Neuro-musculoskeletal simulation of instrumented contracture and spasticity assessment in children with cerebral palsy

BackgroundIncreased resistance in muscles and joints is an important phenomenon in patients with cerebral palsy (CP), and is caused by a combination of neural (e.g. spasticity) and non-neural (e.g. contracture) components. The aim of this study was to simulate instrumented, clinical assessment of the hamstring muscles in CP using a conceptual model of contracture and spasticity, and to determine to what extent contracture can be explained by altered passive muscle stiffness, and spasticity by (purely) velocity-dependent stretch reflex.MethodsInstrumented hamstrings spasticity assessment was performed on 11 children with CP and 9 typically developing children. In this test, the knee was passively stretched at slow and fast speed, and knee angle, applied forces and EMG were measured. A dedicated OpenSim model was created with motion and muscles around the knee only. Contracture was modeled by optimizing the passive muscle stiffness parameters of vasti and hamstrings, based on slow stretch data. Spasticity was modeled using a velocity-dependent feedback controller, with threshold values derived from experimental data and gain values optimized for individual subjects. Forward dynamic simulations were performed to predict muscle behavior during slow and fast passive stretches.ResultsBoth slow and fast stretch data could be successfully simulated by including subject-specific levels of contracture and, for CP fast stretches, spasticity. The RMS errors of predicted knee motion in CP were 1.1 ± 0.9° for slow and 5.9 ± 2.1° for fast stretches. CP hamstrings were found to be stiffer compared with TD, and both hamstrings and vasti were more compliant than the original generic model, except for the CP hamstrings. The purely velocity-dependent spasticity model could predict response during fast passive stretch in terms of predicted knee angle, muscle activity, and fiber length and velocity. Only sustained muscle activity, independent of velocity, was not predicted by our model.ConclusionThe presented individually tunable, conceptual model for contracture and spasticity could explain most of the hamstring muscle behavior during slow and fast passive stretch. Future research should attempt to apply the model to study the effects of spasticity and contracture during dynamic tasks such as gait.

[1]  James W. Lance,et al.  The control of muscle tone, reflexes, and movement , 1980, Neurology.

[2]  Richard W. Bohannon,et al.  Interrater reliability of a modified Ashworth scale of muscle spasticity. , 1987, Physical therapy.

[3]  F.E. Zajac,et al.  An interactive graphics-based model of the lower extremity to study orthopaedic surgical procedures , 1990, IEEE Transactions on Biomedical Engineering.

[4]  A. Thilmann,et al.  The mechanism of spastic muscle hypertonus. Variation in reflex gain over the time course of spasticity. , 1991, Brain : a journal of neurology.

[5]  J. Fridén,et al.  Intraoperative measurement and biomechanical modeling of the flexor carpi ulnaris-to-extensor carpi radialis longus tendon transfer. , 1997, Journal of biomechanical engineering.

[6]  T. Sinkjær,et al.  Soleus long-latency stretch reflexes during walking in healthy and spastic humans , 1999, Clinical Neurophysiology.

[7]  G Staude,et al.  Objective motor response onset detection in surface myoelectric signals. , 1999, Medical engineering & physics.

[8]  J. Harlaar,et al.  Passive stiffness characteristics of ankle plantar flexors in hemiplegia. , 2000, Clinical biomechanics.

[9]  Frans C. T. van der Helm,et al.  Musculoskeletal Systems with Intrinsic and Proprioceptive Feedback , 2000 .

[10]  H Rodgers,et al.  Biomechanical examination of a commonly used measure of spasticity. , 2001, Clinical biomechanics.

[11]  M Gough,et al.  Architecture of the medial gastrocnemius in children with spastic diplegia , 2001, Developmental medicine and child neurology.

[12]  D. Sauser,et al.  Progressive bone and joint abnormalities of the spine and lower extremities in cerebral palsy. , 2002, Radiographics : a review publication of the Radiological Society of North America, Inc.

[13]  D. Thelen.  Adjustment of muscle mechanics model parameters to simulate dynamic contractions in older adults. , 2003, Journal of biomechanical engineering.

[14]  J. W. Fee,et al.  Neuromuscular modeling of spasticity in cerebral palsy , 2004, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[15]  S. Delp,et al.  Evaluation of a Deformable Musculoskeletal Model for Estimating Muscle–Tendon Lengths During Crouch Gait , 2001, Annals of Biomedical Engineering.

[16]  M Gough,et al.  Three-dimensional realisation of muscle morphology and architecture using ultrasound. , 2004, Gait & posture.

[17]  J. Gracies,et al.  Pathophysiology of spastic paresis. II: Emergence of muscle overactivity , 2005, Muscle & nerve.

[18]  B. Dan,et al.  A report: the definition and classification of cerebral palsy April 2006 , 2007, Developmental medicine and child neurology. Supplement.

[19]  Adam P Shortland,et al.  The morphology of the medial gastrocnemius in typically developing children and children with spastic hemiplegic cerebral palsy. , 2007, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[20]  Ayman Habib,et al.  OpenSim: Open-Source Software to Create and Analyze Dynamic Simulations of Movement , 2007, IEEE Transactions on Biomedical Engineering.

[21]  Scott L. Delp,et al.  A Model of the Lower Limb for Analysis of Human Movement , 2010, Annals of Biomedical Engineering.

