Advertisement

Comparative Effectiveness of 4 Exercise Interventions Followed by 2 Years of Exercise Maintenance in Multiple Sclerosis: A Randomized Controlled Trial

  • Tibor Hortobágyi
    Affiliations
    Center for Human Movement Sciences, University Medical Center Groningen, University of Groningen, Groningen, the Netherlands

    Somogy County Kaposi Mór Teaching Hospital, Kaposvár, Hungary

    Department of Sport Biology, Institute of Sport Sciences and Physical Education, University of Pécs, Pécs, Hungary
    Search for articles by this author
  • Pongrác Ács
    Affiliations
    Departments of Epidemiology and Neurosurgery, University Medical Center Groningen, University of Groningen, Groningen, the Netherlands
    Search for articles by this author
  • Petra Baumann
    Affiliations
    Departments of Epidemiology and Neurosurgery, University Medical Center Groningen, University of Groningen, Groningen, the Netherlands

    University of Pécs, Faculty of Health Sciences, Doctoral School of Health Sciences, Pécs, Hungary
    Search for articles by this author
  • Gábor Borbély
    Affiliations
    Departments of Epidemiology and Neurosurgery, University Medical Center Groningen, University of Groningen, Groningen, the Netherlands
    Search for articles by this author
  • György Áfra
    Affiliations
    Departments of Epidemiology and Neurosurgery, University Medical Center Groningen, University of Groningen, Groningen, the Netherlands
    Search for articles by this author
  • Emese Reichardt-Varga
    Affiliations
    Departments of Epidemiology and Neurosurgery, University Medical Center Groningen, University of Groningen, Groningen, the Netherlands
    Search for articles by this author
  • Gergely Sántha
    Affiliations
    Departments of Epidemiology and Neurosurgery, University Medical Center Groningen, University of Groningen, Groningen, the Netherlands
    Search for articles by this author
  • József Tollár
    Correspondence
    Corresponding author József Tollár, Somogy County Kaposi Mór Teaching Hospital, Kaposvár, Tallián Gyula St 20-32, H-7400, Hungary.
    Affiliations
    Somogy County Kaposi Mór Teaching Hospital, Kaposvár, Hungary

    Departments of Epidemiology and Neurosurgery, University Medical Center Groningen, University of Groningen, Groningen, the Netherlands

    University of Pécs, Faculty of Health Sciences, Doctoral School of Health Sciences, Pécs, Hungary

    Department of Dentistry, Oral and Maxillofacial Surgery, Pécs, Hungary

    Department of Medical Imaging, Faculty of Health Sciences, University of Pécs, Hungary

    Széchényi István University, Digital Development Center, Győr, Hungary
    Search for articles by this author

      Abstract

      Objective

      To determine the effects of exergaming (EXE) on quality of life (QOL), motor, and clinical symptoms in multiple sclerosis (MS). We compared the effects of EXE, balance (BAL), cycling (CYC), proprioceptive neuromuscular facilitation (PNF), and a standard care wait-listed control group on clinical and motor symptoms and quality of life (QOL) in people with MS (PwMS) and determined the effects of subsequent maintenance programs for 2 years in a hospital setting.

      Design

      A randomized controlled trial, using before-after test design.

      Setting

      University hospital setting.

      Participants

      Of 82 outpatients with MS, 70 were randomized (N=70), and 68 completed the study.

      Interventions

      The initial high-intensity and high-frequency interventions consisted of 25 one-hour sessions over 5 weeks. After the 5-week-long initial intervention, the 2-year-long maintenance programs followed, consisting of 3 sessions per week, each for 1 hour.

      Main Outcome Measures

      The primary outcome: Multiple Sclerosis Impact Scale (MSIS-29). Secondary outcomes: Measures 5 aspects of health-related QOL (EuroQol 5-Dimension questionnaire), Beck Depression Inventory, 6-minute walk test (6MWT), Berg Balance Scale (BBS), Tinetti Assessment Tool (TAT), and static BAL (center of pressure).

      Results

      MSIS-29 improved most in EXE (11 points), BAL (6), and CYC (6) (all P<.05). QOL improved most in EXE (3 points), CYC, and BAL (2) (all P<.05). TAT and BBS improved significantly (P<.05) but similarly (P>.05) in EXE, BAL, and CYC. 6MWT improved most in EXE (57m), BAL (32m), and CYC (19m) (all P<.001). Standing sway did not change. Maintenance programs further increased the initial exercise-induced gains, robustly in EXE.

      Conclusions

      A total of 25 sessions of EXE, BAL, CYC, and PNF, in this order, improved clinical and motor symptoms and QOL, and subsequent 2-year-long thrice weekly maintenance programs further slowed symptom worsening and improved QOL. EXE was the most and PNF was the least effective to improve clinical symptoms, motor function, and QOL in PwMS.

      Keywords

      List of abbreviations:

      BAL (balance), BBS (Berg Balance Scale), CYC (cycling), EQ-5D (EuroQol 5-Dimension questionnaire), EXE (exergaming), MS (multiple sclerosis), MSIS-29 (Multiple Sclerosis Impact Scale), PNF (proprioceptive neuromuscular facilitation), PwMS (people with multiple sclerosis), pη2 (partial eta squared), 6MWT (6-minute walk test), TAT (Tinetti Assessment Tool)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Archives of Physical Medicine and Rehabilitation
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Reich DS
        • Lucchinetti CF
        • Calabresi PA.
        Multiple sclerosis.
        N Engl J Med. 2018; 378: 169-180
        • Centonze D
        • Leocani L
        • Feys P.
        Advances in physical rehabilitation of multiple sclerosis.
        Curr Opin Neurol. 2020; 33: 255-261
        • Lozinski BM
        • Yong VW.
        Exercise and the brain in multiple sclerosis.
        Mult Scler. 2022; 28: 1167-1172
        • Prosperini L
        • Di Filippo M.
        Beyond clinical changes: rehabilitation-induced neuroplasticity in MS.
        Mult Scler. 2019; 25: 1348-1362
        • Silva BA
        • Miglietta EA
        • Ferrari CC.
        Training the brain: could it improve multiple sclerosis treatment?.
        Rev Neurosci. 2020; 31: 779-792
        • Dalmazane M
        • Gallou-Guyot M
        • Compagnat M
        • et al.
        Effects on gait and balance of home-based active video game interventions in persons with multiple sclerosis: a systematic review.
        Mult Scler Relat Disord. 2021; 51102928
        • Devasahayam AJ
        • Downer MB
        • Ploughman M.
        The effects of aerobic exercise on the recovery of walking ability and neuroplasticity in people with multiple sclerosis: a systematic review of animal and clinical studies.
        Mult Scler Int. 2017; 20174815958
        • Kim Y
        • Mehta T
        • Lai B
        • Motl RW.
        Immediate and sustained effects of interventions for changing physical activity in people with multiple sclerosis: meta-analysis of randomized controlled trials.
        Arch Phys Med Rehabil. 2020; 101: 1414-1436
        • Prosperini L
        • Tomassini V
        • Castelli L
        • et al.
        Exergames for balance dysfunction in neurological disability: a meta-analysis with meta-regression.
        J Neurol. 2021; 268: 3223-3237
        • Hansen D
        • Wens I
        • Keytsman C
        • Eijnde BO
        • Dendale P.
        Is long-term exercise intervention effective to improve cardiac autonomic control during exercise in subjects with multiple sclerosis? A randomized controlled trial.
        Eur J Phys Rehabil Med. 2015; 51: 223-231
        • Schmidt S
        • Wonneberger M.
        Long-term endurance exercise improves aerobic capacity in patients with relapsing-remitting multiple sclerosis: impact of baseline fatigue.
        J Neurol Sci. 2014; 336: 29-35
        • Romberg A
        • Virtanen A
        • Ruutiainen J.
        Long-term exercise improves functional impairment but not quality of life in multiple sclerosis.
        J Neurol. 2005; 252: 839-845
        • Collett J
        • Dawes H
        • Meaney A
        • et al.
