Quantitative Modeling of Spasticity for Clinical Assessment, Treatment and Rehabilitation

Spasticity, a common symptom in patients with upper motor neuron lesions, reduces the ability of a person to freely move their limbs by generating unwanted reflexes. Spasticity can interfere with rehabilitation programs and cause pain, muscle atrophy and musculoskeletal deformities. Despite its prevalence, it is not commonly understood. Widely used clinical scores are neither accurate nor reliable for spasticity assessment and follow up of treatments. Advancement of wearable sensors, signal processing and robotic platforms have enabled new developments and modeling approaches to better quantify spasticity. In this paper, we review quantitative modeling techniques that have been used for evaluating spasticity. These models generate objective measures to assess spasticity and use different approaches, such as purely mechanical modeling, musculoskeletal and neurological modeling, and threshold control-based modeling. We compare their advantages and limitations and discuss the recommendations for future studies. Finally, we discuss the focus on treatment and rehabilitation and the need for further investigation in those directions.

[1]  W. Rymer,et al.  Abnormal muscle coactivation patterns during isometric torque generation at the elbow and shoulder in hemiparetic subjects. , 1995, Brain : a journal of neurology.

[2]  M. Wallen,et al.  Functional outcomes of intramuscular botulinum toxin type a and occupational therapy in the upper limbs of children with cerebral palsy: a randomized controlled trial. , 2007, Archives of physical medicine and rehabilitation.

[3]  Mindy F Levin,et al.  Tonic Stretch Reflex Threshold as a Measure of Ankle Plantar-Flexor Spasticity After Stroke , 2015, Physical Therapy.

[4]  DE Wood,et al.  Theoretical and methodological considerations in the measurement of spasticity , 2005, Disability and rehabilitation.

[5]  Kamiar Aminian,et al.  An Accurate Wearable Foot Clearance Estimation System: Toward a Real-Time Measurement System , 2017, IEEE Sensors Journal.

[6]  T. Twitchell The restoration of motor function following hemiplegia in man. , 1951, Brain : a journal of neurology.

[7]  Kamiar Aminian,et al.  Improving activity recognition using a wearable barometric pressure sensor in mobility-impaired stroke patients , 2015, Journal of NeuroEngineering and Rehabilitation.

[8]  Tao Liu,et al.  Gait Analysis Using Wearable Sensors , 2012, Sensors.

[9]  Hyeok Dong Lee,et al.  Evaluation of Validity and Reliability of Inertial Measurement Unit-Based Gait Analysis Systems , 2018, Annals of rehabilitation medicine.

[10]  G. Johnson,et al.  A systematic review of the Tardieu Scale for the measurement of spasticity , 2006, Disability and rehabilitation.

[11]  S. Hasson,et al.  Electrophysiological evaluation of the Modified Tardieu Scale (MTS) in assessing poststroke wrist flexor spasticity. , 2014, NeuroRehabilitation.

[12]  P. van Vliet,et al.  Reliability of measurements obtained with the modified Ashworth scale in the lower extremities of people with stroke. , 2002, Physical therapy.

[13]  M. Levin,et al.  Relief of hemiparetic spasticity by TENS is associated with improvement in reflex and voluntary motor functions. , 1992, Electroencephalography and clinical neurophysiology.

[14]  J. Opara,et al.  Treatment of spinal spasticity by electrical stimulation. , 1988, Journal of biomedical engineering.

[15]  Xun Chen,et al.  A Regression-Based Framework for Quantitative Assessment of Muscle Spasticity Using Combined EMG and Inertial Data From Wearable Sensors , 2019, Front. Neurosci..

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

[17]  AD Pandyan,et al.  Spasticity: Clinical perceptions, neurological realities and meaningful measurement , 2005, Disability and rehabilitation.

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

[19]  O. J. Espinosa [Hemiplegia]. , 1957, Medicina.

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

[21]  Thomas Seel,et al.  IMU-Based Joint Angle Measurement for Gait Analysis , 2014, Sensors.

[22]  W. Z. Rymer,et al.  Effect of Muscle Biomechanics on the Quantification of Spasticity , 2001, Annals of Biomedical Engineering.

[23]  Kaat Desloovere,et al.  The Intra- and Inter-Rater Reliability of an Instrumented Spasticity Assessment in Children with Cerebral Palsy , 2015, PloS one.

[24]  Robert E Kearney,et al.  Ankle intrinsic stiffness changes with postural sway. , 2019, Journal of biomechanics.

