European consensus on the concepts and measurement of the pathophysiological neuromuscular responses to passive muscle stretch.

BACKGROUND AND PURPOSE: To support clinical decision-making in central neurological disorders, a physical examination is used to assess responses to passive muscle stretch. However, what exactly is being assessed is expressed and interpreted in different ways. A clear diagnostic framework is lacking. Therefore, the aim was to arrive at unambiguous terminology about the concepts and measurement around pathophysiological neuromuscular response to passive muscle stretch. METHODS: During two consensus meetings, 37 experts from 12 European countries filled online questionnaires based on a Delphi approach, followed by plenary discussion after rounds. Consensus was reached for agreement ≥75%. RESULTS: The term hyper-resistance should be used to describe the phenomenon of impaired neuromuscular response during passive stretch, instead of for example 'spasticity' or 'hypertonia'. From there, it is essential to distinguish non-neural (tissue-related) from neural (central nervous system related) contributions to hyper-resistance. Tissue contributions are elasticity, viscosity and muscle shortening. Neural contributions are velocity dependent stretch hyperreflexia and non-velocity dependent involuntary background activation. The term 'spasticity' should only be used next to stretch hyperreflexia, and 'stiffness' next to passive tissue contributions. When joint angle, moment and electromyography are recorded, components of hyper-resistance within the framework can be quantitatively assessed. CONCLUSIONS: A conceptual framework of pathophysiological responses to passive muscle stretch is defined. This framework can be used in clinical assessment of hyper-resistance and will improve communication between clinicians. Components within the framework are defined by objective parameters from instrumented assessment. These parameters need experimental validation in order to develop treatment algorithms based on the aetiology of the clinical phenomena.

Identification of the neural component of torque during manually-applied spasticity assessments in children with cerebral palsy.

Clinical assessment of spasticity is compromised by the difficulty to distinguish neural from non-neural components of increased joint torque. Quantifying the contributions of each of these components is crucial to optimize the selection of anti-spasticity treatments such as botulinum toxin (BTX). The aim of this study was to compare different biomechanical parameters that quantify the neural contribution to ankle joint torque measured during manually-applied passive stretches to the gastrocsoleus in children with spastic cerebral palsy (CP). The gastrocsoleus of 53 children with CP (10.9 ± 3.7 y; females n = 14; bilateral/unilateral involvement n = 28/25; Gross Motor Functional Classification Score I-IV) and 10 age-matched typically developing (TD) children were assessed using a manually-applied, instrumented spasticity assessment. Joint angle characteristics, root mean square electromyography and joint torque were simultaneously recorded during passive stretches at increasing velocities. From the CP cohort, 10 muscles were re-assessed for between-session reliability and 19 muscles were re-assessed 6 weeks post-BTX. A parameter related to mechanical work, containing both neural and non-neural components, was compared to newly developed parameters that were based on the modeling of passive stiffness and viscosity. The difference between modeled and measured response provided a quantification of the neural component. Both types of parameters were reliable (ICC > 0.95) and distinguished TD from spastic muscles (p < 0.001). However, only the newly developed parameters significantly decreased post-BTX (p = 0.012). Identifying the neural and non-neural contributions to increased joint torque allows for the development of individually tailored tone management.

Instrumented assessment of the effect of Botulinum Toxin-A in the medial hamstrings in children with cerebral palsy.

This study examined the sensitivity of an instrumented spasticity assessment of the medial hamstrings (MEH) in children with cerebral palsy (CP). Nineteen children received Botulinum Toxin type A (BTX-A) injections in the MEH. Biomechanical (position and torque) and electrophysiological (surface electromyography, EMG) signals were integrated during manually-performed passive stretches of the MEH at low, medium and high velocity. Signals were examined at each velocity and between stretch velocities, and compared pre and post BTX-A (43 ± 16 days). Average change between pre and post BTX-A was interpreted in view of the minimal detectable change (MDC) calculated from previously published reliability results. Improvements greater than the MDC were found for nearly all EMG-parameters and for torque parameters at high velocity and at high versus low velocity (p<0.03), however large inter-subject variability was noted. Moderate correlations were found between the improvement in EMG and in torque (r=0.52, p<0.05). Biomechanical and electrophysiological parameters proved to be adequately sensitive to assess the response to treatment with BTX-A. Furthermore, studying both parameters at different velocities improves our understanding of spasticity and of the physiological effect of selective tone-reduction. This not only provides a clinical validation of the instrumented assessment, but also opens new avenues for further spasticity research.

A clinical measurement to quantify spasticity in children with cerebral palsy by integration of multidimensional signals.

Most clinical tools for measuring spasticity, such as the Modified Ashworth Scale (MAS) and the Modified Tardieu Scale (MTS), are not sufficiently accurate or reliable. This study investigated the clinimetric properties of an instrumented spasticity assessment. Twenty-eight children with spastic cerebral palsy (CP) and 10 typically developing (TD) children were included. Six of the children with CP were retested to evaluate reliability. To quantify spasticity in the gastrocnemius (GAS) and medial hamstrings (MEH), three synchronized signals were collected and integrated: surface electromyography (sEMG); joint-angle characteristics; and torque. Muscles were manually stretched at low velocity (LV) and high velocity (HV). Spasticity parameters were extracted from the change in sEMG and in torque between LV and HV. Reliability was determined with intraclass-correlation coefficients and the standard error of measurement; validity by assessing group differences and correlating spasticity parameters with the MAS and MTS. Reliability was moderately high for both muscles. Spasticity parameters in both muscles were higher in children with CP than in TD children, showed moderate correlation with the MAS for both muscles and good correlation to the MTS for the MEH. Spasticity assessment based on multidimensional signals therefore provides reliable and clinically relevant measures of spasticity. Moreover, the moderate correlations of the MAS and MTS with the objective parameters further stress the added value of the instrumented measurements to detect and investigate spasticity, especially for the GAS.

To what extent is mean EMG frequency during gait a reflection of functional muscle strength in children with cerebral palsy?

The aim of the current paper was to analyze the potential of the mean EMG frequency, recorded during 3D gait analysis (3DGA), for the evaluation of functional muscle strength in children with cerebral palsy (CP). As walking velocity is known to also influence EMG frequency, it was investigated to which extent the mean EMG frequency is a reflection of underlying muscle strength and/or the applied walking velocity. Surface EMG data of the lateral gastrocnemius (LGAS) and medial hamstrings (MEH) were collected during 3DGA. For each muscle, 20 CP children characterized by a weak and 20 characterized by a strong muscle (LGAS or MEH) were selected. A weak muscle was defined as a manual muscle testing score <3; a strong muscle was defined as a manual muscle testing score ≥4. Patient selection was based on the following inclusion criteria: (a) predominantly spastic type of CP (3-15 years old), (b) either (near) normal muscle strength or muscle weakness in at least one of the studied lower limb muscles, (c) no lower limb Botulinum Toxin-A treatment within 6 months prior to the 3DGA, (d) no history of lower limb surgery, and (e) high-quality noise-free EMG-data. For each muscle, twenty age-related typically developing (TD) children were included as controls. In both muscles a consistent pattern of increasing mean EMG frequency with decreasing muscle strength was observed. This was significant in the LGAS (TD versus weak CP). Walking velocity also had a significant effect on mean EMG frequency in the LGAS. Furthermore, based on R(2) and partial correlations, it could be concluded that both walking velocity and muscle strength have an impact on EMG, but the contribution of muscle strength was always higher. These findings underscore the potential of the mean EMG frequency recorded during 3DGA, for the evaluation of functional muscle strength in children with CP.