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Original research
Collateral status and recanalization after endovascular treatment for acute ischemic stroke
  1. Simone M Uniken Venema1,
  2. Jan Willem Dankbaar2,
  3. Lennard Wolff3,
  4. Adriaan C G M van Es4,
  5. Marieke Sprengers5,
  6. Aad van der Lugt3,
  7. Diederik W J Dippel6,
  8. H. Bart van der Worp1
  9. on behalf of the MR CLEAN Registry investigators
    1. 1Department of Neurology and Neurosurgery, Brain Center, University Medical Centre Utrecht, Utrecht, The Netherlands
    2. 2Department of Radiology, University Medical Center Utrecht Imaging Division, Utrecht, The Netherlands
    3. 3Department of Radiology and Nuclear Medicine, Erasmus Medical Center, Rotterdam, Zuid-Holland, The Netherlands
    4. 4Department of Radiology, Leiden Universitair Medisch Centrum, Leiden, Zuid-Holland, The Netherlands
    5. 5Department of Radiology and Nuclear Medicine, Amsterdam UMC Locatie AMC, Amsterdam, North Holland, The Netherlands
    6. 6Department of Neurology, Erasmus Medical Center, Rotterdam, Zuid-Holland, The Netherlands
    1. Correspondence to Simone M Uniken Venema, University Medical Centre Utrecht Brain Centre, Utrecht, The Netherlands; s.m.unikenvenema{at}umcutrecht.nl

    Abstract

    Background Successful recanalization and good collateral status are associated with good clinical outcomes after endovascular treatment (EVT) for acute ischemic stroke, but the relationships among them are unclear.

    Objective To assess if collateral status is associated with recanalization after EVT and if collateral status modifies the association between successful recanalization and functional outcome.

    Methods We retrospectively analyzed data from the MR CLEAN Registry, a multicenter prospective cohort study of patients with a proximal anterior occlusion who underwent EVT in the Netherlands. We determined collateral status with a previously validated four-point visual grading scale and defined successful recanalization as an extended Thrombolysis in Cerebral Infarction score ≥2B. Functional outcome was determined using the modified Rankin Scale score at 90 days. We assessed, with multivariable logistic regression models, the associations between (1) collateral status and successful recanalization, (2) successful recanalization and functional outcome, (3) collateral status and functional outcome. An interaction of collateral status and successful recanalization was assessed. Subgroup analyses were performed for patients treated with intravenous thrombolysis.

    Results We included 2717 patients, of whom 1898 (70%) had successful recanalization. There was no relationship between collateral status and successful recanalization (adjusted common OR (95% CI) of grades 1, 2, and 3 vs 0: 1.19 (0.82 to 1.72), 1.20 (0.83 to 1.75), and 1.10 (0.74 to 1.63), respectively). Successful recanalization (acOR (95% CI): 2.15 (1.84 to 2.52)) and better collateral grades (acOR (95% CI) of grades 1, 2, and 3 vs 0: 2.12 (1.47 to 3.05), 3.46 (2.43 to 4.92), and 4.16 (2.89 to 5.99), respectively) were both associated with a shift towards better functional outcome, without an interaction between collateral status and successful recanalization. Results were similar for the subgroup of thrombolysed patients.

    Conclusions Collateral status is not associated with the probability of successful recanalization after EVT and does not modify the association between successful recanalization and functional outcome.

    • Stroke
    • Thrombectomy
    • CT Angiography
    • Angiography

    Data availability statement

    Data are available upon reasonable request. Source data from patients cannot be distributed, but syntax and output files from statistical analyses can be made available upon reasonable request to the corresponding author.

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    Data availability statement

    Data are available upon reasonable request. Source data from patients cannot be distributed, but syntax and output files from statistical analyses can be made available upon reasonable request to the corresponding author.

