Cerebral vasospasm after aneurysmal subarachnoid hemorrhage and traumatic brain injury

Current Treatment Options in Neurology

Volumn 16, Issue 1, 2014, Pages

  Izzy, Saef ^a   Muehlschlegel, Susanne ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Aneurysmal subarachnoid hemorrhage; Angiographic vasospasm; Blast injury; Cerebral vasospasm; Delayed cerebral ischemia; Subarachnoid hemorrhage; Traumatic brain injury; Traumatic subarachnoid hemorrhage; Treatment

Indexed keywords

CALCIUM CHANNEL BLOCKING AGENT; CLAZOSENTAN; DANTROLENE; ENDOTHELIN; HEMOGLOBIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; HYPOXIA INDUCIBLE FACTOR 1; MAGNESIUM SULFATE; NITRIC OXIDE; THROMBIN;

ARTICLE; BLOOD VESSEL DIAMETER; BRAIN ANGIOGRAPHY; BRAIN TISSUE; BRAIN VASOSPASM; COMPUTED TOMOGRAPHIC ANGIOGRAPHY; DISEASE SURVEILLANCE; ELECTROENCEPHALOGRAM; HUMAN; INFLAMMATION; MICRODIALYSIS; NEUROMONITORING; OXIMETRY; PATHOPHYSIOLOGY; PERFUSION WEIGHTED IMAGING; RISK FACTOR; SUBARACHNOID HEMORRHAGE; THERMAL DIFFUSION; TRANSCRANIAL DOPPLER; TRAUMATIC BRAIN INJURY;

EID: 84891790836     PISSN: 10928480     EISSN: 15343138     Source Type: Journal    
DOI: 10.1007/s11940-013-0278-x     Document Type: Article

References (99)

1. Connolly Jr ES, Rabinstein AA, Carhuapoma JR, et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: A guideline for healthcare professionals from the American Heart Association/ american Stroke Association. Stroke; J Cereb Circul. 2012;43:1711-37. These are the most updated AHA guidelines for the care of SAH patients.
2. Pluta RM. Delayed cerebral vasospasm and nitric oxide: Review, new hypothesis, and proposed treatment. Pharmacol Therapeut. 2005;105:23-56.
3. Nolan CP, Macdonald RL. Can angiographic vasospasm be used as a surrogate marker in evaluating therapeutic interventions for cerebral vasospasm? Neurosurg Focus. 2006;21:E1.
4. Edlow JA, Caplan LR. Avoiding pitfalls in the diagnosis of subarachnoid hemorrhage. New England J Med. 2000;342:29-36.
5. Rozsa L, Gombi R, Szabo S, Sztermen M. Vasospasm after head injury studied by transcranial Doppler sonography. Radiologia Diagnostica. 1989;30:151-7.
6. Eisenberg HM, Gary Jr HE, Aldrich EF, et al. Initial CT findings in 753 patients with severe head injury. A report from the NIH Traumatic Coma Data Bank. J Neurosurg. 1990;73:688-98.
7. Oertel M, Boscardin WJ, Obrist WD, et al. Posttraumatic vasospasm: The epidemiology, severity, and time course of an underestimated phenomenon: A prospective study performed in 299 patients. J Neurosurg. 2005;103:812-24.
8. Zubkov AY, Lewis AI, Raila FA, Zhang J, Parent AD. Risk factors for the development of posttraumatic cerebral vasospasm. Surgic Neurol. 2000;53:126-30.
9. Taneda M, Kataoka K, Akai F, Asai T, Sakata I. Traumatic subarachnoid hemorrhage as a predictable indicator of delayed ischemic symptoms. J Neurosurg. 1996;84:762-8.
10. Kramer DR, Winer JL, Pease BA, Amar AP, Mack WJ. Cerebral vasospasm in traumatic brain injury. Neurology Research International. 2013;2013:415813.
11. Servadei F, Murray GD, Teasdale GM, et al. Traumatic subarachnoid hemorrhage: Demographic and clinical study of 750 patients from the European brain injury consortium survey of head injuries. Neurosurgery. 2002;50:261-7. discussion 7-9.
12. Bell RS, Ecker RD, Severson 3rd MA, Wanebo JE, Crandall B, Armonda RA. The evolution of the treatment of traumatic cerebrovascular injury during wartime. Neurosurg Focus. 2010;28:E5.
