Early brain injury: A common mechanism in subarachnoid hemorrhage and global cerebral ischemia

Stroke Research and Treatment

Volumn , Issue , 2013, Pages

  Sabri, Mohammed ^a,b   Lass, Elliot ^a,b   MacDonald, R Loch ^a,b,c  

^a ST MICHAEL'S HOSPITAL   (Canada)

^b ST MICHAEL'S HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE;

APOPTOSIS; BLOOD BRAIN BARRIER; BRAIN BLOOD FLOW; BRAIN EDEMA; BRAIN HEMORRHAGE; BRAIN INJURY; BRAIN ISCHEMIA; BRAIN PERFUSION; ENCEPHALITIS; HUMAN; INTRACRANIAL HYPERTENSION; MOLECULAR PATHOLOGY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; SUBARACHNOID HEMORRHAGE;

EID: 84875504759     PISSN: None     EISSN: 20420056     Source Type: Journal    
DOI: 10.1155/2013/394036     Document Type: Review

References (102)

1. Graf C. J., Nibbelink D. W., Cooperative study of intracranial aneurysms and subarachnoid hemorrhage. Report on a randomized treatment study. 3. Intracranial surgery. Stroke 1974 5 4 557 601 2-s2.0-0016086049
2. King J. T. Jr., Epidemiology of aneurysmal subarachnoid hemorrhage. Neuroimaging Clinics of North America 1997 7 4 659 668 2-s2.0-0030812659
3. van Gijn J., Kerr R. S., Rinkel G. J., Subarachnoid haemorrhage. The Lancet 2007 369 9558 306 318 2-s2.0-33846373607 10.1016/S0140-6736(07)60153-6 (Pubitemid 46136491)
4. Hansen-Schwartz J., Vajkoczy P., Macdonald R. L., Pluta R. M., Zhang J. H., Cerebral vasospasm: looking beyond vasoconstriction. Trends in Pharmacological Sciences 2007 28 6 252 256 2-s2.0-34249333412 10.1016/j.tips.2007.04.002 (Pubitemid 46818461)
5. Macdonald R. L., Pluta R. M., Zhang J. H., Cerebral vasospasm after subarachnoid hemorrhage: the emerging revolution. Nature Clinical Practice Neurology 2007 3 5 256 263 2-s2.0-34248524672 10.1038/ncpneuro0490 (Pubitemid 46745473)
6. Cahill W. J., Calvert J. H., Zhang J. H., Mechanisms of early brain injury after subarachnoid hemorrhage. Journal of Cerebral Blood Flow and Metabolism 2006 26 11 1341 1353 2-s2.0-33750350414 10.1038/sj.jcbfm.9600283 (Pubitemid 44629883)
7. Pluta R. M., Hansen-Schwartz J., Dreier J., Zhang J. H., Vajkoczy P., Macdonald R. L., Nishizawa S., Kasuya H., Wellman G., Keller E., Zauner A., Dorsch N., Clark J., Ono S., Kiris T., Leroux P., Cerebral vasospasm following subarachnoid hemorrhage: time for a new world of thought. Neurological Research 2009 31 2 151 158 2-s2.0-62549125030 10.1179/174313209X393564
8. Sehba F. A., Bederson J. B., Mechanisms of acute brain injury after subarachnoid hemorrhage. Neurological Research 2006 28 4 381 398 2-s2.0-33745643550 10.1179/016164106X114991 (Pubitemid 43967786)
9. Sehba F. A., Friedrich V., Early micro vascular changes after subarachnoid hemorrhage. Acta Neurochirurgica 2011 110 1 49 55 2-s2.0-79952279199
10. Sehba F. A., Hou J., Pluta R. M., Zhang J. H.,. The importance of early brain injury after subarachnoid hemorrhage. Progress in Neurobiology 2012 97 14 37
11. Friedrich V., Flores R., Muller A., Bi W., Peerschke E. I., Sehba F. A., Reduction of neutrophil activity decreases early microvascular injury after subarachnoid haemorrhage. Journal of Neuroinflammation 2011 8, article 103
12. Friedrich V., Flores R., Sehba F. A., Cell death starts early after subarachnoid hemorrhage. Neuroscience Letters 2012 512 6 11
