Abstract
Background
Poor clinical condition is the most important predictor of neurological outcome and mortality after subarachnoid hemorrhage (SAH). Rupture of an intracranial aneurysm was shown to be associated with acute ischemic brain injury in poor grade patients in autopsy studies and small magnetic resonance imaging series.
Methods
We performed diffusion-weighted magnetic resonance imaging (DWI) within 96 h of onset in 21 SAH patients with Hunt–Hess grade 4 or 5 enrolled in the Columbia University SAH Outcomes Project between July 2004 and February 2007. We analyzed demographic, radiological, clinical data, and 3 months outcome.
Results
Of the 21 patients 13 were Hunt–Hess grade 5, and eight were grade 4. Eighteen patients (86%) displayed bilateral and symmetric abnormalities on DWI, but not on computed tomography (CT). Involved regions included both anterior cerebral artery territories (16 patients), and less often the thalamus and basal ganglia (4 patients), middle (6 patients) or posterior cerebral artery territories (2 patients), or cerebellum (2 patients). At 1-year, 15 patients were dead (life support had been withdrawn in 6), 2 were moderately to severely disabled (modified Rankin Scale [mRS] = 4–5), and 4 had moderate-to-no disability (mRS = 1–3).
Conclusions
Admission DWI demonstrates multifocal areas of acute ischemic injury in poor grade SAH patients. These ischemic lesions may be related to transient intracranial circulatory arrest, acute vasoconstriction, microcirculatory disturbances, or decreased cerebral perfusion from neurogenic cardiac dysfunction. Ischemic brain injury in poor grade SAH may be a feasible target for acute resuscitation strategies.
Similar content being viewed by others
References
Kreiter KT, Copeland D, Bernardini GL, Bates JE, Peery S, Claassen J, Du YE, Stern Y, Connolly ES, Mayer SA. Predictors of cognitive dysfunction after subarachnoid hemorrhage. Stroke. 2002;33:200–8.
Mayer SA, Kreiter KT, Copeland D, Bernardini GL, Bates JE, Peery S, Claassen J, Du YE, Connolly ES Jr. Global and domain-specific cognitive impairment and outcome after subarachnoid hemorrhage. Neurology. 2002;59:1750–8.
Lagares A, Gomez PA, Lobato RD, Alen JF, Alday R, Campollo J. Prognostic factors on hospital admission after spontaneous subarachnoid haemorrhage. Acta Neurochir. 2001;143:665–72.
Claassen J, Carhuapoma JR, Kreiter KT, Du EY, Connolly ES, Mayer SA. Global cerebral edema after subarachnoid hemorrhage: frequency, predictors, and impact on outcome. Stroke. 2002;33:1225–32.
Naidech AM, Janjua N, Kreiter KT, Ostapkovich ND, Fitzsimmons BF, Parra A, Commichau C, Connolly ES, Mayer SA. Predictors and impact of aneurysm rebleeding after subarachnoid hemorrhage. Arch Neurol. 2005;62:410–6.
Kassell NF, Torner JC, Haley EC Jr, Jane JA, Adams HP, Kongable GL. The international cooperative study on the timing of aneurysm surgery. Part 1: overall management results. J Neurosurg. 1990;73:18–36.
Broderick JP, Brott TG, Duldner JE, Tomsick T, Leach A. Initial and recurrent bleeding are the major causes of death following subarachnoid hemorrhage. Stroke. 1994;25:1342–7.
Schmidt JM, Rincon F, Fernandez A, Resor C, Kowalski RG, Claassen J, Connolly ES, Fitzsimmons BF, Mayer SA. Cerebral infarction associated with acute subarachnoid hemorrhage. Neurocrit Care. 2007;7:10–7.
Hadeishi H, Suzuki A, Yasui N, Hatazawa J, Shimosegawa E. Diffusion-weighted magnetic resonance imaging in patients with subarachnoid hemorrhage. Neurosurgery. 2002;50:741–7.
Busch E, Beaulieu C, de Crespigny A, Moseley ME. Diffusion MR imaging during acute subarachnoid hemorrhage in rats. Stroke. 1998;29:2155–61.
van den Bergh WM, Schepers J, Veldhuis WB, Nicolay K, Tulleken CA, Rinkel GJ. Magnetic resonance imaging in experimental subarachnoid haemorrhage. Acta Neurochir. 2005;147:977–83.
Hunt WE, Hess RM. Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg. 1968;28:14–20.
Teasdale G, Jennett B. Assessment of coma and impaired consciousness. A practical scale. Lancet. 1974;2:81–4.
Knaus WA, Draper EA, Wagner DP, Zimmerman JE. APACHE II: a severity of disease classification system. Crit Care Med. 1985;13:818–29.
Claassen J, Vu A, Kreiter KT, Kowalski RG, Du EY, Ostapkovich N, Fitzsimmons BF, Connolly ES, Mayer SA. Effect of acute physiologic derangements on outcome after subarachnoid hemorrhage. Crit Care Med. 2004;32:832–8.
Wartenberg KE, Schmidt JM, Claassen J, Temes RE, Frontera JA, Ostapkovich N, Parra A, Connolly ES, Mayer SA. Impact of medical complications on outcome after subarachnoid hemorrhage. Crit Care Med. 2006;34:617–23. quiz 624.
Hijdra A, van Gijn J, Nagelkerke NJ, Vermeulen M, van Crevel H. Prediction of delayed cerebral ischemia, rebleeding, and outcome after aneurysmal subarachnoid hemorrhage. Stroke. 1988;19:1250–6.
van Gijn J, Hijdra A, Wijdicks EF, Vermeulen M, van Crevel H. Acute hydrocephalus after aneurysmal subarachnoid hemorrhage. J Neurosurg. 1985;63:355–62.
