Validity, Intra-Rater Reliability and Normative Data of the Neuroflexor™ Device to Measure Spasticity of the Ankle Plantar Flexors after Stroke
DOI:
https://doi.org/10.2340/jrm.v54.2067Keywords:
stroke, muscle spasticity, stretch reflex, outcome assessment, lower extremityAbstract
Objective: Quantification of lower limb spasticity after stroke and the differentiation of neural from passive muscle resistance remain key clinical challenges. The aim of this study was to validate the novel NeuroFlexor foot module, to assess the intrarater reliability of measurements and to identify normative cut-off values.
Methods: Fifteen patients with chronic stroke with clinical history of spasticity and 18 healthy subjects were examined with the NeuroFlexor foot module at controlled velocities. Elastic, viscous and neural components of passive dorsiflexion resistance were quantified (in Newton, N). The neural component, reflecting stretch reflex mediated resistance, was validated against electromyography activity. A test-retest design with a 2-way random effects model permitted study of intra-rater reliability. Finally, data from 73 healthy subjects were used to establish cutoff values according to mean + 3 standard deviations and receiver operating characteristic curve analysis.
Results: The neural component was higher in stroke patients, increased with stretch velocity and correlated with electromyography amplitude. Reliability was high for the neural component (intraclass correlation coefficient model 2.1 (ICC2,1) ≥ 0.903) and good for the elastic component (ICC2,1 ≥ 0.898). Cutoff values were identified, and all patients with neural component above the limit presented pathological electromyography amplitude (area under the curve (AUC) = 1.00, sensitivity = 100%, specificity = 100%).
Conclusion: The NeuroFlexor may offer a clinically feasible and non-invasive way to objectively quantify lower limb spasticity.
LAY ABSTRACT
Spasticity is a sensorimotor impairment, which often occurs after stroke as well as after other injuries to the central nervous system. Spasticity is characterized by increased resistance to passive stretch of weak muscles due to increased reflex activity. Spasticity is currently measured clinically while the examiner passively stretches a muscle. However, the clinical method cannot differentiate resistance due to increased reflex activity from resistance due to muscle stiffness, which can develop over time in weakened muscles. The aim of this study was to evaluate the novel NeuroFlexor foot module, which was developed to quantify and distinguish nerve and muscle components of resistance during passive stretching of the lower limb muscles. By quantifying these factors, one can obtain more reliable information than the clinical examination allows. NeuroFlexor measurements in 15 patients in the chronic stage after stroke and 18 healthy individuals allowed the validity of the method to be evaluated by assessing the relationship with velocity of stretch and by simultaneously examining the reflex activity using surface electromyography. The reliability of NeuroFlexor measurements was studied by comparing repeated measurements. Finally, the study established normal NeuroFlexor values from 73 healthy individuals. The results suggest that the NeuroFlexor foot module may be a valid, reliable and easy-to-use objective method to quantify lower limb spasticity.
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References
Wissel J, Manack A, Brainin M. Toward an epidemiology of poststroke spasticity. Neurology 2013; 80: S13-S19.
https://doi.org/10.1212/WNL.0b013e3182762448 DOI: https://doi.org/10.1212/WNL.0b013e3182762448
Francisco GE, McGuire JR. Poststroke spasticity management. Stroke 2012; 43: 3132-3136.
https://doi.org/10.1161/STROKEAHA.111.639831 DOI: https://doi.org/10.1161/STROKEAHA.111.639831
Zeng H, Chen J, Guo Y, Tan S. Prevalence and risk factors for spasticity after stroke: a systematic review and meta-analysis. Front Neurol 2021; 11: 616097.
https://doi.org/10.3389/fneur.2020.616097 DOI: https://doi.org/10.3389/fneur.2020.616097
Sommerfeld DK, Eek EU, Svensson AK, Holmqvist LW, von Arbin MH. Spasticity after stroke: its occurrence and association with motor impairments and activity limitations. Stroke 2004; 35: 134-139.
