530.
4. Yenari M, Wijman C, Steinberg G. Effects of hypothermia on cerebral metabolism, blood flow and autoregulation. In: Mayer S, Sessler D, eds. Hypothermia in Neurocritical Care. New York: Marcel Dekker, Inc; 2004:141-178.
5. Liu L, Yenari MA. Therapeutic hypothermia: Neuroprotective mechanisms. Front Biosci. 2007;12:816-825.
6. Marion DW, Penrod LE, Kelsey SF, Obrist WD, Kochanek PM, Palmer AM, Wisniewski SR, DeKosky ST. Treatment of traumatic brain injury with moderate hypothermia. N Engl J Med. 1997;336:540-546.
7. Vigue B, Ract C, Zlotine N, Leblanc PE, Samii K, Bissonnette B. Relationship between intracranial pressure, mild hypothermia and temperature-corrected paco2 in patients with traumatic brain injury. Intensive Care Med. 2000;26:722-728.
8. Metz C, Holzschuh M, Bein T, Woertgen C, Frey A, Frey I, Taeger K, Brawanski A. Moderate hypothermia in patients with severe head injury: Cerebral and extracerebral effects. J Neurosurg. 1996;85:533-541.
9. Wagner S, Nagel S, Kluge B, Schwab S, Heiland S, Koziol J, Gardner H, Hacke W. Topographically graded postischemic presence of metal-loproteinases is inhibited by hypothermia. Brain Res. 2003;984:63-75.
10. Hamann GF, Burggraf D, Martens HK, Liebetrau M, Jager G, Wunderlich N, DeGeorgia M, Krieger DW. Mild to moderate hypothermia prevents microvascular basal lamina antigen loss in experimental focal cerebral ischemia. Stroke. 2004;35:764-769.
11. Lee JE, Yoon YJ, Moseley ME, Yenari MA. Reduction in levels of matrix metalloproteinases and increased expression of tissue inhibitor of metalloproteinase-2 in response to mild hypothermia therapy in experimental stroke. J Neurosurg. 2005;103:289-297.
12. Ohta H, Terao Y, Shintani Y, Kiyota Y. Therapeutic time window of post-ischemic mild hypothermia and the gene expression associated with the neuroprotection in rat focal cerebral ischemia. Neurosci Res. 2007; 57:424-433.
13. Han HS, Qiao Y, Karabiyikoglu M, Giffard RG, Yenari MA. Influence of mild hypothermia on inducible nitric oxide synthase expression and reactive nitrogen production in experimental stroke and inflammation. J Neurosci. 2002;22:3921-3928.
14. Xu L, Yenari MA, Steinberg GK, Giffard RG. Mild hypothermia reduces apoptosis of mouse neurons in vitro early in the cascade. J Cereb Blood Flow Metab. 2002;22:21-28.
15. Van Hemelrijck A, Hachimi-Idrissi S, Sarre S, Ebinger G, Michotte Y. Post-ischaemic mild hypothermia inhibits apoptosis in the penumbral region by reducing neuronal nitric oxide synthase activity and thereby preventing endothelin-1-induced hydroxyl radical formation. Eur J Neurosci. 2005;22:1327-1337.
16. Zhao H, Shimohata T, Wang JQ, Sun G, Schaal DW, Sapolsky RM, Steinberg GK. Akt contributes to neuroprotection by hypothermia against cerebral ischemia in rats. J Neurosci. 2005;25:9794-9806.
17. D'Cruz BJ, Fertig KC, Filiano AJ, Hicks SD, DeFranco DB, Callaway CW. Hypothermic reperfusion after cardiac arrest augments brain-derived neurotrophic factor activation. J Cereb Blood Flow Metab. 2002;22:843-851.
18. Schmidt KM, Repine MJ, Hicks SD, DeFranco DB, Callaway CW. Regional changes in glial cell line-derived neurotrophic factor after cardiac arrest and hypothermia in rats. Neurosci Lett. 2004;368:135-139.
19. Boris-Moller F, Kamme F, Wieloch T. The effect of hypothermia on the expression of neurotrophin mrna in the hippocampus following transient cerebral ischemia in the rat. Brain Res Mol Brain Res. 1998;63:163-173.
