Advertisement

White Matter Injury in Global Cerebral Ischemia

  • Shinichi Nakao
  • Yan Xu
Chapter
Part of the Springer Series in Translational Stroke Research book series (SSTSR, volume 4)

Abstract

In chronic cerebral hypoperfusion due to aging, global cerebral ischemia after cardiac arrest, acute and chronic hypoxia in asymptomatic stroke, and diffuse axonal injury after traumatic brain injury, white matter lesions occur not only as a result of secondary degeneration caused by neuronal injuries in the gray matter, but also as a direct consequence of the primary ischemic insults. Not enough attention has been directed to the molecular and cellular mechanisms of white matter injuries in humans. Failures in past stroke therapyclinical trials are partly attributed to misrepresentation of the relevance of white matter to human brain pathology in the preclinical data. Most rodent models either ignore white matter's contribution to the injury process and recovery, or inadequately account for this contribution due to a significantly lower proportion of white matter in the rodent brain compared to the human brain. Future development of effective therapies should place an equal emphasis on gray and white matter injuries.

Keywords

White Matter Traumatic Brain Injury Cardiac Arrest Axonal Injury Global Cerebral Ischemia 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgment

  The authors would like to acknowledge the support from the National Institutes of Health (R01NS036124) and from the Department of Anesthesiology at the University of Pittsburgh.

References

  1. Arai K, Lo EH (2009) Experimental models for analysis of oligodendrocyte pathophysiology in stroke. Exp Transl Stroke Med 1:6CrossRefPubMedGoogle Scholar
  2. Arbelaez A, Castillo M, Mukherji SK (1999) Diffusion-weighted MR imaging of global cerebral anoxia. AJNR Am J Neuroradiol 20:999–1007PubMedGoogle Scholar
  3. Berger T, Walz W, Schnitzer J, Kettenmann H (1992) Gaba- and glutamate-activated currents in glial cells of the mouse corpus callosum slice. J Neurosci Res 31:21–27CrossRefPubMedGoogle Scholar
  4. Büki A, Siman R, Trojanowski JQ, Povlishock JT (1999) The role of calpain-mediated spectrin proteolysis in traumatically induced axonal injury. J Neuropathol Exp Neurol 58:365–375CrossRefPubMedGoogle Scholar
  5. Carty ML, Wixey JA, Colditz PB, Buller KM (2008) Post-insult minocycline treatment attenuates hypoxia-ischemia-induced neuroinflammation and white matter injury in the neonatal rat: a comparison of two different dose regimens. Int J Dev Neurosci 26:477–485CrossRefPubMedGoogle Scholar
  6. Chatterton JE, Awobuluyi M, Premkumar LS, Takahashi H, Talantova M, Shin Y, Cui J, Tu S, Sevarino KA, Nakanishi N, Tong G, Lipton SA, Zhang D (2002) Excitatory glycine receptors containing the nr3 family of nmda receptor subunits. Nature 415:793–798CrossRefPubMedGoogle Scholar
  7. Chen XH, Johnson VE, Uryu K, Trojanowski JQ, Smith DH (2009) A lack of amyloid beta plaques despite persistent accumulation of amyloid beta in axons of long-term survivors of traumatic brain injury. Brain Pathol 19:214–223CrossRefPubMedGoogle Scholar
