Delayed cerebral ischemia after subarachnoid hemorrhage: From vascular spasm to cortical spreading depolarizations

Current Neurovascular Research

Volumn 9, Issue 4, 2012, Pages 310-319

  Zheng, Zelong ^a   Sánchez Porras, Renán ^a   Santos, Edgar ^a   Unterberg, Andreas W ^a   Sakowitz, Oliver W ^a  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

Cerebral vasospasm; Cortical spreading depolarization; Delayed cerebral ischemia; Spreading ischemia; Subarachnoid hemorrhage; Treatment

Indexed keywords

ALBUMIN; ANTICOAGULANT AGENT; CILOSTAZOL; CLAZOSENTAN; DILTIAZEM; ENOXAPARIN; ERYTHROPOIETIN; FASUDIL; KETAMINE; MAGNESIUM SULFATE; NICARDIPINE; NIMODIPINE; NITRIC OXIDE DONOR; NITROPRUSSIDE SODIUM; PRAVASTATIN; SIMVASTATIN; SODIUM NITRITE; TAK 044; TIRILAZAD; VERAPAMIL;

ANEMIA; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BLOOD BRAIN BARRIER; BRAIN BLOOD FLOW; BRAIN ISCHEMIA; BRAIN MICROCIRCULATION; BRAIN PERFUSION; BRAIN VASCULAR RESISTANCE; BRAIN VASOSPASM; COMPUTED TOMOGRAPHIC ANGIOGRAPHY; CONVENTIONAL ANGIOGRAPHY; CORTICAL SPREADING DEPOLARIZATION; DELAYED CEREBRAL ISCHEMIA; DIGITAL SUBTRACTION ANGIOGRAPHY; DOPPLER ECHOGRAPHY; DRUG EFFICACY; DRUG SAFETY; ELECTROCORTICOGRAPHY; ENERGY METABOLISM; GLUCOSE UTILIZATION; HEMOLYSIS; HUMAN; HYPOTENSION; HYPOXIC ISCHEMIC ENCEPHALOPATHY; INTRACRANIAL PRESSURE; LUNG COMPLICATION; MEAN ARTERIAL PRESSURE; MICROTHROMBUS; NEUROLOGIC EXAMINATION; NEUROPROTECTION; NONHUMAN; OXYGEN CONSUMPTION; PATHOPHYSIOLOGY; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); SIDE EFFECT; SPREADING CORTICAL DEPRESSION; SUBARACHNOID HEMORRHAGE; THROMBOCYTE ADHESION; TRANSCRANIAL DOPPLER;

EID: 84870397025     PISSN: 15672026     EISSN: 18755739     Source Type: Journal    
DOI: 10.2174/156720212803530663     Document Type: Article

References (112)

1. Nieuwkamp DJ, Setz LE, Algra A, et al. Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a meta-analysis. Lancet Neurol 2009;8(7):635-42.
2. Vergouwen MD, de Haan RJ, Vermeulen M, Roos YB. Effect of statin treatment on vasospasm, delayed cerebral ischemia, and functional outcome in patients with aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis update. Stroke 2010;41(1):e47-52.
3. Bederson JB, Connolly ES Jr, Batjer HH, et al. American Heart Association. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke 2009;40(3):994-1025.
4. Kassell NF, Torner JC, Haley EC Jr, Jane JA, Adams HP, Kongable GL. The International Cooperative Study on the Timing of Aneurysm Surgery. Part 1: Overall management results. J Neurosurg 1990;73(1):18-36. (Pubitemid 20206379)
5. Hubschmann OR, Kornhauser D. Cortical cellular response in acute subarachnoid hemorrhage. J Neurosurg 1980;52(4):456-62. (Pubitemid 10130633)
6. Beaulieu C, Busch E, de Crespigny A, Moseley ME. Spreading waves of transient and prolonged decreases in water diffusion after subarachnoid hemorrhage in rats. Magn Reson Med 2000;44(1):110-6. (Pubitemid 30439845)
7. Dreier JP, Woitzik J, Fabricius M, et al. Delayed ischemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. Brain 2006;129(Pt 12):3224-37. (Pubitemid 44871438)
8. Dreier JP, Major S, Manning A, et al; COSBID study group. Cortical spreading ischaemia is a novel process involved in ischaemic damage in patients with aneurysmal subarachnoid haemorrhage. Brain 2009;132(Pt 7):1866-81.
