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Neurology Research International
Volume 2013, Article ID 373458, 13 pages
http://dx.doi.org/10.1155/2013/373458
Review Article

Current Controversies in the Prediction, Diagnosis, and Management of Cerebral Vasospasm: Where Do We Stand?

1Vanderbilt University School of Medicine, 1211 Medical Center Drive, Nashville, TN 37232, USA
2Department of Neurological Surgery, Vanderbilt University School of Medicine, 1211 Medical Center Drive, Nashville, TN 37232, USA

Received 7 November 2012; Revised 2 September 2013; Accepted 4 September 2013

Academic Editor: Changiz Geula

Copyright © 2013 Young Lee et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked 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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  17. M. Ryttlefors, P. Enblad, E. Ronne-Engström, L. Persson, D. Ilodigwe, and R. L. Macdonald, “Patient age and vasospasm after subarachnoid hemorrhage,” Neurosurgery, vol. 67, no. 4, pp. 911–917, 2010. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  19. B. A. Bell and L. Symon, “Smoking and subarachnoid haemorrhage,” British Medical Journal, vol. 1, no. 6163, pp. 577–578, 1979. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  64. A. Egge, K. Waterloo, H. Sjøholm, 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. View at Google Scholar · View at Scopus
  65. S. Wolf, “Routine management of volume status after aneurysmal subarachnoid hemorrhage,” Neurocritical Care, vol. 15, no. 2, pp. 275–280, 2011. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  101. J. K. Liao and U. Laufs, “Pleiotropic effects of statins,” Annual Review of Pharmacology and Toxicology, vol. 45, pp. 89–118, 2005. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  118. R. M. McLean, “Magnesium and its therapeutic uses: a review,” The American Journal of Medicine, vol. 96, no. 1, pp. 63–76, 1994. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus