Upper limb muscle strength and wheelchair-related abilities following an exoskeleton-assisted walking programme in individuals with chronic spinal cord injury: An exploratory study
DOI:
https://doi.org/10.2340/jrm.v56.19461Keywords:
Dynamometer, Exoskeleton Device, Locomotion, Muscle Strength, Rehabilitation, Spinal Cord Injury, Upper limb, WheelchairsAbstract
Objectives: To measure the potential effects of an overground exoskeleton-assisted walking programme on upper limb strength and mass, as well as on wheelchair propulsion performances and abilities in individuals with chronic spinal cord injury.
Design: Prospective, single-group, pre–post intervention study.
Participants: Ten individuals with chronic (≥ 18 months) spinal cord injury who use a wheelchair as their primary mode of locomotion and who had little-to-no motor function in the lower limbs.
Methods: Individuals completed a progressive 16-week exoskeleton-assisted walking programme (34 × 1-h sessions, 1–3 sessions/week). Upper limb muscle strength was measured with dynamometers (isokinetic, Jamar). Upper limb lean mass (dual-energy X-ray absorptiometry) was used to calculate relative strength. Field tests (20-m wheelchair propulsion, and slalom test) and the Wheelchair Skills Test Questionnaire determined performances and abilities. Wilcoxon signed-rank tests were used with the following criteria: p < 0.1, effect size ≥ 0.5, and relative variation > 5%.
Results: Only natural velocity during the 20-m wheelchair propulsion test (i.e., fundamental wheelchair ability) changed following the intervention (p = 0.01, effect size = 0.82, relative variation = +14.5%).
Conclusion: Overall, upper limb muscle function did not significantly and meaningfully change following the exoskeleton-assisted walking programme in this population. Additional research is needed to verify how changes in training volume would affect strength and advanced wheelchair-related abilities and performance, as well as the response in individuals who are deconditioned or novices to wheelchair use (e.g., subacute spinal cord injury).
Downloads
References
van Middendorp JJ, Hosman AJF, Donders ART, Pouw MH, Ditunno JF, Curt A, et al. A clinical prediction rule for ambulation outcomes after traumatic spinal cord injury: a longitudinal cohort study. Lancet 2011; 377: 1004-1010.
https://doi.org/10.1016/S0140-6736(10)62276-3 DOI: https://doi.org/10.1016/S0140-6736(10)62276-3
Mateo S, Roby-Brami A, Reilly KT, Rossetti Y, Collet C, Rode G. Upper limb kinematics after cervical spinal cord injury: a review. J Neuroeng Rehabil 2015; 12: 9.
https://doi.org/10.1186/1743-0003-12-9 DOI: https://doi.org/10.1186/1743-0003-12-9
Lalumiere M, Gagnon DH, Routhier F, Bouyer L, Desroches G. Upper extremity kinematics and kinetics during the performance of a stationary wheelie in manual wheelchair users with a spinal cord injury. J Appl Biomech 2014; 30: 574-580.
https://doi.org/10.1123/jab.2013-0333 DOI: https://doi.org/10.1123/jab.2013-0333
Desroches G, Gagnon D, Nadeau S, Popovic MR. Effects of sensorimotor trunk impairments on trunk and upper limb joint kinematics and kinetics during sitting pivot transfers in individuals with a spinal cord injury. Clin Biomech (Bristol, Avon) 2013; 28: 1-9.
https://doi.org/10.1016/j.clinbiomech.2012.11.001 DOI: https://doi.org/10.1016/j.clinbiomech.2012.11.001
Milosevic M, Masani K, Kuipers MJ, Rahouni H, Verrier MC, McConville KM, et al. Trunk control impairment is responsible for postural instability during quiet sitting in individuals with cervical spinal cord injury. Clin Biomech (Bristol, Avon) 2015; 30: 507-512.
https://doi.org/10.1016/j.clinbiomech.2015.03.002 DOI: https://doi.org/10.1016/j.clinbiomech.2015.03.002
Paralyzed Veterans of America Consortium for Spinal Cord Medicine. Preservation of upper limb function following spinal cord injury: a clinical practice guideline for health-care professionals. J Spinal Cord Med 2005; 28: 434-470.
https://doi.org/10.1080/10790268.2005.11753844 DOI: https://doi.org/10.1080/10790268.2005.11753844
Dyson-Hudson TA, Kirshblum SC. Shoulder pain in chronic spinal cord injury, Part 1: epidemiology, etiology, and pathomechanics. J Spinal Cord Med 2004; 27: 4-17.
https://doi.org/10.1080/10790268.2004.11753724 DOI: https://doi.org/10.1080/10790268.2004.11753724
Larsen CM, Juul-Kristensen B, Kasch H, Hartvigsen J, Frich LH, Boyle E, et al. The Danish Spinal Cord Injury Shoulder (DanSCIS) cohort: methodology and primary results. Spinal Cord 2021; 59: 821-831.
https://doi.org/10.1038/s41393-020-00594-1 DOI: https://doi.org/10.1038/s41393-020-00594-1
Samuelsson KAM, Tropp H, Gerdle B. Shoulder pain and its consequences in paraplegic spinal cord-injured, wheelchair users. Spinal Cord 2004; 42: 41-46.
https://doi.org/10.1038/sj.sc.3101490 DOI: https://doi.org/10.1038/sj.sc.3101490
Patel RM, Gelber JD, Schickendantz MS. The weight-bearing shoulder. J Am Acad Orthop Surg 2018; 26: 3-13.
https://doi.org/10.5435/JAAOS-D-15-00598 DOI: https://doi.org/10.5435/JAAOS-D-15-00598
Mulroy SJ, Hafdahl L, Dyson-Hudson T. A primary care provider's guide to shoulder pain after spinal cord injury. Top Spinal Cord Inj Rehabil 2020; 26: 186-196.
https://doi.org/10.46292/sci2603-186 DOI: https://doi.org/10.46292/sci2603-186
Mulroy S, Haubert LL, Eberly V, Conners S, Weiss W. Effectiveness of two intervention programs to prevent shoulder pain after spinal cord injury. Arch Phys Med Rehabil 2017; 98: e174.
https://doi.org/10.1016/j.apmr.2017.09.081 DOI: https://doi.org/10.1016/j.apmr.2017.09.081
Ginis KAM, Scheer JW vd, Latimer-Cheung AE, Barrow A, Bourne C, Carruthers P, et al. Evidence-based scientific exercise guidelines for adults with spinal cord injury: an update and a new guideline. Spinal Cord 2018; 56: 308.
https://doi.org/10.1038/s41393-017-0017-3 DOI: https://doi.org/10.1038/s41393-017-0017-3
Gagnon DH, Roy A, Gabison S, Duclos C, Verrier MC, Nadeau S. Effects of seated postural stability and trunk and upper extremity strength on performance during manual wheelchair propulsion tests in individuals with spinal cord injury: an exploratory study. Rehabil Res Pract 2016; 2016: 6842324.
https://doi.org/10.1155/2016/6842324 DOI: https://doi.org/10.1155/2016/6842324
Ribeiro Neto F, Gomes Costa RR, Tanhoffer RA, Leal JC, Bottaro M, Carregaro RL. Muscle strength cutoff points for functional independence and wheelchair ability in men with spinal cord injury. Arch Phys Med Rehabil 2020; 101: 985-993.
https://doi.org/10.1016/j.apmr.2020.01.010 DOI: https://doi.org/10.1016/j.apmr.2020.01.010
Lauersen JB, Andersen TE, Andersen LB. Strength training as superior, dose-dependent and safe prevention of acute and overuse sports injuries: a systematic review, qualitative analysis and meta-analysis. Br J Sports Med 2018; 52: 1557-1563.
