Acta Neurochirurgica

, Volume 161, Issue 1, pp 177–184 | Cite as

Predictors of cognitive function in the acute phase after aneurysmal subarachnoid hemorrhage

  • Tonje Haug NordenmarkEmail author
  • Tanja Karic
  • Wilhelm Sorteberg
  • Angelika Sorteberg
Original Article - Vascular Neurosurgery - Aneurysm
Part of the following topical collections:
  1. Vascular Neurosurgery – Aneurysm



Cognitive dysfunction is the most common form of neurological impairment after aneurysmal subarachnoid hemorrhage (aSAH) in the chronic phase. Cognitive deficits in the acute phase after aSAH, however, remain scarcely investigated. The aim of the present study was to test cognitive function and to identify medical predictors of cognitive deficits in the acute phase of aSAH.


Prospective study including 51 patients treated for aSAH. Patients were treated in accordance with a standardized institutional protocol and subjected to neuropsychological evaluation around discharge from neurosurgical care. The neuropsychological test results were transformed into a global cognitive impairment index where an index value of 0.00 is considered normal and 1.00 is considered maximally pathological. Patients with an index score of less than 0.75 were considered having good global cognitive function while those with an index score equal to or above 0.75 were considered having poor global cognitive function. Univariate and multiple regression analysis were used to identify medical predictors of cognitive function.


Fifty-seven percent of the patients had poor cognitive function. They showed severe cognitive deficits, with most tests falling well below two standard deviations from the expected normal mean. Poor cognitive function was not reflected in a poor modified Rankin score in almost half of the cases. Patients with good cognitive function showed only mild cognitive deficits with most tests falling only slightly below the normal mean. Delayed memory was the most affected function in both groups. Univariate analysis identified acute hydrocephalus and aSAH-acquired cerebral infarction to be predictors of poor cognitive function. Cerebrospinal fluid drainage in excess of 2000 ml six-folded the risk of poor cognitive function, whereas a new cerebral infarction 11-folded the respective risk of poor cognitive function.


More than half of aSAH patients have severe cognitive deficits in the acute phase. The modified Rankin Score should be combined with neuropsychological screening in the acute phase after aSAH to get a more accurate description of the patients’ disabilities. Acute hydrocephalus and aSAH-acquired cerebral infarction are the strongest predictors of poor cognitive function in the acute phase.


Neuropsychological test Cognitive function Subarachnoid hemorrhage Intracranial aneurysm Neurointensive care 


Compliance with ethical standards

Conflict of interest

All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers’ bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-licensing arrangements) or non-financial interest (such as personal or professional relationships, affiliations, knowledge, or beliefs) in the subject matter or materials discussed in this manuscript.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.