  8. Choi SP, Park HK, Park KN, Kim YM, Ahn KJ, Choi KH, Lee WJ, Jeong SK (2008) The density ratio of grey to white matter on computed tomography as an early predictor of vegetative state or death after cardiac arrest. Emerg Med J 25:666–669CrossRefPubMedGoogle Scholar
  9. Deng Y, Thompson BM, Gao X, Hall ED (2007) Temporal relationship of peroxynitrite-induced oxidative damage, calpain-mediated cytoskeletal degradation and neurodegeneration after traumatic brain injury. Exp Neurol 205:154–165CrossRefPubMedGoogle Scholar
  10. Desmond DW (2002) Cognition and white matter lesions. Cerebrovasc Dis 13(Suppl 2):53–57CrossRefPubMedGoogle Scholar
  11. Dewar D, Dawson D (1995) Tau protein is altered by focal cerebral ischaemia in the rat: an immunohistochemical and immunoblotting study. Brain Res 684:70–78CrossRefPubMedGoogle Scholar
  12. Dewar D, Yam P, McCulloch J (1999) Drug development for stroke: importance of protecting cerebral white matter. Eur J Pharmacol 375:41–50CrossRefPubMedGoogle Scholar
  13. Dewar D, Underhill SM, Goldberg MP (2003) Oligodendrocytes and ischemic brain injury. J Cerebr Blood Flow Metabol 23:263–274CrossRefGoogle Scholar
  14. Els T, Kassubek J, Kubalek R, Klisch J (2004) Diffusion-weighted mri during early global cerebral hypoxia: a predictor for clinical outcome? Acta Neurol Scand 110:361–367CrossRefPubMedGoogle Scholar
  15. Erkinjuntti T, Roman G, Gauthier S (2004) Treatment of vascular dementia-evidence from clinical trials with cholinesterase inhibitors. J Neurol Sci 226:63–66CrossRefPubMedGoogle Scholar
  16. Follett PL, Rosenberg PA, Volpe JJ, Jensen FE (2000) Nbqx attenuates excitotoxic injury in developing white matter. J Neurosci 20:9235–9241PubMedGoogle Scholar
  17. Gennarelli TA, Thibault LE, Adams JH, Graham DI, Thompson CJ, Marcincin RP (1982) Diffuse axonal injury and traumatic coma in the primate. Ann Neurol 12:564–574CrossRefPubMedGoogle Scholar
  18. Gitler D, Spira ME (1998) Real time imaging of calcium-induced localized proteolytic activity after axotomy and its relation to growth cone formation. Neuron 20:1123–1135CrossRefPubMedGoogle Scholar
  19. Gladstone DJ, Black SE, Hakim AM (2002) Toward wisdom from failure: lessons from neuroprotective stroke trials and new therapeutic directions. Stroke 33:2123–2136CrossRefPubMedGoogle Scholar
  20. Goldin A, Beckman JA, Schmidt AM, Creager MA (2006) Advanced glycation end products: sparking the development of diabetic vascular injury. Circulation 114:597–605CrossRefPubMedGoogle Scholar
  21. Gultekin SH, Smith TW (1994) Diffuse axonal injury in craniocerebral trauma. A comparative histologic and immunohistochemical study. Arch Pathol Lab Med 118:168–171PubMedGoogle Scholar
  22. Heurteaux C, Bertaina V, Widmann C, Lazdunski M (1993) K+ channel openers prevent global ischemia-induced expression of c-fos, c-jun, heat shock protein, and amyloid beta-protein precursor genes and neuronal death in rat hippocampus. Proc Natl Acad Sci USA 90: 9431–9435CrossRefPubMedGoogle Scholar
  23. Hewlett KA, Corbett D (2006) Delayed minocycline treatment reduces long-term functional deficits and histological injury in a rodent model of focal ischemia. Neuroscience 141:27–33CrossRefPubMedGoogle Scholar
  24. Hirko AC, Dallasen R, Jomura S, Xu Y (2008) Modulation of inflammatory responses after global ischemia by transplanted umbilical cord matrix stem cells. Stem Cells 26:2893–2901CrossRefPubMedGoogle Scholar
