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January 12, 2021; 96 (2) Article

Efficacy of High-Intensity Aerobic Exercise on Brain MRI Measures in Multiple Sclerosis

View ORCID ProfileMartin Langeskov-Christensen, View ORCID ProfileLars Grøndahl Hvid, View ORCID ProfileMikkel Karl Emil Nygaard, Steffen Ringgaard, View ORCID ProfileHenrik Boye Jensen, View ORCID ProfileHelle Hvilsted Nielsen, View ORCID ProfileThor Petersen, View ORCID ProfileEgon Stenager, View ORCID ProfileSimon Fristed Eskildsen, View ORCID ProfileUlrik Dalgas
First published December 1, 2020, DOI: https://doi.org/10.1212/WNL.0000000000011241
Martin Langeskov-Christensen
From the Section for Sport Science, Department of Public Health (M.L.-C., L.G.H., U.D.), and Center of Functionally Integrative Neuroscience, Department of Clinical Medicine (M.K.E.N., S.F.E.), Aarhus University; MR Research Centre (S.R.) and Multiple Sclerosis Clinic, Department of Neurology (T.P.), Aarhus University Hospital; Brain and Nerve Diseases, Department of Neurology (H.B.J.), Lillebaelt Hospital, Kolding; Department of Regional Health Research (H.B.J.), Department of Neurobiology Research, Institute of Molecular Medicine (H.H.N.), BRIDGE–Brain Research–Inter-Disciplinary Guided Excellence, Department of Clinical Research (H.H.N.), and Department of Regional Health Research (E.S.), University of Southern Denmark, Odense; Department of Neurology (H.H.N.), Odense University Hospital; and MS-Clinic of Southern Jutland (Sønderborg, Kolding, Esbjerg), Department of Neurology (E.S.), Hospital of Southern Denmark, Sønderborg.
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  • ORCID record for Martin Langeskov-Christensen
Lars Grøndahl Hvid
From the Section for Sport Science, Department of Public Health (M.L.-C., L.G.H., U.D.), and Center of Functionally Integrative Neuroscience, Department of Clinical Medicine (M.K.E.N., S.F.E.), Aarhus University; MR Research Centre (S.R.) and Multiple Sclerosis Clinic, Department of Neurology (T.P.), Aarhus University Hospital; Brain and Nerve Diseases, Department of Neurology (H.B.J.), Lillebaelt Hospital, Kolding; Department of Regional Health Research (H.B.J.), Department of Neurobiology Research, Institute of Molecular Medicine (H.H.N.), BRIDGE–Brain Research–Inter-Disciplinary Guided Excellence, Department of Clinical Research (H.H.N.), and Department of Regional Health Research (E.S.), University of Southern Denmark, Odense; Department of Neurology (H.H.N.), Odense University Hospital; and MS-Clinic of Southern Jutland (Sønderborg, Kolding, Esbjerg), Department of Neurology (E.S.), Hospital of Southern Denmark, Sønderborg.
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Mikkel Karl Emil Nygaard
From the Section for Sport Science, Department of Public Health (M.L.-C., L.G.H., U.D.), and Center of Functionally Integrative Neuroscience, Department of Clinical Medicine (M.K.E.N., S.F.E.), Aarhus University; MR Research Centre (S.R.) and Multiple Sclerosis Clinic, Department of Neurology (T.P.), Aarhus University Hospital; Brain and Nerve Diseases, Department of Neurology (H.B.J.), Lillebaelt Hospital, Kolding; Department of Regional Health Research (H.B.J.), Department of Neurobiology Research, Institute of Molecular Medicine (H.H.N.), BRIDGE–Brain Research–Inter-Disciplinary Guided Excellence, Department of Clinical Research (H.H.N.), and Department of Regional Health Research (E.S.), University of Southern Denmark, Odense; Department of Neurology (H.H.N.), Odense University Hospital; and MS-Clinic of Southern Jutland (Sønderborg, Kolding, Esbjerg), Department of Neurology (E.S.), Hospital of Southern Denmark, Sønderborg.
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Steffen Ringgaard
From the Section for Sport Science, Department of Public Health (M.L.-C., L.G.H., U.D.), and Center of Functionally Integrative Neuroscience, Department of Clinical Medicine (M.K.E.N., S.F.E.), Aarhus University; MR Research Centre (S.R.) and Multiple Sclerosis Clinic, Department of Neurology (T.P.), Aarhus University Hospital; Brain and Nerve Diseases, Department of Neurology (H.B.J.), Lillebaelt Hospital, Kolding; Department of Regional Health Research (H.B.J.), Department of Neurobiology Research, Institute of Molecular Medicine (H.H.N.), BRIDGE–Brain Research–Inter-Disciplinary Guided Excellence, Department of Clinical Research (H.H.N.), and Department of Regional Health Research (E.S.), University of Southern Denmark, Odense; Department of Neurology (H.H.N.), Odense University Hospital; and MS-Clinic of Southern Jutland (Sønderborg, Kolding, Esbjerg), Department of Neurology (E.S.), Hospital of Southern Denmark, Sønderborg.
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Henrik Boye Jensen
From the Section for Sport Science, Department of Public Health (M.L.-C., L.G.H., U.D.), and Center of Functionally Integrative Neuroscience, Department of Clinical Medicine (M.K.E.N., S.F.E.), Aarhus University; MR Research Centre (S.R.) and Multiple Sclerosis Clinic, Department of Neurology (T.P.), Aarhus University Hospital; Brain and Nerve Diseases, Department of Neurology (H.B.J.), Lillebaelt Hospital, Kolding; Department of Regional Health Research (H.B.J.), Department of Neurobiology Research, Institute of Molecular Medicine (H.H.N.), BRIDGE–Brain Research–Inter-Disciplinary Guided Excellence, Department of Clinical Research (H.H.N.), and Department of Regional Health Research (E.S.), University of Southern Denmark, Odense; Department of Neurology (H.H.N.), Odense University Hospital; and MS-Clinic of Southern Jutland (Sønderborg, Kolding, Esbjerg), Department of Neurology (E.S.), Hospital of Southern Denmark, Sønderborg.
