Differences in Muscle Synergy Symmetry Between Subacute Post-stroke Patients With Bioelectrically-Controlled Exoskeleton Gait Training and Conventional Gait Training

Understanding the reorganization of the central nervous system after stroke is an important endeavor in order to design new therapies in gait training for stroke patients. Current clinical evaluation scores and gait velocity are insufficient to describe the state of the nervous system, and one aspect where this is lacking is in the quantification of gait symmetry. Previous studies have pointed out that spatiotemporal gait asymmetries are commonly observed in stroke patients with hemiparesis. Such asymmetries are known to cause long-term complications like joint pain and deformation. Recent studies also indicate that spatiotemporal measures showed that gait symmetry worsens after discharge from therapy. This study shows that muscle synergy analysis can be used to quantify gait symmetry and compliment clinical measures. Surface EMG was collected from lower limb muscles of subacute post-stroke patients (with an onset of around 14 days) from two groups, one undergoing robotic-assisted therapy (known as HAL group) and the other undergoing conventional therapy (known as Control group). Muscle synergies from the paretic and non-paretic limb were extracted with Non-Negative Matrix Factorization (NNMF) and compared with each other to obtain a gait symmetry index over therapy sessions. Gait events were tracked with motion tracking (for the HAL group) or foot pressure sensors (for the conventional therapy group). Patients from both groups were assessed over a 3-weeks long gait training program. Results indicated that there were no differences in muscle synergy symmetry for both groups of patients. However, the timing of muscle synergies were observed to be symmetrical in the HAL group, but not for the Control group. Intergroup comparisons of symmetry in muscle synergies and their timings were not significantly different. This could be due to a large variability in recovery in the Control group. Finally, stance time ratio was not observed to improve in both groups after their respective therapies. Interestingly, FIM and FMA scores of both groups were observed to improve after their respective therapies. Analysis of muscle coordination could reveal mechanisms of gait symmetry which could otherwise be difficult to observe with clinical scores.

[1]  A. Mansfield,et al.  Longitudinal change in spatiotemporal gait symmetry after discharge from inpatient stroke rehabilitation , 2020, Disability and rehabilitation.

[2]  Chun Kwang Tan,et al.  Lateral Symmetry of Synergies in Lower Limb Muscles of Acute Post-stroke Patients After Robotic Intervention , 2018, Front. Neurosci..

[3]  Diego Torricelli,et al.  Combining muscle synergies and biomechanical analysis to assess gait in stroke patients. , 2017, Journal of biomechanics.

[4]  Benjamin J. Fregly,et al.  Methodological Choices in Muscle Synergy Analysis Impact Differentiation of Physiological Characteristics Following Stroke , 2017, Front. Comput. Neurosci..

[5]  John W Krakauer,et al.  Agreed definitions and a shared vision for new standards in stroke recovery research: The Stroke Recovery and Rehabilitation Roundtable taskforce , 2017, International journal of stroke : official journal of the International Stroke Society.

[6]  Koji Ohata,et al.  Merging and Fractionation of Muscle Synergy Indicate the Recovery Process in Patients with Hemiplegia: The First Study of Patients after Subacute Stroke , 2016, Neural plasticity.

[7]  J L Pons,et al.  Modular control of gait after incomplete spinal cord injury: differences between sides , 2016, Spinal Cord.

[8]  Dennis R. Louie,et al.  Powered robotic exoskeletons in post-stroke rehabilitation of gait: a scoping review , 2016, Journal of NeuroEngineering and Rehabilitation.

[9]  Katherine M Steele,et al.  Repeatability of muscle synergies within and between days for typically developing children and children with cerebral palsy. , 2016, Gait & posture.

[10]  Emilio Bizzi,et al.  Representation of Muscle Synergies in the Primate Brain , 2015, The Journal of Neuroscience.

[11]  Simon F Giszter,et al.  Motor primitives—new data and future questions , 2015, Current Opinion in Neurobiology.

[12]  W. McIlroy,et al.  Longitudinal Changes in Poststroke Spatiotemporal Gait Asymmetry Over Inpatient Rehabilitation , 2015, Neurorehabilitation and neural repair.

[13]  P. Schwenkreis,et al.  Voluntary driven exoskeleton as a new tool for rehabilitation in chronic spinal cord injury: a pilot study. , 2014, The spine journal : official journal of the North American Spine Society.

[14]  Hideyuki Saitou,et al.  Locomotion improvement using a hybrid assistive limb in recovery phase stroke patients: a randomized controlled pilot study. , 2014, Archives of physical medicine and rehabilitation.

[15]  Rebecca L. Routson,et al.  Modular organization across changing task demands in healthy and poststroke gait , 2014, Physiological reports.

