Behavior After Aneurysmal Subarachnoid Hemorrhage: Cognition and Functional Outcome

  • Timour Al-Khindi
  • R. Loch Macdonald
  • Stephan Mayer
  • Tom A. SchweizerEmail author


Spontaneous subarachnoid hemorrhage (SAH) is a medical emergency characterized by hemorrhage in the subarachnoid space surrounding the brain. In the vast majority of cases (85 %), spontaneous SAH is caused by the rupture of a cerebral aneurysm (aSAH) [1]. The other 15 % are idiopathic and two-thirds of these have a characteristic appearance on computed tomography (CT) and are called benign perimesencephalic SAH (pSAH). The characteristic sign of aSAH is a sudden onset of severe “thunderclap” headache, but patients may also present with vomiting, nausea, photophobia, and nuchal rigidity [2]. A cranial CT scan demonstrates accumulation of blood in the basal cisterns (see Fig. 10.1); patients may also present with hemorrhage into the brain and ventricular system [2]. Hypertension and cigarette smoking are risk factors for aSAH [3]. Although uncommon—the incidence of aSAH in North America is approximately 8–11 per 100,000 persons per year [4, 5]—aSAH carries a poor prognosis, with only 35 % of patients surviving [6, 7]. Indeed, although aSAH accounts for only 7 % of all strokes [8], it is responsible for 27 % of all stroke-related years of life lost before age 65 [9]. The high mortality after aSAH may be partially attributed to misdiagnosis. Up to 50 % of cases are misdiagnosed as migraine or tension-type headache due to failure to obtain lumbar puncture or proper neuroimaging [2]. Despite these statistics, advances in the acute management of aSAH over the past 3 decades—mainly increased use of vascular imaging, reduced delays to treatment, and better acute care management [7]—have substantially reduced mortality after aSAH. In a meta-analysis, Lovelock et al. [7] observed that, while the incidence of aSAH has remained stable over the past 30 years, mortality has been reduced by half and the 30-day case fatality rate has decreased by 0.9 % per annum (Figs. 10.1 and 10.2).


Executive Function Verbal Memory Visual Memory Glasgow Outcome Scale Executive Dysfunction 
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  1. 1.
    van Gijn J, Rinkel GJE. Subarachnoid hemorrhage: diagnosis, causes and management. Brain. 2001;124:249–78.PubMedCrossRefGoogle Scholar
  2. 2.
    Suarez JI, Tarr RW, Selman WR. Aneurysmal subarachnoid hemorrhage. N Engl J Med. 2006;354:387–96.PubMedCrossRefGoogle Scholar
  3. 3.
    Feigin VL, Rinkel GJE, Lawes CMM, Algra A, Bennett DA, van Gijn J, et al. Risk factors for subarachnoid hemorrhage: an updated systematic review of epidemiological studies. Stroke. 2005;36:2773–80.PubMedCrossRefGoogle Scholar
  4. 4.
    King Jr JT. Epidemiology of aneurysmal subarachnoid hemorrhage. Neuroimaging Clin N Am. 1997;7:659–68.PubMedGoogle Scholar
  5. 5.
    Østbye T, Levy AR, Mayo NE. Hospitalization and case-fatality rates for subarachnoid hemorrhage in Canada from 1982 through 1991. Stroke. 1997;28:793–8.PubMedCrossRefGoogle Scholar
  6. 6.
    Feigin VL, Lawes CM, Bennett DA, Barker-Collo SL, Parag V. Worldwide stroke incidence and early case fatality reported in 56 population-based studies: a systematic review. Lancet Neurol. 2009;8:355–69.PubMedCrossRefGoogle Scholar
  7. 7.
    Lovelock CE, Rinkel GJE, Rothwell PM. Time trends in outcome of subarachnoid hemorrhage. Population-based study and systematic review. Neurology. 2010;74:1494–501.PubMedCrossRefGoogle Scholar
  8. 8.
    Feigin VL, Lawes CMM, Bennett DA, Anderson CS. Stroke epidemiology: a review of population-based studies of incidence, prevalence, and case-fatality in the late 20th century. Lancet Neurol. 2003;2:43–53.PubMedCrossRefGoogle Scholar
  9. 9.
    Johnston SC, Selvin S, Gress DR. The burden, trends, mortality from and demographics of subarachnoid hemorrhage. Neurology. 1998;50:1413–8.PubMedCrossRefGoogle Scholar
  10. 10.
    Mavaddat N, Sahakian BJ, Hutchinson PJA, Kirkpatrick PJ. Cognition following subarachnoid hemorrhage from anterior communicating artery aneurysm: relation to timing of surgery. J Neurosurg. 1999;91:402–7.PubMedCrossRefGoogle Scholar
  11. 11.