https://doi.org/10.1161/01.STR.0000105386.05173.5E DOI: https://doi.org/10.1161/01.STR.0000105386.05173.5E
Arene N, Hidler J. Understanding motor impairment in the paretic lower limb after a stroke: a review of the literature. Top Stroke Rehabil 2009; 16: 346-356.
https://doi.org/10.1310/tsr1605-346 DOI: https://doi.org/10.1310/tsr1605-346
Jansen K, De Groote F, Aerts W, De Schutter J, Duysens J, Jonkers I. Altering length and velocity feedback during a neuro-musculoskeletal simulation of normal gait contributes to hemiparetic gait characteristics. J Neuroeng Rehabil 2014; 11: 78.
https://doi.org/10.1186/1743-0003-11-78 DOI: https://doi.org/10.1186/1743-0003-11-78
Lance JW. Symposium synopsis. In: Feldman RG, Young RR, Koella WP, editors. Spasticity, disordered motor control. Chicago: Year Book Medical Publishers; 1980, p. 485-494.
Ashworth B. Preliminary trial of carisoprodol in multiple sclerosis. Practitioner 1964; 192: 540-542.
Patrick E, Ada L. The Tardieu Scale differentiates contracture from spasticity whereas the Ashworth Scale is confounded by it. Clin Rehabil 2006; 20: 173-182.
https://doi.org/10.1191/0269215506cr922oa DOI: https://doi.org/10.1191/0269215506cr922oa
Bohannon RW, Smith MB. Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther 1987; 67: 206-207.
https://doi.org/10.1093/ptj/67.2.206 DOI: https://doi.org/10.1093/ptj/67.2.206
Harb A, Kishner S. Modified Ashworth Scale. StatPearls. Treasure Island (FL): StatPearls Publishing; 2020.
Fleuren JF, Voerman GE, Erren-Wolters CV, Snoek GJ, Rietman JS, Hermens HJ, et al. Stop using the Ashworth Scale for the assessment of spasticity. J Neurol Neurosurg Psychiatry 2010; 81: 46-52.
https://doi.org/10.1136/jnnp.2009.177071 DOI: https://doi.org/10.1136/jnnp.2009.177071
Ansari NN, Naghdi S, Hasson S, Rastgoo M, Amini M, Forogh B. Clinical assessment of ankle plantarflexor spasticity in adult patients after stroke: inter-and intra-rater reliability of the Modified Tardieu Scale. Brain Inj 2013; 27: 605-612.
https://doi.org/10.3109/02699052.2012.750744 DOI: https://doi.org/10.3109/02699052.2012.750744
Li F, Wu Y, Li X. Test-retest reliability and inter-rater reliability of the Modified Tardieu Scale and the Modified Ashworth Scale in hemiplegic patients with stroke. Eur J Phys Rehabil Med 2014; 50: 9-15.
Meseguer-Henarejos AB, Sánchez-Meca J, López-Pina JA, Carles-Hernández R. Inter- and intra-rater reliability of the Modified Ashworth Scale: a systematic review and meta-analysis. Eur J Phys Rehabil Med 2018; 54: 576-590.
https://doi.org/10.23736/S1973-9087.17.04796-7 DOI: https://doi.org/10.23736/S1973-9087.17.04796-7
Gracies JM. Pathophysiology of spastic paresis. I: Paresis and soft tissue changes. Muscle Nerve 2005; 31: 535-551.
https://doi.org/10.1002/mus.20284 DOI: https://doi.org/10.1002/mus.20284
Thibaut A, Chatelle C, Ziegler E, Bruno MA, Laureys S, Gosseries O. Spasticity after stroke: physiology, assessment and treatment. Brain Inj 2013; 27: 1093-1105.
https://doi.org/10.3109/02699052.2013.804202 DOI: https://doi.org/10.3109/02699052.2013.804202
Bethoux F. Spasticity management after stroke. Phys Med Rehabil Clin N Am 2015; 26: 625-639.
https://doi.org/10.1016/j.pmr.2015.07.003 DOI: https://doi.org/10.1016/j.pmr.2015.07.003
Wissel J, Verrier M, Simpson DM, Charles D, Guinto P, Papapetropoulos S, et al. Post-stroke spasticity: predictors of early development and considerations for therapeutic intervention. PM R 2015; 7: 60-67.