20. Vosler PS, Logue ES, Repine MJ, Callaway CW. Delayed hypothermia preferentially increases expression of brain-derived neurotrophic factor exon iii in rat hippocampus after asphyxial cardiac arrest. Brain Res Mol Brain Res. 2005;135:21-29.
21. Hicks SD, DeFranco DB, Callaway CW. Hypothermia during reper-fusion after asphyxial cardiac arrest improves functional recovery and selectively alters stress-induced protein expression. J Cereb Blood Flow Metab. 2000;20:520-530.
22. Hicks SD, Parmele KT, DeFranco DB, Klann E, Callaway CW. Hypothermia differentially increases extracellular signal-regulated kinase and stress-activated protein kinase/c-jun terminal kinase activation in the hippocampus during reperfusion after asphyxial cardiac arrest. Neuroscience. 2000;98:677-685.
23. Han HS, Karabiyikoglu M, Kelly S, Sobel RA, Yenari MA. Mild hypothermia inhibits nuclear factor-kappab translocation in experimental stroke. J Cereb Blood Flow Metab. 2003;23:589-598.
24. Han HS, Yenari MA. Effect of gene expression by therapeutic hypothermia in cerebral ischemia. Future Neurology. 2007;2:435-440.
25. Zhao H, Yenari MA, Cheng D, Sapolsky RM, Steinberg GK. Biphasic cytochrome c release after transient global ischemia and its inhibition by hypothermia. J Cereb Blood Flow Metab. 2005;25:1119-1129.
26. Zhang Z, Sobel RA, Cheng D, Steinberg GK, Yenari MA. Mild hypothermia increases bcl-2 protein expression following global cerebral ischemia. Brain Res Mol Brain Res. 2001;95:75-85.
27. Yenari MA, Iwayama S, Cheng D, Sun GH, Fujimura M, Morita-Fujimura Y, Chan PH, Steinberg GK. Mild hypothermia attenuates cytochrome C release but does not alter bcl-2 expression or caspase activation after experimental stroke. J Cereb Blood Flow Metab. 2002;22:29-38.
28. Inamasu J, Suga S, Sato S, Horiguchi T, Akaji K, Mayanagi K, Kawase T. Postischemic hypothermia attenuates apoptotic cell death in transient focal ischemia in rats. Acta Neurochir Suppl. 2000;76:525-527.
29. Prakasa Babu P, Yoshida Y, Su M, Segura M, Kawamura S, Yasui N. Immunohistochemical expression of bcl-2, bax and cytochrome c following focal cerebral ischemia and effect of hypothermia in rat. Neurosci Lett. 2000;291:196-200.
30. D'Cruz BJ, Logue ES, Falke E, DeFranco DB, Callaway CW. Hypothermia and ERK activation after cardiac arrest. Brain Res. 2005;1064: 108-118.
31. van der Worp HB, Sena ES, Donnan GA, Howells DW, Macleod MR. Hypothermia in animal models of acute ischaemic stroke: A systematic review and meta-analysis. Brain. 2007;130:3063-3074.
32. Yenari MA, Palmer JT, Bracci PM, Steinberg GK. Thrombolysis with tissue plasminogen activator (tPA) is temperature dependent. Thromb Res. 1995;77:475-481.
33. Meden P, Overgaard K, Pedersen H, Boysen G. The influence of body temperature on infarct volume and thrombolytic therapy in a rat embolic stroke model. Brain Res. 1994;647:131-138.
34. Kollmar R, Henninger N, Bardutzky J, Schellinger PD, Schabitz WR, Schwab S. Combination therapy of moderate hypothermia and thrombolysis in experimental thromboembolic stroke: an MRI study. Exp Neurol. 2004;190:204-212.
35. Liu L, XN T, MA Y. Mild hypothermia reduces hemorrhage and blood brain barrier (BBB) disruption following tissue plasminogen activator treatment in experimental stroke. Neurology. 2006;66:A242.