        Exercise for multiple sclerosis: a single-blind randomized trial comparing three exercise intensities.
        Mult Scler. 2011; 17: 594-603
        • Dennett R
        • Madsen LT
        • Connolly L
        • Hosking J
        • Dalgas U
        • Freeman J.
        Adherence and drop-out in randomized controlled trials of exercise interventions in people with multiple sclerosis: A systematic review and meta-analyses.
        Mult Scler Relat Disord. 2020; 43102169
        • Reynolds ER
        • Ashbaugh AD
        • Hockenberry BJ
        • McGrew CA.
        Multiple sclerosis and exercise: a literature review.
        Curr Sports Med Rep. 2018; 17: 31-35
        • Parra-Moreno M
        • Rodriguez-Juan JJ
        • Ruiz-Cardenas JD.
        Use of commercial video games to improve postural balance in patients with multiple sclerosis: a systematic review and meta-analysis of randomised controlled clinical trials.
        Neurologia (Engl Ed). 2018 Mar 7; ([Epub ahead of print])
        • Motl RW
        • Sandroff BM
        • Kwakkel G
        • et al.
        Exercise in patients with multiple sclerosis.
        Lancet Neurol. 2017; 16: 848-856
        • Baird JF
        • Motl RW.
        Response heterogeneity with exercise training and physical activity interventions among persons with multiple sclerosis.
        Neurorehabil Neural Repair. 2019; 33: 3-14
        • Kerling A
        • Keweloh K
        • Tegtbur U
        • et al.
        Effects of a short physical exercise intervention on patients with multiple sclerosis (MS).
        Int J Mol Sci. 2015; 16: 15761-15775
        • Kramer A
        • Dettmers C
        • Gruber M.
        Exergaming with additional postural demands improves balance and gait in patients with multiple sclerosis as much as conventional balance training and leads to high adherence to home-based balance training.
        Arch Phys Med Rehabil. 2014; 95: 1803-1809
        • Cakt BD
        • Nacir B
        • Genc H
        • et al.
        Cycling progressive resistance training for people with multiple sclerosis: a randomized controlled study.
        Am J Phys Med Rehabil. 2010; 89: 446-457
        • Rasova K
        • Havrdova E
        • Brandejsky P
        • Zalisova M
        • Foubikova B
        • Martinkova P.
        Comparison of the influence of different rehabilitation programmes on clinical, spirometric and spiroergometric parameters in patients with multiple sclerosis.
        Mult Scler. 2006; 12: 227-234
        • Razazian N
        • Yavari Z
        • Farnia V
        • et al.
        Exercising impacts on fatigue, depression, and paresthesia in female patients with multiple sclerosis.
        Med Sci Sports Exerc. 2016; 48: 796-803
        • Sadeghi Bahmani D
        • Razazian N
        • Farnia V
        • Alikhani M
        • Tatari F
        • Brand S.
        Compared to an active control condition, in persons with multiple sclerosis two different types of exercise training improved sleep and depression, but not fatigue, paresthesia, and intolerance of uncertainty.
        Mult Scler Relat Disord. 2019; 36101356
        • Korkmaz NC
        • Kirdi N
        • Temucin CM
        • Armutlu K
        • Yakut Y
        • Karabudak R.
        Improvement of muscle strength and fatigue with high voltage pulsed galvanic stimulation in multiple sclerosis patients–a non-randomized controlled trial.
        J Pak Med Assoc. 2011; 61: 736-743
        • Yazgan YZ
        • Tarakci E
        • Tarakci D
        • Ozdincler AR
        • Kurtuncu M.
        Comparison of the effects of two different exergaming systems on balance, functionality, fatigue, and quality of life in people with multiple sclerosis: a randomized controlled trial.
        Mult Scler Relat Disord. 2019; 39101902
        • Tollár J
        • Nagy F
        • Tóth BE
        • et al.
        Exercise effects on multiple sclerosis quality of life and clinical-motor symptoms.
        Med Sci Sports Exerc. 2020; 52: 1007-1014
        • Tollár J
        • Nagy F
        • Hortobágyi T.