    Rinkel GJ, Algra A. Long-term outcomes of patients with aneurysmal subarachnoid haemorrhage. Lancet Neurol. 2011;10:349–56.PubMedCrossRefGoogle Scholar
  12. 12.
    Powell J, Kitchen N, Heslin J, Greenwood R. Psychosocial outcomes at three and nine months after good neurological recovery from aneurysmal subarachnoid haemorrhage: predictors and prognosis. J Neurol Neurosurg Psychiatry. 2002;72:772–81.PubMedCrossRefGoogle Scholar
  13. 13.
    Benke T, Koylu B, Delazer M, Trinka E, Kemmler G. Cholinergic treatment of amnesia following basal forebrain lesion due to aneurysm rupture—an open-label pilot study. Eur J Neurol. 2005;12:791–6.PubMedCrossRefGoogle Scholar
  14. 14.
    Wermer MJH, Kool H, Albrecht KW, Rinkel GJE. Subarachnoid hemorrhage treated with clipping: long-term effects on employment, relationships, personality and mood. Neurosurgery. 2007;60:91–8.PubMedCrossRefGoogle Scholar
  15. 15.
    Cedzich C, Roth A. Neurological and psychosocial outcome after subarachnoid haemorrhage, and the hunt and hess scale as a predictor of clinical outcome. Zentralbl Neurochir. 2005;66:112–8.PubMedCrossRefGoogle Scholar
  16. 16.
    Hütter BO, Gilsbach JM. Which neuropsychological deficits are hidden behind a good outcome (Glasgow = I) after aneurysmal subarachnoid hemorrhage? Neurosurgery. 1993;33:999–1005.PubMedCrossRefGoogle Scholar
  17. 17.
    Passier PECA, Visser-Meily JMA, van Zandvoort MJE, Post MWM, Rinkel GJE, van Heugten C. Prevalence and determinants of cognitive complaints after aneurysmal subarachnoid hemorrhage. Cerebrovasc Dis. 2010;29:557–63.PubMedCrossRefGoogle Scholar
  18. 18.
    Ljunggren B, Sonesson B, Säveland H, Brandt L. Cognitive impairment and adjustment in patients without neurological deficits after aneurysmal SAH and early operation. J Neurosurg. 1985;62:673–9.PubMedCrossRefGoogle Scholar
  19. 19.
    Schuiling WJ, Rinkel GJE, Walchenbach R, de Weerd AW. Disorders of sleep and wake in patients after subarachnoid hemorrhage. Stroke. 2005;36:578–82.PubMedCrossRefGoogle Scholar
  20. 20.
    Sonesson B, Ljunggren B, Säveland H, Brandt L. Cognition and adjustment after late and early operation for ruptured aneurysm. Neurosurgery. 1987;21:279–87.PubMedCrossRefGoogle Scholar
  21. 21.
    McKenna P, Willison JR, Lowe D, Neil-Dwyer G. Recovery after subarachnoid haemorrhage. Br Med J. 1989;299:485–7.CrossRefGoogle Scholar
  22. 22.
    Ravnik J, Starovasnik B, Šešok S, Pirtosek Z, Svigelj V, Bunc G, et al. Long-term cognitive deficits in patients with good outcomes after aneurysmal subarachnoid hemorrhage from anterior communicating artery. Croat Med J. 2006;47:253–63.PubMedGoogle Scholar
  23. 23.
    Cheng H, Shi J. Neuropsychological evaluations and cognitive deficits in patients with aneurysmal SAH. Chin J Clin Psychol. 2005;13:86–7.Google Scholar
  24. 24.
    Cheng H, Shi J, Zhou M. Cognitive assessment in Chinese patients with aneurysmal subarachnoid hemorrhage. Behav Neurol. 2006;17:117–20.PubMedGoogle Scholar
  25. 25.
    Noble AJ, Baisch S, Mendelow AD, Allen L, Kane P, Schenk T. Posttraumatic stress disorder explains reduced quality of life in subarachnoid hemorrhage patients in both short and long term. Neurosurgery. 2008;63:1095–105.PubMedCrossRefGoogle Scholar
  26. 26.
    Hütter BO, Gilsbach JM. Introspective capacities in patients with cognitive deficits after subarachnoid hemorrhage. J Clin Exp Neuropsychol. 1995;17:499–517.PubMedCrossRefGoogle Scholar
  27. 27.
    Hütter BO, Gilsbach JM, Kreitschmann I. Quality of life and cognitive deficits after subarachnoid haemorrhage. Br J Neurosurg. 1995;9:465–75.PubMedCrossRefGoogle Scholar
  28. 28.
