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January 25, 2022; 98 (4) Research Article

Cerebrovascular Collateral Integrity in Pediatric Large Vessel Occlusion

Analysis of the Save ChildS Study

View ORCID ProfileSarah Lee, Bin Jiang, Max Wintermark, Michael Mlynash, Soren Christensen, Ronald Sträter, Gabriel Broocks, Astrid Grams, Franziska Dorn, View ORCID ProfileOmid Nikoubashman, View ORCID ProfileDaniel Kaiser, Andrea Morotti, Ulf Jensen-Kondering, View ORCID ProfileJohannes Trenkler, Markus Möhlenbruch, View ORCID ProfileJens Fiehler, Moritz Wildgruber, André Kemmling, Marios Psychogios, Peter B. Sporns, on behalf of Save ChildS Investigators
First published November 18, 2021, DOI: https://doi.org/10.1212/WNL.0000000000013081
Sarah Lee
From the Department of Neurology & Neurological Sciences, Stanford Stroke Center (S.L., M. Mlynash, S.C.), Department of Neurology & Neurological Sciences (S.L.), Division of Child Neurology, and Department of Radiology (B.J., M. Wintermark), Division of Neuroradiology, Stanford University School of Medicine, CA; Department of Pediatrics (R.S.), University Hospital of Muenster; Department of Diagnostic and Interventional Neuroradiology (G.B., J.F., P.B.S.), University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Department of Neuroradiology (A.G.), Medical University of Innsbruck, Austria; Department of Neuroradiology (F.D.), University Hospital Bonn; Department of Neuroradiology (O.N.), RWTH Aachen University; Department of Neuroradiology (D.K.), University Hospital Carl Gustav Carus, Dresden, Germany; ASST Valcamonica (A.M.), UOSD Neurology, Esine (BS), Brescia, Italy; Department of Radiology and Neuroradiology (U.J.-K.), University Hospital of Schleswig-Holstein, Campus Kiel; Institute of Neuroradiology (U.J.-K.), UKSH Campus Lübeck, Germany; Department of Neuroradiology (J.T.), Kepler University Hospital, Johannes Kepler University Linz, Austria; Department of Neuroradiology (M. Möhlenbruch), Heidelberg University Hospital; Department of Radiology (M. Wildgruber), University Hospital, LMU Munich; Department of Neuroradiology (A.K.), Marburg University Hospital, Germany; and Department of Neuroradiology (M.P., P.B.S.), Clinic for Radiology & Nuclear Medicine, University Hospital Basel, Switzerland.
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Bin Jiang
From the Department of Neurology & Neurological Sciences, Stanford Stroke Center (S.L., M. Mlynash, S.C.), Department of Neurology & Neurological Sciences (S.L.), Division of Child Neurology, and Department of Radiology (B.J., M. Wintermark), Division of Neuroradiology, Stanford University School of Medicine, CA; Department of Pediatrics (R.S.), University Hospital of Muenster; Department of Diagnostic and Interventional Neuroradiology (G.B., J.F., P.B.S.), University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Department of Neuroradiology (A.G.), Medical University of Innsbruck, Austria; Department of Neuroradiology (F.D.), University Hospital Bonn; Department of Neuroradiology (O.N.), RWTH Aachen University; Department of Neuroradiology (D.K.), University Hospital Carl Gustav Carus, Dresden, Germany; ASST Valcamonica (A.M.), UOSD Neurology, Esine (BS), Brescia, Italy; Department of Radiology and Neuroradiology (U.J.-K.), University Hospital of Schleswig-Holstein, Campus Kiel; Institute of Neuroradiology (U.J.-K.), UKSH Campus Lübeck, Germany; Department of Neuroradiology (J.T.), Kepler University Hospital, Johannes Kepler University Linz, Austria; Department of Neuroradiology (M. Möhlenbruch), Heidelberg University Hospital; Department of Radiology (M. Wildgruber), University Hospital, LMU Munich; Department of Neuroradiology (A.K.), Marburg University Hospital, Germany; and Department of Neuroradiology (M.P., P.B.S.), Clinic for Radiology & Nuclear Medicine, University Hospital Basel, Switzerland.
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Max Wintermark
From the Department of Neurology & Neurological Sciences, Stanford Stroke Center (S.L., M. Mlynash, S.C.), Department of Neurology & Neurological Sciences (S.L.), Division of Child Neurology, and Department of Radiology (B.J., M. Wintermark), Division of Neuroradiology, Stanford University School of Medicine, CA; Department of Pediatrics (R.S.), University Hospital of Muenster; Department of Diagnostic and Interventional Neuroradiology (G.B., J.F., P.B.S.), University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Department of Neuroradiology (A.G.), Medical University of Innsbruck, Austria; Department of Neuroradiology (F.D.), University Hospital Bonn; Department of Neuroradiology (O.N.), RWTH Aachen University; Department of Neuroradiology (D.K.), University Hospital Carl Gustav Carus, Dresden, Germany; ASST Valcamonica (A.M.), UOSD Neurology, Esine (BS), Brescia, Italy; Department of Radiology and Neuroradiology (U.J.-K.), University Hospital of Schleswig-Holstein, Campus Kiel; Institute of Neuroradiology (U.J.-K.), UKSH Campus Lübeck, Germany; Department of Neuroradiology (J.T.), Kepler University Hospital, Johannes Kepler University Linz, Austria; Department of Neuroradiology (M. Möhlenbruch), Heidelberg University Hospital; Department of Radiology (M. Wildgruber), University Hospital, LMU Munich; Department of Neuroradiology (A.K.), Marburg University Hospital, Germany; and Department of Neuroradiology (M.P., P.B.S.), Clinic for Radiology & Nuclear Medicine, University Hospital Basel, Switzerland.
