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Research ArticleNeurointervention

Value of Quantitative Collateral Scoring on CT Angiography in Patients with Acute Ischemic Stroke

A.M.M. Boers, R. Sales Barros, I.G.H. Jansen, O.A. Berkhemer, L.F.M. Beenen, B.K. Menon, D.W.J. Dippel, A. van der Lugt, W.H. van Zwam, Y.B.W.E.M. Roos, R.J. van Oostenbrugge, C.H. Slump, C.B.L.M. Majoie and H.A. Marquering on behalf of the MR CLEAN investigators
American Journal of Neuroradiology April 2018, DOI: https://doi.org/10.3174/ajnr.A5623
A.M.M. Boers
aFrom the Departments of Biomedical Engineering and Physics (A.M.M.B., R.S.B., I.G.H.J., H.A.M.)
bRadiology and Nuclear Medicine (A.M.M.B., I.G.H.J., O.A.B., L.F.M.B., C.B.L.M.M., H.A.M.)
dDepartment of Robotics and Mechatronics (A.M.M.B., C.H.S.)
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R. Sales Barros
aFrom the Departments of Biomedical Engineering and Physics (A.M.M.B., R.S.B., I.G.H.J., H.A.M.)
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I.G.H. Jansen
aFrom the Departments of Biomedical Engineering and Physics (A.M.M.B., R.S.B., I.G.H.J., H.A.M.)
bRadiology and Nuclear Medicine (A.M.M.B., I.G.H.J., O.A.B., L.F.M.B., C.B.L.M.M., H.A.M.)
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O.A. Berkhemer
bRadiology and Nuclear Medicine (A.M.M.B., I.G.H.J., O.A.B., L.F.M.B., C.B.L.M.M., H.A.M.)
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L.F.M. Beenen
bRadiology and Nuclear Medicine (A.M.M.B., I.G.H.J., O.A.B., L.F.M.B., C.B.L.M.M., H.A.M.)
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B.K. Menon
fDepartment of Clinical Neurosciences (B.K.M.), Hotchkiss Brain Institute, Cumming School of Medicine, University of Calgary, Foothills Hospital, Calgary, Alberta, Canada
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D.W.J. Dippel
gDepartments of Neurology (D.W.J.D.)
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A. van der Lugt
hRadiology (A.v.d.L.), Erasmus MC, Rotterdam, the Netherlands
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W.H. van Zwam
iDepartment of Radiology (W.H.v.Z.), Maastricht UMC, Maastricht, the Netherlands
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Y.B.W.E.M. Roos
cNeurology (Y.B.W.E.M.R.), Academic Medical Center, Amsterdam, the Netherlands
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R.J. van Oostenbrugge
jDepartment of Neurology (R.J.v.O.), Maastricht UMC and Cardiovascular Research Institute Maastricht, Maastricht, the Netherlands.
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C.H. Slump
dDepartment of Robotics and Mechatronics (A.M.M.B., C.H.S.)
eMIRA Institute for Biomedical Engineering and Technical Medicine (C.H.S.), University of Twente, Enschede, the Netherlands
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C.B.L.M. Majoie
aFrom the Departments of Biomedical Engineering and Physics (A.M.M.B., R.S.B., I.G.H.J., H.A.M.)
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H.A. Marquering
aFrom the Departments of Biomedical Engineering and Physics (A.M.M.B., R.S.B., I.G.H.J., H.A.M.)
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    Fig 1.

    An example of quantitative collateral capacity scoring. A, An axial plane of a baseline CTA image acquired in the peak venous phase with a right-sided M1 segment occlusion of the MCA territory. B, Segmentation results of automated quantitative collateral assessment of the ipsilateral (red) and contralateral (blue) hemispheres. The quantitative collateral score was 46%. C, 3D representation of the segmented vasculature.

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    Fig 2.