36. Bernard SA, Buist M. Induced hypothermia in critical care medicine: A review. Crit Care Med. 2003;31:2041-2051.
37. Bernard SA, Gray TW, Buist MD, Jones BM, Silvester W, Gutteridge G, Smith K. Treatment of comatose survivors of out-of-hospital cardiac arrest with induced hypothermia. N Engl J Med. 2002;346:557-563.
38. Hypothermia after Cardiac Arrest Study Group T. Mild therapeutic hypothermia to improve the neurologic outcome after cardiac arrest. N Engl J Med. 2002;346:549-556.
39. Gluckman PD, Wyatt JS, Azzopardi D, Ballard R, Edwards AD, Ferriero DM, Polin RA, Robertson CM, Thoresen M, Whitelaw A, Gunn AJ. Selective head cooling with mild systemic hypothermia after neonatal encephalopathy: Multicentre randomised trial. Lancet. 2005;365:663-670.
40. Shankaran S, Laptook AR, Ehrenkranz RA, Tyson JE, McDonald SA, Donovan EF, Fanaroff AA, Poole WK, Wright LL, Higgins RD, Finer NN, Carlo WA, Duara S, Oh W, Cotten CM, Stevenson DK, Stoll BJ, Lemons JA, Guillet R, Jobe AH. Whole-body hypothermia for neonates with hypoxic-ischemic encephalopathy. N Engl J Med. 2005;353:1574-1584.
41. Clifton GL, Miller ER, Choi SC, Levin HS, McCauley S, Smith KR Jr, Muizelaar JP, Wagner FC Jr, Marion DW, Luerssen TG, Chesnut RM, Schwartz M. Lack of effect of induction of hypothermia after acute brain injury. N Engl J Med. 2001;344:556-563.
42. Hemmen TM, Lyden PD. Induced hypothermia for acute stroke. Stroke. 2007;38:794-799.
43. Schwab S, Georgiadis D, Berrouschot J, Schellinger PD, Graffagnino C, Mayer SA. Feasibility and safety of moderate hypothermia after massive hemispheric infarction. Stroke. 2001;32:2033-2035.
44. De Georgia MA, Krieger DW, Abou-Chebl A, Devlin TG, Jauss M, Davis SM, Koroshetz WJ, Rordorf G, Warach S. Cooling for acute ischemic brain damage (cool aid): A feasibility trial of endovascular cooling. Neurology. 2004;63:312-317.
45. Lyden PD, Allgren RL, Ng K, Akins P, Meyer B, Al-Sanani F, Lutsep H, Dobak J, Matsubara BS, Zivin J. Intravascular cooling in the treatment of stroke (ICTUS): Early clinical experience. J Stroke Cerebrovas Dis. 2005;14:107-114.
46. Guluma KZ, Hemmen TM, Olsen SE, Rapp KS, Lyden PD. A trial of therapeutic hypothermia via endovascular approach in awake patients with acute ischemic stroke: Methodology. Acad Emerg Med. 2006;13: 820-827.
47. Georgiadis D, Schwarz S, Kollmar R, Schwab S. Endovascular cooling for moderate hypothermia in patients with acute stroke: First results of a novel approach. Stroke. 2001;32:2550-2553.
48. Allers M, Boris-Moller F, Lunderquist A, Wieloch T. A new method of selective, rapid cooling of the brain: An experimental study. Cardiovasc Intervent Radiol. 2006;29:260-263.
49. Rutherford MA, Azzopardi D, Whitelaw A, Cowan F, Renowden S, Edwards AD, Thoresen M. Mild hypothermia and the distribution of cerebral lesions in neonates with hypoxic-ischemic encephalopathy. Pediatrics. 2005;116:1001-1006.
50. Gordon CJ, McMahon B, Richelson E, Padnos B, Katz L. Neurotensin analog nt77 induces regulated hypothermia in the rat. Life Sci. 2003;73: 2611-2623.
51. Tyler-McMahon BM, Stewart JA, Farinas F, McCormick DJ, Richelson E. Highly potent neurotensin analog that causes hypothermia and antino-ciception. Eur J Pharmacol. 2000;390:107-111.
52. Katz LM, Young AS, Frank JE, Wang Y, Park K. Regulated hypothermia reduces brain oxidative stress after hypoxic-ischemia. Brain Res. 2004;1017:85-91.