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Michael Mlynash
From the Department of Neurology & Neurological Sciences, Stanford Stroke Center (S.L., M. Mlynash, S.C.), Department of Neurology & Neurological Sciences (S.L.), Division of Child Neurology, and Department of Radiology (B.J., M. Wintermark), Division of Neuroradiology, Stanford University School of Medicine, CA; Department of Pediatrics (R.S.), University Hospital of Muenster; Department of Diagnostic and Interventional Neuroradiology (G.B., J.F., P.B.S.), University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Department of Neuroradiology (A.G.), Medical University of Innsbruck, Austria; Department of Neuroradiology (F.D.), University Hospital Bonn; Department of Neuroradiology (O.N.), RWTH Aachen University; Department of Neuroradiology (D.K.), University Hospital Carl Gustav Carus, Dresden, Germany; ASST Valcamonica (A.M.), UOSD Neurology, Esine (BS), Brescia, Italy; Department of Radiology and Neuroradiology (U.J.-K.), University Hospital of Schleswig-Holstein, Campus Kiel; Institute of Neuroradiology (U.J.-K.), UKSH Campus Lübeck, Germany; Department of Neuroradiology (J.T.), Kepler University Hospital, Johannes Kepler University Linz, Austria; Department of Neuroradiology (M. Möhlenbruch), Heidelberg University Hospital; Department of Radiology (M. Wildgruber), University Hospital, LMU Munich; Department of Neuroradiology (A.K.), Marburg University Hospital, Germany; and Department of Neuroradiology (M.P., P.B.S.), Clinic for Radiology & Nuclear Medicine, University Hospital Basel, Switzerland.
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Soren Christensen
From the Department of Neurology & Neurological Sciences, Stanford Stroke Center (S.L., M. Mlynash, S.C.), Department of Neurology & Neurological Sciences (S.L.), Division of Child Neurology, and Department of Radiology (B.J., M. Wintermark), Division of Neuroradiology, Stanford University School of Medicine, CA; Department of Pediatrics (R.S.), University Hospital of Muenster; Department of Diagnostic and Interventional Neuroradiology (G.B., J.F., P.B.S.), University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Department of Neuroradiology (A.G.), Medical University of Innsbruck, Austria; Department of Neuroradiology (F.D.), University Hospital Bonn; Department of Neuroradiology (O.N.), RWTH Aachen University; Department of Neuroradiology (D.K.), University Hospital Carl Gustav Carus, Dresden, Germany; ASST Valcamonica (A.M.), UOSD Neurology, Esine (BS), Brescia, Italy; Department of Radiology and Neuroradiology (U.J.-K.), University Hospital of Schleswig-Holstein, Campus Kiel; Institute of Neuroradiology (U.J.-K.), UKSH Campus Lübeck, Germany; Department of Neuroradiology (J.T.), Kepler University Hospital, Johannes Kepler University Linz, Austria; Department of Neuroradiology (M. Möhlenbruch), Heidelberg University Hospital; Department of Radiology (M. Wildgruber), University Hospital, LMU Munich; Department of Neuroradiology (A.K.), Marburg University Hospital, Germany; and Department of Neuroradiology (M.P., P.B.S.), Clinic for Radiology & Nuclear Medicine, University Hospital Basel, Switzerland.
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Ronald Sträter
From the Department of Neurology & Neurological Sciences, Stanford Stroke Center (S.L., M. Mlynash, S.C.), Department of Neurology & Neurological Sciences (S.L.), Division of Child Neurology, and Department of Radiology (B.J., M. Wintermark), Division of Neuroradiology, Stanford University School of Medicine, CA; Department of Pediatrics (R.S.), University Hospital of Muenster; Department of Diagnostic and Interventional Neuroradiology (G.B., J.F., P.B.S.), University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Department of Neuroradiology (A.G.), Medical University of Innsbruck, Austria; Department of Neuroradiology (F.D.), University Hospital Bonn; Department of Neuroradiology (O.N.), RWTH Aachen University; Department of Neuroradiology (D.K.), University Hospital Carl Gustav Carus, Dresden, Germany; ASST Valcamonica (A.M.), UOSD Neurology, Esine (BS), Brescia, Italy; Department of Radiology and Neuroradiology (U.J.-K.), University Hospital of Schleswig-Holstein, Campus Kiel; Institute of Neuroradiology (U.J.-K.), UKSH Campus Lübeck, Germany; Department of Neuroradiology (J.T.), Kepler University Hospital, Johannes Kepler University Linz, Austria; Department of Neuroradiology (M. Möhlenbruch), Heidelberg University Hospital; Department of Radiology (M. Wildgruber), University Hospital, LMU Munich; Department of Neuroradiology (A.K.), Marburg University Hospital, Germany; and Department of Neuroradiology (M.P., P.B.S.), Clinic for Radiology & Nuclear Medicine, University Hospital Basel, Switzerland.
