The cost of imbalance: how balance problems drive energy cost of walking in persons with multiple sclerosis

Authors

  • Sjoerd T. Timmermans Amsterdam UMC location Vrije Universiteit Amsterdam, Rehabilitation Medicine, Amsterdam, the Netherlands; MS Center Amsterdam, Amsterdam UMC location Vrije Universiteit, Amsterdam, The Netherlands; Amsterdam Movement Sciences, Rehabilitation & Development, Amsterdam, The Netherlands
  • Arianne S. Gravesteijn Amsterdam UMC location Vrije Universiteit Amsterdam, Rehabilitation Medicine, Amsterdam, the Netherlands; MS Center Amsterdam, Amsterdam UMC location Vrije Universiteit, Amsterdam, The Netherlands; Amsterdam Movement Sciences, Rehabilitation & Development, Amsterdam, The Netherlands; Amsterdam Neuroscience, Neuroinfection and Inflammation Amsterdam, The Netherlands; Amsterdam Movement Sciences, Ageing & Vitality, Amsterdam, The Netherlands
  • Koen Wishaupt Maastricht University, NUTRIM School of Nutrition and Translational Research in Metabolism, Department of Nutrition and Movement Sciences, Maastricht, The Netherlands
  • Heleen Beckerman Amsterdam UMC location Vrije Universiteit Amsterdam, Rehabilitation Medicine, Amsterdam, the Netherlands; MS Center Amsterdam, Amsterdam UMC location Vrije Universiteit, Amsterdam, The Netherlands; Amsterdam Movement Sciences, Rehabilitation & Development, Amsterdam, The Netherlands
  • Marjolein M. van der Krogt Amsterdam UMC location Vrije Universiteit Amsterdam, Rehabilitation Medicine, Amsterdam, the Netherlands; Amsterdam Movement Sciences, Rehabilitation & Development, Amsterdam, The Netherlands
  • Vincent de Groot Amsterdam UMC location Vrije Universiteit Amsterdam, Rehabilitation Medicine, Amsterdam, the Netherlands; MS Center Amsterdam, Amsterdam UMC location Vrije Universiteit, Amsterdam, The Netherlands; Amsterdam Movement Sciences, Rehabilitation & Development, Amsterdam, The Netherlands

DOI:

https://doi.org/10.2340/jrm.v58.45814

Keywords:

multiple sclerosis, balance, walking speed, energy cost of walking

Abstract

Introduction: People with multiple sclerosis have difficulties walking and show a high energy cost of walking. Balance problems may contribute.

Aim: To investigate the relationship between dynamic balance and energy cost of walking in people with multiple sclerosis, and whether walking speed affects this relationship.

Methods: In a cross-sectional cohort, 20 people with multiple sclerosis walked on an instrumented treadmill at a comfortable and fast walking speed. The energy cost of walking was derived from oxygen consumption. Dynamic balance was approximated as the medio-lateral margin of stability and using balance board testing. Linear mixed models were used, with walking speed as effect modifier.

Results: The mean energy cost of walking was 4.99 J/kg/m at a comfortable and 4.84 J/kg/m at a fast walking speed. The medio-lateral margin of stability was significantly associated with energy cost of walking, with walking speed a significant effect modifier (β = –27.07, 95% CI: –49.32; –4.83). At lower speeds this association was stronger, attenuating at higher speeds.

Discussion: Poorer dynamic balance was associated with higher energy cost of walking, predominantly at lower walking speeds. Jointly improving walking speed and dynamic balance may reduce the energetic burden of walking in this population.

Downloads

Download data is not yet available.

References

Larocca NG. Impact of walking impairment in multiple sclerosis: perspectives of patients and care partners. Patient 2011; 4: 189–201 DOI: https://doi.org/10.2165/11591150-000000000-00000

Motl RW, Suh Y, Dlugonski D, Weikert M, Agiovlasitis S, Fernhall B, et al. Oxygen cost of treadmill and over-ground walking in mildly disabled persons with multiple sclerosis. Neurol Sci 2011; 32: 255–262 DOI: https://doi.org/10.1007/s10072-010-0396-0

Ralston HJ. Energy-speed relation and optimal speed during level walking. Int Z Angew Physiol 1958; 17: 277–283 DOI: https://doi.org/10.1007/BF00698754

Motl RW, Sandroff BM, Suh Y, Sosnoff JJ. Energy cost of walking and its association with gait parameters, daily activity, and fatigue in persons with mild multiple sclerosis. Neurorehabil Neural Repair 2012; 26: 1015–1021 DOI: https://doi.org/10.1177/1545968312437943

Sandroff BM, Klaren RE, Pilutti LA, Motl RW. Oxygen cost of walking in persons with multiple sclerosis: disability matters, but why? Mult Scler Int 2014; 2014: 162765 DOI: https://doi.org/10.1155/2014/162765