9. Diringer MN, Bleck TP, Claude Hemphill J 3rd, et al; Neurocritical Care Society. Critical care management of patients following aneurysmal subarachnoid hemorrhage: recommendations from the Neurocritical Care Society's Multidisciplinary Consensus Conference. Neurocrit Care 2011;15(2):211-40.
10. Frontera JA, Fernandez A, Schmidt JM, et al. Defining vasospasm after subarachnoid hemorrhage: what is the most clinically relevant definition? Stroke 2009;40(6):1963-8.
11. Sakowitz OW, Unterberg AW. Detecting and treating microvascular ischemia after subarachnoid hemorrhage. Curr Opin Crit Care 2006;12(2):103-11.
12. Faraci FM, Heistad DD. Regulation of large cerebral arteries and cerebral microvascular pressure. Circ Res 1990;66(1):8-17. (Pubitemid 20033921)
13. Birk S, Kruuse C, Petersen KA, Jonassen O, Tfelt-Hansen P, Olesen J. The phosphodiesterase 3 inhibitor cilostazol dilates large cerebral arteries in humans without affecting regional cerebral blood flow. J Cereb Blood Flow Metab 2004;24(12):1352-8. (Pubitemid 40019158)
14. Murphy BD, Fox AJ, Lee DH, et al. Identification of penumbra and infarct in acute ischemic stroke using computed tomography perfusion-derived blood flow and blood volume measurements. Stroke 2006;37(7):1771-7. (Pubitemid 44297728)
15. Jost SC, Diringer MN, Zazulia AR, et al. Effect of normal saline bolus on cerebral blood flow in regions with low baseline flow in patients with vasospasm following subarachnoid hemorrhage. J Neurosurg 2005;103(1):25-30. (Pubitemid 43193930)
16. Dankbaar JW, Rijsdijk M, van der Schaaf IC, Velthuis BK, Wermer MJ, Rinkel GJ. Relationship between vasospasm, cerebral perfusion, and delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. Neuroradiology 2009;51(12):813-9.
17. Vergouwen MD, Vermeulen M, Coert BA, Stroes ES, Roos YB. Microthrombosis after aneurysmal subarachnoid hemorrhage: an additional explanation for delayed cerebral ischemia. J Cereb Blood Flow Metab 2008;28(11):1761-70.
18. Rabinstein AA, Weigand S, Atkinson JL, Wijdicks EF. Patterns of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke 2005;36(5):992-7. (Pubitemid 40629290)
19. Herz DA, Baez S, Shulman K. Pial Microcirculation in Subarachnoid Hemorrhage. Stroke 1975;6(4):417-24.
20. Wiernsperger N, Sculz U, Gygax P. Physiological and morphometric analysis of the microcirculation of the cerebral cortex under acute vasospasm. Stroke 1981;12(5):624-7. (Pubitemid 11030066)
21. Ohkuma H, Manabe H., Tanaka M, Suzuki S. Impact of cerebral microcirculatory changes on cerebral blood flow during cerebral vasospasm after aneurysmal subarachnoid hemorrhage. Stroke 2000;31(7):1621-7. (Pubitemid 30437513)
22. Uhl E, Lehmberg J, Steiger HJ, Messmer K. Intraoperative detection of early microvasospasm in patients with subarachnoid hemorrhage by using orthogonal polarization spectral imaging. Neurosurgery 2003;52(6):1307-15.
23. Hashi K, Meyer JS, Shinamaru S, Welch KM, Teraura T. Changes in cerebral vasomotor activity to CO2 and autoregulation following experimetal subarachnoid hemorrhage. J Neurol Sci 1972;17(1):15-22.
