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May 2021; 8 (3) ArticleOpen Access

Exercise Diminishes Plasma Neurofilament Light Chain and Reroutes the Kynurenine Pathway in Multiple Sclerosis

Niklas Joisten, Annette Rademacher, Clemens Warnke, Sebastian Proschinger, Alexander Schenk, David Walzik, Andre Knoop, Mario Thevis, Falk Steffen, Stefan Bittner, Roman Gonzenbach, Jan Kool, Wilhelm Bloch, Jens Bansi, Philipp Zimmer
First published March 29, 2021, DOI: https://doi.org/10.1212/NXI.0000000000000982
Niklas Joisten
From the Department of “Performance and Health (Sports Medicine)” (N.J., A.S., D.W., P.Z.), Institute of Sport and Sport Science, Technical University Dortmund; Department for Molecular and Cellular Sports Medicine (A.R., S.P., W.B.), Institute of Cardiovascular Research and Sports Medicine, German Sport University Cologne; Department of Neurology (C.W.), Faculty of Medicine and University Hospital Cologne, University of Cologne; Center for Preventive Doping Research/Institute of Biochemistry (A.K., M.T.), German Sport University Cologne; Department of Neurology (F.S., S.B.), Focus Program Translational Neuroscience (FTN), and Immunotherapy (FZI), University Medical Center of the Johannes Gutenberg University, Germany; and Department of Neurology (R.G., J.K., J.B.), Clinics of Valens, Rehabilitation Centre Valens, Switzerland.
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Annette Rademacher
From the Department of “Performance and Health (Sports Medicine)” (N.J., A.S., D.W., P.Z.), Institute of Sport and Sport Science, Technical University Dortmund; Department for Molecular and Cellular Sports Medicine (A.R., S.P., W.B.), Institute of Cardiovascular Research and Sports Medicine, German Sport University Cologne; Department of Neurology (C.W.), Faculty of Medicine and University Hospital Cologne, University of Cologne; Center for Preventive Doping Research/Institute of Biochemistry (A.K., M.T.), German Sport University Cologne; Department of Neurology (F.S., S.B.), Focus Program Translational Neuroscience (FTN), and Immunotherapy (FZI), University Medical Center of the Johannes Gutenberg University, Germany; and Department of Neurology (R.G., J.K., J.B.), Clinics of Valens, Rehabilitation Centre Valens, Switzerland.
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Clemens Warnke
From the Department of “Performance and Health (Sports Medicine)” (N.J., A.S., D.W., P.Z.), Institute of Sport and Sport Science, Technical University Dortmund; Department for Molecular and Cellular Sports Medicine (A.R., S.P., W.B.), Institute of Cardiovascular Research and Sports Medicine, German Sport University Cologne; Department of Neurology (C.W.), Faculty of Medicine and University Hospital Cologne, University of Cologne; Center for Preventive Doping Research/Institute of Biochemistry (A.K., M.T.), German Sport University Cologne; Department of Neurology (F.S., S.B.), Focus Program Translational Neuroscience (FTN), and Immunotherapy (FZI), University Medical Center of the Johannes Gutenberg University, Germany; and Department of Neurology (R.G., J.K., J.B.), Clinics of Valens, Rehabilitation Centre Valens, Switzerland.
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Sebastian Proschinger
From the Department of “Performance and Health (Sports Medicine)” (N.J., A.S., D.W., P.Z.), Institute of Sport and Sport Science, Technical University Dortmund; Department for Molecular and Cellular Sports Medicine (A.R., S.P., W.B.), Institute of Cardiovascular Research and Sports Medicine, German Sport University Cologne; Department of Neurology (C.W.), Faculty of Medicine and University Hospital Cologne, University of Cologne; Center for Preventive Doping Research/Institute of Biochemistry (A.K., M.T.), German Sport University Cologne; Department of Neurology (F.S., S.B.), Focus Program Translational Neuroscience (FTN), and Immunotherapy (FZI), University Medical Center of the Johannes Gutenberg University, Germany; and Department of Neurology (R.G., J.K., J.B.), Clinics of Valens, Rehabilitation Centre Valens, Switzerland.
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Alexander Schenk
From the Department of “Performance and Health (Sports Medicine)” (N.J., A.S., D.W., P.Z.), Institute of Sport and Sport Science, Technical University Dortmund; Department for Molecular and Cellular Sports Medicine (A.R., S.P., W.B.), Institute of Cardiovascular Research and Sports Medicine, German Sport University Cologne; Department of Neurology (C.W.), Faculty of Medicine and University Hospital Cologne, University of Cologne; Center for Preventive Doping Research/Institute of Biochemistry (A.K., M.T.), German Sport University Cologne; Department of Neurology (F.S., S.B.), Focus Program Translational Neuroscience (FTN), and Immunotherapy (FZI), University Medical Center of the Johannes Gutenberg University, Germany; and Department of Neurology (R.G., J.K., J.B.), Clinics of Valens, Rehabilitation Centre Valens, Switzerland.
