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Conditioning Studies in Focal Cerebral Ischemia: Model Selection, Physiological Monitoring, and Other Methodological Issues

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Innate Tolerance in the CNS

Part of the book series: Springer Series in Translational Stroke Research ((SSTSR))

Abstract

The earliest studies of preconditioning in experimental stroke examined the potential impact of such interventions on the key variable of cerebral perfusion. Based on limited regional or temporal sampling, these were interpreted to suggest that protection could be dissociated from overt CBF changes, and the majority of conditioning studies in experimental stroke have since focused on cellular protection mechanisms. However, evolving results indicate a strong association between delayed improvements in penumbral perfusion and subsequent tissue protection. This presentation will briefly consider the strengths and limitations of commonly used focal brain ischemia models and address the requirements for adequately monitoring those physiological parameters that are recognized to influence outcome in experimental stroke. It will then summarize observations regarding changes in blood flow and relevant physiological variables in conditioning models.

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References

  • Ábrahám H, Somogyvári-Vigh A, Maderdrut JL, Vigh S, Arimura A (2002) Filament size influences temperature changes and brain damage following middle cerebral artery occlusion in rats. Exp Brain Res 142:131–138

    PubMed  Google Scholar 

  • Alkayed NJ, Goyagi T, Joh H-D, Klaus J, Harder DR, Traystman RJ, Hurn PD (2002) Neuroprotection and P450 2 C11 upregulation after experimental transient ischemic attack. Stroke 33:1677–1684

    PubMed  CAS  Google Scholar 

  • Aronowski J, Strong R, Grotta JC (1997) Reperfusion injury: demonstration of brain damage produced by reperfusion after transient focal ischemia in rats. J Cereb Blood Flow Metab 17:1048–1056

    PubMed  CAS  Google Scholar 

  • Bahjat FR, Williams-Karnesky RL, Kohama SG, West GA, Doyle KP, Spector MD, Hobbs TR, Stenzel-Poore MP (2011) Proof of concept: pharmacological preconditioning with a Toll-like receptor agonist protects against cerebrovascular injury in a primate model of stroke. J Cereb Blood Flow Metab 31:1229–1242

    PubMed  CAS  Google Scholar 

  • Baker CJ, Onesti ST, Solomon RA (1992) Reduction by delayed hypothermia of cerebral infarction following middle cerebral artery occlusion in the rat: a time-course study. J Neurosurg 77:438–444

    PubMed  CAS  Google Scholar 

  • Barber PA, Hoyte L, Colbourne F, Buchan AM (2004) Temperature-regulated model of focal ischemia in the mouse: A study with histopathological and behavioral outcomes. Stroke 35:1720–1725

    PubMed  Google Scholar 

  • Barone FC, Knudsen DJ, Nelson AH, Feuerstein GZ, Willette RN (1993) Mouse strain differences in susceptibility to cerebral ischemia are related to vascular anatomy. J Cereb Blood Flow Metab 13:683–692

    PubMed  CAS  Google Scholar 

  • Barone FC, Feuerstein GZ, White RF (1997) Brain cooling during transient cerebral ischemia provides complete neuroprotection. Neurosci Biobehav Rev 21:31–44

    PubMed  CAS  Google Scholar 

  • Barone FC, White RF, Spera PA, Ellison J, Currie RW, Wang X, Feuerstein GZ (1998) Ischemic preconditioning and brain tolerance: temporal histological and functional outcomes, protein synthesis requirement, and interleukin-1 receptor antagonist and early gene expression. Stroke 29:1937–1951

    PubMed  CAS  Google Scholar 

  • Bederson JB, Pitts LH, Germano SM, Nishimura MC, Davis RL, Bartkowski H (1986) Evaluation of 2,3,5-triphenytetrazolium chloride as a stain for detection and quantification of experimental cerebral infarction in rats. Stroke 17:1304–1308

    PubMed  CAS  Google Scholar 

  • Belayev L, Alonso OF, Busto R, Zhao W, Ginsberg MD (1996) Middle cerebral artery occlusion in the rat by intraluminal suture: neurological and pathological evaluation of an improved model. Stroke 27:1616–1623

    PubMed  CAS  Google Scholar 

  • Belayev L, Zhao W, Busto R, Ginsberg MD (1997) Transient middle cerebral artery occlusion by intraluminal suture: I. Three-dimensional autoradiographic image-analysis of local cerebral glucose metabolism-blood flow interrelationships during ischemia and early recirculation. J Cereb Blood Flow Metab 17:1266–1280

    PubMed  CAS  Google Scholar 

  • Böttiger BW, Krumnikl JJ, Gass P, Schmitz B, Motsch J, Martin E (1997) The cerebral ‘no-reflow’ phenomenon after cardiac arrest in rats – influence of low-flow reperfusion. Resuscitation 34:79–87