13. Sehba F. A., Pluta R. M., Zhang J. H., Metamorphosis of subarachnoid hemorrhage research: from delayed vasospasm to early brain injury. Molecular Neurobiology 2011 43 1 27 40 2-s2.0-79951557739 10.1007/s12035-010-8155-z
14. Budohoski K. P., Czosnyka M., Smielewski P., Kasprowicz M., Helmy A., Bulters D., Pickard J. D., Kirkpatrick P. J., Impairment of cerebral autoregulation predicts delayed cerebral ischemia after subarachnoid hemorrhage: a prospective observational study. Stroke 2012 43 3230 3237
15. Dreier J. P., Major S., Manning A., Woitzik J., Drenckhahn C., Steinbrink J., Tolias C., Oliveira-Ferreira A. I., Fabricius M., Hartings J. A., Vajkoczy P., Lauritzen M., Dirnagl U., Bohner G., Strong A. J., Cortical spreading ischaemia is a novel process involved in ischaemic damage in patients with aneurysmal subarachnoid haemorrhage. Brain 2009 132 7 1866 1881 2-s2.0-67650089668 10.1093/brain/awp102
16. Yuksel S., Tosun Y. B., Cahill J., Solaroglu I., Early brain injury following aneurysmal subarachnoid hemorrhage: emphasis on cellular apoptosis. Turkish Neurosurgery 2012 22 529 533
17. Bernard S. A., Gray T. W., Buist M. D., Jones B. M., Silvester W., Gutteridge G., Smith K., Treatment of comatose survivors of out-of-hospital cardiac arrest with induced hypothermia. The New England Journal of Medicine 2002 346 8 557 563 2-s2.0-0037148929 10.1056/NEJMoa003289 (Pubitemid 34438816)
18. Nussmeier N. A., A review of risk factors for adverse neurologic outcome after cardiac surgery. Journal of Extra-Corporeal Technology 2002 34 1 4 10 2-s2.0-0036193188 (Pubitemid 34211775)
19. Harukuni I., Bhardwaj A., Mechanisms of brain injury after global cerebral ischemia. Neurologic Clinics 2006 24 1 1 21 2-s2.0-31344438217 10.1016/j.ncl.2005.10.004 (Pubitemid 43144627)
20. Hansen-Schwartz J., Hoel N. L., Xu C. B., Svendgaard N. A., Edvinsson L., Subarachnoid hemorrhage-induced upregulation of the 5-HT1B receptor in cerebral arteries in rats. Journal of Neurosurgery 2003 99 1 115 120 2-s2.0-0038647271 (Pubitemid 36753884)
21. Hansen-Schwartz J., Hoel N. L., Zhou M., Xu C. B., Svendgaard N. A., Edvinsson L., Macdonald R. L., Connolly E. S., Selman W. R., Subarachnoid hemorrhage enhances endothelin receptor expression and function in rat cerebral arteries. Neurosurgery 2003 52 5 1188 1195 2-s2.0-0037406222 (Pubitemid 36512985)
22. Johansson S., Povlsen G. K., Edvinsson L., Expressional changes in cerebrovascular receptors after experimental transient forebrain ischemia. PLoS ONE 2012 7 e41852
23. Moskowitz M. A., Lo E. H., Iadecola C., The science of stroke: mechanisms in search of treatments. Neuron 2010 67 2 181 198 2-s2.0-77955487488 10.1016/j.neuron.2010.07.002
24. Yuan J., Neuroprotective strategies targeting apoptotic and necrotic cell death for stroke. Apoptosis 2009 14 4 469 477 2-s2.0-62449153571 10.1007/s10495-008-0304-8
25. Brouwers P. J. A. M., Dippel D. W. J., Vermeulen M., Lindsay K. W., Hasan D., Van Gijn J., Amount of blood on computed tomography as an independent predictor after aneurysm rupture. Stroke 1993 24 6 809 814 2-s2.0-0027210413 (Pubitemid 23163554)
26. Hop J. W., Rinkel G. J. E., Algra A., Van Gijn J., Initial loss of consciousness and risk of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. Stroke 1999 30 11 2268 2271 2-s2.0-0032728804 (Pubitemid 29517719)
