Neurocritical Care

, 15:211 | Cite as

Critical Care Management of Patients Following Aneurysmal Subarachnoid Hemorrhage: Recommendations from the Neurocritical Care Society’s Multidisciplinary Consensus Conference

  • Michael N. Diringer
  • Thomas P. Bleck
  • J. Claude HemphillIII
  • David Menon
  • Lori Shutter
  • Paul Vespa
  • Nicolas Bruder
  • E. Sander ConnollyJr.
  • Giuseppe Citerio
  • Daryl Gress
  • Daniel Hänggi
  • Brian L. Hoh
  • Giuseppe Lanzino
  • Peter Le Roux
  • Alejandro Rabinstein
  • Erich Schmutzhard
  • Nino Stocchetti
  • Jose I. Suarez
  • Miriam Treggiari
  • Ming-Yuan Tseng
  • Mervyn D. I. Vergouwen
  • Stefan Wolf
  • Gregory Zipfel
Review

Abstract

Subarachnoid hemorrhage (SAH) is an acute cerebrovascular event which can have devastating effects on the central nervous system as well as a profound impact on several other organs. SAH patients are routinely admitted to an intensive care unit and are cared for by a multidisciplinary team. A lack of high quality data has led to numerous approaches to management and limited guidance on choosing among them. Existing guidelines emphasize risk factors, prevention, natural history, and prevention of rebleeding, but provide limited discussion of the complex critical care issues involved in the care of SAH patients. The Neurocritical Care Society organized an international, multidisciplinary consensus conference on the critical care management of SAH to address this need. Experts from neurocritical care, neurosurgery, neurology, interventional neuroradiology, and neuroanesthesiology from Europe and North America were recruited based on their publications and expertise. A jury of four experienced neurointensivists was selected for their experience in clinical investigations and development of practice guidelines. Recommendations were developed based on literature review using the GRADE system, discussion integrating the literature with the collective experience of the participants and critical review by an impartial jury. Recommendations were developed using the GRADE system. Emphasis was placed on the principle that recommendations should be based not only on the quality of the data but also tradeoffs and translation into practice. Strong consideration was given to providing guidance and recommendations for all issues faced in the daily management of SAH patients, even in the absence of high quality data.

Keywords

Subarachnoid hemorrhage Critical care Aneurysm Vasospasm Anticonvulsants Hyponatremia Endovascular Fever 

Notes

Acknowledgments

Sponsored by the Neurocritical Care Society with the assistance of an unrestricted grant from Actelion Pharmaceuticals who had no involvement in any aspects of the conference including selection of topics, participants, or development and production of the proceedings.

References

  1. 1.
    Dorhout Mees SM, Rinkel GJ, Feigin VL, et al. Calcium antagonists for aneurysmal subarachnoid haemorrhage. Cochrane Database Syst Rev. 2007:CD000277.Google Scholar
  2. 2.
    Atkins D, Best D, Briss PA, et al. Grading quality of evidence and strength of recommendations. BMJ. 2004;328:1490.PubMedCrossRefGoogle Scholar
  3. 3.
    Fujii Y, Takeuchi S, Sasaki O, Minakawa T, Koike T, Tanaka R. Ultra-early rebleeding in spontaneous subarachnoid hemorrhage. J Neurosurg. 1996;84:35–42.Google Scholar
  4. 4.
    Molyneux AJ, Kerr RS, Yu LM, et al. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet. 2005;366:809–17.PubMedCrossRefGoogle Scholar
  5. 5.
    Roos YB, Rinkel GJ, Vermeulen M, Algra A, van Gijn J. Antifibrinolytic therapy for aneurysmal subarachnoid haemorrhage. Cochrane Database Syst Rev. 2003:CD001245.Google Scholar
  6. 6.
    Hillman J, Fridriksson S, Nilsson O, Yu Z, Saveland H, Jakobsson KE. Immediate administration of tranexamic acid and reduced incidence of early rebleeding after aneurysmal subarachnoid hemorrhage: a prospective randomized study. J Neurosurg. 2002;97:771–8.PubMedCrossRefGoogle Scholar
  7. 7.
    Harrigan MR, Rajneesh KF, Ardelt AA, Fisher WS 3rd. Short-term antifibrinolytic therapy before early aneurysm treatment in subarachnoid hemorrhage: effects on rehemorrhage, cerebral ischemia, and hydrocephalus. Neurosurgery. 2010;67:935–9.PubMedCrossRefGoogle Scholar
  8. 8.
    Starke RM, Kim GH, Fernandez A, et al. Impact of a protocol for acute antifibrinolytic therapy on aneurysm rebleeding after subarachnoid hemorrhage. Stroke. 2008;39:2617–21.PubMedCrossRefGoogle Scholar
  9. 9.
    Tanno Y, Homma M, Oinuma M, Kodama N, Ymamoto T. Rebleeding from ruptured intracranial aneurysms in North Eastern Province of Japan. A cooperative study. J Neurol Sci. 2007;258:11–6.PubMedCrossRefGoogle Scholar
  10. 10.
    Kusumi M, Yamada M, Kitahara T, et al. Rerupture of cerebral aneurysms during angiography–a retrospective study of 13 patients with subarachnoid hemorrhage. Acta Neurochir (Wien). 2005;147:831–7.CrossRefGoogle Scholar
  11. 11.
    Saitoh H, Hayakawa K, Nishimura K, et al. Rerupture of cerebral aneurysms during angiography. AJNR Am J Neuroradiol. 1995;16:539–42.PubMedGoogle Scholar
  12. 12.
    Inagawa T. Ultra-early rebleeding within six hours after aneurysmal rupture. Surg Neurol. 1994;42:130–4.PubMedCrossRefGoogle Scholar
  13. 13.
    Komiyama M, Tamura K, Nagata Y, Fu Y, Yagura H, Yasui T. Aneurysmal rupture during angiography. Neurosurgery. 1993;33:798–803.PubMedCrossRefGoogle Scholar
  14. 14.
    Hashiguchi A, Mimata C, Ichimura H, Morioka M, Kuratsu J. Rebleeding of ruptured cerebral aneurysms during three-dimensional computed tomographic angiography: report of two cases and literature review. Neurosurg Rev. 2007;30:151–4.PubMedCrossRefGoogle Scholar
  15. 15.
    Nakatsuka M, Mizuno S, Uchida A. Extravasation on three-dimensional CT angiography in patients with acute subarachnoid hemorrhage and ruptured aneurysm. Neuroradiology. 2002;44:25–30.PubMedCrossRefGoogle Scholar
  16. 16.
    Choi KS, Chun HJ, Yi HJ, Ko Y, Kim YS, Kim JM. Seizures and epilepsy following aneurysmal subarachnoid hemorrhage: incidence and risk factors. J Korean Neurosurg Soc. 2009;46:93–8.PubMedCrossRefGoogle Scholar
  17. 17.
    Rhoney DH, Tipps LB, Murry KR, Basham MC, Michael DB, Coplin WM. Anticonvulsant prophylaxis and timing of seizures after aneurysmal subarachnoid hemorrhage. Neurology. 2000;55:258–65.PubMedGoogle Scholar
  18. 18.
    Claassen J, Peery S, Kreiter KT, et al. Predictors and clinical impact of epilepsy after subarachnoid hemorrhage. Neurology. 2003;60:208–14.PubMedGoogle Scholar
  19. 19.