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    Footnotes

    • Collaborators MR CLEAN Registry investigators–Executive committee: Diederik W.J. Dippel (Department of Neurology); Aad van der Lugt (Radiology); Charles B.L.M. Majoie (Erasmus MC University Medical Center;Department of Radiology and Nuclear Medicine); Yvo B.W.E.M. Roos (Neurology); Robert J. van Oostenbrugge (Amsterdam UMC, University of Amsterdam, Amsterdam; Department of Neurology); Wim H. van Zwam (Radiology); Jelis Boiten (Neurology); Jan Albert Vos (Radiology) Study coordinators: Ivo G.H. Jansen (Erasmus MC University Medical Center;Department of Radiology and Nuclear Medicine);Maxim J.H.L. Mulder (Department of Neurology), (Radiology); Robert- Jan B. Goldhoorn (Amsterdam UMC, University of Amsterdam, Amsterdam; Department of Neurology), (Radiology); Kars C.J. Compagne (Radiology); Manon Kappelhof (Erasmus MC University Medical Center;Department of Radiology and Nuclear Medicine); Josje Brouwer (Neurology); Sanne J. den Hartog (Department of Neurology),(Radiology), (Public Health); Wouter H. Hinsenveld (Amsterdam UMC, University of Amsterdam, Amsterdam; Department of Neurology), (Radiology); Local principal investigators: Diederik W.J. Dippel (Department of Neurology); Bob Roozenbeek (Department of Neurology); Aad van der Lugt (Radiology); Adriaan C.G.M. van Es (Radiology); Charles B.L.M. Majoie (Erasmus MC University Medical Center;Department of Radiology and Nuclear Medicine); Yvo B.W.E.M. Roos (Neurology); Bart J. Emmer (Erasmus MC University Medical Center;Department of Radiology and Nuclear Medicine); Jonathan M. Coutinho (Neurology); Wouter J. Schonewille (Maastricht University Medical Center and Cardiovascular Research Institute Maastricht (CARIM); Department of Neurology); Jan Albert Vos (Radiology); Marieke J.H. Wermer (Sint Antonius Hospital, Nieuwegein; Department of Neurology); Marianne A.A. van Walderveen (Radiology); Julie Staals (Amsterdam UMC, University of Amsterdam, Amsterdam; Department of Neurology); Robert J. van Oostenbrugge (Amsterdam UMC, University of Amsterdam, Amsterdam; Department of Neurology); Wim H. van Zwam (Radiology); Jeannette Hofmeijer (Leiden University Medical Center; Department of Neurology); Jasper M. Martens (Radiology); Geert J. Lycklama à Nijeholt (Rijnstate Hospital, Arnhem; Department of Radiology); Jelis Boiten (Neurology); Sebastiaan F. de Bruijn (Haaglanden MC, the Hague; Department of Neurology); Lukas C. van Dijk1 (Radiology); H. Bart van der Worp (HAGA Hospital, the Hague; Department of Neurology); Rob H. Lo (Radiology); Ewoud J. van Dijk (University Medical Center Utrecht; Department of Neurology); Hieronymus D. Boogaarts (Neurosurgery); J. de Vries (Elisabeth-TweeSteden ziekenhuis, Tilburg; Department of Neurology); Paul L.M. de Kort (Radboud University Medical Center, Nijmegen; Department of Neurology); Julia van Tuijl (Radboud University Medical Center, Nijmegen; Department of Neurology); Jo P. Peluso (Radiology); Puck Fransen (Elisabeth-TweeSteden ziekenhuis, Tilburg; Department of Neurology); Jan S.P. van den Berg (Elisabeth-TweeSteden ziekenhuis, Tilburg; Department of Neurology); Boudewijn A.A.M. van Hasselt (Radiology); Leo A.M. Aerden (Isala Klinieken, Zwolle; Department of Neurology); René J. Dallinga (Radiology); Maarten Uyttenboogaart (Reinier de Graaf Gasthuis, Delft; Department of Neurology); Omid Eschgi (Radiology); Reinoud P.H. Bokkers (Radiology); Tobien H.C.M.L. Schreuder (University Medical Center Groningen; Department of Neurology); Roel J.J. Heijboer (Radiology); Koos Keizer (Atrium Medical Center, Heerlen; Department of Neurology); Lonneke S.F. Yo (Radiology); Heleen M. den Hertog (Elisabeth-TweeSteden ziekenhuis, Tilburg; Department of Neurology); Tomas Bulut (Radiology); Paul J.A.M. Brouwers (Catharina Hospital, Eindhoven; Department of Neurology). Imaging assessment committee: Charles B.L.M. Majoie (Erasmus MC University Medical Center; Department of Radiology and Nuclear Medicine)(chair); Wim H. van Zwam (Radiology); Aad van der Lugt (Radiology); Geert J. Lycklama à Nijeholt (Rijnstate Hospital, Arnhem; Department of Radiology); Marianne A.A. van Walderveen (Radiology); Marieke E.S. Sprengers (Erasmus MC University Medical Center;Department of Radiology and Nuclear Medicine); Sjoerd F.M. Jenniskens (Radiology); René van den Berg (Erasmus MC University Medical Center; Department of Radiology and Nuclear Medicine); Albert J. Yoo (Department of Radiology, Texas Stroke Institute, Texas, United States of America); Ludo F.M. Beenen (Erasmus MC University Medical Center;Department of Radiology and Nuclear Medicine); Alida A. Postma (Radiology); Stefan D. Roosendaal (Erasmus MC University Medical Center;Department of Radiology and Nuclear Medicine); Bas F.W. van der Kallen (Rijnstate Hospital, Arnhem; Department of Radiology); Ido R. van den Wijngaard (Rijnstate Hospital, Arnhem; Department of Radiology); Adriaan C.G.M. van Es (Radiology); Bart J. Emmer,(Erasmus MC University Medical Center;Department of Radiology and Nuclear Medicine); Jasper M. Martens (Radiology); Lonneke S.F. Yo (Radiology); Jan Albert Vos (Radiology); Joost Bot (Medisch Spectrum Twente, Enschede; Department of Radiology), Pieter-Jan van Doormaal (Radiology); Anton Meijer (Radiology);Elyas Ghariq (Rijnstate Hospital, Arnhem; Department of Radiology); Reinoud P.H. Bokkers (Radiology);Marc P. van Proosdij (Amsterdam UMC, Vrije Universiteit van Amsterdam, Amsterdam; Department of Radiology);G. Menno Krietemeijer (Radiology);Jo P. Peluso (Radiology); Hieronymus D. Boogaarts (Neurosurgery); Rob Lo (Radiology); Wouter Dinkelaar (Radiology); Auke P.A. Appelman (Radiology); Bas Hammer1 (Radiology); Sjoert Pegge (Radiology); Anouk