[16]  Dario Farina,et al.  Motor modules of human locomotion: influence of EMG averaging, concatenation, and number of step cycles , 2014, Front. Hum. Neurosci..

[17]  Richard R Neptune,et al.  The influence of locomotor rehabilitation on module quality and post-stroke hemiparetic walking performance. , 2013, Gait & posture.

[18]  L. Tomasevic,et al.  The myth of the ‘unaffected’ side after unilateral stroke: Is reorganisation of the non‐infarcted corticospinal system to re-establish balance the price for recovery? , 2012, Experimental Neurology.

[19]  Stacie A. Chvatal,et al.  Voluntary and Reactive Recruitment of Locomotor Muscle Synergies during Perturbed Walking , 2012, The Journal of Neuroscience.

[20]  E. Bizzi,et al.  Muscle synergy patterns as physiological markers of motor cortical damage , 2012, Proceedings of the National Academy of Sciences.

[21]  A. Esquenazi,et al.  Safety and tolerance of the ReWalk™ exoskeleton suit for ambulation by people with complete spinal cord injury: A pilot study , 2012, The journal of spinal cord medicine.

[22]  M. Molinari,et al.  Rehabilitation of gait after stroke: a review towards a top-down approach , 2011, Journal of NeuroEngineering and Rehabilitation.

[23]  J. J. Gil,et al.  Lower-Limb Robotic Rehabilitation: Literature Review and Challenges , 2011, J. Robotics.

[24]  Seyed A Safavynia,et al.  Muscle Synergies: Implications for Clinical Evaluation and Rehabilitation of Movement. , 2011, Topics in spinal cord injury rehabilitation.

[25]  Dario Farina,et al.  Impulses of activation but not motor modules are preserved in the locomotion of subacute stroke patients. , 2011, Journal of neurophysiology.

[26]  Kara K. Patterson,et al.  Changes in Gait Symmetry and Velocity After Stroke: A Cross-Sectional Study From Weeks to Years After Stroke , 2010, Neurorehabilitation and neural repair.

[27]  J. Stinear,et al.  A paradox: after stroke, the non‐lesioned lower limb motor cortex may be maladaptive , 2010, The European journal of neuroscience.

[28]  Richard R Neptune,et al.  Merging of healthy motor modules predicts reduced locomotor performance and muscle coordination complexity post-stroke. , 2010, Journal of neurophysiology.

[29]  Kara K. Patterson,et al.  Evaluation of gait symmetry after stroke: a comparison of current methods and recommendations for standardization. , 2010, Gait & posture.

[30]  M. Tresch,et al.  The case for and against muscle synergies , 2022 .

[31]  E. Bizzi,et al.  Stability of muscle synergies for voluntary actions after cortical stroke in humans , 2009, Proceedings of the National Academy of Sciences.

[32]  Francesco Lacquaniti,et al.  Modular Control of Limb Movements during Human Locomotion , 2007, The Journal of Neuroscience.

[33]  L. Ting,et al.  Muscle synergies characterizing human postural responses. , 2007, Journal of neurophysiology.

[34]  H. van der Kooij,et al.  Design and Evaluation of the LOPES Exoskeleton Robot for Interactive Gait Rehabilitation , 2007, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[35]  Henk J Stam,et al.  The effects of balance training on gait late after stroke: a randomized controlled trial , 2006, Clinical rehabilitation.

[36]  Yoshiyuki Sankai,et al.  Control method of robot suit HAL working as operator's muscle using biological and dynamical information , 2005, 2005 IEEE/RSJ International Conference on Intelligent Robots and Systems.

[37]  M. Morari,et al.  Robotic Orthosis Lokomat: A Rehabilitation and Research Tool , 2003, Neuromodulation : journal of the International Neuromodulation Society.

[38]  F. Lacquaniti,et al.  Control of foot trajectory in human locomotion: role of ground contact forces in simulated reduced gravity. , 2002, Journal of neurophysiology.

[39]  H. Sebastian Seung,et al.  Learning the parts of objects by non-negative matrix factorization , 1999, Nature.

[40]  S. Olney,et al.  Hemiparetic gait following stroke. Part I: Characteristics , 1996 .

[41]  A. Matsumura,et al.  Effects of gait training using the Hybrid Assistive Limb® in recovery-phase stroke patients: A 2-month follow-up, randomized, controlled study. , 2017, NeuroRehabilitation.

[42]  Avril Mansfield,et al.  Relationship between asymmetry of quiet standing balance control and walking post-stroke. , 2014, Gait & posture.

[43]  R. Garg,et al.  Understanding gait control in post-stroke: implications for management. , 2012, Journal of bodywork and movement therapies.