53. Katz LM, Young A, Frank JE, Wang Y, Park K. Neurotensin-induced hypothermia improves neurologic outcome after hypoxic-ischemia. Crit Care Med. 2004;32:806-810.
54. Scanlan TS, Suchland KL, Hart ME, Chiellini G, Huang Y, Kruzich PJ, Frascarelli S, Crossley DA, Bunzow JR, Ronca-Testoni S, Lin ET, Hatton D, Zucchi R, Grandy DK. 3-iodothyronamine is an endogenous and rapid-acting derivative of thyroid hormone. Nat Med. 2004;10:638- 642.
55. Doyle KP, Suchland KL, Ciesielski TM, Lessov NS, Grandy DK, Scanlan TS, Stenzel-Poore MP. Novel thyroxine derivatives, thyronamine and 3-iodothyronamine, induce transient hypothermia and marked neuropro-tection against stroke injury. Stroke. 2007;38:2569-2576.
56. Blackstone E, Roth MB. Suspended animation-like state protects mice from lethal hypoxia. Shock. 2007;27:370-372.
57. Dirnagl U, Simon RP, Hallenbeck JM. Ischemic tolerance and endogenous neuroprotection. Trends Neurosci. 2003;26:248-254.
58. Kirino T. Ischemic tolerance. J Cereb Blood Flow Metab. 2002;22: 1283-1296.
59. Chen J, Simon R. Ischemic tolerance in the brain. Neurology. 1997;48: 306-311.
60. Gidday JM. Cerebral preconditioning and ischaemic tolerance. Nat Rev Neurosci. 2006;7:437-448.
61. Nandagopal K, Dawson TM, Dawson VL. Critical role for nitric oxide signaling in cardiac and neuronal ischemic preconditioning and tolerance. J Pharmacol Exp Ther. 2001;297:474-478.
62. Stenzel-Poore MP, Stevens SL, Xiong Z, Lessov NS, Harrington CA, Mori M, Meller R, Rosenzweig HL, Tobar E, Shaw TE, Chu X, Simon RP. Effect of ischaemic preconditioning on genomic response to cerebral ischaemia: similarity to neuroprotective strategies in hibernation and hypoxia-tolerant states. Lancet. 2003;362:1028-1037.
63. Perez-Pinzon MA. Mechanisms of neuroprotection during ischemic preconditioning: lessons from anoxic tolerance. Comp Biochem Physiol A Mol Integr Physiol. 2007;147:291-299.
64. Kitagawa K, Matsumoto M, Tagaya M, Hata R, Ueda H, Niinobe M, Handa N, Fukunaga R, Kimura K, Mikoshiba K, Kamada T. Ischemic tolerance phenomenon found in the brain. Brain Res. 1990;528:21-24.
65. Stagliano NE, Perez-Pinzon MA, Moskowitz MA, Huang PL. Focal ischemic preconditioning induces rapid tolerance to middle cerebral artery occlusion in mice. J Cereb Blood Flow Metab. 1999;19:757-761.
66. Kraig R, Kunkler P. Spreading depression: A teleological means for self-protection from brain ischemia. In: Chan P, ed. Princeton Conference. Cambridge: Cambridge University Press; 2001;142-157.
67. Kobayashi S, Harris VA, Welsh FA. Spreading depression induces tolerance of cortical neurons to ischemia in rat brain. J Cereb Blood Flow Metab. 1995;15:721-727.
68. Sharp FR, Bernaudin M. Hif1 and oxygen sensing in the brain. Nat Rev Neurosci. 2004;5:437-448.
69. Nishio S, Yunoki M, Chen ZF, Anzivino MJ, Lee KS. Ischemic tolerance in the rat neocortex following hypothermic preconditioning. J Neurosurg. 2000;93:845-851.
70. Riepe MW, Kasischke K, Gericke CA, Lowe A, Hellweg R. Increase of hypoxic tolerance in rat hippocampal slices following 3-nitropropionic acid is not mediated by endogenous nerve growth factor. Neurosci Lett. 1996;211:9-12.
