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  • Print publication year: 2016
  • Online publication date: October 2016

Chapter 4 - Vasospasm and delayed cerebral ischemia in aneurysmal subarachnoid hemorrhage

from Section I - Iatrogenic ischemic strokes: peri- and postoperative strokes
1.Rosengart, A J, Schultheiss, K E, Tolentino, J, Macdonald, R L. Prognostic factors for outcome in patients with aneurysmal subarachnoid hemorrhage. Stroke. 2007; 38: 2315–21.
2.Rabinstein, A A, Weigand, S, Atkinson, J L, Wijdicks, E F. Patterns of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke. 2005; 36: 992–7.
3.Nornes, H. The role of intracranial pressure in the arrest of hemorrhage in patients with ruptured intracranial aneurysm. J Neurosurg. 1973; 39: 226–34.
4.Dreier, J P, 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: 658–66.
5.Ostrowski, R P, Colohan, A R, Zhang, J H. Molecular mechanisms of early brain injury after subarachnoid hemorrhage. Neurol Res. 2006; 28: 399414.
6.Vergouwen, M D, Vermeulen, M, van Gijn, J, et al. Definition of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage as an outcome event in clinical trials and observational studies: Proposal of a multidisciplinary research group. Stroke. 2010; 41: 2391–5.
7.Schmidt, J M, Wartenberg, K E, Fernandez, A, et al. Frequency and clinical impact of asymptomatic cerebral infarction due to vasospasm after subarachnoid hemorrhage. J Neurosurg. 2008; 109: 1052–9.
8.Baldwin, M E, Macdonald, R L, Dezheng, H, et al. Early vasospasm on admission angiography in patients with aneurysmal subarachnoid haemorrhage is a predictor for in-hospital complications and poor outcome. Stroke. 2004; 35: 2506–11.
9.Cahill, J, Calvert, J W, Zhang, J H. Mechanisms of early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2006; 26: 1341–53.
10.Pluta, R M. Delayed cerebral vasospasm and nitric oxide: Review, new hypothesis, and proposed treatment. Pharmacol Ther. 2005; 105: 2356.
11.Seifert, V, Loffler, B M, Zimmermann, M, Roux, S, Stolke, D. Endothelin concentrations in patients with aneurysmal subarachnoid hemorrhage. Correlation with cerebral vasospasm, delayed ischemic neurological deficits, and volume of hematoma. J Neurosurg. 1995; 82: 5562.
12.Sehba, F A, Bederson, J B. Mechanisms of acute brain injury after subarachnoid hemorrhage. Neurol Res. 2006; 28: 381–98.
13.Turner, C P, Bergeron, M, Matz, P, et al. Heme oxygenase-1 is induced in glia throughout brain by subarachnoid hemoglobin. J Cereb Blood Flow Metab. 1998; 18: 257–73.
14.Dietrich, H H, Dacey, R G Jr. Molecular keys to the problems of cerebral vasospasm. Neurosurgery. 2000; 46: 517–30.
15.Nishizawa, S, Laher, I. Signaling mechanisms in cerebral vasospasm. Trends Cardiovasc Med. 2005; 15: 2434.
16.Zimmermann, M, Seifert, V. Endothelin and subarachnoid hemorrhage: An overview. Neurosurgery. 1998; 43: 863–75.
17.Fassbender, K, Hodapp, B, Rossol, S, et al. Endothelin-1 in subarachnoid hemorrhage: An acute-phase reactant produced by cerebrospinal fluid leukocytes. Stroke. 2000; 31: 2971–5.
18.Macdonald, R L, Higashida, R T, Keller, E, et al. Randomized trial of clazosentan in patients with aneurysmal subarachnoid hemorrhage undergoing endovascular coiling. Stroke. 2012; 43: 1463–9.
19.Luders, J C, Weihl, C C, Lin, G, et al. Adenoviral gene transfer of nitric oxide synthase increases cerebral blood flow in rats. Neurosurgery. 2000; 47: 1206–14.
20.Clatterbuck, R E, Gailloud, P, Tierney, T, et al. Release of a nitric oxide donor for the prevention of delayed cerebral vasospasm following experimental subarachnoid hemorrhage in nonhuman primates. J Neurosurg. 2005; 103: 745–51.
21.Tierney, T S, Pradilla, G, Wang, P P, Clatterbuck, R E, Tamargo, R J. Intracranial delivery of the nitric oxide donor diethylenetriamine/nitric oxide from a controlled-release polymer: Toxicity in cynomolgus monkeys. Neurosurgery. 2006; 58: 952–60.
22.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. JAMA. 2005; 293: 1477–84.
