Effects and optimal dosage of resistance training on strength, functional capacity, balance, general health perception, and fatigue in people with multiple sclerosis: a systematic review and meta-analysis

References

• Kuhlmann T, Ludwin S, Prat A, et al. An updated histological classification system for multiple sclerosis lesions. Acta Neuropathol. 2017;133(1):13–24.
   PubMed Web of Science ®Google Scholar
• Jørgensen MLK, Dalgas U, Wens I, et al. Muscle strength and power in persons with multiple sclerosis – a systematic review and meta-analysis. J Neurol Sci. 2017;376:225–241.
   PubMed Web of Science ®Google Scholar
• Wens I, Dalgas U, Vandenabeele F, et al. Multiple sclerosis affects skeletal muscle characteristics. PLOS One. 2014;9(9):e108158.
   PubMed Web of Science ®Google Scholar
• Charron S, McKay KA, Tremlett H. Physical activity and disability outcomes in multiple sclerosis: a systematic review (2011-2016)). Mult Scler Relat Disord. 2018;20:169–177.
   PubMed Web of Science ®Google Scholar
• Motl RW, Gosney JL. Effect of exercise training on quality of life in multiple sclerosis: a meta-analysis. Mult Scler. 2008;14(1):129–135.
   PubMed Web of Science ®Google Scholar
• Sokolov AA, Grivaz P, Bove R. Cognitive deficits in multiple sclerosis: recent advances in treatment and neurorehabilitation. Curr Treat Options Neurol. 2018;20(12):53.
   PubMed Web of Science ®Google Scholar
• McDonnell MN, Smith AE, Mackintosh SF. Aerobic exercise to improve cognitive function in adults with neurological disorders: a systematic review. Arch Phys Med Rehabil. 2011;92(7):1044–1052.
   PubMed Web of Science ®Google Scholar
• Sánchez-Lastra MA, Martínez-Aldao D, Molina AJ, et al. Pilates for people with multiple sclerosis: a systematic review and meta-analysis. Mult Scler Relat Disord. 2019;28:199–212.
   PubMedGoogle Scholar
• Kantele S, Karinkanta S, Sievänen H. Effects of long-term whole-body vibration training on mobility in patients with multiple sclerosis: a meta-analysis of randomized controlled trials. J Neurol Sci. 2015;358(1-2):31–37.
   PubMed Web of Science ®Google Scholar
• Kjølhede T, Vissing K, Dalgas U. Multiple sclerosis and progressive resistance training: a systematic review. Mult Scler. 2012;18(9):1215–1228.
   PubMed Web of Science ®Google Scholar
• Schoenfeld BJ, Ogborn D, Krieger JW. Effects of resistance training frequency on measures of muscle hypertrophy: a systematic review and meta-analysis. Sports Med. 2016;46(11):1689–1697.
   PubMed Web of Science ®Google Scholar
• Schoenfeld BJ, Ogborn D, Krieger JW. Dose-response relationship between weekly resistance training volume and increases in muscle mass: a systematic review and meta-analysis. J Sports Sci. 2017;35(11):1073–1082.
   PubMed Web of Science ®Google Scholar
• Peterson MD, Rhea MR, Alvar BA. Maximizing strength development in athletes: a meta-analysis to determine the dose-response relationship. J Strength Cond Res. 2004;18(2):377–382.
   PubMed Web of Science ®Google Scholar
• Rodrigues JA, Pereira ET, de Oliveira CEP, et al. Effect of strength training on physical and mental health and quality of life of people with spinal cord injury: a literature review. Arch Med Dep. 2020;37(3):192–196.
   Google Scholar
• Cruickshank TM, Reyes AR, Ziman MR. A systematic review and meta-analysis of strength training in individuals with multiple sclerosis or Parkinson disease. Medicine. 2015;94(4):e411.
   PubMed Web of Science ®Google Scholar
• Fimland MS, Helgerud J, Gruber M, et al. Enhanced neural drive after maximal strength training in multiple sclerosis patients. Eur J Appl Physiol. 2010;110(2):435–443.
   PubMed Web of Science ®Google Scholar
• Romberg A, Virtanen A, Ruutiainen R. Long-term exercise improves functional impairment but not quality of life in multiple sclerosis. J Neurol. 2005;252(7):839–845.
