Background: Because the pathogenesis of delayed cerebral ischemia (DCI) after subarachnoid hemorrhage (SAH) is unclear, we studied cerebral perfusion at different time points around the occurrence of DCI. Methods: We prospectively enrolled 53 patients admitted to the University Medical Center Utrecht who underwent CT perfusion (CTP) scans on admission, and within 2 weeks after hemorrhage on 2 scheduled time points or during clinical deterioration. The occurrence of DCI was assessed according to predefined criteria by 2 neurological observers blinded to perfusion results. Clinically stable patients (no-DCI) served as reference, and patients with other causes of deterioration (n = 11) were excluded. In DCI patients, the day of DCI onset and in no-DCI patients the median day of DCI onset was taken as t = 0. Scans made before and after DCI were clustered into 5 additional time points. At each time point, cerebral blood volume (CBV) and flow (CBF), and mean transit time (MTT) were measured, and absolute and relative (interhemispheric asymmetry) values were compared between DCI and no-DCI patients. Results: Absolute CBF was lower and MTT was higher in the 18 DCI patients than in the 24 no-DCI patients before, during and after DCI. MTT asymmetry increased during DCI and partially recovered afterwards in DCI patients while it remained constant in no-DCI patients. Absolute and relative CBV remained constant in both groups. Conclusions: Our findings suggest that DCI patients already have diffusely worse perfusion (absolute values) than no-DCI patients before focal worsening (increased asymmetry) occurs and becomes symptomatic. The partial recovery in the measured areas suggests that DCI can be partly reversible.

van Gijn J, Kerr RS, Rinkel GJ: Subarachnoid haemorrhage. Lancet 2007;369:306–318.
Treggiari MM, Walder B, Suter PM, Romand JA: Systematic review of the prevention of delayed ischemic neurological deficits with hypertension, hypervolemia, and hemodilution therapy following subarachnoid hemorrhage. J Neurosurg 2003;98:978–984.
Charpentier C, Audibert G, Guillemin F, Civit T, Ducrocq X, Bracard S, Hepner H, Picard L, Laxenaire MC: Multivariate analysis of predictors of cerebral vasospasm occurrence after aneurysmal subarachnoid hemorrhage. Stroke 1999;30:1402–1408.
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;38:1831–1836.
Stein SC, Levine JM, Nagpal S, LeRoux PD: Vasospasm as the sole cause of cerebral ischemia: How strong is the evidence? Neurosurg Focus 2006;21:E2.
Kozniewska E, Michalik R, Rafalowska J, Gadamski R, Walski M, Frontczak-Baniewicz M, Piotrowski P, Czernicki Z: Mechanisms of vascular dysfunction after subarachnoid hemorrhage. J Physiol Pharmacol 2006;57(suppl 11):145–160.
Romano JG, Rabinstein AA, Arheart KL, Nathan S, Campo-Bustillo I, Koch S, Forteza AM: Microemboli in aneurysmal subarachnoid hemorrhage. J Neuroimaging 2008;18:396–401.
Vergouwen MD, Vermeulen M, Coert BA, Stroes ES, Roos YB: Microthrombosis after aneurysmal subarachnoid hemorrhage: an additional explanation for delayed cerebral ischemia. J Cereb Blood Flow Metab 2008;28:1761–1770.
Dankbaar JW, Rijsdijk M, van der Schaaf IC, Velthuis BK, Wermer MJ, Rinkel GJ: Relationship between vasospasm, cerebral perfusion, and delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. Neuroradiology 2009;51:813–819.
Wintermark M, Thiran JP, Maeder P, Schnyder P, Meuli R: Simultaneous measurement of regional cerebral blood flow by perfusion CT and stable xenon CT: a validation study. AJNR Am J Neuroradiol 2001;22:905–914.
Dankbaar JW, de Rooij NK, Velthuis BK, Frijns CJ, Rinkel GJ, van der Schaaf IC: Diagnosing delayed cerebral ischemia with different CT modalities in patients with subarachnoid hemorrhage with clinical deterioration. Stroke 2009;40:3493–3498.