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Gabriel Broocks
From the Department of Neurology & Neurological Sciences, Stanford Stroke Center (S.L., M. Mlynash, S.C.), Department of Neurology & Neurological Sciences (S.L.), Division of Child Neurology, and Department of Radiology (B.J., M. Wintermark), Division of Neuroradiology, Stanford University School of Medicine, CA; Department of Pediatrics (R.S.), University Hospital of Muenster; Department of Diagnostic and Interventional Neuroradiology (G.B., J.F., P.B.S.), University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Department of Neuroradiology (A.G.), Medical University of Innsbruck, Austria; Department of Neuroradiology (F.D.), University Hospital Bonn; Department of Neuroradiology (O.N.), RWTH Aachen University; Department of Neuroradiology (D.K.), University Hospital Carl Gustav Carus, Dresden, Germany; ASST Valcamonica (A.M.), UOSD Neurology, Esine (BS), Brescia, Italy; Department of Radiology and Neuroradiology (U.J.-K.), University Hospital of Schleswig-Holstein, Campus Kiel; Institute of Neuroradiology (U.J.-K.), UKSH Campus Lübeck, Germany; Department of Neuroradiology (J.T.), Kepler University Hospital, Johannes Kepler University Linz, Austria; Department of Neuroradiology (M. Möhlenbruch), Heidelberg University Hospital; Department of Radiology (M. Wildgruber), University Hospital, LMU Munich; Department of Neuroradiology (A.K.), Marburg University Hospital, Germany; and Department of Neuroradiology (M.P., P.B.S.), Clinic for Radiology & Nuclear Medicine, University Hospital Basel, Switzerland.
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Astrid Grams
From the Department of Neurology & Neurological Sciences, Stanford Stroke Center (S.L., M. Mlynash, S.C.), Department of Neurology & Neurological Sciences (S.L.), Division of Child Neurology, and Department of Radiology (B.J., M. Wintermark), Division of Neuroradiology, Stanford University School of Medicine, CA; Department of Pediatrics (R.S.), University Hospital of Muenster; Department of Diagnostic and Interventional Neuroradiology (G.B., J.F., P.B.S.), University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Department of Neuroradiology (A.G.), Medical University of Innsbruck, Austria; Department of Neuroradiology (F.D.), University Hospital Bonn; Department of Neuroradiology (O.N.), RWTH Aachen University; Department of Neuroradiology (D.K.), University Hospital Carl Gustav Carus, Dresden, Germany; ASST Valcamonica (A.M.), UOSD Neurology, Esine (BS), Brescia, Italy; Department of Radiology and Neuroradiology (U.J.-K.), University Hospital of Schleswig-Holstein, Campus Kiel; Institute of Neuroradiology (U.J.-K.), UKSH Campus Lübeck, Germany; Department of Neuroradiology (J.T.), Kepler University Hospital, Johannes Kepler University Linz, Austria; Department of Neuroradiology (M. Möhlenbruch), Heidelberg University Hospital; Department of Radiology (M. Wildgruber), University Hospital, LMU Munich; Department of Neuroradiology (A.K.), Marburg University Hospital, Germany; and Department of Neuroradiology (M.P., P.B.S.), Clinic for Radiology & Nuclear Medicine, University Hospital Basel, Switzerland.
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Franziska Dorn
From the Department of Neurology & Neurological Sciences, Stanford Stroke Center (S.L., M. Mlynash, S.C.), Department of Neurology & Neurological Sciences (S.L.), Division of Child Neurology, and Department of Radiology (B.J., M. Wintermark), Division of Neuroradiology, Stanford University School of Medicine, CA; Department of Pediatrics (R.S.), University Hospital of Muenster; Department of Diagnostic and Interventional Neuroradiology (G.B., J.F., P.B.S.), University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Department of Neuroradiology (A.G.), Medical University of Innsbruck, Austria; Department of Neuroradiology (F.D.), University Hospital Bonn; Department of Neuroradiology (O.N.), RWTH Aachen University; Department of Neuroradiology (D.K.), University Hospital Carl Gustav Carus, Dresden, Germany; ASST Valcamonica (A.M.), UOSD Neurology, Esine (BS), Brescia, Italy; Department of Radiology and Neuroradiology (U.J.-K.), University Hospital of Schleswig-Holstein, Campus Kiel; Institute of Neuroradiology (U.J.-K.), UKSH Campus Lübeck, Germany; Department of Neuroradiology (J.T.), Kepler University Hospital, Johannes Kepler University Linz, Austria; Department of Neuroradiology (M. Möhlenbruch), Heidelberg University Hospital; Department of Radiology (M. Wildgruber), University Hospital, LMU Munich; Department of Neuroradiology (A.K.), Marburg University Hospital, Germany; and Department of Neuroradiology (M.P., P.B.S.), Clinic for Radiology & Nuclear Medicine, University Hospital Basel, Switzerland.