13. Armonda RA, Bell RS, Vo AH, et al. Wartime traumatic cerebral vasospasm: Recent review of combat casualties. Neurosurgery. 2006;59:1215-25 discussion 25.
14. Arutiunov AI, Baron MA, Majorova NA. The role of mechanical factors in the pathogenesis of short-term and prolonged spasm of the cerebral arteries. J Neurosurg. 1974;40:459-72.
15. Frontera JA, Fernandez A, Schmidt JM, et al. Defining vasospasm after subarachnoid hemorrhage: What is the most clinically relevant definition? Stroke; J Cereb Circul. 2009;40:1963-8.
16. Claassen J, Bernardini GL, Kreiter K, et al. Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: The Fisher scale revisited. Stroke; J Cereb Circul. 2001;32:2012-20.
17. Hunt WE, Hess RM. Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg. 1968;28:14-20.
18. Gonzalez NR, Boscardin WJ, Glenn T, Vinuela F, Martin NA. Vasospasm probability index: A combination of transcranial doppler velocities, cerebral blood flow, and clinical risk factors to predict cerebral vasospasm after aneurysmal subarachnoid hemorrhage. J Neurosurg. 2007;107:1101-12.
19. Schmidt JM, Wartenberg KE, Fernandez A, et al. Frequency and clinical impact of asymptomatic cerebral infarction due to vasospasm after subarachnoid hemorrhage. J Neurosurg. 2008;109:1052-9.
20. Diringer MN, Bleck TP, Claude Hemphill 3rd J, et al. Critical care management of patients following aneurysmal subarachnoid hemorrhage: Recommendations from the Neurocritical Care Society's Multidisciplinary Consensus Conference. Neurocritical care. 2011;15:211-40. This is a multidisciplinary guideline about the critical care management of SAH with an extensive review of the SAH treatment literature.
21. Rabinstein AA, Friedman JA, Weigand SD, et al. Predictors of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke; J Cereb Circul. 2004;35:1862-6.
22. Rabinstein AA, Weigand S, Atkinson JL, Wijdicks EF. Patterns of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke; J Cereb Circul. 2005;36:992-7.
23. Findlay JM, Weir BK, Steinke D, Tanabe T, Gordon P, Grace M. Effect of intrathecal thrombolytic therapy on subarachnoid clot and chronic vasospasm in a primate model of SAH. J Neurosurg. 1988;69:723-35.
24. Tsuji T, Cook DA, Weir BK, Handa Y. Effect of clot removal on cerebrovascular contraction after subarachnoid hemorrhage in the monkey: Pharmacological study. Heart Vessel. 1996;11:69-79.
25. Findlay JM, Kassell NF, Weir BK, et al. A randomized trial of intraoperative, intracisternal tissue plasminogen activator for the prevention of vasospasm. Neurosurgery. 1995;37:168-76. discussion 77-8.
26. Fisher CM, Kistler JP, Davis JM. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery. 1980;6:1-9.
27. Friedman JA, Goerss SJ, Meyer FB, et al. Volumetric quantification of Fisher Grade 3 aneurysmal subarachnoid hemorrhage: A novel method to predict symptomatic vasospasm on admission computerized tomography scans. J Neurosurg. 2002;97:401-7.
28. Macdonald RL, Weir BK. A review of hemoglobin and the pathogenesis of cerebral vasospasm. Stroke; J Cereb Circul. 1991;22:971-82.
29. Lin CL, Shih HC, Dumont AS, et al. The effect of 17beta-estradiol in attenuating experimental subarachnoid hemorrhage-induced cerebral vasospasm. J Neurosurg. 2006;104:298-304.
30. Oldfield EH, Loomba JJ, Monteith SJ, et al. Safety and pharmacokinetics of sodium nitrite in patients with subarachnoid hemorrhage: A Phase IIA study. J Neurosurg. 2013;119:634-41.
31. Mukherjee KK, Singh SK, Khosla VK, Mohindra S, Salunke P. Safety and efficacy of sildenafil citrate in reversal of cerebral vasospasm: A feasibility study. Surgic Neurol Internat. 2012;3:3.
