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Research ArticleAdult Brain

FLAIR Vascular Hyperintensities as a Surrogate of Collaterals in Acute Stroke: DWI Matters

L. Legrand, A. Le Berre, P. Seners, J. Benzakoun, W. Ben Hassen, S. Lion, G. Boulouis, J.-P. Cottier, V. Costalat, S. Bracard, Y. Berthezene, C. Ozsancak, C. Provost, O. Naggara, J.-C. Baron, G. Turc, C. Oppenheim and On behalf of the PREDICT-RECANAL Collaborators
American Journal of Neuroradiology January 2023, 44 (1) 26-32; DOI: https://doi.org/10.3174/ajnr.A7733
L. Legrand
aFrom the Institute of Psychiatry and Neuroscience of Paris (L.L., A.L.B., J.B., W.B.H., C.P., O.N., J.-C.B., G.T., C. Oppenheim), Université Paris Cité, Institut National de la Santé et de la Recherche Médicale U1266, Federation Hospitalo-Universitaire NeuroVasc, Paris, France
bDepartments of Neuroradiology (L.L., A.L.B., J.B., W.B.H., C.P., O.N., C. Oppenheim)
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A. Le Berre
aFrom the Institute of Psychiatry and Neuroscience of Paris (L.L., A.L.B., J.B., W.B.H., C.P., O.N., J.-C.B., G.T., C. Oppenheim), Université Paris Cité, Institut National de la Santé et de la Recherche Médicale U1266, Federation Hospitalo-Universitaire NeuroVasc, Paris, France
bDepartments of Neuroradiology (L.L., A.L.B., J.B., W.B.H., C.P., O.N., C. Oppenheim)
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P. Seners
dDepartment of Neurology (P.S.), Hôpital Fondation Rothschild, Paris, France
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J. Benzakoun
aFrom the Institute of Psychiatry and Neuroscience of Paris (L.L., A.L.B., J.B., W.B.H., C.P., O.N., J.-C.B., G.T., C. Oppenheim), Université Paris Cité, Institut National de la Santé et de la Recherche Médicale U1266, Federation Hospitalo-Universitaire NeuroVasc, Paris, France
bDepartments of Neuroradiology (L.L., A.L.B., J.B., W.B.H., C.P., O.N., C. Oppenheim)
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W. Ben Hassen
aFrom the Institute of Psychiatry and Neuroscience of Paris (L.L., A.L.B., J.B., W.B.H., C.P., O.N., J.-C.B., G.T., C. Oppenheim), Université Paris Cité, Institut National de la Santé et de la Recherche Médicale U1266, Federation Hospitalo-Universitaire NeuroVasc, Paris, France
bDepartments of Neuroradiology (L.L., A.L.B., J.B., W.B.H., C.P., O.N., C. Oppenheim)
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S. Lion
eEdmus Services (S.L.), Fondation Edmus, Lyon, France
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G. Boulouis
fDepartment of Diagnostic and Interventional Neuroradiology (G.B., J-.P.C.), Bretonneau Hospital, University of Tours, Institut National de la Santé et de la Recherche Médicale 1253 iBrain, Tours, France
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J.-P. Cottier
fDepartment of Diagnostic and Interventional Neuroradiology (G.B., J-.P.C.), Bretonneau Hospital, University of Tours, Institut National de la Santé et de la Recherche Médicale 1253 iBrain, Tours, France