24. Kamiya K, Kuyama H, Symon L. An experimental study of the acute stage of subarachnoid hemorrhage. J Neurosurg 1983;59(6):917-24. (Pubitemid 14205876)
25. Yamamoto S, Nishizawa S, Tsukada H, et al. Cerebral autoregulation following subarachnoid hemorrhage in rats: chronic vasospasm shifts the upper and lower limits of the autoregulatory range toward higher blood pressure. Brain Res 1998;782(1-2):194-201. (Pubitemid 28122994)
26. Sehba FA, Bederson JB. Mechanisms of acute brain injury after subarachnoid hemorrhage. Neurol Res 2006;28(4):381-98. (Pubitemid 43967786)
27. Cahill J, Calvert JW, Zhang JH. Mechanisms of early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab 2006;26(11):1341-53. (Pubitemid 44629883)
28. Ostrowski RP, Colohan AR, Zhang JH. Molecular mechanisms of early brain injury after subarachnoid hemorrhage. Neurol Res 2006;28(4):399-414. (Pubitemid 43967787)
29. Suzuki M, Kudo A, Otawara Y, Hirashima Y, Takaku A, Ogawa A. Extrinsic pathway of blood coagulation and thrombin in the cerebrospinal fluid after subarachnoid hemorrhage. Neurosurgery 1999;44(3):487-94. (Pubitemid 29098322)
30. Frijns CJ, Fijnheer R, Algra A, van Mourik JA, van Gijn J, Rinkel GJ. Early circulating levels of endothelial cell activation markers in aneurysmal subarachnoid haemorrhage: associations with cerebral ischaemic events and outcome. J Neurol Neurosurg Psychiatry 2006;77(1):77-83. (Pubitemid 43022697)
31. Hirashima Y, Nakamura S, Endo S, Kuwayama N, Naruse Y, Takaku. A. Elevation of platelet activating factor, inflammatory cytokines, and coagulation factors in the internal jugular vein of patients with subarachnoid hemorrhage. Neurochem Res 1997;22(10):1249-55. (Pubitemid 27440793)
32. Hirashima Y, Nakamura S, Suzuki M, et al. Cerebrospinal fluid tissue factor and thrombin-antithrombin III complex as indicators of tissue injury after subarachnoid hemorrhage. Stroke 1997;28(9):1666-70. (Pubitemid 27391431)
33. Suzuki S, Kimura M, Souma M, Ohkima H, Shimizu T, Iwabuchi T. Cerebral microthrombosis in symptomatic cerebral vasospasm - a quantitative histological study in autopsy cases. Neurol Med Chir (Tokyo) 1990;30(5):309-16. (Pubitemid 20270142)
34. Giller CA, Giller AM, Landreneau F. Detection of emboli after surgery for intracerebral aneurysms. Neurosurgery 1998;42(3):490-4. (Pubitemid 28128733)
35. van den Bergh WM; MASH Study Group, Algra A, Dorhout Mees SM, et al. Randomized controlled trial of acetylsalicylic acid in aneurysmal subarachnoid hemorrhage: the MASH Study. Stroke 2006;37(9):2326-30. (Pubitemid 44337178)
36. Siironen J, Juvela S, Varis J, et al. No effect of enoxaparin on outcome of aneurysmal subarachnoid hemorrhage: a randomized, double-blind, placebo-controlled clinical trial. J Neurosurg 2003;99(6):953-9. (Pubitemid 44717388)
37. Leao AAP. Spreading depression of activity in cerebral cortex. J Neurophysiol 1944;7(6):359-90.
38. Lauritzen M, Dreier JP, Fabricius M, Hartings JA, Graf R, Strong AJ. Clinical relevance of cortical spreading depression in neurological disorders: migraine, malignant stroke, subarachnoid and intracranial haemorrhage, and traumatic brain injury. J Cereb Blood Flow Metab 2011;31(1):17-35.
39. Somjen GG. Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol Rev 2001;81(3):1065-96. (Pubitemid 32606666)
40. Fabricius M, Jensen LH, Lauritzen M. Microdialysis of interstitial amino acids during spreading depression and anoxic depolarization in rat neocortex. Brain Res 1993;612(1-2):61-9. (Pubitemid 23167263)
41. Strong AJ, Dardis R. Depolarisation phenomena in traumatic and ischaemic brain injury. Adv Tech Stand Neurosurg 2005;30:3-49.
42. Dreier JP. The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat Med 2011;17(4):439-47.
43. Haghir H, Kovac S, Speckmann EJ, Zilles K, Gorji A. Patterns of neurotransmitter receptor distributions following cortical spreading depression. Neuroscience 2009;163(4):1340-52.
