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September 06, 2016; 87 (10) ArticleOpen Access

The 11-year long-term follow-up study from the randomized BENEFIT CIS trial

Ludwig Kappos, Gilles Edan, Mark S. Freedman, Xavier Montalbán, Hans-Peter Hartung, Bernhard Hemmer, Edward J. Fox, Frederik Barkhof, Sven Schippling, Andrea Schulze, Dirk Pleimes, Christoph Pohl, Rupert Sandbrink, Gustavo Suarez, Eva-Maria Wicklein, For the BENEFIT Study Group
First published August 10, 2016, DOI: https://doi.org/10.1212/WNL.0000000000003078
Ludwig Kappos
From Neurology (L.K.), Departments of Medicine, Clinical Research, Biomedicine and Biomedical Engineering, University Hospital Basel, Switzerland; CHU–Hopital Pontchaillou (G.E.), Rennes, France; University of Ottawa (M.S.F.), and the Ottawa Hospital Research Institute, Ottawa, Canada; Hospital Universitari Vall d'Hebron (X.M.), Ps. Vall d'Hebron, Barcelona, Spain; Department of Neurology (H.-P.H., R.S.), Medical Faculty, Heinrich-Heine Universität, Düsseldorf; Technische Universität München (B.H.), Munich, Germany; Central Texas Neurology Consultants (E.J.F.), Round Rock, TX; VU University Medical Center (F.B.), Amsterdam, the Netherlands; Neuroimmunology and Multiple Sclerosis Research (S.S.), Department of Neurology, University Hospital Zurich and University of Zurich, Switzerland; Bayer Pharma AG (A.S., C.P., E.-M.W.), Berlin; Myelo Therapeutics GmbH (D.P.), Berlin; University Hospital of Bonn (C.P.), Germany; and Bayer HealthCare Pharmaceuticals (G.S.), Whippany, NJ.
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Gilles Edan
From Neurology (L.K.), Departments of Medicine, Clinical Research, Biomedicine and Biomedical Engineering, University Hospital Basel, Switzerland; CHU–Hopital Pontchaillou (G.E.), Rennes, France; University of Ottawa (M.S.F.), and the Ottawa Hospital Research Institute, Ottawa, Canada; Hospital Universitari Vall d'Hebron (X.M.), Ps. Vall d'Hebron, Barcelona, Spain; Department of Neurology (H.-P.H., R.S.), Medical Faculty, Heinrich-Heine Universität, Düsseldorf; Technische Universität München (B.H.), Munich, Germany; Central Texas Neurology Consultants (E.J.F.), Round Rock, TX; VU University Medical Center (F.B.), Amsterdam, the Netherlands; Neuroimmunology and Multiple Sclerosis Research (S.S.), Department of Neurology, University Hospital Zurich and University of Zurich, Switzerland; Bayer Pharma AG (A.S., C.P., E.-M.W.), Berlin; Myelo Therapeutics GmbH (D.P.), Berlin; University Hospital of Bonn (C.P.), Germany; and Bayer HealthCare Pharmaceuticals (G.S.), Whippany, NJ.
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Mark S. Freedman
From Neurology (L.K.), Departments of Medicine, Clinical Research, Biomedicine and Biomedical Engineering, University Hospital Basel, Switzerland; CHU–Hopital Pontchaillou (G.E.), Rennes, France; University of Ottawa (M.S.F.), and the Ottawa Hospital Research Institute, Ottawa, Canada; Hospital Universitari Vall d'Hebron (X.M.), Ps. Vall d'Hebron, Barcelona, Spain; Department of Neurology (H.-P.H., R.S.), Medical Faculty, Heinrich-Heine Universität, Düsseldorf; Technische Universität München (B.H.), Munich, Germany; Central Texas Neurology Consultants (E.J.F.), Round Rock, TX; VU University Medical Center (F.B.), Amsterdam, the Netherlands; Neuroimmunology and Multiple Sclerosis Research (S.S.), Department of Neurology, University Hospital Zurich and University of Zurich, Switzerland; Bayer Pharma AG (A.S., C.P., E.-M.W.), Berlin; Myelo Therapeutics GmbH (D.P.), Berlin; University Hospital of Bonn (C.P.), Germany; and Bayer HealthCare Pharmaceuticals (G.S.), Whippany, NJ.
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Xavier Montalbán
From Neurology (L.K.), Departments of Medicine, Clinical Research, Biomedicine and Biomedical Engineering, University Hospital Basel, Switzerland; CHU–Hopital Pontchaillou (G.E.), Rennes, France; University of Ottawa (M.S.F.), and the Ottawa Hospital Research Institute, Ottawa, Canada; Hospital Universitari Vall d'Hebron (X.M.), Ps. Vall d'Hebron, Barcelona, Spain; Department of Neurology (H.-P.H., R.S.), Medical Faculty, Heinrich-Heine Universität, Düsseldorf; Technische Universität München (B.H.), Munich, Germany; Central Texas Neurology Consultants (E.J.F.), Round Rock, TX; VU University Medical Center (F.B.), Amsterdam, the Netherlands; Neuroimmunology and Multiple Sclerosis Research (S.S.), Department of Neurology, University Hospital Zurich and University of Zurich, Switzerland; Bayer Pharma AG (A.S., C.P., E.-M.W.), Berlin; Myelo Therapeutics GmbH (D.P.), Berlin; University Hospital of Bonn (C.P.), Germany; and Bayer HealthCare Pharmaceuticals (G.S.), Whippany, NJ.
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Hans-Peter Hartung
From Neurology (L.K.), Departments of Medicine, Clinical Research, Biomedicine and Biomedical Engineering, University Hospital Basel, Switzerland; CHU–Hopital Pontchaillou (G.E.), Rennes, France; University of Ottawa (M.S.F.), and the Ottawa Hospital Research Institute, Ottawa, Canada; Hospital Universitari Vall d'Hebron (X.M.), Ps. Vall d'Hebron, Barcelona, Spain; Department of Neurology (H.-P.H., R.S.), Medical Faculty, Heinrich-Heine Universität, Düsseldorf; Technische Universität München (B.H.), Munich, Germany; Central Texas Neurology Consultants (E.J.F.), Round Rock, TX; VU University Medical Center (F.B.), Amsterdam, the Netherlands; Neuroimmunology and Multiple Sclerosis Research (S.S.), Department of Neurology, University Hospital Zurich and University of Zurich, Switzerland; Bayer Pharma AG (A.S., C.P., E.-M.W.), Berlin; Myelo Therapeutics GmbH (D.P.), Berlin; University Hospital of Bonn (C.P.), Germany; and Bayer HealthCare Pharmaceuticals (G.S.), Whippany, NJ.
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Bernhard Hemmer
From Neurology (L.K.), Departments of Medicine, Clinical Research, Biomedicine and Biomedical Engineering, University Hospital Basel, Switzerland; CHU–Hopital Pontchaillou (G.E.), Rennes, France; University of Ottawa (M.S.F.), and the Ottawa Hospital Research Institute, Ottawa, Canada; Hospital Universitari Vall d'Hebron (X.M.), Ps. Vall d'Hebron, Barcelona, Spain; Department of Neurology (H.-P.H., R.S.), Medical Faculty, Heinrich-Heine Universität, Düsseldorf; Technische Universität München (B.H.), Munich, Germany; Central Texas Neurology Consultants (E.J.F.), Round Rock, TX; VU University Medical Center (F.B.), Amsterdam, the Netherlands; Neuroimmunology and Multiple Sclerosis Research (S.S.), Department of Neurology, University Hospital Zurich and University of Zurich, Switzerland; Bayer Pharma AG (A.S., C.P., E.-M.W.), Berlin; Myelo Therapeutics GmbH (D.P.), Berlin; University Hospital of Bonn (C.P.), Germany; and Bayer HealthCare Pharmaceuticals (G.S.), Whippany, NJ.
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Edward J. Fox
