Advertisement

Characteristics of MRI Findings after Subarachnoid Hemorrhage and D-Dimer as a Predictive Value for Early Brain Injury

      Highlights

      • Elevated D-dimer levels were associated with poor outcomes.
      • Early brain injury (EBI) was frequently observed in the paramedian frontal lobe.
      • EBI had significantly higher incidence of poor-grade SAH and poor outcomes.
      • Patients with EBI had significantly higher D-dimer levels than those without EBI.

      Abstract

      Background

      The pathological mechanisms of early brain injury (EBI) have remained obscure. Several studies have reported on the neuroradiological findings of EBI. However, to our knowledge, no study has attempted to explore the mechanism of EBI after subarachnoid hemorrhage (SAH). Therefore, this study evaluates whether the initial plasma D-dimer levels were associated with EBI, classifies magnetic resonance imaging (MRI) findings, and speculates about the mechanism of EBI.

      Methods

      This study included 97 patients hospitalized within 24 h from the onset of nontraumatic SAH. The patients underwent MRI within 0–5 days from onset (before vasospasm) to detect EBI. EBI was radiologically defined as diffusion-weighted imaging (DWI)-positive lesions that appear dark on apparent diffusion coefficient maps, excluding procedure-related lesions. EBI, plasma D-dimer levels, and clinical features were retrospectively investigated.

      Results

      Elevated D-dimer levels were associated with poor outcomes. Patients with EBI had significantly higher D-dimer levels than those without EBI. EBI was detected in 24 patients (27.3%) of all, and in 22 (45%) of 49 patients with World Federation of Neurosurgical Societies (WFNS) grade 4–5 SAH. EBI was frequently observed in the paramedian frontal lobe. There were several types of the pathology in EBI, including widespread symmetrical cerebral cortex lesions, focal cortex lesions, periventricular injury, and other lesions impossible to classify due to unknown mechanisms such as thrombotic complication and microcirculatory disturbance, ultra-early spasm, and spreading depolarization.

      Conclusions

      This study suggests that D-dimer levels predict poor outcomes in patients with SAH and that EBI was associated high D-dimer levels.