44. Jander S, Schroeter M, Peters O, Witte OW, Stoll G. Cortical spreading depression induces proinflammatory cytokine gene expression in the rat brain. J Cereb Blood Flow Metab 2001;21(3):218-25. (Pubitemid 32207421)
45. Gursoy-Ozdemir Y, Qiu J, Matsuoka N, et al. Cortical spreading depression activates and upregulates MMP-9. J Clin Invest 2004;113(10):1447-55. (Pubitemid 39071700)
46. Fabricius M, Fuhr S, Bhatia R, et al. Cortical spreading depression and peri-infarct depolarization in acutely injured human cerebral cortex. Brain 2006;129(Pt 3):778-90. (Pubitemid 43278239)
47. Strong AJ, Anderson PJ, Watts HR, et al. Peri-infarct depolarizations lead to loss of perfusion in ischaemic gyrencephalic cerebral cortex. Brain 2007;130(Pt 4):995-1008. (Pubitemid 47355590)
48. Strong AJ, Hartings JA, Dreier JP. Cortical spreading depression: an adverse but treatable factor in intensive care? Curr Opin Crit Care 2007;13(2):126-33. (Pubitemid 46328325)
49. Brouwers PJ, Dippel DW, Vermeulen M, Lindsay KW, Hasan D, van Gijn J. Amount of blood on computed tomography as an independent predictor after aneurysm rupture. Stroke 1993;24(6):809-14. (Pubitemid 23163554)
50. Pluta RM, Afshar JK, Boock RJ, Oldfield EH. Temporal changes in perivascular concentrations of oxyhemoglobin, deoxyhemoglobin, and methemoglobin after subarachnoid hemorrhage. J Neurosurg 1998;88(3):557-61. (Pubitemid 28114731)
51. Levitt P, Wilson WP, Wilkins RH. The effects of subarachnoid blood on the electrocorticogram of the cat. J Neurosurg 1971;35(2):185-91.
52. Dreier JP, Ebert N, Priller J, et al. Products of hemolysis in the subarachnoid space inducing spreading ischemia in the cortex and focal necrosis in rats: a model for delayed ischemic neurological deficits after subarachnoid hemorrhage? J Neurosurg 2000;93(4):658-66. (Pubitemid 32799301)
53. Okamoto S, Handa H, Toda N. Role of intrinsic arachidonate metabolites in the vascular action of erythrocyte breakdown products. Stroke 1984;15(1):60-4. (Pubitemid 14182396)
54. Toda N. Hemolysate inhibits cerebral artery relaxation. J Cereb Blood Flow Metab 1988;8(1):46-53. (Pubitemid 18045943)
55. Wellum GR, Irvine TW Jr, Zervas NT. Dose responses of cerebral arteries of the dog, rabbit, and man to human hemoglobin in vitro. J Neurosurg 1980;53(4):486-90. (Pubitemid 10003556)
56. Gorji A. Spreading depression: a review of the clinical relevance. Brain Res Brain Res Rev 2001;38(1-2):33-60. (Pubitemid 34066496)
57. Bosche B, Graf R, Ernestus RI, et al. Members of the Cooperative Study of Brain Injury Depolarizations (COSBID). Recurrent spreading depolarizations after subarachnoid hemorrhage decreases oxygen availability in human cerebral cortex. Ann Neurol 2010;67(5):607-17.
58. Woitzik J, Dreier JP, Hecht N, et al; COSBID study group. Delayed cerebral ischemia and spreading depolarization in absence of angiographic vasospasm after subarachnoid hemorrhage. J Cereb Blood Flow Metab 2012;32(2):203-12.
59. Dankbaar JW, Slooter AJ, Rinkel GJ, Schaaf IC. Effect of different components of triple-H therapy on cerebral perfusion in patients with aneurysmal subarachnoid haemorrhage: a systematic review. Crit Care 2010;14(1):R23.
60. Lennihan L, Mayer SA, Fink ME, et al. Effect of hypervolemic therapy on cerebral blood flow after subarachnoid hemorrhage: a randomized controlled trial. Stroke 2000;31(2):383-91. (Pubitemid 30078170)
61. Egge A, Waterloo K, Sjøholm H, Solberg T, Ingebrigtsen T, Romner B. Prophylactic hyperdynamic postoperative fluid therapy after aneurysmal subarachnoid hemorrhage: a clinical, prospective, randomized, controlled study. Neurosurgery 2001;49(3):593-605.
62. Lee KH, Lukovits T, Friedman JA. "Triple-H" therapy for cerebral vasospasm following subarachnoid hemorrhage. Neurocrit Care 2006;4(1):68-76. (Pubitemid 43269464)
63. Sakowitz OW, Raabe A, Vucak D, Kiening KL, Unterberg AW. Contemporary management of aneurysmal subarachnoid hemorrhage in Germany: results of a survey among 100 neurosurgical departments. Neurosurgery 2006;58(1):137-45.