    PubMed  Google Scholar 

  • 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 ipsilateral common carotid arteries. J Cereb Blood Flow Metab 8:474–485

    PubMed  CAS  Google Scholar 

  • Buchan AM, Xue D, Slivka A (1992) A new model of temporary focal neocortical ischemia in the rat. Stroke 23:273–279

    PubMed  CAS  Google Scholar 

  • Chen ST, Hsu CY, Hogan EL, Maricq H, Balentine JD (1986) A model of focal ischemic stroke in the rat: reproducible extensive cortical infarction. Stroke 17:738–743

    PubMed  CAS  Google Scholar 

  • Chen H, Chopp M, Welch KMA (1991) Effect of mild hyperthermia on the ischemic infarct volume after middle cerebral artery occlusion in the rat. Neurology 41:1133–1135

    PubMed  CAS  Google Scholar 

  • Chen J, Graham SH, Zhu RL, Simon RP (1996) Stress proteins and tolerance to focal cerebral ischemia. J Cereb Blood Flow Metab 16:566–577

    PubMed  CAS  Google Scholar 

  • Chesselet M-F, Gonzales C, Lin C-S, Polsky K, Jin B-K (1990) Ischemic damage in the striatum of adult gerbils: relative sparing of somatostatinergic and cholinergic interneurons contrasts with loss of efferent neurons. Exp Neurol 110:209–218

    PubMed  CAS  Google Scholar 

  • Chi OZ, Hunter C, Liu X, Chokshi SK, Weiss HR (2010a) Effects of fentanyl pretreatment on regional cerebral blood flow in focal cerebral ischemia in rats. Pharmacology 85:153–157

    PubMed  CAS  Google Scholar 

  • Chi OZ, Hunter C, Liu X, Weiss HR (2010b) The effects of isoflurane pretreatment on cerebral blood flow, capillary permeability, and oxygen consumption in focal cerebral ischemia in rats. Anesth Analg 110:1412–1418

    PubMed  CAS  Google Scholar 

  • Chileuitt L, Leber K, McCalden T, Weinstein PR (1996) Induced hypertension during ischemia reduces infarct area after temporary middle cerebral artery occlusion in rats. Surg Neurol 46:229–234

    PubMed  CAS  Google Scholar 

  • Cole DJ, Schell RM, Drummond JC, Patel PM, Mercantonio S (1992) Focal cerebral ischemia in rats: effect of phenylephrine-induced hypertension during reperfusion. J Neurosurg Anesthesiol 4:78–84

    PubMed  CAS  Google Scholar 

  • Connolly ES, Winfree CJ, Stern DM, Solomon RA, Pinsky DJ (1996) Procedural and strain-related variables significantly affect outcome in a murine model of focal cerebral ischemia. Neurosurgery 38:523–532

    PubMed  Google Scholar 

  • Constantinides C, Mean R, Jannsen BJ (2011) Effects of isoflurane anesthesia on the cardiovascular function of the C57BL/6 mouse. ILAR J 52:22–32

    Google Scholar 

  • Coyle P (1986) Different susceptibilities to cerebral infarction in spontaneously hypertensive (SHR) and normotensive Sprague–Dawley rats. Stroke 17:520–525

    PubMed  CAS  Google Scholar 

  • Coyle P, Odenheimer DJ, Sing CF (1984) Cerebral infarction after middle cerebral artery occlusion in progenies of spontaneously stroke-prone and normal rats. Stroke 15:711–716

    PubMed  CAS  Google Scholar 

  • Crowell RM, Olsson Y, Klatzo I, Ommaya A (1970) Temporary occlusion of the middle cerebral artery in the monkey: clinical and pathological observations. Stroke 1:439–448

    PubMed  CAS  Google Scholar 

  • Currie RW, Ellison JA, White RF, Feuerstein GZ, Wang X, Barone FC (2000) Benign focal ischemic preconditioning induces neuronal Hsp70 and prolonged astrogliosis with expression of Hsp27. Brain Res 863:169–181

    PubMed  CAS  Google Scholar 

  • Dawson DA, Furuya K, Gotoh J, Nakao Y, Hallenbeck JM (1999) Cerebrovascular hemodynamics and ischemic tolerance: lipopolysaccharide-induced resistance to focal cerebral ischemia is not due to changes in severity of the initial ischemic insult, but is associated with preservation of microvascular perfusion. J Cereb Blood Flow Metab 19:616–623

