Aneurysmal subarachnoid hemorrhage occurs in approximately 30,000 persons in the United States each year. Around 30 percent of patients with aneurysmal subarachnoid hemorrhage suffer from cerebral ischemia and infarction due to cerebral vasospasm, a leading cause of treatable death and disability following aneurysmal subarachnoid hemorrhage. Methods used to predict, diagnose, and manage vasospasm are the topic of recent active research. This paper utilizes a comprehensive review of the recent literature to address controversies surrounding these topics. Evidence regarding the effect of age, smoking, and cocaine use on the incidence and outcome of vasospasm is reviewed. The abilities of different computed tomography grading schemes to predict vasospasm in the aftermath of subarachnoid hemorrhage are presented. Additionally, the utility of different diagnostic methods for the detection and visualization of vasospasm, including transcranial Doppler ultrasonography, CT angiography, digital subtraction angiography, and CT perfusion imaging is discussed. Finally, the recent literature regarding interventions for the prophylaxis and treatment of vasospasm, including hyperdynamic therapy, albumin, calcium channel agonists, statins, magnesium sulfate, and endothelin antagonists is summarized. Recent studies regarding each topic were reviewed for consensus recommendations from the literature, which were then presented. 1. Introduction Aneurysmal subarachnoid hemorrhage (aSAH) is a relatively rare cause of stroke, occurring in approximately 30,000 persons in the United States each year. However, its impact equals that of cerebral ischemia, the most common cause of stroke, due to its higher morbidity, higher mortality, and occurrence in younger individuals. Approximately 20 to 30 percent of patients with aSAH suffer from cerebral ischemia and infarction due to cerebral vasospasm, which is the number one cause of treatable death and disability following aSAH. Vasospasm occurs most frequently at 7 to 8 days after aSAH and can last for a prolonged period. Clinical vasospasm is defined as a decline in neurologic status due to vasospasm and can result in severe morbidity and mortality. However, clinical vasospasm has also been observed after other invasive and traumatic processes such as craniotomy and traumatic brain injury. The pathogenesis and etiology of this vasospasm are very poorly understood, and treatments to prevent post-SAH vasospasm are widely varied and have greatly different magnitudes of effectiveness. New methods to predict, diagnosis, and manage
References
[1]
C. M. Fisher, G. H. Roberson, and R. G. Ojemann, “Cerebral vasospasm with ruptured saccular aneurysm—the clinical manifestations,” Neurosurgery, vol. 1, no. 3, pp. 245–248, 1977.
[2]
S. Ferguson and R. L. Macdonald, “Predictors of cerebral infarction in patients with aneurysmal subarachnoid hemorrhage,” Neurosurgery, vol. 60, no. 4, pp. 658–667, 2007.
[3]
A. A. Rabinstein, J. A. Friedman, S. D. Weigand et al., “Predictors of cerebral infarction in aneurysmal subarachnoid hemorrhage,” Stroke, vol. 35, no. 8, pp. 1862–1866, 2004.
[4]
M. D. I. Vergouwen, D. Ilodigwe, and R. L. MacDonald, “Cerebral infarction after subarachnoid hemorrhage contributes to poor outcome by vasospasm-dependent and -independent effects,” Stroke, vol. 42, no. 4, pp. 924–929, 2011.
[5]
M. D. I. Vergouwen, M. Vermeulen, J. van Gijn 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, vol. 41, no. 10, pp. 2391–2395, 2010.
[6]
N. K. de Rooij, F. H. H. Linn, J. A. van der Plas, A. Algra, and G. J. E. Rinkel, “Incidence of subarachnoid haemorrhage: a systematic review with emphasis on region, age, gender and time trends,” Journal of Neurology, Neurosurgery and Psychiatry, vol. 78, no. 12, pp. 1365–1372, 2007.
[7]
L. Artiola i Fortuny and L. Prieto-Valiente, “Long-term prognosis in surgically treated intracranial aneurysms—part 1: mortality,” Journal of Neurosurgery, vol. 54, no. 1, pp. 26–34, 1981.
[8]
C. Charpentier, G. Audibert, F. Guillemin et al., “Multivariate analysis of predictors of cerebral vasospasm occurrence after aneurysmal subarachnoid hemorrhage,” Stroke, vol. 30, no. 7, pp. 1402–1408, 1999.
[9]
S. P. Kale, R. C. Edgell, A. Alshekhlee, et al., “Age-associated vasospasm in aneurysmal subarachnoid hemorrhage,” Journal of Stroke and Cerebrovascular Diseases, vol. 22, no. 1, pp. 22–27, 2013.
[10]
S. N. Magge, H. I. Chen, R. Ramakrishna et al., “Association of a younger age with an increased risk of angiographic and symptomatic vasospasms following subarachnoid hemorrhage,” Journal of Neurosurgery, vol. 112, no. 6, pp. 1208–1215, 2010.
[11]
C. H. Rabb, G. Tang, L. S. Chin, and S. L. Giannotta, “A statistical analysis of factors related to symptomatic cerebral vasospasm,” Acta Neurochirurgica, vol. 127, no. 1-2, pp. 27–31, 1994.