  25. Honda F, Imai H, Ishikawa M, Kubota C, Shimizu T, Fukunaga M, Saito N (2006) Cilostazol attenuates gray and white matter damage in a rodent model of focal cerebral ischemia. Stroke 37:223–228CrossRefPubMedGoogle Scholar
  26. Imai H, Masayasu H, Dewar D, Graham DI, Macrae IM (2001) Ebselen protects both gray and white matter in a rodent model of focal cerebral ischemia. Stroke 32:2149–2154CrossRefPubMedGoogle Scholar
  27. Imai H, McCulloch J, Graham DI, Masayasu H, Macrae IM (2002) New method for the quantitative assessment of axonal damage in focal cerebral ischemia. J Cerebr Blood Flow Metabol 22:1080–1089CrossRefGoogle Scholar
  28. Inamasu J, Miyatake S, Nakatsukasa M, Koh H, Yagami T (2011) Loss of gray-white matter discrimination as an early ct sign of brain ischemia/hypoxia in victims of asphyxial cardiac arrest. Emerg Radiol 18:295–298CrossRefPubMedGoogle Scholar
  29. Irving EA, Yatsushiro K, McCulloch J, Dewar D (1997) Rapid alteration of tau in oligodendrocytes after focal ischemic injury in the rat: involvement of free radicals. J Cerebr Blood Flow Metabol 17:612–622CrossRefGoogle Scholar
  30. Irving EA, Bentley DL, Parsons AA (2001) Assessment of white matter injury following prolonged focal cerebral ischaemia in the rat. Acta Neuropathol 102:627–635PubMedGoogle Scholar
  31. Johnson VE, Stewart W (2012) Smith DH. Axonal pathology in traumatic brain injury, Exp NeurolGoogle Scholar
  32. Kamide T, Kitao Y, Takeichi T, Okada A, Mohri H, Schmidt AM, Kawano T, Munesue S, Yamamoto Y, Yamamoto H, Hamada J, Hori O (2012) Rage mediates vascular injury and inflammation after global cerebral ischemia. Neurochem Int 60:220–228CrossRefPubMedGoogle Scholar
  33. Káradóttir R, Cavelier P, Bergersen LH, Attwell D (2005) Nmda receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 438:1162–1166CrossRefPubMedGoogle Scholar
  34. Kubo K, Nakao S, Jomura S, Sakamoto S, Miyamoto E, Xu Y, Tomimoto H, Inada T, Shingu K (2009) Edaravone, a free radical scavenger, mitigates both gray and white matter damages after global cerebral ischemia in rats. Brain Res 1279:139–146CrossRefPubMedGoogle Scholar
  35. Lee EJ, Lee MY, Chen HY, Hsu YS, Wu TS, Chen ST, Chang GL (2005) Melatonin attenuates gray and white matter damage in a mouse model of transient focal cerebral ischemia. J Pineal Res 38:42–52CrossRefPubMedGoogle Scholar
  36. Liachenko S, Tang P, Hamilton RL, Xu Y (1998) A reproducible model of circulatory arrest and remote resuscitation in rats for NMR investigation. Stroke 29:1229–1238, discussion 1238-1229CrossRefPubMedGoogle Scholar
  37. Liachenko S, Tang P, Hamilton RL, Xu Y (2001) Regional dependence of cerebral reperfusion after circulatory arrest in rats. J Cerebr Blood Flow Metabol 21:1320–1329CrossRefGoogle Scholar
  38. Liachenko S, Tang P, Xu Y (2003) Deferoxamine improves early postresuscitation reperfusion after prolonged cardiac arrest in rats. J Cerebr Blood Flow Metabol 23:574–581CrossRefGoogle Scholar
  39. Lin B, Ginsberg MD, Busto R (2001) Hyperglycemic but not normoglycemic global ischemia induces marked early intraneuronal expression of beta-amyloid precursor protein. Brain Res 888:107–116CrossRefPubMedGoogle Scholar