    PubMed  CAS  Google Scholar 

  • Drummond JC, Oh Y-S, Cole DJ, Shapiro HM (1989) Phenylephrine-induced hypertension reduces ischemia following middle cerebral artery occlusion in rats. Stroke 20:1538–1544

    PubMed  CAS  Google Scholar 

  • Duverger D, MacKenzie ET (1988) The quantification of cerebral infarction following focal ischemia in the rat: influence of strain, arterial pressure, blood glucose concentration, and age. J Cereb Blood Flow Metab 8:449–461

    PubMed  CAS  Google Scholar 

  • Furuya K, Zhu L, Kawahara N, Abe O, Kirino T (2005) Differences in infarct evolution between lipopolysaccharide-induced tolerant and nontolerant conditions to focal cerebral ischemia. J Neurosurg 103:715–723

    PubMed  Google Scholar 

  • Gao H, Liu Y, Lu S, Xiang B, Wang C (2006) A reversible middle cerebral artery occlusion model using intraluminal balloon technique in monkeys. J Stroke Cerebrovasc Dis 15:202–208

    PubMed  Google Scholar 

  • Gao-Yu C, Cong-Yina D, Li-Jun Z, Fei L, Hua F (2011) Effects of hyperbaric oxygen preconditioning on energy metabolism and glutamate level in the peri-infarct area following permanent MCAO. Undersea Hyperb Med 38:91–99

    PubMed  Google Scholar 

  • Ginsberg MD, Prado R, Dietrich WD, Busto R, Watson BD (1987) Hyperglycemia reduces the extent of cerebral infarction in rats. Stroke 18:570–574

    PubMed  CAS  Google Scholar 

  • 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 29:166–175

    PubMed  CAS  Google Scholar 

  • Hashimoto M, Zhao L, Nowak TS Jr (2008) Temporal thresholds for infarction and hypothermic protection in Long-Evans rats: factors affecting apparent “reperfusion injury” after transient focal ischemia. Stroke 39:421–426

    PubMed  Google Scholar 

  • He Z, Yamawaki T, Yang S, Day AL, Simpkins JW, Naritomi H (1999) Experimental model of small deep infarcts involving the hypothalamus in rats: changes in body temperature and postural reflex. Stroke 30:2743–2751

    PubMed  CAS  Google Scholar 

  • Henrich-Noack P, Striggow F, Reiser G, Reymann KG (2006) Preconditioning with thrombin can be protective or worsen damage after endothelin-1-induced focal ischemia in rats. J Neurosci Res 83:469–475

    PubMed  CAS  Google Scholar 

  • Herrmann O, Tarabin V, Suzuki S, Attigah N, Coserea I, Schneider A, Vogel J, Prinz S, Schwab S, Monyer H, Brombacher F, Schwaninger M (2003) Regulation of body temperature and neuroprotection by endogenous intrerleukin-6 in cerebral ischemia. J Cereb Blood Flow Metab 23:406–415

    PubMed  CAS  Google Scholar 

  • Hiramatsu K, Kassell NF, Goto Y, Soleau S, Lee KS (1993) A reproducible model of reversible, focal, neocortical ischemia in Sprague–Dawley rat. Acta Neurochir (Wien) 120:66–71

    CAS  Google Scholar 

  • Hossmann K-A (1988) Resuscitation potentials after prolonged global cerebral ischemia in cats. Crit Care Med 16:964–971

    PubMed  CAS  Google Scholar 

  • Hoyte LC, Papadakis M, Barber PA, Buchan AM (2006) Improved regional cerebral blood flow is important for the protection seen in a mouse model of late phase ischemic preconditioning. Brain Res 1121:231–237

    PubMed  CAS  Google Scholar 

  • Hu Q, Ma Q, Zhan Y, He Z, Tang J, Zhou C, Zhang J (2011) Isoflurane enhanced hemorrhagic transformation by impairing antioxidant enzymes in hyperglycemic rats with middle cerebral artery occlusion. Stroke 42:1750–1756

    PubMed  CAS  Google Scholar 

  • 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 12:359–370

    PubMed  CAS  Google Scholar 

  • Kader A, Brisman MH, Maraire N, Huh J-T, Solomon RA (1992) The effect of mild hypothermia on permanent focal ischemia in the rat. Neurosurgery 31:1056–1061

    PubMed  CAS  Google Scholar 

  • Kamada H, Yu F, Nito F, Chan PH (2007) Influence of hyperglycemia on oxidative stress and matrix metalloproteinase-9 activation after focal cerebral ischemia/reperfusion in rats. Stroke 38:1044–1049

    PubMed  CAS  Google Scholar 

  • Kametsu Y, Osuga S, Hakim AM (2003) Apoptosis occurs in the penumbra zone during short-duration focal ischemia in the rat. J Cereb Blood Flow Metab 23:416–422