[25]  Lorenzo Fiori,et al.  Biomechanical Load Evaluation by Means of Wearable Devices in Industrial Environments: An Inertial Motion Capture System and sEMG Based Protocol , 2018 .

[26]  Simona Crea,et al.  Technologically-advanced assessment of upper-limb spasticity: a pilot study. , 2018, European journal of physical and rehabilitation medicine.

[27]  B. Bhakta,et al.  Management of spasticity in stroke. , 2000, British medical bulletin.

[28]  Brian Caulfield,et al.  Evaluating rehabilitation exercise performance using a single inertial measurement unit , 2013, 2013 7th International Conference on Pervasive Computing Technologies for Healthcare and Workshops.

[29]  A. G. Feldman,et al.  Stretch reflex spatial threshold measure discriminates between spasticity and rigidity , 2013, Clinical Neurophysiology.

[30]  N. Mayer,et al.  Clinicophysiologic concepts of spasticity and motor dysfunction in adults with an upper motoneuron lesion , 1997, Muscle & nerve. Supplement.

[31]  Hermano Igo Krebs,et al.  Summary of Human Ankle Mechanical Impedance During Walking , 2016, IEEE Journal of Translational Engineering in Health and Medicine.

[32]  William Z Rymer,et al.  The relation between Ashworth scores and neuromechanical measurements of spasticity following stroke , 2008, Journal of NeuroEngineering and Rehabilitation.

[33]  Nebahat Sezer,et al.  Chronic complications of spinal cord injury. , 2015, World journal of orthopedics.

[34]  C. Oreja-Guevara,et al.  Spasticity in multiple sclerosis: results of a patient survey , 2013, The International journal of neuroscience.

[35]  Á. Pascual-Leone,et al.  Reduction of Spasticity With Repetitive Transcranial Magnetic Stimulation in Patients With Spinal Cord Injury , 2010, Neurorehabilitation and neural repair.

[36]  Michael P Barnes,et al.  Are we underestimating the clinical efficacy of botulinum toxin (type A)? Quantifying changes in spasticity, strength and upper limb function after injections of Botox® to the elbow flexors in a unilateral stroke population , 2002, Clinical rehabilitation.

[37]  Kamiar Aminian,et al.  Ambulatory system for human motion analysis using a kinematic sensor: monitoring of daily physical activity in the elderly , 2003, IEEE Transactions on Biomedical Engineering.

[38]  Ö. Ekeberg,et al.  Neural and non-neural related properties in the spastic wrist flexors: An optimization study. , 2017, Medical engineering & physics.

[39]  A. Santiago,et al.  Development of a wearable ZigBee sensor system for upper limb rehabilitation robotics , 2012, 2012 4th IEEE RAS & EMBS International Conference on Biomedical Robotics and Biomechatronics (BioRob).

[40]  E. Dinya,et al.  Recovery of motor disability and spasticity in post-stroke after repetitive transcranial magnetic stimulation (rTMS) , 2008, Brain Research Bulletin.

[41]  K. Aminian,et al.  Ambulatory measurement of 3D knee joint angle. , 2008, Journal of biomechanics.

[42]  Ying Cheng,et al.  Motor Function Evaluation of Hemiplegic Upper-Extremities Using Data Fusion from Wearable Inertial and Surface EMG Sensors , 2017, Sensors.

[43]  Anatol G. Feldman,et al.  Stretch-reflex threshold modulation during active elbow movements in post-stroke survivors with spasticity , 2017, Clinical Neurophysiology.

[44]  A. Fugl-Meyer,et al.  The post-stroke hemiplegic patient. 1. a method for evaluation of physical performance. , 1975, Scandinavian journal of rehabilitation medicine.

[45]  E. Roth,et al.  Biomechanic changes in passive properties of hemiplegic ankles with spastic hypertonia. , 2004, Archives of physical medicine and rehabilitation.

[46]  Hyung-Soon Park,et al.  Haptic recreation of elbow spasticity , 2011, 2011 IEEE International Conference on Rehabilitation Robotics.

[47]  M. Levin,et al.  Regulation of stretch reflex threshold in elbow flexors in children with cerebral palsy: a new measure of spasticity , 2000, Developmental medicine and child neurology.

[48]  Thomas Bauermann,et al.  Occurence and Clinical Predictors of Spasticity After Ischemic Stroke , 2010, Stroke.

[49]  DE Wood,et al.  Biomechanical approaches applied to the lower and upper limb for the measurement of spasticity: A systematic review of the literature , 2005, Disability and rehabilitation.