32. Semenza G. Signal transduction to hypoxia-inducible factor 1. Biochem Pharmacol. 2002;64:993-8.
33. Hishikawa T, Ono S, Ogawa T, Tokunaga K, Sugiu K, Date I. Effects of deferoxamine-activated hypoxiainducible factor-1 on the brainstem after subarachnoid hemorrhage in rats. Neurosurgery. 2008;62:232-40. discussion 40-1.
34. Yan J, Chen C, Lei J, et al. 2-methoxyestradiol reduces cerebral vasospasm after 48 hours of experimental subarachnoid hemorrhage in rats. Exp Neurol. 2006;202:348-56.
35. Yanagisawa M, Kurihara H, Kimura S, et al. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature. 1988;332:411-5.
36. Yamaji T, Johshita H, Ishibashi M, et al. Endothelin family in human plasma and cerebrospinal fluid. The Journal of Clinical Endocrinology and Metabolism. 1990;71:1611-5.
37. Rubanyi GM, Polokoff MA. Endothelins: Molecular biology, biochemistry, pharmacology, physiology, and pathophysiology. Pharmacol Rev. 1994;46:325-415.
38. Macdonald RL, Higashida RT, Keller E, et al. Randomized trial of clazosentan in patients with aneurysmal subarachnoid hemorrhage undergoing endovascular coiling. Stroke; J Cereb Circul. 2012;43:1463-9. These are results from the promising Phase II trial of clazosentan.
39. Sugawara T, Jadhav V, Ayer R, Chen W, Suzuki H, Zhang JH. Thrombin inhibition by argatroban ameliorates early brain injury and improves neurological outcomes after experimental subarachnoid hemorrhage in rats. Stroke; J Cereb Circul. 2009;40:1530-2.
40. Kai Y, Hirano K, Maeda Y, Nishimura J, Sasaki T, Kanaide H. Prevention of the hypercontractile response to thrombin by proteinase-activated receptor-1 antagonist in subarachnoid hemorrhage. Stroke; J Cereb Circul. 2007;38:3259-65.
41. Tsurutani H, Ohkuma H, Suzuki S. Effects of thrombin inhibitor on thrombin-related signal transduction and cerebral vasospasm in the rabbit subarachnoid hemorrhage model. Stroke; J Cereb Circul. 2003;34:1497-500.
42. Dumont AS, Dumont RJ, Chow MM, et al. Cerebral vasospasm after subarachnoid hemorrhage: Putative role of inflammation. Neurosurgery. 2003;53:123-33. discussion 33-5.
43. Bowman G, Bonneau RH, Chinchilli VM, Tracey KJ, Cockroft KM. A novel inhibitor of inflammatory cytokine production (CNI-1493) reduces rodent posthemorrhagic vasospasm. Neurocrit Care. 2006;5:222-9.
44. Grisham MB, Granger DN, Lefer DJ. Modulation of leukocyte-endothelial interactions by reactive metabolites of oxygen and nitrogen: Relevance to ischemic heart disease. Free radical Biology & Medicine. 1998;25:404-33.
45. Fassbender K, Hodapp B, Rossol S, et al. Endothelin-1 in subarachnoid hemorrhage: An acute-phase reactant produced by cerebrospinal fluid leukocytes. Stroke; J Cereb Circul. 2000;31:2971-5.
46. McGirt MJ, Pradilla G, Legnani FG, et al. Systemic administration of simvastatin after the onset of experimental subarachnoid hemorrhage attenuates cerebral vasospasm. Neurosurgery. 2006;58:945-51. discussion 51.
47. Tseng MY, Czosnyka M, Richards H, Pickard JD, Kirkpatrick PJ. Effects of acute treatment with statins on cerebral autoregulation in patients after aneurysmal subarachnoid hemorrhage. Neurosurg Focus. 2006;21:E10.
48. ClinicalTrials.gov. Simvastatin in Aneurysmal Subarachnoid Haemorrhage (STASH) a Multicentre Randomised Controlled Clinical Trial. 2013.
49. Wilkins RH, Odom GL. Intracranial arterial spasm associated with craniocerebral trauma. J Neurosurg. 1970;32:626-33.
50. Steiger HJ, Aaslid R, Stooss R, Seiler RW. Transcranial doppler monitoring in head injury: Relations between type of injury, flow velocities, vasoreactivity, and outcome. Neurosurgery. 1994;34:79-85. discussion 6.