    PubMed  Google Scholar 

  • Kanemitsu H, Nakagomi T, Tamura A, Tsuchiya T, Kono G, Sano K (2002) Differences in the extent of primary ischemic damage between middle cerebral artery coagulation and intraluminal occlusion models. J Cereb Blood Flow Metab 22:1196–1204

    PubMed  CAS  Google Scholar 

  • Kapinya KJ, Löwl D, Fütterer C, Maurer M, Waschke KF, Isaev NK, Dirnagl U (2002) Tolerance against ischemic neuronal injury can be induced by volatile anesthetics and is inducible NO synthase dependent. Stroke 33:1889–1898

    PubMed  CAS  Google Scholar 

  • Kaplan B, Brint S, Tanabe J, Jacewicz M, Wang X-J, Pulsinelli WA (1991) Temporal thresholds for neocortical infarction in rats subjected to reversible focal cerebral ischemia. Stroke 22:1032–1039

    PubMed  CAS  Google Scholar 

  • Katchanov J, Waeber C, Gertz K, Gietz A, Winter B, Bruck W, Dirnagl U, Veh RW, Endres M (2003) Selective neuronal vulnerability following mild focal brain ischemia in the mouse. Brain Pathol 13:452–464

    PubMed  Google Scholar 

  • Kawaguchi M, Kimbro JR, Drummond JC, Cole DJ, Kelly PJ, Patel PM (2000) Isoflurane delays but does not prevent cerebral infarction in rats subjected to focal ischemia. Anesthesiology 92:1335–1342

    PubMed  CAS  Google Scholar 

  • Kawahara N, Ruetzler CA, Mies G, Klatzo I (1999) Cortical spreading depression increases protein synthesis and upregulates basic fibroblast growth factor. Exp Neurol 158:27–36

    PubMed  CAS  Google Scholar 

  • Kawai N, Keep RF, Betz AL (1997) Hyperglycemia and the vascular effects of cerebral ischemia. Stroke 28:149–154

    PubMed  CAS  Google Scholar 

  • Kent TA, Soukup VM, Fabian RH (2001) Heterogeneity affecting outcome from acute stroke therapy: making reperfusion worse. Stroke 32:2318–2327

    PubMed  CAS  Google Scholar 

  • Keum S, Marchuk DA (2009) A locus mapping to mouse chromosome 7 determines infarct volume in a mouse model of ischemic stroke. Circ Cardiovasc Genet 2:591–598

    PubMed  CAS  Google Scholar 

  • Koizumi J, Yoshida Y, Nakazawa T, Ooneda G (1986) Experimental studies of ischemic brain edema. 1. A new experimental model of cerebral embolism in rats in which recirculation can be introduced in the ischemic area. Jpn J Stroke 8:1–8

    Google Scholar 

  • Korematsu K, Goto S, Nagahiro S, Ushio Y (1993) Changes of immunoreactivity for synaptophysin (‘protein p38’) following a transient cerebral ischemia in the rat striatum. Brain Res 616:320–324

    PubMed  CAS  Google Scholar 

  • Kuraoka M, Furuta T, Matsuwaki T, Omatsu T, Ishii Y, Kyuwa S, Yoshikawa Y (2009) Direct experimental occlusion of the distal middle cerebral artery induces high reproducibility of brain ischemia in mice. Exp Anim 58:19–29

    PubMed  CAS  Google Scholar 

  • Kuroiwa T, Bonnekoh P, Hossmann K-A (1990) Prevention of postischemic hyperthermia prevents ischemic injury of CA1 neurons in gerbils. J Cereb Blood Flow Metab 10:550–556

    PubMed  CAS  Google Scholar 

  • Lattermann R, Schricker T, Wachter U, Georgieff M, Goertz A (2001) Understanding the mechanisms by which isoflurane modifies the hyperglycemic response to surgery. Anesth Analg 93:121–127

    PubMed  CAS  Google Scholar 

  • Lauritzen M, Dreier JP, Fabricius M, Hartings JA, Graf R, Strong AJ (2011) 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

    PubMed  Google Scholar 

  • Li Y, Chopp M, Jiang N, Zhang ZG, Zaloga C (1995) Induction of DNA fragmentation after 10 to 120 minutes of focal cerebral ischemia in rats. Stroke 26:1252–1257

    PubMed  CAS  Google Scholar 

  • Li F, Omae T, Fisher M (1999) Spontaneous hyperthermia and its mechanism in the intraluminal suture middle cerebral artery occlusion model of rats. Stroke 30:2464–2470