From Neurology (L.K.), Departments of Medicine, Clinical Research, Biomedicine and Biomedical Engineering, University Hospital Basel, Switzerland; CHU–Hopital Pontchaillou (G.E.), Rennes, France; University of Ottawa (M.S.F.), and the Ottawa Hospital Research Institute, Ottawa, Canada; Hospital Universitari Vall d'Hebron (X.M.), Ps. Vall d'Hebron, Barcelona, Spain; Department of Neurology (H.-P.H., R.S.), Medical Faculty, Heinrich-Heine Universität, Düsseldorf; Technische Universität München (B.H.), Munich, Germany; Central Texas Neurology Consultants (E.J.F.), Round Rock, TX; VU University Medical Center (F.B.), Amsterdam, the Netherlands; Neuroimmunology and Multiple Sclerosis Research (S.S.), Department of Neurology, University Hospital Zurich and University of Zurich, Switzerland; Bayer Pharma AG (A.S., C.P., E.-M.W.), Berlin; Myelo Therapeutics GmbH (D.P.), Berlin; University Hospital of Bonn (C.P.), Germany; and Bayer HealthCare Pharmaceuticals (G.S.), Whippany, NJ.
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Frederik Barkhof
From Neurology (L.K.), Departments of Medicine, Clinical Research, Biomedicine and Biomedical Engineering, University Hospital Basel, Switzerland; CHU–Hopital Pontchaillou (G.E.), Rennes, France; University of Ottawa (M.S.F.), and the Ottawa Hospital Research Institute, Ottawa, Canada; Hospital Universitari Vall d'Hebron (X.M.), Ps. Vall d'Hebron, Barcelona, Spain; Department of Neurology (H.-P.H., R.S.), Medical Faculty, Heinrich-Heine Universität, Düsseldorf; Technische Universität München (B.H.), Munich, Germany; Central Texas Neurology Consultants (E.J.F.), Round Rock, TX; VU University Medical Center (F.B.), Amsterdam, the Netherlands; Neuroimmunology and Multiple Sclerosis Research (S.S.), Department of Neurology, University Hospital Zurich and University of Zurich, Switzerland; Bayer Pharma AG (A.S., C.P., E.-M.W.), Berlin; Myelo Therapeutics GmbH (D.P.), Berlin; University Hospital of Bonn (C.P.), Germany; and Bayer HealthCare Pharmaceuticals (G.S.), Whippany, NJ.
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Sven Schippling
From Neurology (L.K.), Departments of Medicine, Clinical Research, Biomedicine and Biomedical Engineering, University Hospital Basel, Switzerland; CHU–Hopital Pontchaillou (G.E.), Rennes, France; University of Ottawa (M.S.F.), and the Ottawa Hospital Research Institute, Ottawa, Canada; Hospital Universitari Vall d'Hebron (X.M.), Ps. Vall d'Hebron, Barcelona, Spain; Department of Neurology (H.-P.H., R.S.), Medical Faculty, Heinrich-Heine Universität, Düsseldorf; Technische Universität München (B.H.), Munich, Germany; Central Texas Neurology Consultants (E.J.F.), Round Rock, TX; VU University Medical Center (F.B.), Amsterdam, the Netherlands; Neuroimmunology and Multiple Sclerosis Research (S.S.), Department of Neurology, University Hospital Zurich and University of Zurich, Switzerland; Bayer Pharma AG (A.S., C.P., E.-M.W.), Berlin; Myelo Therapeutics GmbH (D.P.), Berlin; University Hospital of Bonn (C.P.), Germany; and Bayer HealthCare Pharmaceuticals (G.S.), Whippany, NJ.
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Andrea Schulze
From Neurology (L.K.), Departments of Medicine, Clinical Research, Biomedicine and Biomedical Engineering, University Hospital Basel, Switzerland; CHU–Hopital Pontchaillou (G.E.), Rennes, France; University of Ottawa (M.S.F.), and the Ottawa Hospital Research Institute, Ottawa, Canada; Hospital Universitari Vall d'Hebron (X.M.), Ps. Vall d'Hebron, Barcelona, Spain; Department of Neurology (H.-P.H., R.S.), Medical Faculty, Heinrich-Heine Universität, Düsseldorf; Technische Universität München (B.H.), Munich, Germany; Central Texas Neurology Consultants (E.J.F.), Round Rock, TX; VU University Medical Center (F.B.), Amsterdam, the Netherlands; Neuroimmunology and Multiple Sclerosis Research (S.S.), Department of Neurology, University Hospital Zurich and University of Zurich, Switzerland; Bayer Pharma AG (A.S., C.P., E.-M.W.), Berlin; Myelo Therapeutics GmbH (D.P.), Berlin; University Hospital of Bonn (C.P.), Germany; and Bayer HealthCare Pharmaceuticals (G.S.), Whippany, NJ.