   PubMed Web of Science ®Google Scholar
• Garrett M, Hogan N, Larkin A, et al. Exercise in the community for people with minimal gait impairment due to MS: an assessor-blind randomized controlled trial. Mult Scler. 2013;19(6):782–789.
   PubMed Web of Science ®Google Scholar
• Manca A, Cabboi MP, Dragone D, et al. Resistance training for muscle weakness in multiple sclerosis: direct versus contralateral approach in individuals with ankle Dorsiflexors' Disparity in Strength. Arch Phys Med Rehabil. 2017;98(7):1348–1356.
   PubMed Web of Science ®Google Scholar
• Keser I, Meric A, Kirdi N, et al. Comparing routine neurorehabilitation programme with callisthenic exercises in multiple sclerosis. NeuroRehabilitation. 2011;29(1):91–98.
   PubMed Web of Science ®Google Scholar
• White LJ, McCoy SC, Castellano V, et al. Resistance training improves strength and functional capacity in persons with multiple sclerosis. Mult Scler. 2004;10(6):668–674.
   PubMed Web of Science ®Google Scholar
• Kjølhede T, Vissing K, De Place L, et al. Neuromuscular adaptations to long-term progressive resistance training translates to improved functional capacity for people with multiple sclerosis and is maintained at follow-up. Mult Scler. 2015;21(5):599–611.
   PubMed Web of Science ®Google Scholar
• Torres Pareja M, Peinado Palomino D, Vaquerizo García J, et al. Evaluación de un programa de entrenamiento de fuerza en personas con esclerosis múltiple. CCD. 2019;14(42):265–275.
   Google Scholar
• Karpatkin HI, Cohen ET, Klein S, et al. The effect of maximal strength training on strength, walking, and balance in people with multiple sclerosis: a pilot study. Mult Scler Int. 2016;2016(6):5235971.
   PubMedGoogle Scholar
• Sabapathy NM, Minahan CL, Turner GT, et al. Comparing endurance- and resistance-exercise training in people with multiple sclerosis: a randomized pilot study. Clin Rehabil. 2011;25(1):14–24.
   PubMed Web of Science ®Google Scholar
• Platta ME, Ensari I, Motl RW, et al. Effect of exercise training on fitness in multiple sclerosis: a meta-analysis. Arch Phys Med Rehabil. 2016;97(9):1564–1572.
   PubMed Web of Science ®Google Scholar
• Bosnak-Guclu M, Guclu-Gunduz A, Nazliel B, et al. Comparison of functional exercise capacity, pulmonary function and respiratory muscle strength in patients with multiple sclerosis with different disability levels and healthy controls. J Rehabil Med. 2012;44(1):80–86.
   PubMed Web of Science ®Google Scholar
• Citaker S, Guclu-Gunduz A, Yazici G, et al. Relationship between lower extremity isometric muscle strength and standing balance in patients with multiple sclerosis. NRE. 2013;33(2):293–298.
   PubMedGoogle Scholar
• Sosnoff JJ, Socie MJ, Boes MK, et al. Mobility, balance and falls in persons with multiple sclerosis. PLOS One. 2011;6(11):e28021.
   PubMed Web of Science ®Google Scholar
• Bento PCB, Pereira G, Ugrinowitsch C, et al. Peak torque and rate of torque development in elderly with and without fall history. Clin Biomech. 2010;25(5):450–454.
   PubMed Web of Science ®Google Scholar
• Flachenecker P, Kümpfel T, Kallmann B, et al. Fatigue in multiple sclerosis: a comparison of different rating scales and correlation to clinical parameters. Mult Scler. 2002;8(6):523–526.
   PubMed Web of Science ®Google Scholar
• Kalron A. The correlation between symptomatic fatigue to definite measures of gait in people with multiple sclerosis. Gait Posture. 2016;44:178–183.
   PubMed Web of Science ®Google Scholar
• Andreasen AK, Stenager E, Dalgas U. The effect of exercise therapy on fatigue in multiple sclerosis. Mult Scler. 2011;17(9):1041–1054.
   PubMed Web of Science ®Google Scholar
• Motl RW, Pilutti LA. Is physical exercise a multiple sclerosis disease modifying treatment? Expert Rev Neurother. 2016;16(8):951–960.
