Lynn Bar-On

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.

Spasticity and Its Contribution to Hypertonia in Cerebral Palsy

Spasticity is considered an important neural contributor to muscle hypertonia in children with cerebral palsy (CP). It is most often treated with antispasticity medication, such as Botulinum Toxin-A. However, treatment response is highly variable. Part of this variability may be due to the inability of clinical tests to differentiate between the neural (e.g., spasticity) and nonneural (e.g., soft tissue properties) contributions to hypertonia, leading to the terms “spasticity” and “hypertonia” often being used interchangeably. Recent advancements in instrumented spasticity assessments offer objective measurement methods for distinction and quantification of hypertonia components. These methods can be applied in clinical settings and their results used to fine-tune and improve treatment. We reviewed current advancements and new insights with respect to quantifying spasticity and its contribution to muscle hypertonia in children with CP. First, we revisit what is known about spasticity in children with CP, including the various definitions and its pathophysiology. Second, we summarize the state of the art on instrumented spasticity assessment in CP and review the parameters developed to quantify the neural and nonneural components of hypertonia. Lastly, the impact these quantitative parameters have on clinical decision-making is considered and recommendations for future clinical and research investigations are discussed.

Is an Instrumented Spasticity Assessment an Improvement Over Clinical Spasticity Scales in Assessing and Predicting the Response to Integrated Botulinum Toxin Type A Treatment in Children With Cerebral Palsy

OBJECTIVE To compare responsiveness and predictive ability of clinical and instrumented spasticity assessments after botulinum toxin type A (BTX) treatment combined with casting in the medial hamstrings (MEHs) in children with spastic cerebral palsy (CP). DESIGN Prospective cohort study. SETTING Hospital. PARTICIPANTS Consecutive sample of children (N=31; 40 MEH muscles) with CP requiring BTX injections. INTERVENTION Clinical and instrumented spasticity assessments before and on average ± SD 53±14 days after BTX. MAIN OUTCOME MEASURES Clinical spasticity scales included the Modified Ashworth Scale and the Modified Tardieu Scale. The instrumented spasticity assessment integrated biomechanical (position and torque) and electrophysiological (surface electromyography) signals during manually performed low- and high-velocity passive stretches of the MEHs. Signals were compared between both stretch velocities and were examined pre- and post-BTX. Responsiveness of clinical and instrumented assessments was compared by percentage exact agreement. Prediction ability was assessed with a logistic regression and the area under the receiver operating characteristic (ROC) curves of the baseline parameters of responders versus nonresponders. RESULTS Both clinical and instrumented parameters improved post-BTX (P≤.005); however, they showed a low percentage exact agreement. The baseline Modified Tardieu Scale was the only clinical scale predictive for response (area under the ROC curve=0.7). For the instrumented assessment, baseline values of root mean square (RMS) electromyography and torque were better predictors for a positive response (area under the ROC curve=.82). Baseline RMS electromyography remained an important predictor in the logistic regression. CONCLUSIONS The instrumented spasticity assessment showed higher responsiveness than the clinical scales. The amount of RMS electromyography is considered a promising parameter to predict treatment response.

The relation between spasticity and muscle behavior during the swing phase of gait in children with cerebral palsy

There is much debate about how spasticity contributes to the movement abnormalities seen in children with spastic cerebral palsy (CP). This study explored the relation between stretch reflex characteristics in passive muscles and markers of spasticity during gait. Twenty-four children with CP underwent 3D gait analysis at three walking velocity conditions (self-selected, faster and fastest). The gastrocnemius (GAS) and medial hamstrings (MEHs) were assessed at rest using an instrumented spasticity assessment that determined the stretch-reflex threshold, expressed in terms of muscle lengthening velocity. Muscle activation was quantified with root mean square electromyography (RMS-EMG) during passive muscle stretch and during the muscle lengthening periods in the swing phase of gait. Parameters from passive stretch were compared to those from gait analysis. In about half the children, GAS peak muscle lengthening velocity during the swing phase of gait did not exceed its stretch reflex threshold. In contrast, in the MEHs the threshold was always exceeded. In the GAS, stretch reflex thresholds were positively correlated to peak muscle lengthening velocity during the swing phase of gait at the faster (r = 0.46) and fastest (r = 0.54) walking conditions. In the MEHs, a similar relation was found, but only at the faster walking condition (r = 0.43). RMS-EMG during passive stretch showed moderate correlations to RMS-EMG during the swing phase of gait in the GAS (r = 0.46-0.56) and good correlations in the MEHs (r = 0.69-0.77) at all walking conditions. RMS-EMG during passive stretch showed no correlations to peak muscle lengthening velocity during gait. We conclude that a reduced stretch reflex threshold in the GAS and MEHs constrains peak muscle lengthening velocity during gait in children with CP. With increasing walking velocity, this constraint is more marked in the GAS, but not in the MEHs. Hyper-activation of stretch reflexes during passive stretch is related to muscle activation during the swing phase of gait, but has a limited contribution to reduced muscle lengthening velocity during swing. Larger studies are required to confirm these results, and to investigate the contribution of other impairments such as passive stiffness and weakness to reduced muscle lengthening velocity during the swing phase of gait.

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.