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Dirk Pleimes
From Neurology (L.K.), Departments of Medicine, Clinical Research, Biomedicine and Biomedical Engineering, University Hospital Basel, Switzerland; CHU–Hopital Pontchaillou (G.E.), Rennes, France; University of Ottawa (M.S.F.), and the Ottawa Hospital Research Institute, Ottawa, Canada; Hospital Universitari Vall d'Hebron (X.M.), Ps. Vall d'Hebron, Barcelona, Spain; Department of Neurology (H.-P.H., R.S.), Medical Faculty, Heinrich-Heine Universität, Düsseldorf; Technische Universität München (B.H.), Munich, Germany; Central Texas Neurology Consultants (E.J.F.), Round Rock, TX; VU University Medical Center (F.B.), Amsterdam, the Netherlands; Neuroimmunology and Multiple Sclerosis Research (S.S.), Department of Neurology, University Hospital Zurich and University of Zurich, Switzerland; Bayer Pharma AG (A.S., C.P., E.-M.W.), Berlin; Myelo Therapeutics GmbH (D.P.), Berlin; University Hospital of Bonn (C.P.), Germany; and Bayer HealthCare Pharmaceuticals (G.S.), Whippany, NJ.
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Christoph Pohl
From Neurology (L.K.), Departments of Medicine, Clinical Research, Biomedicine and Biomedical Engineering, University Hospital Basel, Switzerland; CHU–Hopital Pontchaillou (G.E.), Rennes, France; University of Ottawa (M.S.F.), and the Ottawa Hospital Research Institute, Ottawa, Canada; Hospital Universitari Vall d'Hebron (X.M.), Ps. Vall d'Hebron, Barcelona, Spain; Department of Neurology (H.-P.H., R.S.), Medical Faculty, Heinrich-Heine Universität, Düsseldorf; Technische Universität München (B.H.), Munich, Germany; Central Texas Neurology Consultants (E.J.F.), Round Rock, TX; VU University Medical Center (F.B.), Amsterdam, the Netherlands; Neuroimmunology and Multiple Sclerosis Research (S.S.), Department of Neurology, University Hospital Zurich and University of Zurich, Switzerland; Bayer Pharma AG (A.S., C.P., E.-M.W.), Berlin; Myelo Therapeutics GmbH (D.P.), Berlin; University Hospital of Bonn (C.P.), Germany; and Bayer HealthCare Pharmaceuticals (G.S.), Whippany, NJ.
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Rupert Sandbrink
From Neurology (L.K.), Departments of Medicine, Clinical Research, Biomedicine and Biomedical Engineering, University Hospital Basel, Switzerland; CHU–Hopital Pontchaillou (G.E.), Rennes, France; University of Ottawa (M.S.F.), and the Ottawa Hospital Research Institute, Ottawa, Canada; Hospital Universitari Vall d'Hebron (X.M.), Ps. Vall d'Hebron, Barcelona, Spain; Department of Neurology (H.-P.H., R.S.), Medical Faculty, Heinrich-Heine Universität, Düsseldorf; Technische Universität München (B.H.), Munich, Germany; Central Texas Neurology Consultants (E.J.F.), Round Rock, TX; VU University Medical Center (F.B.), Amsterdam, the Netherlands; Neuroimmunology and Multiple Sclerosis Research (S.S.), Department of Neurology, University Hospital Zurich and University of Zurich, Switzerland; Bayer Pharma AG (A.S., C.P., E.-M.W.), Berlin; Myelo Therapeutics GmbH (D.P.), Berlin; University Hospital of Bonn (C.P.), Germany; and Bayer HealthCare Pharmaceuticals (G.S.), Whippany, NJ.
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Gustavo Suarez