51. Alford PW, Dabiri BE, Goss JA, Hemphill MA, Brigham MD, Parker KK. Blast-induced phenotypic switching in cerebral vasospasm. Proc Natl Acad Sci U S A. 2011;108:12705-10.
52. Fukuda T, Hasue M, Ito H. Does traumatic subarachnoid hemorrhage caused by diffuse brain injury cause delayed ischemic brain damage? Comparison with subarachnoid hemorrhage caused by ruptured intracranial aneurysms. Neurosurgery. 1998;43:1040-9.
53. Woitzik J, Dreier JP, Hecht N, et al. Delayed cerebral ischemia and spreading depolarization in absence of angiographic vasospasm after subarachnoid hemorrhage. Journal of Cerebral Blood Flow and Metabolism: Official Journal of the International Society of Cerebral Blood Flow and Metabolism. 2012;32:203-12. Interesting, albeit small study in SAH patients revealing that DCI can occur in the absence of cVSP but may be due to spreading depolorizations.
54. Dreier JP, Drenckhahn C, Woitzik J, et al. Spreading ischemia after aneurysmal subarachnoid hemorrhage. Acta Neurochirurgica Supplement. 2013;115:125-9.
55. 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 hemorrhage, and traumatic brain injury. Journal of Cerebral Blood Flow and Metabolism: Official Journal of the International Society of Cerebral Blood Flow and Metabolism. 2011;31:17-35.
56. Hartings JA, Bullock MR, Okonkwo DO, et al. Spreading depolarisations and outcome after traumatic brain injury: A prospective observational study. Lancet Neurol. 2011;10:1058-64. An intriguing, large study in TBI patients that shows that spreading depolorizations are associated with worse clinical outcomes after TBI, without proving causality.
57. Deb S, Gogos AJ, Drummond KJ, Teddy PJ. The role of transcranial Doppler ultrasound monitoring in patients with aneurysmal subarachnoid haemorrhage. Journal of Clinical Neuroscience: Official Journal of the Neurosurgical Society of Australasia. 2012;19:950-5.
58. Jakobsen M, Enevoldsen E, Dalager T. Spasm index in subarachnoid haemorrhage: Consequences of vasospasm upon cerebral blood flow and oxygen extraction. Acta Neurol Scand. 1990;82:311-20.
59. Lindegaard KF, Nornes H, Bakke SJ, Sorteberg W, Nakstad P. Cerebral vasospasm diagnosis by means of angiography and blood velocity measurements. Acta Neurochir. 1989;100:12-24.
60. Washington CW, Zipfel GJ. Participants in the International Multi-disciplinary Consensus Conference on the Critical Care Management of Subarachnoid H. Detection and monitoring of vasospasm and delayed cerebral ischemia: A review and assessment of the literature. Neurocrit Care. 2011;15:312-7.
61. Dankbaar JW, de Rooij NK, Velthuis BK, Frijns CJ, Rinkel GJ, van der Schaaf IC. Diagnosing delayed cerebral ischemia with different CT modalities in patients with subarachnoid hemorrhage with clinical deterioration. Stroke; J Cereb Circul. 2009;40:3493-8.
62. Sanelli PC, Ugorec I, Johnson CE, et al. Using quantitative CT perfusion for evaluation of delayed cerebral ischemia following aneurysmal subarachnoid hemorrhage. AJNR American Journal of Neuroradiology. 2011;32:2047-53.
63. Rordorf G, Koroshetz WJ, Copen WA, et al. Diffusion-and perfusion-weighted imaging in vasospasm after subarachnoid hemorrhage. Stroke; J Cereb Circul. 1999;30:599-605.
64. Vespa PM, Nuwer MR, Juhasz C, et al. Early detection of vasospasm after acute subarachnoid hemorrhage using continuous EEG ICU monitoring. Electroencephalogr Clin Neurophysiol. 1997;103:607-15.
65. Claassen J, Mayer SA, Hirsch LJ. Continuous EEG monitoring in patients with subarachnoid hemorrhage. Journal of Clinical Neurophysiology: Official Publication of the American Electroencephalographic Society. 2005;22:92-8.