    Case examples of 4 patients with different visually scored collateral grades and corresponding quantitative collateral scores. Each panel shows a maximum-intensity-projection of the CTA image (left) and the segmented vasculature for qCS calculation (right). The automated segmentation on the ipsilateral side is shown in blue and the segmentation on the contralateral side is shown in red. A, Absent collaterals (visual collateral score = 0). CTA of an 83-year-old man with a left-sided M2 occlusion acquired in the early arterial phase. Follow-up infarct volume was 205 mL, and the mRS score was 6. B, Poor collaterals (vCS = 1). CTA of a 79-year-old man with a right-sided M1 occlusion acquired in the equilibrium phase. FIV was 245 mL, and the mRS score was 6. C, Moderate collaterals (vCS = 2). CTA of a 45-year-old woman with a left-sided M1 occlusion acquired in the peak arterial phase. FIV was 24 mL, and the mRS score was 2. D, Good collaterals (vCS = 3). CTA of a 76-year-old woman with a left-sided ICA-T occlusion acquired in the late venous phase. FIV was 48 mL, and the mRS score was 3.

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    Fig 3.

    Distribution of quantitative collateral scores per visual collateral score, ranging from absent collaterals (0% filling of the occluded territory) to good collaterals (100% filling of the occluded territory). The quantitative collateral score was significantly different among all visual collateral score groups, except for absent collaterals (grade 0) versus poor collaterals (grade 1).

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    Fig 4.

    Receiver operating characteristic curve analysis of visual and quantitative collateral scores for discriminating favorable outcome (mRS 0–2) with areas under the curve of, respectively, 0.65 and 0.68 (A) and large infarct (FIV of >90 mL) with areas under the curve of, respectively, 0.69 and 0.71 (B).

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    Fig 5.

    Bar graphs depict the proportion of functional independence (mRS 0–2) by quantitative collateral score strata for CTA image acquisition in the early arterial phase (A) and arteriovenous phase (B), and by visual collateral scores in the early arterial phase (C) and arteriovenous phase (D).

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    Table 1:

    Baseline characteristics

    CharacteristicAll (N = 442)
    Age in years, median [IQR]66 [54–76]
    Female sex, % (n)41.4 (183)
    Left hemisphere infarct, % (n)52.9 (234)
    NIHSS score at baseline, median [IQR]18 [14–22]
    Alteplase (tPA) delivered, % (n)88.9 (392)
    Allocated to endovascular therapy, % (n)46.8 (207)
    Atrial fibrillation, % (n)26.7 (118)
    Myocardial infarction, % (n)14.9 (66)
    Peripheral arterial disease, % (n)5.2 (23)
    Diabetes mellitus, % (n)13.6 (60)
    Hypertension, % (n)45.4 (200)
    History of ischemic stroke, % (n)10.6 (47)
    Tobacco use, % (n)26.3 (116)
    Use of statins, % (n)79.4 (350)
    Onset to randomization in minutes, median [IQR]201 [150–256]
    Prestroke modified Rankin Scale score, % (n)
        079.9 (353)
        110.4 (46)
        ≥25.7 (25)
    ASPECTS at baseline, % (n)
        0–42.2 (10)
        5–711.2 (49)
        8–1086.6 (381)
    Occlusion location, % (n)
        ICA0.7 (3)
        ICA-T27.4 (121)
        M163.3 (280)
        M28.6 (38)
    • View popup
    Table 2:

    Spearman rank ρ (95% CI) of collateral measures with outcomes for all studies and per CTA acquisition phase