[12]
M. T. Torbey, T.-K. Hauser, A. Bhardwaj et al., “Effect of age on cerebral blood flow velocity and incidence of vasospasm after aneurysmal subarachnoid hemorrhage,” Stroke, vol. 32, no. 9, pp. 2005–2011, 2001.
[13]
G. Lanzino, N. F. Kassell, T. P. Germanson et al., “Age and outcome after aneurysmal subarachnoid hemorrhage: why do older patients fare worse?” Journal of Neurosurgery, vol. 85, no. 3, pp. 410–418, 1996.
[14]
T. Inagawa, “Cerebral vasospasm in elderly patients treated by early operation for ruptured intracranial aneurysms,” Acta Neurochirurgica, vol. 115, no. 3-4, pp. 79–85, 1992.
[15]
T. M. Lasner, R. J. Weil, H. A. Riina et al., “Cigarette smoking-induced increase in the risk of symptomatic vasospasm after aneurysmal subarachnoid hemorrhage,” Journal of Neurosurgery, vol. 87, no. 3, pp. 381–384, 1997.
[16]
M. J. McGirt, J. C. Mavropoulos, L. Y. McGirt et al., “Leukocytosis as an independent risk factor for cerebral vasospasm following aneurysmal subarachnoid hemorrhage,” Journal of Neurosurgery, vol. 98, no. 6, pp. 1222–1226, 2003.
[17]
M. Ryttlefors, P. Enblad, E. Ronne-Engstr？m, L. Persson, D. Ilodigwe, and R. L. Macdonald, “Patient age and vasospasm after subarachnoid hemorrhage,” Neurosurgery, vol. 67, no. 4, pp. 911–917, 2010.
[18]
H. G. Boecher-Schnarz, K. Ungersboeck, P. Ulrich, G. Fries, A. Wild, and A. Perneczky, “Transcranial Doppler diagnosis of cerebral vasospasm following subarachnoid haemorrhage: correlation and analysis of results in relation to the age of patients,” Acta Neurochirurgica, vol. 127, no. 1-2, pp. 32–36, 1994.
[19]
B. A. Bell and L. Symon, “Smoking and subarachnoid haemorrhage,” British Medical Journal, vol. 1, no. 6163, pp. 577–578, 1979.
[20]
V. Feigin, V. Parag, C. M. M. Lawes et al., “Smoking and elevated blood pressure are the most important risk factors for subarachnoid hemorrhage in the Asia-Pacific region: an overview of 26 cohorts involving 306 620 participants,” Stroke, vol. 36, no. 7, pp. 1360–1365, 2005.
[21]
S. Juvela, M. Hillbom, H. Numminen, and P. Koskinen, “Cigarette smoking and alcohol consumption as risk factors for aneurysmal subarachnoid hemorrhage,” Stroke, vol. 24, no. 5, pp. 639–646, 1993.
[22]
B. K. A. Weir, G. L. Kongable, N. F. Kassell, J. R. Schultz, L. L. Truskowski, and A. Sigrest, “Cigarette smoking as a cause of aneurysmal subarachnoid hemorrhage and risk for vasospasm: a report of the Cooperative Aneurysm Study,” Journal of Neurosurgery, vol. 89, no. 3, pp. 405–411, 1998.
[23]
D. G. Caralis, U. Deligonul, M. J. Kern, and J. D. Cohen, “Smoking is a risk factor for coronary spasm in young women,” Circulation, vol. 85, no. 3, pp. 905–909, 1992.
[24]
M. Nobuyoshi, M. Abe, H. Nosaka et al., “Statistical analysis of clinical risk factors for coronary artery spasm: identification of the most important determinant,” American Heart Journal, vol. 124, no. 1, pp. 32–38, 1992.
[25]
M. Sugiishi and F. Takatsu, “Cigarette smoking is a major risk factor for coronary spasm,” Circulation, vol. 87, no. 1, pp. 76–79, 1993.
[26]
D. B. Seder, J. M. Schmidt, N. Badjatia et al., “Transdermal nicotine replacement therapy in cigarette smokers with acute subarachnoid hemorrhage,” Neurocritical Care, vol. 14, no. 1, pp. 77–83, 2011.
[27]
J. E. Conway and R. J. Tamargo, “Cocaine use is an independent risk factor for cerebral vasospasm after aneurysmal subarachnoid hemorrhage,” Stroke, vol. 32, no. 10, pp. 2338–2343, 2001.
[28]
T. Boco and R. L. Macdonald, “Absence of acute cerebral vasoconstriction after cocaine-associated subarachnoid hemorrhage,” Neurocritical Care, vol. 1, no. 4, pp. 449–454, 2004.
[29]
A. Alaraj, A. Wallace, N. Mander, V. Aletich, F. T. Charbel, and S. Amin-Hanjani, “Effect of acute cocaine use on vasospasm and outcome in aneurysmal subarachnoid hemorrhage,” World Neurosurgery, vol. 73, no. 4, pp. 357–360, 2010.
[30]
M. Mizukami, T. Takemae, T. Tazawa, T. Kawase, and T. Matsuzaki, “Value of computed tomography in the prediction of cerebral vasospasm after aneurysm rupture,” Neurosurgery, vol. 7, no. 6, pp. 583–586, 1980.