    PubMed  CAS  Google Scholar 

  • 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 1191:157–167

    PubMed  CAS  Google Scholar 

  • Ma J, Zhao L, Nowak TS Jr (2006) Selective, reversible occlusion of the middle cerebral artery in rats by an intraluminal approach: optimized filament design and methodology. J Neurosci Methods 156:76–83

    PubMed  Google Scholar 

  • Majid A, He YY, Gidday JM, Kaplan SS, Gonzales ER, Park PS, Fenstermacher JD, Wei L, Choi DW, Hsu CY (2000) Differences in vulnerability to permanent focal cerebral ischemia among 3 common mouse strains. Stroke 31:2707–2714

    PubMed  CAS  Google Scholar 

  • Marcoux FW, Morawetz RB, Crowell RM, DeGirolami U, Halsey JH (1982) Differential regional vulnerability in transient focal cerebral ischemia. Stroke 13:339–346

    PubMed  CAS  Google Scholar 

  • Markgraf CG, Kraydieh S, Prado R, Watson BD, Dietrich WD, Ginsberg MD (1993) Comparative histopathologic consequences of photothrombotic occlusion of the distal middle cerebral artery in Sprague–Dawley and Wistar rats. Stroke 24:286–293

    PubMed  CAS  Google Scholar 

  • Matějovská I, Bernášková K, Krýsl D, Mareš J (2008) Influence of melatonin pretreatment and preconditioning by hypobaric hypoxia on the development of cortical photothrombotic ischemic lesion. Physiol Res 57:283–288

    PubMed  Google Scholar 

  • Matsushima K, Hakim A (1995) Transient forebrain ischemia protects against subsequent focal cerebral ischemia without changing cerebral perfusion. Stroke 26:1047–1052

    PubMed  CAS  Google Scholar 

  • Matsushima K, Hogan MJ, Hakim AM (1996) Cortical spreading depression protects against subsequent focal cerebral ischemia in rats. J Cereb Blood Flow Metab 16:221–226

    PubMed  CAS  Google Scholar 

  • McColl BW, Carswell HV, McCulloch J, Horsburgh K (2004) Extension of cerebral hypoperfusion and ischaemic pathology beyond MCA territory after intraluminal filament occlusion in C57Bl/6 J mice. Brain Res 997:14–22

    Google Scholar 

  • Meade CA, Figueredo-Cardenas G, Fusco F, Nowak TS Jr, Pulsinelli WA, Reiner A (2000) Transient global ischemia in rats yields striatal projection neuron and interneuron loss resembling that in Huntington’s disease. Exp Neurol 166:307–323

    PubMed  CAS  Google Scholar 

  • Meden P, Overgaard K, Pedersen H, Boysen G (1994) The influence of body temperature on infarct volume and thrombolytic therapy in a rat embolic stroke model. Brain Res 647:131–138

    PubMed  CAS  Google Scholar 

  • Meisel C, Prass K, Braun J, Victorov I, Wolf T, Megow D, Halle E, Volk H-D, Dirnagl U, Meisel A (2004) Preventive antibacterial treatment improves the general medical and neurological outcome in a mouse model of stroke. Stroke 35:2–6

    PubMed  CAS  Google Scholar 

  • Morikawa E, Ginsberg MD, Dietrich WD, Duncan RC, Kraydieh S, Globus MY-T, Busto R (1992) The significance of brain temperature in focal cerebral ischemia: histopathological consequences of middle cerebral artery occlusion in the rat. J Cereb Blood Flow Metab 12:380–389

    PubMed  CAS  Google Scholar 

  • Mullins PG, Reid DG, Hockings PD, Hadingham SJ, Campbell CA, Chalk JB, Doddrell DM (2001) Ischaemic preconditioning in the rat brain: a longitudinal magnetic resonance imaging (MRI) study. NMR Biomed 14:204–209

    PubMed  CAS  Google Scholar 

  • Muramatsu H, Karikó K, Welsh FA (2004) Induction of tolerance to focal ischemia in rat brain: dissociation between cortical lesioning and spreading depression. J Cereb Blood Flow Metab 24:1167–1171

    PubMed  CAS  Google Scholar 

  • Nagasawa H, Kogure K (1989) Correlation between cerebral blood flow and histological changes in a new rat model of middle cerebral artery occlusion. Stroke 20:1037–1043

    PubMed  CAS  Google Scholar 

  • Nedergaard M, Astrup J (1986) Infarct rim: effect of hyperglycemia on direct current potential and [14  C]2-deoxyglucose phosphorylation. J Cereb Blood Flow Metab 6:607–615