27. Schmidt J. M., Rincon F., Fernandez A., Resor C., Kowalski R. G., Claassen J., Connolly E. S., Fitzsimmons B. F. M., Mayer S. A., Cerebral infarction associated with acute subarachnoid hemorrhage. Neurocritical Care 2007 7 1 10 17 2-s2.0-36949022901 10.1007/s12028-007-0003-2 (Pubitemid 350242672)
28. Aoki K., Zubkov A. Y., Ross I. B., Zhang J. H., Therapeutic effect of caspase inhibitors in the prevention of apoptosis and reversal of chronic cerebral vasospasm. Journal of Clinical Neuroscience 2002 9 6 672 677 2-s2.0-0036853583 10.1054/jocn.2002.1088 (Pubitemid 35364743)
29. Cahill J., Calvert J. W., Solaroglu I., Zhang J. H., Vasospasm and p53-induced apoptosis in an experimental model of subarachnoid hemorrhage. Stroke 2006 37 7 1868 1874 2-s2.0-33745964653 10.1161/01.STR.0000226995.27230.96 (Pubitemid 44297744)
30. Nau R., Haase S., Bunkowski S., Brück W., Neuronal apoptosis in the denate gyrus in humans with subarachnoid hemorrage and cerebral hypoxia. Brain Pathology 2002 12 3 329 336 2-s2.0-0036019160 (Pubitemid 34743215)
31. Prunell G. F., Svendgaard N. A., Alkass K., Mathiesen T., Delayed cell death related to acute cerebral blood flow changes following subarachnoid hemorrhage in the rat brain. Journal of Neurosurgery 2005 102 6 1046 1054 2-s2.0-23144450763 10.3171/jns.2005.102.6.1046 (Pubitemid 43193974)
32. Güresir E., Raabe A., Jaiimsin A., Dias S., Raab P., Seifert V., Vatter H., Histological evidence of delayed ischemic brain tissue damage in the rat double-hemorrhage model. Journal of the Neurological Sciences 2010 293 1-2 18 22 2-s2.0-77952107753 10.1016/j.jns.2010.03.023
33. Cheng G., Wei L., Zhi-Dan S., Shi-Guang Z., Xiang-Zhen L., Atorvastatin ameliorates cerebral vasospasm and early brain injury after subarachnoid hemorrhage and inhibits caspase-dependent apoptosis pathway. BMC Neuroscience 2009 10, article 7 2-s2.0-62149115304 10.1186/1471-2202-10-7
34. Endo H., Nito C., Kamada H., Yu F., Chan P. H., Reduction in oxidative stress by superoxide dismutase overexpression attenuates acute brain injury after subarachnoid hemorrhage via activation of Akt/glycogen synthase kinase-3 β survival signaling. Journal of Cerebral Blood Flow and Metabolism 2007 27 5 975 982 2-s2.0-34247475177 10.1038/sj.jcbfm.9600399 (Pubitemid 46659025)
35. Hasegawa Y., Suzuki H., Sozen T., Altay O., Zhang J. H., Apoptotic mechanisms for neuronal cells in early brain injury after subarachnoid hemorrhage. Acta Neurochirurgica 2011 110 1 43 48 2-s2.0-79952278438
36. Matz P., Weinstein P., States B., Honkaniemi J., Sharp F. R., Subarachnoid injections of lysed blood induce the hsp70 stress gene and produce DNA fragmentation in focal areas of the rat brain. Stroke 1996 27 3 504 513 2-s2.0-0029927608 (Pubitemid 26081450)
37. Dhawan J., Benveniste H., Luo Z., Nawrocky M., Smith S. D., Biegon A., A new look at glutamate and ischemia: NMDA agonist improves long-term functional outcome in a rat model of stroke. Future Neurology 2011 6 823 834
38. Choi D. W., Excitotoxic cell death. Journal of Neurobiology 1992 23 9 1261 1276 2-s2.0-0026497926 10.1002/neu.480230915
39. Zhou C., Yamaguchi M., Kusaka G., Schonholz C., Nanda A., Zhang J. H., Caspase inhibitors prevent endothelial apoptosis and cerebral vasospasm in dog model of experimental subarachnoid hemorrhage. Journal of Cerebral Blood Flow and Metabolism 2004 24 4 419 431 2-s2.0-1842533559 (Pubitemid 38452233)