    Naidech AM, Kreiter KT, Janjua N, et al. Phenytoin exposure is associated with functional and cognitive disability after subarachnoid hemorrhage. Stroke. 2005;36:583–7.PubMedCrossRefGoogle Scholar
  20. 20.
    Rosengart AJ, Huo JD, Tolentino J, et al. Outcome in patients with subarachnoid hemorrhage treated with antiepileptic drugs. J Neurosurg. 2007;107:253–60.PubMedCrossRefGoogle Scholar
  21. 21.
    Chumnanvej S, Dunn IF, Kim DH. Three-day phenytoin prophylaxis is adequate after subarachnoid hemorrhage. Neurosurgery. 2007;60:99–102.PubMedCrossRefGoogle Scholar
  22. 22.
    Little AS, Kerrigan JF, McDougall CG, et al. Nonconvulsive status epilepticus in patients suffering spontaneous subarachnoid hemorrhage. J Neurosurg. 2007;106:805–11.PubMedCrossRefGoogle Scholar
  23. 23.
    Claassen J, Hirsch LJ, Frontera JA, et al. Prognostic significance of continuous EEG monitoring in patients with poor-grade subarachnoid hemorrhage. Neurocrit Care. 2006;4:103–12.PubMedCrossRefGoogle Scholar
  24. 24.
    Dennis LJ, Claassen J, Hirsch LJ, Emerson RG, Connolly ES, Mayer SA. Nonconvulsive status epilepticus after subarachnoid hemorrhage. Neurosurgery. 2002;51:1136–43.PubMedCrossRefGoogle Scholar
  25. 25.
    Hravnak M, Frangiskakis JM, Crago EA, et al. Elevated cardiac troponin I and relationship to persistence of electrocardiographic and echocardiographic abnormalities after aneurysmal subarachnoid hemorrhage. Stroke. 2009;40:3478–84.PubMedCrossRefGoogle Scholar
  26. 26.
    Deibert E, Barzilai B, Braverman AC, et al. Clinical significance of elevated troponin I levels in patients with nontraumatic subarachnoid hemorrhage. J Neurosurg. 2003;98:741–6.PubMedCrossRefGoogle Scholar
  27. 27.
    Wartenberg KE, Schmidt JM, Claassen J, et al. Impact of medical complications on outcome after subarachnoid hemorrhage. Crit Care Med. 2006;34:617–23.PubMedCrossRefGoogle Scholar
  28. 28.
    Banki N, Kopelnik A, Tung P, et al. Prospective analysis of prevalence, distribution, and rate of recovery of left ventricular systolic dysfunction in patients with subarachnoid hemorrhage. J Neurosurg. 2006;105:15–20.PubMedCrossRefGoogle Scholar
  29. 29.
    Lee VH, Oh JK, Mulvagh SL, Wijdicks EF. Mechanisms in neurogenic stress cardiomyopathy after aneurysmal subarachnoid hemorrhage. Neurocrit Care. 2006;5:243–9.PubMedCrossRefGoogle Scholar
  30. 30.
    Coghlan LA, Hindman BJ, Bayman EO, et al. Independent associations between electrocardiographic abnormalities and outcomes in patients with aneurysmal subarachnoid hemorrhage: findings from the intraoperative hypothermia aneurysm surgery trial. Stroke. 2009;40:412–8.PubMedCrossRefGoogle Scholar
  31. 31.
    Friedman JA, Pichelmann MA, Piepgras DG, et al. Pulmonary complications of aneurysmal subarachnoid hemorrhage. Neurosurgery. 2003;52:1025–31.PubMedCrossRefGoogle Scholar
  32. 32.
    Solenski NJ, Haley EC Jr, Kassell NF, et al. Medical complications of aneurysmal subarachnoid hemorrhage: a report of the multicenter, cooperative aneurysm study. Participants of the Multicenter Cooperative Aneurysm Study. Crit Care Med. 1995;23:1007–17.PubMedCrossRefGoogle Scholar
  33. 33.
    Vespa PM, Bleck TP. Neurogenic pulmonary edema and other mechanisms of impaired oxygenation after aneurysmal subarachnoid hemorrhage. Neurocrit Care. 2004;1:157–70.PubMedCrossRefGoogle Scholar
  34. 34.
    Muroi C, Keller M, Pangalu A, Fortunati M, Yonekawa Y, Keller E. Neurogenic pulmonary edema in patients with subarachnoid hemorrhage. J Neurosurg Anesthesiol. 2008;20:188–92.PubMedCrossRefGoogle Scholar
  35. 35.
    Kahn JM, Caldwell EC, Deem S, Newell DW, Heckbert SR, Rubenfeld GD. Acute lung injury in patients with subarachnoid hemorrhage: incidence, risk factors, and outcome. Crit Care Med. 2006;34:196–202.PubMedCrossRefGoogle Scholar
  36. 36.
    Sheikhazadi A, Gharehdaghi J. Survey of sudden death from aneurysmal subarachnoid hemorrhage in cadavers referred to Legal Medicine Organization of Tehran, 2001–2005. Am J Forensic Med Pathol. 2009;30:358–61.PubMedCrossRefGoogle Scholar
  37. 37.
    Hasan D, Wijdicks EF, Vermeulen M. Hyponatremia is associated with cerebral ischemia in patients with aneurysmal subarachnoid hemorrhage. Ann Neurol. 1990;27:106–8.PubMedCrossRefGoogle Scholar
  38. 38.
    Wijdicks EF, Vermeulen M, Hijdra A, van Gijn J. Hyponatremia and cerebral infarction in patients with ruptured intracranial aneurysms: is fluid restriction harmful? Ann Neurol. 1985;17:137–40.PubMedCrossRefGoogle Scholar
  39. 39.
    Wijdicks EF, Vermeulen M, ten Haaf JA, Hijdra A, Bakker WH, van Gijn J. Volume depletion and natriuresis in patients with a ruptured intracranial aneurysm. Ann Neurol. 1985;18:211–6.PubMedCrossRefGoogle Scholar
  40. 40.
    Diringer MN, Wu KC, Verbalis JG, Hanley DF. Hypervolemic therapy prevents volume contraction but not hyponatremia following subarachnoid hemorrhage. Ann Neurol. 1992;31:543–50.PubMedCrossRefGoogle Scholar
  41. 41.
    Hoff RG, van Dijk GW, Algra A, Kalkman CJ, Rinkel GJ. Fluid balance and blood volume measurement after aneurysmal subarachnoid hemorrhage. Neurocrit Care. 2008;8:391–7.PubMedCrossRefGoogle Scholar
  42. 42.
    Hoff RG, Rinkel GJ, Verweij BH, Algra A, Kalkman CJ. Nurses’ prediction of volume status after aneurysmal subarachnoid haemorrhage: a prospective cohort study. Crit Care. 2008;12:R153.PubMedCrossRefGoogle Scholar
  43. 43.
    Hoff R, Rinkel G, Verweij B, Algra A, Kalkman C. Blood volume measurement to guide fluid therapy after aneurysmal subarachnoid hemorrhage: a prospective controlled study. Stroke. 2009;40:2575–7.PubMedCrossRefGoogle Scholar
  44. 44.
