Metabolic and perfusion responses to recurrent peri-infarct depolarization during focal ischemia in the Spontaneously Hypertensive Rat: Dominant contribution of sporadic CBF decrements to infarct expansion

Journal of Cerebral Blood Flow and Metabolism

Volumn 31, Issue 9, 2011, Pages 1863-1873

  Takeda, Yoshimasa ^a,b   Zhao, Liang ^a   Jacewicz, Michael ^a   Pulsinelli, William A ^a   Nowak Jr , Thaddeus S ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b OKAYAMA UNIVERSITY MEDICAL SCHOOL   (Japan)

Author keywords

CBF; focal ischemia; MCAO; peri infarct depolarization; spreading depression

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD FLOW; BRAIN INFARCTION; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; BRAIN METABOLISM; BRAIN PERFUSION; CONTROLLED STUDY; DEPOLARIZATION; HYPEREMIA; LONG TERM DEPRESSION; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVE CELL INHIBITION; NONHUMAN; PERI INFARCT DEPOLARIZATION; PRIORITY JOURNAL; RAT; SPONTANEOUSLY HYPERTENSIVE RAT;

ANIMALS; CEREBROVASCULAR CIRCULATION; CEREBRUM; CORTICAL SPREADING DEPRESSION; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; RATS; RATS, INBRED SHR;

EID: 80052424061     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2011.62     Document Type: Article

References (40)