    All Studies (N = 442)Early Arterial (n = 91)Peak Arterial (n = 56)Equilibrium (n = 123)Peak Venous (n = 114)Late Venous (n = 58)
    Follow-up infarct volume
        Visual collateral score−.44 (−.53 to −.36)a−.35 (−.55 to −.13)a−.46 (−.65 to −.21a−.51 (−.64 to −.35)a−.49 (−.64 to −.29a−.47 (−.66 to −.24)a
        Quantitative collateral score−.46 (−.54 to −.37)a−.45 (−.62 to −.24)a−.46 (−.66 to −.19)a−.51 (−.65 to −.34)a−.41 (−.56 to −.20)a−.52 (−.70 to −.29)a
    mRS at 90 days
        Visual collateral score−.31 (−.39 to −.22)a−.19 (−.38 to .03)−.22 (−.49 to −.04)−.28 (−.49 to −.15)a−.29 (−.45 to −.09)a−.41 (−.63 to −.19)a
        Quantitative collateral score−.40 (−.48 to −.32)a−.35 (−.53 to −.13)a−.34 (−.55 to −.10)a−.38 (−.58 to −.25)a−.30 (−.42 to −.08)a−.37 (−.59 to −.12)a
    • ↵a Significant correlation at P < .01.

    • View popup
    Table 3:

    Results of adjusted and unadjusted regression analyses for the effect of collateral capacity on follow-up infarct volume

    AdjustedUnadjusted
    β Log-Transformed (95% CI)aExp. (β)bP Valueβ Log-Transformed (95% CI)aExp. (β)bP Value
    Visual collateral score per 1 point−0.49 (−0.61 to −0.37)0.60<.001−0.59 (−0.71 to −0.47)0.54<.001
    Quantitative collateral score per 10%−0.13 (−0.16 to −0.099)0.88<.001−0.14 (−0.18 to −0.11)0.87<.001
    • Note:—Exp. (β) indicates exponent of β.

    • ↵a Due to the non-normal distribution of follow-up infarct volume, a log +1 transformation was performed to best fit the assumptions associated with the linear regression model.

    • ↵b Exponent of β was calculated to determine the relative difference of follow-up infarct volume with an increase in collateral scores.

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    Table 4:

    Results of adjusted and unadjusted regression analyses for the effect of collateral capacity on modified Rankin Scale

    AdjustedUnadjusted
    Odds Ratio (95% CI)P ValueOdds Ratio (95% CI)P Value
    Visual collateral score per 1 point0.61 (0.50–0.75)<.0010.51 (0.42–0.62)<.001
    Quantitative collateral score per 10%0.81 (0.77–0.86)<.0010.85 (0.81–0.90)<.001
    • View popup
    Table 5:

    P values of interaction analysis for primary and secondary outcome measures

    FIV (Continuous)FIV ≤90 mL vs FIV >90 mLmRS (Ordinal)mRS 0–2 vs 3–6
    vCS-unadjusted analysis.40.43.23.11
    vCS-adjusted analysis.60.54.10.075
    qCS-unadjusted analysis.15.75.048a.049a
    qCS-adjusted analysis.33.48.081.18
    • ↵a P < .05, 2-sided.

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A.M.M. Boers, R. Sales Barros, I.G.H. Jansen, O.A. Berkhemer, L.F.M. Beenen, B.K. Menon, D.W.J. Dippel, A. van der Lugt, W.H. van Zwam, Y.B.W.E.M. Roos, R.J. van Oostenbrugge, C.H. Slump, C.B.L.M. Majoie, H.A. Marquering
Value of Quantitative Collateral Scoring on CT Angiography in Patients with Acute Ischemic Stroke
American Journal of Neuroradiology Apr 2018, DOI: 10.3174/ajnr.A5623

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Value of Quantitative Collateral Scoring on CT Angiography in Patients with Acute Ischemic Stroke
A.M.M. Boers, R. Sales Barros, I.G.H. Jansen, O.A. Berkhemer, L.F.M. Beenen, B.K. Menon, D.W.J. Dippel, A. van der Lugt, W.H. van Zwam, Y.B.W.E.M. Roos, R.J. van Oostenbrugge, C.H. Slump, C.B.L.M. Majoie, H.A. Marquering
American Journal of Neuroradiology Apr 2018, DOI: 10.3174/ajnr.A5623
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