        Vastly different exercise programs similarly improve parkinsonian symptoms: a randomized clinical trial.
        Gerontology. 2019; 65: 120-127
        • Tollár J
        • Nagy F
        • Kovács N
        • Hortobágyi T.
        A high-intensity multicomponent agility intervention improves Parkinson patients' clinical and motor symptoms.
        Arch Phys Med Rehabil. 2018; 99: 2478-2484
        • Tollár J
        • Nagy F
        • Kovács N
        • Hortobágyi T.
        Two-year agility maintenance training slows the progression of parkinsonian symptoms.
        Med Sci Sports Exerc. 2019; 51: 237-245
        • Tollár J
        • Nagy F
        • Moizs M
        • Tóth BE
        • Sanders LMJ
        • Hortobágyi T.
        Diverse exercises similarly reduce older adults' mobility limitations.
        Med Sci Sports Exerc. 2019; 51: 1809-1816
        • Hobart J
        • Lamping D
        • Fitzpatrick R
        • Riazi A
        • Thompson A.
        The Multiple Sclerosis Impact Scale (MSIS-29): a new patient-based outcome measure.
        Brain. 2001; 124: 962-973
        • Riazi A
        • Hobart JC
        • Lamping DL
        • Fitzpatrick R
        • Thompson AJ.
        Multiple Sclerosis Impact Scale (MSIS-29): reliability and validity in hospital based samples.
        J Neurol Neurosurg Psychiatry. 2002; 73: 701-704
        • Kuspinar A
        • Mayo NE.
        A review of the psychometric properties of generic utility measures in multiple sclerosis.
        Pharmacoeconomics. 2014; 32: 759-773
        • Subica AM
        • Fowler JC
        • Elhai JD
        • et al.
        Factor structure and diagnostic validity of the Beck Depression Inventory-II with adult clinical inpatients: comparison to a gold-standard diagnostic interview.
        Psychol Assess. 2014; 26: 1106-1115
        • Kegelmeyer DA
        • Kloos AD
        • Thomas KM
        • Kostyk SK.
        Reliability and validity of the Tinetti Mobility Test for individuals with Parkinson disease.
        Phys Ther. 2007; 87: 1369-1378
        • Cattaneo D
        • Regola A
        • Meotti M.
        Validity of six balance disorders scales in persons with multiple sclerosis.
        Disabil Rehabil. 2006; 28: 789-795
        • Decavel P
        • Moulin T
        • Sagawa Jr., Y
        Gait tests in multiple sclerosis: reliability and cut-off values.
        Gait Posture. 2019; 67: 37-42
        • Wajda DA
        • Motl RW
        • Sosnoff JJ.
        Three-month test-retest reliability of center of pressure motion during standing balance in individuals with multiple sclerosis.
        Int J MS Care. 2016; 18: 59-62
        • Faul F
        • Erdfelder E
        • Lang AG
        • Buchner A.
        G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences.
        Behav Res Methods. 2007; 39: 175-191
        • Costelloe L
        • O'Rourke K
        • Kearney H
        • et al.
        The patient knows best: significant change in the physical component of the Multiple Sclerosis Impact Scale (MSIS-29 physical).
        J Neurol Neurosurg Psychiatry. 2007; 78: 841-844
        • Cohen J.
        Statistical power for the behavioral sciences.
        Erblaum, Hillsdale, NJ1988
        • Garrett M
        • Hogan N
        • Larkin A
        • Saunders J
        • Jakeman P
        • Coote S.
        Exercise in the community for people with minimal gait impairment due to MS: an assessor-blind randomized controlled trial.
        Mult Scler. 2013; 19: 782-789
        • Prosperini L
        • Fortuna D
        • Gianni C
        • Leonardi L
        • Marchetti MR
        • Pozzilli C.
        Home-based balance training using the Wii balance board: a randomized, crossover pilot study in multiple sclerosis.
        Neurorehabil Neural Repair. 2013; 27: 516-525
        • Di Tella S
        • Pagliari C
        • Blasi V
        • Mendozzi L
        • Rovaris M
        • Baglio F.
        Integrated telerehabilitation approach in multiple sclerosis: a systematic review and meta-analysis.
        J Telemed Telecare. 2020; 26: 385-399
        • Wiles CM