    Hoff RG, Rinkel GJ, Verweij BH, Algra A, Kalkman CJ. Pulmonary edema and blood volume after aneurysmal subarachnoid hemorrhage: a prospective observational study. Crit Care. 2010;14:R43.PubMedCrossRefGoogle Scholar
  45. 45.
    Mutoh T, Ishikawa T, Nishino K, Yasui N. Evaluation of the FloTrac uncalibrated continuous cardiac output system for perioperative hemodynamic monitoring after subarachnoid hemorrhage. J Neurosurg Anesthesiol. 2009;21:218–25.PubMedCrossRefGoogle Scholar
  46. 46.
    Moretti R, Pizzi B. Inferior vena cava distensibility as a predictor of fluid responsiveness in patients with subarachnoid hemorrhage. Neurocrit Care. 2010;13:3–9.PubMedCrossRefGoogle Scholar
  47. 47.
    Levy ML, Rabb CH, Zelman V, Giannotta SL. Cardiac performance enhancement from dobutamine in patients refractory to hypervolemic therapy for cerebral vasospasm. J Neurosurg. 1993;79:494–9.PubMedCrossRefGoogle Scholar
  48. 48.
    Mutoh T, Kazumata K, Ishikawa T, Terasaka S. Performance of bedside transpulmonary thermodilution monitoring for goal-directed hemodynamic management after subarachnoid hemorrhage. Stroke. 2009;40:2368–74.PubMedCrossRefGoogle Scholar
  49. 49.
    Lennihan L, Mayer SA, Fink ME, et al. Effect of hypervolemic therapy on cerebral blood flow after subarachnoid hemorrhage: a randomized controlled trial. Stroke. 2000;31:383–91.PubMedCrossRefGoogle Scholar
  50. 50.
    Rosenwasser RH, Jallo JI, Getch CC, Liebman KE. Complications of Swan-Ganz catheterization for hemodynamic monitoring in patients with subarachnoid hemorrhage. Neurosurgery. 1995;37:872–5.PubMedCrossRefGoogle Scholar
  51. 51.
    Hasan D, Vermeulen M, Wijdicks EF, Hijdra A, van Gijn J. Effect of fluid intake and antihypertensive treatment on cerebral ischemia after subarachnoid hemorrhage. Stroke. 1989;20:1511–5.PubMedCrossRefGoogle Scholar
  52. 52.
    Solomon RA, Post KD, McMurtry JG 3rd. Depression of circulating blood volume in patients after subarachnoid hemorrhage: implications for the management of symptomatic vasospasm. Neurosurgery. 1984;15:354–61.PubMedCrossRefGoogle Scholar
  53. 53.
    Kassell NF, Peerless SJ, Durward QJ, Beck DW, Drake CG, Adams HP. Treatment of ischemic deficits from vasospasm with intravascular volume expansion and induced arterial hypertension. Neurosurgery. 1982;11:337–43.PubMedCrossRefGoogle Scholar
  54. 54.
    Lennihan L, Mayer SA, Fink ME, et al. Effect of hypervolemic therapy on cerebral blood flow after subarachnoid hemorrhage: a randomized controlled trial. Stroke. 2000;31:383–91.PubMedCrossRefGoogle Scholar
  55. 55.
    Egge A, Waterloo K, Sjoholm H, Solberg T, Ingebrigtsen T, Romner B. Prophylactic hyperdynamic postoperative fluid therapy after aneurysmal subarachnoid hemorrhage: a clinical, prospective, randomized, controlled study. Neurosurgery. 2001;49:593–605.PubMedGoogle Scholar
  56. 56.
    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.PubMedCrossRefGoogle Scholar
  57. 57.
    Mutoh T, Ishikawa T, Suzuki A, Yasui N. Continuous cardiac output and near-infrared spectroscopy monitoring to assist in management of symptomatic cerebral vasospasm after subarachnoid hemorrhage. Neurocrit Care. 2010;13:331–8.PubMedCrossRefGoogle Scholar
  58. 58.
    Hasan D, Lindsay KW, Wijdicks EF, et al. Effect of fludrocortisone acetate in patients with subarachnoid hemorrhage. Stroke. 1989;20:1156–61.PubMedCrossRefGoogle Scholar
  59. 59.
    Mori T, Katayama Y, Kawamata T, Hirayama T. Improved efficiency of hypervolemic therapy with inhibition of natriuresis by fludrocortisone in patients with aneurysmal subarachnoid hemorrhage. J Neurosurg. 1999;91:947–52.PubMedCrossRefGoogle Scholar
  60. 60.
    Woo MH, Kale-Pradhan PB. Fludrocortisone in the treatment of subarachnoid hemorrhage-induced hyponatremia. Ann Pharmacother. 1997;31:637–9.PubMedGoogle Scholar
  61. 61.
    Moro N, Katayama Y, Kojima J, Mori T, Kawamata T. Prophylactic management of excessive natriuresis with hydrocortisone for efficient hypervolemic therapy after subarachnoid hemorrhage. Stroke. 2003;34:2807–11.PubMedCrossRefGoogle Scholar
  62. 62.
    Katayama Y, Haraoka J, Hirabayashi H, et al. A randomized controlled trial of hydrocortisone against hyponatremia in patients with aneurysmal subarachnoid hemorrhage. Stroke. 2007;38:2373–5.PubMedCrossRefGoogle Scholar
  63. 63.
    Alberti O, Becker R, Benes L, Wallenfang T, Bertalanffy H. Initial hyperglycemia as an indicator of severity of the ictus in poor-grade patients with spontaneous subarachnoid hemorrhage. Clin Neurol Neurosurg. 2000;102:78–83.PubMedCrossRefGoogle Scholar
  64. 64.
    Claassen J, Vu A, Kreiter KT, et al. Effect of acute physiologic derangements on outcome after subarachnoid hemorrhage. Crit Care Med. 2004;32:832–8.PubMedCrossRefGoogle Scholar
  65. 65.
    Kruyt ND, Biessels GJ, de Haan RJ, et al. Hyperglycemia and clinical outcome in aneurysmal subarachnoid hemorrhage: a meta-analysis. Stroke. 2009;40:e424–30.PubMedCrossRefGoogle Scholar
  66. 66.
    Lanzino G, Kassell NF, Germanson T, Truskowski L, Alves W. Plasma glucose levels and outcome after aneurysmal subarachnoid hemorrhage. J Neurosurg. 1993;79:885–91.PubMedCrossRefGoogle Scholar
  67. 67.
    Bell DA, Strong AJ. Glucose/insulin infusions in the treatment of subarachnoid haemorrhage: a feasibility study. Br J Neurosurg. 2005;19:21–4.PubMedCrossRefGoogle Scholar
  68. 68.
    Bilotta F, Spinelli A, Giovannini F, Doronzio A, Delfini R, Rosa G. The effect of intensive insulin therapy on infection rate, vasospasm, neurologic outcome, and mortality in neurointensive care unit after intracranial aneurysm clipping in patients with acute subarachnoid hemorrhage: a randomized prospective pilot trial. J Neurosurg Anesthesiol. 2007;19:156–60.PubMedCrossRefGoogle Scholar
  69. 69.
    Schlenk F, Nagel A, Graetz D, Sarrafzadeh AS. Hyperglycemia and cerebral glucose in aneurysmal subarachnoid hemorrhage. Intensive Care Med. 2008;34:1200–7.PubMedCrossRefGoogle Scholar
  70. 70.