van der Hoorn (Radiology); Saman Vinke (Neurosurgery). Writing committee: Diederik W.J. Dippel (Department of Neurology) (chair); Aad van der Lugt (Radiology); Charles B.L.M. Majoie (Erasmus MC University Medical Center; Department of Radiology and Nuclear Medicine); Yvo B.W.E.M. Roos (Neurology); Robert J. van Oostenbrugge (Amsterdam UMC, University of Amsterdam, Amsterdam; Department of Neurology); Wim H. van Zwam (Radiology); Geert J. Lycklama à Nijeholt (Rijnstate Hospital, Arnhem; Department of Radiology); Jelis Boiten (Neurology); Jan Albert Vos (Radiology); Wouter J. Schonewille (Maastricht University Medical Center and Cardiovascular Research Institute Maastricht (CARIM); Department of Neurology); Jeannette Hofmeijer (Leiden University Medical Center; Department of Neurology); Jasper M. Martens (Radiology); H. Bart van der Worp (HAGA Hospital, the Hague; Department of Neurology); Rob H. Lo (Radiology) Adverse event committee: Robert J. van Oostenbrugge (Amsterdam UMC, University of Amsterdam, Amsterdam; Department of Neurology)(chair);Jeannette Hofmeijer (Leiden University Medical Center; Department of Neurology); H. Zwenneke Flach (Radiology); Trial methodologist: Hester F. Lingsma (Public Health) Research nurses / local trial coordinators: Naziha el Ghannouti (Department of Neurology); Martin Sterrenberg1; Wilma Pellikaan (Maastricht University Medical Center and Cardiovascular Research Institute Maastricht (CARIM); Department of Neurology); Rita Sprengers (Neurology); Marjan Elfrink (Leiden University Medical Center; Department of Neurology); Michelle Simons (Leiden University Medical Center; Department of Neurology); Marjolein Vossers (Radiology); Joke de Meris (Neurology); Tamara Vermeulen (Neurology); Annet Geerlings (University Medical Center Utrecht; Department of Neurology); Gina van Vemde (Elisabeth-TweeSteden ziekenhuis, Tilburg; Department of Neurology); Tiny Simons (University Medical Center Groningen; Department of Neurology); Gert Messchendorp (Reinier de Graaf Gasthuis, Delft; Department of Neurology);Nynke Nicolaij (Reinier de Graaf Gasthuis, Delft; Department of Neurology);Hester Bongenaar (Atrium Medical Center, Heerlen; Department of Neurology);Karin Bodde (Isala Klinieken, Zwolle; Department of Neurology);Sandra Kleijn (Catharina Hospital, Eindhoven; Department of Neurology); Jasmijn Lodico (Catharina Hospital, Eindhoven; Department of Neurology); Hanneke Droste (Catharina Hospital, Eindhoven; Department of Neurology); Maureen Wollaert (Amsterdam UMC, University of Amsterdam, Amsterdam; Department of Neurology); Sabrina Verheesen (Amsterdam UMC, University of Amsterdam, Amsterdam; Department of Neurology); D. Jeurrissen (Amsterdam UMC, University of Amsterdam, Amsterdam; Department of Neurology); Erna Bos (Sint Antonius Hospital, Nieuwegein; Department of Neurology); Yvonne Drabbe (Haaglanden MC, the Hague; Department of Neurology); Michelle Sandiman (Haaglanden MC, the Hague; Department of Neurology); Nicoline Aaldering (Leiden University Medical Center; Department of Neurology); Berber Zweedijk (HAGA Hospital, the Hague; Department of Neurology); Jocova Vervoort (Radboud University Medical Center, Nijmegen; Department of Neurology); Eva Ponjee (Elisabeth-TweeSteden ziekenhuis, Tilburg; Department of Neurology); Sharon Romviel (University Medical Center Utrecht; Department of Neurology); Karin Kanselaar (University Medical Center Utrecht; Department of Neurology); Denn Barning (Radiology). PhD / Medical students: Esmee Venema (Public Health); Vicky Chalos(Department of Neurology),(Public Health); Ralph R. Geuskens (Erasmus MC University Medical Center;Department of Radiology and Nuclear Medicine); Tim van Straaten (University Medical Center Utrecht; Department of Neurology); Saliha Ergezen (Department of Neurology); Roger R.M. Harmsma(Department of Neurology); Daan Muijres(Department of Neurology); Anouk de Jong (Department of Neurology); Olvert A. Berkhemer (Department of Neurology),(Erasmus MC University Medical Center;Department of Radiology and Nuclear Medicine), (Radiology); Anna M.M. Boers (Erasmus MC University Medical Center;Department of Radiology and Nuclear Medicine), (Biomedical Engineering & Physics); J. Huguet (Erasmus MC University Medical Center;Department of Radiology and Nuclear Medicine); P.F.C. Groot (Erasmus MC University Medical Center;Department of Radiology and Nuclear Medicine); Marieke A. Mens (Erasmus MC University Medical Center;Department of Radiology and Nuclear Medicine); Katinka R. van Kranendonk (Erasmus MC University Medical Center;Department of Radiology and Nuclear Medicine); Kilian M. Treurniet (Erasmus MC University Medical Center;Department of Radiology and Nuclear Medicine); Manon L. Tolhuisen (Erasmus MC University Medical Center;Department of Radiology and Nuclear Medicine), (Biomedical Engineering & Physics); Heitor Alves (Erasmus MC University Medical Center; Department of Radiology and Nuclear Medicine); Annick J. Weterings (Erasmus MC University Medical Center;Department of Radiology and Nuclear Medicine), Eleonora L.F. Kirkels (Erasmus MC University Medical Center;Department of Radiology and Nuclear Medicine), Eva J.H.F. Voogd (Leiden University Medical Center; Department of Neurology); Lieve M. Schupp (Erasmus MC University Medical Center;Department of Radiology and Nuclear Medicine); Sabine L. Collette (Reinier de Graaf Gasthuis, Delft; Department of Neurology), (Radiology); Adrien E.D. Groot (Neurology); Natalie E. LeCouffe (Neurology); Praneeta R. Konduri (Biomedical Engineering & Physics); Haryadi Prasetya (Biomedical Engineering & Physics); Nerea Arrarte-Terreros (Biomedical Engineering & Physics); Lucas A. Ramos (Biomedical Engineering & Physics).