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V. Costalat
gDepartment of Interventional Neuroradiology (V.C.), Centre Hospitalier Regional Universitaire Gui de Chauliac, Montpellier, France
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S. Bracard
hDepartment of Diagnostic and Interventional Neuroradiology (S.B.), University Hospital of Nancy, Institut National de la Santé et de la Recherche Médicale U947, Nancy, France
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Y. Berthezene
iDepartment of Neuroradiology (Y.B.), Hospices Civils de Lyon, Lyon, France
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C. Ozsancak
jDepartment of Neurology (C. Ozsancak), Orleans Hospital, Orleans, France
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C. Provost
aFrom the Institute of Psychiatry and Neuroscience of Paris (L.L., A.L.B., J.B., W.B.H., C.P., O.N., J.-C.B., G.T., C. Oppenheim), Université Paris Cité, Institut National de la Santé et de la Recherche Médicale U1266, Federation Hospitalo-Universitaire NeuroVasc, Paris, France
bDepartments of Neuroradiology (L.L., A.L.B., J.B., W.B.H., C.P., O.N., C. Oppenheim)
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O. Naggara
aFrom the Institute of Psychiatry and Neuroscience of Paris (L.L., A.L.B., J.B., W.B.H., C.P., O.N., J.-C.B., G.T., C. Oppenheim), Université Paris Cité, Institut National de la Santé et de la Recherche Médicale U1266, Federation Hospitalo-Universitaire NeuroVasc, Paris, France
bDepartments of Neuroradiology (L.L., A.L.B., J.B., W.B.H., C.P., O.N., C. Oppenheim)
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J.-C. Baron
aFrom the Institute of Psychiatry and Neuroscience of Paris (L.L., A.L.B., J.B., W.B.H., C.P., O.N., J.-C.B., G.T., C. Oppenheim), Université Paris Cité, Institut National de la Santé et de la Recherche Médicale U1266, Federation Hospitalo-Universitaire NeuroVasc, Paris, France
cNeurology (J.-C.B., G.T.), Groupe Hospitalier Universitaire-Paris Psychiatrie et Neurosciences, Sainte-Anne Hospital, Paris, France
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G. Turc
aFrom the Institute of Psychiatry and Neuroscience of Paris (L.L., A.L.B., J.B., W.B.H., C.P., O.N., J.-C.B., G.T., C. Oppenheim), Université Paris Cité, Institut National de la Santé et de la Recherche Médicale U1266, Federation Hospitalo-Universitaire NeuroVasc, Paris, France
cNeurology (J.-C.B., G.T.), Groupe Hospitalier Universitaire-Paris Psychiatrie et Neurosciences, Sainte-Anne Hospital, Paris, France
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C. Oppenheim
aFrom the Institute of Psychiatry and Neuroscience of Paris (L.L., A.L.B., J.B., W.B.H., C.P., O.N., J.-C.B., G.T., C. Oppenheim), Université Paris Cité, Institut National de la Santé et de la Recherche Médicale U1266, Federation Hospitalo-Universitaire NeuroVasc, Paris, France
bDepartments of Neuroradiology (L.L., A.L.B., J.B., W.B.H., C.P., O.N., C. Oppenheim)
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    FIG 1.