64. Connolly ES Jr, Rabinstein AA, Carhuapoma JR, et al; on behalf of the American Heart Association Stroke Council, Council on Cardiovascular Radiology and Intervention, Council on Cardiovascular Nursing, Council on Cardiovascular Surgery and Anesthesia, and Council on Clinical Cardiology. Guidelines for the Management of Aneurysmal Subarachnoid Hemorrhage: A Guideline for Healthcare Professionals From the American Heart Association/American Stroke Association. Stroke. 2012;43(6):1711-37.
65. Allen GS, Ahn HS, Preziosi TJ, et al. Cerebral arterial spasm-a controlled trial of nimodipine in patients with subarachnoid hemorrhage. N Engl J Med 1983;308(11):619-24. (Pubitemid 13152325)
66. Philippon J, Grob R, Dagreou F, Guggiari M, Rivierez M, Viars P: Prevention of vasospasm in subarachnoid haemorrhage. A controlled study with nimodipine. Acta Neurochir 1986;82(3-4):110-4. (Pubitemid 17198717)
67. Mee E, Dorrance D, Lowe D, Neil-Dwyer G. Controlled study of nimodipine in aneurysm patients treated early after subarachnoid hemorrhage. Neurosurgery 1988;22(3):484-91. (Pubitemid 18095950)
68. Petruk KC, West M, Mohr G, et al. Nimodipine treatment in poorgrade aneurysm patients. Results of a multicenter double-blind placebo-controlled trial. J Neurosurg 1988;68(4):505-17.
69. Feigin VL, Rinkel GJ, Algra A, Vermeulen M, van Gijn J. Calcium antagonists in patients with aneurysmal subarachnoid hemorrhage: a systematic review. Neurology 1998;50(4):876-83. (Pubitemid 28212809)
70. Choi HA, Ko SB, Chen H, et al. Acute Effects of Nimodipine on Cerebral Vasculature and Brain Metabolism in High Grade Subarachnoid Hemorrhage Patients. Neurocrit Care. 2012;16(3):363-7.
71. Abe K, Iwanaga H, Inada E. Effect of nicardipine and diltiazem on internal carotid artery blood flow velocity and local cerebral blood flow during cerebral aneurysm surgery for subarachnoid hemorrhage. J Clin Anesth 1994;6(2):99-105. (Pubitemid 24134603)
72. Hui C, Lau KP. Efficacy of intra-arterial nimodipine in the treatment of cerebral vasospasm complicating subarachnoid haemorrhage. Clin Radiol 2005;60(9):1030-6. (Pubitemid 41194675)
73. Schmidt U, Bittner E, Pivi S, Marota JJ. Hemodynamic management and outcome of patients treated for cerebral vasospasm with intraarterial nicardipine and/or milrinone. Anesth Analg 2010;110(3):895-902.
74. Kasuya H. Clinical trial of nicardipine prolonged-release implants for preventing cerebral vasospasm: multicenter cooperative study in Tokyo. Acta Neurochir Suppl 2011;110(Pt 2):165-7.
75. Macdonald RL, Kassell NF, Mayer S, et al; CONSCIOUS-1 Investigators. Clazosentan to overcome neurological ischemia and infarction occurring after subarachnoid hemorrhage (CONSCIOUS-1): randomized, double-blind, placebo-controlled phase 2 dose-finding trial. Stroke 2008;39(11):3015-21.
76. Macdonald RL, Higashida RT, Keller E, et al. Clazosentan, an endothelin receptor antagonist, in patients with aneurysmal subarachnoid haemorrhage undergoing surgical clipping: a randomised, double-blind, placebo-controlled phase 3 trial (CONSCIOUS-2). Lancet Neurol 2011;10(7):618-25.
77. Macdonald RL, Higashida RT, Keller E, et al. Randomized Trial of Clazosentan in Patients With Aneurysmal Subarachnoid Hemorrhage Undergoing Endovascular Coiling. Stroke. 2012;43(6):1463-9
78. Suarez JI, Participants in the International Multidisciplinary Consensus Conference on the Critical Care Management of Subarachnoid Hemorrhage. Magnesium sulfate administration in subarachnoid hemorrhage. Neurocrit Care 2011;15(2):302-7.
79. Rabinstein AA, Lanzino G, Wijdicks EF. Multidisciplinary management and emerging therapeutic strategies in aneurysmal subarachnoid haemorrhage. Lancet Neurol 2010;9(5):504-19.