   PubMed Web of Science ®Google Scholar
• Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta analyses: the PRISMA statement. PLOS Med 2009;6(7): e1000097.
   PubMed Web of Science ®Google Scholar
• Thompson AJ, Banwell BL, Barkhof F, et al. Diagnosis of multiple sclerosis: 2017 revisions of the McDonald criteria. Lancet Neurol. 2018;17(2):162–173.
   PubMed Web of Science ®Google Scholar
• Akobeng AK. Principles of evidence based medicine. Arch Dis Child. 2005;90(8):837–840.
   PubMed Web of Science ®Google Scholar
• Higgins JPT, Altman DG, Gøtzsche PC, et al. The Cochrane Collaboration's tool for assessing risk of bias in randomised trials. BMJ. 2011;343:d5928.
   PubMed Web of Science ®Google Scholar
• Egger M, Smith GD, Schneider M, et al. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315(7109):629–634.
   PubMed Web of Science ®Google Scholar
• Higgins JPT. Cochrane handbook for systematic reviews of interventions. Version 5.1.0. Chichester (England). Cochrane Collab; 2011.
   Google Scholar
• Cohen J. Statistical power analysis for the behavioral sciences. New York (USA): Lawrence Erlbaum Associates; 2013.
   Google Scholar
• Hoffman JR editor. NSCA’s guide to program design. Champaign (IL): Human Kinetics; 2012.
   Google Scholar
• Souza EO, Ugrinowitsch C, Tricoli V, et al. Early adaptations to six weeks of non-periodized and periodized strength training regimens in recreational males. J Sport Sci Med. 2014;13(3):604–609.
   PubMed Web of Science ®Google Scholar
• Higgins JPT, Altman DG, Sterne JAC. Chapter 8: assessing risk of bias in included studies. In Cochrane handbook for systematic reviews of interventions. Version 5.1.0. Chichester (England): The Cochrane Collaboration; 2011.
   Google Scholar
• Broekmans T, Roelants M, Feys P, et al. Effects of long-term resistance training and simultaneous electro-stimulation on muscle strength and functional mobility in multiple sclerosis. Mult Scler. 2011;17(4):468–477.
   PubMed Web of Science ®Google Scholar
• Callesen J, Cattaneo D, Brincks J, et al. How does strength training and balance training affect gait and fatigue in patients with multiple sclerosis? A study protocol of a randomized controlled trial. NeuroRehabilitation. 2018;42(2):131–142.
   PubMed Web of Science ®Google Scholar
• Dalgas U, Stenager E, Jakobsen J, et al. Fatigue, mood and quality of life improve in MS patients after progressive resistance training. Mult Scler. 2010;16(4):480–490.
   PubMed Web of Science ®Google Scholar
• Dalgas U, Stenager E, Jakobsen J, et al. Resistance training improves muscle strength and functional capacity in multiple sclerosis. Neurology. 2009;73(18):1478–1674.
   PubMed Web of Science ®Google Scholar
• de Souza-Teixeira F, Costilla S, Ayán C, et al. Effects of resistance training in multiple sclerosis. Int J Sports Med. 2009;30(04):245–250.
   PubMedGoogle Scholar
• Dodd KJ, Taylor NF, Shields N, et al. Progressive resistance training did not improve walking but can improve muscle performance, quality of life and fatigue in adults with multiple sclerosis: a randomized controlled trial. Mult Scler. 2011;17(11):1362–1374.
   PubMed Web of Science ®Google Scholar
• Frevel D, Mäurer M. Internet-based home training is capable to improve balance in multiple sclerosis: a randomized controlled trial. Eur J Phys Rehabil Med. 2015;51(1):23–30.
   PubMed Web of Science ®Google Scholar
• Hogan N, Kehoe M, Larkin A, et al. The effect of community exercise interventions for people with MS who use bilateral support for gait. Mult Scler Int. 2014;2014:109142.
   PubMedGoogle Scholar
• Medina-Perez C, De Souza-Teixeira F, Fernandez-Gonzalo R, et al. Effects of a resistance training program and subsequent detraining on muscle strength and muscle power in multiple sclerosis patients. NeuroRehabilitation. 2014;34(3):523–530.