23.McGirt, M J, Lynch, J R, Parra, A, et al. Simvastatin increases endothelial nitric oxide synthase and ameliorates cerebral vasospasm resulting from subarachnoid hemorrhage. Stroke. 2002; 33: 2950–6.
24.McGirt, M J, Pradilla, G, Legnani, F G, et al. Systemic administration of simvastatin after the onset of experimental subarachnoid hemorrhage attenuates cerebral vasospasm. Neurosurgery. 2006; 58: 945–51.
25.Tseng, M Y, Czosnyka, M, Richards, H, Pickard, J D, Kirkpatrick, P J. Effects of acute treatment with pravastatin on cerebral vasospasm, autoregulation, and delayed ischemic deficits after aneurysmal subarachnoid hemorrhage: A phase II randomized placebo-controlled trial. Stroke. 2005; 36: 1627–32.
26.Dreier, J P, Korner, K, Ebert, N, et al. Nitric oxide scavenging by hemoglobin or nitric oxide synthase inhibition by n-nitro-l-arginine induces cortical spreading ischemia when K+ is increased in the subarachnoid space. J Cereb Blood Flow Metab. 1998; 18: 978–90.
27.Ishiguro, M, Wellman, T L, Honda, A, et al. Emergence of a R-type Ca2+ channel (CAV 2.3) contributes to cerebral artery constriction after subarachnoid hemorrhage. Circ Res. 2005; 96: 419–26.
28.Pluta, R M, Hansen-Schwartz, J, Dreier, J, et al. Cerebral vasospasm following subarachnoid hemorrhage: Time for a new world of thought. Neurol Res. 2009; 31: 151–8.
29.Kusaka, G, Ishikawa, M, Nanda, A, Granger, D N, Zhang, J H. Signaling pathways for early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2004; 24: 916–25.
30.Birse, S H, Tom, M I. Incidence of cerebral infarction associated with ruptured intracranial aneurysms. A study of 8 unoperated cases of anterior cerebral aneurysm. Neurology. 1960; 10: 101–6.
31.Dreier, J P, Woitzik, J, Fabricius, M, et al. Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. Brain. 2006; 129: 3224–37.
32.Stein, S C, Levine, J M, Nagpal, S, LeRoux, P D. Vasospasm as the sole cause of cerebral ischemia: how strong is the evidence? Neurosurg Focus. 2006; 21: E2.
33.Park, S, Yamaguchi, M, Zhou, Z, et al. Neurovascular protection reduces early brain injury after subarachnoid hemorrhage. Stroke. 2004; 35: 2412–17.
34.Fisher, C M, Kistler, J P, Davis, J M. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery, 1980; 6: 19.
35.Kistler, J P, Crowell, R M, Davis, K R. The relation of cerebral vasospasm to the extent and location of subarachnoid blood visualized by CT scan: A prospective study. Neurology, 1983; 33: 424–36.
36.Claassen, J, Bernardini, G L, Kreiter, K et al. Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: The Fisher scale revisited. Stroke. 2001; 32: 2012–20.
37.Connolly, E S Jr., Rabinstein, A, Carhuapoma, J R, et al. 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. 2012; 43: 1711–37.
38.Diringer, M N, Bleck, T P, Claude Hemphill, J 3rd, et al. Critical care management of patients following aneurysmal subarachnoid hemorrhage: Recommendations from the Neurocritical Care Society’s multidisciplinary consensus conference. Neurocrit Care. 2011; 15: 211–40.
39.Washington, C W, Zipfel, G J. Detection and monitoring of vasospasm and delayed cerebral ischemia: A review and assessment of the literature. Neurocrit Care. 2011; 15: 312–17.
40.Sloan, M A, Alexandrov, A V, Tegeler, C H, et al. Assessment: Transcranial Doppler ultrasonography: Report of the therapeutics and technology assessment subcommittee of the American Academy of Neurology. Neurology. 2004; 62: 1468–81.
41.Harrigan, M R, Magnano, C R, Guterman, L R, Hopkins, L N. Computed tomographic perfusion in the management of aneurysmal subarachnoid hemorrhage: New application of an existent technique. Neurosurgery. 2005; 56: 304–17.
42.Greenberg, E D, Gold, R, Reichman, M, et al. Diagnostic accuracy of CT angiography and CT perfusion for cerebral vasospasm: A meta-analysis. Am J Neuroradiol. 2010; 31: 1853–60.
43.Stocchetti, N. Triggers for aggressive interventions in subarachnoid hemorrhage. Neurocrit Care. 2011; 15: 324–8.
44.Hanggi, D. Monitoring and detection of vasospasm II: EEG and invasive monitoring. Neurocrit Care. 2011; 15: 318–23.