71. Raval AP, Dave KR, Perez-Pinzon MA. Resveratrol mimics ischemic preconditioning in the brain. J Cereb Blood Flow Metab. 2006;26: 1141-1147.
72. Ruscher K, Freyer D, Karsch M, Isaev N, Megow D, Sawitzki B, Priller J, Dirnagl U, Meisel A. Erythropoietin is a paracrine mediator of ische-mic tolerance in the brain: Evidence from an in vitro model. J Neurosci. 2002;22:10291-10301.
73. Perez-Pinzon MA, Xu GP, Dietrich WD, Rosenthal M, Sick TJ. Rapid preconditioning protects rats against ischemic neuronal damage after 3 but not 7 days of reperfusion following global cerebral ischemia. J Cereb Blood Flow Metab. 1997;17:175-182.
74. Douen AG, AkiyamaK, Hogan MJ, Wang F, Dong L, Chow AK, Hakim A. Preconditioning with cortical spreading depression decreases intrais-chemic cerebral glutamate levels and down-regulates excitatory amino acid transporters eaat1 and eaat2 from rat cerebal cortex plasma membranes. J Neurochem. 2000;75:812-818.
75. Dave KR, Lange-Asschenfeldt C, Raval AP, Prado R, Busto R, Saul I, Perez-Pinzon MA. Ischemic preconditioning ameliorates excitotoxicity by shifting glutamate/gamma-aminobutyric acid release and biosynthesis. J Neurosci Res. 2005;82:665-673.
76. Johns L, Sinclair AJ, Davies JA. Hypoxia/hypoglycemia-induced amino acid release is decreased in vitro by preconditioning. Biochem Biophys Res Commun. 2000;276:134-136.
77. Tanaka H, Calderone A, Jover T, Grooms SY, Yokota H, Zukin RS, Bennett MV. Ischemic preconditioning acts upstream of glur2 down-regulation to afford neuroprotection in the hippocampal ca1. Proc Natl Acad Sci U S A. 2002;99:2362-2367.
78. Aizenman E, Sinor JD, Brimecombe JC, Herin GA. Alterations of N-methyl-D-aspartate receptor properties after chemical ischemia. J Pharmacol Exp Ther. 2000;295:572-577.
79. Sommer C, Fahrner A, Kiessling M. [3h]muscimol binding to gamma-aminobutyric acid(a) receptors is upregulated in Ca1 neurons of the gerbil hippocampus in the ischemia-tolerant state. Stroke. 2002;33: 1698-1705.
80. Dave KR, Saul I, Busto R, Ginsberg MD, Sick TJ, Perez-Pinzon MA. Ischemic preconditioning preserves mitochondrial function after global cerebral ischemia in rat hippocampus. J Cereb Blood Flow Metab. 2001;21:1401-1410.
81. Sharp FR, Ran R, Lu A, Tang Y, Strauss KI, Glass T, Ardizzone T, Bernaudin M. Hypoxic preconditioning protects against ischemic brain injury. NeuroRx. 2004;1:26-35.
82. Bergeron M, Gidday JM, Yu AY, Semenza GL, Ferriero DM, Sharp FR. Role of hypoxia-inducible factor-1 in hypoxia-induced ischemic tolerance in neonatal rat brain. Ann Neurol. 2000;48:285-296.
83. Liu M, Alkayed NJ. Hypoxic preconditioning and tolerance via hypoxia inducible factor (HIF) 1alpha-linked induction of p450 2c11 epoxygen-ase in astrocytes. J Cereb Blood Flow Metab. 2005;25:939-948.
84. Janier MF, Vanoverschelde JL, Bergmann SR. Ischemic preconditioning stimulates anaerobic glycolysis in the isolated rabbit heart. Am J Physiol. 1994;267:H1353-H1360.
85. Yabe K, Nasa Y, Sato M, Iijima R, Takeo S. Preconditioning preserves mitochondrial function and glycolytic flux during an early period of reperfusion in perfused rat hearts. Cardiovasc Res. 1997;33:677-685.
86. Jones NM, Bergeron M. Hypoxic preconditioning induces changes in HIF-1 target genes in neonatal rat brain. J Cereb Blood Flow Metab. 2001;21:1105-1114.