   PubMed Web of Science ®Google Scholar
• Moradi M, Sahraian MA, Aghsaie A, et al. Effects of eight-week resistance training program in men with multiple sclerosis. Asian J Sports Med. 2015;6(2):e22838.
   PubMedGoogle Scholar
• DeBolt LS, McCubbin JA. The effects of home-based resistance exercise on balance, power, and mobility in adults with multiple sclerosis. Arch Phys Med Rehabil. 2004;85(2):290–297.
   PubMed Web of Science ®Google Scholar
• Coote S, Hughes L, Rainsford G, et al. Pilot randomized trial of progressive resistance exercise augmented by neuromuscular electrical stimulation for people with multiple sclerosis who use walking aids. Arch Phys Med Rehabil. 2015;96(2):197–204.
   PubMed Web of Science ®Google Scholar
• Patrocinio de Oliveira CE, Moreira OC, Carrión-Yagual ZM, et al. Effects of classic progressive resistance training versus eccentric-enhanced resistance training in people with multiple sclerosis. Arch Phys Med Rehabil. 2018;99(5):819–825.
   PubMed Web of Science ®Google Scholar
• Hayes HA, Gappmaier E, Lastayo PC. Effects of high-intensity resistance training on strength, mobility, balance, and fatigue in individuals with multiple sclerosis: a randomized controlled trial. J Neurol Phys Ther. 2011;35(1):2–10.
   PubMed Web of Science ®Google Scholar
• Jonsdottir J, Gervasoni E, Bowman T, et al. Intensive multimodal training to improve gait resistance, mobility, balance and cognitive function in persons with multiple sclerosis: a pilot randomized controlled trial. Front Neurol. 2018;28(9):800.
   Google Scholar
• Teixeira F de S, Gonzalo RF, Murúa JAH, et al. Elastic band training for multiple sclerosis patients: a pilot study. J Phys Ther Sci. 2011;23(2):307–311.
   Google Scholar
• Eftekhari E, Mostahfezian M, Etemadifar M, et al. Resistance training and vibration improve muscle strength and functional capacity in female patients with multiple sclerosis. Asian J Sports Med. 2012;3(4):279–284.
   PubMedGoogle Scholar
• Filipi ML, Kucera DL, Filipi EO, et al. Improvement in strength following resistance training in MS patients despite varied disability levels. NRE. 2011;28(4):373–382.
   Google Scholar
• Gonzales B, Chopard G, Charry B, et al. Effects of a training program involving body cooling on physical and cognitive capacities and quality of life in multiple sclerosis patients: a pilot study. Eur Neurol. 2017;78(1-2):71–77.
   PubMed Web of Science ®Google Scholar
• Gutierrez GM, Chow JW, Tillman MD, et al. Resistance training improves gait kinematics in persons with multiple sclerosis. Arch Phys Med Rehabil. 2005;86(9):1824–1829.
   PubMed Web of Science ®Google Scholar
• Hameau S, Bensmail D, Roche N, et al. Adaptations of fatigue and fatigability after a short intensive, combined rehabilitation program in patients with multiple sclerosis. J Rehabil Med. 2018;50(1):59–66.
   PubMed Web of Science ®Google Scholar
• Heine M, Richards R, Geurtz B, et al. Preliminary effectiveness of a sequential exercise intervention on gait function in ambulant patients with multiple sclerosis – a pilot study. Clin Biomech. 2019;62:1–6.
   PubMed Web of Science ®Google Scholar
• Kierkegaard M, Lundberg IE, Olsson T, et al. High-intensity resistance training in multiple sclerosis – an exploratory study of effects on immune markers in blood and cerebrospinal fluid, and on mood, fatigue, health-related quality of life, muscle strength, walking and cognition. J Neurol Sci. 2016;362:251–257.
   PubMed Web of Science ®Google Scholar
• Kratz AL, Atalla M, Whibley D, et al. Calling out MS fatigue: feasibility and preliminary effects of a pilot randomized telephone-delivered exercise intervention for multiple sclerosis fatigue. J Neurol Phys Ther. 2020;44(1):23–31.
   PubMed Web of Science ®Google Scholar
• Manca A, Cabboi MP, Ortu E, et al. Effect of contralateral strength training on muscle weakness in people with multiple sclerosis: proof-of-concept case series. Phys Ther. 2016;96(6):828–838.