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Omid Nikoubashman
From the Department of Neurology & Neurological Sciences, Stanford Stroke Center (S.L., M. Mlynash, S.C.), Department of Neurology & Neurological Sciences (S.L.), Division of Child Neurology, and Department of Radiology (B.J., M. Wintermark), Division of Neuroradiology, Stanford University School of Medicine, CA; Department of Pediatrics (R.S.), University Hospital of Muenster; Department of Diagnostic and Interventional Neuroradiology (G.B., J.F., P.B.S.), University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Department of Neuroradiology (A.G.), Medical University of Innsbruck, Austria; Department of Neuroradiology (F.D.), University Hospital Bonn; Department of Neuroradiology (O.N.), RWTH Aachen University; Department of Neuroradiology (D.K.), University Hospital Carl Gustav Carus, Dresden, Germany; ASST Valcamonica (A.M.), UOSD Neurology, Esine (BS), Brescia, Italy; Department of Radiology and Neuroradiology (U.J.-K.), University Hospital of Schleswig-Holstein, Campus Kiel; Institute of Neuroradiology (U.J.-K.), UKSH Campus Lübeck, Germany; Department of Neuroradiology (J.T.), Kepler University Hospital, Johannes Kepler University Linz, Austria; Department of Neuroradiology (M. Möhlenbruch), Heidelberg University Hospital; Department of Radiology (M. Wildgruber), University Hospital, LMU Munich; Department of Neuroradiology (A.K.), Marburg University Hospital, Germany; and Department of Neuroradiology (M.P., P.B.S.), Clinic for Radiology & Nuclear Medicine, University Hospital Basel, Switzerland.
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Daniel Kaiser
From the Department of Neurology & Neurological Sciences, Stanford Stroke Center (S.L., M. Mlynash, S.C.), Department of Neurology & Neurological Sciences (S.L.), Division of Child Neurology, and Department of Radiology (B.J., M. Wintermark), Division of Neuroradiology, Stanford University School of Medicine, CA; Department of Pediatrics (R.S.), University Hospital of Muenster; Department of Diagnostic and Interventional Neuroradiology (G.B., J.F., P.B.S.), University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Department of Neuroradiology (A.G.), Medical University of Innsbruck, Austria; Department of Neuroradiology (F.D.), University Hospital Bonn; Department of Neuroradiology (O.N.), RWTH Aachen University; Department of Neuroradiology (D.K.), University Hospital Carl Gustav Carus, Dresden, Germany; ASST Valcamonica (A.M.), UOSD Neurology, Esine (BS), Brescia, Italy; Department of Radiology and Neuroradiology (U.J.-K.), University Hospital of Schleswig-Holstein, Campus Kiel; Institute of Neuroradiology (U.J.-K.), UKSH Campus Lübeck, Germany; Department of Neuroradiology (J.T.), Kepler University Hospital, Johannes Kepler University Linz, Austria; Department of Neuroradiology (M. Möhlenbruch), Heidelberg University Hospital; Department of Radiology (M. Wildgruber), University Hospital, LMU Munich; Department of Neuroradiology (A.K.), Marburg University Hospital, Germany; and Department of Neuroradiology (M.P., P.B.S.), Clinic for Radiology & Nuclear Medicine, University Hospital Basel, Switzerland.
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Andrea Morotti
From the Department of Neurology & Neurological Sciences, Stanford Stroke Center (S.L., M. Mlynash, S.C.), Department of Neurology & Neurological Sciences (S.L.), Division of Child Neurology, and Department of Radiology (B.J., M. Wintermark), Division of Neuroradiology, Stanford University School of Medicine, CA; Department of Pediatrics (R.S.), University Hospital of Muenster; Department of Diagnostic and Interventional Neuroradiology (G.B., J.F., P.B.S.), University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Department of Neuroradiology (A.G.), Medical University of Innsbruck, Austria; Department of Neuroradiology (F.D.), University Hospital Bonn; Department of Neuroradiology (O.N.), RWTH Aachen University; Department of Neuroradiology (D.K.), University Hospital Carl Gustav Carus, Dresden, Germany; ASST Valcamonica (A.M.), UOSD Neurology, Esine (BS), Brescia, Italy; Department of Radiology and Neuroradiology (U.J.-K.), University Hospital of Schleswig-Holstein, Campus Kiel; Institute of Neuroradiology (U.J.-K.), UKSH Campus Lübeck, Germany; Department of Neuroradiology (J.T.), Kepler University Hospital, Johannes Kepler University Linz, Austria; Department of Neuroradiology (M. Möhlenbruch), Heidelberg University Hospital; Department of Radiology (M. Wildgruber), University Hospital, LMU Munich; Department of Neuroradiology (A.K.), Marburg University Hospital, Germany; and Department of Neuroradiology (M.P., P.B.S.), Clinic for Radiology & Nuclear Medicine, University Hospital Basel, Switzerland.
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Ulf Jensen-Kondering