80. van den Bergh WM, Albrecht KW, Berkelbach van der Sprenkel JW, Rinkel GJ. Magnesium therapy after aneurysmal subarachnoid haemorrhage a dose-finding study for long term treatment. Acta Neurochir (Wien) 2003;145(3):195-9. (Pubitemid 36359700)
81. van den Bergh WM, Algra A, van Kooten F, et al; MASH Study Group. Magnesium sulfate in aneurysmal subarachnoid hemorrhage: a randomized controlled trial. Stroke 2005;36(5):1011-5. (Pubitemid 40629294)
82. Wong GK, Poon WS, Chan MT, et al; IMASH Investigators. Intravenous magnesium sulphate for aneurysmal subarachnoid hemorrhage (IMASH): a randomized, double-blinded, placebocontrolled, multicenter phase III trial. Stroke 2010;41(5):921-6.
83. Muroi C, Seule M, Mishima K, Keller E. Novel treatments for vasospasm after subarachnoid hemorrhage. Curr Opin Crit Care 2012;18(2):119-26.
84. Castanares-Zapatero D, Hantson P. Pharmacological treatment of delayed cerebral ischemia and vasospasm in subarachnoid hemorrhage. Ann Intensive Care 2011;1(1):12.
85. Tseng MY; Participants in the International Multidisciplinary Consensus Conference on the Critical Care Management of Subarachnoid Hemorrhage. Summary of evidence on immediate statins therapy following aneurysmal subarachnoid hemorrhage. Neurocrit Care 2011;15(2):298-301.
86. Clark FL, White RP. Endothelium and cerebral vasospasm. J Neurosurg 1989;70(4):657-9.
87. Agrawal A, Patir R, Kato Y, Chopra S, Sano H, Kanno T. Role of intraventricular sodium nitroprusside in vasospasm secondary to aneurysmal subarachnoid haemorrhage: a 5-year prospective study with review of the literature. Minim Invasive Neurosurg 2009;52(1):5-8.
88. Fathi AR, Pluta RM, Bakhtian KD, Qi M, Lonser RR. Reversal of cerebral vasospasm via intravenous sodium nitrite after subarachnoid hemorrhage in primates. J Neurosurg 2011;115(6):1213-20.
89. Shibuya M, Suzuki Y, Sugita K, et al. Effect of AT877 on cerebral vasospasm after aneurysmal subarachnoid hemorrhage. Results of a prospective placebo-controlled double-blind trial. J Neurosurg 1992;76(4):571-7.
90. Liu GJ, Wang ZJ, Wang YF, et al. Systematic assessment and meta-analysis of the efficacy and safety of fasudil in the treatment of cerebral vasospasm in patients with subarachnoid hemorrhage. Eur J Clin Pharmacol 2012;68(2):131-9.
91. Huh PW, Belayev L, Zhao W, Busto R, Saul I, Ginsberg MD. The effect of high-dose albumin therapy on local cerebral perfusion after transient focal cerebral ischemia in rats. Brain Res 1998;804(1):105-13. (Pubitemid 28410484)
92. Suarez JI, Shannon L, Zaidat OO, et al. Effect of human albumin administration on clinical outcome and hospital cost in patients with subarachnoid hemorrhage. J Neurosurg 2004;100(4):585-90. (Pubitemid 38372836)
93. Suarez JI, Martin RH, Calvillo E, et al; ALISAH Investigators. The Albumin in Subarachnoid Hemorrhage (ALISAH) multicenter pilot clinical trial: safety and neurologic outcomes. Stroke 2012;43(3):683-90.
94. Koshimura K, Murakami Y, Sohmiya M, Tanaka J, Kato Y. Effects of erythropoietin on neuronal activity. J Neurochem 1999;72(6):2565-72. (Pubitemid 29242209)
95. Kumral A, Ozer E, Yilmaz O, et al. Neuroprotective effect of erythropoietin on hypoxic-ischemic brain injury in neonatal rats. Biol Neonate 2003;83(3):224-8. (Pubitemid 36351232)
96. Springborg JB, Møller C, Gideon P, Jørgensen OS, Juhler M, Olsen NV. Erythropoietin in patients with aneurysmal subarachnoid haemorrhage: a double blind randomised clinical trial. Acta Neurochir (Wien) 2007;149(11):1089-101.