[31]
J. M. Davis, K. R. Davis, and R. M. Crowell, “Subarachnoid hemorrhage secondary to ruptured intracranial aneurysm: prognostic significance of cranial CT,” American Journal of Roentgenology, vol. 134, no. 4, pp. 711–715, 1980.
[32]
S. A. Dupont, E. F. M. Wijdicks, E. M. Manno, G. Lanzino, R. D. Brown Jr., and A. A. Rabinstein, “Timing of computed tomography and prediction of vasospasm after aneurysmal subarachnoid hemorrhage,” Neurocritical Care, vol. 11, no. 1, pp. 71–75, 2009.
[33]
C. G. Harrod, B. R. Bendok, and H. H. Batjer, “Prediction of cerebral vasospasm in patients presenting with aneurysmal subarachnoid hemorrhage: a review,” Neurosurgery, vol. 56, no. 4, pp. 633–652, 2005.
[34]
A. Hijdra, J. van Gijn, N. J. D. Nagelkerke, M. Vermeulen, and H. van Crevel, “Prediction of delayed cerebral ischemia, rebleeding, and outcome after aneurysmal subarachnoid hemorrhage,” Stroke, vol. 19, no. 10, pp. 1250–1256, 1988.
[35]
C. M. Fisher, J. P. Kistler, and J. M. Davis, “Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning,” Neurosurgery, vol. 6, no. 1, pp. 1–9, 1980.
[36]
J. P. Kistler, R. M. Crowell, K. R. Davis, et al., “The relation of cerebral vasospasm to the extent and location of subarachnoid blood visualized by CT scan: a prospective study,” Neurology, vol. 33, no. 4, pp. 424–436, 1983.
[37]
H. P. Adams Jr., N. F. Kassell, J. C. Torner, and E. C. Haley Jr., “Predicting cerebral ischemia after aneurysmal subarachnoid hemorrhage: influences of clinical condition, CT results, and antifibrinolytic therapy. A report of the cooperative aneurysm study,” Neurology, vol. 37, no. 10, pp. 1586–1591, 1987.
[38]
D. G. Grosset, I. McDonald, M. Cockburn, J. Straiton, and R. R. Bullock, “Prediction of delayed neurological deficit after subarachnoid haemorrhage: a CT blood load and Doppler velocity approach,” Neuroradiology, vol. 36, no. 6, pp. 418–421, 1994.
[39]
P. J. A. M. Brouwers, D. W. J. Dippel, M. Vermeulen, K. W. Lindsay, D. Hasan, and J. van Gijn, “Amount of blood on computed tomography as an independent predictor after aneurysm rupture,” Stroke, vol. 24, no. 6, pp. 809–814, 1993.
[40]
J. Claassen, G. L. Bernardini, K. Kreiter et al., “Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: the fisher scale revisited,” Stroke, vol. 32, no. 9, pp. 2012–2020, 2001.
[41]
R. L. Macdonald, A. Rosengart, D. Huo, and T. Karrison, “Factors associated with the development of vasospasm after planned surgical treatment of aneurysmal subarachnoid hemorrhage,” Journal of Neurosurgery, vol. 99, no. 4, pp. 644–652, 2003.
[42]
M. L. Smith, J. M. Abrahams, S. Chandela, M. J. Smith, R. W. Hurst, and P. D. Le Roux, “Subarachnoid hemorrhage on computed tomography scanning and the development of cerebral vasospasm: the Fisher grade revisited,” Surgical Neurology, vol. 63, no. 3, pp. 229–234, 2005.
[43]
J. A. Frontera, J. Claassen, J. M. Schmidt et al., “Prediction of symptomatic vasospasm after subarachnoid hemorrhage: the modified fisher scale,” Neurosurgery, vol. 59, no. 1, pp. 21–26, 2006.
[44]
S.-B. Ko, H. A. Choi, A. M. Carpenter et al., “Quantitative analysis of hemorrhage volume for predicting delayed cerebral ischemia after subarachnoid hemorrhage,” Stroke, vol. 42, no. 3, pp. 669–674, 2011.
[45]
P. Klimo Jr. and R. H. Schmidt, “Computed tomography grading schemes used to predict cerebral vasospasm after aneurysmal subarachnoid hemorrhage: a historical review,” Neurosurgical Focus, vol. 21, no. 3, pp. 1–8, 2006.
[46]
G. S. Allen, H. S. Ahn, T. J. Preziosi, et al., “Cerebral arterial spasm: a controlled trial of nimodipine in patients with subarachnoid hemorrhage,” The New England Journal of Medicine, vol. 308, no. 11, pp. 619–624, 1983.
[47]
A. G. W. van Norden, G. W. van Dijk, M. D. van Huizen, A. Algra, and G. J. E. Rinkel, “Interobserver agreement and predictive value for outcome of two rating scales for the amount of extravasated blood after aneurysmal subarachnoid haemorrhage,” Journal of Neurology, vol. 253, no. 9, pp. 1217–1220, 2006.