    Thompson JN, Sheldrick R, Berry E. Cognitive and mental health difficulties following subarachnoid hemorrhage. Neuropsychol Rehabil. 2011;21:92–102.PubMedCrossRefGoogle Scholar
  29. 29.
    Hunt WE, Hess RM. Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg. 1968;28:14–20.PubMedCrossRefGoogle Scholar
  30. 30.
    Haug T, Sorteberg A, Finset A, Lindegaard KF, Lundar T, Sorteberg W. Cognitive functioning and health-related quality of life 1 year after aneurysmal subarachnoid hemorrhage in preoperative comatose patients (Hunt and Hess Grade V patients). Neurosurgery. 2010;66:474–84.CrossRefGoogle Scholar
  31. 31.
    Powell J, Kitchen N, Heslin J, Greenwood R. Psychosocial outcomes at 18 months after good neurological recovery from aneurysmal subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry. 2004;75:1119–24.PubMedCrossRefGoogle Scholar
  32. 32.
    Buchanan KM, Elias LJ, Goplen GB. Differing perspectives on outcome after subarachnoid haemorrhage: the patient, the relative, the neurosurgeon. Neurosurgery. 2000;46:831–8.PubMedGoogle Scholar
  33. 33.
    Ogden JA, Mee EW, Henning M. A prospective study of impairment of cognition and memory and recovery after subarachnoid hemorrhage. Neurosurgery. 1993;33:572–86.PubMedCrossRefGoogle Scholar
  34. 34.
    Fisher C, Kistler J, Davis J. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery. 1980;6:1–9.PubMedCrossRefGoogle Scholar
  35. 35.
    Kreiter KT, Copeland D, Bernardini GL, Bates JE, Peery S, Claassen J, et al. Predictors of cognitive dysfunction after subarachnoid hemorrhage. Stroke. 2002;33:200–9.PubMedCrossRefGoogle Scholar
  36. 36.
    Egge A, Waterloo K, Sjøholm H, Solberg T, Ingebrigtsen T, Romner B. Prophylactic hyperdynamic postoperative fluid therapy after aneurysmal subarachnoid hemorrhage: a clinical, prospective, randomized, controlled study. Neurosurgery. 2001;49:593–606.PubMedGoogle Scholar
  37. 37.
    Hütter BO, Gilsbach JM. Early neuropsychological sequelae of aneurysm surgery and subarachnoid hemorrhage. Acta Neurochir (Wien). 1996;138:1370–8.CrossRefGoogle Scholar
  38. 38.
    Hütter BO, Kreitschmann-Andermahr I, Gilsbach JM. Cognitive deficits in the acute stage after subarachnoid hemorrhage. Neurosurgery. 1998;43:1054–65.PubMedCrossRefGoogle Scholar
  39. 39.
    Frazer D, Ahuja A, Watkins L, Cipolotti L. Coiling versus clipping for the treatment of aneurysmal subarachnoid hemorrhage: a longitudinal investigation into cognitive outcome. Neurosurgery. 2007;60:434–42.PubMedCrossRefGoogle Scholar
  40. 40.
    Penninx JF, Visser-Meily JMA, Passier PECA, Rinkel GJE, Post MW, Van Zandvoort MJE. The prognostic value of neuropsychological examination after SAH. Behav Neurol. 2010;23:173–5.PubMedGoogle Scholar
  41. 41.
    Mustonen T, Koivisto T, Vanninen R, Hänninen T, Vapalahti M, Hernesniemi J, et al. Heterogeneity of cerebral perfusion 1 week after haemorrhage is an independent predictor of clinical outcome in patients with aneurysmal subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry. 2008;79:1128–33.PubMedCrossRefGoogle Scholar
  42. 42.
    Bendel P, Koivisto T, Hänninen T, Kolehmainen A, Könönen M, Hurskainen H, et al. Subarachnoid hemorrhage is followed by temporomesial volume loss. Neurology. 2006;67:575–82.PubMedCrossRefGoogle Scholar
  43. 43.
    Ogden JA, Utley T, Mee EW. Neurological and psychosocial outcome 4 to 7 years after subarachnoid hemorrhage. Neurosurgery. 1997;41:25–34.PubMedCrossRefGoogle Scholar
  44. 44.
    Barth M, Thomé C, Schmiedek P, Weiss C, Kasuya H, Vajcokzy P. Characterization of functional outcome and quality of life following subarachnoid hemorrhage in patients treated with and without nicardipine prolonged-release implants. J Neurosurg. 2009;110:955–60.PubMedCrossRefGoogle Scholar
  45. 45.