87. Hall ED, Braughler JM. Free radicals in CNS injury. Res Publ Assoc Res Nerv Ment Dis. 1993;71:81-105.
88. Vlessis AA, Widener LL, Bartos D. Effect of peroxide, sodium, and calcium on brain mitochondrial respiration in vitro: Potential role in cerebral ischemia and reperfusion. J Neurochem. 1990;54:1412-1418.
89. Kannan K, Jain SK. Oxidative stress and apoptosis. Pathophysiology. 2000;7:153-163.
90. Goldstein LB, Adams R, Alberts MJ, Appel LJ, Brass LM, Bushnell CD, Culebras A, Degraba TJ, Gorelick PB, Guyton JR, Hart RG, Howard G, Kelly-Hayes M, Nixon JV, Sacco RL. Primary prevention of ischemic stroke: A guideline from the American Heart Association/American Stroke Association Stroke Council: Cosponsored by the Atherosclerotic Peripheral Vascular Disease Interdisciplinary Working Group; Cardiovascular Nursing Council; Clinical Cardiology Council; Nutrition, Physical Activity, and Metabolism couNcil; and the Quality of Care and Outcomes Research Interdisciplinary Working Group: The American Academy of Neurology affirms the value of this guideline. Stroke. 2006;37:1583-1633.
91. Weih M, Kallenberg K, Bergk A, Dirnagl U, Harms L, Wernecke KD, Einhaupl KM. Attenuated stroke severity after prodromal tia: A role for ischemic tolerance in the brain? Stroke. 1999;30:1851-1854.
92. Moncayo J, de Freitas GR, Bogousslavsky J, Altieri M, van Melle G. Do transient ischemic attacks have a neuroprotective effect? Neurology. 2000;54:2089-2094.
93. Castillo J, Moro MA, Blanco M, Leira R, Serena J, Lizasoain I, Davalos A. The release of tumor necrosis factor-alpha is associated with ischemic tolerance in human stroke. Ann Neurol. 2003;54:811-819.
94. Wegener S, Gottschalk B, Jovanovic V, Knab R, Fiebach JB, Schellinger PD, Kucinski T, Jungehulsing GJ, Brunecker P, Muller B, Banasik A, Amberger N, Wernecke KD, Siebler M, Rother J, Villringer A, Weih M. Transient ischemic attacks before ischemic stroke: Preconditioning the human brain? A multicenter magnetic resonance imaging study. Stroke. 2004;35:616-621.
95. Arboix A, Cabeza N, Garcia-Eroles L, Massons J, Oliveres M, Targa C, Balcells M. Relevance of transient ischemic attack to early neurological recovery after nonlacunar ischemic stroke. Cerebrovasc Dis. 2004;18: 304-311.
96. Schaller B. Ischemic preconditioning as induction of ischemic tolerance after transient ischemic attacks in human brain: Its clinical relevance. Neurosci Lett. 2005;377:206-211.
97. Johnston SC. Ischemic preconditioning from transient ischemic attacks? Data from the northern california tia study. Stroke. 2004;35:2680-2682.
98. Murry CE, Richard VJ, Reimer KA, Jennings RB. Ischemic preconditioning slows energy metabolism and delays ultrastructural damage during a sustained ischemic episode. Circ Res. 1990;66:913-931.
99. Kloner RA, Jennings RB. Consequences of brief ischemia: Stunning, preconditioning, and their clinical implications: Part 1. Circulation. 2001;104:2981-2989.
100. Kloner RA, Jennings RB. Consequences of brief ischemia: Stunning, preconditioning, and their clinical implications: Part 2. Circulation. 2001;104:3158-3167.
101. Yamagishi H, Akioka K, Hirata K, Sakanoue Y, Toda I, Yoshiyama M, Teragaki M, Takeuchi K, Yoshikawa J, Ochi H. Effects of preinfarction angina on myocardial injury in patients with acute myocardial infarction: A study with resting 123i-bmipp and 201t1 myocardial spect. J Nucl Med. 2000;41:830-836.
102. Yellon DM, Alkhulaifi AM, Pugsley WB. Preconditioning the human myocardium. Lancet. 1993;342:276-277.