[48]
C. S. Ogilvy and B. S. Carter, “A proposed comprehensive grading system to predict outcome for surgical management of intracranial aneurysms,” Neurosurgery, vol. 42, no. 5, pp. 959–970, 1998.
[49]
G. M. Ibrahim, S. Weidauer, and R. L. Macdonald, “Interobserver variability in the interpretation of computed tomography following aneurysmal subarachnoid hemorrhage,” Journal of Neurosurgery, vol. 115, no. 6, pp. 1191–1196, 2011.
[50]
E. Svensson, J.-E. Starmark, S. Ekholm, C. von Essen, and A. Johansson, “Analysis of interobserver disagreement in the assessment of subarachnoid blood and acute hydrocephalus on CT scans,” Neurological Research, vol. 18, no. 6, pp. 487–494, 1996.
[51]
A. H. Kramer, M. Hehir, B. Nathan et al., “A comparison of 3 radiographic scales for the prediction of delayed ischemia and prognosis following subarachnoid hemorrhage,” Journal of Neurosurgery, vol. 109, no. 2, pp. 199–207, 2008.
[52]
S. A. Dupont, E. F. M. Wijdicks, E. M. Manno, G. Lanzino, and A. A. Rabinstein, “Prediction of angiographic vasospasm after aneurysmal subarachnoid hemorrhage: value of the hijdra sum scoring system,” Neurocritical Care, vol. 11, no. 2, pp. 172–176, 2009.
[53]
M. van der Jagt, D. Hasan, H. W. C. Bijvoet, H. Pieterman, P. J. Koudstaal, and C. J. J. Avezaat, “Interobserver variability of cisternal blood on CT after aneurysmal subarachnoid hemorrhage,” Neurology, vol. 54, no. 11, pp. 2156–2158, 2000.
[54]
D. S. Rosen and R. L. Macdonald, “Subarachnoid hemorrhage grading scales: a systematic review,” Neurocritical Care, vol. 2, no. 2, pp. 110–118, 2005.
[55]
A.-M. Leffers and A. Wagner, “Neurologic complications of cerebral angiography: a retrospective study of complication rate and patient risk factors,” Acta Radiologica, vol. 41, no. 3, pp. 204–210, 2000.
[56]
C. Lysakowski, B. Walder, M. C. Costanza, and M. R. Tramèr, “Transcranial Doppler versus angiography in patients with vasospasm due to a ruptured cerebral aneurysm: a systematic review,” Stroke, vol. 32, no. 10, pp. 2292–2298, 2001.
[57]
L. Mascia, L. Fedorko, K. terBrugge et al., “The accuracy of transcranial Doppler to detect vasospasm in patients with aneurysmal subarachnoid hemorrhage,” Intensive Care Medicine, vol. 29, no. 7, pp. 1088–1094, 2003.
[58]
G. B. Anderson, R. Ashforth, D. E. Steinke, and J. M. Findlay, “CT angiography for the detection of cerebral vasospasm in patients with acute subarachnoid hemorrhage,” American Journal of Neuroradiology, vol. 21, no. 6, pp. 1011–1015, 2000.
[59]
M. Pham, A. Johnson, A. J. Bartsch et al., “CT perfusion predicts secondary cerebral infarction after aneurysmal subarachnoid hemorrhage,” Neurology, vol. 69, no. 8, pp. 762–765, 2007.
[60]
S. Binaghi, M. L. Colleoni, P. Maeder et al., “CT angiography and perfusion CT in cerebral vasospasm after subarachnoid hemorrhage,” American Journal of Neuroradiology, vol. 28, no. 4, pp. 750–758, 2007.
[61]
E. D. Greenberg, R. Gold, M. Reichman et al., “Diagnostic accuracy of CT angiography and CT perfusion for cerebral vasospasm: a meta-analysis,” American Journal of Neuroradiology, vol. 31, no. 10, pp. 1853–1860, 2010.
[62]
R. D. Stevens, N. S. Naval, M. A. Mirski, G. Citerio, and P. J. Andrews, “Intensive care of aneurysmal subarachnoid hemorrhage: an international survey,” Intensive Care Medicine, vol. 35, no. 9, pp. 1556–1566, 2009.
[63]
L. Lennihan, S. A. Mayer, M. E. Fink et al., “Effect of hypervolemic therapy on cerebral blood flow after subarachnoid hemorrhage: a randomized controlled trial,” Stroke, vol. 31, no. 2, pp. 383–391, 2000.
[64]
A. Egge, K. Waterloo, H. Sj？holm, T. Solberg, T. Ingebrigtsen, and B. Romner, “Prophylactic hyperdynamic postoperative fluid therapy after aneurysmal subarachnoid hemorrhage: a clinical, prospective, randomized, controlled study,” Neurosurgery, vol. 49, no. 3, pp. 593–606, 2001.
[65]
S. Wolf, “Routine management of volume status after aneurysmal subarachnoid hemorrhage,” Neurocritical Care, vol. 15, no. 2, pp. 275–280, 2011.
[66]
N. F. Kassell, S. J. Peerless, Q. J. Durward, D. W. Beck, C. G. Drake, and H. P. Adams, “Treatment of ischemic deficits from vasospasm with intravascular volume expansion and induced arterial hypertension,” Neurosurgery, vol. 11, no. 3, pp. 337–343, 1982.