40. Park S., Yamaguchi M., Zhou C., Calvert J. W., Tang J., Zhang J. H., Neurovascular protection reduces early brain injury after subarachnoid hemorrhage. Stroke 2004 35 10 2412 2417 2-s2.0-4744345481 10.1161/01.STR. 0000141162.29864.e9 (Pubitemid 39311273)
41. Endo H., Nito C., Kamada H., Yu F., Chan P. H., Akt/GSK3 β survival signaling is involved in acute brain injury after subarachnoid hemorrhage in rats. Stroke 2006 37 8 2140 2146 2-s2.0-33747183699 10.1161/01.STR.0000229888. 55078.72 (Pubitemid 44309917)
42. Li R. W. S., Tse C. M., Man R. Y. K., Vanhoutte P. M., Leung G. P. H., Inhibition of human equilibrative nucleoside transporters by dihydropyridine-type calcium channel antagonists. European Journal of Pharmacology 2007 568 1-3 75 82 2-s2.0-34250858008 10.1016/j.ejphar.2007.04.033 (Pubitemid 46976908)
43. Shintani T., Klionsky D. J., Autophagy in health and disease: a double-edged sword. Science 2004 306 5698 990 995 2-s2.0-8344242220 10.1126/science.1099993 (Pubitemid 39482894)
44. Jing C. H., Wang L., Liu P. P., Wu C., Ruan D., Chen G., Autophagy activation is associated with neuroprotection against apoptosis via a mitochondrial pathway in a rat model of subarachnoid hemorrhage. Neuroscience 2012 213 144 153
45. Codogno P., Meijer A. J., Autophagy and signaling: their role in cell survival and cell death. Cell Death and Differentiation 2005 12 supplement 2 1509 1518 2-s2.0-27644466759 10.1038/sj.cdd.4401751 (Pubitemid 41553987)
46. Lee J. Y., He Y., Sagher O., Keep R., Hua Y., Xi G., Activated autophagy pathway in experimental subarachnoid hemorrhage. Brain Research 2009 1287 126 135 2-s2.0-68049094975 10.1016/j.brainres.2009.06.028
47. Wang Z., Shi X. Y., Yin J., Zuo G., Zhang J., Chen G., Role of autophagy in early brain injury after experimental subarachnoid hemorrhage. Journal of Molecular Neuroscience 2012 46 192 202 2-s2.0-79959727818 10.1007/s12031-011- 9575-6
48. Dirnagl U., Iadecola C., Moskowitz M. A., Pathobiology of ischaemic stroke: an integrated view. Trends in Neurosciences 1999 22 9 391 397 2-s2.0-0033199996 10.1016/S0166-2236(99)01401-0 (Pubitemid 29453643)
49. Leist M., Nicotera P., The shape of cell death. Biochemical and Biophysical Research Communications 1997 236 1 1 9 2-s2.0-0031561136 10.1006/bbrc.1997.6890 (Pubitemid 27341828)
50. Ankarcrona M., Dypbukt J. M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S. A., Nicotera P., Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 1995 15 4 961 973 2-s2.0-0028793257
51. Graham S. H., Chen J., Programmed cell death in cerebral ischemia. Journal of Cerebral Blood Flow and Metabolism 2001 21 2 99 109 2-s2.0-0035122040 (Pubitemid 32143971)
52. Sugawara T., Fujimura M., Noshita N., Kim G. W., Saito A., Hayashi T., Narasimhan P., Maier C. M., Chan P. H., Neuronal death/survival signaling pathways in cerebral ischemia. NeuroRx 2004 1 1 17 25 2-s2.0-7644238227 10.1602/neurorx.1.1.17 (Pubitemid 46589339)
53. Sabri M., Kawashima A., Ai J., Macdonald R. L., Neuronal and astrocytic apoptosis after subarachnoid hemorrhage: a possible cause for poor prognosis. Brain Research 2008 1238 163 171 2-s2.0-55349084723 10.1016/j.brainres.2008.08. 031
54. Pluta R. M., New regulatory, signaling pathways, and sources of nitric oxide. Acta Neurochirurgica 2011 110 1 7 12 2-s2.0-79952277085
