Feasibility of robot-based perturbed-balance training during treadmill walking in a high-functioning chronic stroke subject: a case-control study

Zlatko Matjačić, Matjaž Zadravec, Andrej Olenšek, Zlatko Matjačić, Matjaž Zadravec, Andrej Olenšek

Abstract

Background: For stroke survivors, balance deficits that persist after the completion of the rehabilitation process lead to a significant risk of falls. We have recently developed a balance-assessment robot (BAR-TM) that enables assessment of balancing abilities during walking. The purpose of this study was to test feasibility of using the BAR-TM in an experimental perturbed-balance training program with a selected high-functioning stroke survivor.

Methods: A control and an individual with right-side chronic hemiparesis post-stroke were studied. The individual post-stroke underwent thirty sessions of balance-perturbed training that involved walking on an instrumented treadmill while the BAR-TM delivered random pushes to the participant's pelvis; these pushes were in various directions, at various speeds, and had various perturbation amplitudes. We assessed kinematics, kinetics, electromyography, and spatio-temporal responses to outward-directed perturbations of amplitude 60 N (before training) and 60 N and 90 N (after training) commencing on contact of either the nonparetic-left foot (LL-NP/L perturbation) or the paretic-right foot (RR-P/R perturbation) while the treadmill was running at a speed of 0.4 m/s.

Results: Before training, the individual post-stroke primarily responded to LL-NP/L perturbations with an in-stance response on the non-paretic leg in a similar way to the control participant. After training, the individual post-stroke added adequate stepping by making a cross-step with the paretic leg that enabled successful rejection of the perturbation at lower and higher amplitudes. Before training, the individual post-stroke primarily responded to RR-P/R perturbations with fast cross-stepping using the left, non-paretic leg while in-stance response was entirely missing. After training, the stepping with the non-paretic leg was supplemented by partially recovered ability to exercise in-stance responses on the paretic leg and this enabled successful rejection of the perturbation at lower and higher amplitudes. The assessed kinematics, kinetics, electromyography, and spatio-temporal responses provided insight into the relative share of each balancing strategy that the selected individual post-stroke used to counteract LL-NP/L and RR-P/R perturbations before and after the training.

Conclusions: The main finding of this case-control study is that robot-based perturbed-balance training may be a feasible approach. It resulted in an improvement the selected post-stroke participant's ability to counteract outward-directed perturbations.

Trial registration: ClinicalTrials.gov Identifier: NCT03285919 - retrospectively registered.

Keywords: Ankle strategy; Center of mass; Center of pressure; Ground reaction forces; Hip strategy; Perturbed walking; Stepping response.

Conflict of interest statement

Ethics approval and consent to participate

Ethical approval for this study was obtained from Republic of Slovenia National Medical Ethics Committee, decision number 80/03/15. Both participants gave signed, written, informed consent.

Consent for publication

Both participants gave consent to use and publish data in such way that anonymity is assured.

Competing interests

The authors declare that they have no competing interests. However, ZM and AO are the co-authors of the patent applications describing BAR device (US 14/718341 and EP 2922517).