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Helle Hvilsted Nielsen
From the Section for Sport Science, Department of Public Health (M.L.-C., L.G.H., U.D.), and Center of Functionally Integrative Neuroscience, Department of Clinical Medicine (M.K.E.N., S.F.E.), Aarhus University; MR Research Centre (S.R.) and Multiple Sclerosis Clinic, Department of Neurology (T.P.), Aarhus University Hospital; Brain and Nerve Diseases, Department of Neurology (H.B.J.), Lillebaelt Hospital, Kolding; Department of Regional Health Research (H.B.J.), Department of Neurobiology Research, Institute of Molecular Medicine (H.H.N.), BRIDGE–Brain Research–Inter-Disciplinary Guided Excellence, Department of Clinical Research (H.H.N.), and Department of Regional Health Research (E.S.), University of Southern Denmark, Odense; Department of Neurology (H.H.N.), Odense University Hospital; and MS-Clinic of Southern Jutland (Sønderborg, Kolding, Esbjerg), Department of Neurology (E.S.), Hospital of Southern Denmark, Sønderborg.
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Thor Petersen
From the Section for Sport Science, Department of Public Health (M.L.-C., L.G.H., U.D.), and Center of Functionally Integrative Neuroscience, Department of Clinical Medicine (M.K.E.N., S.F.E.), Aarhus University; MR Research Centre (S.R.) and Multiple Sclerosis Clinic, Department of Neurology (T.P.), Aarhus University Hospital; Brain and Nerve Diseases, Department of Neurology (H.B.J.), Lillebaelt Hospital, Kolding; Department of Regional Health Research (H.B.J.), Department of Neurobiology Research, Institute of Molecular Medicine (H.H.N.), BRIDGE–Brain Research–Inter-Disciplinary Guided Excellence, Department of Clinical Research (H.H.N.), and Department of Regional Health Research (E.S.), University of Southern Denmark, Odense; Department of Neurology (H.H.N.), Odense University Hospital; and MS-Clinic of Southern Jutland (Sønderborg, Kolding, Esbjerg), Department of Neurology (E.S.), Hospital of Southern Denmark, Sønderborg.
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Egon Stenager
From the Section for Sport Science, Department of Public Health (M.L.-C., L.G.H., U.D.), and Center of Functionally Integrative Neuroscience, Department of Clinical Medicine (M.K.E.N., S.F.E.), Aarhus University; MR Research Centre (S.R.) and Multiple Sclerosis Clinic, Department of Neurology (T.P.), Aarhus University Hospital; Brain and Nerve Diseases, Department of Neurology (H.B.J.), Lillebaelt Hospital, Kolding; Department of Regional Health Research (H.B.J.), Department of Neurobiology Research, Institute of Molecular Medicine (H.H.N.), BRIDGE–Brain Research–Inter-Disciplinary Guided Excellence, Department of Clinical Research (H.H.N.), and Department of Regional Health Research (E.S.), University of Southern Denmark, Odense; Department of Neurology (H.H.N.), Odense University Hospital; and MS-Clinic of Southern Jutland (Sønderborg, Kolding, Esbjerg), Department of Neurology (E.S.), Hospital of Southern Denmark, Sønderborg.
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Simon Fristed Eskildsen
From the Section for Sport Science, Department of Public Health (M.L.-C., L.G.H., U.D.), and Center of Functionally Integrative Neuroscience, Department of Clinical Medicine (M.K.E.N., S.F.E.), Aarhus University; MR Research Centre (S.R.) and Multiple Sclerosis Clinic, Department of Neurology (T.P.), Aarhus University Hospital; Brain and Nerve Diseases, Department of Neurology (H.B.J.), Lillebaelt Hospital, Kolding; Department of Regional Health Research (H.B.J.), Department of Neurobiology Research, Institute of Molecular Medicine (H.H.N.), BRIDGE–Brain Research–Inter-Disciplinary Guided Excellence, Department of Clinical Research (H.H.N.), and Department of Regional Health Research (E.S.), University of Southern Denmark, Odense; Department of Neurology (H.H.N.), Odense University Hospital; and MS-Clinic of Southern Jutland (Sønderborg, Kolding, Esbjerg), Department of Neurology (E.S.), Hospital of Southern Denmark, Sønderborg.
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Ulrik Dalgas
From the Section for Sport Science, Department of Public Health (M.L.-C., L.G.H., U.D.), and Center of Functionally Integrative Neuroscience, Department of Clinical Medicine (M.K.E.N., S.F.E.), Aarhus University; MR Research Centre (S.R.) and Multiple Sclerosis Clinic, Department of Neurology (T.P.), Aarhus University Hospital; Brain and Nerve Diseases, Department of Neurology (H.B.J.), Lillebaelt Hospital, Kolding; Department of Regional Health Research (H.B.J.), Department of Neurobiology Research, Institute of Molecular Medicine (H.H.N.), BRIDGE–Brain Research–Inter-Disciplinary Guided Excellence, Department of Clinical Research (H.H.N.), and Department of Regional Health Research (E.S.), University of Southern Denmark, Odense; Department of Neurology (H.H.N.), Odense University Hospital; and MS-Clinic of Southern Jutland (Sønderborg, Kolding, Esbjerg), Department of Neurology (E.S.), Hospital of Southern Denmark, Sønderborg.
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Citation
Efficacy of High-Intensity Aerobic Exercise on Brain MRI Measures in Multiple Sclerosis
Martin Langeskov-Christensen, Lars Grøndahl Hvid, Mikkel Karl Emil Nygaard, Steffen Ringgaard, Henrik Boye Jensen, Helle Hvilsted Nielsen, Thor Petersen, Egon Stenager, Simon Fristed Eskildsen, Ulrik Dalgas
Neurology Jan 2021, 96 (2) e203-e213; DOI: 10.1212/WNL.0000000000011241