    Mayer SA, Kreiter KT, Copeland D, Bernardini GL, Bates JE, Peery S, et al. Global and domain-specific cognitive impairment and outcome after subarachnoid hemorrhage. Neurology. 2002;59:1750–8.PubMedCrossRefGoogle Scholar
  46. 46.
    Ørbo M, Waterloo K, Egge A, Isaksen J, Ingebrigtsen T, Romner B. Predictors for cognitive impairment one year after surgery for aneurysmal subarachnoid hemorrhage. J Neurol. 2008;255:1770–6.PubMedCrossRefGoogle Scholar
  47. 47.
    Martinaud O, Perin B, Gérardin E, Proust F, Bioux S, Gars DL, et al. Anatomy of executive deficit following ruptured anterior communicating artery aneurysm. Eur J Neurol. 2009;16:595–601.PubMedCrossRefGoogle Scholar
  48. 48.
    Proust F, Martinaud O, Gérardin E, Derrey S, Levèque S, Bioux S, et al. Quality of life and brain damage after microsurgical clip occlusion or endovascular coil embolization for ruptured anterior communicating artery aneurysms: neuropsychological assessment. J Neurosurg. 2009;110:19–29.PubMedCrossRefGoogle Scholar
  49. 49.
    Romner B, Sonesson B, Ljunggren B, Brandt L, Säveland H, Holtås S. Late magnetic resonance imaging related to neurobehavioral functioning after aneurysmal subarachnoid hemorrhage. Neurosurgery. 1989;25:390–7.PubMedCrossRefGoogle Scholar
  50. 50.
    Drake CG. Report of World Federation of Neurological Surgeons Committee on a universal subarachnoid hemorrhage grading scale. J Neurosurg. 1988;68:985–6.Google Scholar
  51. 51.
    Berry E, Jones RA, West CG, Brown JD. Outcome of subarachnoid haemorrhage. An analysis of surgical variables, cognitive and emotional sequelae related to SPECT scanning. Br J Neurosurg. 1997;11:378–87.PubMedCrossRefGoogle Scholar
  52. 52.
    Richardson JTE. Performance in free recall following rupture and repair of intracranial aneurysm. Brain Cogn. 1989;9:210–26.PubMedCrossRefGoogle Scholar
  53. 53.
    Haug T, Sorteberg A, Sorteberg W, Lindegaard K, Lundar T, Finset A. Cognitive outcome after subarachnoid hemorrhage: time course of recovery and relationship to clinical, radiological and management parameters. Neurosurgery. 2007;60:649–57.PubMedCrossRefGoogle Scholar
  54. 54.
    Elwood RE. The California Verbal Learning Test: psychometric characteristics and clinical application. Neuropsychol Rev. 1995;5:173–7.PubMedCrossRefGoogle Scholar
  55. 55.
    Wechsler D. Wechsler memory scale-revised. San Antonio, TX: The Psychological Corporation; 1987.Google Scholar
  56. 56.
    Osterrieth PA. Le test de copie d’une figure complexe. Arch Psychol. 1944;30:206–356.Google Scholar
  57. 57.
    Rey A. L’examen psychologique dans les cas d’encéphalopathie traumatique. Arch Psychol. 1941;28:286–340.Google Scholar
  58. 58.
    Koivisto T, Vanninen R, Hurskainen H, Saari T, Hernesniemi J, Vapalahti M. Outcomes of early endovascular versus surgical treatment of ruptured cerebral aneurysms: a prospective randomized study. Stroke. 2000;31:2369–77.PubMedCrossRefGoogle Scholar
  59. 59.
    Graetz D, Nagel A, Schlenk F, Sakowitz O, Vajkoczy P, Sarrafzadeh A. High ICP as trigger of proinflammatory IL-6 cytokine activation in aneurysmal subarachnoid hemorrhage. Neurol Res. 2010;32:728–35.PubMedCrossRefGoogle Scholar
  60. 60.
    Chaichana KL, Pradilla G, Huang J, Tamargo RJ. Role of inflammation (leukocyte-endothelial cell interactions) in vasospasm after subarachnoid hemorrhage. World Neurosurg. 2010;73:22–41.PubMedCrossRefGoogle Scholar
  61. 61.
    D’Esposito M, Alexander MP, Fischer R, McGlinchey-Berroth R, O’Connor M. Recovery of memory and executive function following anterior communicating artery aneurysm rupture. J Int Neuropsychol Soc. 1996;2:565–70.PubMedCrossRefGoogle Scholar
  62. 62.
    Rushworth MF, Kennerley SW, Walton ME. Cognitive neuroscience: resolving conflict in and over the medial frontal cortex. Curr Biol. 2005;15:R54–6.PubMedCrossRefGoogle Scholar
  63. 63.