      Key Words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Journal of Stroke and Cerebrovascular Diseases
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Kazumata K
        • Kamiyama H
        • Ishikawa T
        • et al.
        Current surgical outcome in poor grade patients with subarachnoid hemorrhage.
        Surg Cereb Stroke (Jpn). 2004; 32: 103-106
        • Kuroda S
        • Ishikawa T
        • Hokari M
        • et al.
        Epidemiology,therapy and functional outcome of aneurysmal subarachnoid hemorrhage in sapporo between 2003-2007: an area-specific, group-based study by hokkaido university hospital group.
        Surg Cereb Stroke (Jpn). 2009; 37: 109-115
        • Laidlaw JD
        • Siu KH.
        Poor-grade aneurysmal subarachnoid hemorrhage: outcome after treatment with urgent surgery.
        Neurosurgery. 2003; 53 (discussion 1280-1272): 1275-1280
        • van Gijn J
        • Kerr RS
        • Rinkel GJ.
        Subarachnoid haemorrhage.
        Lancet. 2007; 369: 306-318
        • Wartenberg KE
        • Schmidt JM
        • Claassen J
        • et al.
        Impact of medical complications on outcome after subarachnoid hemorrhage.
        Crit Care Med. 2006; 34 (quiz 624): 617-623
        • Muroi C
        • Hugelshofer M
        • Seule M
        • et al.
        Correlation among systemic inflammatory parameter, occurrence of delayed neurological deficits, and outcome after aneurysmal subarachnoid hemorrhage.
        Neurosurgery. 2013; 72 (discussion 375): 367-375
        • Dhar R
        • Diringer MN.
        The burden of the systemic inflammatory response predicts vasospasm and outcome after subarachnoid hemorrhage.
        Neurocritic care. 2008; 8: 404-412
        • Hokari M
        • Uchida K
        • Shimbo D
        • et al.
        Acute systematic inflammatory response syndrome and serum biomarkers predict outcomes after subarachnoid hemorrhage.
        J Clin Neurosci. 2020; 78: 108-113
        • McMahon CJ
        • Hopkins S
        • Vail A
        • et al.
        Inflammation as a predictor for delayed cerebral ischemia after aneurysmal subarachnoid haemorrhage.
        J Neurointervent Surg. 2013; 5: 512-517
        • Kusaka G
        • Ishikawa M
        • Nanda A
        • et al.
        Signaling pathways for early brain injury after subarachnoid hemorrhage.
        J Cerebr Blood Flow Metabol. 2004; 24: 916-925
        • Frontera JA
        • Aledort L
        • Gordon E
        • et al.
        Early platelet activation, inflammation and acute brain injury after a subarachnoid hemorrhage: a pilot study.
        J Thromb Haemost. 2012; 10: 711-713
        • Hirashima Y
        • Nakamura S
        • Endo S
        • et al.
        Elevation of platelet activating factor, inflammatory cytokines, and coagulation factors in the internal jugular vein of patients with subarachnoid hemorrhage.
        Neurochem Res. 1997; 22: 1249-1255
        • Ilveskero S
        • Juvela S
        • Siironen J
        • et al.
        D-dimer predicts outcome after aneurysmal subarachnoid hemorrhage: no effect of thromboprophylaxis on coagulation activity.
        Neurosurgery. 2005; 57 (discussion 16-24): 16-24
        • Juvela S
        • Siironen J.
        D-dimer as an independent predictor for poor outcome after aneurysmal subarachnoid hemorrhage.
        Stroke. 2006; 37: 1451-1456
        • Parra A.
        Are d-dimer levels after aneurysmal subarachnoid hemorrhage predictive of outcome?.
        Nat Clin Prac Neurol. 2006; 2: 592-593
        • Fukuda H
        • Lo B
        • Yamamoto Y
        • et al.
        Plasma d-dimer may predict poor functional outcomes through systemic complications after aneurysmal subarachnoid hemorrhage.
        J Neurosurg. 2017; 127: 284-290
        • De Marchis GM
        • Filippi CG
        • Guo X
        • et al.
        Brain injury visible on early mri after subarachnoid hemorrhage might predict neurological impairment and functional outcome.
        Neurocritic Care. 2015; 22: 74-81
        • Frontera JA
        • Ahmed W
        • Zach V
        • et al.
        Acute ischaemia after subarachnoid haemorrhage, relationship with early brain injury and impact on outcome: a prospective quantitative mri study.
        J Neurol Neurosurg Psychiatry. 2015; 86: 71-78
        • Hadeishi H
        • Suzuki A
        • Yasui N
        • et al.
        Diffusion-weighted magnetic resonance imaging in patients with subarachnoid hemorrhage.
        Neurosurgery. 2002; 50 (discussion 747-748): 741-747
        • Wartenberg KE
        • Sheth SJ