  40. Liu K, Mori S, Takahashi HK, Tomono Y, Wake H, Kanke T, Sato Y, Hiraga N, Adachi N, Yoshino T, Nishibori M (2007) Anti-high mobility group box 1 monoclonal antibody ameliorates brain infarction induced by transient ischemia in rats. FASEB J 21:3904–3916CrossRefPubMedGoogle Scholar
  41. Luyt CE, Galanaud D, Perlbarg V, Vanhaudenhuyse A, Stevens RD, Gupta R, Besancenot H, Krainik A, Audibert G, Combes A, Chastre J, Benali H, Laureys S, Puybasset L (2012) Neuro imaging for coma E, recovery C. Diffusion tensor imaging to predict long-term outcome after cardiac arrest: a bicentric pilot study. Anesthesiology 117:1311–1321CrossRefPubMedGoogle Scholar
  42. Madden DJ, Bennett IJ, Burzynska A, Potter GG, Chen NK, Song AW (1822) Diffusion tensor imaging of cerebral white matter integrity in cognitive aging. Biochimica et Biophysica Acta 2012:386–400Google Scholar
  43. Manning SM, Talos DM, Zhou C, Selip DB, Park HK, Park CJ, Volpe JJ, Jensen FE (2008) Nmda receptor blockade with memantine attenuates white matter injury in a rat model of periventricular leukomalacia. J Neurosci 28:6670–6678CrossRefPubMedGoogle Scholar
  44. Matute C (2006) Oligodendrocyte nmda receptors: a novel therapeutic target. Trends Mol Med 12: 289–292CrossRefPubMedGoogle Scholar
  45. Matute C (2011) Glutamate and atp signalling in white matter pathology. J Anat 219:53–64CrossRefPubMedGoogle Scholar
  46. Maxwell WL, Watt C, Pediani JD, Graham DI, Adams JH, Gennarelli TA (1991) Localisation of calcium ions and calcium-atpase activity within myelinated nerve fibres of the adult guinea-pig optic nerve. J Anat 176:71–79PubMedGoogle Scholar
  47. Maxwell WL, Domleo A, McColl G, Jafari SS, Graham DI (2003) Post-acute alterations in the axonal cytoskeleton after traumatic axonal injury. J Neurotrauma 20:151–168CrossRefPubMedGoogle Scholar
  48. McCracken E, Fowler JH, Dewar D, Morrison S, McCulloch J (2002) Grey matter and white matter ischemic damage is reduced by the competitive ampa receptor antagonist, spd 502. J Cerebr Blood Flow Metabol 22:1090–1097CrossRefGoogle Scholar
  49. Metter RB, Rittenberger JC, Guyette FX, Callaway CW (2011) Association between a quantitative ct scan measure of brain edema and outcome after cardiac arrest. Resuscitation 82:1180–1185CrossRefPubMedGoogle Scholar
  50. Micu I, Jiang Q, Coderre E, Ridsdale A, Zhang L, Woulfe J, Yin X, Trapp BD, McRory JE, Rehak R, Zamponi GW, Wang W, Stys PK (2006) Nmda receptors mediate calcium accumulation in myelin during chemical ischaemia. Nature 439:988–992PubMedGoogle Scholar
  51. Miyamoto E, Tomimoto H, Nakao Si S, Wakita H, Akiguchi I, Miyamoto K, Shingu K (2001) Caudoputamen is damaged by hypocapnia during mechanical ventilation in a rat model of chronic cerebral hypoperfusion. Stroke 32:2920–2925CrossRefPubMedGoogle Scholar
  52. Miyamoto E, Nakao S, Tomimoto H, Wakita H, Yamada M, Masuzawa M, Takahira K, Sakamoto S, Shingu K (2004) Ketamine attenuates hypocapnia-induced neuronal damage in the caudoputamen in a rat model of chronic cerebral hypoperfusion. Neurosci Lett 354:26–29CrossRefPubMedGoogle Scholar
  53. Mustafa AG, Singh IN, Wang J, Carrico KM, Hall ED (2010) Mitochondrial protection after traumatic brain injury by scavenging lipid peroxyl radicals. J Neurochem 114:271–280PubMedGoogle Scholar