Lyden PD, Lau GT. A critical appraisal of stroke evaluation and rating scales. Stroke. 1991;22:1345–52.
Crompton MR. The pathogenesis of cerebral infarction following the rupture of cerebral berry aneurysms. Brain. 1964;87:491–510.
Birse SH, Tom MI. Incidence of cerebral infarction associated with ruptured intracranial aneurysms. A study of 8 unoperated cases of anterior cerebral aneurysm. Neurology. 1960;10:101–6.
Smith B. Cerebral pathology in subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry. 1963;26:535–9.
Phan TG, Huston J 3rd, Campeau NG, Wijdicks EF, Atkinson JL, Fulgham JR. Value of diffusion-weighted imaging in patients with a nonlocalizing examination and vasospasm from subarachnoid hemorrhage. Cerebrovasc Dis. 2003;15:177–81.
Liu Y, Soppi V, Mustonen T, Kononen M, Koivisto T, Koskela A, Rinne J, Vanninen RL. Subarachnoid hemorrhage in the subacute stage: elevated apparent diffusion coefficient in normal-appearing brain tissue after treatment. Radiology. 2007;242:518–25.
Weidauer S, Lanfermann H, Raabe A, Zanella F, Seifert V, Beck J. Impairment of cerebral perfusion and infarct patterns attributable to vasospasm after aneurysmal subarachnoid hemorrhage: a prospective MRI and DSA study. Stroke. 2007;38:1831–6.
Grote E, Hassler W. The critical first minutes after subarachnoid hemorrhage. Neurosurgery. 1988;22:654–61.
Bergquist E, Bergstrom K. Angiographic documentation of the development of cerebral circulatory arrest. Acta Radiol Diagn. 1972;12:7–11.
Krasznai L, Grote EH. Acute vasoparalysis after subarachnoid haemorrhage and cerebral trauma: general reflex phenomenon? Neurol Res. 1994;16:40–4.
Shigeno T, Fritschka E, Brock M, Schramm J, Shigeno S, Cervos-Navarro J. Cerebral edema following experimental subarachnoid hemorrhage. Stroke. 1982;13:368–79.
Kuyama H, Ladds A, Branston NM, Nitta M, Symon L. An experimental study of acute subarachnoid haemorrhage in baboons: changes in cerebral blood volume, blood flow, electrical activity and water content. J Neurol Neurosurg Psychiatry. 1984;47:354–64.
Kamiya K, Kuyama H, Symon L. An experimental study of the acute stage of subarachnoid hemorrhage. J Neurosurg. 1983;59:917–24.
Sehba FA, Mostafa G, Friedrich V Jr, Bederson JB. Acute microvascular platelet aggregation after subarachnoid hemorrhage. J Neurosurg. 2005;102:1094–100.
Ohkuma H, Manabe H, Tanaka M, Suzuki S. Impact of cerebral microcirculatory changes on cerebral blood flow during cerebral vasospasm after aneurysmal subarachnoid hemorrhage. Stroke. 2000;31:1621–7.
Qureshi AI, Sung GY, Suri MA, Straw RN, Guterman LR, Hopkins LN. Prognostic value and determinants of ultra-early angiographic vasospasm after aneurysmal subarachnoid hemorrhage. Neurosurgery. 1999;44:967–73.
Bederson JB, Levy AL, Ding WH, Kahn R, DiPerna CA, Jenkins AL 3rd, Vallabhajosyula P. Acute vasoconstriction after subarachnoid hemorrhage. Neurosurgery. 1998;42:352–60.
Baldwin ME, Macdonald RL, Huo D, Novakovic RL, Goldenberg FD, Frank JI, Rosengart AJ. Early vasospasm on admission angiography in patients with aneurysmal subarachnoid hemorrhage is a predictor for in-hospital complications and poor outcome. Stroke. 2004;35:2506–11.
Mayer SA, Fink ME, Homma S, Sherman D, LiMandri G, Lennihan L, Solomon RA, Klebanoff LM, Beckford A, Raps EC. Cardiac injury associated with neurogenic pulmonary edema following subarachnoid hemorrhage. Neurology. 1994;44:815–20.
Tung P, Kopelnik A, Banki N, Ong K, Ko N, Lawton MT, Gress D, Drew B, Foster E, Parmley W, Zaroff J. Predictors of neurocardiogenic injury after subarachnoid hemorrhage. Stroke. 2004;35:548–51.
Dreier JP, Woitzik J, Fabricius M, Bhatia R, Major S, Drenckhahn C, Lehmann TN, Sarrafzadeh A, Willumsen L, Hartings JA, Sakowitz OW, Seemann JH, Thieme A, Lauritzen M, Strong AJ. Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. Brain. 2006;129:3224–37.
Latour LL, Hasegawa Y, Formato JE, Fisher M, Sotak CH. Spreading waves of decreased diffusion coefficient after cortical stimulation in the rat brain. Magn Reson Med. 1994;32:189–98.
Mild therapeutic hypothermia to improve the neurologic outcome after cardiac arrest. N Engl J Med. 2002;346:549–56.
Tseng MY, Al-Rawi PG, Pickard JD, Rasulo FA, Kirkpatrick PJ. Effect of hypertonic saline on cerebral blood flow in poor-grade patients with subarachnoid hemorrhage. Stroke. 2003;34:1389–96.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wartenberg, K.E., Sheth, S.J., Michael Schmidt, J. et al. Acute Ischemic Injury on Diffusion-Weighted Magnetic Resonance Imaging after Poor Grade Subarachnoid Hemorrhage. Neurocrit Care 14, 407–415 (2011). https://doi.org/10.1007/s12028-010-9488-1
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12028-010-9488-1