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Research ArticleBrain
Open Access

Cerebrovascular Collaterals Correlate with Disease Severity in Adult North American Patients with Moyamoya Disease

M.K. Strother, M.D. Anderson, R.J. Singer, L. Du, R.D. Moore, Y. Shyr, T.R. Ladner, D. Arteaga, M.A. Day, P.F. Clemmons and M.J. Donahue
American Journal of Neuroradiology July 2014, 35 (7) 1318-1324; DOI: https://doi.org/10.3174/ajnr.A3883
M.K. Strother
aFrom the Departments of Radiology and Radiological Sciences (M.K.S., M.D.A., R.D.M., T.R.L., D.A., M.A.D., P.F.C., M.J.D.)
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M.D. Anderson
aFrom the Departments of Radiology and Radiological Sciences (M.K.S., M.D.A., R.D.M., T.R.L., D.A., M.A.D., P.F.C., M.J.D.)
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R.J. Singer
fSection of Neurosurgery (R.J.S.), Dartmouth-Hitchcock Medical Center, Lebanon, New Hampshire.
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L. Du
eVanderbilt Center for Quantitative Sciences (L.D., Y.S.); Vanderbilt University School of Medicine, Nashville, Tennessee
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R.D. Moore
aFrom the Departments of Radiology and Radiological Sciences (M.K.S., M.D.A., R.D.M., T.R.L., D.A., M.A.D., P.F.C., M.J.D.)
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Y. Shyr
eVanderbilt Center for Quantitative Sciences (L.D., Y.S.); Vanderbilt University School of Medicine, Nashville, Tennessee
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T.R. Ladner
aFrom the Departments of Radiology and Radiological Sciences (M.K.S., M.D.A., R.D.M., T.R.L., D.A., M.A.D., P.F.C., M.J.D.)
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D. Arteaga
aFrom the Departments of Radiology and Radiological Sciences (M.K.S., M.D.A., R.D.M., T.R.L., D.A., M.A.D., P.F.C., M.J.D.)
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M.A. Day
aFrom the Departments of Radiology and Radiological Sciences (M.K.S., M.D.A., R.D.M., T.R.L., D.A., M.A.D., P.F.C., M.J.D.)
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P.F. Clemmons
aFrom the Departments of Radiology and Radiological Sciences (M.K.S., M.D.A., R.D.M., T.R.L., D.A., M.A.D., P.F.C., M.J.D.)
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M.J. Donahue
aFrom the Departments of Radiology and Radiological Sciences (M.K.S., M.D.A., R.D.M., T.R.L., D.A., M.A.D., P.F.C., M.J.D.)
bNeurology (M.J.D.)
cPsychiatry (M.J.D)
dPhysics and Astronomy (M.J.D.)
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    Fig 1.

    Modified Suzuki scoring. Anteroposterior projections from DSA demonstrate a moderately stenosed left ICA without anterior cerebral artery or MCA involvement or Moyamoya perforators (mSS I) (A); an occluded left M1 with well-developed ICA Moyamoya perforators (mSS II) (B); an occluded right ICA, A1 and M1 with extensive Moyamoya perforators (mSS III) (C); and an occluded left ICA, M1 and A1 with absent Moyamoya perforators (mSS IV)—external carotid collaterals are visualized from a common carotid injection (D).

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    Fig 2.

    PcomA/ICA ratio method. Lateral projection from DSA with the PcomA/ICA ratio in a patient with MMD with distal ICA occlusion beyond the PcomA origin.

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    Fig 3.

    PcomA/ICA ratio in subjects with MMD versus control subjects by hemisphere. The PcomA/ICA ratio in a patient with MMD (n = 1) was significantly higher (P < .001) compared with control subjects (n = 0). Orange dots are observations for the left cerebral hemisphere, and blue dots are for the right cerebral hemisphere. The dark band represents the median in this boxplot.

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    Fig 4.

    PcomA/ICA ratio in patients with MMD by mSS and hemisphere. The PcomA/ICA ratio increased with increasing mSS (P = .024). Orange dots are observations for the left cerebral hemisphere, and blue dots are for the right cerebral hemisphere.

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    Fig 5.