   PubMed Web of Science ®Google Scholar
• Manca A, Dvir Z, Dragone D, et al. Time course of strength adaptations following high-intensity resistance training in individuals with multiple sclerosis. Eur J Appl Physiol. 2017;117(4):731–743.
   PubMed Web of Science ®Google Scholar
• 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. 2019;67:102–106.
   PubMed Web of Science ®Google Scholar
• Mañago MM, Hebert JR, Kittelson J, et al. Feasibility of a targeted strengthening program to improve gait in people with multiple sclerosis: a brief report. Int J Rehabil Res. 2018;41(4):364–367.
   PubMed Web of Science ®Google Scholar
• Roppolo M, Mulasso A, Gollin M, et al. The role of fatigue in the associations between exercise and psychological health in multiple sclerosis: direct and indirect effects. Ment Health Phys Act. 2013;6(2):87–94.
   Web of Science ®Google Scholar
• Taylor NF, Dodd KJ, Prasad D, et al. Progressive resistance exercise for people with multiple sclerosis. Disabil Rehabil. 2006;28(18):1119–1126.
   PubMed Web of Science ®Google Scholar
• Hosseini SS, Rajabi H, Sahraian MA, et al. Effects of 8-week home-based yoga and resistance training on muscle strength, functional capacity and balance in patients with multiple sclerosis: a randomized controlled study. Asian J Sports Med. 2018;9(3):9.
   Google Scholar
• Moghadasi A, Ghasemi G, Sadeghi-Demneh E, et al. The effect of total body resistance exercise on mobility, proprioception, and muscle strength of the knee in people with multiple sclerosis. J Sport Rehabil. 2020;29(2):192–199.
   PubMed Web of Science ®Google Scholar
• Gomez-Illan R, Reina R, Barbado D, et al. Effects of maximal strength training on perceived-fatigue and functional mobility in persons with relapsing-remitting multiple sclerosis. Medicina. 2020;56(12):711–718.
   PubMedGoogle Scholar
• Andreu-Caravaca L, Ramos-Campo DJ, Chung LH, et al. Fast-velocity resistance training improves force development and mobility in multiple sclerosis. Int J Sports Med. 2021;1:1–7.
   Google Scholar
• Aidar FJ, Carneiro AL, Costa Moreira O, et al. Effects of resistance training on the physical condition of people with multiple sclerosis. J Sports Med Phys Fitness. 2018;58(7–8):1127–1134.
   PubMed Web of Science ®Google Scholar
• Akbar N, Sandroff BM, Wylie GR, et al. Progressive resistance exercise training and changes in resting-state functional connectivity of the caudate in persons with multiple sclerosis and severe fatigue: a proof-of-concept study. Neuropsychol Rehabil. 2020;30(1):54–66.
   PubMed Web of Science ®Google Scholar
• Kera T, Kawai H, Takahashi J, et al. Association between ground reaction force in sit-to-stand motion and falls in community-dwelling older Japanese individuals. Arch Gerontol Geriatr. 2020;91:104221.
   PubMed Web of Science ®Google Scholar
• Kjølhede T, Vissing K, Langeskov-Christensen D, et al. Relationship between muscle strength parameters and functional capacity in persons with mild to moderate degree multiple sclerosis. Mult Scler Relat Disord. 2015;4(2):151–158.
   PubMed Web of Science ®Google Scholar
• Ramari C, Moraes AG, Tauil CB, et al. Knee flexor strength and balance control impairment may explain declines during prolonged walking in women with mild multiple sclerosis. Mult Scler Relat Disord. 2018;20:181–185.
   PubMed Web of Science ®Google Scholar
• Yahia A, Ghroubi S, Mhiri C, et al. Relationship between muscular strength, gait and postural parameters in multiple sclerosis. Ann Phys Rehabil Med. 2011;54(3):144–155.
   PubMedGoogle Scholar
• Thoumie P, Lamotte D, Cantalloube S, et al. Motor determinants of gait in 100 ambulatory patients with multiple sclerosis. Mult Scler. 2005;11(4):485–491.
