Advertisement
Original research| Volume 99, ISSUE 11, P2175-2182, November 2018

Associations Between Muscle Synergies and Treatment Outcomes in Cerebral Palsy Are Robust Across Clinical Centers

Published:April 10, 2018DOI:https://doi.org/10.1016/j.apmr.2018.03.006

      Highlights

      • Synergies were associated with posttreatment gait outcomes.
      • This association was independent of treatment group at both centers.
      • Less impaired motor control was associated with faster walking posttreatment.
      • Less impaired motor control was associated with greater improvements in kinematics.
      • Associations were similar across 2 commonly used clinical muscle sets.

      Abstract

      Objective

      To determine whether patient-specific differences in motor control quantified using muscle synergy analysis were associated with changes in gait after treatment of cerebral palsy (CP) across 2 clinical centers with different treatments and clinical protocols.

      Design

      Retrospective cohort study.

      Setting

      Clinical medical center.

      Participants

      Center 1: children with CP (n=473) and typically developing (TD) children (n=84). Center 2: children with CP (n=163) and TD children (n=12).

      Interventions

      Standard clinical care at each center.

      Main Outcome Measures

      The Dynamic Motor Control Index During Walking (walk-DMC) was computed from electromyographic data during gait using muscle synergy analysis. Regression analysis was used to evaluate whether pretreatment walking speed or kinematics, muscle synergies, treatment group, prior treatment, or age were associated with posttreatment changes in gait at both clinical centers.

      Results

      Walk-DMC was significantly associated with changes in speed and kinematics after treatment with similar regression models at both centers. Children with less impaired motor control were more likely to have improvements in walking speed and gait kinematics after treatment, independent of treatment group.

      Conclusions

      Dynamic motor control evaluated with synergy analysis was associated with changes in gait after treatment at both centers, despite differences in treatments and clinical protocols. This study further supports the finding that walk-DMC provides additional information, not captured in traditional gait analysis, that may be useful for treatment planning.

      Keywords

      List of abbreviations:

      BTA (botulinum toxin type A), CP (cerebral palsy), GDI (Gait Deviation Index), SDR (selective dorsal rhizotomy), SEMLS (single-event multilevel orthopedic surgery), TD (typically developing), tVAF (total variance accounted for), walk-DMC (Dynamic Motor Control Index During Walking)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Archives of Physical Medicine and Rehabilitation
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Cahill-Rowley K.
        • Rose J.
        Etiology of impaired selective motor control: emerging evidence and its implications for research and treatment in cerebral palsy.
        Dev Med Child Neurol. 2014; 56: 522-528
        • Steele K.M.
        • Rozumalski A.
        • Schwartz M.H.
        Muscle synergies and complexity of neuromuscular control during gait are altered in individuals with cerebral palsy.
        Dev Med Child Neurol. 2015; 57: 1176-1182
        • Schwartz M.H.
        • Rozumalski A.
        • Steele K.M.
        Dynamic motor control is associated with treatment outcomes for children with cerebral palsy.
        Dev Med Child Neurol. 2016; 58: 1139-1145
        • Begley C.G.
        • Ioannidis J.P.
        Reproducibility in science: improving the standard for basic and preclinical research.
        Circ Res. 2015; 116: 116-126
        • Gormley M.E.
        • Gaebler-Spira D.
        • Delgado M.R.
        Use of botulinum toxin type A in pediatric patients with cerebral palsy: a three-center retrospective chart review.
        J Child Neurol. 2001; 16: 113-118
        • Mclaughlin J.
        • Bjornson K.
        • Temkin N.
        • et al.
        Selective dorsal rhizotomy: meta-analysis of three randomized controlled trials.
        Dev Med Child Neurol. 2002; 44: 17-25
        • Lamberts R.P.
        • Burger M.
        • Toit J.
        • Langerak N.G.
        A systematic review of the effects of single-event multilevel surgery on gait parameters in children with spastic cerebral palsy.
        PLoS One. 2016; 11: 1-22
        • Ting L.H.
        • Chiel H.J.
        • Trumbower R.D.
        • et al.
        Perspective neuromechanical principles underlying movement modularity and their implications for rehabilitation.
        Neuron. 2015; 86: 38-54
        • Tresch M.C.
        • Jarc A.
        The case for and against muscle synergies.
        Curr Opin Neurobiol. 2009; 19: 601
        • Neptune R.R.
        • Clark D.J.
        • Kautz S.A.
        Modular control of human walking: a simulation study.
        J Biomech. 2009; 42: 1282-1287
        • Oliveira A.S.
        • Gizzi L.
        • Farina D.
        • Kersting U.G.
        Motor modules of human locomotion: influence of EMG averaging, concatenation, and number of step cycles.
        Front Hum Neurosci. 2014; 8: 335
        • Clark D.J.
        • Ting L.H.
        • Zajac F.E.
        • Neptune R.R.
        • Kautz S.A.
        Merging of healthy motor modules predicts reduced locomotor performance and muscle coordination complexity post-stroke.
        J Neurophysiol. 2010; 103: 844-857
        • Routson R.L.
        • Clark D.J.
        • Bowden M.G.
        • Kautz S.A.
        • Neptune R.R.
        The influence of locomotor rehabilitation on module quality and post-stroke hemiparetic walking performance.
        Gait Posture. 2013; 38: 511-517
        • Tang L.
        • Li F.
        • Cao S.
        • Zhang X.
        • Wu D.
        • Chen X.
        Muscle synergy analysis in children with cerebral palsy.
        J Neural Eng. 2015; 12: 046017
        • Cappellini G.
        • Ivanenko Y.P.
        • Martino G.
        • et al.
        Immature spinal locomotor output in children with cerebral palsy.
        Front Physiol. 2016; 7: 478
        • Shuman B.
        • Goudriaan M.
        • Bar-On L.
        • Schwartz M.H.
        • Desloovere K.
        • Steele K.M.
        Repeatability of muscle synergies within and between days for typically developing children and children with cerebral palsy.
        Gait Posture. 2016; 45: 127-132
        • Shuman B.R.
        • Schwartz M.H.
        • Steele K.M.
        Electromyography data processing impacts muscle synergies during gait for unimpaired children and children with cerebral palsy.
        Front Comput Neurosci. 2017; 11: 50
        • Schwartz M.H.
        • Rozumalski A.
        The Gait Deviation Index: a new comprehensive index of gait pathology.
        Gait Posture. 2008; 28: 351-357
        • Li Y.
        • Ngom A.
        The non-negative matrix factorization toolbox for biological data mining.
        Source Code Biol Med. 2013; 8: 1-26
        • Kim H.
        • Park H.
        Sparse non-negative matrix factorizations via alternating non-negativity-constrained least squares for microarray data analysis.
        Bioinformatics. 2007; 23: 1495-1502
        • Tresch M.C.
        • Cheung V.C.
        • d’Avella A.
        Matrix factorization algorithms for the identification of muscle synergies: evaluation on simulated and experimental data sets.
        J Neurophysiol. 2006; 95: 2199-2212
        • Hof A.L.
        Scaling gait data to body size.
        Gait Posture. 1996; 4: 222-223
        • Dominici N.
        • Dominici N.
        • Ivanenko Y.P.
        • et al.
        Locomotor primitives in newborn babies and their development.
        Science. 2011; 334: 997-999
        • Maclellan M.J.
        • Ivanenko Y.P.
        • Massaad F.
        • Bruijn S.M.
        • Duysens J.
        • Lacquaniti F.
        Muscle activation patterns are bilaterally linked during split-belt treadmill walking in humans.
        J Neurophysiol. 2014; 111: 1541-1552
        • Sauerbrei W.
        The use of resampling methods to simplify regression models in medical statistics.
        Appl Stat. 1999; 48: 313-329
        • Baker R.
        • Mcginley J.L.
        • Schwartz M.
        • Thomason P.
        • Rodda J.
        • Graham H.K.
        The minimal clinically important difference for the Gait Profile Score.
        Gait Posture. 2012; 35: 612-615
        • Oeffinger D.
        • Bagley A.
        • Rogers S.
        • et al.
        Outcome tools used for ambulatory children with cerebral palsy: responsiveness and minimum clinically important differences.
        Dev Med Child Neurol. 2010; 50: 918-925
        • Rutz E.
        • Donath S.
        • Tirosh O.
        • Graham H.K.
        • Baker R.
        Explaining the variability improvements in gait quality as a result of single event multi-level surgery in cerebral palsy.
        Gait Posture. 2013; 38: 455-460
        • Hicks J.L.
        • Delp S.L.
        • Schwartz M.H.
        Can biomechanical variables predict improvement in crouch gait?.
        Gait Posture. 2012; 34: 197-201
        • Huenaerts C.
        • Molenaers G.
        • Nieuwenhuys A.
        • Pauwels P.
        • Monari D.
        • Desloovere K.
        Session OS12 multilevel problems in cerebral palsy.
        Gait Posture. 2015; 42: S54-S55
        • Molenaers G.
        • Van Campenhout A.
        • Fagard K.
        • De Cat J.
        • Desloovere K.
        The use of botulinum toxin A in children with cerebral palsy, with a focus on the lower limb.
        J Child Orthop. 2010; 4: 183-195