From the Department of Neurology & Neurological Sciences, Stanford Stroke Center (S.L., M. Mlynash, S.C.), Department of Neurology & Neurological Sciences (S.L.), Division of Child Neurology, and Department of Radiology (B.J., M. Wintermark), Division of Neuroradiology, Stanford University School of Medicine, CA; Department of Pediatrics (R.S.), University Hospital of Muenster; Department of Diagnostic and Interventional Neuroradiology (G.B., J.F., P.B.S.), University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Department of Neuroradiology (A.G.), Medical University of Innsbruck, Austria; Department of Neuroradiology (F.D.), University Hospital Bonn; Department of Neuroradiology (O.N.), RWTH Aachen University; Department of Neuroradiology (D.K.), University Hospital Carl Gustav Carus, Dresden, Germany; ASST Valcamonica (A.M.), UOSD Neurology, Esine (BS), Brescia, Italy; Department of Radiology and Neuroradiology (U.J.-K.), University Hospital of Schleswig-Holstein, Campus Kiel; Institute of Neuroradiology (U.J.-K.), UKSH Campus Lübeck, Germany; Department of Neuroradiology (J.T.), Kepler University Hospital, Johannes Kepler University Linz, Austria; Department of Neuroradiology (M. Möhlenbruch), Heidelberg University Hospital; Department of Radiology (M. Wildgruber), University Hospital, LMU Munich; Department of Neuroradiology (A.K.), Marburg University Hospital, Germany; and Department of Neuroradiology (M.P., P.B.S.), Clinic for Radiology & Nuclear Medicine, University Hospital Basel, Switzerland.
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Johannes Trenkler
From the Department of Neurology & Neurological Sciences, Stanford Stroke Center (S.L., M. Mlynash, S.C.), Department of Neurology & Neurological Sciences (S.L.), Division of Child Neurology, and Department of Radiology (B.J., M. Wintermark), Division of Neuroradiology, Stanford University School of Medicine, CA; Department of Pediatrics (R.S.), University Hospital of Muenster; Department of Diagnostic and Interventional Neuroradiology (G.B., J.F., P.B.S.), University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Department of Neuroradiology (A.G.), Medical University of Innsbruck, Austria; Department of Neuroradiology (F.D.), University Hospital Bonn; Department of Neuroradiology (O.N.), RWTH Aachen University; Department of Neuroradiology (D.K.), University Hospital Carl Gustav Carus, Dresden, Germany; ASST Valcamonica (A.M.), UOSD Neurology, Esine (BS), Brescia, Italy; Department of Radiology and Neuroradiology (U.J.-K.), University Hospital of Schleswig-Holstein, Campus Kiel; Institute of Neuroradiology (U.J.-K.), UKSH Campus Lübeck, Germany; Department of Neuroradiology (J.T.), Kepler University Hospital, Johannes Kepler University Linz, Austria; Department of Neuroradiology (M. Möhlenbruch), Heidelberg University Hospital; Department of Radiology (M. Wildgruber), University Hospital, LMU Munich; Department of Neuroradiology (A.K.), Marburg University Hospital, Germany; and Department of Neuroradiology (M.P., P.B.S.), Clinic for Radiology & Nuclear Medicine, University Hospital Basel, Switzerland.
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Markus Möhlenbruch
From the Department of Neurology & Neurological Sciences, Stanford Stroke Center (S.L., M. Mlynash, S.C.), Department of Neurology & Neurological Sciences (S.L.), Division of Child Neurology, and Department of Radiology (B.J., M. Wintermark), Division of Neuroradiology, Stanford University School of Medicine, CA; Department of Pediatrics (R.S.), University Hospital of Muenster; Department of Diagnostic and Interventional Neuroradiology (G.B., J.F., P.B.S.), University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Department of Neuroradiology (A.G.), Medical University of Innsbruck, Austria; Department of Neuroradiology (F.D.), University Hospital Bonn; Department of Neuroradiology (O.N.), RWTH Aachen University; Department of Neuroradiology (D.K.), University Hospital Carl Gustav Carus, Dresden, Germany; ASST Valcamonica (A.M.), UOSD Neurology, Esine (BS), Brescia, Italy; Department of Radiology and Neuroradiology (U.J.-K.), University Hospital of Schleswig-Holstein, Campus Kiel; Institute of Neuroradiology (U.J.-K.), UKSH Campus Lübeck, Germany; Department of Neuroradiology (J.T.), Kepler University Hospital, Johannes Kepler University Linz, Austria; Department of Neuroradiology (M. Möhlenbruch), Heidelberg University Hospital; Department of Radiology (M. Wildgruber), University Hospital, LMU Munich; Department of Neuroradiology (A.K.), Marburg University Hospital, Germany; and Department of Neuroradiology (M.P., P.B.S.), Clinic for Radiology & Nuclear Medicine, University Hospital Basel, Switzerland.
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Jens Fiehler