55. Afshar J. K. B., Pluta R. M., Boock R. J., Thompson B. G., Oldfield E. H., Effect of intracarotid nitric oxide on primate cerebral vasospasm after subarachnoid hemorrhage. Journal of Neurosurgery 1995 83 1 118 122 2-s2.0-0029063436
56. Pluta R. M., Dejam A., Grimes G., Gladwin M. T., Oldfield E. H., Nitrite infusions to prevent delayed cerebral vasospasm in a primate model of subarachnoid hemorrhage. Journal of the American Medical Association 2005 293 12 1477 1484 2-s2.0-15044344420 10.1001/jama.293.12.1477 (Pubitemid 40393292)
57. Schwartz A. Y., Sehba F. A., Bederson J. B., Decreased nitric oxide availability contributes to acute cerebral ischemia after subarachnoid hemorrhage. Neurosurgery 2000 47 1 208 215 2-s2.0-0034519628 10.1097/00006123-200007000-00042 (Pubitemid 32047780)
58. Sehba F. A., Schwartz A. Y., Chereshnev I., Bederson J. B., Acute decrease in cerebral nitric oxide levels after subarachnoid hemorrhage. Journal of Cerebral Blood Flow and Metabolism 2000 20 3 604 611 2-s2.0-0034104821 (Pubitemid 30164904)
59. Yatsushige H., Calvert J. W., Cahill J., Zhang J. H., Limited role of inducible nitric oxide synthase in blood-brain barrier function after experimental subarachnoid hemorrhage. Journal of Neurotrauma 2006 23 12 1874 1882 2-s2.0-33845952417 10.1089/neu.2006.23.1874 (Pubitemid 46034457)
60. Sabri M., Ai J., Knight B., Tariq A., Jeon H., Shang X., Marsden P. A., MacDonald R. L., Uncoupling of endothelial nitric oxide synthase after experimental subarachnoid hemorrhage. Journal of Cerebral Blood Flow and Metabolism 2011 31 1 190 199 2-s2.0-78650905978 10.1038/jcbfm.2010.76
61. Sabri M., Ai J., Marsden P. A., Macdonald R. L., Simvastatin re-couples dysfunctional endothelial nitric oxide synthase in experimental subarachnoid hemorrhage. PLoS ONE 2011 6 2 2-s2.0-79952030438 10.1371/journal.pone.0017062 e17062
62. Huang Z., Huang P. L., Ma J., Meng W., Ayata C., Fishman M. C., Moskowitz M. A., Enlarged infarcts in endothelial nitric oxide synthase knockout mice are attenuated by nitro-L-arginine. Journal of Cerebral Blood Flow and Metabolism 1996 16 5 981 987 2-s2.0-0029780767 (Pubitemid 26292066)
63. Lo E. H., Dalkara T., Moskowitz M. A., Mechanisms, challenges and opportunities in stroke. Nature Reviews Neuroscience 2003 4 5 399 415 2-s2.0-0037868093 10.1038/nrn1106 (Pubitemid 37280178)
64. Erşahin M., Toklu H. Z., Çetinel S., Yüksel M., Erzik C., Berkman M. Z., Yeen B. Ç., Şener G., Alpha lipoic acid alleviates oxidative stress and preserves blood brain permeability in rats with subarachnoid hemorrhage. Neurochemical Research 2010 35 3 418 428 2-s2.0-76849084850 10.1007/s11064-009-0072-z
65. Imperatore C., Germanò A., D'Avella D., Tomasello F., Costa G., Effects of the radical scavenger AVS on behavioral and BBB changes after experimental subarachnoid hemorrhage. Life Sciences 2000 66 9 779 790 2-s2.0-0034695433 10.1016/S0024-3205(99)00651-7 (Pubitemid 30077850)
66. Lin C. L., Hsu Y. T., Lin T. K., Morrow J. D., Hsu J. C., Hsu Y. H., Hsieh T. C., Tsay P. K., Yen H. C., Increased levels of F2-isoprostanes following aneurysmal subarachnoid hemorrhage in humans. Free Radical Biology and Medicine 2006 40 8 1466 1473 2-s2.0-33646035846 10.1016/j.freeradbiomed.2005. 12.019