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Abstract

Objective To determine whether 24 weeks of high-intensity progressive aerobic exercise (PAE) affects brain MRI measures in people with multiple sclerosis (MS).

Methods We conducted a randomized, controlled, phase 2 trial (with a crossover follow-up) including an exercise group (supervised PAE followed by self-guided physical activity) and a waitlist group (habitual lifestyle followed by supervised PAE). Mildly to severely impaired patients with MS aged 18–65 years were randomized (1:1). The primary outcome was percentage brain volume change (PBVC) after 24 weeks, analyzed using the intention-to-treat principle.

Results Eighty-six participants were recruited. PBVC did not change over the intervention period (mean between-group change +0.12%, 95% confidence interval [CI] −0.27 to 0.51, p = 0.55). In contrast, cardiorespiratory fitness (+3.5 mL O2/min/kg, 2.0 to 5.1, p < 0.01) and annualized relapse rate (0.00, 0.00–0.07 vs +0.45, 0.28 to 0.61, p < 0.01) improved in the exercise group.

Conclusion These findings do not support a neuroprotective effect of PAE in terms of total brain atrophy in people with MS and it did not lead to a statistically significant difference in gray matter parenchymal fraction. PAE led to improvements in cardiorespiratory fitness and a lower relapse rate. While these exploratory findings cautiously support PAE as a potential adjunct disease-modifying treatment in MS, further investigations are warranted.

Clinicaltrials.gov identifier NCT02661555.

Classification of evidence This study provides Level I evidence that 24 weeks of high-intensity PAE did not elicit disease-modifying effects in PBVC in people with MS. Exploratory analyses showed that PAE may reduce relapse rate.

Glossary

6MWT=
6-Minute Walk Test;
ARR=
absolute risk reduction;
BPF=
brain parenchymal fraction;
DKI=
diffusion kurtosis imaging;
DMT=
disease-modifying treatment;
EDSS=
Expanded Disability Status Scale;
FA=
fractional anisotropy;
FLAIR=
fluid-attenuated inversion recovery;
GM=
gray matter;
GMPF=
gray matter parenchymal fraction;
HRmax=
maximum heart rate;
KFA=
kurtosis fractional anisotropy;
MD=
mean diffusivity;
MKT=
mean kurtosis tensor;
MS=
multiple sclerosis;
MSIS=
MS Impact Scale;
NNT=
number needed to treat;
PAE=
progressive aerobic exercise;
PBVC=
percentage brain volume change;
PRT=
progressive resistance training;
pwMS=
people with multiple sclerosis;
RCT=
randomized controlled trial;
SIENA=
structural imaging evaluation of normalized atrophy;
sNfL=
serum neurofilament light chain;
WMPF=
white matter parenchymal fraction

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.

  • Class of Evidence: NPub.org/coe

  • Received February 18, 2020.
  • Accepted in final form August 11, 2020.
  • © 2020 American Academy of Neurology
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