66. Khaldi A, Zauner A, ReinertM,Woodward JJ, BullockMR. Measurement of nitric oxide and brain tissue oxygen tension in patients after severe subarachnoid hemorrhage. Neurosurgery. 2001;49:33-8. discussion 8-40.
67. Jaeger M, Schuhmann MU, Soehle M, Nagel C, Meixensberger J. Continuous monitoring of cerebrovascular autoregulation after subarachnoid hemorrhage by brain tissue oxygen pressure reactivity and its relation to delayed cerebral infarction. Stroke; J Cereb Circul. 2007;38:981-6.
68. Barth M, Woitzik J, Weiss C, et al. Correlation of clinical outcome with pressure-, oxygen-, and flowrelated indices of cerebrovascular reactivity in patients following aneurysmal SAH. Neurocritical care. 2010;12:234-43.
69. Kistka H, Dewan MC, Mocco J. Evidence-based cerebral vasospasm surveillance. Neurology Research International. 2013;2013:256713.
70. Unterberg AW, Sakowitz OW, Sarrafzadeh AS, Benndorf G, Lanksch WR. Role of bedside microdialysis in the diagnosis of cerebral vasospasm following aneurysmal subarachnoid hemorrhage. J Neurosurg. 2001;94:740-9.
71. Staub F, Graf R, Gabel P, Kochling M, Klug N, Heiss WD. Multiple interstitial substances measured by microdialysis in patients with subarachnoid hemorrhage. Neurosurgery. 2000;47:1106-15. discussion 15-6.
72. Vajkoczy P, Horn P, Thome C, Munch E, Schmiedek P. Regional cerebral blood flow monitoring in the diagnosis of delayed ischemia following aneurysmal subarachnoid hemorrhage. J Neurosurg. 2003;98:1227-34.
73. von Helden A, Schneider GH, Unterberg A, Lanksch WR. Monitoring of jugular venous oxygen saturation in comatose patients with subarachnoid haemorrhage and intracerebral haematomas. Acta Neurochir Suppl. 1993;59:102-6.
74. Heran NS, Hentschel SJ, Toyota BD. Jugular bulb oximetry for prediction of vasospasm following subarachnoid hemorrhage. The Canadian Journal of Neurological Sciences. 2004;31:80-6.
75. Dorhout Mees SM, Rinkel GJ, Feigin VL, et al. Calcium antagonists for aneurysmal subarachnoid haemorrhage. The Cochrane database of systematic reviews 2007:CD000277.
76. Philippon J, Grob R, Dagreou F, Guggiari M, Rivierez M, Viars P. Prevention of vasospasm in subarachnoid haemorrhage. A controlled study with nimodipine. Acta neurochirurgica. 1986;82:110-4.
77. Tani E, Matsumoto T. Continuous elevation of intracellular Ca2+ is essential for the development of cerebral vasospasm. Curr Vasc Pharmacol. 2004;2:13-21.
78. Yamaura I, Tani E, Saido TC, Suzuki K, Minami N, Maeda Y. Calpain-calpastatin system of canine basilar artery in vasospasm. J Neurosurg. 1993;79:537-43.
79. Muehlschlegel S, Sims Jr. Dantrolene: Mechanisms of neuroprotection and possible clinical applications in the neurointensive care unit. Neurocritical care. 2009;10:103-15.
80. Frandsen A, Schousboe A. Dantrolene prevents glutamate cytotoxicity and Ca2+ release from intracellular stores in cultured cerebral cortical neurons. J Neurochem. 1991;56:1075-8.
81. Salomone S, Soydan G, Moskowitz MA, Sims Jr. Inhibition of cerebral vasoconstriction by dantrolene and nimodipine. Neurocritical care. 2009;10:93-102.
82. Muehlschlegel S, Rordorf G, Bodock M, Sims Jr. Dantrolene mediates vasorelaxation in cerebral vasoconstriction: A case series. Neurocritical care. 2009;10:116-21.
83. Muehlschlegel S, Rordorf G, Sims J. Effects of a single dose of dantrolene in patients with cerebral vasospasm after subarachnoid hemorrhage: A prospective pilot study. Stroke; J Cereb Circul. 2011;42:1301-6.