    Pasternak JJ, McGregor DG, Schroeder DR, et al. Hyperglycemia in patients undergoing cerebral aneurysm surgery: its association with long-term gross neurologic and neuropsychological function. Mayo Clin Proc. 2008;83:406–17.PubMedCrossRefGoogle Scholar
  71. 71.
    Badjatia N, Topcuoglu MA, Buonanno FS, et al. Relationship between hyperglycemia and symptomatic vasospasm after subarachnoid hemorrhage. Crit Care Med. 2005;33:1603–9.PubMedCrossRefGoogle Scholar
  72. 72.
    Naidech AM, Levasseur K, Liebling S, et al. Moderate Hypoglycemia is associated with vasospasm, cerebral infarction, and 3-month disability after subarachnoid hemorrhage. Neurocrit Care. 2010;12:181–7.PubMedCrossRefGoogle Scholar
  73. 73.
    Helbok R, Schmidt JM, Kurtz P, et al. Systemic glucose and brain energy metabolism after subarachnoid hemorrhage. Neurocrit Care. 2010;12:317–23.PubMedCrossRefGoogle Scholar
  74. 74.
    Schlenk F, Graetz D, Nagel A, Schmidt M, Sarrafzadeh AS. Insulin-related decrease in cerebral glucose despite normoglycemia in aneurysmal subarachnoid hemorrhage. Crit Care. 2008;12:R9.PubMedCrossRefGoogle Scholar
  75. 75.
    Finfer S, Chittock DR, Su SY, et al. Intensive versus conventional glucose control in critically ill patients. N Engl J Med. 2009;360:1283–97.PubMedCrossRefGoogle Scholar
  76. 76.
    Fernandez A, Schmidt JM, Claassen J, et al. Fever after subarachnoid hemorrhage: risk factors and impact on outcome. Neurology. 2007;68:1013–9.PubMedCrossRefGoogle Scholar
  77. 77.
    Kilpatrick MM, Lowry DW, Firlik AD, Yonas H, Marion DW. Hyperthermia in the neurosurgical intensive care unit. Neurosurgery. 2000;47:850–5.PubMedCrossRefGoogle Scholar
  78. 78.
    Todd MM, Hindman BJ, Clarke WR, et al. Perioperative fever and outcome in surgical patients with aneurysmal subarachnoid hemorrhage. Neurosurgery. 2009;64:897–908.PubMedCrossRefGoogle Scholar
  79. 79.
    Naidech AM, Bendok BR, Bernstein RA, et al. Fever burden and functional recovery after subarachnoid hemorrhage. Neurosurgery. 2008;63:212–7.PubMedCrossRefGoogle Scholar
  80. 80.
    Diringer MN, Reaven NL, Funk SE, Uman GC. Elevated body temperature independently contributes to increased length of stay in neurologic intensive care unit patients. Crit Care Med. 2004;32:1489–95.PubMedCrossRefGoogle Scholar
  81. 81.
    Oliveira-Filho J, Ezzeddine MA, Segal AZ, et al. Fever in subarachnoid hemorrhage: relationship to vasospasm and outcome. Neurology. 2001;56:1299–304.PubMedGoogle Scholar
  82. 82.
    Rabinstein AA, Sandhu K. Non-infectious fever in the neurological intensive care unit: incidence, causes and predictors. J Neurol Neurosurg Psychiatry. 2007;78:1278–80.PubMedCrossRefGoogle Scholar
  83. 83.
    Commichau C, Scarmeas N, Mayer SA. Risk factors for fever in the neurologic intensive care unit. Neurology. 2003;60:837–41.PubMedGoogle Scholar
  84. 84.
    Oddo M, Frangos S, Milby A, et al. Induced normothermia attenuates cerebral metabolic distress in patients with aneurysmal subarachnoid hemorrhage and refractory fever. Stroke. 2009;40:1913–6.PubMedCrossRefGoogle Scholar
  85. 85.
    Doran TF, De Angelis C, Baumgardner RA, Mellits ED. Acetaminophen: more harm than good for chickenpox? J Pediatr. 1989;114:1045–8.PubMedCrossRefGoogle Scholar
  86. 86.
    Graham NM, Burrell CJ, Douglas RM, Debelle P, Davies L. Adverse effects of aspirin, acetaminophen, and ibuprofen on immune function, viral shedding, and clinical status in rhinovirus-infected volunteers. J Infect Dis. 1990;162:1277–82.PubMedCrossRefGoogle Scholar
  87. 87.
    Aiyagari V, Diringer MN. Fever control and its impact on outcomes: what is the evidence? J Neurol Sci. 2007;261:39–46.PubMedCrossRefGoogle Scholar
  88. 88.
    Mayer S, Commichau C, Scarmeas N, Presciutti M, Bates J, Copeland D. Clinical trial of an air-circulating cooling blanket for fever control in critically ill neurologic patients. Neurology. 2001;56:292–8.PubMedGoogle Scholar
  89. 89.
    Dippel DW, van Breda EJ, van Gemert HM, et al. Effect of paracetamol (acetaminophen) on body temperature in acute ischemic stroke: a double-blind, randomized phase II clinical trial. Stroke. 2001;32:1607–12.PubMedCrossRefGoogle Scholar
  90. 90.
    Cormio M, Citerio G. Continuous low dose diclofenac sodium infusion to control fever in neurosurgical critical care. Neurocrit Care. 2007;6:82–9.PubMedCrossRefGoogle Scholar
  91. 91.
    Mayer SA, Kowalski RG, Presciutti M, et al. Clinical trial of a novel surface cooling system for fever control in neurocritical care patients. Crit Care Med. 2004;32:2508–15.PubMedCrossRefGoogle Scholar
  92. 92.
    Diringer MN. Treatment of fever in the neurologic intensive care unit with a catheter-based heat exchange system. Crit Care Med. 2004;32:559–64.PubMedCrossRefGoogle Scholar
  93. 93.
    Carhuapoma JR, Gupta K, Coplin WM, Muddassir SM, Meratee MM. Treatment of refractory fever in the neurosciences critical care unit using a novel, water-circulating cooling device. A single-center pilot experience. J Neurosurg Anesthesiol. 2003;15:313–8.PubMedCrossRefGoogle Scholar
  94. 94.
    Hoedemaekers CW, Ezzahti M, Gerritsen A, van der Hoeven JG. Comparison of cooling methods to induce and maintain normo- and hypothermia in intensive care unit patients: a prospective intervention study. Crit Care. 2007;11:R91.PubMedCrossRefGoogle Scholar
  95. 95.
    Badjatia N, Strongilis E, Gordon E, et al. Metabolic impact of shivering during therapeutic temperature modulation: the Bedside Shivering Assessment Scale. Stroke. 2008;39:3242–7.PubMedCrossRefGoogle Scholar
  96. 96.
    Tomte O, Draegni T, Mangschau A, Jacobsen D, Auestad B, Sunde K. A comparison of intravascular and surface cooling techniques in comatose cardiac arrest survivors. Crit Care Med. 2011;39:443–9.PubMedCrossRefGoogle Scholar
  97. 97.
    Mack WJ, Ducruet AF, Hickman ZL, et al. Doppler ultrasonography screening of poor-grade subarachnoid hemorrhage patients increases the diagnosis of deep venous thrombosis. Neurol Res. 2008;30:889–92.PubMedCrossRefGoogle Scholar
  98. 98.