  1. 1.
    Bendel P, Koivisto T, Niskanen E, Kononen M, Aikia M, Hanninen T, Koskenkorva P, Vanninen R (2009) Brain atrophy and neuropsychological outcome after treatment of ruptured anterior cerebral artery aneurysms: a voxel-based morphometric study. Neuroradiology 51:711–722. CrossRefGoogle Scholar
  2. 2.
    Bendel P, Koivisto T, Aikia M, Niskanen E, Kononen M, Hanninen T, Vanninen R (2010) Atrophic enlargement of CSF volume after subarachnoid hemorrhage: correlation with neuropsychological outcome. AJNR Am J Neuroradiol 31:370–376. CrossRefGoogle Scholar
  3. 3.
    Benedict R (1997) Brief visuospatial memory test-revised: professional manual. Psychological Assessment Resources, Inc, LutzGoogle Scholar
  4. 4.
    Berry E, Jones RA, West CG, Brown JD (1997) Outcome of subarachnoid haemorrhage. An analysis of surgical variables, cognitive and emotional sequelae related to SPECT scanning. Br J Neurosurg 11:378–387CrossRefGoogle Scholar
  5. 5.
    Dehdashti AR, Rilliet B, Rufenacht DA, de Tribolet N (2004) Shunt-dependent hydrocephalus after rupture of intracranial aneurysms: a prospective study of the influence of treatment modality. J Neurosurg 101:402–407. CrossRefGoogle Scholar
  6. 6.
    Delis D, Kaplan K, Kramer J (2001) Delis and Kaplan executive function system. Harcourt Brace & Co, San AntonioGoogle Scholar
  7. 7.
    Finger S, Walbran B, Stein DG (1973) Brain damage and behavioral recovery: serial lesion phenomena. Brain Res 63:1–18CrossRefGoogle Scholar
  8. 8.
    Fisher CM, Roberson GH, Ojemann RG (1977) Cerebral vasospasm with ruptured saccular aneurysm--the clinical manifestations. Neurosurgery 1:245–248CrossRefGoogle Scholar
  9. 9.
    Haug T, Sorteberg A, Sorteberg W, Lindegaard KF, Lundar T, Finset A (2007) Cognitive outcome after aneurysmal subarachnoid hemorrhage: time course of recovery and relationship to clinical, radiological, and management parameters. Neurosurgery 60:649–656; discussion 656-647. CrossRefGoogle Scholar
  10. 10.
    Heaton RK, Grant I, Matthews C (1991) Comprehensive norms for an expanded halstead-reitan neuropsychological battery: demographic corrections, research findings, and clinical applications. Psychological Assessment Resources, OdessaGoogle Scholar
  11. 11.
    Hillis AE, Anderson N, Sampath P, Rigamonti D (2000) Cognitive impairments after surgical repair of ruptured and unruptured aneurysms. J Neurol Neurosurg Psychiatry 69:608–615CrossRefGoogle Scholar
  12. 12.
    Hunt WE, Hess RM (1968) Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg 28:14–20. CrossRefGoogle Scholar
  13. 13.
    Hütter B (2000) Neuropsychological Sequelae of subarachnoid hemorrhage and its treatment. Springer Verlag, Wien. CrossRefGoogle Scholar
  14. 14.
    Hutter BO, Kreitschmann-Andermahr I, Gilsbach JM (1998) Cognitive deficits in the acute stage after subarachnoid hemorrhage. Neurosurgery 43:1054–1065CrossRefGoogle Scholar
  15. 15.
    Investigators ISUIA (1998) Unruptured intracranial aneurysms--risk of rupture and risks of surgical intervention. International Study of Unruptured Intracranial Aneurysms Investigators. N Engl J Med 339:1725–1733. CrossRefGoogle Scholar
  16. 16.
    Isseroff A, Leveton L, Freeman G, Lewis ME, Stein DG (1976) Differences in the behavioral effects of single-stage and serial lesions of the hippocampus. Exp Neurol 53:339–354CrossRefGoogle Scholar
  17. 17.
    Jartti P, Karttunen A, Isokangas JM, Jartti A, Koskelainen T, Tervonen O (2008) Chronic hydrocephalus after neurosurgical and endovascular treatment of ruptured intracranial aneurysms. Acta Radiol 49:680–686. CrossRefGoogle Scholar
  18. 18.
    Jennett B, Bond M (1975) Assessment of outcome after severe brain damage. Lancet 1:480–484CrossRefGoogle Scholar
  19. 19.
    Kreiter KT, Copeland D, Bernardini GL, Bates JE, Peery S, Claassen J, Du YE, Stern Y, Connolly ES, Mayer SA (2002) Predictors of cognitive dysfunction after subarachnoid hemorrhage. Stroke 33:200–208CrossRefGoogle Scholar
  20. 20.
    Larsson C, Ronnberg J, Forssell A, Nilsson LG, Lindberg M, Angquist KA (1989) Verbal memory function after subarachnoid haemorrhage determined by the localisation of the ruptured aneurysm. Br J Neurosurg 3:549–560CrossRefGoogle Scholar
