Relative aerobic load of walking in people with multiple sclerosis
DOI:
https://doi.org/10.2340/jrm.v56.13352Keywords:
anaerobic threshold, cardiorespiratory fitness, energy metabolism, gait, rehabilitationAbstract
Objective: To examine the energy demand of walking relative to aerobic capacity in people with multiple sclerosis.
Design: Cross-sectional cohort study.
Patients: A total of 45 people with multiple sclerosis (32 females), median disease duration 15 years (interquartile range (IQR) 9; 20), median Expanded Disability Status Scale 4 (min–max range: 2.0; 6.0).
Methods: Aerobic capacity, derived from a cardiopulmonary exercise test and gas exchange measurements, assessed during a 6-min overground walk test at comfortable speed, were analysed. The relative aerobic load of walking was determined as the energy demand of walking relative to oxygen uptake at peak and at the first ventilatory threshold. Healthy reference data were used for clinical inference.
Results: People with multiple sclerosis walk at a mean relative aerobic load of 60.0% (standard deviation 12.8%) relative to peak aerobic capacity, and 89.1% (standard deviation 19.9%) relative to the first ventilatory threshold. Fourteen participants walked above the first ventilatory threshold (31%). Peak aerobic capacity was reduced in 45% of participants, and energy demands were increased in 52% of participants.
Conclusion: People with multiple sclerosis walk at a relative aerobic load close to their first ventilatory threshold. A high relative aerobic load can guide clinicians to improve aerobic capacity or reduce the energy demands of walking.
Downloads
References
McGinley MP, Goldschmidt CH, Rae-Grant AD. Diagnosis and treatment of multiple sclerosis: a review. JAMA 2021; 325: 765-779.
https://doi.org/10.1001/jama.2020.26858 DOI: https://doi.org/10.1001/jama.2020.26858
Kister I, Bacon TE, Chamot E, Salter AR, Cutter GR, Kalina JT, et al. Natural history of multiple sclerosis symptoms. Int J MS Care 2013; 15: 146-158.
https://doi.org/10.7224/1537-2073.2012-053 DOI: https://doi.org/10.7224/1537-2073.2012-053
Comber L, Galvin R, Coote S. Gait deficits in people with multiple sclerosis: a systematic review and meta-analysis. Gait Posture 2017; 51: 25-35.
https://doi.org/10.1016/j.gaitpost.2016.09.026 DOI: https://doi.org/10.1016/j.gaitpost.2016.09.026
Larocca NG. Impact of walking impairment in multiple sclerosis: perspectives of patients and care partners. Patient 2011; 4: 189-201.
https://doi.org/10.2165/11591150-000000000-00000 DOI: https://doi.org/10.2165/11591150-000000000-00000
Sandroff BM, Motl RW, Suh Y. Accelerometer output and its association with energy expenditure in persons with multiple sclero-sis. J Rehabil Res Dev 2012; 49: 467-475.
https://doi.org/10.1682/JRRD.2011.03.0063 DOI: https://doi.org/10.1682/JRRD.2011.03.0063
Langeskov-Christensen M, Heine M, Kwakkel G, Dalgas U. Aerobic capacity in persons with multiple sclerosis: a systematic re-view and meta-analysis. Sports Med 2015; 45: 905-923.
https://doi.org/10.1007/s40279-015-0307-x DOI: https://doi.org/10.1007/s40279-015-0307-x
Motl RW, Sandroff BM, Suh Y, Sosnoff JJ. Energy cost of walking and its association with gait parameters, daily activity, and fa-tigue in persons with mild multiple sclerosis. Neurorehabil Neural Repair 2012; 26: 1015-1021.
https://doi.org/10.1177/1545968312437943 DOI: https://doi.org/10.1177/1545968312437943
American Thoracic Society, American College of Chest Physicians. ATS/ACCP Statement on cardiopulmonary exercise testing. Am J Respir Crit Care Med 2003; 167: 211-277.
https://doi.org/10.1164/rccm.167.2.211 DOI: https://doi.org/10.1164/rccm.167.2.211
Poole DC, Rossiter HB, Brooks GA, Gladden LB. The anaerobic threshold: 50+ years of controversy. J Physiol 2021; 599: 737-767.
https://doi.org/10.1113/JP279963 DOI: https://doi.org/10.1113/JP279963
Blokland I, Gravesteijn A, Busse M, Groot F, van Bennekom C, van Dieen J, et al. The relationship between relative aerobic load, energy cost, and speed of walking in individuals post-stroke. Gait Posture 2021; 89: 193-199.