    Ray WZ, Strom RG, Blackburn SL, Ashley WW, Sicard GA, Rich KM. Incidence of deep venous thrombosis after subarachnoid hemorrhage. J Neurosurg. 2009;110:1010–4.PubMedCrossRefGoogle Scholar
  99. 99.
    Collen JF, Jackson JL, Shorr AF, Moores LK. Prevention of venous thromboembolism in neurosurgery: a metaanalysis. Chest. 2008;134:237–49.PubMedCrossRefGoogle Scholar
  100. 100.
    Tseng MY, Czosnyka M, Richards H, Pickard JD, Kirkpatrick PJ. 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.PubMedCrossRefGoogle Scholar
  101. 101.
    Lynch JR, Wang H, McGirt MJ, et al. Simvastatin reduces vasospasm after aneurysmal subarachnoid hemorrhage: results of a pilot randomized clinical trial. Stroke. 2005;36:2024–6.PubMedCrossRefGoogle Scholar
  102. 102.
    Chou SH, Smith EE, Badjatia N, et al. A randomized, double-blind, placebo-controlled pilot study of simvastatin in aneurysmal subarachnoid hemorrhage. Stroke. 2008;39:2891–3.PubMedCrossRefGoogle Scholar
  103. 103.
    Vergouwen MD, Meijers JC, Geskus RB, et al. Biologic effects of simvastatin in patients with aneurysmal subarachnoid hemorrhage: a double-blind, placebo-controlled randomized trial. J Cereb Blood Flow Metab. 2009;29:1444–53.PubMedCrossRefGoogle Scholar
  104. 104.
    Jaschinski U, Scherer K, Lichtwarck M, Forst H. Impact of treatment with pravastatin on delayed ischemic disease and mortality after aneurysmal subarachnoid hemorrhage. Crit Care. 2008;12:P112.CrossRefGoogle Scholar
  105. 105.
    Macedo S, Bello Y, Silva A, Siqueira C, Siqueira S, Brito L. Effects of simvastatin in prevention of vasospasm in nontraumatic subarachnoid hemorrhage: preliminary data. Crit Care. 2009;13:P103.CrossRefGoogle Scholar
  106. 106.
    Kramer AH, Gurka MJ, Nathan B, Dumont AS, Kassell NF, Bleck TP. Statin use was not associated with less vasospasm or improved outcome after subarachnoid hemorrhage. Neurosurgery. 2008;62:422–7.PubMedCrossRefGoogle Scholar
  107. 107.
    Kerz T, Victor A, Beyer C, Trapp I, Heid F, Reisch R. A case control study of statin and magnesium administration in patients after aneurysmal subarachnoid hemorrhage: incidence of delayed cerebral ischemia and mortality. Neurol Res. 2008;30:893–7.PubMedCrossRefGoogle Scholar
  108. 108.
    Kern M, Lam MM, Knuckey NW, Lind CR. Statins may not protect against vasospasm in subarachnoid haemorrhage. J Clin Neurosci. 2009;16:527–30.PubMedCrossRefGoogle Scholar
  109. 109.
    McGirt MJ, Garces Ambrossi GL, Huang J, Tamargo RJ. Simvastatin for the prevention of symptomatic cerebral vasospasm following aneurysmal subarachnoid hemorrhage: a single-institution prospective cohort study. J Neurosurg. 2009;110:968–74.PubMedCrossRefGoogle Scholar
  110. 110.
    Singhal AB, Topcuoglu MA, Dorer DJ, Ogilvy CS, Carter BS, Koroshetz WJ. SSRI and statin use increases the risk for vasospasm after subarachnoid hemorrhage. Neurology. 2005;64:1008–13.PubMedCrossRefGoogle Scholar
  111. 111.
    Kramer AH, Fletcher JJ. Statins in the management of patients with aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. Neurocrit Care. 2009;12:285–96.CrossRefGoogle Scholar
  112. 112.
    Vergouwen MD, de Haan RJ, Vermeulen M, Roos YB. Effect of statin treatment on vasospasm, delayed cerebral ischemia, and functional outcome in patients with aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis update. Stroke. 2009;41:e47–52.PubMedCrossRefGoogle Scholar
  113. 113.
    Blanco M, Nombela F, Castellanos M, et al. Statin treatment withdrawal in ischemic stroke: a controlled randomized study. Neurology. 2007;69:904–10.PubMedCrossRefGoogle Scholar
  114. 114.
    Heeschen C, Hamm CW, Laufs U, Snapinn S, Bohm M, White HD. Withdrawal of statins increases event rates in patients with acute coronary syndromes. Circulation. 2002;105:1446–52.PubMedCrossRefGoogle Scholar
  115. 115.
    Spencer FA, Fonarow GC, Frederick PD, et al. Early withdrawal of statin therapy in patients with non-ST-segment elevation myocardial infarction: national registry of myocardial infarction. Arch Intern Med. 2004;164:2162–8.PubMedCrossRefGoogle Scholar
  116. 116.
    Sadeh M. Action of magnesium sulfate in the treatment of preeclampsia-eclampsia. Stroke. 1989;20:1273–5.PubMedCrossRefGoogle Scholar
  117. 117.
    Taccone FS. Vasodilation and neuroprotection: the magnesium saga in subarachnoid hemorrhage. Crit Care Med. 2010;38:1382–4.PubMedCrossRefGoogle Scholar
  118. 118.
    Marinov MB, Harbaugh KS, Hoopes PJ, Pikus HJ, Harbaugh RE. Neuroprotective effects of preischemia intraarterial magnesium sulfate in reversible focal cerebral ischemia. J Neurosurg. 1996;85:117–24.PubMedCrossRefGoogle Scholar
  119. 119.
    van den Bergh WM, Algra A, van Kooten F, et al. Magnesium sulfate in aneurysmal subarachnoid hemorrhage: a randomized controlled trial. Stroke. 2005;36:1011–5.PubMedCrossRefGoogle Scholar
  120. 120.
    Westermaier T, Stetter C, Vince GH, et al. Prophylactic intravenous magnesium sulfate for treatment of aneurysmal subarachnoid hemorrhage: a randomized, placebo-controlled, clinical study. Crit Care Med. 2010;38:1284–90.PubMedCrossRefGoogle Scholar
  121. 121.
    Schmid-Elsaesser R, Kunz M, Zausinger S, Prueckner S, Briegel J, Steiger HJ. Intravenous magnesium versus nimodipine in the treatment of patients with aneurysmal subarachnoid hemorrhage: a randomized study. Neurosurgery. 2006;58:1054–65.PubMedCrossRefGoogle Scholar
  122. 122.
    Muroi C, Terzic A, Fortunati M, Yonekawa Y, Keller E. Magnesium sulfate in the management of patients with aneurysmal subarachnoid hemorrhage: a randomized, placebo-controlled, dose-adapted trial. Surg Neurol. 2008;69:33–9.PubMedCrossRefGoogle Scholar
  123. 123.
    Veyna RS, Seyfried D, Burke DG, et al. Magnesium sulfate therapy after aneurysmal subarachnoid hemorrhage. J Neurosurg. 2002;96:510–4.PubMedCrossRefGoogle Scholar
  124. 124.
    Wong GK, Chan MT, Boet R, Poon WS, Gin T. Intravenous magnesium sulfate after aneurysmal subarachnoid hemorrhage: a prospective randomized pilot study. J Neurosurg Anesthesiol. 2006;18:142–8.PubMedCrossRefGoogle Scholar
  125. 125.