    Anteroposterior (A) and lateral (B) projections from DSA with right vertebral injection in patient with MMD demonstrate leptomeningeal cortical branches (arrows) from the PCA to the left parietal and temporal lobes.

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    Fig 6.

    Lateral projections from DSA in 3 patients with Moyamoya disease, with the AchoA identified by the arrow. A, The AchoA appears normal without proliferative vessels (stage zero). B, The AchoA is thickened with distal branching (stage I). C, The AchoA is dilated, and abnormal branches serve as collaterals (stage II).

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    Table 1:

    Modified Suzuki scoring

    ScoreDescription of classification
    0No evidence of disease
    IMild-to-moderate stenosis around ICA bifurcation with absent or slightly developed ICA MMDa
    IISevere stenosis around the ICA bifurcation or occlusion of either proximal anterior or MCA branches with well-developed ICA MMD
    IIIOcclusion of both anterior and MCA branches with well-developed ICA MMD (only a few of anterior or MCA branches or both are faintly opacified in antegrade fashion through meshwork of ICA MMD)
    IVComplete occlusion of both anterior and MCA branches with absent or small amount of ICA MMD (without opacification of either anterior or MCA branches in antegrade fashion)
    • ↵a ICA Moyamoya disease indicates perforating collateral vessels at or around the terminal ICA.

    • View popup
    Table 2:

    Collateral and clinical characteristics by modified Suzuki score in subjects with Moyamoya diseasea

    Metric (P Value)N0 (n = 6)I (n = 7)II (n = 30)III (n = 20)IV (n = 15)
    PcomA/ICAb (.024)640.1250.2050.2950.3300.520
    LMC (.001)78
        117% (1)29% (2)63% (19)80% (16)93% (14)
        283% (5)71% (5)37% (11)20% (4)7% (1)
    CT/MR (.06)c78
        183% (5)57% (4)37% (11)15% (3)33% (5)
        217% (1)42% (3)60% (18)70% (14)67% (10)
        30% (0)0% (0)3% (1)15% (3)0% (0)
    AchoA (<.001)78
        083% (5)43% (3)13% (4)5% (1)7% (1)
        117% (1)43% (3)37% (11)10% (2)0% (0)
        20% (0)14% (1)50% (15)85% (17)33% (5)
        NV0% (0)0% (0)0% (0)0% (0)60% (9)
    P1 (.14)78
        1100% (6)86% (6)90% (27)95% (19)67% (10)
        20% (0)14% (1)10% (3)5% (1)33% (5)
    • Note:—N indicates the number of nonmissing values; NV, not visualized.

    • ↵a Numbers after percentages are frequencies.

    • ↵b PcomA/ICA ratio provided is median.

    • ↵c CT/MR 1—no infarct or hemorrhage, 2—infarct, 3—hemorrhage.

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    Table 3:

    Distribution of anterior choroidal artery grades by imaging findingsa

    Symptom of HemisphereNAchoA Grade
    0 (No.)1 (No.)2 (No.)
    No symptom2429% (7)33% (8)38% (9)
    Infarct4117% (7)22% (9)61% (25)
    Hemorrhage40% (0)0% (0)100% (4)
    • Note:—N indicates the number of nonmissing values.

    • ↵a P = .18.

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American Journal of Neuroradiology: 35 (7)
American Journal of Neuroradiology
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M.K. Strother, M.D. Anderson, R.J. Singer, L. Du, R.D. Moore, Y. Shyr, T.R. Ladner, D. Arteaga, M.A. Day, P.F. Clemmons, M.J. Donahue
Cerebrovascular Collaterals Correlate with Disease Severity in Adult North American Patients with Moyamoya Disease
American Journal of Neuroradiology Jul 2014, 35 (7) 1318-1324; DOI: 10.3174/ajnr.A3883

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Cerebrovascular Collaterals Correlate with Disease Severity in Adult North American Patients with Moyamoya Disease
M.K. Strother, M.D. Anderson, R.J. Singer, L. Du, R.D. Moore, Y. Shyr, T.R. Ladner, D. Arteaga, M.A. Day, P.F. Clemmons, M.J. Donahue
American Journal of Neuroradiology Jul 2014, 35 (7) 1318-1324; DOI: 10.3174/ajnr.A3883
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