From the Department of Neurology & Neurological Sciences, Stanford Stroke Center (S.L., M. Mlynash, S.C.), Department of Neurology & Neurological Sciences (S.L.), Division of Child Neurology, and Department of Radiology (B.J., M. Wintermark), Division of Neuroradiology, Stanford University School of Medicine, CA; Department of Pediatrics (R.S.), University Hospital of Muenster; Department of Diagnostic and Interventional Neuroradiology (G.B., J.F., P.B.S.), University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Department of Neuroradiology (A.G.), Medical University of Innsbruck, Austria; Department of Neuroradiology (F.D.), University Hospital Bonn; Department of Neuroradiology (O.N.), RWTH Aachen University; Department of Neuroradiology (D.K.), University Hospital Carl Gustav Carus, Dresden, Germany; ASST Valcamonica (A.M.), UOSD Neurology, Esine (BS), Brescia, Italy; Department of Radiology and Neuroradiology (U.J.-K.), University Hospital of Schleswig-Holstein, Campus Kiel; Institute of Neuroradiology (U.J.-K.), UKSH Campus Lübeck, Germany; Department of Neuroradiology (J.T.), Kepler University Hospital, Johannes Kepler University Linz, Austria; Department of Neuroradiology (M. Möhlenbruch), Heidelberg University Hospital; Department of Radiology (M. Wildgruber), University Hospital, LMU Munich; Department of Neuroradiology (A.K.), Marburg University Hospital, Germany; and Department of Neuroradiology (M.P., P.B.S.), Clinic for Radiology & Nuclear Medicine, University Hospital Basel, Switzerland.
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Moritz Wildgruber
From the Department of Neurology & Neurological Sciences, Stanford Stroke Center (S.L., M. Mlynash, S.C.), Department of Neurology & Neurological Sciences (S.L.), Division of Child Neurology, and Department of Radiology (B.J., M. Wintermark), Division of Neuroradiology, Stanford University School of Medicine, CA; Department of Pediatrics (R.S.), University Hospital of Muenster; Department of Diagnostic and Interventional Neuroradiology (G.B., J.F., P.B.S.), University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Department of Neuroradiology (A.G.), Medical University of Innsbruck, Austria; Department of Neuroradiology (F.D.), University Hospital Bonn; Department of Neuroradiology (O.N.), RWTH Aachen University; Department of Neuroradiology (D.K.), University Hospital Carl Gustav Carus, Dresden, Germany; ASST Valcamonica (A.M.), UOSD Neurology, Esine (BS), Brescia, Italy; Department of Radiology and Neuroradiology (U.J.-K.), University Hospital of Schleswig-Holstein, Campus Kiel; Institute of Neuroradiology (U.J.-K.), UKSH Campus Lübeck, Germany; Department of Neuroradiology (J.T.), Kepler University Hospital, Johannes Kepler University Linz, Austria; Department of Neuroradiology (M. Möhlenbruch), Heidelberg University Hospital; Department of Radiology (M. Wildgruber), University Hospital, LMU Munich; Department of Neuroradiology (A.K.), Marburg University Hospital, Germany; and Department of Neuroradiology (M.P., P.B.S.), Clinic for Radiology & Nuclear Medicine, University Hospital Basel, Switzerland.
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André Kemmling
From the Department of Neurology & Neurological Sciences, Stanford Stroke Center (S.L., M. Mlynash, S.C.), Department of Neurology & Neurological Sciences (S.L.), Division of Child Neurology, and Department of Radiology (B.J., M. Wintermark), Division of Neuroradiology, Stanford University School of Medicine, CA; Department of Pediatrics (R.S.), University Hospital of Muenster; Department of Diagnostic and Interventional Neuroradiology (G.B., J.F., P.B.S.), University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Department of Neuroradiology (A.G.), Medical University of Innsbruck, Austria; Department of Neuroradiology (F.D.), University Hospital Bonn; Department of Neuroradiology (O.N.), RWTH Aachen University; Department of Neuroradiology (D.K.), University Hospital Carl Gustav Carus, Dresden, Germany; ASST Valcamonica (A.M.), UOSD Neurology, Esine (BS), Brescia, Italy; Department of Radiology and Neuroradiology (U.J.-K.), University Hospital of Schleswig-Holstein, Campus Kiel; Institute of Neuroradiology (U.J.-K.), UKSH Campus Lübeck, Germany; Department of Neuroradiology (J.T.), Kepler University Hospital, Johannes Kepler University Linz, Austria; Department of Neuroradiology (M. Möhlenbruch), Heidelberg University Hospital; Department of Radiology (M. Wildgruber), University Hospital, LMU Munich; Department of Neuroradiology (A.K.), Marburg University Hospital, Germany; and Department of Neuroradiology (M.P., P.B.S.), Clinic for Radiology & Nuclear Medicine, University Hospital Basel, Switzerland.
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Marios Psychogios