  21. 21.
    Le Roux PD, Elliott JP, Newell DW, Grady MS, Winn HR (1996) Predicting outcome in poor-grade patients with subarachnoid hemorrhage: a retrospective review of 159 aggressively managed cases. J Neurosurg 85:39–49. CrossRefGoogle Scholar
  22. 22.
    Levin HS, O'Donnell VM, Grossman RG (1979) The Galveston orientation and amnesia test. A practical scale to assess cognition after head injury. J Nerv Ment Dis 167:675–684CrossRefGoogle Scholar
  23. 23.
    Lindekleiv HM, Njolstad I, Ingebrigtsen T, Mathiesen EB (2011) Incidence of aneurysmal subarachnoid hemorrhage in Norway, 1999-2007. Acta Neurol Scand 123:34–40. CrossRefGoogle Scholar
  24. 24.
    Ogden JA, Mee EW, Henning M (1993) A prospective study of impairment of cognition and memory and recovery after subarachnoid hemorrhage. Neurosurgery 33:572–586 discussion 586-577Google Scholar
  25. 25.
    Orbo M, Waterloo K, Egge A, Isaksen J, Ingebrigtsen T, Romner B (2008) Predictors for cognitive impairment one year after surgery for aneurysmal subarachnoid hemorrhage. J Neurol 255:1770–1776. CrossRefGoogle Scholar
  26. 26.
    Passier PE, Visser-Meily JM, van Zandvoort MJ, Post MW, Rinkel GJ, van Heugten C (2010) Prevalence and determinants of cognitive complaints after aneurysmal subarachnoid hemorrhage. Cerebrovasc Dis 29:557–563. CrossRefGoogle Scholar
  27. 27.
    Rankin J (1957) Cerebral vascular accidents in patients over the age of 60. III. Diagnosis and treatment. Scott Med J 2:254–268Google Scholar
  28. 28.
    Ravnik J, Starovasnik B, Sesok S, Pirtosek Z, Svigelj V, Bunc G, Bosnjak R (2006) Long-term cognitive deficits in patients with good outcomes after aneurysmal subarachnoid hemorrhage from anterior communicating artery. Croat Med J 47:253–263Google Scholar
  29. 29.
    Richardson JT (1989) Performance in free recall following rupture and repair of intracranial aneurysm. Brain Cogn 9:210–226CrossRefGoogle Scholar
  30. 30.
    Samra SK, Giordani B, Caveney AF, Clarke WR, Scott PA, Anderson S, Thompson BG, Todd MM (2007) Recovery of cognitive function after surgery for aneurysmal subarachnoid hemorrhage. Stroke 38:1864–1872. CrossRefGoogle Scholar
  31. 31.
    Santiago-Ramajo S, Katati MJ, Perez-Garcia M, Coin-Mejias MA, Vilar-Lopez R, Caracuel-Romero A, Arjona-Moron V (2007) Neuropsychological evaluation of the treatments applied to intracranial aneurysms in a Spanish sample. J Clin Exp Neuropsychol 29:634–641. CrossRefGoogle Scholar
  32. 32.
    Sethi H, Moore A, Dervin J, Clifton A, MacSweeney JE (2000) Hydrocephalus: comparison of clipping and embolization in aneurysm treatment. J Neurosurg 92:991–994. CrossRefGoogle Scholar
  33. 33.
    Sorteberg W, Slettebo H, Eide PK, Stubhaug A, Sorteberg A (2008) Surgical treatment of aneurysmal subarachnoid haemorrhage in the presence of 24-h endovascular availability: management and results. Br J Neurosurg 22:53–62. CrossRefGoogle Scholar
  34. 34.
    Stenhouse LM, Knight RG, Longmore BE, Bishara SN (1991) Long-term cognitive deficits in patients after surgery on aneurysms of the anterior communicating artery. J Neurol Neurosurg Psychiatry 54:909–914CrossRefGoogle Scholar
  35. 35.
    Toma AK, Holl E, Kitchen ND, Watkins LD (2011) Evans’ index revisited: the need for an alternative in normal pressure hydrocephalus. Neurosurgery 68:939–944. CrossRefGoogle Scholar
  36. 36.
    Wechsler D (2008) Wechsler adult intelligence scale, fourth edn. Pearson, San AntonioGoogle Scholar
  37. 37.
    Williams MT, Braun AA, Amos-Kroohs RM, McAllister JP 2nd, Lindquist DM, Mangano FT, Vorhees CV, Yuan W (2014) Kaolin-induced ventriculomegaly at weaning produces long-term learning, memory, and motor deficits in rats. Int J Dev Neurosci 35:7–15. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Physical Medicine and RehabilitationOslo University Hospital, UllevålOsloNorway
  2. 2.Department of NeurosurgeryOslo University Hospital, RikshospitaletOsloNorway
  3. 3.Institute of Clinical MedicineUniversity of OsloOsloNorway

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