[50]  Kaat Desloovere,et al.  Manually controlled instrumented spasticity assessments: a systematic review of psychometric properties , 2014, Developmental medicine and child neurology.

[51]  B. Erhan,et al.  The effects of different injection techniques of botulinum toxin a in post-stroke patients with plantar flexor spasticity , 2018, Acta Neurologica Belgica.

[52]  Tapas Mondal,et al.  Wearable Sensors for Remote Health Monitoring , 2017, Sensors.

[53]  P. Filipetti,et al.  [Interest of anesthetic blocks for assessment of the spastic patient. A series of 815 motor blocks]. , 2003, Neuro-Chirurgie.

[54]  Anders Fagergren,et al.  Validation of a New Biomechanical Model to Measure Muscle Tone in Spastic Muscles , 2011, Neurorehabilitation and neural repair.

[55]  Kamiar Aminian,et al.  Gait and Foot Clearance Parameters Obtained Using Shoe-Worn Inertial Sensors in a Large-Population Sample of Older Adults , 2013, Sensors.

[56]  Etienne Burdet,et al.  A Clustering-Based Approach to Identify Joint Impedance During Walking , 2020, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[57]  Marko Munih,et al.  Using Inertial Measurement Units and Electromyography to Quantify Movement during Action Research Arm Test Execution , 2018, Sensors.

[58]  Electrical Stimulation for Modulation of Spasticity in Hemiplegic and Spinal Cord Injury Subjects , 2001, Neuromodulation : journal of the International Neuromodulation Society.

[59]  N. Mercuri,et al.  Changes in spasticity following functional electrical stimulation cycling in patients with spinal cord injury: A systematic review , 2020, The journal of spinal cord medicine.

[60]  Etienne Burdet,et al.  A simple tool to measure spasticity in spinal cord injury subjects , 2017, 2017 International Conference on Rehabilitation Robotics (ICORR).

[61]  Chandramouli Krishnan,et al.  Validity and repeatability of inertial measurement units for measuring gait parameters. , 2017, Gait & posture.

[62]  J S Rietman,et al.  Stop using the Ashworth Scale for the assessment of spasticity , 2009, Journal of Neurology, Neurosurgery & Psychiatry.

[63]  Pagamas Piriyaprasarth,et al.  The reliability of knee joint position testing using electrogoniometry , 2008, BMC musculoskeletal disorders.

[64]  L. Ada,et al.  Contribution of thixotropy, spasticity, and contracture to ankle stiffness after stroke , 2000, Journal of neurology, neurosurgery, and psychiatry.

[65]  C. Blomstrand,et al.  Increased muscle tone and contracture late after ischemic stroke , 2020, Brain and behavior.

[66]  B M Jolles,et al.  Functional calibration procedure for 3D knee joint angle description using inertial sensors. , 2009, Journal of biomechanics.

[67]  Katherine M Steele,et al.  Repeatability of electromyography recordings and muscle synergies during gait among children with cerebral palsy. , 2019, Gait & posture.

[68]  S. N. Sidek,et al.  Clasp-Knife Model of Muscle Spasticity for Simulation of Robot-Human Interaction , 2019, IEEE Access.

[69]  K.,et al.  Reliability of measurements of muscle tone and muscle power in stroke patients. , 2000, Age and ageing.

[70]  J M Rothstein,et al.  Goniometric reliability in a clinical setting. Elbow and knee measurements. , 1984, Physical therapy.

[71]  A. G. Feldman,et al.  Implicit learning and generalization of stretch response modulation in humans. , 2016, Journal of neurophysiology.

[72]  Chul-Gyu Song,et al.  Portable measurement system for the objective evaluation of the spasticity of hemiplegic patients based on the tonic stretch reflex threshold. , 2011, Medical engineering & physics.

[73]  AD Pandyan,et al.  Spasticity, an impairment that is poorly defined and poorly measured , 2009, Clinical rehabilitation.

[74]  Junaidah Bte Mustafa Kamal.,et al.  Remote health monitoring. , 2013 .

[75]  Yasuhiro Kagamihara,et al.  [Pathophysiology of spasticity]. , 2014, Brain and nerve = Shinkei kenkyu no shinpo.

[76]  E S Grood,et al.  A joint coordinate system for the clinical description of three-dimensional motions: application to the knee. , 1983, Journal of biomechanical engineering.