   PubMed Web of Science ®Google Scholar
• Broekmans T, Gijbels D, Eijnde BO, et al. The relationship between upper leg muscle strength and walking capacity in persons with multiple sclerosis. Mult Scler. 2013;19(1):112–119.
   PubMed Web of Science ®Google Scholar
• Thoumie P, Mevellec E. Relation between walking speed and muscle strength is affected by somatosensory loss in multiple sclerosis. J Neurol Neurosurg Psychiatry. 2002;73(3):313–315.
   PubMed Web of Science ®Google Scholar
• Emerson NS, Stout JR, Fukuda DH, et al. Resistance training improves capacity to delay neuromuscular fatigue in older adults. Arch Gerontol Geriatr. 2015;61(1):27–32.
   PubMed Web of Science ®Google Scholar
• Razazian N, Kazeminia M, Moayedi H, et al. The impact of physical exercise on the fatigue symptoms in patients with multiple sclerosis: a systematic review and meta-analysis. BMC Neurol. 2020;20(1):93.
   PubMed Web of Science ®Google Scholar
• Asano M, Finlayson ML. Meta-analysis of three different types of fatigue management interventions for people with multiple sclerosis: exercise, education, and medication. Mult Scler Int. 2014;2014:798285.
   PubMedGoogle Scholar
• Krupp LB, Pollina DA. Mechanisms and management of fatigue in progressive neurological disorders. Curr Opin Neurol. 1996;9(6):456–460.
   PubMed Web of Science ®Google Scholar
• Newman MA, Dawes H, van den Berg M, et al. Can aerobic treadmill training reduce the effort of walking and fatigue in people with multiple sclerosis: a pilot study. Mult Scler. 2007;13(1):113–119.
   PubMedGoogle Scholar
• Taul-Madsen L, Connolly L, Dennett R, et al. Is aerobic or resistance training the most effective exercise modality for improving lower extremity physical function and perceived fatigue in people with multiple sclerosis? A systematic review and meta-analysis. Arch Phys Med Rehabil. 2021;102(10):2032–2048.
   PubMed Web of Science ®Google Scholar
• Jenkins NDM, Miramonti AA, Hill EC, et al. Greater neural adaptations following high- vs. low-load resistance training. Front Physiol. 2017;29:8. 331.
   Google Scholar
• Blazevich AJ, Wilson CJ, Alcaraz PE, et al. Effects of resistance training movement pattern and velocity on isometric muscular rate of force development: a systematic review with meta-analysis and meta-regression. Sports Med. 2020;50(5):943–963.
   PubMed Web of Science ®Google Scholar
• Balso C, Cafarelli E. Adaptations in the activation of human skeletal muscle induced by short-term isometric resistance training. J Appl Physiol. 2007;103(1):402–411.
   PubMed Web of Science ®Google Scholar
• Aagaard P, Simonsen EB, Andersen JL, et al. Neural adaptation to resistance training: changes in evoked V-wave and H-reflex responses. J Appl Physiol. 2002;92(6):2309–2318.
   PubMed Web of Science ®Google Scholar
• Folland JP, Williams AG. The adaptations to strength training: morphological and neurological contributions to increased strength. Sports Med. 2007;37(2):145–168.
   PubMed Web of Science ®Google Scholar
• Grgic J, Schoenfeld BJ, Davies TB, et al. Effect of resistance training frequency on gains in muscular strength: a systematic review and meta-analysis. Sports Med. 2018;48(5):1207–1220.
   PubMed Web of Science ®Google Scholar
• Brigatto FA, Braz TV, Zanini TC da C, et al. Effect of resistance training frequency on neuromuscular performance and muscle morphology after 8 weeks in trained men. J Strength Cond Res. 2019;33(8):2104–2116.
   PubMed Web of Science ®Google Scholar
• Veldhuijzen Van Zanten JJCS, Pilutti LA, Duda JL, et al. Sedentary behaviour in people with multiple sclerosis: is it time to stand up against MS? Mult Scler. 2016;22(10):1250–1256.
   PubMed Web of Science ®Google Scholar
• Cuijpers P, Weitz E, Cristea IA, et al. Pre-post effect sizes should be avoided in meta-analyses. Epidemiol Psychiatr Sci. 2017;26(4):364–368.
   PubMed Web of Science ®Google Scholar