67. Macdonald R. L., Weir B. K., Cerebral vasospasm and free radicalse. Free Radical Biology and Medicine 1994 16 5 633 643 2-s2.0-0028327284 10.1016/0891-5849(94)90064-7 (Pubitemid 24136610)
68. Marzatico F., Gaetani P., Tartara F., Bertorelli L., Feletti F., Adinolfi D., Tancioni F., Rodriguez Y Baena R., Antioxidant status and α 1-antiproteinase activity in subarachnoid hemorrhage patients. Life Sciences 1998 63 10 821 826 2-s2.0-0031614783 10.1016/S0024-3205(98)00338-5 (Pubitemid 28378320)
69. Sakaki S., Kuwabara H., Ohta S., Biological defence mechanism in the pathogenesis of prolonged cerebral vasospasm in the patients with ruptured intracranial aneurysms. Stroke 1986 17 2 196 202 2-s2.0-0022651682 (Pubitemid 16125239)
70. Miller A. A., Budzyn K., Sobey C. G., Vascular dysfunction in cerebrovascular disease: mechanisms and therapeutic intervention. Clinical Science 2010 119 1 1 17 2-s2.0-77954919974 10.1042/CS20090649
71. Paravicini T. M., Sobey C. G., Cerebral vascular effects of reactive oxygen species: recent evidence for a role of NADPH-oxidase. Clinical and Experimental Pharmacology and Physiology 2003 30 11 855 859 2-s2.0-0345599152 10.1046/j.1440-1681.2003.03920.x (Pubitemid 37506153)
72. Didion S. P., Faraci F. M., Effects of NADH and NADPH on superoxide levels and cerebral vascular tone. American Journal of Physiology 2002 282 2 H688 H695 2-s2.0-0036081660 (Pubitemid 34654995)
73. Kim D. E., Suh Y. S., Lee M. S., Kim K. Y., Lee J. H., Lee H. S., Hong K. W., Kim C. D., Vascular NAD(P)H oxidase triggers delayed cerebral vasospasm after subarachnoid hemorrhage in rats. Stroke 2002 33 11 2687 2691 2-s2.0-0036842342 10.1161/01.STR.0000033071.99143.9E (Pubitemid 35266442)
74. Ayer R. E., Zhang J. H., Oxidative stress in subarachnoid haemorrhage: significance in acute brain injury and vasospasm. Acta Neurochirurgica 2008 104 33 41 2-s2.0-44449172082 10.1007/978-3-211-75718-5-7
75. Marklund N., Östman B., Nalmo L., Persson L., Hillered L., Hypoxanthine, uric acid and allantoin as indicators of in vivo free radical reactions. Description of a HPLC method and human brain microdialysis data. Acta Neurochirurgica 2000 142 10 1135 1142 2-s2.0-0033755816 10.1007/s007010070042
76. Kim P., Yaksh T. L., Romero S. D., Sundt T. M. Jr., Production of uric acid in cerebrospinal fluid after subarachnoid hemorrhage in dogs: investigation of the possible role of xanthine oxidase in chronic vasospasm. Neurosurgery 1987 21 1 39 44 2-s2.0-0023191132 (Pubitemid 17105471)
77. Goto S., Xue R., Sugo N., Sawada M., Blizzard K. K., Poitras M. F., Johns D. C., Dawson T. M., Dawson V. L., Crain B. J., Traystman R. J., Mori S., Hurn P. D., Poly(ADP-ribose) polymerase impairs early and long-term experimental stroke recovery. Stroke 2002 33 4 1101 1106 2-s2.0-0036218940 10.1161/01.STR.0000014203.65693.1E (Pubitemid 34293598)
78. Chaichana K. L., Pradilla G., Huang J., Tamargo R. J., Role of inflammation (leukocyte-endothelial cell interactions) in vasospasm after subarachnoid hemorrhage. World Neurosurgery 2010 73 1 22 41 2-s2.0-77953246444 10.1016/j.surneu.2009.05.027
79. Dumont A. S., Dumont R. J., Chow M. M., Lin C. L., Calisaneller T., Ley K. F., Kassell N. F., Lee K. S., Barrow D. L., Macdonald R. L., Hoh B. L., Ogilvy C. S., Lawton M. T., Cerebral vasospasm after subarachnoid hemorrhage: putative role of inflammation. Neurosurgery 2003 53 1 123 135 2-s2.0-0038725119 (Pubitemid 36801515)