    Wong GK, Poon WS, Chan MT, 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.PubMedCrossRefGoogle Scholar
  126. 126.
    Vergouwen MD, 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.PubMedCrossRefGoogle Scholar
  127. 127.
    Frontera JA, Fernandez A, Schmidt JM, et al. Defining vasospasm after subarachnoid hemorrhage: what is the most clinically relevant definition? Stroke. 2009;40:1963–8.PubMedCrossRefGoogle Scholar
  128. 128.
    Kreiter KT, Mayer SA, Howard G, et al. Sample size estimates for clinical trials of vasospasm in subarachnoid hemorrhage. Stroke. 2009;40:2362–7.PubMedCrossRefGoogle Scholar
  129. 129.
    Vergouwen MD, Etminan N, Ilodigwe D, Macdonald RL. Lower incidence of cerebral infarction correlates with improved functional outcome after aneurysmal subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2011;31:1545–53.PubMedCrossRefGoogle Scholar
  130. 130.
    Pickard JD, Murray GD, Illingworth R, et al. Effect of oral nimodipine on cerebral infarction and outcome after subarachnoid haemorrhage: British aneurysm nimodipine trial. BMJ. 1989;298:636–42.PubMedCrossRefGoogle Scholar
  131. 131.
    Allen GS, Ahn HS, Preziosi TJ, et al. Cerebral arterial spasm—a controlled trial of nimodipine in patients with subarachnoid hemorrhage. N Engl J Med. 1983;308:619–24.PubMedCrossRefGoogle Scholar
  132. 132.
    Rabinstein AA, Weigand S, Atkinson JL, Wijdicks EF. Patterns of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke. 2005;36:992–7.PubMedCrossRefGoogle Scholar
  133. 133.
    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.PubMedCrossRefGoogle Scholar
  134. 134.
    Shimoda M, Takeuchi M, Tominaga J, Oda S, Kumasaka A, Tsugane R. Asymptomatic versus symptomatic infarcts from vasospasm in patients with subarachnoid hemorrhage: serial magnetic resonance imaging. Neurosurgery. 2001;49:1341–8.PubMedCrossRefGoogle Scholar
  135. 135.
    Chaudhary SR, Ko N, Dillon WP, et al. Prospective evaluation of multidetector-row CT angiography for the diagnosis of vasospasm following subarachnoid hemorrhage: a comparison with digital subtraction angiography. Cerebrovasc Dis. 2008;25:144–50.PubMedCrossRefGoogle Scholar
  136. 136.
    Yoon DY, Choi CS, Kim KH, Cho BM. Multidetector-row CT angiography of cerebral vasospasm after aneurysmal subarachnoid hemorrhage: comparison of volume-rendered images and digital subtraction angiography. AJNR Am J Neuroradiol. 2006;27:370–7.PubMedGoogle Scholar
  137. 137.
    Wintermark M, Ko NU, Smith WS, Liu S, Higashida RT, Dillon WP. Vasospasm after subarachnoid hemorrhage: utility of perfusion CT and CT angiography on diagnosis and management. AJNR Am J Neuroradiol. 2006;27:26–34.PubMedGoogle Scholar
  138. 138.
    Wintermark M, Dillon WP, Smith WS, et al. Visual grading system for vasospasm based on perfusion CT imaging: comparisons with conventional angiography and quantitative perfusion CT. Cerebrovasc Dis. 2008;26:163–70.PubMedCrossRefGoogle Scholar
  139. 139.
    Carrera E, Schmidt JM, Oddo M, et al. Transcranial Doppler for predicting delayed cerebral ischemia after subarachnoid hemorrhage. Neurosurgery. 2009;65:316–23.PubMedCrossRefGoogle Scholar
  140. 140.
    Lysakowski C, Walder B, Costanza MC, Tramer MR. Transcranial Doppler versus angiography in patients with vasospasm due to a ruptured cerebral aneurysm: a systematic review. Stroke. 2001;32:2292–8.PubMedCrossRefGoogle Scholar
  141. 141.
    Sloan MA, Alexandrov AV, Tegeler CH, 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.PubMedGoogle Scholar
  142. 142.
    Meixensberger J, Vath A, Jaeger M, Kunze E, Dings J, Roosen K. Monitoring of brain tissue oxygenation following severe subarachnoid hemorrhage. Neurol Res. 2003;25:445–50.PubMedCrossRefGoogle Scholar
  143. 143.
    Sarrafzadeh A, Haux D, Plotkin M, Ludemann L, Amthauer H, Unterberg A. Bedside microdialysis reflects dysfunction of cerebral energy metabolism in patients with aneurysmal subarachnoid hemorrhage as confirmed by 15 O-H2 O-PET and 18 F-FDG-PET. J Neuroradiol. 2005;32:348–51.PubMedCrossRefGoogle Scholar
  144. 144.
    Sarrafzadeh AS, Haux D, Ludemann L, et al. Cerebral ischemia in aneurysmal subarachnoid hemorrhage: a correlative microdialysis-PET study. Stroke. 2004;35:638–43.PubMedCrossRefGoogle Scholar
  145. 145.
    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.PubMedCrossRefGoogle Scholar
  146. 146.
    Vath A, Kunze E, Roosen K, Meixensberger J. Therapeutic aspects of brain tissue pO2 monitoring after subarachnoid hemorrhage. Acta Neurochir Suppl. 2002;81:307–9.PubMedGoogle Scholar
  147. 147.
    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. 2007;38:981–6.PubMedCrossRefGoogle Scholar
  148. 148.
    Stuart RM, Waziri A, Weintraub D, et al. Intracortical EEG for the detection of vasospasm in patients with poor-grade subarachnoid hemorrhage. Neurocrit Care. 2010;13:355–8.PubMedCrossRefGoogle Scholar
  149. 149.
    Mori K, Arai H, Nakajima K, Tajima A, Maeda M. Hemorheological and hemodynamic analysis of hypervolemic hemodilution therapy for cerebral vasospasm after aneurysmal subarachnoid hemorrhage. Stroke. 1995;26:1620–6.PubMedCrossRefGoogle Scholar
  150. 150.
    Raabe A, Beck J, Keller M, Vatter H, Zimmermann M, Seifert V. Relative importance of hypertension compared with hypervolemia for increasing cerebral oxygenation in patients with cerebral vasospasm after subarachnoid hemorrhage. J Neurosurg. 2005;103:974–81.PubMedCrossRefGoogle Scholar
  151. 151.
    Ekelund A, Reinstrup P, Ryding E, 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 Neurochir (Wien). 2002;144:703–12.CrossRefGoogle Scholar
  152. 152.
    Brown FD, Hanlon K, Mullan S. Treatment of aneurysmal hemiplegia with dopamine and mannitol. J Neurosurg. 1978;49:525–9.PubMedCrossRefGoogle Scholar
  153. 153.
    Otsubo H, Takemae T, Inoue T, Kobayashi S, Sugita K. Normovolaemic induced hypertension therapy for cerebral vasospasm after subarachnoid haemorrhage. Acta Neurochir. 1990;103:18–26.CrossRefGoogle Scholar
  154. 154.