    Illustrative case of good collaterals. MR imaging of a patient around 60 years of age obtained 108 minutes after stroke onset. Hyperintense lesions in the left MCA territory on admission DWI (A) and FVH on admission FLAIR (B), with FVHASPECTS of 5 and FVH-DWI mismatchASPECTS of 4. Grade 4 collaterals on early phase (C), mid phase (D), and late phase (E) of collateral flow maps (subtracted dynamic susceptibility contrast perfusion imaging). Note complete and rapid (from mid phase) collateral blood flow to the vascular bed in the entire ischemic territory by retrograde perfusion.

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    FIG 2.

    Illustrative case of poor collaterals. MR imaging of a patient around 70 years of age obtained 83 minutes after stroke onset. Hyperintense lesions in the left MCA territory on admission DWI (A) and FVH on admission FLAIR (B), with FVHASPECTS of 6 and FVH-DWI mismatchASPECTS of 1. Grade 2 collaterals on early phase (C), mid phase (D), and late phase (E) of collateral flow maps (subtracted dynamic susceptibility contrast perfusion imaging). Note rapid collaterals to the periphery of ischemic site with persistence of some of the defect (arrowheads).

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    FIG 3.

    ROC curves of FVH-DWI mismatchASPECTS (blue) and FVHASPECTS (red) to predict good (grades 3–4) collaterals. The area under the ROC curve was higher for FVH-DWI mismatchASPECTS (0.80; 95% CI, 0.74–0.87) than for FVHASPECTS (0.52; 95% CI, 0.44–0.60), P < .001 for comparison.

Tables

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  • Baseline characteristics of the population and univariate relationships with collateral gradea

    Whole Cohort (n = 209)Good Collaterals (Grades 3 and 4) (n = 133)Poor Collaterals (Grades 1 and 2) (n = 76)P Value
    Patient characteristics
     Age (yr)72 (61–80)72 (61–81)71 (60–80).39
     Men118 (56)73 (55)45 (59).54
     Hypertension118 (56)80 (60)38 (50).16
     Diabetes mellitus32 (15)23 (17)9 (12).29
     Current smoking26 (12)15 (11)11 (14).50
    Pre-IVT characteristics
     NIHSS score16 (9–19.5)14 (7–18)17 (14–21)<.001
     Onset-to-IVT time (min)160 (130–193.5)158 (127–195)161 (135–186).67
    Pre-IVT MRI
     Onset-to-MRI time (min)123 (96–154)122 (94–159)124 (101–154).74
     Occlusion site.26
      ICA-T/L36 (17)22 (17)14 (18)
      M1124 (60)75 (56)49 (65)
      M249 (23)36 (27)13 (17)
     DWI volume (mL)12 (5–25)8 (2–13)33 (16–54)<.001
     PWI volumes (mL)
      Tmax > 4 s133 (83–187)119 (70–168)176 (114–209)<.001
      Tmax > 6 s83 (44–127)64 (35–108)119 (71–166)<.001
      Tmax > 10 s31 (13–63)18 (8–44)61 (34–95)<.001
     HIR0.43 (0.30–0.53)0.36 (0.22–0.45)0.53 (0.46–0.62)<.001
     PWI-DWI mismatch profile186 (91%)127 (96%)59 (81%)<.001
     Mismatch ratio5.6 (3.0–11.1)8.2 (4.4–18.7)3.2 (2.0–5.0).001
     FVH-DWI mismatchASPECTS3 (2–5)4 (3–5)2 (0–2.75)<.001
     FVHASPECTS5 (4–5)5 (4–5.5)5 (4–5).76
    • Note:—HIR indicates Tmax > 10-second/Tmax > 6-second volume; ICA-T/L, ICA T or L occlusion; Mismatch ratio, Tmax > 6-second volume/DWI volume; PWI-DWI mismatch profile, Tmax > 6-second volume >1.8 × DWI volume.

    • ↵a Categoric variables are expressed as number (%), and continuous variables, as median (IQR). Four patients had missing PWI volume data (1 patient with good collaterals and 3 patients with poor collaterals).

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L. Legrand, A. Le Berre, P. Seners, J. Benzakoun, W. Ben Hassen, S. Lion, G. Boulouis, J.-P. Cottier, V. Costalat, S. Bracard, Y. Berthezene, C. Ozsancak, C. Provost, O. Naggara, J.-C. Baron, G. Turc, C. Oppenheim, On behalf of the PREDICT-RECANAL Collaborators
FLAIR Vascular Hyperintensities as a Surrogate of Collaterals in Acute Stroke: DWI Matters
American Journal of Neuroradiology Jan 2023, 44 (1) 26-32; DOI: 10.3174/ajnr.A7733

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FLAIR Hyperintensities and Collaterals in Stroke
L. Legrand, A. Le Berre, P. Seners, J. Benzakoun, W. Ben Hassen, S. Lion, G. Boulouis, J.-P. Cottier, V. Costalat, S. Bracard, Y. Berthezene, C. Ozsancak, C. Provost, O. Naggara, J.-C. Baron, G. Turc, C. Oppenheim, On behalf of the PREDICT-RECANAL Collaborators
American Journal of Neuroradiology Jan 2023, 44 (1) 26-32; DOI: 10.3174/ajnr.A7733
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