  54. Nizri E, Hamra-Amitay Y, Sicsic C, Lavon I, Brenner T (2006) Anti-inflammatory properties of cholinergic up-regulation: a new role for acetylcholinesterase inhibitors. Neuropharmacology 50:540–547CrossRefPubMedGoogle Scholar
  55. Okonkwo DO, Povlishock JT (1999) An intrathecal bolus of cyclosporin a before injury preserves mitochondrial integrity and attenuates axonal disruption in traumatic brain injury. J Cerebr Blood Flow Metabol 19:443–451CrossRefGoogle Scholar
  56. Pantoni L (2010) Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol 9:689–701CrossRefPubMedGoogle Scholar
  57. Pantoni L, Garcia JH (1997) Pathogenesis of leukoaraiosis: a review. Stroke 28:652–659CrossRefPubMedGoogle Scholar
  58. Pantoni L, Garcia JH, Gutierrez JA (1996) Cerebral white matter is highly vulnerable to ischemia. Stroke 27:1641–1646, discussion 1647CrossRefPubMedGoogle Scholar
  59. Patneau DK, Wright PW, Winters C, Mayer ML, Gallo V (1994) Glial cells of the oligodendrocyte lineage express both kainate- and ampa-preferring subtypes of glutamate receptor. Neuron 12:357–371CrossRefPubMedGoogle Scholar
  60. Pavlov VA, Tracey KJ (2005) The cholinergic anti-inflammatory pathway. Brain Behav Immun 19:493–499CrossRefPubMedGoogle Scholar
  61. Pluta R, Kida E, Lossinsky AS, Golabek AA, Mossakowski MJ, Wisniewski HM (1994) Complete cerebral ischemia with short-term survival in rats induced by cardiac arrest. I. Extracellular accumulation of Alzheimer's beta-amyloid protein precursor in the brain. Brain Res 649:323–328CrossRefPubMedGoogle Scholar
  62. Povlishock JT, Buki A, Koiziumi H, Stone J, Okonkwo DO (1999) Initiating mechanisms involved in the pathobiology of traumatically induced axonal injury and interventions targeted at blunting their progression. Acta Neurochir Suppl 73:15–20PubMedGoogle Scholar
  63. Salter MG, Fern R (2005) Nmda receptors are expressed in developing oligodendrocyte processes and mediate injury. Nature 438:1167–1171CrossRefPubMedGoogle Scholar
  64. Schäbitz WR, Li F, Fisher M (2000) The N-methyl-d-aspartate antagonist cns 1102 protects cerebral gray and white matter from ischemic injury following temporary focal ischemia in rats. Stroke 31:1709–1714CrossRefPubMedGoogle Scholar
  65. Schmidt R, Scheltens P, Erkinjuntti T, Pantoni L, Markus HS, Wallin A, Barkhof F, Fazekas F (2004) White matter lesion progression: a surrogate endpoint for trials in cerebral small-vessel disease. Neurology 63:139–144CrossRefPubMedGoogle Scholar
  66. Schmidt R, Grazer A, Enzinger C, Ropele S, Homayoon N, Pluta-Fuerst A, Schwingenschuh P, Katschnig P, Cavalieri M, Schmidt H, Langkammer C, Ebner F, Fazekas F (2011) Mri-detected white matter lesions: do they really matter? J Neural Transm 118:673–681CrossRefPubMedGoogle Scholar
  67. Storozheva ZI, Proshin AT, Sherstnev VV, Storozhevykh TP, Senilova YE, Persiyantseva NA, Pinelis VG, Semenova NA, Zakharova EI, Pomytkin IA (2008) Dicholine salt of succinic acid, a neuronal insulin sensitizer, ameliorates cognitive deficits in rodent models of normal aging, chronic cerebral hypoperfusion, and beta-amyloid peptide-(25–35)-induced amnesia. BMC Pharmacol 8:1CrossRefPubMedGoogle Scholar
  68. Strich S (1961) Shearing of nerve fibres as a cause of brain damage due to head injury: a pathological study of twenty cases. Lancet 278:443–448CrossRefGoogle Scholar