[67]
K. Mori, H. Arai, K. Nakajima, A. Tajima, and M. Maeda, “Hemorheological and hemodynamic analysis of hypervolemic hemodilution therapy for cerebral vasospasm after aneurysmal subarachnoid hemorrhage,” Stroke, vol. 26, no. 9, pp. 1620–1626, 1995.
[68]
M. M. Treggiari, B. Walder, P. M. Suter, and J.-A. Romand, “Systematic review of the prevention of delayed ischemic neurological deficits with hypertension, hypervolemia, and hemodilution therapy following subarachnoid hemorrhage,” Journal of Neurosurgery, vol. 98, no. 5, pp. 978–984, 2003.
[69]
A. Raabe, J. Beck, M. Keller, H. Vatter, M. Zimmermann, and V. Seifert, “Relative importance of hypertension compared with hypervolemia for increasing cerebral oxygenation in patients with cerebral vasospasm after subarachnoid hemorrhage,” Journal of Neurosurgery, vol. 103, no. 6, pp. 974–981, 2005.
[70]
H. Otsubo, T. Takemae, T. Inoue, S. Kobayashi, and K. Sugita, “Normovolaemic induced hypertension therapy for cerebral vasospasm after subarachnoid haemorrhage,” Acta Neurochirurgica, vol. 103, no. 1-2, pp. 18–26, 1990.
[71]
B. L. Hoh, B. S. Carter, and C. S. Ogilvy, “Risk of hemorrhage from unsecured, unruptured aneurysms during and after hypertensive hypervolemic therapy,” Neurosurgery, vol. 50, no. 6, pp. 1207–1212, 2002.
[72]
G. L. Bernardini, S. A. Mayer, S. B. Kossoff, L. Hacein-Bey, R. A. Solomon, and J. Pile-Spellman, “Anticoagulation and induced hypertension after endovascular treatment for ruptured intracranial aneurysms,” Critical Care Medicine, vol. 29, no. 3, pp. 641–644, 2001.
[73]
J. Platz, E. Güresir, H. Vatter et al., “Unsecured intracranial aneurysms and induced hypertension in cerebral vasospasm: is induced hypertension safe?” Neurocritical Care, vol. 14, no. 2, pp. 168–175, 2011.
[74]
A. Ekelund, P. Reinstrup, E. Ryding et al., “Effects of Iso- and hypervolemic hemodilution on regional cerebral blood flow and oxygen delivery for patients with vasospasm after aneurysmal subarachnoid hemorrhage,” Acta Neurochirurgica, vol. 144, no. 7, pp. 703–713, 2002.
[75]
S. C. Jost, M. N. Diringer, A. R. Zazulia et al., “Effect of normal saline bolus on cerebral blood flow in regions with low baseline flow in patients with vasospasm following subarachnoid hemorrhage,” Journal of Neurosurgery, vol. 103, no. 1, pp. 25–30, 2005.
[76]
M.-Y. Tseng, P. G. Al-Rawi, M. Czosnyka et al., “Enhancement of cerebral blood flow using systemic hypertonic saline therapy improves outcome in patients with poor-grade spontaneous subarachnoid hemorrhage,” Journal of Neurosurgery, vol. 107, no. 2, pp. 274–282, 2007.
[77]
M.-Y. Tseng, P. G. Al-Rawi, J. D. Pickard, F. A. Rasulo, and P. J. Kirkpatrick, “Effect of hypertonic saline on cerebral blood flow in poor-grade patients with subarachnoid hemorrhage,” Stroke, vol. 34, no. 6, pp. 1389–1396, 2003.
[78]
S. Tabuchi, N. Hirano, M. Tanabe et al., “Relationship of hypotension and cerebral vasospasm in patients with aneurysmal subarachnoid hemorrhage,” Neurological Research, vol. 28, no. 2, pp. 196–199, 2006.
[79]
R. P. Tummala, R. N. Sheth, and R. C. Heros, “Hemodilution and fluid management in neurosurgery,” Clinical Neurosurgery, vol. 53, pp. 238–251, 2006.
[80]
A. M. Naidech, J. Drescher, M. L. Ault, A. Shaibani, H. H. Batjer, and M. J. Alberts, “Higher hemoglobin is associated with less cerebral infarction, poor outcome, and death after subarachnoid hemorrhage,” Neurosurgery, vol. 59, no. 4, pp. 775–779, 2006.
[81]
A. M. Naidech, B. Jovanovic, K. E. Wartenberg et al., “Higher hemoglobin is associated with improved outcome after subarachnoid hemorrhage,” Critical Care Medicine, vol. 35, no. 10, pp. 2383–2389, 2007.
[82]
M. J. Smith, P. D. Le Roux, J. P. Elliott, and H. R. Winn, “Blood transfusion and increased risk for vasospasm and poor outcome after subarachnoid hemorrhage,” Journal of Neurosurgery, vol. 101, no. 1, pp. 1–7, 2004.