Sebastiao E, Bollaert RE, Hubbard EA, Motl RW. Gait variability and energy cost of oveground walking in persons with multiple sclerosis: a cross-sectional study. Am J Phys Med Rehabil 2018; 97: 646–650 DOI: https://doi.org/10.1097/PHM.0000000000000935

Filli L, Sutter T, Easthope CS, Killeen T, Meyer C, Reuter K, et al. Profiling walking dysfunction in multiple sclerosis: characterisation, classification and progression over time. Sci Rep 2018; 8: 4984 DOI: https://doi.org/10.1038/s41598-018-22676-0

Martin CL, Phillips BA, Kilpatrick TJ, Butzkueven H, Tubridy N, McDonald E, et al. Gait and balance impairment in early multiple sclerosis in the absence of clinical disability. Mult Scler 2006; 12: 620–628. https://doi.org/10.1177/1352458506070658 DOI: https://doi.org/10.1177/1352458506070658

Theunissen K, Plasqui G, Boonen A, Brauwers B, Timmermans A, Meyns P, et al. The relationship between walking speed and the energetic cost of walking in persons with multiple sclerosis and healthy controls: a systematic review. Neurorehabil Neural Repair 2021; 35: 486–500 DOI: https://doi.org/10.1177/15459683211005028

Buoite Stella A, Morelli ME, Giudici F, Sartori A, Manganotti P, di Prampero PE. Comfortable walking speed and energy cost of locomotion in patients with multiple sclerosis. Eur J Appl Physiol 2020; 120: 551–566. https://doi.org/10.1007/s00421-019-04295-3 DOI: https://doi.org/10.1007/s00421-019-04295-3

Kalron A, Frid L, Menascu S, Givon U. The association between gait variability with the energy cost of walking depends on the fall status in people with multiple sclerosis without mobility aids. Gait Posture 2019; 74: 231–235 DOI: https://doi.org/10.1016/j.gaitpost.2019.09.021

Brandstadter R, Ayeni O, Krieger SC, Harel NY, Escalon MX, Katz Sand I, et al. Detection of subtle gait disturbance and future fall risk in early multiple sclerosis. Neurology 2020; 94: e1395–e1406 DOI: https://doi.org/10.1212/WNL.0000000000008938

Hof AL, Gazendam MG, Sinke WE. The condition for dynamic stability. J Biomech 2005; 38: 1–8 DOI: https://doi.org/10.1016/j.jbiomech.2004.03.025

Herssens N, van Criekinge T, Saeys W, Truijen S, Vereeck L, van Rompaey V, et al. An investigation of the spatio-temporal parameters of gait and margins of stability throughout adulthood. J R Soc Interface 2020; 17: 20200194 DOI: https://doi.org/10.1098/rsif.2020.0194

Lencioni T, Carpinella I, Rabuffetti M, Cattaneo D, Ferrarin M. Measures of dynamic balance during level walking in healthy adult subjects: relationship with age, anthropometry and spatio-temporal gait parameters. Proc Inst Mech Eng H 2020; 234: 131–140 DOI: https://doi.org/10.1177/0954411919889237

Peebles AT, Reinholdt A, Bruetsch AP, Lynch SG, Huisinga JM. Dynamic margin of stability during gait is altered in persons with multiple sclerosis. J Biomech 2016; 49: 3949–3955 DOI: https://doi.org/10.1016/j.jbiomech.2016.11.009

Kalron A, Frid L, Menascu S. Gait characteristics in adolescents with multiple sclerosis. Pediatr Neurol 2017; 68: 73–76 DOI: https://doi.org/10.1016/j.pediatrneurol.2016.11.004

Yahia A, Ghroubi S, Mhiri C, Elleuch MH. Relationship between muscular strength, gait and postural parameters in multiple sclerosis. Ann Phys Rehabil Med 2011; 54: 144–155 DOI: https://doi.org/10.1016/j.rehab.2011.02.004

Bruijn SM, van Dieen JH, Meijer OG, Beek PJ. Is slow walking more stable? J Biomech 2009; 42: 1506–1512 DOI: https://doi.org/10.1016/j.jbiomech.2009.03.047

Hobart JC, Riazi A, Lamping DL, Fitzpatrick R, Thompson AJ. Measuring the impact of MS on walking ability: the 12-Item MS Walking Scale (MSWS-12). Neurology 2003; 60: 31–36 DOI: https://doi.org/10.1212/WNL.60.1.31

Van den Bogert AJ, Geijtenbeek T, Even-Zohar O, Steenbrink F, Hardin EC. A real-time system for biomechanical analysis of human movement and muscle function. Med Biol Eng Comput 2013; 51: 1069–1077 DOI: https://doi.org/10.1007/s11517-013-1076-z