  69. Stys PK (1995) Protective effects of antiarrhythmic agents against anoxic injury in cns white matter. J Cerebr Blood Flow Metabol 15:425–432CrossRefGoogle Scholar
  70. Stys PK (1998) Anoxic and ischemic injury of myelinated axons in cns white matter: from mechanistic concepts to therapeutics. J Cerebr Blood Flow Metabol 18:2–25CrossRefGoogle Scholar
  71. Stys PK, Lipton SA (2007) White matter nmda receptors: an unexpected new therapeutic target? Trends Pharmacol Sci 28:561–566CrossRefPubMedGoogle Scholar
  72. Stys PK, Waxman SG, Ransom BR (1992) Ionic mechanisms of anoxic injury in mammalian cns white matter: role of na+ channels and na(+)-ca2+ exchanger. J Neurosci 12:430–439PubMedGoogle Scholar
  73. Takahashi S, Higano S, Ishii K, Matsumoto K, Sakamoto K, Iwasaki Y, Suzuki M (1993) Hypoxic brain damage: cortical laminar necrosis and delayed changes in white matter at sequential MR imaging. Radiology 189:449–456PubMedGoogle Scholar
  74. Tayeb HO, Yang HD, Price BH, Tarazi FI (2012) Pharmacotherapies for alzheimer's disease: beyond cholinesterase inhibitors. Pharmacol Ther 134:8–25CrossRefPubMedGoogle Scholar
  75. Tekkök SB, Goldberg MP (2001) Ampa/kainate receptor activation mediates hypoxic oligodendrocyte death and axonal injury in cerebral white matter. J Neurosci 21:4237–4248PubMedGoogle Scholar
  76. Tomimoto H, Wakita H, Akiguchi I, Nakamura S, Kimura J (1994) Temporal profiles of accumulation of amyloid beta/a4 protein precursor in the gerbil after graded ischemic stress. J Cerebr Blood Flow Metabol 14:565–573CrossRefGoogle Scholar
  77. Torbey MT, Selim M, Knorr J, Bigelow C, Recht L (2000) Quantitative analysis of the loss of distinction between gray and white matter in comatose patients after cardiac arrest. Stroke 31: 2163–2167CrossRefPubMedGoogle Scholar
  78. Tsuruta R, Fujita M, Ono T, Koda Y, Koga Y, Yamamoto T, Nanba M, Shitara M, Kasaoka S, Maruyama I, Yuasa M, Maekawa T (2010) Hyperglycemia enhances excessive superoxide anion radical generation, oxidative stress, early inflammation, and endothelial injury in forebrain ischemia/reperfusion rats. Brain Res 1309:155–163CrossRefPubMedGoogle Scholar
  79. Ueno Y, Zhang N, Miyamoto N, Tanaka R, Hattori N, Urabe T (2009) Edaravone attenuates white matter lesions through endothelial protection in a rat chronic hypoperfusion model. Neuroscience 162:317–327CrossRefPubMedGoogle Scholar
  80. Vicente E, Degerone D, Bohn L, Scornavaca F, Pimentel A, Leite MC, Swarowsky A, Rodrigues L, Nardin P, de Almeida LM, Gottfried C, Souza DO, Netto CA, Goncalves CA (2009) Astroglial and cognitive effects of chronic cerebral hypoperfusion in the rat. Brain Res 1251:204–212CrossRefPubMedGoogle Scholar
  81. Wakita H, Tomimoto H, Akiguchi I, Kimura J (1994) Glial activation and white matter changes in the rat brain induced by chronic cerebral hypoperfusion: an immunohistochemical study. Acta Neuropathol 87:484–492CrossRefPubMedGoogle Scholar
  82. Wakita H, Tomimoto H, Akiguchi I, Kimura J (1995) Protective effect of cyclosporin a on white matter changes in the rat brain after chronic cerebral hypoperfusion. Stroke 26:1415–1422CrossRefPubMedGoogle Scholar