    Stuss DT, Alexander MP, Hamer L, Palumbo C, Dempster R, Binns M, et al. The effects of focal anterior and posterior brain lesions on verbal fluency. J Int Neuropsychol Soc. 1998;4:265–78.PubMedGoogle Scholar
  64. 64.
    Richardson JTE. Cognitive performance following rupture and repair of intracranial aneurysm. Acta Neurol Scand. 1991;83:110–22.PubMedCrossRefGoogle Scholar
  65. 65.
    Squire LR, Stark CEL, Clark RE. The medial temporal lobe. Annu Rev Neurosci. 2004;27:279–306.PubMedCrossRefGoogle Scholar
  66. 66.
    Vilkki JS, Juvela S, Siironen J, Ilvonen T, Varis J, Porras M. Relationship of local infarctions to cognitive and psychosocial impairments after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2004;55:790–803.PubMedCrossRefGoogle Scholar
  67. 67.
    Fletcher PC, Henson RNA. Frontal lobes and human memory: insights from functional neuroimaging. Brain. 2001;124:849–81.PubMedCrossRefGoogle Scholar
  68. 68.
    Kivisaari RP, Salonen O, Servo A, Autti T, Hernesniemi J, Öhman J. MR imaging after aneurysmal subarachnoid hemorrhage and surgery: a long-term follow-up study. AJNR Am J Neuroradiol. 2001;22:1143–8.PubMedGoogle Scholar
  69. 69.
    Vilkki J, Holst P, Öhman J, Servo A, Heiskanen O. Cognitive deficits related to computed tomographic findings after surgery for a ruptured intracranial aneurysm. Neurosurgery. 1989;25:166–72.PubMedCrossRefGoogle Scholar
  70. 70.
    Stuss DT, Levine B. Adult clinical neuropsychology: lessons from studies of the frontal lobes. Annu Rev Psychol. 2002;53:401–33.PubMedCrossRefGoogle Scholar
  71. 71.
    Anderson SW, Todd MM, Hindman BJ, Clarke WR, Torner JC, Tranel D, IHAST Investigators, et al. Effects of intraoperative hypothermia on neuropsychological outcomes after intracranial aneurysm surgery. Ann Neurol. 2006;60:518–27.PubMedCrossRefGoogle Scholar
  72. 72.
    Noble AJ, Schenk T. Posttraumatic stress disorder in the family and friends of patients who have suffered spontaneous subarachnoid hemorrhage. J Neurosurg. 2008;109:1027–33.PubMedCrossRefGoogle Scholar
  73. 73.
    Akyuz M, Erylmaz M, Ozdemir C, Goksu E, Ucar T, Tuncer R. Effect of temporary clipping on frontal lobe functions in patients with ruptured aneurysm of the anterior communicating artery. Acta Neurol Scand. 2005;112:293–7.PubMedCrossRefGoogle Scholar
  74. 74.
    Egge A, Waterloo K, Sjøholm H, Ingebrigtsen T, Forsdahl S, Jacobsen EA, et al. Outcome 1 year after aneurysmal subarachnoid hemorrhage: relation between cognitive performance and neuroimaging. Acta Neurol Scand. 2005;112:76–80.PubMedCrossRefGoogle Scholar
  75. 75.
    Hillis AE, Anderson N, Sampath P, Rigamonti D. Cognitive impairments after surgical repair of ruptured and unruptured aneurysms. J Neurol Neurosurg Psychiatry. 2000;69:608–15.PubMedCrossRefGoogle Scholar
  76. 76.
    Samra SK, Giordani B, Caveney AF, Clarke WR, Scott PA, Anderson S, et al. Recovery of cognitive function after surgery for aneurysmal subarachnoid hemorrhage. Stroke. 2007;38:1864–72.PubMedCrossRefGoogle Scholar
  77. 77.
    Manning L, Pierot L, Dufour A. Anterior and non-anterior ruptured aneurysms: memory and frontal lobe function performance following coiling. Eur J Neurol. 2005;12:466–74.PubMedCrossRefGoogle Scholar
  78. 78.
    Shallice T. Specific impairments of planning. Philos Trans R Soc Lond B Biol Sci. 1982;298:199–209.PubMedCrossRefGoogle Scholar
  79. 79.
    Papagno C, Rizzo S, Ligori L, Lima J, Riggio A. Memory and executive functions in aneurysms of the anterior communicating artery. J Clin Exp Neuropsychol. 2003;25:24–35.PubMedCrossRefGoogle Scholar
  80. 80.