        • Michael Schmidt J
        • et al.
        Acute ischemic injury on diffusion-weighted magnetic resonance imaging after poor grade subarachnoid hemorrhage.
        Neurocritic Care. 2011; 14: 407-415
        • Shibuya M
        • Suzuki Y
        • Sugita K
        • et al.
        Effect of at877 on cerebral vasospasm after aneurysmal subarachnoid hemorrhage. Results of a prospective placebo-controlled double-blind trial.
        J Neurosurg. 1992; 76: 571-577
        • Shinohara Y
        • Yamaguchi T.
        Outline of the japanese guidelines for the management of stroke 2004 and subsequent revision.
        Int J Stroke. 2008; 3: 55-62
        • Matsuda N
        • Naraoka M
        • Ohkuma H
        • et al.
        Effect of cilostazol on cerebral vasospasm and outcome in patients with aneurysmal subarachnoid hemorrhage: a randomized, double-blind, placebo-controlled trial.
        Cerebrovasc Dis. 2016; 42: 97-105
        • Senbokuya N
        • Kinouchi H
        • Kanemaru K
        • et al.
        Effects of cilostazol on cerebral vasospasm after aneurysmal subarachnoid hemorrhage: a multicenter prospective, randomized, open-label blinded end point trial.
        J Neurosurg. 2013; 118: 121-130
        • Al-Tamimi YZ
        • Orsi NM
        • Quinn AC
        • et al.
        A review of delayed ischemic neurologic deficit following aneurysmal subarachnoid hemorrhage: historical overview, current treatment, and pathophysiology.
        World Neurosurg. 2010; 73: 654-667
        • Kamiya K
        • Kuyama H
        • Symon L.
        An experimental study of the acute stage of subarachnoid hemorrhage.
        J Neurosurg. 1983; 59: 917-924
        • Kim S
        • Sano K
        [the role of platelets and erythrocytes in disturbance of cerebral microcirculation (author's transl)].
        Neurol Med Chir (Tokyo). 1977; 17: 135-144
        • Asano T
        • Sano K.
        Pathogenetic role of no-reflow phenomenon in experimental subarachnoid hemorrhage in dogs.
        J Neurosurg. 1977; 46: 454-466
        • Ishikawa M
        • Kajimura M
        • Morikawa T
        • et al.
        Cortical microcirculatory disturbance in the super acute phase of subarachnoid hemorrhage - in vivo analysis using two-photon laser scanning microscopy.
        J Neurol Sci. 2016; 368: 326-333
        • Ishikawa M
        • Kajimura M
        • Morikawa T
        • et al.
        Leukocyte plugging and cortical capillary flow after subarachnoid hemorrhage.
        Acta Neurochir (Wien). 2016; 158: 1057-1067
        • Ohkuma H
        • Manabe H
        • Tanaka M
        • et al.
        Impact of cerebral microcirculatory changes on cerebral blood flow during cerebral vasospasm after aneurysmal subarachnoid hemorrhage.
        Stroke. 2000; 31: 1621-1627
        • van den Bergh WM
        • Schepers J
        • Veldhuis WB
        • et al.
        Magnetic resonance imaging in experimental subarachnoid haemorrhage.
        Acta Neurochir (Wien). 2005; 147 (discussion 983): 977-983
        • Busch E
        • Beaulieu C
        • de Crespigny A
        • et al.
        Diffusion mr imaging during acute subarachnoid hemorrhage in rats.
        Stroke. 1998; 29: 2155-2161
        • Bederson JB
        • Levy AL
        • Ding WH
        • et al.
        Acute vasoconstriction after subarachnoid hemorrhage.
        Neurosurgery. 1998; 42 (discussion 360-352): 352-360
        • Bederson JB
        • Germano IM
        • Guarino L.
        Cortical blood flow and cerebral perfusion pressure in a new noncraniotomy model of subarachnoid hemorrhage in the rat.
        Stroke. 1995; 26 (discussion 1091-1082): 1086-1091
        • Eriksen N
        • Rostrup E
        • Fabricius M
        • et al.
        Early focal brain injury after subarachnoid hemorrhage correlates with spreading depolarizations.
        Neurology. 2019; 92: e326-e341
        • Hartings JA
        • York J
        • Carroll CP
        • et al.
        Subarachnoid blood acutely induces spreading depolarizations and early cortical infarction.
        Brain. 2017; 140: 2673-2690
        • Behrouz R
        • Birnbaum LA
        • Jones PM
        • et al.
        Focal neurological deficit at onset of aneurysmal subarachnoid hemorrhage: frequency and causes.
        J Stroke Cerebrovasc Dis. 2016; 25: 2644-2647
        • Sorimachi T
        • Yokota K
        • Hirayama A
        • et al.
        Hemiparesis without responsible hematomas in patients with subarachnoid hemorrhage undergoing early aneurysmal repair.
        World Neurosurg. 2019; 121: e614-e620