    PubMed  CAS  Google Scholar 

  • Nishino K, Nowak TS Jr (2004) Time course and cellular distribution of hsp27 and hsp72 stress protein expression in a quantitative gerbil model of ischemic injury and tolerance: thresholds for hsp72 induction and hilar lesioning in the context of ischemic preconditioning. J Cereb Blood Flow Metab 24:167–178

    PubMed  CAS  Google Scholar 

  • Oliff HS, Weber E, Miyazaki B, Marek P (1995) Infarct volume varies with rat strain and vendor in focal cerebral ischemia induced by transcranial middle cerebral artery occlusion. Brain Res 699:329–331

    PubMed  CAS  Google Scholar 

  • Otori T, Greenberg JH, Welsh FA (2003) Cortical spreading depression causes a long-lasting decrease in cerebral blood flow and induces tolerance to permanent focal ischemia in rat brain. J Cereb Blood Flow Metab 23:43–50

    PubMed  Google Scholar 

  • Özdemir YG, Bolay H, Erdem E, Dalkara T (1999) Occlusion of the MCA by an intraluminal filament may cause disturbances in the hippocampal blood flow due to anomalies of circle of Willis and filament thickness. Brain Res 822:260–264

    PubMed  Google Scholar 

  • Pappius HM (1981) Local cerebral glucose utilization in thermally traumatized rat brain. Ann Neurol 9:484–491

    PubMed  CAS  Google Scholar 

  • Patel PM, Drummond GR, Cole DJ, Kelly PJ, Watson M (1998) Isoflurane and pentobarbital reduce the frequency of transient ischemic depolarizations during focal ischemia in rats. Anesth Analg 86:773–780

    PubMed  CAS  Google Scholar 

  • Pedrono E, Durukan A, Strbian D, Marinkovic I, Shekhar S, Pitkonen M, Abo-Ramadan U, Tatlisumak T (2010) An optimized mouse model for transient ischemic attack. J Neuropathol Exp Neurol 69:188–195

    PubMed  Google Scholar 

  • Prado R, Ginsberg MD, Dietrich WD, Watson BD, Busto R (1988) Hyperglycemia increases infarct size in collaterally perfused but not end-arterial vascular territories. J Cereb Blood Flow Metab 8:186–192

    PubMed  CAS  Google Scholar 

  • Pulsinelli WA, Brierley JB, Plum F (1982) Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol 11:491–498

    PubMed  CAS  Google Scholar 

  • Purcell JE, Lenhard SC, White RF, Schaeffer T, Barone FC, Chandra S (2003) Strain-dependent response to cerebral ischemic preconditioning: differences between spontaneously hypertensive and stroke prone spontaneously hypertensive rats. Neurosci Lett 339:151–155

    PubMed  CAS  Google Scholar 

  • Quast MJ, Wei J, Huang NC, Brunder DG, Sell SL, Gonzalez JM, Hillman GR, Kent TA (1997) Perfusion deficit parallels exacerbation of cerebral ischemia/reperfusion injury in hyperglycemic rats. J Cereb Blood Flow Metab 17:553–559

    PubMed  CAS  Google Scholar 

  • Ren Y, Hashimoto M, Pulsinelli WA, Nowak TS Jr (2004) Hypothermic protection in rat focal ischemia models: strain differences and relevance to “reperfusion injury”. J Cereb Blood Flow Metab 24:42–53

    PubMed  Google Scholar 

  • Ridenour TR, Warner DS, Todd MM, McAllister AC (1992) Mild hypothermia reduces infarct size resulting from temporary but not permanent focal ischemia in rats. Stroke 23:733–738

    PubMed  CAS  Google Scholar 

  • Robinson RG, Shoemaker WJ, Schlumpf M, Valk T, Bloom FE (1975) Effect of experimental cerebral infarction in rat brain on catecholamines and behaviour. Nature 255:332–334

    PubMed  CAS  Google Scholar 

  • 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 17:857–864

    PubMed  CAS  Google Scholar 

  • Sharkey J, Ritchie IM, Kelly PAT (1993) Perivascular microapplication of endothelin-1: a new model of focal cerebral ischaemia in the rat. J Cereb Blood Flow Metab 13:865–871

    PubMed  CAS  Google Scholar 

  • Shigeno T, Teasdale GM, McCulloch J, Graham DI (1985) Recirculation model following MCA occlusion in rats. Cerebral blood flow, cerebrovascular permeability, and brain edema. J Neurosurg 63:272–277

    PubMed  CAS  Google Scholar 

  • Sick TJ, Tang R, Pérez-Pinzón MA (1999) Cerebral blood flow does not mediate the effect of brain temperature on recovery of extracellular potassium ion activity after transient focal ischemia in the rat. Brain Res 821:400–406