https://doi.org/10.1016/j.pmrj.2014.08.946 DOI: https://doi.org/10.1016/j.pmrj.2014.08.946
Tao W, Yan D, Li JH, Shi ZH. Gait improvement by low-dose botulinum toxin A injection treatment of the lower limbs in subacute stroke patients. J Phys Ther Sci 2015; 27: 759-762.
https://doi.org/10.1589/jpts.27.759 DOI: https://doi.org/10.1589/jpts.27.759
Dong Y, Wu T, Hu X, Wang T. Efficacy and safety of botulinum toxin type A for upper limb spasticity after stroke or traumatic brain injury: a systematic review with meta-analysis and trial sequential analysis. Eur J Phys Rehabil Med 2017; 53: 256-267.
https://doi.org/10.23736/S1973-9087.16.04329-X DOI: https://doi.org/10.23736/S1973-9087.16.04329-X
Santamato A, Cinone N, Panza F, Letizia S, Santoro L, Lozupone M, et al. Botulinum toxin type A for the treatment of lower limb spasticity after stroke. Drugs 2019; 79: 143-160.
https://doi.org/10.1007/s40265-018-1042-z DOI: https://doi.org/10.1007/s40265-018-1042-z
Mahmood A, Veluswamy SK, Hombali A, Mullick A, N M, Solomon JM. Effect of transcutaneous electrical nerve stimulation on spasticity in adults with stroke: a systematic review and meta-analysis. Arch Phys Med Rehabil 2019; 100: 751-768.
https://doi.org/10.1016/j.apmr.2018.10.016 DOI: https://doi.org/10.1016/j.apmr.2018.10.016
Palmcrantz S, Pennati GV, Bergling H, Borg J. Feasibility and potential effects of using the electro-dress Mollii on spasticity and functioning in chronic stroke. J Neuroeng Rehabil 2020; 17: 109.
https://doi.org/10.1186/s12984-020-00740-z DOI: https://doi.org/10.1186/s12984-020-00740-z
Han P, Zhang W, Kang L, Ma Y, Fu L, Jia L, et al. Clinical evidence of exercise benefits for stroke. Adv Exp Med Biol 2017; 1000: 131-151.
https://doi.org/10.1007/978-981-10-4304-8_9 DOI: https://doi.org/10.1007/978-981-10-4304-8_9
Bani-Ahmed A. The evidence for prolonged muscle stretching in ankle joint management in upper motor neuron lesions: considerations for rehabilitation - a systematic review. Top Stroke Rehabil 2019; 26: 153-161.
https://doi.org/10.1080/10749357.2018.1550958 DOI: https://doi.org/10.1080/10749357.2018.1550958
Luo Z, Lo WLA, Bian R, Wong S, Li L. Advanced quantitative estimation methods for spasticity: a literature review. J Int Med Res 2020; 48: 300060519888425.
https://doi.org/10.1177/0300060519888425 DOI: https://doi.org/10.1177/0300060519888425
Lindberg PG, Gaverth J, Islam M, Fagergren A, Borg J, Forssberg H. Validation of a new biomechanical model to measure muscle tone in spastic muscles. Neurorehabil Neural Repair 2011; 25: 617-625.
https://doi.org/10.1177/1545968311403494 DOI: https://doi.org/10.1177/1545968311403494
Gäverth J, Sandgren M, Lindberg PG, Forssberg H, Eliasson AC. Test-retest and inter-rater reliability of a method to measure wrist and finger spasticity. J Rehabil Med 2013; 45: 630-636.
https://doi.org/10.2340/16501977-1160 DOI: https://doi.org/10.2340/16501977-1160
Gaverth J, Eliasson AC, Kullander K, Borg J, Lindberg PG, Forssberg H. Sensitivity of the NeuroFlexor method to measure change in spasticity after treatment with botulinum toxin A in wrist and finger muscles. J Rehabil Med 2014; 46: 629-634.