1. Back T, Hoehn M, Mies G, Busch E, Schmitz B, Kohno K, Hossmann K-A (2000) Penumbral tissue alkalosis in focal cerebral ischemia: relationship to energy metabolism, blood flow, and steady potential. Ann Neurol 47:485-92 (Pubitemid 30194605)
2. Back T, Kohno K, Hossmann K-A (1994) Cortical negative DC deflections following middle cerebral artery occlusion and KCl-induced spreading depression: effect on blood flow, tissue oxygenation, and electroencephalogram. J Cereb Blood Flow Metab 14:12-9
3. Branston NM, Strong AJ, Symon L (1977) Extracellular potassium activity, evoked potential and tissue blood flow. Relationships during progressive ischemia in baboon cerebral cortex. J Neurol Sci 32:305-21 (Pubitemid 8109810)
4. Brennan KC, Beltrán-Parrazal L, López-Valdés HE, Theriot J, Toga AW, Charles AC (2007) Distinct vascular conduction with cortical spreading depression. J Neurophysiol 97:4143-51 (Pubitemid 47080646)
5. Brint S, Jacewicz M, Kiessling M, Tanabe J, Pulsinelli W (1988) Focal brain ischemia in the rat: methods for reproducible neocortical infarction using tandem occlusion of the distal middle cerebral and ispilateral common carotid arteries. J Cereb Blood Flow Metab 8:474-85
6. Dohmen C, Sakowitz OW, Fabricius M, Bosche B, Reith-meier T, Ernestus R-I, Brinker G, Dreier JP, Woitzik J, Strong AJ, Graf R (2008) Spreading depolarizations occur in human ischemic stroke with high incidence. Ann Neurol 63:720-8 (Pubitemid 351945531)
7. Dreier JP, Körner K, Ebert N, Görner A, Rubin I, Back T, Lindauer U, Wolf T, Villringer A, Einhäupl KM, Lauritzen M, Dirnagl U (1998) Nitric oxide scavenging by hemoglobin or nitric oxide synthase inhibition by N-nitro-L-arginine induces cortical spreading ischemia when K+ is increased in the subarachnoid space. J Cereb Blood Flow Metab 18:978-90 (Pubitemid 28427865)
8. Dreier JP, Major S, Manning A, Woitzik J, Drenckhahn C, Steinbrink J, Tolias C, Oliveira-Ferreira AI, Fabricius M, Hartings JA, Vajkoczy P, Lauritzen M, Dirnagl U, Bohner G, Strong AJ (2009) Cortical spreading ischaemia is a novel process involved in ischaemic damage in patients with aneurysmal subarachnoid haemorrhage. Brain 132:1866-81
9. Dunn AK, Bolay H, Moskowitz MA, Boas DA (2001) Dynamic imaging of cerebral blood flow using laser speckle. J Cereb Blood Flow Metab 21:195-201 (Pubitemid 32207418)
10. Gault LM, Lin C-W, LaManna JC, Lust WD (1994) Changes in energy metabolites, cGMP and intracellular pH during cortical spreading depression. Brain Res 641:176-80 (Pubitemid 24087501)
11. Hartings JA, Rolli ML, Lu X-CM, Tortella FC (2003) Delayed secondary phase of peri-infarct depolarizations after focal cerebral ischemia: relation to infarct growth and neuroprotection. J Neurosci 23:11602-10 (Pubitemid 38021287)
12. Hashemi P, Bhatia R, Nakamura H, Dreier JP, Graf R, Strong AJ, Boutelle MG (2009) Persisting depletion of brain glucose following cortical spreading depression, despite apparent hyperaemia: evidence for risk of an adverse effect of Leão's spreading depression. J Cereb Blood Flow Metab 29:166-75
13. Higuchi T, Takeda Y, Hashimoto M, Nagano O, Hirakawa M (2002) Dynamic changes in cortical NADH fluorescence and direct current potential in rat focal ischemia: relationship between propagation of recurrent depolarization and growth of the ischemic core. J Cereb Blood Flow Metab 22:71-9 (Pubitemid 34038385)
14. Jacewicz M, Tanabe J, Pulsinelli WA (1992) The CBF threshold and dynamics for focal cerebral infarction in spontaneously hypertensive rats. J Cereb Blood Flow Metab 12:359-70
15. Kaplan B, Brint S, Tanabe J, Jacewicz M, Wang X-J, Pulsinelli WA (1991) Temporal thresholds for neocor-tical infarction in rats subjected to reversible focal cerebral ischemia. Stroke 22:1032-9
16. Kumagai T, Walberer M, Nakamura H, Endepols H, Sué M, Vollmar S, Adib S, Mies G, Yoshimine T, Schroeter M, Graf R (2010) Distinct spatiotemporal patterns of spreading depolarizations during early infarct evolution: evidence from real-time imaging. J Cereb Blood Flow Metab 31:580-92
17. Lauritzen M, Dreier JP, Fabricius M, Hartings JA, Graf R, Strong AJ (2010) Clinical relevance of cortical spreading depression in neurological disorders: migraine, malignant stroke, subarachnoid and intracranial hemorrhage, and traumatic brain injury. J Cereb Blood Flow Metab 31:17-35
18. Lowry OH, Passonneau JV (1972) A Flexible System of Enzymatic Analysis. New York: Academic Press
19. Luckl J, Keating J, Greenberg JH (2008) Alpha-chloralose is a suitable anesthetic for chronic focal cerebral ischemia studies in the rat: a comparative study. Brain Res 1191:157-67
