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  • Endovascular treatment in anterior circulation stroke beyond 6.5 hours after onset or time last seen well: results from the MR CLEAN Registry

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Original research
Endovascular treatment in anterior circulation stroke beyond 6.5 hours after onset or time last seen well: results from the MR CLEAN Registry
  1. Luuk Dekker1,
  2. Esmee Venema2,3,
  3. F Anne V Pirson4,
  4. Charles B L M Majoie5,
  5. Bart J Emmer5,
  6. Ivo G H Jansen5,
  7. Maxim J H L Mulder2,
  8. Robin Lemmens6,7,8,
  9. Robert-Jan B Goldhoorn4,
  10. Marieke J H Wermer1,
  11. Jelis Boiten9,
  12. Geert J Lycklama à Nijeholt10,
  13. Yvo B W E M Roos11,
  14. Adriaan C G M van Es10,12,
  15. Hester F Lingsma3,
  16. Diederik W J Dippel2,
  17. Wim H van Zwam13,
  18. Robert J van Oostenbrugge4,
  19. Ido R van den Wijngaard1,9
  20. on behalf of the MR CLEAN Registry investigators
    1. 1 Neurology, Leiden University Medical Centre, Leiden, The Netherlands
    2. 2 Neurology, Erasmus MC, Rotterdam, The Netherlands
    3. 3 Public Health, Erasmus MC, Rotterdam, The Netherlands
    4. 4 Neurology, Maastricht University Medical Centre+, Maastricht, The Netherlands
    5. 5 Radiology and Nuclear Medicine, Amsterdam University Medical Centre, Location AMC, Amsterdam, The Netherlands
    6. 6 Neurology, University Hospitals Leuven, Leuven, Belgium
    7. 7 Neurosciences, Experimental Neurology and Leuven Brain Institute, University of Leuven, Leuven, Belgium
    8. 8 VIB, Center for Brain & Disease Research, Laboratory of Neurobiology, Leuven, Belgium
    9. 9 Neurology, Haaglanden Medical Centre, Den Haag, The Netherlands
    10. 10 Radiology, Haaglanden Medical Centre, Den Haag, The Netherlands
    11. 11 Neurology, Amsterdam University Medical Centre, Location AMC, Amsterdam, The Netherlands
    12. 12 Radiology, Leiden University Medical Centre, Leiden, The Netherlands
    13. 13 Radiology, Maastricht University Medical Centre+, Maastricht, The Netherlands
    1. Correspondence to Dr Esmee Venema; e.venema{at}erasmusmc.nl

    Abstract

    Background Randomised controlled trials with perfusion selection have shown benefit of endovascular treatment (EVT) for ischaemic stroke between 6 and 24 hours after symptom onset or time last seen well. However, outcomes after EVT in these late window patients without perfusion imaging are largely unknown. We assessed their characteristics and outcomes in routine clinical practice.

    Methods The Multicenter Randomized Clinical Trial of Endovascular Treatment for Acute Ischemic Stroke in the Netherlands Registry, a prospective, multicentre study in the Netherlands, included patients with an anterior circulation occlusion who underwent EVT between 2014 and 2017. CT perfusion was no standard imaging modality. We used adjusted ordinal logistic regression analysis to compare patients treated within versus beyond 6.5 hours after propensity score matching on age, prestroke modified Rankin Scale (mRS), National Institutes of Health Stroke Scale, Alberta Stroke Programme Early CT Score (ASPECTS), collateral status, location of occlusion and treatment with intravenous thrombolysis. Outcomes included 3-month mRS score, functional independence (defined as mRS 0–2), and death.

    Results Of 3264 patients who underwent EVT, 106 (3.2%) were treated beyond 6.5 hours (median 8.5, IQR 6.9–10.6), of whom 93 (87.7%) had unknown time of stroke onset. CT perfusion was not performed in 87/106 (80.2%) late window patients. Late window patients were younger (mean 67 vs 70 years, p<0.04) and had slightly lower ASPECTS (median 8 vs 9, p<0.01), but better collateral status (collateral score 2–3: 68.3% vs 57.7%, p=0.03). No differences were observed in proportions of functional independence (43.3% vs 40.5%, p=0.57) or death (24.0% vs 28.9%, p=0.28). After matching, outcomes remained similar (adjusted common OR for 1 point improvement in mRS 1.04, 95% CI 0.56 to 1.93).

    Conclusions Without the use of CT perfusion selection criteria, EVT in the 6.5–24-hour time window was not associated with poorer outcome in selected patients with favourable clinical and CT/CT angiography characteristics. randomised controlled trials with lenient inclusion criteria are needed to identify more patients who can benefit from EVT in the late window.