Manually controlled instrumented spasticity assessments: a systematic review of psychometric properties

The first aim of this study was to systematically review and critically assess manually controlled instrumented spasticity assessment methods that combine multidimensional signals. The second aim was to extract a set of quantified parameters that are psychometrically sound to assess spasticity in a clinical setting.

Repeatability of muscle synergies within and between days for typically developing children and children with cerebral palsy

Muscle synergies are typically calculated from electromyographic (EMG) signals using nonnegative matrix factorization. Synergies identify weighted groups of muscles that are commonly activated together during a task, such as walking. Synergy analysis has become an emerging tool to evaluate neuromuscular control; however, the repeatability of synergies between trials and days has not been evaluated. The goal of this study was to evaluate the repeatability of synergy complexity and structure in unimpaired individuals and individuals with cerebral palsy (CP). EMG data were collected from eight lower-limb muscles during gait for six typically developing (TD) children and five children with CP on two separate days, over three walking speeds. To evaluate synergy complexity, we calculated the total variance accounted for by one synergy (tVAF1). On a given day, the average range in tVAF1 between gait cycles was 18.2% for TD and 19.1% for CP. The average standard deviation in tVAF1 between gait cycles was 4.9% for TD and 5.0% for CP. Average tVAF1 calculated across gait cycles was not significantly different between days for TD or CP participants. Comparing synergy structure, the average (standard deviation) within day correlation coefficients of synergy weights for two or more synergies were 0.89 (0.15) for TD and 0.88 (0.15) for CP. Between days, the average correlation coefficient of synergy weights for two or more synergies was greater than 0.89 for TD and 0.74 for CP. These results demonstrate that synergy complexity and structure averaged over multiple gait cycles are repeatable between days in both TD and CP groups.

Muscle Activation Patterns When Passively Stretching Spastic Lower Limb Muscles of Children with Cerebral Palsy

The definition of spasticity as a velocity-dependent activation of the tonic stretch reflex during a stretch to a passive muscle is the most widely accepted. However, other mechanisms are also thought to contribute to pathological muscle activity and, in patients post-stroke and spinal cord injury can result in different activation patterns. In the lower-limbs of children with spastic cerebral palsy (CP) these distinct activation patterns have not yet been thoroughly explored. The aim of the study was to apply an instrumented assessment to quantify different muscle activation patterns in four lower-limb muscles of children with CP. Fifty-four children with CP were included (males/females n = 35/19; 10.8±3.8 yrs; bilateral/unilateral involvement n =  32/22; Gross Motor Functional Classification Score I–IV) of whom ten were retested to evaluate intra-rater reliability. With the subject relaxed, single-joint, sagittal-plane movements of the hip, knee, and ankle were performed to stretch the lower-limb muscles at three increasing velocities. Muscle activity and joint motion were synchronously recorded using inertial sensors and electromyography (EMG) from the adductors, medial hamstrings, rectus femoris, and gastrocnemius. Muscles were visually categorised into activation patterns using average, normalized root mean square EMG (RMS-EMG) compared across increasing position zones and velocities. Based on the visual categorisation, quantitative parameters were defined using stretch-reflex thresholds and normalized RMS-EMG. These parameters were compared between muscles with different activation patterns. All patterns were dominated by high velocity-dependent muscle activation, but in more than half, low velocity-dependent activation was also observed. Muscle activation patterns were found to be both muscle- and subject-specific (p<0.01). The intra-rater reliability of all quantitative parameters was moderate to good. Comparing RMS-EMG between incremental position zones during low velocity stretches was found to be the most sensitive in categorizing muscles into activation patterns (p<0.01). Future studies should investigate whether muscles with different patterns react differently to treatment.

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.

The Intra- and Inter-Rater Reliability of an Instrumented Spasticity Assessment in Children with Cerebral Palsy

Aim Despite the impact of spasticity, there is a lack of objective, clinically reliable and valid tools for its assessment. This study aims to evaluate the reliability of various performance- and spasticity-related parameters collected with a manually controlled instrumented spasticity assessment in four lower limb muscles in children with cerebral palsy (CP). Method The lateral gastrocnemius, medial hamstrings, rectus femoris and hip adductors of 12 children with spastic CP (12.8 years, ±4.13 years, bilateral/unilateral involvement n=7/5) were passively stretched in the sagittal plane at incremental velocities. Muscle activity, joint motion, and torque were synchronously recorded using electromyography, inertial sensors, and a force/torque load-cell. Reliability was assessed on three levels: (1) intra- and (2) inter-rater within session, and (3) intra-rater between session. Results Parameters were found to be reliable in all three analyses, with 90% containing intra-class correlation coefficients >0.6, and 70% of standard error of measurement values <20% of the mean values. The most reliable analysis was intra-rater within session, followed by intra-rater between session, and then inter-rater within session. The Adds evaluation had a slightly lower level of reliability than that of the other muscles. Conclusions Limited intrinsic/extrinsic errors were introduced by repeated stretch repetitions. The parameters were more reliable when the same rater, rather than different raters performed the evaluation. Standardisation and training should be further improved to reduce extrinsic error when different raters perform the measurement. Errors were also muscle specific, or related to the measurement set-up. They need to be accounted for, in particular when assessing pre-post interventions or longitudinal follow-up. The parameters of the instrumented spasticity assessment demonstrate a wide range of applications for both research and clinical environments in the quantification of spasticity.