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Photo of an individual post-stroke walking on an instrumented treadmill while being embraced by the BAR-TM perturbing device; computer screen shows the middle of the BAR-TM working space as well as the current position and orientation of the pelvis in transverse plane (left). Top view illustration of both outward perturbation directions: RR-P/R – perturbation to the right triggered at right-foot contact; LL-NP/L – perturbation to the left triggered at left-foot contact (right)
Fig. 2
Fig. 2
Kinematics and kinetics of balancing responses following LL-NP/L perturbation. The first row shows interaction forces between BAR-TM and participant’s pelvis in the frontal plane. The second row shows the trajectories of COPx (solid lines) and COMx (dotted lines), while the third row shows GRFx trajectories. The fourth row shows COPy (solid lines) and COMy (dotted lines) trajectories, and the fifth row shows GRFy trajectories. The left column shows the balancing responses of the individual post-stroke prior to the training (experimental condition BEFORE_60 – blue line) along with the unperturbed walking trajectories (green line). The middle column shows balancing responses of the individual post-stroke after the training (experimental conditions AFTER_60 – blue line and AFTER_90 – red line) along with the unperturbed walking trajectories (green line). The right column shows balancing responses of the control participant (experimental conditions CONTROL_60 – blue line and CONTROL_90 – red line) along with the unperturbed walking trajectories (green line). Half a stride prior to and two and a half strides following the perturbation commencement are shown. Stride is defined as the period between two consecutive left-foot contacts. The trajectories displayed show mean values and standard deviations of twenty balancing responses while, for clarity, only the mean values of twenty blocks of three consecutive strides of unperturbed walking are shown. Underneath each column, six consecutive stance phases of both legs are schematically indicated to enable easier cross-referencing with other figures. Subscript 0 denotes stance phases of both legs for steps taken before commencement of a perturbation, while subscripts 1 and 2 denote stance phases of each leg for steps taken after the commencement of a perturbation. P/R – paretic/right; NP/L – non-paretic/left
Fig. 3
Fig. 3
Mean values and standard deviations (twenty repetitions) of step lengths, widths, and step times for two steps prior to (P/R0 and NP/L0) and four consecutive steps following LL-NP/L perturbation commencement (P/R1, NP/L1, P/R2 and NP/L2). The left column shows data for experimental conditions BEFORE_60, AFTER_60 and CONTROL_60, while the right column shows data for experimental conditions AFTER_90 and CONTROL_90. Footprints illustrating unperturbed stepping and stepping following LL-NP/L perturbation with indication of step lengths (SL), step widths (SW) and step times (ST) is provided at the bottom for the experimental condition BEFORE_60
Fig. 4
Fig. 4
EMG responses following LL-NP/L perturbation. Left box shows responses for the muscles of the left leg (NP/L) while the right box shows responses for the muscles of the right leg (P/R). The left column in each box shows perturbed muscular activity of the individual post-stroke prior to the training (experimental condition BEFORE_60 – blue line) along with the unperturbed muscular activity (green line). The middle column in each box shows perturbed muscular activity of the individual post-stroke after the training (experimental conditions AFTER_60 – blue line and AFTER_90 – red line) along with the unperturbed muscular activity (green line). The right column in each box shows perturbed muscular activity of the control participant (experimental conditions CONTROL_60 – blue line and CONTROL_90 – red line) along with the unperturbed muscular activity (green line). Half of the stride prior to and two and a half strides following the perturbation commencement are shown. Stride is defined as the period between two consecutive left-foot contacts. The trajectories displayed show mean values and standard deviations of twenty balancing responses while, for clarity, only the mean values of twenty blocks of three consecutive strides of unperturbed walking are shown. Underneath each column, six consecutive stance phases of both legs are schematically indicated to enable easier cross-referencing with other figures
Fig. 5
Fig. 5
Kinematics and kinetics of balancing responses following RR_P/R perturbation. The first row shows interaction forces between BAR-TM and participant’s pelvis in the frontal plane. The second row shows the trajectories of COPx (solid lines) and COMx (dotted lines), while the third row shows GRFx trajectories. The fourth row shows COPy (solid lines) and COMy (dotted lines) trajectories, and the fifth row shows GRFy trajectories. The left column shows the balancing responses of the individual post-stroke prior to the training (experimental condition BEFORE_60 – blue line) along with the unperturbed walking trajectories (green line). The middle column shows balancing responses of the individual post-stroke after the training (experimental conditions AFTER_60 – blue line and AFTER_90 – red line) along with the unperturbed walking trajectories (green line). The right column shows balancing responses of the control participant (experimental conditions CONTROL_60 – blue line and CONTROL_90 – red line) along with the unperturbed walking trajectories (green line). Half a stride prior to and two and a half of strides following the perturbation commencement are shown. Stride is defined as the period between two consecutive right-foot contacts. Displayed trajectories show mean values and standard deviations of twenty balancing responses while, for clarity, only the mean values of twenty blocks of three consecutive strides of unperturbed walking are shown. Underneath each column, six consecutive stance phases of both legs are schematically indicated to enable easier cross-referencing with other figures. Subscript 0 denotes stance phases of both legs for steps taken before commencement of a perturbation, while subscripts 1 and 2 denote stance phases of each leg for steps taken after the commencement of a perturbation. P/R – paretic/right; NP/L – non-paretic/left
Fig. 6
Fig. 6
Comparison of GRFx responses following RR-P/R perturbation in two consecutive P/R steps before and after training in the individual post-stroke for all perturbing experimental conditions along with the unperturbed trajectories. After the training, hip-strategy GRFx force impulses immediately after right-foot contact can be seen for both perturbation strengths in both P/R0 (0–50% of GC; less pronounced) and P/R1 (100–150% of GC; more pronounced) stance phases
Fig. 7
Fig. 7
Mean values and standard deviations (twenty repetitions) of step lengths, step widths, and step times for two steps prior to (NP/L0 and P/R0) and four consecutive steps following RR-P/R perturbation commencement (NP/L1, P/R1, NP/L2 and P/R2). The left column shows data for experimental conditions BEFORE_60, AFTER_60 and CONTROL_60, while the right column shows data for experimental conditions AFTER_90 and CONTROL_90. Footprints illustrating unperturbed stepping and stepping following RR-P/R perturbation with indication of step lengths (SL), step widths (SW) and step times (ST) is provided at the bottom for the experimental condition BEFORE_60
Fig. 8
Fig. 8
EMG responses following RR-P/R perturbation. Left box shows responses for the muscles of the left leg (NP/L) while the right box shows responses for the muscles of the right leg (P/R). The left column in each box shows perturbed muscular activity of the individual post-stroke prior to the training (experimental condition BEFORE_60 – blue line) along with the unperturbed muscular activity (green line). The middle column in each box shows perturbed muscular activity of the individual post-stroke after the training (experimental conditions AFTER_60 – blue line and AFTER_90 – red line) along with the unperturbed muscular activity (green line). The right column in each box shows perturbed muscular activity of the control participant (experimental conditions CONTROL_60 – blue line and CONTROL_90 – red line) along with the unperturbed muscular activity (green line). Half of the stride prior to and two and a half strides following the perturbation commencement are shown. Stride is defined as the period between two consecutive right-foot contacts. The trajectories displayed show mean values and standard deviations of twenty balancing responses while, for clarity, only the mean values of twenty blocks of three consecutive strides of unperturbed walking are shown. Underneath each column, six consecutive stance phases of both legs are schematically indicated to enable easier cross-referencing with other figures