    • Thrombectomy
    • Stroke

    Data availability statement

    Individual patient data cannot be made available, because no patient approval has been obtained for sharing data, even in coded form. However, syntax and output files of statistical analyses can be made available upon reasonable request.

    https://creativecommons.org/licenses/by/4.0/

    This is an open access article distributed in accordance with the Creative Commons Attribution 4.0 Unported (CC BY 4.0) license, which permits others to copy, redistribute, remix, transform and build upon this work for any purpose, provided the original work is properly cited, a link to the licence is given, and indication of whether changes were made. See: https://creativecommons.org/licenses/by/4.0/.

    https://doi.org/10.1136/svn-2020-000803

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      Data availability statement

      Individual patient data cannot be made available, because no patient approval has been obtained for sharing data, even in coded form. However, syntax and output files of statistical analyses can be made available upon reasonable request.

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      Supplementary material

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      Footnotes

      • Collaborators The MR CLEAN Registry investigators: Jan Albert Vos, (Radiology, Sint Antonius Hospital, Nieuwegein); Kars C.J. Compagne, (Radiology, Erasmus MC University Medical Center); Manon Kappelhof (Department of Radiology and Nuclear Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam); Josje Brouwer (Neurology, Amsterdam UMC, University of Amsterdam, Amsterdam); Sanne J. den Hartog (Department of Neurology, Radiology, Public Health, Erasmus MC University Medical Center); Wouter H. Hinsenveld (Department of Neurology, Radiology, Maastricht University Medical Center and Cardiovascular Research Institute Maastricht (CARIM)); Bob Roozenbeek (Department of Neurology, Erasmus MC University Medical Center); Jonathan M. Coutinho (Neurology, Amsterdam UMC, University of Amsterdam, Amsterdam); Marianne A.A. van Walderveen (Radiology, Leiden University Medical Center); Julie Staals (Department of Neurology, Maastricht University Medical Center and Cardiovascular Research Institute Maastricht (CARIM)); Jeannette Hofmeijer (Department of Neurology, Rijnstate Hospital, Arnhem); Jasper M. Martens (Radiology, Rijnstate Hospital, Arnhem); Sebastiaan F. de Bruijnl (Department of Neurology, HAGA Hospital, the Hague); Lukas C. van Dijk (Radiology, HAGA Hospital, the Hague); H. Bart van der Worp (Department of Neurology, University Medical Center Utrecht); Rob H. Lo (Radiology, University Medical Center Utrecht); Ewoud J. van Dijk (Department of Neurology, Radboud University Medical Center, Nijmegen); Hieronymus D. Boogaarts (Neurosurgery, Radboud University Medical Center, Nijmegen); J. de Vries (Department of Neurology, Isala Klinieken, Zwolle); Paul L.M. de Kort (Department of Neurology, Elisabeth-TweeSteden ziekenhuis, Tilburg); Julia van Tuijl (Department of Neurology, Elisabeth-TweeSteden ziekenhuis, Tilburg); Jo P. Peluso (Radiology, Elisabeth-TweeSteden ziekenhuis, Tilburg); Puck Fransen (Department of Neurology, Isala Klinieken, Zwolle); Jan S.P. van den Berg (Department of Neurology, Isala Klinieken, Zwolle); Boudewijn A.A.M. van Hasselt (Radiology, Isala Klinieken, Zwolle); Leo A.M. Aerden (Department of Neurology,Reinier de Graaf Gasthuis, Delft); René J. Dallinga (Radiology, Reinier de Graaf Gasthuis, Delft); Maarten Uyttenboogaart; Omid Eschgi (Department of Neurology, University Medical Center Groningen); Reinoud P.H. Bokkers (Radiology, University Medical Center Groningen); Tobien H.C.M.L. Schreuder (Department of Neurology, Atrium Medical Center, Heerlen); Roel J.J. Heijboer (Radiology, Atrium Medical Center, Heerlen); Koos Keizer (Department of Neurology, Catharina Hospital, Eindhoven); Lonneke S.F. Yo (Radiology, Catharina Hospital, Eindhoven); Heleen M. den Hertog (Department of Neurology, Isala Klinieken, Zwolle); Emiel J.C. Sturm (Radiology, Medical Spectrum Twente, Enschede); Paul J.A.M. Brouwers (Department of Neurology, Medical Spectrum Twente, Enschede); Marieke E.S. Sprengers (Department of Radiology and Nuclear Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam); Sjoerd F.M. Jenniskens (Radiology, Radboud University Medical Center, Nijmegen); René van den Berg (Department of Radiology and Nuclear Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam); Albert J. Yoo (Department of Radiology, Texas Stroke Institute, Texas, United States of America); Ludo F.M. Beenen (Department of Radiology and Nuclear Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam); Alida A. Postma (Radiology, Maastricht University Medical Center and Cardiovascular Research Institute Maastricht (CARIM)); Stefan D. Roosendaal (Department of Radiology and Nuclear Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam); Bas F.W. van der Kallen (Department of Radiology, Haaglanden MC, the Hague); Ido R. van den Wijngaard (Department of Radiology, Haaglanden MC, the Hague); Adriaan C.G.M. van Es (Radiology, Rijnstate Hospital, Arnhem); Joost Bot (Department of Radiology, Amsterdam UMC, Vrije Universiteit van Amsterdam, Amsterdam); Pieter-Jan van Doormaal (Radiology, Erasmus MC University Medical Center); Anton Meijer (Radiology, Radboud University Medical Center, Nijmegen); Elyas Ghariq (Department of Radiology, Haaglanden MC, the Hague); Marc P. van Proosdij (Department of Radiology, Noordwest Ziekenhuisgroep, Alkmaar); G. Menno Krietemeijer (Radiology, Catharina Hospital, Eindhoven); Dick Gerrits (Radiology, Medical Spectrum Twente, Enschede); Wouter Dinkelaar (Radiology, Erasmus MC University Medical Center); Auke P.A. Appelman (Radiology, University Medical Center Groningen); Bas Hammer (Radiology, HAGA Hospital, the