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Research ArticleNeurointervention

Cerebral Angiography for Evaluation of Patients with CT Angiogram-Negative Subarachnoid Hemorrhage: An 11-Year Experience

J.J. Heit, G.T. Pastena, R.G. Nogueira, A.J. Yoo, T.M. Leslie-Mazwi, J.A. Hirsch and J.D. Rabinov
American Journal of Neuroradiology February 2016, 37 (2) 297-304; DOI: https://doi.org/10.3174/ajnr.A4503
J.J. Heit
aFrom the Department of Radiology (J.J.H.), Interventional Neuroradiology Division, Stanford University Hospital, Stanford, California
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G.T. Pastena
bDepartment of Radiology (G.T.P.), Albany Medical Center, Albany, New York
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R.G. Nogueira
cDepartments of Neurology, Neurosurgery, and Radiology (R.G.N.), Emory University School of Medicine, Marcus Stroke and Neuroscience Center, Atlanta, Georgia
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A.J. Yoo
eTexas Stroke Institute (A.J.Y.), Plano, Texas.
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T.M. Leslie-Mazwi
dDepartment of Neuroradiology and Interventional Neuroradiology (T.M.L.-M., J.A.H., J.D.R.), Massachusetts General Hospital, Boston, Massachusetts
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J.A. Hirsch
aFrom the Department of Radiology (J.J.H.), Interventional Neuroradiology Division, Stanford University Hospital, Stanford, California
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J.D. Rabinov
aFrom the Department of Radiology (J.J.H.), Interventional Neuroradiology Division, Stanford University Hospital, Stanford, California
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    Fig 1.

    Noncontrast head CT examples of SAH. Perimesencephalic SAH: axial image from a noncontrast head CT demonstrates acute SAH in the prepontine and interpeduncular cistern, consistent with a perimesencephalic pattern of SAH (A). Sulcal SAH: axial image from a noncontrast head CT demonstrates acute SAH in the left precentral sulcus and in the sulci overlying the left middle frontal gyrus, consistent with a sulcal pattern of SAH (B). Diffuse SAH: axial image from a noncontrast head CT demonstrates acute SAH in the bilateral Sylvian fissures, overlying the sulci of the bilateral temporal lobes, consistent with a diffuse pattern of SAH. Note also intraventricular hemorrhage within the third ventricle (C). Isolated IVH: axial image from a noncontrast head CT demonstrates acute intraventricular hemorrhage casting the right lateral ventricle (D).

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    Fig 2.

    Cerebral arterial vasculitis identified on DSA. A 45-year-old woman who presented with sulcal SAH (arrow) isolated to the left Sylvian fissure (A). A CTA at the time of admission demonstrated multifocal arterial narrowing (arrowheads) within the bilateral anterior and middle cerebral arteries (B). DSA identified more extensive bilateral arterial irregularity with multifocal narrowing and dilation that was consistent with vasculitis.

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    Fig 3.

    Supraclinoid internal carotid artery aneurysm identified on repeat DSA. A 72-year-old man who presented with perimesencephalic SAH that is localized near the right clinoid process (A). An initial CTA performed on the day of presentation did not identify a lesion responsible for the SAH (B). DSA performed on the day after presentation demonstrates relative narrowing of the right supraclinoid internal carotid artery, the right middle cerebral artery, and the right anterior cerebral artery in the anteroposterior (C) and lateral (D) projections, which was thought to represent early vaspospasm. A follow-up DSA was performed 7 days after presentation, which demonstrates an irregular saccular outpouching (arrows) arising from the supraclinoid internal carotid artery in the anteroposterior (E) and lateral (F) projections, consistent with a dissecting aneurysm.

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    Fig 4.

    Basilar artery aneurysm identified on repeat CTA and DSA. A 65-year-old woman who presented with diffuse SAH in the basal cisterns and bilateral Sylvian fissures. Note hydrocephalus (A and D). A maximum-intensity-projection image from a CTA (B) and a DSA (C) performed on the day of presentation demonstrate no evidence of an aneurysm arising from the basilar artery. A follow-up CTA (E) and DSA (F) performed 7 days after presentation demonstrate an aneurysm arising from the posterior aspect of the basilar artery, consistent with a perforator artery aneurysm.