References

    1. Weerdesteyn V, de Niet M, van Duijnhoven HJR, Geurts ACH. Falls in individuals with stroke. J Rehab Res Dev. 2008;48(8):1195–1214. doi: 10.1682/JRRD.2007.09.0145.
    1. Krasovsky T, Lamontagne A, Feldman AG, Levin MF. Reduced gait stability in high-functioning poststroke individuals. J Neurophysiol. 2013;109:77–88. doi: 10.1152/jn.00552.2012.
    1. Holt RR, Simpson D, Jenner JR, Kirker SGB. Ground reaction force after a sideways push as a measure of balance in recovery from stroke. Clin Rehabil. 2000;14(1):88–95. doi: 10.1191/026921500668655351.
    1. Punt M, Bruijn SM, Roeles S, van de Port IG, Wittink H, van Dieen JH. Responses to gait perturbations in stroke survivors who prospectively experienced falls or no falls. J Biomech. 2017;55:56–63. doi: 10.1016/j.jbiomech.2017.02.010.
    1. Hof AL, Vermerris SM, Gjaltema WA. Balance responses to lateral perturbations in human treadmill walking. J Exp Biol. 2010;213:2655–2664. doi: 10.1242/jeb.042572.
    1. Hof AL. The equations of motion for a standing human reveal three mechanisms for balance. J Biomech. 2007;40:451–457. doi: 10.1016/j.jbiomech.2005.12.016.
    1. Vlutters M, van Asseldonk EHF, van der Kooij H. Center of mass velocity based predictions in balance recovery following pelvis perturbations during human walking. J Exp Biol. 2016;219(10):1514–1523. doi: 10.1242/jeb.129338.
    1. Matjačić Z, Zadravec M, Olenšek A. An effective balancing response to lateral perturbations at pelvis level during slow walking requires control in all three planes of motion. J Biomech. 2017;60:79–90. doi: 10.1016/j.jbiomech.2017.06.020.
    1. Schmidt H, Werner C, Bernhardt R, Hesse S, Kruger J. Gait rehabilitation machines based on programmable footplates. J Neuroeng Rehabil. 2007;4:2. doi: 10.1186/1743-0003-4-2.
    1. Verheyden GS, Weerdesteyn V, Pickering RM, et al. Interventions for preventing falls in people after stroke. Cochrane DatabaseSyst Rev. 2013;(5):CD008728. 10.1002/14651858.CD008728.pub2
    1. Mansfield A, Schinkel-Ivy A, Danells CJ, et al. Does perturbation training prevent falls after discharge from stroke rehabilitation? A prospective cohort study with historical control. J Stroke Cerebrovas Dis. 2017;26:2174–2180. doi: 10.1016/j.jstrokecerebrovasdis.2017.04.041.
    1. Olenšek A, Zadravec M, Matjačić Z. A novel robot for imposing perturbations during overground walking: mechanism, control and normative stepping responses. J Neuroeng Rehabil. 2016;13(1):55. doi: 10.1186/s12984-016-0160-7.
    1. Wade DT. Measurement in neurological rehabilitation. New York: Oxford University Press; 1992.
    1. Yang F, Pai Y. Can sacral marker approximate center of mass during gait and slip-fall recovery among community-dwelling older adults? J Biomech. 2014;47:3807–3812. doi: 10.1016/j.jbiomech.2014.10.027.
    1. Willems PA, Gosseye TP. Does an instrumented treadmill correctly measure the ground reaction forces? Biol Open. 2013;2:1421–1424. doi: 10.1242/bio.20136379.
    1. Raja B, Neptune RR, Kautz SA. Quantifiable patterns of limb loading and unloading during hemiparetic gait: relation to kinetic and kinematic parameters. J Rehab Res Dev. 2012;49:1293–1304. doi: 10.1682/JRRD.2011.02.0018.
    1. Qiao M, Jindrich L. Compensations during unsteady locomotion. Integr Comp Biol. 2014;54:1109–1121. doi: 10.1093/icb/icu058.
    1. Zadravec M, Olenšek A, Matjačić Z. The comparison of stepping responses following perturbations applied to pelvis during overground and treadmill walking. Technol Health Care. 2017; 10.3233/THC-160798.
    1. Shirota C, van Asseldonk E, Matjačić Z, Vallery H, Barralon P, Maggioni S, Buurke JH, Veneman JF. Robot-supported assessment of balance in standing and walking. J Neuroeng Rehabil. 2017;14:80. doi: 10.1186/s12984-017-0273-7.

Source: PubMed

3
Se inscrever