Hague); Sjoert Pegge (Radiology, Radboud University Medical Center, Nijmegen); Anouk van der Hoorn (Radiology, Radboud University Medical Center, Nijmegen); Saman Vinke (Neurosurgery, Radboud University Medical Center, Nijmegen); Wouter J. Schonewille (Department of Neurology, Sint Antonius Hospital, Nieuwegein); Naziha el Ghannouti (Department of Neurology, Erasmus MC University Medical Center); Martin Sterrenberg (Department of Neurology, Erasmus MC University Medical Center); Wilma Pellikaan (Department of Neurology, Sint Antonius Hospital, Nieuwegein); Rita Sprengers (Neurology, Amsterdam UMC, University of Amsterdam, Amsterdam); Marjan Elfrink (Department of Neurology, University Medical Center Groningen); Michelle Simons (Department of Neurology, Rijnstate Hospital, Arnhem); Marjolein Vossers (Radiology, Rijnstate Hospital, Arnhem); Joke de Meris (Neurology, Haaglanden MC, the Hague); Tamara Vermeulen (Neurology, Haaglanden MC, the Hague); Annet Geerlings (Department of Neurology, RadbouAnnet Geerlingsd University Medical Center, Nijmegen); Gina van Vemde (Department of Neurology, Isala Klinieken, Zwolle); Tiny Simons (Department of Neurology, Atrium Medical Center, Heerlen); Gert Messchendorp (Department of Neurology, University Medical Center Groningen); Nynke Nicolaij (Department of Neurology, University Medical Center Groningen); Hester Bongenaar (Department of Neurology, Catharina Hospital, Eindhoven); Karin Bodde (Department of Neurology, Reinier de Graaf Gasthuis, Delft); Sandra Kleijn (Department of Neurology, Medical Spectrum Twente, Enschede); Jasmijn Lodico (Department of Neurology, Medical Spectrum Twente, Enschede); Hanneke Droste (Department of Neurology, Medical Spectrum Twente, Enschede); Maureen Wollaert (Department of Neurology, Maastricht University Medical Center and Cardiovascular Research Institute Maastricht (CARIM)); Sabrina Verheesen (Department of Neurology, Maastricht University Medical Center and Cardiovascular Research Institute Maastricht (CARIM)); D. Jeurrissen (Department of Neurology, Maastricht University Medical Center and Cardiovascular Research Institute Maastricht (CARIM)); Erna Bos (Department of Neurology, Leiden University Medical Center); Yvonne Drabbe (Department of Neurology, HAGA Hospital, the Hague); Michelle Sandiman (Department of Neurology, HAGA Hospital, the Hague); Nicoline Aaldering (Department of Neurology, Rijnstate Hospital, Arnhem); Berber Zweedijk (Department of Neurology, University Medical Center Utrecht); Jocova Vervoort (Department of Neurology, Elisabeth-TweeSteden ziekenhuis, Tilburg); Eva Ponjee (Department of Neurology, Isala Klinieken, Zwolle); Sharon Romviel (Department of Neurology, RadbouAnnet Geerlingsd University Medical Center, Nijmegen); Karin Kanselaar1 (Department of Neurology, RadbouAnnet Geerlingsd University Medical Center, Nijmegen); Denn Barning (Radiology, Leiden University Medical Center); Vicky Chalos (Department of Neurology, Public Health, Erasmus MC University Medical Center); Ralph R. Geuskens (Department of Radiology and Nuclear Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam); Tim van Straaten (Department of Neurology, RadbouAnnet Geerlingsd University Medical Center, Nijmegen); Saliha Ergezen (Department of Neurology, Erasmus MC University Medical Center); Roger R.M. Harmsma (Department of Neurology, Erasmus MC University Medical Center); Daan Muijres (Department of Neurology, Erasmus MC University Medical Center); Olvert A. Berkhemer (Department of Neurology, Erasmus MC University Medical Center; Department of Radiology and Nuclear Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam and Radiology, Maastricht University Medical Center and Cardiovascular Research Institute Maastricht (CARIM)); Anna M.M. Boers (Department of Radiology and Nuclear Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam and Biomedical Engineering & Physics, Amsterdam UMC, University of Amsterdam, Amsterdam); J. Huguet (Department of Radiology and Nuclear Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam); P.F.C. Groot (Department of Radiology and Nuclear Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam); Marieke A. Mens (Department of Radiology and Nuclear Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam); Katinka R. van Kranendonk (Department of Radiology and Nuclear Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam); Kilian M. Treurniet (Department of Radiology and Nuclear Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam); Manon L. Tolhuisen (Department of Radiology and Nuclear Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam and Biomedical Engineering & Physics, Amsterdam UMC, University of Amsterdam, Amsterdam); Heitor Alves (Department of Radiology and Nuclear Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam); Annick J. Weterings (Department of Radiology and Nuclear Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam); Eleonora L.F. Kirkels (Department of Radiology and Nuclear Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam); Eva J.H.F. Voogd (Department of Neurology, Rijnstate Hospital, Arnhem); Lieve M. Schupp (Department of Radiology and Nuclear Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam); Sabine Collette (Department of Neurology, Radiology, University Medical Center Groningen); Adrien E.D. Groot (Neurology, Amsterdam UMC, University of Amsterdam, Amsterdam); Natalie E. LeCouffe (Neurology, Amsterdam UMC, University of Amsterdam, Amsterdam); Praneeta R. Konduri (Biomedical Engineering & Physics, Amsterdam UMC, University of Amsterdam, Amsterdam); Haryadi Prasetya (Biomedical Engineering & Physics, Amsterdam UMC, University of Amsterdam, Amsterdam); Nerea Arrarte-Terreros (Biomedical Engineering & Physics, Amsterdam UMC, University of Amsterdam, Amsterdam); Lucas A. Ramos (Biomedical Engineering & Physics, Amsterdam UMC, University of Amsterdam, Amsterdam).