97. Tseng MY, Hutchinson PJ, Richards HK, et al. Acute systemic erythropoietin therapy to reduce delayed ischemic deficits following aneurysmal subarachnoid hemorrhage: a Phase II randomized, double-blind, placebo-controlled trial. Clinical article. J Neurosurg 2009;111(1):171-80.
98. Zhang S, Wang L, Liu M, Wu B. Tirilazad for aneurysmal subarachnoid haemorrhage. Cochrane Database Syst Rev 2010; (2): CD006778.
99. Klimo P Jr, Kestle JR, MacDonald JD, Schmidt RH. Marked reduction of cerebral vasospasm with lumbar drainage of cerebrospinal fluid after subarachnoid hemorrhage. J Neurosurg 2004;100(2):215-24. (Pubitemid 38140223)
100. Al-Tamimi YZ, Bhargava D, Feltbower RG, et al. Lumbar drainage of cerebrospinal fluid after aneurysmal subarachnoid hemorrhage: a prospective, randomized, controlled trial (LUMAS). Stroke 2012;43(3):677-82.
101. Bardutzky J, Witsch J, Jüttler E, Schwab S, Vajkoczy P, Wolf S. EARLYDRAIN-outcome after early lumbar CSF-drainage in aneurysmal subarachnoid hemorrhage: study protocol for a randomized controlled trial. Trials 2011;12:203.
102. Zwienenberg-Lee M, Hartman J, Rudisill N, et al. Balloon Prophylaxis for Aneurysmal Vasospasm (BPAV) Study Group. Effect of prophylactic transluminal balloon angioplasty on cerebral vasospasm and outcome in patients with Fisher grade III subarachnoid hemorrhage: results of a phase II multicenter, randomized, clinical trial. Stroke 2008;39(6):1759-65.
103. Dreier JP, Windmüller O, Petzold G, Lindauer U, Einhäupl KM, Dirnagl U. Ischemia triggered by red blood cell products in the subarachnoid space is inhibited by nimodipine administration or moderate volume expansion/hemodilution in rats. Neurosurgery 2002;51(6):1457-67. (Pubitemid 36098695)
104. Richter F, Ebersberger A, Schaible HG. Blockade of voltage-gated calcium channels in rat inhibits repetitive cortical spreading depression. Neurosci Lett 2002;334(2):123-6. (Pubitemid 35341637)
105. Kaube H, Goadsby PJ. Anti-migraine compounds fail to modulate the propagation of cortical spreading depression in the cat. Eur Neurol 1994;34(1):30-5. (Pubitemid 24014718)
106. Gorelova NA, Koroleva VI, Amemori T, Pavlík V, Burs J Ketamine blockade of cortical spreading depression in rats. Electroencephalogr Clin Neurophysiol 1987;66(4):440-7. (Pubitemid 17030609)
107. Hernándéz-Cáceres J, Macias-González R, Brozek G, Bures J. Systemic ketamine blocks cortical spreading depression but does not delay the onset of terminal anoxic depolarization in rats. Brain Res 1987;437(2):360-4. (Pubitemid 18016224)
108. Sakowitz OW, Kiening KL, Krajewski KL, et al. Preliminary evidence that ketamine inhibits spreading depolarizations in acute human brain injury. Stroke 2009;40(8):e519-22.
109. Hertle DN, Dreier JP, Woitzik J, et al. for the Cooperative Study of Brain Injury Depolarizations (COSBID). Effect of analgesics and sedatives on the occurrence of spreading depolarizations accompanying acute brain injury. Brain. 2012;135(Pt 8):2390-8.
110. Welters ID, Hafer G, Menzebach A, et al. Ketamine inhibits transcription factors activator protein 1 and nuclear factor-kappaB, interleukin-8 production, as well as CD11b and CD16 expression: studies in human leukocytes and leukocytic cell lines. Anesth Analg 2010;110(3):934-41.
111. Shin HK, Dunn AK, Jones PB, et al. Normobaric hyperoxia improves cerebral blood flow and oxygenation, and inhibits periinfarct depolarizations in experimental focal ischaemia. Brain 2007;130(Pt 6):1631-42. (Pubitemid 47355921)
112. Sasaki T, Takeda Y, Taninishi H, Arai M, Shiraishi K, Morita K. Dynamic changes in cortical NADH fluorescence in rat focal ischemia: evaluation of the effects of hypothermia on propagation of peri-infarct depolarization by temporal and spatial analysis. Neurosci Lett 2009;449(1):61-5.