    Kosnik EJ, Hunt WE. Postoperative hypertension in the management of patients with intracranial arterial aneurysms. J Neurosurg. 1976;45:148–54.PubMedCrossRefGoogle Scholar
  155. 155.
    Touho H, Karasawa J, Ohnishi H, Shishido H, Yamada K, Shibamoto K. Evaluation of therapeutically induced hypertension in patients with delayed cerebral vasospasm by xenon-enhanced computed tomography. Neurol Med Chir (Tokyo). 1992;32:671–8.CrossRefGoogle Scholar
  156. 156.
    Darby JM, Yonas H, Marks EC, Durham S, Snyder RW, Nemoto EM. Acute cerebral blood flow response to dopamine-induced hypertension after subarachnoid hemorrhage. J Neurosurg. 1994;80:857–64.PubMedCrossRefGoogle Scholar
  157. 157.
    Muizelaar JP, Becker DP. Induced hypertension for the treatment of cerebral ischemia after subarachnoid hemorrhage. Direct effect on cerebral blood flow. Surg Neurol. 1986;25:317–25.PubMedCrossRefGoogle Scholar
  158. 158.
    Miller JA, Dacey RG Jr, Diringer MN. Safety of hypertensive hypervolemic therapy with phenylephrine in the treatment of delayed ischemic deficits after subarachnoid hemorrhage. Stroke. 1995;26:2260–6.PubMedCrossRefGoogle Scholar
  159. 159.
    Kim DH, Joseph M, Ziadi S, Nates J, Dannenbaum M, Malkoff M. Increases in cardiac output can reverse flow deficits from vasospasm independent of blood pressure: a study using xenon computed tomographic measurement of cerebral blood flow. Neurosurgery. 2003;53:1044–51.CrossRefGoogle Scholar
  160. 160.
    Fraticelli AT, Cholley BP, Losser MR, Saint Maurice JP, Payen D. Milrinone for the treatment of cerebral vasospasm after aneurysmal subarachnoid hemorrhage. Stroke. 2008;39:893–8.PubMedCrossRefGoogle Scholar
  161. 161.
    Schmidt U, Bittner E, Pivi S, Marota JJ. Hemodynamic management and outcome of patients treated for cerebral vasospasm with intraarterial nicardipine and/or milrinone. Anesth Analg. 2010;110:895–902.PubMedCrossRefGoogle Scholar
  162. 162.
    Apostolides PJ, Greene KA, Zabramski JM, Fitzgerald JW, Spetzler RF. Intra-aortic balloon pump counterpulsation in the management of concomitant cerebral vasospasm and cardiac failure after subarachnoid hemorrhage: technical case report. Neurosurgery. 1996;38:1056–9.PubMedCrossRefGoogle Scholar
  163. 163.
    Hoh BL, Carter BS, Ogilvy CS. Risk of hemorrhage from unsecured, unruptured aneurysms during and after hypertensive hypervolemic therapy. Neurosurgery. 2002;50:1207–11.PubMedGoogle Scholar
  164. 164.
    Bernardini GL, Mayer SA, Kossoff SB, Hacein-Bey L, Solomon RA, Pile-Spellman J. Anticoagulation and induced hypertension after endovascular treatment for ruptured intracranial aneurysms. Crit Care Med. 2001;29:641–4.PubMedCrossRefGoogle Scholar
  165. 165.
    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.PubMedCrossRefGoogle Scholar
  166. 166.
    Khatri R, Tariq N, Vazquez G, Suri MF, Ezzeddine MA, Qureshi AI. Outcomes after nontraumatic subarachnoid hemorrhage at hospitals offering angioplasty for cerebral vasospasm: a national level analysis in the United States. Neurocrit Care. 2011;15:34–41.Google Scholar
  167. 167.
    Sampson TR, Dhar R, Diringer MN. Factors associated with the development of anemia after subarachnoid hemorrhage. Neurocrit Care. 2010;12:4–9.PubMedCrossRefGoogle Scholar
  168. 168.
    Kramer AH, Gurka MJ, Nathan B, Dumont AS, Kassell NF, Bleck TP. Complications associated with anemia and blood transfusion in patients with aneurysmal subarachnoid hemorrhage. Crit Care Med. 2008;36:2070–5.PubMedCrossRefGoogle Scholar
  169. 169.
    Kramer AH, Zygun DA, Bleck TP, Dumont AS, Kassell NF, Nathan B. Relationship between hemoglobin concentrations and outcomes across subgroups of patients with aneurysmal subarachnoid hemorrhage. Neurocrit Care. 2009;10:157–65.PubMedCrossRefGoogle Scholar
  170. 170.
    Naidech AM, Drescher J, Ault ML, Shaibani A, Batjer HH, Alberts MJ. Higher hemoglobin is associated with less cerebral infarction, poor outcome, and death after subarachnoid hemorrhage. Neurosurgery. 2006;59:775–9.PubMedCrossRefGoogle Scholar
  171. 171.
    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.PubMedCrossRefGoogle Scholar
  172. 172.
    Dhar R, Zazulia AR, Videen TO, Zipfel GJ, Derdeyn CP, Diringer MN. Red blood cell transfusion increases cerebral oxygen delivery in anemic patients with subarachnoid hemorrhage. Stroke. 2009;40:3039–44.PubMedCrossRefGoogle Scholar
  173. 173.
    Benson DW, Williams GR Jr, Spencer FC, Yates AJ. The use of hypothermia after cardiac arrest. Anesth Analg. 1959;38:423–8.PubMedCrossRefGoogle Scholar
  174. 174.
    Hebert PC, Wells G, Blajchman MA, et al. A multicenter, randomized, controlled clinical trial of transfusion requirements in critical care. Transfusion requirements in critical care investigators, Canadian Critical Care Trials Group. N Engl J Med. 1999;340:409–17.PubMedCrossRefGoogle Scholar
  175. 175.
    Levine J, Kofke A, Cen L, et al. Red blood cell transfusion is associated with infection and extracerebral complications after subarachnoid hemorrhage. Neurosurgery. 2010;66:312–8.PubMedCrossRefGoogle Scholar
  176. 176.
    Qureshi AI, Suri MF, Sung GY, et al. Prognostic significance of hypernatremia and hyponatremia among patients with aneurysmal subarachnoid hemorrhage. Neurosurgery. 2002;50:749–55.PubMedCrossRefGoogle Scholar
  177. 177.
    Audibert G, Steinmann G, de Talance N, et al. Endocrine response after severe subarachnoid hemorrhage related to sodium and blood volume regulation. Anesth Analg. 2009;108:1922–8.PubMedCrossRefGoogle Scholar
  178. 178.
    Peters JP, Welt LG, Sims EAH. A salt-wasting syndrome associated with cerebral disease. Trans Assoc Am Physicians. 1950;63:57–64.PubMedGoogle Scholar
  179. 179.
    Rabinstein AA, Wijdicks EF. Hyponatremia in critically ill neurological patients. Neurologist. 2003;9:290–300.PubMedCrossRefGoogle Scholar
  180. 180.
    Palmer BF. Hyponatraemia in a neurosurgical patient: syndrome of inappropriate antidiuretic hormone secretion versus cerebral salt wasting. Nephrol Dial Transplant. 2000;15:262–8.PubMedCrossRefGoogle Scholar
  181. 181.