20. Luckl J, Zhou C, Durduran T, Yodh AG, Greenberg JH (2009) Characterization of periinfarct flow transients with laser speckle and Doppler after middle cerebral artery occlusion in the rat. J Neurosci Res 87:1219-29
21. Lust WD, Feussner GK, Barbehenn EK, Passonneau JV (1981) The enzymatic measurement of adenine nucleo-tides and P-creatine in picomole amounts. Anal Bio-chem 110:258-66 (Pubitemid 11103682)
22. Mies G (1997) Blood flow dependent duration of cortical depolarizations in the periphery of focal ischemia of rat brain. Neurosci Lett 221:165-8 (Pubitemid 27049224)
23. Mies G, Paschen W (1984) Regional changes of blood flow, glucose, and ATP content determined on brain sections during a single passage of spreading depression in rat brain cortex. Exp Neurol 84:249-58 (Pubitemid 14141440)
24. Nakamura H, Strong AJ, Dohmen C, Sakowitz OW, Vollmar S, Sué M, Kracht L, Hashemi P, Bhatia R, Yoshimine T, Dreier JP, Dunn AK, Graf R (2010) Spreading depolarizations cycle around and enlarge focal ischaemic brain lesions. Brain 133:1994-2006
25. Nakao Y, Itoh Y, Kuang T-Y, Cook M, Jehle J, Sokoloff L (2001) Effects of anesthesia on functional activation of cerebral blood flow and metabolism. Proc Natl Acad Sci USA 98:7593-8 (Pubitemid 32567993)
26. Nallet H, MacKenzie ET, Roussel S (2000) Haemodynamic correlates of penumbral depolarization following cerebral ischaemia. Brain Res 879:122-9
27. Ohta K, Graf R, Rosner G, Heiss W-D (2001) Calcium ion transients in peri-infarct depolarizations may deterio-rate ion homeostasis and expand infarction in focal cerebral ischemia in cats. Stroke 32:535-43 (Pubitemid 32155248)
28. Oliveira-Ferreira AI, Milakara D, Alam M, Jorks D, Major S, Hartings JA, Lückl J, Martus P, Graf R, Dohmen C, Bohner G, Woitzik J, Dreier JP, group ftCs (2010) Experimental and preliminary clinical evidence of an ischemic zone with prolonged negative DC shifts surrounded by a normally perfused tissue belt with persistent electrocorticographic depression. J Cereb Blood Flow Metab 30:1504-19
29. Piilgaard H, Lauritzen M (2009) Persistent increase in oxygen consumption and impaired neurovascular coupling after spreading depression in rat neocortex. J Cereb Blood Flow Metab 29:1517-27
30. Pinard E, Nallet H, MacKenzie ET, Seylaz J, Roussel S (2002) Penumbral microcirculatory changes associated with peri-infarct depolarizations in the rat. Stroke 33:606-12 (Pubitemid 34123414)
31. Pontén U, Ratcheson R, Salford L, Siesjö BK (1973) Optimal freezing conditions for cerebral metabolites in rats. J Neurochem 21:1127-38
32. Risher WC, Ard D, Yuan J, Kirov SA (2010) Recurrent spontaneous spreading depepolarizations facilitate acute dendritic injury in the ischemic penumbra. J Neurosci 30:9859-68
33. Saito R, Graf R, Hübel K, Fujita T, Rosner G, Heiss W-D (1997) Reduction of infarct volume by halothane: effect on cerebral blood flow or perifocal spreading depression-like depolarizations. J Cereb Blood Flow Metab 17:857-64 (Pubitemid 27377640)
34. Selman WR, Lust WD, Pundik S, Zhou Y, Ratcheson RA (2004) Compromised metabolic recovery following spontaneous spreading depression in the penumbra. Brain Res 999:167-74 (Pubitemid 38167389)
35. Shin HK, Dunn AK, Jones PB, Boas DA, Moskowitz MA, Ayata C (2006) Vasoconstrictive neurovascular coupling during focal ischemic depolarizations. J Cereb Blood Flow Metab 26:1018-30 (Pubitemid 44134074)
36. Silver IA, Erecińska M (1994) Extracellular glucose concentration in mammalian brain: continuous monitoring of changes during increased neuronal activity and upon limitation in oxygen supply in normo-, hypo-, and hyperglycemic animals. J Neurosci 14:5068-76
37. Strong AJ, Anderson PJ, Watts HR, Virley DJ, Lloyd A, Irving EA, Nagafuji T, Ninomiya M, Nakamura H, Dunn AK, Graf R (2007) Peri-infarct depolarizations lead to loss of perfusion in ischaemic gyrencephalic cerebral cortex. Brain 130:995-1008 (Pubitemid 47355590)
38. Sukhotinsky I, Dilekoz E, Moskowitz MA, Ayata C (2008) Hypoxia and hypotension transform the blood flow response to cortical spreading depression from hyper-emia into hypoperfusion in the rat. J Cereb Blood Flow Metab 28:1369-76 (Pubitemid 351896654)
39. Van Uitert RL, Sage JI, Levy DE, Duffy TE (1981) Comparison of radiolabeled butanol and iodoanti-pyrine as cerebral blood flow markers. Brain Res 222:365-72 (Pubitemid 11000345)
40. Zhao L, Nowak Jr TS (2006) CBF changes associated with focal ischemic preconditioning in the Spontaneously Hypertensive Rat. J Cereb Blood Flow Metab 26:1128-40 (Pubitemid 44268175)