Tables

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    Table 1:

    Demographic data of patients presenting with subarachnoid or isolated intraventricular hemorrhage without a causative lesion on CTA

    TotalMenWomen
    No. of Patients230118112
    Mean age (yr)545554
    Age range19–9221–9219–87
    SAH found by CT216106110
    SAH found by lumbar puncture1477
    Mean time between CTA and DSA (days)1.51.02.0
    Time range between CTA and DSA (days)0–1100–50–110
    Second follow-up study performed (No. of patients)1698683
    Mean time between initial and follow-up study (days)332442
    Time range between initial and follow-up study (days)0–18360–2030–1836
    Second follow-up modality
        CTA542826
        DSA984553
        MRI/MRA17107
    • View popup
    Table 2:

    Pattern of subarachnoid hemorrhage and the presence of intraventricular hemorrhage

    AllMenWomen
    Pattern of SAH
        None29 (13%)15 (14%)14 (12%)
        Perimesencephalic71 (31%)38 (34%)33 (28%)
        Sulcal37 (16%)15 (14%)a22 (18%)
        Diffuse93 (40%)43 (39%)50 (42%)
    Xanthochromia on lumbar puncture16 (7%)8 (7%)8 (7%)
    Isolated intraventricular hemorrhage13 (6%)7 (6%)6 (5%)
    • ↵a P = .0001 by Fisher exact test.

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    Table 3:

    Diagnosis as determined by digital subtraction angiography

    AllMenWomen
    Diagnosis after initial DSA
        No causative lesion201 (87%)110 (55%)a91 (45%)
        Aneurysm12 (5%)3 (25%)9 (75%)
        Arteriovenous malformation2 (1%)1 (50%)1 (50%)
        Arteriovenous fistula1 (0.5%)1 (100%)0 (0%)
        Vasculitis/vasculopathy15 (7%)3 (21)b11 (79%)
    • ↵a P = .01 by Fisher exact test.

    • ↵b P = .03 by Fisher exact test.

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    Table 4:

    Subarachnoid hemorrhage pattern and final diagnosisa

    Pattern of SAH
    No SAHbPerimesencephalicSulcalDiffuseIVH
    No source identified068 (96%)24 (65%)79 (85%)13 (100%)
    Aneurysm/pseudoaneurysm02 (3%)016 (17%)0
    AVF001 (3%)00
    AVM001 (3%)00
    Vasculitis01 (1.5%)12 (32%)00
    Cavernous malformation1 (3%)0000
    • ↵a Percentages reflect patient percentage with a vascular pathology within each SAH pattern.

    • ↵b “No SAH” refers to patients with xanthochromia or isolated IVH.

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    Table 5:

    Additional diagnosis identified on follow-up CTA, DSA, or MRI

    AllMenWomen
    Total No. of patients undergoing follow-up studies1698683
    Additional diagnosis after follow-up studies:
        Aneurysm/pseudoaneurysm6 (4%)3 (3%)3 (4%)
        Cavernous malformation1 (0.6%)0 (0%)1 (1%)
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American Journal of Neuroradiology: 37 (2)
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J.J. Heit, G.T. Pastena, R.G. Nogueira, A.J. Yoo, T.M. Leslie-Mazwi, J.A. Hirsch, J.D. Rabinov
Cerebral Angiography for Evaluation of Patients with CT Angiogram-Negative Subarachnoid Hemorrhage: An 11-Year Experience
American Journal of Neuroradiology Feb 2016, 37 (2) 297-304; DOI: 10.3174/ajnr.A4503

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Cerebral Angiography for Evaluation of Patients with CT Angiogram-Negative Subarachnoid Hemorrhage: An 11-Year Experience
J.J. Heit, G.T. Pastena, R.G. Nogueira, A.J. Yoo, T.M. Leslie-Mazwi, J.A. Hirsch, J.D. Rabinov
American Journal of Neuroradiology Feb 2016, 37 (2) 297-304; DOI: 10.3174/ajnr.A4503
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