[77]  Nikolaos G. Bourbakis,et al.  A Survey on Wearable Sensor-Based Systems for Health Monitoring and Prognosis , 2010, IEEE Transactions on Systems, Man, and Cybernetics, Part C (Applications and Reviews).

[78]  Symposium synopsis , 1986 .

[79]  J. Jankovic Parkinson’s disease: clinical features and diagnosis , 2008, Journal of Neurology, Neurosurgery, and Psychiatry.

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

[81]  Ilse Jonkers,et al.  A spasticity model based on feedback from muscle force explains muscle activity during passive stretches and gait in children with cerebral palsy , 2018, PloS one.

[82]  R WARTENBERG,et al.  Pendulousness of the Legs as a Diagnostic Test , 1951, Neurology.

[83]  A. Joseph Threlkeld,et al.  Differentiation between the contributions of shortening reaction and stretch-induced inhibition to rigidity in Parkinson’s disease , 2011, Experimental Brain Research.

[84]  Hyung-Soon Park,et al.  Position as Well as Velocity Dependence of Spasticity—Four-Dimensional Characterizations of Catch Angle , 2018, Front. Neurol..

[85]  Eduardo Palermo,et al.  Spasticity Measurement Based on Tonic Stretch Reflex Threshold in Children with Cerebral Palsy Using the PediAnklebot , 2017, Front. Hum. Neurosci..

[86]  E. Chao,et al.  An electrogoniometric study of knee motion in normal gait. , 1970, The Journal of bone and joint surgery. American volume.

[87]  Anatol G. Feldman,et al.  The role of stretch reflex threshold regulation in normal and impaired motor control , 1994, Brain Research.

[88]  R. E. Lrvine Movement Therapy in Hemiplegia: A Neurophysiological Approach , 1972 .

[89]  Mindy F Levin,et al.  Threshold position control and the principle of minimal interaction in motor actions. , 2007, Progress in brain research.

[90]  D. Farina,et al.  Surface Electromyography for Noninvasive Characterization of Muscle , 2001, Exercise and sport sciences reviews.

[91]  Yi-Ning Wu,et al.  The use of a portable muscle tone measurement device to measure the effects of botulinum toxin type a on elbow flexor spasticity. , 2005, Archives of physical medicine and rehabilitation.

[92]  Darragh F Whelan,et al.  Technology in Rehabilitation: Evaluating the Single Leg Squat Exercise with Wearable Inertial Measurement Units. , 2016, Methods of information in medicine.

[93]  Kian Jalaleddini,et al.  Ankle Joint Intrinsic Dynamics is More Complex than a Mass-Spring-Damper Model , 2017, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[94]  S. Kim,et al.  Characterization of Spastic Ankle Flexors Based on Viscoelastic Modeling for Accurate Diagnosis , 2020 .

[95]  David Burke,et al.  Pathophysiology of spasticity in stroke , 2013, Neurology.

[96]  M. Granat,et al.  Electrical stimulation of wrist extensors in poststroke hemiplegia. , 1999, Stroke.

[97]  H Rodgers,et al.  A review of the properties and limitations of the Ashworth and modified Ashworth Scales as measures of spasticity , 1999, Clinical rehabilitation.

[98]  恭秀 中山,et al.  modified Ashworth scaleによる痙縮評価の日内変動に関する研究 , 2004 .

[99]  Lena H. Ting,et al.  Force encoding in muscle spindles during stretch of passive muscle , 2017, PLoS Comput. Biol..

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

[101]  Etienne Burdet,et al.  The Influence of Posture, Applied Force and Perturbation Direction on Hip Joint Viscoelasticity , 2020, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[102]  Anatol G. Feldman,et al.  Spasticity measurement based on tonic stretch reflex threshold in stroke using a portable device , 2008, Clinical Neurophysiology.

[103]  Terry K K Koo,et al.  A neuromusculoskeletal model to simulate the constant angular velocity elbow extension test of spasticity. , 2006, Medical engineering & physics.

[104]  Y. Wang,et al.  A dynamic neuromuscular model for describing the pendulum test of spasticity , 1997, IEEE Transactions on Biomedical Engineering.

[105]  J. M. Rothstein,et al.  Goniometric Reliability in a Clinical Setting , 1983 .

[106]  Faicel Chamroukhi,et al.  Physical Human Activity Recognition Using Wearable Sensors , 2015, Sensors.

[107]  Andreas Daffertshofer,et al.  Improving EMG-based muscle force estimation by using a high-density EMG grid and principal component analysis , 2006, IEEE Transactions on Biomedical Engineering.