https://doi.org/10.1136/bjsports-2018-099078 DOI: https://doi.org/10.1136/bjsports-2018-099078
Alamro RA, Chisholm AE, Williams AMM, Carpenter MG, Lam T. Overground walking with a robotic exoskeleton elicits trunk muscle activity in people with high-thoracic motor-complete spinal cord injury. J Neuroeng Rehabil 2018; 15: 109.
https://doi.org/10.1186/s12984-018-0453-0 DOI: https://doi.org/10.1186/s12984-018-0453-0
Escalona MJ, Brosseau R, Vermette M, Comtois AS, Aubertin-Leheudre M, Duclos C, et al. Cardiorespiratory demand and rate of perceived exertion during overground walking with a robotic exoskeleton in long-term manual wheelchair users with chronic spinal cord injury: a cross-sectional study. Ann Phys Rehabil Med 2018; 61: 215-223.
https://doi.org/10.1016/j.rehab.2017.12.008 DOI: https://doi.org/10.1016/j.rehab.2017.12.008
Karelis AD, Carvalho LP, Castillo MJ, Gagnon DH, Aubertin-Leheudre M. Effect on body composition and bone mineral density of walking with a robotic exoskeleton in adults with chronic spinal cord injury. J Rehabil Med 2017; 49: 84-87.
https://doi.org/10.2340/16501977-2173 DOI: https://doi.org/10.2340/16501977-2173
Smith AJJ, Fournier BN, Nantel J, Lemaire ED. Estimating upper extremity joint loads of persons with spinal cord injury walking with a lower extremity powered exoskeleton and forearm crutches. J Biomech 2020; 107: 109835.
https://doi.org/10.1016/j.jbiomech.2020.109835 DOI: https://doi.org/10.1016/j.jbiomech.2020.109835
Bass A, Aubertin-Leheudre M, Vincent C, Karelis AD, Morin SN, McKerral M, et al. Effects of an overground walking program with a robotic exoskeleton on long-term manual wheelchair users with a chronic spinal cord injury: protocol for a self-controlled interventional study. JMIR Res Protoc 2020; 9: e19251.
https://doi.org/10.2196/19251 DOI: https://doi.org/10.2196/19251
Bass A, Aubertin-Leheudre M, Morin SN, Gagnon DH. Preliminary training volume and progression algorithm to tackle fragility fracture risk during exoskeleton-assisted overground walking in individuals with a chronic spinal cord injury. Spinal Cord Ser Cases 2022; 8: 29.
https://doi.org/10.1038/s41394-022-00498-7 DOI: https://doi.org/10.1038/s41394-022-00498-7
McArdle WD, Katch FI, Katch VL. Exercise physiology: nutrition, energy, and human performance. 9th ed. Philadelphia: Wolters Kluwer; 2023.
Gil-Agudo A, Del Ama-Espinosa A, Pérez-Rizo E, Pérez-Nombela S, Pablo Rodríguez-Rodríguez L. Upper limb joint kinetics during manual wheelchair propulsion in patients with different levels of spinal cord injury. J Biomech 2010; 43: 2508-2515.
https://doi.org/10.1016/j.jbiomech.2010.05.021 DOI: https://doi.org/10.1016/j.jbiomech.2010.05.021
Vanlandewijck Y, Theisen D, Daly D. Wheelchair propulsion biomechanics. Sports Med 2001; 31: 339-367.
https://doi.org/10.2165/00007256-200131050-00005 DOI: https://doi.org/10.2165/00007256-200131050-00005
Neto FR, Gomes Costa RR, Dorneles JR, Gonçalves CW, Veloso J, Carregaro RL. Handgrip strength cutoff points for functional independence and wheelchair ability in men with spinal cord injury. Top Spinal Cord Inj Rehabil 2021; 27: 60-69.