  83. Wakita H, Tomimoto H, Akiguchi I, Kimura J (1998) Dose-dependent, protective effect of fk506 against white matter changes in the rat brain after chronic cerebral ischemia. Brain Res 792: 105–113CrossRefPubMedGoogle Scholar
  84. Wakita H, Tomimoto H, Akiguchi I, Lin JX, Miyamoto K, Oka N (1999) A cyclooxygenase-2 inhibitor attenuates white matter damage in chronic cerebral ischemia. Neuroreport 10:1461–1465CrossRefPubMedGoogle Scholar
  85. Wang L, Yushmanov VE, Liachenko SM, Tang P, Hamilton RL, Xu Y (2002) Late reversal of cerebral perfusion and water diffusion after transient focal ischemia in rats. J Cerebr Blood Flow Metabol 22:253–261CrossRefGoogle Scholar
  86. Wang J, Zhang HY, Tang XC (2010) Huperzine a improves chronic inflammation and cognitive decline in rats with cerebral hypoperfusion. J Neurosci Res 88:807–815PubMedGoogle Scholar
  87. Watanabe T, Zhang N, Liu M, Tanaka R, Mizuno Y, Urabe T (2006) Cilostazol protects against brain white matter damage and cognitive impairment in a rat model of chronic cerebral hypoperfusion. Stroke 37:1539–1545CrossRefPubMedGoogle Scholar
  88. Weil ZM (2012) Ischemia-induced hyperglycemia: consequences, neuroendocrine regulation, and a role for rage. Horm Behav 62:280–285CrossRefPubMedGoogle Scholar
  89. Weiss N, Galanaud D, Carpentier A, Naccache L, Puybasset L (2007) Clinical review: prognostic value of magnetic resonance imaging in acute brain injury and coma. Crit Care 11:230CrossRefPubMedGoogle Scholar
  90. White ML, Zhang Y, Helvey JT, Omojola MF (2013) Anatomical patterns and correlated mri findings of non-perinatal hypoxic-ischaemic encephalopathy. Br J Radiol 86:20120464CrossRefPubMedGoogle Scholar
  91. Wijdicks EF, Campeau NG, Miller GM (2001) MR imaging in comatose survivors of cardiac resuscitation. AJNR Am J Neuroradiol 22:1561–1565PubMedGoogle Scholar
  92. Xu Y, Liachenko S, Tang P (2002) Dependence of early cerebral reperfusion and long-term outcome on resuscitation efficiency after cardiac arrest in rats. Stroke 33:837–843CrossRefPubMedGoogle Scholar
  93. Xu Y, Liachenko SM, Tang P, Chan PH (2009) Faster recovery of cerebral perfusion in sod1-overexpressed rats after cardiac arrest and resuscitation. Stroke 40:2512–2518CrossRefPubMedGoogle Scholar
  94. Yam PS, Takasago T, Dewar D, Graham DI, McCulloch J (1997) Amyloid precursor protein accumulates in white matter at the margin of a focal ischaemic lesion. Brain Res 760:150–157CrossRefPubMedGoogle Scholar
  95. Yam PS, Dewar D, McCulloch J (1998) Axonal injury caused by focal cerebral ischemia in the rat. J Neurotrauma 15:441–450CrossRefPubMedGoogle Scholar
  96. Yam PS, Dunn LT, Graham DI, Dewar D, McCulloch J (2000) Nmda receptor blockade fails to alter axonal injury in focal cerebral ischemia. J Cerebr Blood Flow Metabol 20:772–779CrossRefGoogle Scholar
  97. Zhang J, Takahashi HK, Liu K, Wake H, Liu R, Maruo T, Date I, Yoshino T, Ohtsuka A, Mori S, Nishibori M (2011) Anti-high mobility group box-1 monoclonal antibody protects the blood-brain barrier from ischemia-induced disruption in rats. Stroke 42:1420–1428CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Department of Anesthesiology, Faculty of MedicineKinki UniversityOsakaJapan
  2. 2.Department of AnesthesiologyUniversity of Pittsburgh School of MedicinePittsburghUSA

Personalised recommendations