https://doi.org/10.2340/16501977-1824 DOI: https://doi.org/10.2340/16501977-1824
Andringa A, van Wegen E, van de Port I, Kwakkel G, Meskers C. Measurement properties of the NeuroFlexor device for quantifying neural and non-neural components of wrist hyper-resistance in chronic stroke. Front Neurol 2019; 10: 730.
https://doi.org/10.3389/fneur.2019.00730 DOI: https://doi.org/10.3389/fneur.2019.00730
Pennati GV, Plantin J, Borg J, Lindberg PG. Normative NeuroFlexor data for detection of spasticity after stroke: a cross-sectional study. J Neuroeng Rehabil 2016; 13: 30.
https://doi.org/10.1186/s12984-016-0133-x DOI: https://doi.org/10.1186/s12984-016-0133-x
Pennati GV, Bergling H, Carment L, Borg J, Lindberg PG, Palmcrantz S. Effects of 60 min electrostimulation with the EXOPULSE mollii suit on objective signs of spasticity. Front Neurol 2021; 12: 1741.
https://doi.org/10.3389/fneur.2021.706610 DOI: https://doi.org/10.3389/fneur.2021.706610
Currier DP. Elements of research in physical therapy. 3rd edn. Baltimore: Williams & Wilkins; 1990.
Vaz S, Falkmer T, Passmore AE, Parsons R, Andreou P. The case for using the repeatability coefficient when calculating test-retest reliability. PLoS One 2013; 8: e73990.
https://doi.org/10.1371/journal.pone.0073990 DOI: https://doi.org/10.1371/journal.pone.0073990
Le Sant G, Nordez A, Hug F, Andrade R, Lecharte T, McNair PJ, et al. Effects of stroke injury on the shear modulus of the lower leg muscle during passive dorsiflexion. J Appl Physiol (1985) 2019; 126: 11-22.
https://doi.org/10.1152/japplphysiol.00968.2017 DOI: https://doi.org/10.1152/japplphysiol.00968.2017
Koo TK, Mak AF. A neuromusculoskeletal model to simulate the constant angular velocity elbow extension test of spasticity. Med Eng Phys 2006; 28: 60-69.
https://doi.org/10.1016/j.medengphy.2005.03.012 DOI: https://doi.org/10.1016/j.medengphy.2005.03.012
Burridge JH, Wood DE, Hermens HJ, Voerman GE, Johnson GR, Wijck FV, et al. Theoretical and methodological considerations in the measurement of spasticity. Disabil Rehabil 2005; 27: 69-80.
https://doi.org/10.1080/09638280400014592 DOI: https://doi.org/10.1080/09638280400014592
Aloraini SM, Gäverth J, Yeung E, MacKay-Lyons M. Assessment of spasticity after stroke using clinical measures: a systematic review. Disabil Rehabil 2015; 37: 2313-2323.
https://doi.org/10.3109/09638288.2015.1014933 DOI: https://doi.org/10.3109/09638288.2015.1014933
Wood DE, Burridge JH, van Wijck FM, McFadden C, Hitchcock RA, Pandyan AD, et al. Biomechanical approaches applied to the lower and upper limb for the measurement of spasticity: a systematic review of the literature. Disabil Rehabil 2005; 27: 19-32.
https://doi.org/10.1080/09638280400014683 DOI: https://doi.org/10.1080/09638280400014683
Cha Y, Arami A. Quantitative modeling of spasticity for clinical assessment, treatment and rehabilitation. Sensors 2020; 20: 5046.
https://doi.org/10.3390/s20185046 DOI: https://doi.org/10.3390/s20185046
Baude M, Nielsen JB, Gracies JM. The neurophysiology of deforming spastic paresis: a revised taxonomy. Ann Phys Rehabil Med 2019; 62: 426-430.
https://doi.org/10.1016/j.rehab.2018.10.004 DOI: https://doi.org/10.1016/j.rehab.2018.10.004
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Copyright (c) 2023 Gaia Valentina Pennati, Loïc Carment, Alison K. Godbolt, Jeanette Plantin, Jörgen Borg, Påvel G. Lindberg

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