From the Department of Neurology & Neurological Sciences, Stanford Stroke Center (S.L., M. Mlynash, S.C.), Department of Neurology & Neurological Sciences (S.L.), Division of Child Neurology, and Department of Radiology (B.J., M. Wintermark), Division of Neuroradiology, Stanford University School of Medicine, CA; Department of Pediatrics (R.S.), University Hospital of Muenster; Department of Diagnostic and Interventional Neuroradiology (G.B., J.F., P.B.S.), University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Department of Neuroradiology (A.G.), Medical University of Innsbruck, Austria; Department of Neuroradiology (F.D.), University Hospital Bonn; Department of Neuroradiology (O.N.), RWTH Aachen University; Department of Neuroradiology (D.K.), University Hospital Carl Gustav Carus, Dresden, Germany; ASST Valcamonica (A.M.), UOSD Neurology, Esine (BS), Brescia, Italy; Department of Radiology and Neuroradiology (U.J.-K.), University Hospital of Schleswig-Holstein, Campus Kiel; Institute of Neuroradiology (U.J.-K.), UKSH Campus Lübeck, Germany; Department of Neuroradiology (J.T.), Kepler University Hospital, Johannes Kepler University Linz, Austria; Department of Neuroradiology (M. Möhlenbruch), Heidelberg University Hospital; Department of Radiology (M. Wildgruber), University Hospital, LMU Munich; Department of Neuroradiology (A.K.), Marburg University Hospital, Germany; and Department of Neuroradiology (M.P., P.B.S.), Clinic for Radiology & Nuclear Medicine, University Hospital Basel, Switzerland.
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Peter B. Sporns
From the Department of Neurology & Neurological Sciences, Stanford Stroke Center (S.L., M. Mlynash, S.C.), Department of Neurology & Neurological Sciences (S.L.), Division of Child Neurology, and Department of Radiology (B.J., M. Wintermark), Division of Neuroradiology, Stanford University School of Medicine, CA; Department of Pediatrics (R.S.), University Hospital of Muenster; Department of Diagnostic and Interventional Neuroradiology (G.B., J.F., P.B.S.), University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Department of Neuroradiology (A.G.), Medical University of Innsbruck, Austria; Department of Neuroradiology (F.D.), University Hospital Bonn; Department of Neuroradiology (O.N.), RWTH Aachen University; Department of Neuroradiology (D.K.), University Hospital Carl Gustav Carus, Dresden, Germany; ASST Valcamonica (A.M.), UOSD Neurology, Esine (BS), Brescia, Italy; Department of Radiology and Neuroradiology (U.J.-K.), University Hospital of Schleswig-Holstein, Campus Kiel; Institute of Neuroradiology (U.J.-K.), UKSH Campus Lübeck, Germany; Department of Neuroradiology (J.T.), Kepler University Hospital, Johannes Kepler University Linz, Austria; Department of Neuroradiology (M. Möhlenbruch), Heidelberg University Hospital; Department of Radiology (M. Wildgruber), University Hospital, LMU Munich; Department of Neuroradiology (A.K.), Marburg University Hospital, Germany; and Department of Neuroradiology (M.P., P.B.S.), Clinic for Radiology & Nuclear Medicine, University Hospital Basel, Switzerland.
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From the Department of Neurology & Neurological Sciences, Stanford Stroke Center (S.L., M. Mlynash, S.C.), Department of Neurology & Neurological Sciences (S.L.), Division of Child Neurology, and Department of Radiology (B.J., M. Wintermark), Division of Neuroradiology, Stanford University School of Medicine, CA; Department of Pediatrics (R.S.), University Hospital of Muenster; Department of Diagnostic and Interventional Neuroradiology (G.B., J.F., P.B.S.), University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Department of Neuroradiology (A.G.), Medical University of Innsbruck, Austria; Department of Neuroradiology (F.D.), University Hospital Bonn; Department of Neuroradiology (O.N.), RWTH Aachen University; Department of Neuroradiology (D.K.), University Hospital Carl Gustav Carus, Dresden, Germany; ASST Valcamonica (A.M.), UOSD Neurology, Esine (BS), Brescia, Italy; Department of Radiology and Neuroradiology (U.J.-K.), University Hospital of Schleswig-Holstein, Campus Kiel; Institute of Neuroradiology (U.J.-K.), UKSH Campus Lübeck, Germany; Department of Neuroradiology (J.T.), Kepler University Hospital, Johannes Kepler University Linz, Austria; Department of Neuroradiology (M. Möhlenbruch), Heidelberg University Hospital; Department of Radiology (M. Wildgruber), University Hospital, LMU Munich; Department of Neuroradiology (A.K.), Marburg University Hospital, Germany; and Department of Neuroradiology (M.P., P.B.S.), Clinic for Radiology & Nuclear Medicine, University Hospital Basel, Switzerland.
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Cerebrovascular Collateral Integrity in Pediatric Large Vessel Occlusion
Analysis of the Save ChildS Study
Sarah Lee, Bin Jiang, Max Wintermark, Michael Mlynash, Soren Christensen, Ronald Sträter, Gabriel Broocks, Astrid Grams, Franziska Dorn, Omid Nikoubashman, Daniel Kaiser, Andrea Morotti, Ulf Jensen-Kondering, Johannes Trenkler, Markus Möhlenbruch, Jens Fiehler, Moritz Wildgruber, André Kemmling, Marios Psychogios, Peter B. Sporns, on behalf of Save ChildS Investigators
Neurology Jan 2022, 98 (4) e352-e363; DOI: 10.1212/WNL.0000000000013081