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David Walzik
From the Department of “Performance and Health (Sports Medicine)” (N.J., A.S., D.W., P.Z.), Institute of Sport and Sport Science, Technical University Dortmund; Department for Molecular and Cellular Sports Medicine (A.R., S.P., W.B.), Institute of Cardiovascular Research and Sports Medicine, German Sport University Cologne; Department of Neurology (C.W.), Faculty of Medicine and University Hospital Cologne, University of Cologne; Center for Preventive Doping Research/Institute of Biochemistry (A.K., M.T.), German Sport University Cologne; Department of Neurology (F.S., S.B.), Focus Program Translational Neuroscience (FTN), and Immunotherapy (FZI), University Medical Center of the Johannes Gutenberg University, Germany; and Department of Neurology (R.G., J.K., J.B.), Clinics of Valens, Rehabilitation Centre Valens, Switzerland.
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Andre Knoop
From the Department of “Performance and Health (Sports Medicine)” (N.J., A.S., D.W., P.Z.), Institute of Sport and Sport Science, Technical University Dortmund; Department for Molecular and Cellular Sports Medicine (A.R., S.P., W.B.), Institute of Cardiovascular Research and Sports Medicine, German Sport University Cologne; Department of Neurology (C.W.), Faculty of Medicine and University Hospital Cologne, University of Cologne; Center for Preventive Doping Research/Institute of Biochemistry (A.K., M.T.), German Sport University Cologne; Department of Neurology (F.S., S.B.), Focus Program Translational Neuroscience (FTN), and Immunotherapy (FZI), University Medical Center of the Johannes Gutenberg University, Germany; and Department of Neurology (R.G., J.K., J.B.), Clinics of Valens, Rehabilitation Centre Valens, Switzerland.
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Mario Thevis
From the Department of “Performance and Health (Sports Medicine)” (N.J., A.S., D.W., P.Z.), Institute of Sport and Sport Science, Technical University Dortmund; Department for Molecular and Cellular Sports Medicine (A.R., S.P., W.B.), Institute of Cardiovascular Research and Sports Medicine, German Sport University Cologne; Department of Neurology (C.W.), Faculty of Medicine and University Hospital Cologne, University of Cologne; Center for Preventive Doping Research/Institute of Biochemistry (A.K., M.T.), German Sport University Cologne; Department of Neurology (F.S., S.B.), Focus Program Translational Neuroscience (FTN), and Immunotherapy (FZI), University Medical Center of the Johannes Gutenberg University, Germany; and Department of Neurology (R.G., J.K., J.B.), Clinics of Valens, Rehabilitation Centre Valens, Switzerland.
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Falk Steffen
From the Department of “Performance and Health (Sports Medicine)” (N.J., A.S., D.W., P.Z.), Institute of Sport and Sport Science, Technical University Dortmund; Department for Molecular and Cellular Sports Medicine (A.R., S.P., W.B.), Institute of Cardiovascular Research and Sports Medicine, German Sport University Cologne; Department of Neurology (C.W.), Faculty of Medicine and University Hospital Cologne, University of Cologne; Center for Preventive Doping Research/Institute of Biochemistry (A.K., M.T.), German Sport University Cologne; Department of Neurology (F.S., S.B.), Focus Program Translational Neuroscience (FTN), and Immunotherapy (FZI), University Medical Center of the Johannes Gutenberg University, Germany; and Department of Neurology (R.G., J.K., J.B.), Clinics of Valens, Rehabilitation Centre Valens, Switzerland.
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Stefan Bittner
From the Department of “Performance and Health (Sports Medicine)” (N.J., A.S., D.W., P.Z.), Institute of Sport and Sport Science, Technical University Dortmund; Department for Molecular and Cellular Sports Medicine (A.R., S.P., W.B.), Institute of Cardiovascular Research and Sports Medicine, German Sport University Cologne; Department of Neurology (C.W.), Faculty of Medicine and University Hospital Cologne, University of Cologne; Center for Preventive Doping Research/Institute of Biochemistry (A.K., M.T.), German Sport University Cologne; Department of Neurology (F.S., S.B.), Focus Program Translational Neuroscience (FTN), and Immunotherapy (FZI), University Medical Center of the Johannes Gutenberg University, Germany; and Department of Neurology (R.G., J.K., J.B.), Clinics of Valens, Rehabilitation Centre Valens, Switzerland.
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Roman Gonzenbach
