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Research ArticleNeurointervention

Angiographic Assessment of Pial Collaterals as a Prognostic Indicator Following Intra-arterial Thrombolysis for Acute Ischemic Stroke

Gregory A. Christoforidis, Yousef Mohammad, Dimitris Kehagias, Bindu Avutu and Andrew P. Slivka
American Journal of Neuroradiology August 2005, 26 (7) 1789-1797;
Gregory A. Christoforidis
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Yousef Mohammad
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Dimitris Kehagias
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Bindu Avutu
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Andrew P. Slivka
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  • Fig 1.
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    Fig 1.

    Scoring of the anatomic extent of pial collateral blood flow from the ACA territory to the MCA territory during occlusion of the M1 segment. Scoring corresponds to the angiographically visible retrograde reconstitution of the MCA segments on the delayed venous phase. Each color is depicts the furthest extent of retrograde opacification depicted on anteroposterior cerebral angiograms for each pial collateral score.

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    Fig 2.

    Anteroposterior (A and C) and lateral (B and C) images from a left internal carotid artery angiogram obtained during the early (A and B) and delayed angiographic phases (C and D) in a patient with acute ischemic stroke due to occlusion at the M1 segment (arrow). Note the retrograde opacification of the MCA branches via pial collateral vessels extending from the ACA (arrowheads). Because there is reverse opacification of the MCA extending to the distal M1 segment, a pial collateral formation score of 1 was assigned.

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    TABLE 1:

    Infarct volumes (cm3) distributed according to pial collateral score and recanalization result

    Collateral ScoreCompletea Recanalization Mean (σ, n)Partial and Nob Recanalization Mean (σ, n)Total Mean (σ, n)
    12.53 (2.92, 12)68.55 (53.59, 15)39.23 (51.67, 27)
    232.47 (12.90, 3)41.93 (25.09, 6)38.78 (21.38, 9)
    381.66 (31.13, 5)122.04 (54.83, 5)101.85 (47.11, 10)
    4 and 5154.28 (136.04, 4)392.9 (125.209, 3)256.54 (175.35, 7)
    1 and 28.52 (13.57, 15)60.98 (48.17, 21)39.12 (45.69, 36)
    3–5113.93 (94.27, 9)223.61 (160.78, 8)165.55 (137.61, 17)
        Total48.05 (76.95, 24)105.84 (116.58, 29)79.67 (103.83, 53)
    • a P = .003, Wilcoxon rank sum test for statistically significant increase in infarct volume with increase in pial collateral score.

    • b P =.0067, Wilcoxon rank sum test for statistically significant increase in infarct volume with increase in pial collateral score.

    • View popup
    TABLE 2:

    Clinical outcome (presentation NIHSS, change in NIHSS, discharge NIHSS, and modified Rankin) distribution according to pial collateral score and recanalization

    Pial Collateral ScoreRecanalizationNo.Presentation NIHSS Score Median (Range)Change in NIHSS Score Median (Range)Discharge NIHSS Score Median (Range)Discharge Modified Rankin Scale Score Median (Range)
    1Complete1213.5 (4–23)9.5 (0–15)1.5 (0–19)1.5 (0.5)
    Partial/none1511 (5–30)2 (−12–11)10 (0–30)4 (0–5)
    2Complete316 (14–16)12 (10–16)2 (0–6)2 (0–3)
    Partial/none68.5 (5–21)0 (−6–6)10 (3–20)4 (1–5)
    3Complete516 (12–21)9 (−10–15)6 (3–22)3 (1–5)
    Partial/none517 (15–22)5 (1–9)14 (8–18)4 (4–4)
    4 and 5Complete413.5 (7–26)1 (−16–5)10.5 (6–42)4.5 (4–6)
    Partial/none319 (17–29)0 (−25–4)25 (19–42)5 (4–6)
        TotalComplete2415 (4–26)9 (−16–16)5 (0–42)3 (0–6)
    Partial/none2915 (0–30)2 (−25–11)11 (0–42)4 (0–6)
    • View popup
    TABLE 3:

    Infarct volume (cm3) distribution according to pial collateral score, occlusion site, and recanalization

    Collateral ScoreComplete RecanalizationPartial/No RecanalizationCombined
    ProximalDistalProximalDistalProximalDistal
    Mean (σ, n)Mean (σ, n)Mean (σ, n)Mean (σ, n)Mean (σ, n)Mean (σ, n)
    1 and 2*9.4†6.2‡68.3a49.241.334.83
    (14.7, 11)(11.3, 4)(50.7, 13)(44.4, 8)(48.3, 24)(41.7, 12)
    3–5*153.0†82.7‡247.7a55.1213.378.1
    (66.7, 4)(40.00, 5)(157.3, 7)(na, 1)(149.9, 11)(38.4, 6)
        Total47.748.7131.149.895.349.2
    (91.1, 15)(50.1, 9)(131.0, 20)(41.5, 9)(121.4, 35)(44.7, 18)
    • a Unable to prove statistical significance.

    • * P = .0040, Wilcoxon rank sum test.

    • † P = .0139, Wilcoxon rank sum test.

    • ‡ P = .0023, Wilcoxon rank sum test.

    • View popup
    TABLE 4:

    Linear regression analysis model performed with significant predictive factors for infarct volume (age per year, high collateral score, distal occlusion site, and complete recanalization)

    Predictive FactorEstimateaStandard Errort ratioP > |t|
    Age per year1.9070.662.880.0059
    High collateral score130.7321.216.16<0.0001
    Distal occlusion site−46.5320.80−2.240.030
    Complete recanalization−72.4920.80−3.840.0007
    Intercept45.7150.720.900.37
    • Note.—F ratio, 15.43; P > F < 0.0001; root square = 0.563; root mean square error = 71.48.

    • a Estimates indicate change in infarct volume based on indicated predictive factors. For example, high collateral score (3–5) is estimated to increase infarct value by 130.73 cm3.

    • View popup
    TABLE 5:

    Linear regression analysis model performed only with significant predictive factors for discharge NIHSS score (age per year, high collateral score, and complete recanalization)

    Predictive FactorEstimateStandard Errort ratioP > |t|
    Age per year0.2470.0683.63.0007
    High collateral score7.732.183.54.0009
    Complete recanalization7.532.053.68.0006
    Intercept3.004.950.61.547
    • Note.—NIHSS was considered as a continuous variable for the purpose of this analysis.

    • View popup
    TABLE 6:

    Multivariate logistic regression analysis model for poor outcome (modified Rankin scale score > 2) performed with predictive factors (age per year, high collateral score, and complete recanalization)

    Predictive FactorEstimateStandard Errorχ2P > χ2
    Age per year−0.06200.03064.10.0429
    High collateral score3.271.2996.33.0119
    Complete recanalization2.650.8908.88.0029
    Intercept−1.0191.870.30.586
    • Note.—Whole model test: R2 = 0.3476; P < .0001.

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American Journal of Neuroradiology: 26 (7)
American Journal of Neuroradiology
Vol. 26, Issue 7
1 Aug 2005
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Gregory A. Christoforidis, Yousef Mohammad, Dimitris Kehagias, Bindu Avutu, Andrew P. Slivka
Angiographic Assessment of Pial Collaterals as a Prognostic Indicator Following Intra-arterial Thrombolysis for Acute Ischemic Stroke
American Journal of Neuroradiology Aug 2005, 26 (7) 1789-1797;

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Angiographic Assessment of Pial Collaterals as a Prognostic Indicator Following Intra-arterial Thrombolysis for Acute Ischemic Stroke
Gregory A. Christoforidis, Yousef Mohammad, Dimitris Kehagias, Bindu Avutu, Andrew P. Slivka
American Journal of Neuroradiology Aug 2005, 26 (7) 1789-1797;
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