https://doi.org/10.1016/j.gaitpost.2021.07.012 DOI: https://doi.org/10.1016/j.gaitpost.2021.07.012
Wezenberg D, van der Woude LH, Faber WX, de Haan A, Houdijk H. Relation between aerobic capacity and walking ability in older adults with a lower-limb amputation. Arch Phys Med Rehabil 2013; 94: 1714-1720.
https://doi.org/10.1016/j.apmr.2013.02.016 DOI: https://doi.org/10.1016/j.apmr.2013.02.016
Manca A, Cano A, Ventura L, Martinez G, Frid L, Deriu F, et al. Sex-based differences in oxygen cost of walking and energy equiva-lents in minimally disabled individuals with multiple sclerosis and controls. Int J MS Care 2022; 24: 54-61.
https://doi.org/10.7224/1537-2073.2020-112 DOI: https://doi.org/10.7224/1537-2073.2020-112
Gravesteijn AS, Beckerman H, de Jong BA, Hulst HE, de Groot V. Neuroprotective effects of exercise in people with progressive multiple sclerosis (Exercise PRO-MS): study protocol of a phase II trial. BMC Neurol 2020; 20: 177.
https://doi.org/10.1186/s12883-020-01765-6 DOI: https://doi.org/10.1186/s12883-020-01765-6
Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 1983; 33: 1444-1452.
https://doi.org/10.1212/WNL.33.11.1444 DOI: https://doi.org/10.1212/WNL.33.11.1444
Nolte S, Rein R, Quittmann OJ. Data processing strategies to determine maximum oxygen uptake: a systematic scoping review and experimental comparison with guidelines for reporting. Sports Med 2023; 10.1007/s40279-023-01903-3.
https://doi.org/10.1007/s40279-023-01903-3 DOI: https://doi.org/10.1007/s40279-023-01903-3
Albouaini K, Egred M, Alahmar A, Wright DJ. Cardiopulmonary exercise testing and its application. Postgrad Med J 2007; 83: 675-682.
https://doi.org/10.1136/hrt.2007.121558 DOI: https://doi.org/10.1136/hrt.2007.121558
Heine M, Hoogervorst EL, Hacking HG, Verschuren O, Kwakkel G. Validity of maximal exercise testing in people with multiple scle-rosis and low to moderate levels of disability. Phys Ther 2014; 94: 1168-1175.
https://doi.org/10.2522/ptj.20130418 DOI: https://doi.org/10.2522/ptj.20130418
Borg GA. Psychophysical bases of perceived exertion. Med Sci Sports Exerc 1982; 14: 377-381.
https://doi.org/10.1249/00005768-198205000-00012 DOI: https://doi.org/10.1249/00005768-198205000-00012
Holland AE, Dowman L, Fiore J Jr, Brazzale D, Hill CJ, McDonald CF. Cardiorespiratory responses to 6-minute walk test in interstitial lung disease: not always a submaximal test. BMC Pulm Med 2014; 14: 136.
https://doi.org/10.1186/1471-2466-14-136 DOI: https://doi.org/10.1186/1471-2466-14-136
Plasschaert F, Jones K, Forward M. Energy cost of walking: solving the paradox of steady state in the presence of variable walking speed. Gait Posture 2009; 29: 311-316.
https://doi.org/10.1016/j.gaitpost.2008.09.015 DOI: https://doi.org/10.1016/j.gaitpost.2008.09.015
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.
https://doi.org/10.1038/s41598-019-45602-4 DOI: https://doi.org/10.1038/s41598-019-45602-4
Shvartz E, Reibold RC. Aerobic fitness norms for males and females aged 6 to 75 years: a review. Aviat Space Environ Med 1990; 61: 3-11.