        • Newcombe RG
        • Fuller KJ
        • et al.
        Controlled randomised crossover trial of the effects of physiotherapy on mobility in chronic multiple sclerosis.
        J Neurol Neurosurg Psychiatry. 2001; 70: 174-179
        • Edwards T
        • Pilutti LA.
        The effect of exercise training in adults with multiple sclerosis with severe mobility disability: a systematic review and future research directions.
        Mult Scler Relat Disord. 2017; 16: 31-39
        • Latimer-Cheung AE
        • Pilutti LA
        • Hicks AL
        • et al.
        Effects of exercise training on fitness, mobility, fatigue, and health-related quality of life among adults with multiple sclerosis: a systematic review to inform guideline development.
        Arch Phys Med Rehabil. 2013; 94: 1800-1828
        • Brichetto G
        • Spallarossa P
        • de Carvalho ML
        • Battaglia MA.
        The effect of Nintendo(R) Wii(R) on balance in people with multiple sclerosis: a pilot randomized control study.
        Mult Scler. 2013; 19: 1219-1221
        • Straudi S
        • Fanciullacci C
        • Martinuzzi C
        • et al.
        The effects of robot-assisted gait training in progressive multiple sclerosis: a randomized controlled trial.
        Mult Scler. 2016; 22: 373-384
        • Timmermans ST
        • de Groot V
        • Beckerman H.
        Ten-year disease progression in multiple sclerosis: walking declines more rapidly than arm and hand function.
        Mult Scler Relat Disord. 2020; 45102343
        • Hvid LG
        • Feys P
        • Baert I
        • Kalron A
        • Dalgas U.
        Accelerated trajectories of walking capacity across the adult life span in persons with multiple sclerosis: an underrecognized challenge.
        Neurorehabil Neural Repair. 2020; 34: 360-369
        • Zaenker P
        • Favret F
        • Lonsdorfer E
        • Muff G
        • de Seze J
        • Isner-Horobeti ME.
        High-intensity interval training combined with resistance training improves physiological capacities, strength and quality of life in multiple sclerosis patients: a pilot study.
        Eur J Phys Rehabil Med. 2018; 54: 58-67
        • Wens I
        • Dalgas U
        • Vandenabeele F
        • et al.
        High intensity aerobic and resistance exercise can improve glucose tolerance in persons with multiple sclerosis: a randomized controlled trial.
        Am J Phys Med Rehabil. 2017; 96: 161-166
        • Orban A
        • Garg B
        • Sammi MK
        • et al.
        Effect of high-intensity exercise on multiple sclerosis function and phosphorous magnetic resonance spectroscopy outcomes.
        Med Sci Sports Exerc. 2019; 51: 1380-1386
        • Manca A
        • Martinez G
        • Cereatti A
        • et al.
        Isokinetic predictors of gait speed increase following high-intensity resistance training of the ankle dorsiflexors in people with multiple sclerosis: a pilot study.
        Clin Biomech (Bristol, Avon). 2019; 67: 102-106
        • Keytsman C
        • Hansen D
        • Wens I
        • O Eijnde B
        Impact of high-intensity concurrent training on cardiovascular risk factors in persons with multiple sclerosis - pilot study.
        Disabil Rehabil. 2019; 41: 430-435
        • Thomas S
        • Fazakarley L
        • Thomas PW
        • et al.
        Mii-vitaliSe: a pilot randomised controlled trial of a home gaming system (Nintendo Wii) to increase activity levels, vitality and well-being in people with multiple sclerosis.
        BMJ Open. 2017; 7e016966
        • Steen Krawcyk R
        • Vinther A
        • Petersen NC
        • et al.
        Effect of home-based high-intensity interval training in patients with lacunar stroke: a randomized controlled trial.
        Front Neurol. 2019; 10: 664
        • Kolmos M
        • Krawcyk RS
        • Kruuse C.
        Effect of high-intensity training on endothelial function in patients with cardiovascular and cerebrovascular disease: a systematic review.
        SAGE Open Med. 2016; 42050312116682253