80. Erşahin M., Toklu H. Z., Erzik C., Çetinel Ş.., Akakin D., Veliolu-Öünç A., Tetik Ş.., Özdemir Z. N., Şener G., Yeen B. Ç., The anti-inflammatory and neuroprotective effects of ghrelin in subarachnoid hemorrhage-induced oxidative brain damage in rats. Journal of Neurotrauma 2010 27 6 1143 1155 2-s2.0-77953929950 10.1089/neu.2009.1210
81. Sozen T., Tsuchiyama R., Hasegawa Y., Suzuki H., Jadhav V., Nishizawa S., Zhang J. H., Role of interleukin-1 β in early brain injury after subarachnoid hemorrhage in mice. Stroke 2009 40 7 2519 2525 2-s2.0-67650064909 10.1161/STROKEAHA.109.549592
82. Sugawara T., Jadhav V., Ayer R., Chen W., Suzuki H., Zhang J. H., Thrombin inhibition by argatroban ameliorates early brain injury and improves neurological outcomes after experimental subarachnoid hemorrhage in rats. Stroke 2009 40 4 1530 1532 2-s2.0-65249125759 10.1161/STROKEAHA.108.531699
83. Zhou M. L., Shi J. X., Hang C. H., Cheng H. L., Qi X. P., Mao L., Chen K. F., Yin H. X., Potential contribution of nuclear factor- B to cerebral vasospasm after experimental subarachnoid hemorrhage in rabbits. Journal of Cerebral Blood Flow and Metabolism 2007 27 9 1583 1592 2-s2.0-34548131647 10.1038/sj.jcbfm.9600456 (Pubitemid 47301442)
84. Fassbender K., Hodapp B., Rossol S., Bertsch T., Schmeck J., Schutt S., Fritzinger M., Horn P., Vajkoczy P., Wendel-Wellner M., Ragoschke A., Kuehl S., Brunner J., Schurer L., Schmiedeck P., Hennerici M., Endothelin-1 in subarachnoid hemorrhage: an acute-phase reactant produced by cerebrospinal fluid leukocytes. Stroke 2000 31 2971 2975
85. McGirt M. J., Mavropoulos J. C., McGirt L. Y., Alexander M. J., Friedman A. H., Laskowitz D. T., Lynch J. R., Leukocytosis as an independent risk factor for cerebral vasospasm following aneurysmal subarachnoid hemorrhage. Journal of Neurosurgery 2003 98 6 1222 1226 2-s2.0-0037850709 (Pubitemid 36617925)
86. Momin E. N., Schwab K. E., Chaichana K. L., Miller-Lotan R., Levy A. P., Tamargo R. J., Controlled delivery of nitric oxide inhibits leukocyte migration and prevents vasospasm in haptoglobin 2-2 mice after subarachnoid hemorrhage. Neurosurgery 2009 65 5 937 945 2-s2.0-70350291828 10.1227/01.NEU.0000356974. 14230.B8
87. Jia W., Wang R., Zhao J., Liu I. Y., Zhang D., Wang X., Han X., E-selectin expression increased in human ruptured cerebral aneurysm tissues. Canadian Journal of Neurological Sciences 2011 38 858 862
88. Ginis I., Jaiswal R., Klimanis D., Liu J., Greenspon J., Hallenbeck J. M., TNF- α -induced tolerance to ischemic injury involves differential control of NF- B transactivation: the role of NF- B association with p300 adaptor. Journal of Cerebral Blood Flow and Metabolism 2002 22 2 142 152 2-s2.0-0036167642 (Pubitemid 34135645)
89. Ayer R., Jadhav V., Sugawara T., Zhang J. H., The neuroprotective effects of cyclooxygenase-2 inhibition in a mouse model of aneurysmal subarachnoid hemorrhage. Acta Neurochirurgica 2011 111 145 149 2-s2.0-79960687273 10.1007/978-3-7091-0693-8-24
90. Claassen J., Carhuapoma J. R., Kreiter K. T., Du E. Y., Connolly E. S., Mayer S. A., Global cerebral edema after subarachnoid hemorrhage: frequency, predictors, and impact on outcome. Stroke 2002 33 5 1225 1232 2-s2.0-0036094267 10.1161/01.STR.0000015624.29071.1F (Pubitemid 34520392)