    PubMed  CAS  Google Scholar 

  • Smith M-L, Auer RN, Siesjo BK (1984) The density and distribution of ischemic brain injury in the rat following 2–10 min of forebrain ischemia. Acta Neuropathol (Berl) 64:319–332

    CAS  Google Scholar 

  • Smrcka M, Ogilvy CS, Crow RJ, Maynard KI, Kawamata T, Ames A III (1998) Induced hypertension improves regional blood flow and protects against infarction during focal ischemia: time course of changes in blood flow measured by laser Doppler imaging. Neurosurgery 42:617–625

    PubMed  CAS  Google Scholar 

  • Sommer C (2008) Ischemic preconditioning: postischemic structural changes in brain. J Neuropathol Exp Neurol 67:85–92

    PubMed  CAS  Google Scholar 

  • Stagliano NE, Pérez-Pinzón MA, Moskowitz MA, Huang PL (1999) Focal ischemic preconditioning induces rapid tolerance to middle cerebral artery occlusion in mice. J Cereb Blood Flow Metab 19:757–761

    PubMed  CAS  Google Scholar 

  • Sutherland BA, Papadakis M, Chen R-L, Buchan AM (2011) Cerebral blood flow alteration in neuroprotection following focal ischemia. J Physiol 589:4105–4114

    PubMed  CAS  Google Scholar 

  • Takeda Y, Zhao L, Jacewicz M, Pulsinelli W, Nowak TS Jr (2011) Metabolic and perfusion responses to peri-infarct depolarization during focal ischemia in the spontaneously hypertensive rat: dominant contribution of sporadic CBF decrements to infarct expansion. J Cereb Blood Flow Metab 31:1863–1873

    PubMed  Google Scholar 

  • Tamura A, Graham D, McCulloch J, Teasdale G (1981a) Focal cerebral ischemia in the rat: 1. Description of technique and early neuropathological consequences following middle cerebral artery occlusion. J Cereb Blood Flow Metab 1:53–60

    PubMed  CAS  Google Scholar 

  • Tamura A, Graham DI, McCulloch J, Teasdale GM (1981b) Focal cerebral ischaemia in the rat: 2. Regional cerebral blood flow determined by [14  C]iodoantipyrine autoradiography following middle cerebral artery occlusion. J Cereb Blood Flow Metab 1:61–69

    PubMed  CAS  Google Scholar 

  • Tanaka K, Kawano T, Tomino T, Kawano H, Okada T, Oshita S, Takahashi A, Nakaya Y (2009) Mechanisms of impaired glucose tolerance and insulin secretion during isoflurane anesthesia. Anesthesiology 111:1044–1051

    PubMed  CAS  Google Scholar 

  • Wang L, Kitano H, Hurn PD, Murphy SJ (2008) Estradiol attenuates neuroprotective benefits of isoflurane preconditioning in ischemic mouse brain. J Cereb Blood Flow Metab 28:1824–1834

    PubMed  CAS  Google Scholar 

  • Warner DS, Ludwig PS, Pearlstein R, Brinkhoust AD (1995) Halothane reduces focal ischemic injury in the rat when brain temperature is controlled. Anesthesiology 82:1237–1245

    PubMed  CAS  Google Scholar 

  • Watson B, Dietrich W, Watchel M, Ginsberg M (1985) Induction of reproducible brain infarction by photochemically initiated thrombosis. Ann Neurol 17:497–504

    PubMed  CAS  Google Scholar 

  • West GA, Golshani KJ, Doyle KP, Lessov NS, Hobbs TR, Kohama SG, Pike MM, Kroenke CD, Grafe MR, Spector MD, Tobar ET, Simon RP, Stenzel-Poore MP (2009) A new model of cortical stroke in the rhesus macaque. J Cereb Blood Flow Metab 29:1175–1186

    PubMed  Google Scholar 

  • Xi GM, Wang HQ, He GH, Huang CF, Wei GY (2004) Evaluation of murine models of permanent focal cerebral ischemia. Chin Med J 117:389–394

    PubMed  Google Scholar 

  • Yanamoto H, Hong S-C, Soleau S, Kassell NF, Lee KS (1996) Mild postischemic hypothermia limits cerebral injury following transient focal ischemia in rat neocortex. Brain Res 718:207–211

    PubMed  CAS  Google Scholar 

  • Yanamoto H, Hashimoto N, Nagata I, Kikuchi H (1998) Infarct tolerance against temporary focal ischemia following spreading depression in rat brain. Brain Res 784:239–249

    PubMed  CAS  Google Scholar 

  • Yanamoto H, Nagata I, Niitsu Y, Zhang Z, Xue J-H, Sakai N, Kikuchi H (2001) Prolonged mild hypothermia therapy protects the brain against permanent focal ischemia. Stroke 32:232–239