    Bellebaum C, Schäfers L, Schoch B, Wanke I, Stolke D, Forsting M, et al. Clipping versus coiling: neuropsychological follow up after aneurysmal subarachnoid haemorrhage (SAH). J Clin Exp Neuropsychol. 2004;26:1081–92.PubMedCrossRefGoogle Scholar
  81. 81.
    Salmond CH, DeVito EE, Clark L, Menon DK, Chatfield DA, Pickard JD, et al. Impulsivity, reward sensitivity, and decision-making in subarachnoid hemorrhage survivors. J Int Neuropsychol Soc. 2006;12:697–706.PubMedCrossRefGoogle Scholar
  82. 82.
    Uski TK, Lilja Å, Säveland H, Ekman R, Sonesson B, Brandt L. Cognitive functioning and cerebrospinal fluid concentrations of neuropeptides for patients with good neurological outcomes after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2000;47:812–8.PubMedCrossRefGoogle Scholar
  83. 83.
    Cahill J, Zhang JH. Subarachnoid hemorrhage: is it time for a new direction? Stroke. 2009;40:S86–7.PubMedCrossRefGoogle Scholar
  84. 84.
    Bendel P, Koivisto T, Aikiä M, Niskanen E, Könönen M, Hänninen T, et al. Atrophic enlargement of CSF volume after subarachnoid hemorrhage: correlation with neuropsychological outcome. AJNR Am J Neuroradiol. 2010;31:370–6.PubMedCrossRefGoogle Scholar
  85. 85.
    Bendel P, Koivisto T, Niskanen E, Könönen M, Aikiä M, Hänninen T, et al. Brain atrophy and neuropsychological outcome after treatment of ruptured anterior cerebral artery aneurysms: a voxel-based morphometric study. Neuroradiology. 2009;51:711–22.PubMedCrossRefGoogle Scholar
  86. 86.
    Haug T, Sorteberg A, Sorteberg W, Lindegaard K, Lundar T, Finset A. Cognitive functioning and health related quality of life after rupture of an aneurysm on the anterior communicating artery versus middle cerebral artery. Br J Neurosurg. 2009;23:507–15.PubMedCrossRefGoogle Scholar
  87. 87.
    Nelson HE. A modified card sorting test sensitive to frontal lobe defects. Cortex. 1976;12:313–24.PubMedCrossRefGoogle Scholar
  88. 88.
    Stroop JR. Studies of interference in serial verbal reactions. J Exp Psychol. 1935;18:643–62.CrossRefGoogle Scholar
  89. 89.
    Jennett B, Bond M. Assessment of outcome after severe brain damage. Lancet. 1975;1:480–4.PubMedCrossRefGoogle Scholar
  90. 90.
    Shallice T, Evans ME. The involvement of the frontal lobes in cognitive estimation. Cortex. 1978;14:294–303.PubMedCrossRefGoogle Scholar
  91. 91.
    Desantis A, Laiacona M, Barbarotto R, Basso A, Villani R, Spagnoli D, et al. Neuropsychological outcome of patients operated upon for an intracranial aneurysm: analysis of general prognostic factors and of the effects of the location of the aneurysm. J Neurol Neurosurg Psychiatry. 1989;52:1135–40.PubMedCrossRefGoogle Scholar
  92. 92.
    Dikmen SS, Heaton RK, Grant I, Temkin NR. Test-retest reliability and practice effects of expanded Halstead-Reitan Neuropsychological Test Battery. J Int Neuropsychol Soc. 1999;5:346–56.PubMedCrossRefGoogle Scholar
  93. 93.
    Basso MR, Bornstein RA, Lang JM. Practice effects on commonly used measures of executive function across twelve months. Clin Neuropsychol. 1999;13:283–92.PubMedCrossRefGoogle Scholar
  94. 94.
    Chahal N, Barker-Collo S, Feigin V. Cognitive and functional outcomes of 5-year subarachnoid haemorrhage survivors: comparison to matched healthy controls. Neuroepidemiology. 2011;37:31–8.PubMedCrossRefGoogle Scholar
  95. 95.
    Satzger W, Niedermeier N, Schönberger J, Engel RR, Beck OJ. Timing of operation for ruptured cerebral aneurysm and long-term recovery of cognitive functions. Acta Neurochir (Wien). 1995;136:168–74.CrossRefGoogle Scholar
  96. 96.
    Christiansen C, Baum C. Occupational therapy. Enabling function and well-being. Thorofare, NJ: Slack; 1997.Google Scholar
  97. 97.
    Hackett ML, Anderson CS. Health outcomes 1 year after subarachnoid hemorrhage: an international population-based study. Neurology. 2000;55:658–62.PubMedCrossRefGoogle Scholar
  98. 98.
    Pasternak JJ, McGregor DG, Schroeder DR, Lanier WL, Shi Q, Hindman BJ, 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
  99. 99.