Rabinstein AA, Friedman JA, Weigand SD, McClelland RL, Fulgham JR, Manno EM, Atkinson JL, Wijdicks EF: Predictors of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke 2004;35:1862–1866.
Hijdra A, Brouwers PJ, Vermeulen M, van Gijn J: Grading the amount of blood on computed tomograms after subarachnoid hemorrhage. Stroke 1990;21:1156–1161.
Chaudhary SR, Ko N, Dillon WP, Yu MB, Liu S, Criqui GI, Higashida RT, Smith WS, Wintermark M: Prospective evaluation of multidetector-row CT angiography for the diagnosis of vasospasm following subarachnoid hemorrhage: a comparison with digital subtraction angiography. Cerebrovasc Dis 2008;25:144–150.
Voldby B, Enevoldsen EM, Jensen FT: Regional CBF, intraventricular pressure, and cerebral metabolism in patients with ruptured intracranial aneurysms. J Neurosurg 1985;62:48–58.
Kealey SM, Loving VA, Delong DM, Eastwood JD: User-defined vascular input function curves: influence on mean perfusion parameter values and signal-to-noise ratio. Radiology 2004;231:587–593.
van der Schaaf I, Vonken EJ, Waaijer A, Velthuis B, Quist M, van Osch T: Influence of partial volume on venous output and arterial input function. AJNR Am J Neuroradiol 2006;27:46–50.
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;38:981–986.
Parsons MW, Pepper EM, Bateman GA, Wang Y, Levi CR: Identification of the penumbra and infarct core on hyperacute noncontrast and perfusion CT. Neurology 2007;68:730–736.
Schaefer PW, Roccatagliata L, Ledezma C, Hoh B, Schwamm LH, Koroshetz W, Gonzalez RG, Lev MH: First-pass quantitative CT perfusion identifies thresholds for salvageable penumbra in acute stroke patients treated with intra-arterial therapy. AJNR Am J Neuroradiol 2006;27:20–25.
Wintermark M, Flanders AE, Velthuis B, Meuli R, van Leeuwen M, Goldsher D, Pineda C, Serena J, van der Schaaf I, Waaijer A, Anderson J, Nesbit G, Gabriely I, Medina V, Quiles A, Pohlman S, Quist M, Schnyder P, Bogousslavsky J, Dillon WP, Pedraza S: Perfusion-CT assessment of infarct core and penumbra: receiver operating characteristic curve analysis in 130 patients suspected of acute hemispheric stroke. Stroke: 2006;37:979–985.
Condette-Auliac S, Bracard S, Anxionnat R, Schmitt E, Lacour JC, Braun M, Meloneto J, Cordebar A, Yin L, Picard L: Vasospasm after subarachnoid hemorrhage: interest in diffusion-weighted MR imaging. Stroke 2001;32:1818–1824.
van Gijn J: Facts versus theories: an everlasting struggle. Cerebrovasc Dis 2010;30:330–339.
Talacchi A: Sequential measurements of cerebral blood flow in the acute phase of subarachnoid hemorrhage. J Neurosurg Sci 1993;37:9–18.
Nabavi DG, LeBlanc LM, Baxter B, Lee DH, Fox AJ, Lownie SP, Ferguson GG, Craen RA, Gelb AW, Lee TY: Monitoring cerebral perfusion after subarachnoid hemorrhage using CT. Neuroradiology 2001;43:7–16.
van der Schaaf I, Wermer MJ, van der Graaf Y, Hoff RG, Rinkel GJ, Velthuis BK: CT after subarachnoid hemorrhage: relation of cerebral perfusion to delayed cerebral ischemia. Neurology 2006;66:1533–1538.
van der Schaaf I, Wermer MJ, van der Graaf Y, Velthuis BK, van de Kraats CI, Rinkel GJ: Prognostic value of cerebral perfusion-computed tomography in the acute stage after subarachnoid hemorrhage for the development of delayed cerebral ischemia. Stroke 2006;37:409–413.
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