[22]  Maarten F Bobbert,et al.  Robust passive dynamics of the musculoskeletal system compensate for unexpected surface changes during human hopping. , 2009, Journal of applied physiology.

[23]  Erwin de Vlugt,et al.  The relation between neuromechanical parameters and Ashworth score in stroke patients , 2010, Journal of NeuroEngineering and Rehabilitation.

[24]  M. Schwartz,et al.  The identification and treatment of gait problems in cerebral palsy , 2009 .

[25]  A. Shortland,et al.  Dynamic measurement of gastrocnemius belly length during walking in typically developing children and children with cerebral palsy , 2009 .

[26]  M. Lebiedowska,et al.  Knee resistance during passive stretch in patients with hypertonia , 2009, Journal of Neuroscience Methods.

[27]  J. Harlaar,et al.  Dynamic spasticity of plantar flexor muscles in cerebral palsy gait. , 2010, Journal of rehabilitation medicine.

[28]  K. Himmelmann,et al.  The changing panorama of cerebral palsy in Sweden. X. Prevalence and origin in the birth‐year period 1999–2002 , 2010, Acta paediatrica.

[29]  Josien C van den Noort,et al.  Evaluation of the catch in spasticity assessment in children with cerebral palsy. , 2010, Archives of physical medicine and rehabilitation.

[30]  D. Wenger.  The Identification and Treatment of Gait Problems in Cerebral Palsy, 2nd Edition , 2010 .

[31]  P. Suetens,et al.  Level of subject-specific detail in musculoskeletal models affects hip moment arm length calculation during gait in pediatric subjects with increased femoral anteversion. , 2011, Journal of biomechanics.

[32]  Jack Crosbie,et al.  No change in calf muscle passive stiffness after botulinum toxin injection in children with cerebral palsy , 2011, Developmental medicine and child neurology.

[33]  Lucas R. Smith,et al.  Hamstring contractures in children with spastic cerebral palsy result from a stiffer extracellular matrix and increased in vivo sarcomere length , 2011, The Journal of physiology.

[34]  Fan Gao,et al.  In Vivo Evaluations of Morphologic Changes of Gastrocnemius Muscle Fascicles and Achilles Tendon in Children with Cerebral Palsy , 2011, American journal of physical medicine & rehabilitation.

[35]  Richard Baker,et al.  Medial gastrocnemius muscle volume and fascicle length in children aged 2 to 5 years with cerebral palsy , 2011, Developmental medicine and child neurology.

[36]  Yupeng Ren,et al.  Changes of calf muscle-tendon biomechanical properties induced by passive-stretching and active-movement training in children with cerebral palsy. , 2011, Journal of applied physiology.

[37]  Erwin de Vlugt,et al.  Differentiation between non-neural and neural contributors to ankle joint stiffness in cerebral palsy , 2013, Journal of NeuroEngineering and Rehabilitation.

[38]  S. Delp,et al.  How robust is human gait to muscle weakness? , 2011, Gait & posture.

[39]  L. Leistritz,et al.  The growth and the development of gastro-soleus contracture in cerebral palsy , 2013 .

[40]  K Desloovere,et al.  A clinical measurement to quantify spasticity in children with cerebral palsy by integration of multidimensional signals. , 2013, Gait & posture.

[41]  Ilse Jonkers,et al.  Altering length and velocity feedback during a neuro-musculoskeletal simulation of normal gait contributes to hemiparetic gait characteristics , 2014, Journal of NeuroEngineering and Rehabilitation.

[42]  Thomas Sinkjær,et al.  Passive muscle properties are altered in children with cerebral palsy before the age of 3 years and are difficult to distinguish clinically from spasticity , 2013, Developmental medicine and child neurology.

[43]  Peter A. Huijing,et al.  Intramuscular Connective Tissue Differences in Spastic and Control Muscle: A Mechanical and Histological Study , 2014, PloS one.

[44]  J Harlaar,et al.  Identification of the neural component of torque during manually-applied spasticity assessments in children with cerebral palsy. , 2014, Gait & posture.

[45]  K. Desloovere,et al.  Instrumented assessment of the effect of Botulinum Toxin-A in the medial hamstrings in children with cerebral palsy. , 2014, Gait & posture.

[46]  Goele Pipeleers,et al.  A new method for estimating subject‐specific muscle–tendon parameters of the knee joint actuators: a simulation study , 2014, International journal for numerical methods in biomedical engineering.

[47]  Kaat Desloovere,et al.  The relation between spasticity and muscle behavior during the swing phase of gait in children with cerebral palsy. , 2014, Research in developmental disabilities.

[48]  K. Desloovere,et al.  Muscle Activation Patterns When Passively Stretching Spastic Lower Limb Muscles of Children with Cerebral Palsy , 2014, PloS one.

[49]  Stephen F. Keevil,et al.  Lower limb muscle volumes in bilateral spastic cerebral palsy , 2014, Brain and Development.

[50]  R. Lieber,et al.  Pathophysiology of muscle contractures in cerebral palsy. , 2015, Physical medicine and rehabilitation clinics of North America.

[51]  Jaap Harlaar,et al.  The validity and reliability of modelled neural and tissue properties of the ankle muscles in children with cerebral palsy. , 2015, Gait & posture.

[52]  L. Döderlein,et al.  Effects of ankle–foot braces on medial gastrocnemius morphometrics and gait in children with cerebral palsy , 2015, Journal of children's orthopaedics.