[83]
J. Levine, A. Kofke, L. Cen et al., “Red blood cell transfusion is associated with infection and extracerebral complications after subarachnoid hemorrhage,” Neurosurgery, vol. 66, no. 2, pp. 312–318, 2010.
[84]
A. M. Naidech, A. Shaibani, R. K. Garg et al., “Prospective, randomized trial of higher goal hemoglobin after subarachnoid hemorrhage,” Neurocritical Care, vol. 13, no. 3, pp. 313–320, 2010.
[85]
P. Chittiboina, B. Guthikonda, C. Wollblad, and S. A. Conrad, “A computational simulation of the effect of hemodilution on oxygen transport in middle cerebral artery vasospasm,” Journal of Cerebral Blood Flow and Metabolism, vol. 31, no. 11, pp. 2209–2217, 2011.
[86]
J. S. Robinson, M. S. Walid, S. Hyun, R. O'Connell, C. Menard, and B. Bohleber, “Computational modeling of HHH therapy and impact of blood pressure and hematocrit,” World Neurosurgery, vol. 74, no. 2-3, pp. 294–296, 2010.
[87]
E. S. Connolly, A. A. Rabinstein, J. R. Carhuapoma et al., “Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American heart association/american stroke association,” Stroke, vol. 43, no. 6, pp. 1711–1737, 2012.
[88]
I. Yamakami, K. Isobe, and A. Yamaura, “Effects of intravascular volume expansion on cerebral blood flow in patients with ruptured cerebral aneurysms,” Neurosurgery, vol. 21, no. 3, pp. 303–309, 1987.
[89]
J. I. Suarez, L. Shannon, O. O. Zaida et al., “Effect of human albumin administration on clinical outcome and hospital cost in patients with subarachnoid hemorrhage,” Journal of Neurosurgery, vol. 100, no. 4, pp. 585–590, 2004.
[90]
V. L. Feigin, G. J. E. Rinkel, A. Algra, M. Vermeulen, and J. van Gijn, “Calcium antagonists in patients with aneurysmal subarachnoid hemorrhage: a systematic review,” Neurology, vol. 50, no. 4, pp. 876–883, 1998.
[91]
G. Neil-Dwyer, E. Mee, D. Dorrance, and D. Lowe, “Early intervention with nimodipine in subarachnoid haemorrhage,” European Heart Journal, vol. 8, pp. 41–47, 1987.
[92]
K. C. Petruk, M. West, G. Mohr et al., “Nimodipine treatment in poor-grade aneurysm patients. Results of a multicenter double-blind placebo-controlled trial,” Journal of Neurosurgery, vol. 68, no. 4, pp. 505–517, 1988.
[93]
J. Philippon, R. Grob, F. Dagreou, M. Guggiari, M. Rivierez, and P. Viars, “Prevention of vasospasm in subarachnoid haemorrhage. A controlled study with nimodipine,” Acta Neurochirurgica, vol. 82, no. 3-4, pp. 110–114, 1986.
[94]
J. D. Pickard, G. D. Murray, R. Illingworth et al., “Effect of oral nimodipine on cerebral infarction and outcome after subarachnoid haemorrhage: British aneurysm nimodipine trial,” British Medical Journal, vol. 298, no. 6674, pp. 636–642, 1989.
[95]
S. M. Dorhout Mees, G. J. E. Rinkel, V. L. Feigin et al., “Calcium antagonists for aneurysmal subarachnoid haemorrhage,” Cochrane Database of Systematic Reviews, no. 3, Article ID CD000277, 2007.
[96]
M. K. Athar and J. M. Levine, “Treatment options for cerebral vasospasm in aneurysmal subarachnoid hemorrhage,” Neurotherapeutics, vol. 9, no. 1, pp. 37–43, 2012.
[97]
J. B. Bederson, E. S. Connolly Jr., H. H. Batjer 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, vol. 40, no. 3, pp. 994–1025, 2009.
[98]
M. N. Diringer, T. P. Bleck, J. C. Hemphill III et al., “Critical care management of patients following aneurysmal subarachnoid hemorrhage: recommendations from the Neurocritical Care Society's Multidisciplinary Consensus Conference,” Neurocritical Care, vol. 15, no. 2, pp. 211–240, 2011.
[99]
G. J. Velat, M. M. Kimball, J. D. Mocco, and B. L. Hoh, “Vasospasm after aneurysmal subarachnoid hemorrhage: review of randomized controlled trials and meta-analyses in the literature,” World Neurosurgery, vol. 76, no. 5, pp. 446–454, 2011.
[100]
A. Y. Zubkov and A. A. Rabinstein, “Medical management of cerebral vasospasm: present and future,” Neurological Research, vol. 31, no. 6, pp. 626–631, 2009.
[101]
J. K. Liao and U. Laufs, “Pleiotropic effects of statins,” Annual Review of Pharmacology and Toxicology, vol. 45, pp. 89–118, 2005.
[102]
U. Laufs, V. la Fata, and J. K. Liao, “Inhibition of 3-hydroxy-3-methylglutaryl (HMG)-CoA reductase blocks hypoxia-mediated down-regulation of endothelial nitric oxide synthase,” Journal of Biological Chemistry, vol. 272, no. 50, pp. 31725–31729, 1997.