From the Department of “Performance and Health (Sports Medicine)” (N.J., A.S., D.W., P.Z.), Institute of Sport and Sport Science, Technical University Dortmund; Department for Molecular and Cellular Sports Medicine (A.R., S.P., W.B.), Institute of Cardiovascular Research and Sports Medicine, German Sport University Cologne; Department of Neurology (C.W.), Faculty of Medicine and University Hospital Cologne, University of Cologne; Center for Preventive Doping Research/Institute of Biochemistry (A.K., M.T.), German Sport University Cologne; Department of Neurology (F.S., S.B.), Focus Program Translational Neuroscience (FTN), and Immunotherapy (FZI), University Medical Center of the Johannes Gutenberg University, Germany; and Department of Neurology (R.G., J.K., J.B.), Clinics of Valens, Rehabilitation Centre Valens, Switzerland.
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Jan Kool
From the Department of “Performance and Health (Sports Medicine)” (N.J., A.S., D.W., P.Z.), Institute of Sport and Sport Science, Technical University Dortmund; Department for Molecular and Cellular Sports Medicine (A.R., S.P., W.B.), Institute of Cardiovascular Research and Sports Medicine, German Sport University Cologne; Department of Neurology (C.W.), Faculty of Medicine and University Hospital Cologne, University of Cologne; Center for Preventive Doping Research/Institute of Biochemistry (A.K., M.T.), German Sport University Cologne; Department of Neurology (F.S., S.B.), Focus Program Translational Neuroscience (FTN), and Immunotherapy (FZI), University Medical Center of the Johannes Gutenberg University, Germany; and Department of Neurology (R.G., J.K., J.B.), Clinics of Valens, Rehabilitation Centre Valens, Switzerland.
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Wilhelm Bloch
From the Department of “Performance and Health (Sports Medicine)” (N.J., A.S., D.W., P.Z.), Institute of Sport and Sport Science, Technical University Dortmund; Department for Molecular and Cellular Sports Medicine (A.R., S.P., W.B.), Institute of Cardiovascular Research and Sports Medicine, German Sport University Cologne; Department of Neurology (C.W.), Faculty of Medicine and University Hospital Cologne, University of Cologne; Center for Preventive Doping Research/Institute of Biochemistry (A.K., M.T.), German Sport University Cologne; Department of Neurology (F.S., S.B.), Focus Program Translational Neuroscience (FTN), and Immunotherapy (FZI), University Medical Center of the Johannes Gutenberg University, Germany; and Department of Neurology (R.G., J.K., J.B.), Clinics of Valens, Rehabilitation Centre Valens, Switzerland.
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Jens Bansi
From the Department of “Performance and Health (Sports Medicine)” (N.J., A.S., D.W., P.Z.), Institute of Sport and Sport Science, Technical University Dortmund; Department for Molecular and Cellular Sports Medicine (A.R., S.P., W.B.), Institute of Cardiovascular Research and Sports Medicine, German Sport University Cologne; Department of Neurology (C.W.), Faculty of Medicine and University Hospital Cologne, University of Cologne; Center for Preventive Doping Research/Institute of Biochemistry (A.K., M.T.), German Sport University Cologne; Department of Neurology (F.S., S.B.), Focus Program Translational Neuroscience (FTN), and Immunotherapy (FZI), University Medical Center of the Johannes Gutenberg University, Germany; and Department of Neurology (R.G., J.K., J.B.), Clinics of Valens, Rehabilitation Centre Valens, Switzerland.
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Philipp Zimmer
From the Department of “Performance and Health (Sports Medicine)” (N.J., A.S., D.W., P.Z.), Institute of Sport and Sport Science, Technical University Dortmund; Department for Molecular and Cellular Sports Medicine (A.R., S.P., W.B.), Institute of Cardiovascular Research and Sports Medicine, German Sport University Cologne; Department of Neurology (C.W.), Faculty of Medicine and University Hospital Cologne, University of Cologne; Center for Preventive Doping Research/Institute of Biochemistry (A.K., M.T.), German Sport University Cologne; Department of Neurology (F.S., S.B.), Focus Program Translational Neuroscience (FTN), and Immunotherapy (FZI), University Medical Center of the Johannes Gutenberg University, Germany; and Department of Neurology (R.G., J.K., J.B.), Clinics of Valens, Rehabilitation Centre Valens, Switzerland.
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Citation
Exercise Diminishes Plasma Neurofilament Light Chain and Reroutes the Kynurenine Pathway in Multiple Sclerosis
Niklas Joisten, Annette Rademacher, Clemens Warnke, Sebastian Proschinger, Alexander Schenk, David Walzik, Andre Knoop, Mario Thevis, Falk Steffen, Stefan Bittner, Roman Gonzenbach, Jan Kool, Wilhelm Bloch, Jens Bansi, Philipp Zimmer
Neurol Neuroimmunol Neuroinflamm May 2021, 8 (3) e982; DOI: 10.1212/NXI.0000000000000982