Chung LH, Remelius JG, Van Emmerik RE, Kent-Braun JA. Leg power asymmetry and postural control in women with multiple sclerosis. Med Sci Sports Exerc 2008; 40: 1717–1724 DOI: https://doi.org/10.1249/MSS.0b013e31817e32a3

Larson RD, McCully KK, Larson DJ, Pryor WM, White LJ. Bilateral differences in lower-limb performance in individuals with multiple sclerosis. J Rehabil Res Dev 2013; 50: 215–222 DOI: https://doi.org/10.1682/JRRD.2011.10.0189

Das Gupta S, Bobbert MF, Kistemaker DA. The metabolic cost of walking in healthy young and older adults: a systematic review and meta analysis. Sci Rep 2019; 9: 9956 DOI: https://doi.org/10.1038/s41598-019-45602-4

Brown C, Simonsick E, Schrack J, Ferrucci L. Impact of balance on the energetic cost of walking and gait speed. J Am Geriatr Soc 2023; 71: 3489–3497 DOI: https://doi.org/10.1111/jgs.18521

Matsubara JH, Wu M, Gordon KE. Metabolic cost of lateral stabilization during walking in people with incomplete spinal cord injury. Gait Posture 2015; 41: 646–651 DOI: https://doi.org/10.1016/j.gaitpost.2015.01.015

Jeng B, Sandroff BM, Motl RW. Energetic cost of walking and spasticity in persons with multiple sclerosis with moderate disability. NeuroRehabilitation 2018; 43: 483–489 DOI: https://doi.org/10.3233/NRE-182498

Arpin DJ, Gehringer JE, Wilson TW, Kurz MJ. A reduced somatosensory gating response in individuals with multiple sclerosis is related to walking impairment. J Neurophysiol 2017; 118: 2052–2058 DOI: https://doi.org/10.1152/jn.00260.2017

Gravesteijn AS, Timmermans ST, Aarts J, Hulst HE, De Jong BA, Beckerman H, et al. Relative aerobic load of walking in people with multiple sclerosis. J Rehabil Med 2024; 56: jrm13352 DOI: https://doi.org/10.2340/jrm.v56.13352

Donelan JM, Kram R, Kuo AD. Mechanical and metabolic determinants of the preferred step width in human walking. Proc Biol Sci 2001; 268: 1985–1992 DOI: https://doi.org/10.1098/rspb.2001.1761

Boudarham J, Hameau S, Zory R, Hardy A, Bensmail D, Roche N. Coactivation of lower limb muscles during gait in patients with multiple sclerosis. PLoS One 2016; 11: e0158267 DOI: https://doi.org/10.1371/journal.pone.0158267

Namayeshi T, Lee PVS, Ackland D. Gait balance recovery after tripping: the influence of walking speed and ground inclination on muscle and joint function. J Biomech 2024; 172: 112178 DOI: https://doi.org/10.1016/j.jbiomech.2024.112178

Shirota C, Simon AM, Kuiken TA. Recovery strategy identification throughout swing phase using kinematic data from the tripped leg. Annu Int Conf IEEE Eng Med Biol Soc 2014; 2014: 6199–6202 DOI: https://doi.org/10.1109/EMBC.2014.6945045

Karpatkin HI, Benson A, Gardner N, Leb N, Ramos N, Xu HM, et al. Pilot trial of speed-intensive gait training on balance and walking in people with multiple sclerosis. Int J Ther Rehabil 2020; 27 DOI: https://doi.org/10.12968/ijtr.2020.0059

Dal U, Erdogan T, Resitoglu B, Beydagi H. Determination of preferred walking speed on treadmill may lead to high oxygen cost on treadmill walking. Gait Posture 2010; 31: 366–369 DOI: https://doi.org/10.1016/j.gaitpost.2010.01.006

Malatesta D, Canepa M, Menendez Fernandez A. The effect of treadmill and overground walking on preferred walking speed and gait kinematics in healthy, physically active older adults. Eur J Appl Physiol 2017; 117: 1833–1843 DOI: https://doi.org/10.1007/s00421-017-3672-3

Buurke TJW, Lamoth CJC, van der Woude LHV, den Otter R. Handrail holding during treadmill walking reduces locomotor learning in able-bodied persons. IEEE Trans Neural Syst Rehabil Eng 2019; 27: 1753–1759 DOI: https://doi.org/10.1109/TNSRE.2019.2935242

Additional Files

Published

2026-09-18

How to Cite

Timmermans, S. T., Gravesteijn, A. S., Wishaupt, K., Beckerman, H., van der Krogt, M. M., & de Groot, V. (2026). The cost of imbalance: how balance problems drive energy cost of walking in persons with multiple sclerosis. Journal of Rehabilitation Medicine, 58, jrm45814. https://doi.org/10.2340/jrm.v58.45814

Issue

Section

Original Report

Categories