[103]
G. O'Driscoll, D. Green, and R. R. Taylor, “Simvastatin, an HMG-coenzyme A reductase inhibitor, improves endothelial function within 1 month,” Circulation, vol. 95, no. 5, pp. 1126–1131, 1997.
[104]
M. J. McGirt, J. R. Lynch, A. Parra et al., “Simvastatin increases endothelial nitric oxide synthase and ameliorates cerebral vasospasm resulting from subarachnoid hemorrhage,” Stroke, vol. 33, no. 12, pp. 2950–2956, 2002.
[105]
S. H.-Y. Chou, E. E. Smith, N. Badjatia et al., “A randomized, double-blind, placebo-controlled pilot study of simvastatin in aneurysmal subarachnoid hemorrhage,” Stroke, vol. 39, no. 10, pp. 2891–2893, 2008.
[106]
J. R. Lynch, H. Wang, M. J. McGirt et al., “Simvastatin reduces vasospasm after aneurysmal subarachnoid hemorrhage: results of a pilot randomized clinical trial,” Stroke, vol. 36, no. 9, pp. 2024–2026, 2005.
[107]
M.-Y. Tseng, M. Czosnyka, H. Richards, J. D. Pickard, and P. J. Kirkpatrick, “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, vol. 36, no. 8, pp. 1627–1632, 2005.
[108]
M. D. I. Vergouwen, J. C. Meijers, R. B. Geskus et al., “Biologic effects of simvastatin in patients with aneurysmal subarachnoid hemorrhage: a double-blind, placebo-controlled randomized trial,” Journal of Cerebral Blood Flow and Metabolism, vol. 29, no. 8, pp. 1444–1453, 2009.
[109]
M. Kern, M. M. F. Lam, N. W. Knuckey, and C. R. P. Lind, “Statins may not protect against vasospasm in subarachnoid haemorrhage,” Journal of Clinical Neuroscience, vol. 16, no. 4, pp. 527–530, 2009.
[110]
T. Kerz, A. Victor, C. Beyer, I. Trapp, F. Heid, and R. Reisch, “A case control study of statin and magnesium administration in patients after aneurysmal subarachnoid hemorrhage: incidence of delayed cerebral ischemia and mortality,” Neurological Research, vol. 30, no. 9, pp. 893–897, 2008.
[111]
A. H. Kramer, M. J. Gurka, B. Nathan, A. S. Dumont, N. F. Kassell, and T. P. Bleck, “Statin use was not associated with less vasospasm or improved outcome after subarachnoid hemorrhage,” Neurosurgery, vol. 62, no. 2, pp. 422–427, 2008.
[112]
M. J. McGirt, G. L. Garces Ambrossi, J. Huang, and R. J. Tamargo, “Simvastatin for the prevention of symptomatic cerebral vasospasm following aneurysmal subarachnoid hemorrhage: a single-institution prospective cohort study: clinical article,” Journal of Neurosurgery, vol. 110, no. 5, pp. 968–974, 2009.
[113]
S. I. Moskowitz, C. Ahrens, J. J. Provencio, M. Chow, and P. A. Rasmussen, “Prehemorrhage statin use and the risk of vasospasm after aneurysmal subarachnoid hemorrhage,” Surgical Neurology, vol. 71, no. 3, pp. 311–317, 2009.
[114]
A. B. Singhal, M. A. Topcuoglu, D. J. Dorer, C. S. Ogilvy, B. S. Carter, and W. J. Koroshetz, “SSRI and statin use increases the risk for vasospasm after subarachnoid hemorrhage,” Neurology, vol. 64, no. 6, pp. 1008–1013, 2005.
[115]
V. A. H. Sillberg, G. A. Wells, and J. J. Perry, “Do statins improve outcomes and reduce the incidence of vasospasm after aneurysmal subarachnoid hemorrhage: a meta-analysis,” Stroke, vol. 39, no. 9, pp. 2622–2626, 2008.
[116]
A. H. Kramer and J. J. Fletcher, “Statins in the management of patients with aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis,” Neurocritical Care, vol. 12, no. 2, pp. 285–296, 2010.
[117]
M. D. I. Vergouwen, R. J. de Haan, M. Vermeulen, and Y. B. W. E. M. Roos, “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, vol. 41, no. 1, pp. e47–e52, 2010.
[118]
R. M. McLean, “Magnesium and its therapeutic uses: a review,” The American Journal of Medicine, vol. 96, no. 1, pp. 63–76, 1994.
[119]
K. W. Muir, “Magnesium for neuroprotection in ischaemic stroke: rationale for use and evidence of effectiveness,” CNS Drugs, vol. 15, no. 12, pp. 921–930, 2001.
[120]
G. J. Pyne, T. A. D. Cadoux-Hudson, and J. F. Clark, “Magnesium protection against in vitro cerebral vasospasm after subarachnoid haemorrhage,” British Journal of Neurosurgery, vol. 15, no. 5, pp. 409–415, 2001.
[121]
D. W. Choi and S. M. Rothman, “The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death,” Annual Review of Neuroscience, vol. 13, pp. 171–182, 1990.