    Dombovy ML, Drew-Cates J, Serdans R. Recovery and rehabilitation following subarachnoid haemorrhage. Part I: outcome after inpatient rehabilitation. Brain Inj. 1998;12:443–54.PubMedCrossRefGoogle Scholar
  100. 100.
    Ślusarz R, Beuth W, Książkiewicz B. Postsurgical examination of functional outcome of patients having undergone surgical treatment of intracranial aneurysm. Scand J Caring Sci. 2009;23:130–9.PubMedCrossRefGoogle Scholar
  101. 101.
    Mahoney F, Barthel D. Functional evaluation: the Barthel Index. Md State Med J. 1965;14:61–5.PubMedGoogle Scholar
  102. 102.
    Kim DH, Haney CL, van Ginhoven G. Utility of outcome measures after treatment for intracranial aneurysms: a prospective trial involving 520 patients. Stroke. 2005;36:792–6.PubMedCrossRefGoogle Scholar
  103. 103.
    Katz S, Down TD, Cash HR, Grotz RC. Progress in development of the index of ADL. Gerontologist. 1970;10:20–30.PubMedCrossRefGoogle Scholar
  104. 104.
    Lawton MP, Brody EM. Assessment of older people: self-maintaining and instrumental activities of daily living. Gerontologist. 1969;9:179–86.PubMedCrossRefGoogle Scholar
  105. 105.
    Fernandez A, Schmidt JM, Claassen J, Pavlicova M, Huddleston D, Kreiter KT, et al. Fever after subarachnoid hemorrhage: risk factors and impact on outcome. Neurology. 2007;68:1013–9.PubMedCrossRefGoogle Scholar
  106. 106.
    Kirkness CJ, Thompson JM, Ricker BA, Buzaitis A, Newell DW, Dikmen S, et al. The impact of aneurysmal subarachnoid hemorrhage on functional outcome. J Neurosci Nurs. 2002;34:134–41.PubMedCrossRefGoogle Scholar
  107. 107.
    Dombovy ML, Drew-Cates J, Serdans R. Recovery and rehabilitation following subarachnoid haemorrhage. Part II: long-term follow-up. Brain Inj. 1998;12:887–94.PubMedCrossRefGoogle Scholar
  108. 108.
    Carter BS, Buckley D, Ferraro R, Rordorf G, Ogilvy CS. Factors associated with reintegration to normal living after subarachnoid hemorrhage. Neurosurgery. 2000;46:1326–33.PubMedCrossRefGoogle Scholar
  109. 109.
    Haug T, Sorteberg A, Sorteberg W, Lindegaard KF, Lundar T, Finset A. Surgical repair of unruptured and ruptured middle cerebral artery aneurysms: impact on cognitive functioning and health-related quality of life. Neurosurgery. 2009;64:412–20.PubMedCrossRefGoogle Scholar
  110. 110.
    Morris PG, Wilson JTL, Dunn L. Anxiety and depression after spontaneous subarachnoid hemorrhage. Neurosurgery. 2004;54:47–54.PubMedCrossRefGoogle Scholar
  111. 111.
    Tomberg T, Orasson A, Linnamägi Ü, Toomela A, Pulver A, Asser T. Coping strategies in patients following subarachnoid haemorrhage. Acta Neurol Scand. 2001;104:148–55.PubMedCrossRefGoogle Scholar
  112. 112.
    Hop JW, Rinkel GJE, Algra A, van Gijn J. Changes in functional outcome and quality of life in patients and caregivers after aneurysmal subarachnoid hemorrhage. J Neurosurg. 2001;95:957–63.PubMedCrossRefGoogle Scholar
  113. 113.
    Witelson SF, Pallie W. Left hemisphere specialization for language in the newborn: neuroanatomical evidence of asymmetry. Brain. 1973;96:641–6.PubMedCrossRefGoogle Scholar
  114. 114.
    van Swieten JC, Koudstaal PJ, Visser MC, Schouten HJA, van Gijn J. Interobserver agreement for the assessment of handicap in stroke patients. Stroke. 1988;19:604–7.PubMedCrossRefGoogle Scholar
  115. 115.
    Molyneux A, Kerr R, Stratton I, Sandercock P, Clarke M, Shrimpton J, International Subarachnoid Aneurysm Trial (ISAT) Collaborative Group, et al. International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet. 2002;360:1267–74.PubMedCrossRefGoogle Scholar
  116. 116.
    Mukerji N, Holliman D, Baisch S, Noble A, Schenk T, Nath F. Neuropsychologic impact of treatment modalities in subarachnoid hemorrhage: clipping is no different from coiling. World Neurosurg. 2010;74:129–38.PubMedCrossRefGoogle Scholar
  117. 117.