https://doi.org/10.46292/sci20-00040 DOI: https://doi.org/10.46292/sci20-00040
Gagnon DH, Décary S, Charbonneau MF. The timed manual wheelchair slalom test: a reliable and accurate performance-based outcome measure for individuals with spinal cord injury. Arch Physical Med Rehabil 2011; 92: 1339-1343.
https://doi.org/10.1016/j.apmr.2011.02.005 DOI: https://doi.org/10.1016/j.apmr.2011.02.005
Gagnon DH, Roy A, Verrier MC, Duclos C, Craven BC, Nadeau S. Do performance-based wheelchair propulsion test detect changes among manual wheelchair users with spinal cord injury during inpatient rehabilitation in Quebec? Arch Physical Med Rehabil 2016; 97: 1214-1218.
https://doi.org/10.1016/j.apmr.2016.02.018 DOI: https://doi.org/10.1016/j.apmr.2016.02.018
Dalhousie University. Guide du Programme d'habiletés en fauteuil roulant (WSP-F): Version 5.4 canadienne-française. [Wheelchair Skills Program Manual Version 5.4.]. [Electronic Publication (in French)] 2024 [cited 2024 Oct 23]; Available from: https://wheelchairskillsprogram.ca/wp-content/uploads/Guide-du-WSP-F-5.4.1.pdf
Fritz CO, Morris PE, Richler JJ. Effect size estimates: Current use, calculations, and interpretation. J Exp Psychol Gen 2012; 141: 2-18.
https://doi.org/10.1037/a0024338 DOI: https://doi.org/10.1037/a0024338
Cohen J. Statistical power analysis. Current directions in psychological science 1992; 1: 98-101.
https://doi.org/10.1111/1467-8721.ep10768783 DOI: https://doi.org/10.1111/1467-8721.ep10768783
Kawalilak CE, Johnston JD, Olszynski WP, Kontulainen SA. Least significant changes and monitoring time intervals for high-resolution pQCT-derived bone outcomes in postmenopausal women. J Musculoskelet Neuronal Interact 2015; 15: 190-196.
Pradon D, Pinsault N, Zory R, Routhier F. Could mobility performance measures be used to evaluate wheelchair skills? J Rehabil Med 2012; 44: 276-279.
https://doi.org/10.2340/16501977-0919 DOI: https://doi.org/10.2340/16501977-0919
Tamburella F, Lorusso M, Tramontano M, Fadlun S, Masciullo M, Scivoletto G. Overground robotic training effects on walking and secondary health conditions in individuals with spinal cord injury: systematic review. J Neuroeng Rehabil 2022; 19: 27.
https://doi.org/10.1186/s12984-022-01003-9 DOI: https://doi.org/10.1186/s12984-022-01003-9
Xiang XN, Zong HY, Ou Y, Yu X, Cheng H, Du CP, et al. Exoskeleton-assisted walking improves pulmonary function and walking parameters among individuals with spinal cord injury: a randomized controlled pilot study. J Neuroeng Rehabil 2021; 18: 86.
https://doi.org/10.1186/s12984-021-00880-w DOI: https://doi.org/10.1186/s12984-021-00880-w
Williams AMM, Deegan E, Walter M, Stothers L, Lam T. Exoskeleton gait training to improve lower urinary tract function in people with motor-complete spinal cord injury: a randomized pilot trial. J Rehabil Med 2021; 53: jrm00222.
https://doi.org/10.2340/16501977-2864 DOI: https://doi.org/10.2340/16501977-2864
Asselin P, Cirnigliaro CM, Kornfeld S, Knezevic S, Lackow R, Elliott M, et al. Effect of exoskeletal-assisted walking on soft tissue body composition in persons with spinal cord injury. Arch Phys Med Rehabil 2021; 102: 196-202.
https://doi.org/10.1016/j.apmr.2020.07.018 DOI: https://doi.org/10.1016/j.apmr.2020.07.018
American College of Sports Medicine, Liguori G, Feito Y, Fountaine C, Roy BA. ACSM's guidelines for exercise testing and prescription. 11th ed. Philadelphia: Wolters Kluwer; 2022.