[122]
J. W. Johnson and P. Ascher, “Voltage-dependent block by intracellular Mg2+ of N-methyl-D-aspartate-activated channels,” Biophysical Journal, vol. 57, no. 5, pp. 1085–1090, 1990.
[123]
R. Boet and E. Mee, “Magnesium sulfate in the management of patients with fisher grade 3 subarachnoid hemorrhage: a pilot study,” Neurosurgery, vol. 47, no. 3, pp. 602–607, 2000.
[124]
R. Y. Chia, R. S. Hughes, and M. K. Morgan, “Magnesium: a useful adjunct in the prevention of cerebral vasospasm following aneurysmal subarachnoid haemorrhage,” Journal of Clinical Neuroscience, vol. 9, no. 3, pp. 279–281, 2002.
[125]
C. Muroi, A. Terzic, M. Fortunati, Y. Yonekawa, and E. Keller, “Magnesium sulfate in the management of patients with aneurysmal subarachnoid hemorrhage: a randomized, placebo-controlled, dose-adapted trial,” Surgical Neurology, vol. 69, no. 1, pp. 33–39, 2008.
[126]
R. Schmid-Elsaesser, M. Kunz, S. Zausinger, S. Prueckner, J. Briegel, and H.-J. Steiger, “Intravenous magnesium versus nimodipine in the treatment of patients with aneurysmal subarachnoid hemorrhage: a randomized study,” Neurosurgery, vol. 58, no. 6, pp. 1054–1064, 2006.
[127]
W. M. van den Bergh, K. W. Albrecht, J. W. Berkelbach van der Sprenkel, and G. J. E. Rinkel, “Magnesium therapy after aneurysmal subarachnoid haemorrhage a dose-finding study for long term treatment,” Acta Neurochirurgica, vol. 145, no. 3, pp. 195–199, 2003.
[128]
W. M. van den Bergh, “Magnesium sulfate in aneurysmal subarachnoid hemorrhage: a randomized controlled trial,” Stroke, vol. 36, no. 5, pp. 1011–1015, 2005.
[129]
R. S. Veyna, D. Seyfried, D. G. Burke et al., “Magnesium sulfate therapy after aneurysmal subarachnoid hemorrhage,” Journal of Neurosurgery, vol. 96, no. 3, pp. 510–514, 2002.
[130]
G. K. C. Wong, M. T. V. Chan, R. Boet, W. S. Poon, and T. Gin, “Intravenous magnesium sulfate after aneurysmal subarachnoid hemorrhage: a prospective randomized pilot study,” Journal of Neurosurgical Anesthesiology, vol. 18, no. 2, pp. 142–148, 2006.
[131]
G. K. C. Wong, W. S. Poon, M. T. V. Chan et al., “Intravenous magnesium sulphate for aneurysmal subarachnoid hemorrhage (IMASH): a randomized, double-blinded, placebo-controlled, multicenter phase III trial,” Stroke, vol. 41, no. 5, pp. 921–926, 2010.
[132]
T. Westermaier, C. Stetter, G. H. Vince et al., “Prophylactic intravenous magnesium sulfate for treatment of aneurysmal subarachnoid hemorrhage: a randomized, placebo-controlled, clinical study,” Critical Care Medicine, vol. 38, no. 5, pp. 1284–1290, 2010.
[133]
M. Yanagisawa, H. Kurihara, S. Kimura et al., “A novel potent vasoconstrictor peptide produced by vascular endothelial cells,” Nature, vol. 332, no. 6163, pp. 411–415, 1988.
[134]
H. Kobayashi, M. Hayashi, S. Kobayashi, M. Kabuto, Y. Handa, and H. Kawano, “Effect of endothelin on the canine basilar artery,” Neurosurgery, vol. 27, no. 3, pp. 357–361, 1990.
[135]
S. M. Papadopoulos, L. L. Gilbert, R. C. Webb, and C. J. D'Amato, “Characterization of contractile responses to endothelin in human cerebral arteries: implications for cerebral vasospasm,” Neurosurgery, vol. 26, no. 5, pp. 810–815, 1990.
[136]
R. Suzuki, H. Masaoka, Y. Hirata, F. Marumo, E. Isotani, and K. Hirakawa, “The role of endothelin-1 in the origin of cerebral vasospasm in patients with aneurysmal subarachnoid hemorrhage,” Journal of Neurosurgery, vol. 77, no. 1, pp. 96–100, 1992.
[137]
R. L. MacDonald, N. F. Kassell, S. Mayer 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, vol. 39, no. 11, pp. 3015–3021, 2008.
[138]
R. L. Macdonald, R. T. Higashida, E. Keller et al., “Randomized trial of clazosentan in patients with aneurysmal subarachnoid hemorrhage undergoing endovascular coiling,” Stroke, vol. 43, no. 6, pp. 1463–1469, 2012.
[139]
R. L. Macdonald, R. M. Pluta, and J. H. Zhang, “Cerebral vasospasm after subarachnoid hemorrhage: the emerging revolution,” Nature Clinical Practice Neurology, vol. 3, no. 5, pp. 256–263, 2007.
