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Measuring levels of muscle fatigue in spastic cerebral palsy

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passive extension of the wrist with extended fingers, and at about 7 years of age by assessment of supination and shoulder and elbow flexion. In these children the contrac-ture formation progressed throughout childhood and adolescence. Children who were classified as having no voluntary means of ambulating (GMFCS level V) and children with no manual ability except perhaps the ability to push a big button (MACS level V) were at much higher risk of developing contractures compared to those at other MACS and GMFCS levels.

Contracture formation has traditionally been attributed to spasticity; the more spastic the child is, the higher the risk for contractures. Moreover, this clinical point of view is supported by a population-based study on how spasticity of the calf muscles is related to the passive range of motion. But spasticity cannot be the only factor of impor-tance as children with no increased muscle tone also devel-oped contractures and it is clinically difficult to distinguish spasticity from short and stiff muscles.2

Disuse has also been suggested to promote contracture development, as children with severe CP (MACS level V and GMFCS level V) rarely move their limbs, proposing an analogous contracture effect as when casting a frac-ture. But, surprisingly, a higher proportion of children

with dystonic CP were found to have contractures com-pared to bilateral or unilateral spastic CP, indicating that involuntary alternating flexing and extending joint movements does not protect the muscles as previously thought.

One could postulate that contracture formation is more of a parallel phenomenon to spasticity and disuse, and not simply a result of it. Biopsies of the biceps brachii muscle collected from children with fixed contractures have shown an increased amount of extracellular matrix around muscle fiber bundles that may increase stiffness. There are also fewer satellite cells and a reduced ribosomal RNA synthe-sis, both leading to diminished growth of the muscle.3 Fur-thermore, ultrasound investigation of the gastrosoleus muscle has shown that CP hampers muscle growth as early as 15 months of age, long before spasticity peaks at the age of 4 years and contractures have not yet developed.4,5 There are thus many factors influencing passive range of motion of the joints in CP.

Hopefully, children with CP who are prone to contrac-tures can be identified early by clinical examination or, for example, ultrasound imaging of muscle size and myopathic changes. Preventive measures could then be individually tailored and prescribed to suit each individual child.

REFERENCES

1. Hedberg-Graff J, Granstr€om F, Arner M, Krumlinde-Sundholm L. Upper-limb contracture development in children with cerebral palsy: a population-based study. Dev Med Child Neurol 2019;61: 204–11.

2. H€agglund G, Wagner P. Spasticity of the gastrosoleus muscle is related to the development of reduced passive dorsiflexion of the ankle in children with cerebral palsy: a

registry analysis of 2,796 examinations in 355 children. Acta Orthop 2011;82: 744–8.

3. Von Walden F, Gantelius S, Liu C, et al. Muscle con-tractures in patients with cerebral palsy and acquired brain injury are associated with extracellular matrix expansion, pro-inflammatory gene expression, and reduced rRNA synthesis. Muscle Nerve 2018;58: 277–85.

4. Herskind A, Ritterband-Rosenbaum A, Willerslev-Olsen M, et al. Muscle growth is reduced in 15-month-old chil-dren with cerebral palsy. Dev Med Child Neurol 2016;58: 485–91.

5. H€agglund G, Wagner P. Development of spasticity with age in a total population of children with cerebral palsy. BMC Musculoskelet Disord 2008;9: 150.

Measuring levels of muscle fatigue in spastic cerebral palsy

SEBASTIEN RATEL

|

ERIC DORE

|

PASCALE DUCHE

Laboratoire des Adaptations Metaboliques a l’Exercice en conditions Physiologiques et Pathologiques (EA 3533, AME2P), Clermont-Auvergne University, Clermont-Ferrand, France.

doi: 10.1111/dmcn.14046

This commentary is on the original article by Eken et al. on pages 212– 218 of this issue.

Eken et al.1 provide ample evidence that children with spastic cerebral palsy (CP) fatigue more during walking at a self-selected speed than typically developing peers. This finding was attributed to the greater fatigability of calf muscles in children with CP, as evidenced by the larger increase in electromyographic (EMG) activity of the

gastrocnemius medialis and soleus muscles. In contrast, no difference in EMG activity of thigh muscles (rectus femoris and semitendinosus) was observed between both groups. While the topic is very appropriate and highly worthwhile, the paper is lacking in some important aspects of fatigue which we would like to shed light on.

One first point of consideration is that individuals with CP have large amounts of coactivation/cocontraction of agonist and antagonist muscles around the same joint, which could increase energy expenditure and as a result lead to a faster/higher rate of muscle fatigue. In that respect, Unnithan et al.2showed in children with CP that thigh and calf muscle coactivation rates accounted for 51.4% and 42.8% respectively of the variability in oxygen uptake at a speed of 3km/h. Another major point is that

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children with CP could have longer periods of muscle acti-vation than non-disabled peers.3These longer muscle phasic activities during each cycle may also contribute to increase the energy cost of walking and thus the fatigability in individuals with CP. In addition, children diagnosed with spastic CP could exhibit a tissue- (coactivation) related ankle hyperresistance leading to a reduced passive ankle dorsiflex-ion during the stance phase of gait.4 Such phenomenon

could contribute toward abnormal locomotion, wasted mechanical energy, and thus high levels of fatigue.

No information on the physical activity level of children with CP was provided in the study by Eken et al.1 Yet,

such information is required since those with high biome-chanical walking economy were found to be more physi-cally active and less fatigable.5In our opinion, the level of habitual physical activity should be systematically quanti-fied using objective or subjective methods such as accelerometry, diary, or questionnaires to compare children with CP to non-disabled peers more equitably. Further research is needed to determine whether exercise programs used to improve walking economy increase the level of physical activity and whether any improvement in habitual physical activity translates into a reduced energy cost of gait and lower levels of fatigue in CP.

REFERENCES

1. Eken MM, Brændvik SM, Bardal EM, et al. