Surface electromyography normalization affects the interpretation of muscle activity and coactivation in children with cerebral palsy during walking

Investigating muscle activity and coactivation with surface electromyography (sEMG) gives insight into pathological muscle function during activities like walking in people with neuromuscular impairments, such as children with cerebral palsy (CP). There is large variation in the amount of coactivation reported during walking in children with CP, possibly due to the inconsistent handling of sEMG and in calculating the coactivation index. The aim of this study was to evaluate how different approaches of handling sEMG may affect the interpretation of muscle activity and coactivation, by looking at both absolute and normalized sEMG. Twenty-three ambulatory children with CP and 11 typically developing (TD) children participated. We conducted a three-dimensional gait analysis (3DGA) with concurrent sEMG measurements of tibialis anterior, soleus, gastrocnemius medialis, rectus femoris, and hamstring medialis. They walked barefoot at a self-selected, comfortable speed back and forth a 7-m walkway. The gait cycle extracted from the 3DGA was divided into six phases, and for each phase, root mean square sEMG amplitude was calculated (sEMG-RMS-abs), and also normalized to peak amplitude of the linear envelope (50-ms running RMS window) during the gait cycle (sEMG-RMS-norm). The coactivation index was calculated using sEMG-RMS-abs and sEMG-RMS-norm values and by using two different indices. Differences between TD children's legs and the affected legs of children with CP were tested with a mixed model. The between-subject muscle activity variability was more evenly distributed using sEMG-RMS-norm; however, potential physiological variability was eliminated as a result of normalization. Differences between groups in one gait phase using sEMG-RMS-abs showed opposite differences in another phase using sEMG-RMS-norm for three of the five muscles investigated. The CP group showed an increased coactivation index in two out of three muscle pairs using sEMG-RMS-abs and in all three muscle pairs using sEMG-RMS-norm. These results were independent of index calculation method. Moreover, the increased coactivation indices could be explained by either reduced agonist activity or increased antagonist activity. Thus, differences in muscle activity and coactivation index between the groups change after normalization. However, because we do not know the truth, we cannot conclude whether to normalize and recommend incorporating both

The Effect of Increased Gait Speed on Asymmetry and Variability in Children With Cerebral Palsy

Gait of children and adolescents with cerebral palsy (CP) is often reported to be more asymmetric and variable than gait of typically developing (TD) peers. As this may lead to less stable and less efficient gait, a relevant clinical question is how asymmetry may be improved and variability reduced in this population. The main objective of the current study was to investigate whether higher walking speed would affect gait symmetry and gait variability in children and adolescents with CP. Data from clinical gait analyses of 43 children and adolescents (29 males and 14 females) with unilateral (n = 28) or bilateral (n = 15) CP were included. Mean age was 11.3 ± 3.4 years, with level I (n = 26) or level II (n = 17) according to the Gross Motor Function Classification System (GMFCS). Corresponding data from 20 TD peers, matched in age and gender, were included as reference. Step time, step length, single support, and stance phase were studied at two different gait speeds: preferred and fast walking speed. Symmetry index and coefficient of variation were used as measures of asymmetry and variability, respectively. Results indicated that all participants managed to increase gait speed when instructed to do so. Overall, increased speed did not result in a more asymmetrical or variable gait, except for an increase in step length asymmetry and a difference in response between GMFCS levels I and II in variability. This implies that manipulation of gait speed may be useful clinically without necessarily making gait more unstable. However, some increase in step length asymmetry may be inevitable when gait speed is increased in people with CP

Ventilatory efficiency and aerobic capacity in people with multiple sclerosis: A randomized study

Objectives: To assess ventilatory efficiency and aerobic capacity in people with multiple sclerosis and whether treadmill walking or progressive strength training has an effect on these parameters in this population. Methods: In all, 24 adults with multiple sclerosis with an Expanded Disability Status Scale score of ≤6 completed a cardiopulmonary exercise test before and after 8 weeks of exercise. They were randomized to treadmill walking of low-to-moderate intensity (50%–70% of peak heart rate) or progressive strength training (six repetitions × two at 80% of one repetition maximum). Both groups exercised for 30 min three times per week. Primary outcome measure was ventilatory efficiency measured as the minute ventilation/carbon dioxide production (VE/VCO 2 ) ratio and oxygen uptake efficiency slope. Secondary outcome was aerobic capacity, measured as peak oxygen uptake (VO 2peak ). Results: Despite low aerobic capacity, ventilatory efficiency was found to be within normal range. After 8 weeks of exercise, no significant between-group differences emerged in (1) VE/VCO 2 ratio (26 ± 2.2 to 26 ± 2.0, 29 ± 2.0 to 28 ± 2.3, p  = 0.66), (2) oxygen uptake efficiency slope (2697 ± 442 to 2701 ± 577, 2473 ± 800 to 2481 ± 896, p  = 0.71), or (3) VO 2peak in mL/kg/min (28 ± 4.4 to 30 ± 4.3, 29 ± 6.7 to 29 ± 6.4, p  = 0.38) in treadmill walking and progressive strength training, respectively. There were no significant within-group differences either. No adverse events occurred during cardiopulmonary exercise test or exercise training. Conclusion: In people with mild-to-moderate multiple sclerosis, 8 weeks of treadmill walking of low-to-moderate intensity or progressive strength training did not have any effect on ventilatory efficiency or aerobic capacity. Although aerobic capacity was lower than reference values, ventilatory efficiency was not reduced

Energy cost of gait in children and the effect of speed, age, and body size

Background: Energy cost (EC) of comfortable walking is often used in clinical evaluation of children with altered gait function. EC is presented as energy expenditure per kg bodyweight per meter, either in total (grossEC) or in addition to resting energy expenditure (netEC). GrossEC is considered more reliable and netEC less affected by between-subject variations in speed, age, and body size. However, the effect of the individual child's speed on EC is rarely considered, while altered gait function may affect both speed and EC. Research question: To what extent are grossEC and netEC affected by within-subject variation in speed and between-subject variations in speed, age, and body size? Methods: Forty-two typically developing children (7–15 y) were included in this cross-sectional study. Age, height, and bodyweight were obtained. Breath-to-breath gas-exchange measures of VO2 and VCO2 were conducted during rest and five over-ground gait conditions: walking at slow, comfortable, and fast speed, jogging and running. All conditions lasted 3–5 min. Body surface area, non-dimensional speed, grossEC, and netEC were calculated. Regression analyses and mixed model analyses were conducted to explain the effect of speed, age, and body size on variations in EC. Results: GrossEC showed a non-significant, concave up relation to within-subject variation in speed, with a minimum around comfortable/fast walking speed. NetEC had a strong positive linear relation to within-subject variation in speed. For each gait condition, grossEC was more affected by between-subject variations in speed, age, and body size compared to netEC. However, the effect of age and body size was not eliminated for netEC but was quadratic. Significance: Although normalised to speed and bodyweight, grossEC and netEC are still affected by those factors. However, they are affected differently for within- and between-subject variations. This must be considered when interpreting EC in children in relation to gait function

Ventilatory efficiency and aerobic capacity in people with multiple sclerosis: A randomized study

Objectives: To assess ventilatory efficiency and aerobic capacity in people with multiple sclerosis and whether treadmill walking or progressive strength training has an effect on these parameters in this population. Methods: In all, 24 adults with multiple sclerosis with an Expanded Disability Status Scale score of ≤6 completed a cardiopulmonary exercise test before and after 8 weeks of exercise. They were randomized to treadmill walking of low-to-moderate intensity (50%–70% of peak heart rate) or progressive strength training (six repetitions × two at 80% of one repetition maximum). Both groups exercised for 30 min three times per week. Primary outcome measure was ventilatory efficiency measured as the minute ventilation/carbon dioxide production (VE/VCO2) ratio and oxygen uptake efficiency slope. Secondary outcome was aerobic capacity, measured as peak oxygen uptake (VO2peak). Results: Despite low aerobic capacity, ventilatory efficiency was found to be within normal range. After 8 weeks of exercise, no significant between-group differences emerged in (1) VE/VCO2 ratio (26 ± 2.2 to 26 ± 2.0, 29 ± 2.0 to 28 ± 2.3, p = 0.66), (2) oxygen uptake efficiency slope (2697 ± 442 to 2701 ± 577, 2473 ± 800 to 2481 ± 896, p = 0.71), or (3) VO2peak in mL/kg/min (28 ± 4.4 to 30 ± 4.3, 29 ± 6.7 to 29 ± 6.4, p = 0.38) in treadmill walking and progressive strength training, respectively. There were no significant within-group differences either. No adverse events occurred during cardiopulmonary exercise test or exercise training. Conclusion: In people with mild-to-moderate multiple sclerosis, 8 weeks of treadmill walking of low-to-moderate intensity or progressive strength training did not have any effect on ventilatory efficiency or aerobic capacity. Although aerobic capacity was lower than reference values, ventilatory efficiency was not reduced

Effectiveness of resistance training in combination with botulinum toxin-A on hand and arm use in children with cerebral palsy: a pre-post intervention study

Background The aim of this pilot study was to examine the effects of additional resistance training after use of Botulinum Toxin-A (BoNT-A) on the upper limbs in children with cerebral palsy (CP). Methods Ten children with CP (9–17 years) with unilaterally affected upper limbs according to Manual Ability Classification System II were assigned to two intervention groups. One group received BoNT-A treatment (group B), the other BoNT-A plus eight weeks resistance training (group BT). Hand and arm use were evaluated by means of the Melbourne assessment of unilateral upper limb function (Melbourne) and Assisting Hand Assessment (AHA). Measures of muscle strength, muscle tone, and active range of motion were used to assess neuromuscular body function. Measurements were performed before and two and five months after intervention start. Change scores and differences between the groups in such scores were subjected to Mann–Whitney U and Wilcoxon Signed Rank tests, respectively. Results Both groups had very small improvements in AHA and Melbourne two months after BoNT-A injections, without differences between groups. There were significant, or close to significant, short-term treatment effects in favour of group BT for muscle strength in injected muscles (elbow flexion strength, p = .08) and non-injected muscles (elbow extension and supination strength, both p = .05), without concomitant increases in muscle tone. Active supination range improved in both groups, but more so in group BT (p = .09). There were no differences between the groups five months after intervention start. Conclusions Resistance training strengthens non-injected muscles temporarily and may reduce short-term strength loss that results from BoNT-A injections without increasing muscle tone. Moreover, additional resistance training may increase active range of motion to a greater extent than BoNT-A alone. None of the improvements in neuromuscular impairments further augmented use of the hand and arm. Larger clinical trials are needed to establish whether resistance training can counteract strength loss caused by BoNT-A, whether the combination of BoNT-A and resistance training is superior to BoNT-A or resistance training alone in improving active range of motion, and whether increased task-related training is a more effective approach to improve hand and arm use in children with CP

Lower limb muscle fatigue during walking in children with cerebral palsy

Aim To investigate whether more prominent signs of muscle fatigue occur during self‐paced walking in children with cerebral palsy (CP) compared to typically developing peers. Method In this case–control study, 13 children with CP (four males, nine females; mean age [SD] 11y 4mo [3y 8mo]; nine in Gross Motor Function Classification System [GMFCS] level I, three in GMFCS level II, and one in GMFCS level III) and 14 typically developing peers (nine males, five females; mean age [SD] 9y 10mo [1y 10mo]) walked 5 minutes overground at a self‐selected walking speed. Electromyography (EMG) median frequency and root mean square (RMS) were identified per gait cycle from EMG recordings of the tibialis anterior, gastrocnemius medialis, soleus, rectus femoris, and semitendinosus. Rate of change in those variables was analysed using mixed linear model analyses. Results The decrease in EMG median frequency of gastrocnemius medialis and soleus and increase in EMG‐RMS of tibialis anterior, gastrocnemius medialis, and soleus were significantly larger in the most affected leg of children with CP compared with typically developing peers. Interpretation Increased selective muscle fatigue of the lower leg muscles was observed during self‐paced walking in children with mild‐to‐moderate severe CP. This could contribute to and account for limited walking capacity

The WE-Study: does botulinum toxin A make walking easier in children with cerebral palsy?: Study protocol for a randomized controlled trial

Background Intramuscular injections of botulinum toxin A (BoNT-A) have been a cornerstone in the treatment of spasticity for the last 20 years. In Norway, the treatment is now offered to two out of three children with spastic cerebral palsy (CP). However, despite its common use, the evidence for its functional effects is limited and inconclusive. The objective of this study is to determine whether BoNT-A makes walking easier in children with CP. We hypothesize that injections with BoNT-A in the calf muscles will reduce energy cost during walking, improve walking capacity, increase habitual physical activity, reduce pain and improve self-perceived performance and satisfaction. Methods/design This randomized, double-blinded, placebo-controlled, multicenter trial is conducted in a clinical setting involving three health regions in Norway. Ninety-six children with spastic CP, referred for single-level injections with BoNT-A in the calf muscles, will be invited to participate. Those who are enrolled will be randomized to receive either injections with BoNT-A (Botox®) or 0.9% saline in the calf muscles. Stratification according to age and study center will be made. The allocation ratio will be 1:1. Main inclusion criteria are (1) age 4 − 17.5 years, (2) Gross Motor Function Classification System levels I and II, (3) no BoNT-A injections in the lower limbs during the past 6 months and (4) no orthopedic surgery to the lower limbs during the past 2 years. The outcome measures will be made at baseline and 4, 12 (primary endpoint) and 24 weeks after injections. Primary outcome is change in energy cost during walking. Secondary outcomes are change in walking capacity, change in activity, perceived change in performance and satisfaction in mobility tasks, and pain. The primary analysis will use a linear mixed model to test for difference in change in the outcome measures between the groups. The study is approved by the Regional Ethical Committee and The Norwegian Medicines Agency. Recruitment started in September 2015. Discussion The evaluation of effect is comprehensive and includes objective standardized tests and measures on both impairment and activity level. Results are to be expected by spring 2019

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