Buoite Stella A, Morelli ME, Giudici F, Sartori A, Manganotti P, di Prampero PE. Comfortable walking speed and energy cost of loco-motion 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
Heine M, Wens I, Langeskov-Christensen M, Verschuren O, Eijnde BO, Kwakkel G, et al. Cardiopulmonary fitness is related to dis-ease severity in multiple sclerosis. Mult Scler 2016; 22: 231-238.
https://doi.org/10.1177/1352458515581437 DOI: https://doi.org/10.1177/1352458515581437
Paap D, Takken T. Reference values for cardiopulmonary exercise testing in healthy adults: a systematic review. Expert Rev Cardio-vasc Ther 2014; 12: 1439-1453.
https://doi.org/10.1586/14779072.2014.985657 DOI: https://doi.org/10.1586/14779072.2014.985657
Ludlow LW, Weyand PG. Energy expenditure during level human walking: seeking a simple and accurate predictive solution. J Appl Physiol 2016; 120: 481-494.
https://doi.org/10.1152/japplphysiol.00864.2015 DOI: https://doi.org/10.1152/japplphysiol.00864.2015
Ralston HJ. Energy-speed relation and optimal speed during level walking. Int Z Angew Physiol 1958; 17: 277-283.
https://doi.org/10.1007/BF00698754 DOI: https://doi.org/10.1007/BF00698754
Balemans AC, Bolster EA, Brehm MA, Dallmeijer AJ. Physical strain: a new perspective on walking in cerebral palsy. Arch Phys Med Rehabil 2017; 98: 2507-2513.
https://doi.org/10.1016/j.apmr.2017.05.004 DOI: https://doi.org/10.1016/j.apmr.2017.05.004
Slaman J, Bussmann J, van der Slot WM, Stam HJ, Roebroeck ME, van den Berg-Emons RJ, et al. Physical strain of walking relates to activity level in adults with cerebral palsy. Arch Phys Med Rehabil 2013; 94: 896-901.
https://doi.org/10.1016/j.apmr.2012.11.005 DOI: https://doi.org/10.1016/j.apmr.2012.11.005
Shephard RJ. Independence: a new reason for recommending regular exercise to your patients. Phys Sportsmed 2009; 37: 115-118.
https://doi.org/10.3810/PSM.2009.04.1691 DOI: https://doi.org/10.3810/PSM.2009.04.1691
Eriksen L, Gronbaek M, Helge JW, Tolstrup JS. Cardiorespiratory fitness in 16 025 adults aged 18-91 years and associations with physical activity and sitting time. Scand J Med Sci Sports 2016; 26: 1435-1443.
https://doi.org/10.1111/sms.12608 DOI: https://doi.org/10.1111/sms.12608
Rapp D, Scharhag J, Wagenpfeil S, Scholl J. Reference values for peak oxygen uptake: cross-sectional analysis of cycle ergometry-based cardiopulmonary exercise tests of 10 090 adult German volunteers from the Prevention First Registry. BMJ Open 2018; 8: e018697.
https://doi.org/10.1136/bmjopen-2017-018697 DOI: https://doi.org/10.1136/bmjopen-2017-018697
Kaminsky LA, Imboden MT, Arena R, Myers J. Reference standards for cardiorespiratory fitness measured with cardiopulmonary exercise testing using cycle ergometry: data from the Fitness Registry and the Importance of Exercise National Database (FRIEND) Registry. Mayo Clin Proc 2017; 92: 228-233.
https://doi.org/10.1016/j.mayocp.2016.10.003 DOI: https://doi.org/10.1016/j.mayocp.2016.10.003
Myers J, Ashley E. Dangerous curves. A perspective on exercise, lactate, and the anaerobic threshold. Chest 1997; 111: 787-795.
https://doi.org/10.1378/chest.111.3.787 DOI: https://doi.org/10.1378/chest.111.3.787
Hodges LD, Nielsen T, Baken D. Physiological measures in participants with chronic fatigue syndrome, multiple sclerosis and healthy controls following repeated exercise: a pilot study. Clin Physiol Funct Imaging 2018; 38: 639-644.
https://doi.org/10.1111/cpf.12460 DOI: https://doi.org/10.1111/cpf.12460
Klaren RE, Sandroff BM, Fernhall B, Motl RW. Comprehensive profile of cardiopulmonary exercise testing in ambulatory persons with multiple sclerosis. Sports Med 2016; 46: 1365-1379.
https://doi.org/10.1007/s40279-016-0472-6 DOI: https://doi.org/10.1007/s40279-016-0472-6
Vainshelboim B, Arena R, Kaminsky LA, Myers J. Reference standards for ventilatory threshold measured with cardiopulmonary exercise testing: the fitness registry and the importance of exercise: a national database. Chest 2020; 157: 1531-1537.
https://doi.org/10.1016/j.chest.2019.11.022 DOI: https://doi.org/10.1016/j.chest.2019.11.022
Londeree BR. Effect of training on lactate/ventilatory thresholds: a meta-analysis. Med Sci Sports Exerc 1997; 29: 837-843.