91. Meguro T., Chen B., Lancon J., Zhang J. H., Oxyhemoglobin induces caspase-mediated cell death in cerebral endothelial cells. Journal of Neurochemistry 2001 77 4 1128 1135 2-s2.0-0035019389 10.1046/j.1471-4159.2001. 00313.x (Pubitemid 32467067)
92. Gao Y., Yokota R., Tang S., Ashton A. W., Ware J. A., Reversal of angiogenesis in vitro, induction of apoptosis, and inhibition of Akt phosphorylation in endothelial cells by thromboxane A2. Circulation Research 2000 87 9 739 745 2-s2.0-0034721883
93. Yan J., Li L., Khatibi N. H., Yang L., Wang K., Zhang W., Martin R. D., Han J., Zhang J., Zhou C., Blood-brain barrier disruption following subarchnoid hemorrhage may be faciliated through PUMA induction of endothelial cell apoptosis from the endoplasmic reticulum. Experimental Neurology 2011 230 2 240 247 2-s2.0-79958741053 10.1016/j.expneurol.2011.04.022
94. Guo Z., Sun X., He Z., Jiang Y., Zhang X., Zhang J. H., Matrix metalloproteinase-9 potentiates early brain injury after subarachnoid hemorrhage. Neurological Research 2010 32 7 715 720 2-s2.0-77955632657 10.1179/016164109X12478302362491
95. Sehba F. A., Mostafa G., Knopman J., Friedrich V. Jr., Bederson J. B., Acute alterations in microvascular basal lamina after subarachnoid hemorrhage. Journal of Neurosurgery 2004 101 4 633 640 2-s2.0-7944234917 10.3171/jns.2004.101.4.0633 (Pubitemid 43186422)
96. Suzuki H., Hasegawa Y., Chen W., Kanamaru K., Zhang J. H., Recombinant osteopontin in cerebral vasospasm after subarachnoid hemorrhage. Annals of Neurology 2010 68 5 650 660 2-s2.0-78249269131 10.1002/ana.22102
97. Yatsushige H., Ostrowski R. P., Tsubokawa T., Colohan A., Zhang J. H., Role of c-Jun N-terminal kinase in early brain injury after subarachnoid hemorrhage. Journal of Neuroscience Research 2007 85 7 1436 1448 2-s2.0-34248155678 10.1002/jnr.21281 (Pubitemid 46724387)
98. Schöller K., Trinkl A., Klopotowski M., Thal S. C., Plesnila N., Trabold R., Hamann G. F., Schmid-Elsaesser R., Zausinger S., Characterization of microvascular basal lamina damage and blood-brain barrier dysfunction following subarachnoid hemorrhage in rats. Brain Research 2007 1142 1 237 246 2-s2.0-33947161412 10.1016/j.brainres.2007.01.034 (Pubitemid 46413192)
99. Danton G. H., Dietrich W. D., Inflammatory mechanisms after ischemia and stroke. Journal of Neuropathology and Experimental Neurology 2003 62 2 127 136 2-s2.0-0037312886 (Pubitemid 36176947)
100. Han H. S., Yenari M. A., Cellular targets of brain inflammation in stroke. Current Opinion in Investigational Drugs 2003 4 5 522 529 2-s2.0-0038518255 (Pubitemid 36717196)
101. Germanò A., Caffo M., Angileri F. F., Arcadi F., Newcomb-Fernandez J., Caruso G., Meli F., Pineda J. A., Lewis S. B., Wang K. K. W., Bramanti P., Costa C., Hayes R. L., NMDA receptor antagonist felbamate reduces behavioral deficits and blood-brain barrier permeability changes after experimental subarachnoid hemorrhage in the rat. Journal of Neurotrauma 2007 24 4 732 744 2-s2.0-34249849556 10.1089/neu.2006.0181 (Pubitemid 46996032)
102. Unterberg A. W., Sakowitz O. W., Sarrafzadeh A. S., Benndorf G., Lanksch W. R., Role of bedside microdialysis in the diagnosis of cerebral vasospasm following aneurysmal subarachnoid hemorrhage. Journal of Neurosurgery 2001 94 5 740 749 2-s2.0-0034877318 (Pubitemid 32799622)