    • Contributors Simone M. Uniken Venema: study concept, statistical analysis, interpretation of the results, drafting of the manuscript. Jan Willem Dankbaar, Lennard Wolff, Adriaan C. G. M. van Es, Marieke Sprengers, Aad van der Lugt, Diederik W. J. Dippel: critical revision of the manuscript. H. Bart van der Worp: study concept, interpretation of the results, critical revision of the manuscript. H. Bart van der Worp is the guarantor of this work.

    • Funding The MR CLEAN Registry was partly funded by TWIN (Toegepast Wetenschappelijk Instituut voor Neuromodulatie) Foundation, Erasmus MC Medical Center, Maastricht University Medical Center, and Academic Medical Center Amsterdam. Simone M. Uniken Venema performed this work as coordinator of the trial MR ASAP, which is funded by Netherlands Cardiovascular Research Initiative, an initiative from the Dutch Heart Foundation.

    • Competing interests Simone M. Uniken Venema, Jan Willem Dankbaar, Lennard Wolff, Adriaan C. G. M. van Es, Marieke Sprengers report no disclosures; Diederik W. J. Dippel: reports funding from the Dutch Heart Foundation, Brain Foundation Netherlands, The Netherlands Organisation for Health Research and Development, Health Holland Top Sector Life Sciences and Health, and unrestricted grants from Penumbra Inc., Stryker, Medtronic, Cerenovus and Thrombolytic Science, LLC for research, all paid to his institution; Aad van der Lugt: reports funding from the Dutch Heart Foundation, Brain Foundation Netherlands, The Netherlands Organisation for Health Research and Development, Health Holland Top Sector Life Sciences and Health, and unrestricted grants from Penumbra Inc., Stryker, Medtronic, Cerenovus, and Thrombolytic Science, LLC for research, all paid to his institution; H. Bart van der Worp: received fees for consultation for Bayer and LivaNova, all paid to his institution.

    • Provenance and peer review Not commissioned; externally peer reviewed.

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