Kressler J, Thomas CK, Field-Fote EC, Sanchez J, Widerström-Noga E, Cilien DC, et al. Understanding therapeutic benefits of overground bionic ambulation: exploratory case series in persons with chronic, complete spinal cord injury. Arch Phys Med Rehabil 2014; 95: 1878-1887.e1874.
https://doi.org/10.1016/j.apmr.2014.04.026 DOI: https://doi.org/10.1016/j.apmr.2014.04.026
Gagnon DH, Cunha JD, Boyer-Delestre M, Bosquet L, Duclos C. How does wearable robotic exoskeleton affect overground walking performance measured with the 10-m and six-minute walk tests after a basic locomotor training in healthy individuals? Gait Posture 2017; 58: 340-345.
https://doi.org/10.1016/j.gaitpost.2017.08.027 DOI: https://doi.org/10.1016/j.gaitpost.2017.08.027
Mulroy SJ, Gronley JK, Newsam CJ, Perry J. Electromyographic activity of shoulder muscles during wheelchair propulsion by paraplegic persons. Arch Phys Med Rehabil 1996; 77: 187-193.
https://doi.org/10.1016/S0003-9993(96)90166-5 DOI: https://doi.org/10.1016/S0003-9993(96)90166-5
Ozmen T, Yuktasir B, Yildirim NU, Yalcin B, Willems ME. Explosive strength training improves speed and agility in wheelchair basketball athletes. Revista Brasileira de Medicina do Esporte 2014; 20: 97-100.
https://doi.org/10.1590/1517-86922014200201568 DOI: https://doi.org/10.1590/1517-86922014200201568
Turbanski S, Schmidtbleicher D. Effects of heavy resistance training on strength and power in upper extremities in wheelchair athletes. J Strength Cond Res 2010; 24: 8-16.
https://doi.org/10.1519/JSC.0b013e3181bdddda DOI: https://doi.org/10.1519/JSC.0b013e3181bdddda
Paulson T, Goosey-Tolfrey V. Current perspectives on profiling and enhancing wheelchair court sport performance. Int J Sports Physiol Perform 2017; 12: 275-286.
https://doi.org/10.1123/ijspp.2016-0231 DOI: https://doi.org/10.1123/ijspp.2016-0231
Keeler L, Kirby RL, Parker K, McLean KD, Hayden JA. Effectiveness of the Wheelchair Skills Training Program: a systematic review and meta-analysis. Disabil Rehabil Assist Technol 2019; 14: 391-409.
https://doi.org/10.1080/17483107.2018.1456566 DOI: https://doi.org/10.1080/17483107.2018.1456566
Gant KL, Nagle KG, Cowan RE, Field-Fote EC, Nash MS, Kressler J, et al. Body system effects of a multi-modal training program targeting chronic, motor complete thoracic spinal cord injury. J Neurotrauma 2018; 35: 411-423.
https://doi.org/10.1089/neu.2017.5105 DOI: https://doi.org/10.1089/neu.2017.5105
Wong SL. Grip strength reference values for Canadians aged 6 to 79: Canadian Health Measures Survey, 2007 to 2013. Health Reports 2016; 27: 3-10.
Beck LA, Bombardier CH, Richmond M, Gorman P, Marsolais EB, Hawryluk GWJ, et al. Identification and management of cardiometabolic risk after spinal cord injury: clinical practice guideline for health care providers. 2018. Available from: https://pva.org/wp-content/uploads/2021/09/cpg_cardiometabolic-risk_digital.pdf.
Published
How to Cite
License
Copyright (c) 2024 Alec Bass, Mylène Aubertin-Leheudre, Claude Vincent, Cyril Duclos, Dany H. Gagnon

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.