From Neurology (L.K.), Departments of Medicine, Clinical Research, Biomedicine and Biomedical Engineering, University Hospital Basel, Switzerland; CHU–Hopital Pontchaillou (G.E.), Rennes, France; University of Ottawa (M.S.F.), and the Ottawa Hospital Research Institute, Ottawa, Canada; Hospital Universitari Vall d'Hebron (X.M.), Ps. Vall d'Hebron, Barcelona, Spain; Department of Neurology (H.-P.H., R.S.), Medical Faculty, Heinrich-Heine Universität, Düsseldorf; Technische Universität München (B.H.), Munich, Germany; Central Texas Neurology Consultants (E.J.F.), Round Rock, TX; VU University Medical Center (F.B.), Amsterdam, the Netherlands; Neuroimmunology and Multiple Sclerosis Research (S.S.), Department of Neurology, University Hospital Zurich and University of Zurich, Switzerland; Bayer Pharma AG (A.S., C.P., E.-M.W.), Berlin; Myelo Therapeutics GmbH (D.P.), Berlin; University Hospital of Bonn (C.P.), Germany; and Bayer HealthCare Pharmaceuticals (G.S.), Whippany, NJ.
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Eva-Maria Wicklein
From Neurology (L.K.), Departments of Medicine, Clinical Research, Biomedicine and Biomedical Engineering, University Hospital Basel, Switzerland; CHU–Hopital Pontchaillou (G.E.), Rennes, France; University of Ottawa (M.S.F.), and the Ottawa Hospital Research Institute, Ottawa, Canada; Hospital Universitari Vall d'Hebron (X.M.), Ps. Vall d'Hebron, Barcelona, Spain; Department of Neurology (H.-P.H., R.S.), Medical Faculty, Heinrich-Heine Universität, Düsseldorf; Technische Universität München (B.H.), Munich, Germany; Central Texas Neurology Consultants (E.J.F.), Round Rock, TX; VU University Medical Center (F.B.), Amsterdam, the Netherlands; Neuroimmunology and Multiple Sclerosis Research (S.S.), Department of Neurology, University Hospital Zurich and University of Zurich, Switzerland; Bayer Pharma AG (A.S., C.P., E.-M.W.), Berlin; Myelo Therapeutics GmbH (D.P.), Berlin; University Hospital of Bonn (C.P.), Germany; and Bayer HealthCare Pharmaceuticals (G.S.), Whippany, NJ.
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From Neurology (L.K.), Departments of Medicine, Clinical Research, Biomedicine and Biomedical Engineering, University Hospital Basel, Switzerland; CHU–Hopital Pontchaillou (G.E.), Rennes, France; University of Ottawa (M.S.F.), and the Ottawa Hospital Research Institute, Ottawa, Canada; Hospital Universitari Vall d'Hebron (X.M.), Ps. Vall d'Hebron, Barcelona, Spain; Department of Neurology (H.-P.H., R.S.), Medical Faculty, Heinrich-Heine Universität, Düsseldorf; Technische Universität München (B.H.), Munich, Germany; Central Texas Neurology Consultants (E.J.F.), Round Rock, TX; VU University Medical Center (F.B.), Amsterdam, the Netherlands; Neuroimmunology and Multiple Sclerosis Research (S.S.), Department of Neurology, University Hospital Zurich and University of Zurich, Switzerland; Bayer Pharma AG (A.S., C.P., E.-M.W.), Berlin; Myelo Therapeutics GmbH (D.P.), Berlin; University Hospital of Bonn (C.P.), Germany; and Bayer HealthCare Pharmaceuticals (G.S.), Whippany, NJ.
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The 11-year long-term follow-up study from the randomized BENEFIT CIS trial
Ludwig Kappos, Gilles Edan, Mark S. Freedman, Xavier Montalbán, Hans-Peter Hartung, Bernhard Hemmer, Edward J. Fox, Frederik Barkhof, Sven Schippling, Andrea Schulze, Dirk Pleimes, Christoph Pohl, Rupert Sandbrink, Gustavo Suarez, Eva-Maria Wicklein, For the BENEFIT Study Group
Neurology Sep 2016, 87 (10) 978-987; DOI: 10.1212/WNL.0000000000003078