    Santiago-Ramajo S, Katati MJ, Pérez-García M, Coín-Mejias MA, Vilar-Lopez R, Caracuel-Romero A, et al. Neuropsychological evaluation of the treatments applied to intracranial aneurysms in a Spanish sample. J Clin Exp Neuropsychol. 2007;29:634–41.PubMedCrossRefGoogle Scholar
  118. 118.
    Wong GKC, Wong R, Mok VCT, Fan DS, Leung G, Wong A, et al. Clinical study on cognitive dysfunction after spontaneous subarachnoid haemorrhage: patient profiles and relationship to cholinergic dysfunction. Acta Neurochir. 2009;151:1601–7.PubMedCrossRefGoogle Scholar
  119. 119.
    Fontanella M, Perozzo P, Ursone R, Garbossa D, Bergui M. Neuropsychological assessment after microsurgical clipping or endovascular treatment for anterior communicating artery aneurysm. Acta Neurochir. 2003;145:867–72.PubMedCrossRefGoogle Scholar
  120. 120.
    Hadjivassiliou M, Tooth CL, Romanowski CAJ, Byrne J, Battersby RD, Oxbury S, et al. Aneurysmal SAH: cognitive outcome and structural damage after clipping or coiling. Neurology. 2001;56:1672–7.PubMedCrossRefGoogle Scholar
  121. 121.
    Bendel P, Koivisto T, Könönen M, Hänninen T, Hurskainen H, Saari T, et al. MR imaging of the brain 1 year after aneurysmal subarachnoid hemorrhage: randomize study comparing surgical with endovascular treatment. Radiology. 2008;246:543–52.PubMedCrossRefGoogle Scholar
  122. 122.
    Santiago-Ramajo S, Katati MJ, Pérez-García M, Arjona-Moron V. Evaluating the recovery of cognitive impairment in subarachnoid hemorrhage taking into consideration the practice effects. Neurosurgery. 2010;67:1497–504.PubMedCrossRefGoogle Scholar
  123. 123.
    Brilstra EH, Hop JW, Rinkel GJE. Quality of life after perimesencephalic haemorrhage. J Neurol Neurosurg Psychiatry. 1997;63:382–4.PubMedCrossRefGoogle Scholar
  124. 124.
    Rinkel GJ, Wijdicks EF, Vermeulen M, Hageman LM, Tans JT, van Gijn J. Outcome in perimesencephalic (nonaneurysmal) subarachnoid hemorrhage: a follow-up study in 37 patients. Neurology. 1990;40:1130–2.PubMedCrossRefGoogle Scholar
  125. 125.
    Marquardt G, Niebauer T, Schick U, Lorenz R. Long term follow up after perimesencephalic subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry. 2000;69:127–30.PubMedCrossRefGoogle Scholar
  126. 126.
    Madureira S, Canhão P, Guerreiro M, Ferro JM. Cognitive and emotional consequences of perimesencephalic subarachnoid hemorrhage. J Neurol. 2000;415:862–7.CrossRefGoogle Scholar
  127. 127.
    Tooth CL, Tindale WB, Hadjivassiliou M, Romanowski CA, Hunt E, Pantke R, et al. Subcortical hypoperfusion following surgery for aneurysmal subarachnoid haemorrhage: implications for cognitive performance? Behav Neurol. 2000;12:39–51.PubMedGoogle Scholar
  128. 128.
    Rabinstein AA, Friedman JA, Weigand SD, McClelland RL, Fulgham JR, Manno EM, et al. Predictors of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke. 2004;35:1862–6.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Timour Al-Khindi
    • 1
  • R. Loch Macdonald
    • 2
    • 3
  • Stephan Mayer
    • 4
  • Tom A. Schweizer
    • 5
    • 6
    • 7
    • 8
    Email author
  1. 1.Johns Hopkins University School of MedicineBaltimoreUSA
  2. 2.Division of NeurosurgerySt. Michael’s HospitalTorontoCanada
  3. 3.Department of SurgeryUniversity of TorontoTorontoCanada
  4. 4.Neurological Intensive Care UnitColumbia University Medical CenterNew YorkUSA
  5. 5.Keenan Research Centre, Li Ka Shing Knowledge InstituteSt. Michael’s HospitalTorontoCanada
  6. 6.Institute of Biomedical EngineeringUniversity of TorontoTorontoCanada
  7. 7.Heart and Stroke Foundation, Centre for Stroke RecoveryTorontoCanada
  8. 8.Division of Neurosurgery, Department of SurgeryUniversity of Toronto, St. Michael’s HospitalTorontoCanada

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