    PubMed  CAS  Google Scholar 

  • Yip PK, He YY, Hsu CY, Garg N, Marangos P, Hogan EL (1991) Effect of plasma glucose on infarct size in focal cerebral ischemia-reperfusion. Neurology 41:899–905

    PubMed  CAS  Google Scholar 

  • Zausinger S, Baethmann A, Schmid-Elsaesser R (2002) Anesthetic methods in rats determine outcome after experimental focal cerebral ischemia: mechanical ventilation is required to obtain controlled experimental conditions. Brain Res Protoc 9:112–121

    CAS  Google Scholar 

  • Zea Longa E, Weinstein PR, Carlson S, Cummins R (1989) Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20:84–91

    Google Scholar 

  • Zhan X, Kim C, Sharp FR (2008) Very brief focal ischemia simulating transient ischemic attacks (TIAs) can injure brain and induce Hsp70 protein. Brain Res 1234:183–197

    PubMed  CAS  Google Scholar 

  • Zhang J, Yang Z-J, Klaus JA, Koehler RC, Huang J (2008) Delayed tolerance with repetitive transient focal ischemic preconditioning in the mouse. Stroke 39:967–974

    PubMed  Google Scholar 

  • Zhao L, Nowak TS Jr. (2006a) Cortical lesions that suppress resting cerebral blood flow and metabolism are required for robust neuroprotection by focal ischemic preconditioning in the Spontaneously Hypertensive Rat Program No. 680.4 [Abstract]. 2006 Neuroscience Meeting Planner. Atlanta, GA: Society for Neuroscience [Online]

    Google Scholar 

  • Zhao L, Nowak TS Jr (2006b) CBF changes associated with focal ischemic preconditioning in the spontaneously hypertensive rat. J Cereb Blood Flow Metab 26:1128–1140

    PubMed  CAS  Google Scholar 

  • Zhao L, Nowak TS Jr. (2011a) Anesthesia confounds in experimental stroke and preconditioning [Abstract]. Stroke 42:e213 [Online]

    Google Scholar 

  • Zhao L, Nowak TS Jr. (2011b) Attenuated peri-infarct depolarization and improved CBF following lesion-induced preconditioning in the Spontaneously Hypertensive Rat Abstract 311, Scientific Program [Abstract]. XXVth International Symposium on Cerebral Blood Flow and Metabolism, Barcelona [Online]

    Google Scholar 

  • Zhao L, Nowak TS Jr. (2011c) Blood glucose variability in preconditioning studies: confounding effects of prior isoflurane and buprenorphine exposure during experimental stroke Program No. 63.14 [Abstract]. 2011 Neuroscience Meeting Planner. Washington, DC: Society for Neuroscience [Online]

    Google Scholar 

  • Zhao Q, Memezawa H, Smith M-L, Siesjö BK (1994) Hyperthermia complicates middle cerebral artery occlusion induced by intraluminal filament. Brain Res 649:253–259

    PubMed  CAS  Google Scholar 

  • Zhu CZ, Auer RN (1995) Graded hypotension and MCA occlusion duration: effect in transient focal ischemia. J Cereb Blood Flow Metab 15:980–988

    PubMed  CAS  Google Scholar 

  • Zhu W, Wang L, Zhang L, Palmateer JM, Libal NL, Hurn PD, Herson PS, Murphy SJ (2010) Isoflurane preconditioning neuroprotection in experimental focal stroke is androgen-dependent in male mice. Neuroscience 169:758–769

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Neurology, University of Tennessee Health Science Center, 855 Monroe Ave., Link 415, Memphis, TN, 38163, USA

    Thaddeus S. Nowak Jr. & Liang Zhao

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  1. Thaddeus S. Nowak Jr.
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  2. Liang Zhao
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Correspondence to Thaddeus S. Nowak Jr. .

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  1. , Departments of Neurosurgery, Washington University School of Medicine, South Kingshighway Boulevard, St. Louis, 63110, Missouri, USA

    Jeffrey M. Gidday

  2. , Department of Neurology, University of Miami Miller School of Med, Miami, 33136, Florida, USA

    Miguel A. Perez-Pinzon

  3. Loma Linda University, 11234 Anderson Street, Room 2562B, Loma Linda, 92354, California, USA

    John H. Zhang

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Nowak, T.S., Zhao, L. (2013). Conditioning Studies in Focal Cerebral Ischemia: Model Selection, Physiological Monitoring, and Other Methodological Issues. In: Gidday, J., Perez-Pinzon, M., Zhang, J. (eds) Innate Tolerance in the CNS. Springer Series in Translational Stroke Research. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-9695-4_13

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