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Abstract

Objective: To assess outcomes for patients treated with interferon beta-1b immediately after clinically isolated syndrome (CIS) or after a short delay.

Methods: Participants in BENEFIT (Betaferon/Betaseron in Newly Emerging MS for Initial Treatment) were randomly assigned to receive interferon beta-1b (early treatment) or placebo (delayed treatment). After conversion to clinically definite multiple sclerosis (CDMS) or 2 years, patients on placebo could switch to interferon beta-1b or another treatment. Eleven years after randomization, patients were reassessed.

Results: Two hundred seventy-eight (59.4%) of the original 468 patients (71.3% of those eligible at participating sites) were enrolled (early: 167 [57.2%]; delayed: 111 [63.1%]). After 11 years, risk of CDMS remained lower in the early-treatment arm compared with the delayed-treatment arm (p = 0.0012), with longer time to first relapse (median [Q1, Q3] days: 1,888 [540, not reached] vs 931 [253, 3,296]; p = 0.0005) and lower overall annualized relapse rate (0.21 vs 0.26; p = 0.0018). Only 25 patients (5.9%, overall; early, 4.5%; delayed, 8.3%) converted to secondary progressive multiple sclerosis. Expanded Disability Status Scale scores remained low and stable, with no difference between treatment arms (median [Q1, Q3]: 2.0 [1.0, 3.0]). The early-treatment group had better Paced Auditory Serial Addition Task–3 total scores (p = 0.0070). Employment rates remained high, and health resource utilization tended to be low in both groups. MRI metrics did not differ between groups.

Conclusions: Although the delay in treatment was relatively short, several clinical outcomes favored earlier treatment. Along with low rates of disability and disease progression in both groups, this supports the value of treatment at CIS.

ClinicalTrials.gov identifier: NCT01795872.

Classification of evidence: This study provides Class IV evidence that early compared to delayed treatment prolongs time to CDMS in CIS after 11 years.

GLOSSARY

ARR=
annualized relapse rate;
BENEFIT=
Betaferon/Betaseron in Newly Emerging MS for Initial Treatment;
CDMS=
clinically definite multiple sclerosis;
CI=
confidence interval;
CIS=
clinically isolated syndrome;
DMT=
disease-modifying therapy;
EDSS=
Expanded Disability Status Scale;
EQ-5D=
EuroQoL–5 Dimension;
FAMS=
Functional Assessment of Multiple Sclerosis;
Gd+=
gadolinium-enhancing;
KM=
Kaplan-Meier;
MS=
multiple sclerosis;
PASAT=
Paced Auditory Serial Addition Task;
Q=
quartile;
RR=
risk ratio;
SDMT=
Symbol Digit Modalities Test;
SPMS=
secondary progressive multiple sclerosis

Footnotes

  • ↵† Deceased.

  • BENEFIT Study Group coinvestigators are listed at Neurology.org.

  • Go to Neurology.org for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article. The Article Processing Charge was paid by Bayer Pharma AG/Bayer HealthCare Pharmaceuticals.

  • Supplemental data at Neurology.org

  • Editorial, page 970

  • Received September 28, 2015.
  • Accepted in final form April 14, 2016.
  • © 2016 American Academy of Neurology

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND), which permits downloading and sharing the work provided it is properly cited. The work cannot be changed in any way or used commercially.

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