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Abstract

Objective To examine acute (single-bout) and training effects of high-intensity interval training (HIIT) vs standard exercise therapy (moderate continuous training [MCT]) on plasma neurofilament light chain (pNfL) and kynurenine (KYN) pathway of tryptophan degradation metabolites in persons with multiple sclerosis (pwMS).

Methods Sixty-nine pwMS (Expanded Disability Status Scale score 3.0–6.0) were randomly assigned to a HIIT or an MCT group. Changes in pNfL and KYN pathway metabolites measured in blood plasma were assessed before, after, and 3 hours after the first training session as well as after the 3-week training intervention.

Results Acute exercise reduced pNfL and increased the KYN pathway flux toward the neuroprotective kynurenic acid (KA). Changes in pNfL correlated positively with changes in KA and negatively with the quinolinic acid-to-KA ratio. HIIT consistently led to greater effects than MCT. Following the 3-week training intervention, the KYN pathway was activated in HIIT compared with MCT.

Conclusion Future studies and clinical assessments of pNfL should consider acute exercise as confounding factor for measurement reliability. Moreover, exercise-induced KYN pathway rerouting might mediate neuroprotection, potentially underlying the benefits in rehabilitation for pwMS.

Classification of Evidence This study provides Class II evidence that acute HIIT diminishes pNfL and increases KA levels, and 3 weeks of HIIT activate the KYN pathway in pwMS.

Trial Registration Information Clinical trial registration number: NCT03652519.

Glossary

CV=
coefficient of variation;
EDSS=
Expanded Disability Status Scale;
HIIT=
high-intensity interval training;
HPLC-MS/MS=
high-performance liquid chromatography–tandem mass spectrometry;
IL-6=
interleukin-6;
KA=
kynurenic acid;
KYN=
kynurenine;
MCT=
moderate continuous training;
pNfL=
plasma neurofilament light chain;
pwMS=
persons with multiple sclerosis;
QA=
quinolinic acid;
TRP=
tryptophan

Footnotes

  • Go to Neurology.org/NN for full disclosures. Funding information is provided at the end of the article.

  • ↵* These authors contributed equally to this work.

  • ↵† These authors share senior authorship.

  • The Article Processing Charge was funded by the authors.

  • Received October 21, 2020.
  • Accepted in final form January 21, 2021.
  • Copyright © 2021 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the 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 without permission from the journal.

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