https://doi.org/10.1097/00005768-199706000-00016 DOI: https://doi.org/10.1097/00005768-199706000-00016
Gaskill SE, Ruby BC, Walker AJ, Sanchez OA, Serfass RC, Leon AS. Validity and reliability of combining three methods to determine ventilatory threshold. Med Sci Sports Exerc 2001; 33: 1841-1848.
https://doi.org/10.1097/00005768-200111000-00007 DOI: https://doi.org/10.1097/00005768-200111000-00007
Bentley DJ, Newell J, Bishop D. Incremental exercise test design and analysis: implications for performance diagnostics in endu-rance athletes. Sports Med 2007; 37: 575-586.
https://doi.org/10.2165/00007256-200737070-00002 DOI: https://doi.org/10.2165/00007256-200737070-00002
Zuniga JM, Housh TJ, Camic CL, Bergstrom HC, Schmidt RJ, Johnson GO. The effect of different exercise protocols and regression-based algorithms on the assessment of the anaerobic threshold. J Strength Cond Res 2014; 28: 2507-2512.
https://doi.org/10.1519/JSC.0000000000000440 DOI: https://doi.org/10.1519/JSC.0000000000000440
Ainsworth BE, Haskell WL, Whitt MC, Irwin ML, Swartz AM, Strath SJ, et al. Compendium of physical activities: an update of acti-vity codes and MET intensities. Med Sci Sports Exerc 2000; 32: S498-504.
https://doi.org/10.1097/00005768-200009001-00009 DOI: https://doi.org/10.1097/00005768-200009001-00009
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.
https://doi.org/10.1177/15459683211005028 DOI: https://doi.org/10.1177/15459683211005028
Gaskill SE, Walker AJ, Serfass RA, Bouchard C, Gagnon J, Rao DC, et al. Changes in ventilatory threshold with exercise training in a sedentary population: the HERITAGE Family Study. Int J Sports Med 2001; 22: 586-592.
https://doi.org/10.1055/s-2001-18522 DOI: https://doi.org/10.1055/s-2001-18522
Manfredini F, Straudi S, Lamberti N, Patergnani S, Tisato V, Secchiero P, et al. Rehabilitation improves mitochondrial energetics in progressive multiple sclerosis: the significant role of robot-assisted gait training and of the personalized intensity. Diagnostics (Basel) 2020; 10: 834.
https://doi.org/10.3390/diagnostics10100834 DOI: https://doi.org/10.3390/diagnostics10100834
Bregman DJ, Harlaar J, Meskers CG, de Groot V. Spring-like ankle foot orthoses reduce the energy cost of walking by taking over ankle work. Gait Posture 2012; 35: 148-153.
https://doi.org/10.1016/j.gaitpost.2011.08.026 DOI: https://doi.org/10.1016/j.gaitpost.2011.08.026
Heine M, Richards R, Geurtz B, Los F, Rietberg M, Harlaar J, et al. Preliminary effectiveness of a sequential exercise intervention on gait function in ambulant patients with multiple sclerosis - a pilot study. Clin Biomech (Bristol, Avon) 2019; 62: 1-6.
https://doi.org/10.1016/j.clinbiomech.2018.12.012 DOI: https://doi.org/10.1016/j.clinbiomech.2018.12.012
Additional Files
Published
How to Cite
License
Copyright (c) 2024 Arianne S. Gravesteijn, Sjoerd T. Timmermans, Jip Aarts, Hanneke E. Hulst, Brigit A. de Jong, Heleen Beckerman, Vincent de Groot
This work is licensed under a Creative Commons Attribution 4.0 International License.
All digitalized JRM contents is available freely online. The Foundation for Rehabilitation Medicine owns the copyright for all material published until volume 40 (2008), as from volume 41 (2009) authors retain copyright to their work and as from volume 49 (2017) the journal has been published Open Access, under CC-BY-NC licences (unless otherwise specified). The CC-BY-NC licenses allow third parties to copy and redistribute the material in any medium or format and to remix, transform, and build upon the material for non-commercial purposes, provided proper attribution to the original work.
From 2024, articles are published under the CC-BY licence. This license permits sharing, adapting, and using the material for any purpose, including commercial use, with the condition of providing full attribution to the original publication.
Funding data
-
Stichting MS Research
Grant numbers 18-358f