      • Contributors LD and IRvdW: conception and design of the study. LD and FAVP: drafting of the manuscript. LD: data and statistical analysis. EV and HFL: supervision of statistical analysis. IGHJ, MJHLM and R-JBG: acquisition of clinical data. CBLMM, YBWEMR, DWJD, WHvZ and RJvO: members of the trial executive committee and critical review and revision. BJE, RL, MJHLW, JB, GJLàN and ACGMvE: critical review and revision for valuable intellectual content. All authors provided final approval of the version to be published.

      • Funding The MR CLEAN Registry was partly funded by TWIN Foundation, Erasmus MC University Medical Center, Maastricht University Medical Center and Academic Medical Center Amsterdam. No funding was obtained for this specific substudy. Robin Lemmens is a senior clinical investigator of FWO Flanders.

      • Competing interests Erasmus MC received funds from Stryker and Bracco Imaging by DWJD. MUMC received funds from Stryker and Codman for consultations by WHvZ. WHvZ and RJvO are principal investigators for the MR CLEAN-LATE trial. R-JBG and FAVP are coordinating researchers for MR CLEAN-LATE. CBLMM received funds from TWIN Foundation (related to this project, paid to institution) and from CVON/Dutch Heart Foundation, Stryker, European Commission, Health Evaluation Netherlands (unrelated; all paid to institution). YBWEMR, CBLMM and IGHJ are shareholders of Nico.lab, a company that focuses on the use of artificial intelligence for medical imaging analysis. RL reports institutional fees from Ischamaview for consultancy. The other authors had no conflicting interests.

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