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Abstract

Background and Objectives Robust cerebrovascular collaterals in adult patients with large vessel occlusion stroke have been associated with longer treatment windows, better recanalization rates, and improved outcomes, but the role of collaterals in pediatric stroke is not known. The primary aim was to determine whether favorable collaterals correlated with better radiographic and clinical outcomes in children with ischemic stroke who underwent thrombectomy.

Methods This study analyzed a subset of children enrolled in SaveChildS, a retrospective, multicenter, observational cohort study of 73 pediatric patients with stroke who underwent thrombectomy between 2000 and 2018 at 27 US and European centers. Included patients had baseline angiographic imaging and follow-up modified Rankin Scale scores available for review. Posterior circulation occlusions were excluded. Cerebrovascular collaterals were graded on acute neuroimaging by 2 blinded neuroradiologists according to the Tan collateral score, in which favorable collaterals are defined as >50% filling and unfavorable collaterals as <50% filling distal to the occluded vessel. Collateral status was correlated with clinical and neuroimaging characteristics and outcomes. Between-group comparisons were performed with the Wilcoxon rank-sum test for continuous variables or Fisher exact test for binary variables.

Results Thirty-three children (mean age 10.9 [SD ±4.9]) years were included; 14 (42.4%) had favorable collaterals. Median final stroke volume as a percent of total brain volume (TBV) was significantly lower in patients with favorable collaterals (1.35% [interquartile range (IQR) 1.14%–3.76%] vs 7.86% [IQR 1.54%–11.07%], p = 0.049). Collateral status did not correlate with clinical outcome, infarct growth, or final Alberta Stroke Program Early CT Score (ASPECTS) in our cohort. Patients with favorable collaterals had higher baseline ASPECTS (7 [IQR 6–8] vs 5.5 [4–6], p = 0.006), smaller baseline ischemic volume (1.57% TBV [IQR 1.09%–2.29%] vs 3.42% TBV [IQR 1.26%–5.33%], p = 0.035), and slower early infarct growth rate (2.4 mL/h [IQR 1.5–5.1 mL/h] vs 10.4 mL/h [IQR 3.0–30.7 mL/h], p = 0.028).

Discussion Favorable collaterals were associated with smaller final stroke burden and slower early infarct growth rate but not with better clinical outcome in our study. Prospective studies are needed to determine the impact of collaterals in childhood stroke.

Classification of Evidence This study provides Class II evidence that in children with ischemic stroke undergoing thrombectomy, favorable collaterals were associated with improved radiographic outcomes but not with better clinical outcomes.

Glossary

ASPECTS=
Alberta Stroke Program Early CT Score;
CI=
confidence interval;
CRISP=
CT Perfusion to Predict Response to Recanalization in Ischemic Stroke Project;
DAWN=
Diffusion-Weighted Imaging or CTP Assessment With Clinical Mismatch in the Triage of Wake-Up and Late Presenting Strokes Undergoing Neurointervention With Trevo;
DEFUSE 3=
Endovascular Therapy Following Imaging Evaluation for Ischemic Stroke;
DWI=
diffusion weighted-imaging;
ECASS=
European Cooperative Acute Stroke Study;
MR=
magnetic resonance;
mRS=
modified Rankin Scale;
mTICI=
modified Thrombolysis in Cerebral Infarction;
NIHSS=
NIH Stroke Scale;
PSOM=
Pediatric Stroke Outcome Measure;
TBV=
total brain volume

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Save ChildS Investigators coinvestigators are listed in appendix 2 at the end of the article.

  • Editorial, page 135

  • Class of Evidence: NPub.org/coe

  • Received June 21, 2021.
  • Accepted in final form November 4, 2021.
  • © 2021 American Academy of Neurology
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