    Brimioulle S, Orellana-Jimenez C, Aminian A, Vincent JL. Hyponatremia in neurological patients: cerebral salt wasting versus inappropriate antidiuretic hormone secretion. Intensive Care Med. 2008;34:125–31.PubMedCrossRefGoogle Scholar
  182. 182.
    Suarez JI, Qureshi AI, Parekh PD, et al. Administration of hypertonic (3%) sodium chloride/acetate in hyponatremic patients with symptomatic vasospasm following subarachnoid hemorrhage. J Neurosurg Anesthesiol. 1999;11:178–84.PubMedCrossRefGoogle Scholar
  183. 183.
    Bhardwaj A. Neurological impact of vasopressin dysregulation and hyponatremia. Ann Neurol. 2006;59:229–36.PubMedCrossRefGoogle Scholar
  184. 184.
    Rabinstein AA. Vasopressin antagonism: potential impact on neurologic disease. Clin Neuropharmacol. 2006;29:87–93.PubMedCrossRefGoogle Scholar
  185. 185.
    Murphy T, Dhar R, Diringer M. Conivaptan bolus dosing for the correction of hyponatremia in the neurointensive care unit. Neurocrit Care. 2009;11:14–9.PubMedCrossRefGoogle Scholar
  186. 186.
    Dimopoulou I, Kouyialis AT, Tzanella M, et al. High incidence of neuroendocrine dysfunction in long-term survivors of aneurysmal subarachnoid hemorrhage. Stroke. 2004;35:2884–9.PubMedCrossRefGoogle Scholar
  187. 187.
    Dimopoulou I, Tsagarakis S, Douka E, et al. The low-dose corticotropin stimulation test in acute traumatic and non-traumatic brain injury: incidence of hypo-responsiveness and relationship to outcome. Intensive Care Med. 2004;30:1216–9.PubMedCrossRefGoogle Scholar
  188. 188.
    Savaridas T, Andrews PJ, Harris B. Cortisol dynamics following acute severe brain injury. Intensive Care Med. 2004;30:1479–83.PubMedCrossRefGoogle Scholar
  189. 189.
    Bendel S, Koivisto T, Ruokonen E, et al. Pituitary-adrenal function in patients with acute subarachnoid haemorrhage: a prospective cohort study. Crit Care. 2008;12:R126.PubMedCrossRefGoogle Scholar
  190. 190.
    Weant KA, Sasaki-Adams D, Dziedzic K, Ewend M. Acute relative adrenal insufficiency after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2008;63:645–9.PubMedCrossRefGoogle Scholar
  191. 191.
    Hashi K, Takakura K, Sano K, Ohta T, Saito I, Okada K. Intravenous hydrocortisone in large doses in the treatment of delayed ischemic neurological deficits following subarachnoid hemorrhage—results of a multi-center controlled double-blind clinical study. No To Shinkei. 1988;40:373–82.PubMedGoogle Scholar
  192. 192.
    Gomis P, Graftieaux JP, Sercombe R, Hettler D, Scherpereel B, Rousseaux P. Randomized, double-blind, placebo-controlled, pilot trial of high-dose methylprednisolone in aneurysmal subarachnoid hemorrhage. J Neurosurg. 2010;112:681–8.PubMedCrossRefGoogle Scholar
  193. 193.
    Weant KA, Sasaki-Adams D, Dziedzic K, Ewend M. Acute relative adrenal insufficiency after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2008;63:645–9.PubMedCrossRefGoogle Scholar
  194. 194.
    Bardach NS, Olson SJ, Elkins JS, Smith WS, Lawton MT, Johnston SC. Regionalization of treatment for subarachnoid hemorrhage: a cost-utility analysis. Circulation. 2004;109:2207–12.PubMedCrossRefGoogle Scholar
  195. 195.
    Cross DT 3rd, Tirschwell DL, Clark MA, et al. Mortality rates after subarachnoid hemorrhage: variations according to hospital case volume in 18 states. J Neurosurg. 2003;99:810–7.PubMedCrossRefGoogle Scholar
  196. 196.
    Bardach NS, Zhao S, Gress DR, Lawton MT, Johnston SC. Association between subarachnoid hemorrhage outcomes and number of cases treated at California hospitals. Stroke. 2002;33:1851–6.PubMedCrossRefGoogle Scholar
  197. 197.
    Cowan JA Jr, Dimick JB, Wainess RM, Upchurch GR Jr, Thompson BG. Outcomes after cerebral aneurysm clip occlusion in the United States: the need for evidence-based hospital referral. J Neurosurg. 2003;99:947–52.PubMedCrossRefGoogle Scholar
  198. 198.
    Berman MF, Solomon RA, Mayer SA, Johnston SC, Yung PP. Impact of hospital-related factors on outcome after treatment of cerebral aneurysms. Stroke. 2003;34:2200–7.PubMedCrossRefGoogle Scholar
  199. 199.
    Committee on Comparative Effectiveness Research Prioritization IoM. Initial National Priorities for Comparative Effectiveness Research. Washington, DC: The National Academies Press; 2009.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Michael N. Diringer
    • 1
  • Thomas P. Bleck
    • 2
  • J. Claude HemphillIII
    • 3
  • David Menon
    • 4
  • Lori Shutter
    • 5
  • Paul Vespa
    • 6
  • Nicolas Bruder
    • 7
  • E. Sander ConnollyJr.
    • 8
  • Giuseppe Citerio
    • 9
  • Daryl Gress
    • 10
  • Daniel Hänggi
    • 11
  • Brian L. Hoh
    • 12
  • Giuseppe Lanzino
    • 13
  • Peter Le Roux
    • 14
  • Alejandro Rabinstein
    • 13
  • Erich Schmutzhard
    • 15
  • Nino Stocchetti
    • 16
  • Jose I. Suarez
    • 17
  • Miriam Treggiari
    • 18
  • Ming-Yuan Tseng
    • 19
  • Mervyn D. I. Vergouwen
    • 20
  • Stefan Wolf
    • 21
  • Gregory Zipfel
    • 22
  1. 1.Neurology/Neurosurgery Intensive Care UnitWashington UniversitySt. LouisUSA
  2. 2.Rush Medical CollegeChicagoUSA
  3. 3.University of California at San FranciscoSan FranciscoUSA
  4. 4.University of CambridgeCambridgeUK
  5. 5.University of CincinnatiCincinnatiUSA
  6. 6.University of California at Los AngelesLos AngelesUSA
  7. 7.Université de la MéditerranéeMarseilleFrance
  8. 8.Columbia UniversityNew YorkUSA
  9. 9.San Gerardo HospitalMonzaItaly
  10. 10.University of VirginiaCharlottesvilleUSA
  11. 11.Heinrich-Heine UniversityDüsseldorfGermany
  12. 12.University of FloridaGainesvilleUSA
  13. 13.Mayo ClinicRochesterUSA
  14. 14.University of PennsylvaniaPhiladelphiaUSA
  15. 15.University Hospital InnsbruckInnsbruckAustria
  16. 16.Fondazione IRCCS Cà Granda–Ospedale Policlinico, Milan UniversityMilanItaly
  17. 17.Baylor College of MedicineHoustonUSA
  18. 18.University of WashingtonSt. LouisUSA
  19. 19.Nottingham University HospitalsNottinghamUK
  20. 20.University of UtrechtUtrechtThe Netherlands
  21. 21.Freie Universität BerlinBerlinGermany
  22. 22.Washington UniversitySt. LouisUSA

Personalised recommendations