84. Majidi S, Grigoryan M, Tekle WG, Qureshi AI. Intraarterial dantrolene for refractory cerebral vasospasm after aneurysmal subarachnoid hemorrhage. Neurocritical care. 2012;17:245-9.
85. ClinicalTrials.gov. Safety Study of Dantrolene to Treat Cerebral Vasospasm After Subarachnoid Hemorrhage. 2013. www.ClinicalTrials.gov
86. Treggiari MM, Deem S. Which H is the most important in triple-H therapy for cerebral vasospasm? Curr Opin Crit Care. 2009;15:83-6.
87. Muench E, Horn P, Bauhuf C, et al. Effects of hypervolemia and hypertension on regional cerebral blood flow, intracranial pressure, and brain tissue oxygenation after subarachnoid hemorrhage. Crit Care Med. 2007;35:1844-51. quiz 52.
88. Naidech AM, Jovanovic B, Wartenberg KE, et al. Higher hemoglobin is associated with improved outcome after subarachnoid hemorrhage. Crit Care Med. 2007;35:2383-9.
89. Zwienenberg-Lee M, Hartman J, Rudisill N, et al. 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; J Cereb Circul. 2008;39:1759-65.
90. Vergouwen MD, Meijers JC, Geskus RB, et al. Biologic effects of simvastatin in patients with aneurysmal subarachnoid hemorrhage: A double-blind, placebocontrolled randomized trial. Journal of Cerebral Blood Flow and Metabolism: Official Journal of the International Society of Cerebral Blood Flow and Metabolism. 2009;29:1444-53.
91. Macdonald RL, Kassell NF, Mayer S, et al. Clazosentan to overcome neurological ischemia and infarction occurring after subarachnoid hemorrhage (CONSCIOUS-1): Randomized, double-blind, placebo-controlled phase 2 dose-finding trial. Stroke; J Cereb Circul. 2008;39:3015-21.
92. Macdonald RL, Higashida RT, Keller E, et al. Clazosentan, an endothelin receptor antagonist, in patients with aneurysmal subarachnoid haemorrhage undergoing surgical clipping: A randomised, doubleblind, placebo-controlled phase 3 trial (CONSCIOUS-2). Lancet neurology. 2011;10:618-25. This is a Phase III trial reporting the absence of efficacy of clazosentan in SAH.
93. Macdonald RL, Higashida RT, Keller E, et al. Randomised trial of clazosentan, an endothelin receptor antagonist, in patients with aneurysmal subarachnoid hemorrhage undergoing surgical clipping (CONSCIOUS-2). Acta Neurochir Suppl. 2013;115:27-31. This is the second negative trial of clazosentan in SAH.
94. Wong GK, Poon WS, Chan MT, et al. Intravenous magnesium sulphate for aneurysmal subarachnoid hemorrhage (IMASH): A randomized, doubleblinded, placebo-controlled, multicenter phase III trial. Stroke; J Cereb Circul. 2010;41:921-6.
95. Shimoda M, Oda S, Tsugane R, Sato O. Intracranial complications of hypervolemic therapy in patients with a delayed ischemic deficit attributed to vasospasm. J Neurosurg. 1993;78:423-9.
96. Lee JH, Martin NA, Alsina G, et al. Hemodynamically significant cerebral vasospasm and outcome after head injury: A prospective study. J Neurosurg. 1997;87:221-33.
97. Roos YB, de Haan RJ, Beenen LF, Groen RJ, Albrecht KW, Vermeulen M. Complications and outcome in patients with aneurysmal subarachnoid haemorrhage: A prospective hospital based cohort study in the Netherlands. J Neurol Neurosurg Psychiatry. 2000;68:337-41.
98. Shimoda M, Takeuchi M, Tominaga J, Oda S, Kumasaka A, Tsugane R.Asymptomatic versus symptomatic infarcts from vasospasm in patients with subarachnoid hemorrhage: Serialmagnetic resonance imaging.Neurosurgery. 2001;49:1341-8. discussion 8-50.
99. Suarez JI, Qureshi AI, Yahia AB, et al. Symptomatic vasospasm diagnosis after subarachnoid hemorrhage: Evaluation of transcranial Doppler ultrasound and cerebral angiography as related to compromised vascular distribution. Critical care medicine. 2002;30:1348-55.