45.Dorhout Mees, S M, Rinkel, G J, Feigin, V L, et al. Calcium antagonists for aneurysmal subarachnoid hemorrhage. Stroke. 2008; 39: 514–15.
46.Philippon, J, Grob, R, Dagreou, F, et al. Prevention of vasospasm in subarachnoid haemorrhage. A controlled study with nimodipine. Acta Neurochirurgica. 1986; 82: 110–14.
47.Treggiari, M M, Walder, B, Suter, P M, Romand, J A. Systematic review of the prevention of delayed ischemic neurological deficits with hypertension, hypervolemia, and hemodilution therapy following subarachnoid hemorrhage. J Neurosurg. 2003; 98: 978–84.
48.Rinkel, G J, Feigin, V L, Algra, A, van Gijn, J. Circulatory volume expansion therapy for aneurysmal subarachnoid haemorrhage. Cochrane Database Syst Rev. 2004; CD000483.
49.Hasan, D, Vermeulen, M, Wijdicks, E F, Hijdra, A, van Gijn, J. Effect of fluid intake and antihypertensive treatment on cerebral ischemia after subarachnoid hemorrhage. Stroke. 1989; 20: 1511–15.
50.Wong, G K, Poon, W S, Chan, M T, et al. Intravenous magnesium sulphate for aneurysmal subarachnoid hemorrhage (IMASH): A randomized, double-blinded, placebo-controlled, multicenter phase III trial. Stroke. 2010; 41: 921–6.
51.Dorhout Mees, S M, Algra, A, et al. Magnesium for aneurysmal subarachnoid haemorrhage (MASH-2): A randomised placebo-controlled trial. Lancet. 2012; 380: 44–9.
52.Tseng, M Y. Summary of evidence on immediate statins therapy following aneurysmal subarachnoid hemorrhage. Neurocrit Care. 2011; 15: 298301.
53.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. 2008; 39: 1759–65.
54.Diringer, M N, Axelrod, Y. Hemodynamic manipulation in the neuro-intensive care unit: Cerebral perfusion pressure therapy in head injury and hemodynamic augmentation for cerebral vasospasm. Curr Opin Crit Care. 2007; 13: 156–62.
55.Lee, K H, Lukovits, T, Friedman, J A. “Triple-H” therapy for cerebral vasospasm following subarachnoid hemorrhage. Neurocrit Care. 2006; 4: 6876.
56.Meyer, R, Deem, S, Yanez, N D, et al. Current practices of triple-H prophylaxis and therapy in patients with subarachnoid hemorrhage. Neurocrit Care. 2011; 14: 2436.
57.Platz, J, Guresir, E, Vatter, H, et al. Unsecured intracranial aneurysms and induced hypertension in cerebral vasospasm: Is induced hypertension safe? Neurocrit Care. 2011; 14: 168–75.
58.Le Roux, P D. Anemia and transfusion after subarachnoid hemorrhage. Neurocrit Care. 2011; 15: 342–53.
59.Naidech, A M, Shaibani, A, Garg, R K, et al. Prospective, randomized trial of higher goal hemoglobin after subarachnoid hemorrhage. Neurocrit Care. 2011; 13: 313–20.
60.Frontera, J A, Fernandez, A, Schmidt, J M, et al. Clinical response to hypertensive hypervolemic therapy and outcome after subarachnoid hemorrhage. Neurosurgery. 2010; 66: 3541.
61.Kimball, M M, Velat, G J, Hoh, B L. Critical care guidelines on the endovascular management of cerebral vasospasm. Neurocrit Care. 2011; 15: 336–41.
62.Stuart, R M, Helbok, R, Kurtz, P, et al. High-dose intra-arterial verapamil for the treatment of cerebral vasospasm after subarachnoid hemorrhage: Prolonged effects on hemodynamic parameters and brain metabolism. Neurosurgery. 2011; 68: 337–45.
63.Tejada, J G, Taylor, R A, Ugurel, M S, et al. Safety and feasibility of intra-arterial nicardipine for the treatment of subarachnoid hemorrhage-associated vasospasm: Initial clinical experience with high-dose infusions. Am J Neuroradiol. 2007; 28: 844–8.
64.Shankar, J J, dos Santos, M P, Deus-Silva, L, Lum, C. Angiographic evaluation of the effect of intra-arterial milrinone therapy in patients with vasospasm from aneurysmal subarachnoid hemorrhage. Neuroradiology. 2011; 53: 123–8.
65.Jestaedt, L, Pham, M, Bartsch, A J, et al. The impact of balloon angioplasty on the evolution of vasospasm-related infarction after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2008; 62: 610–17.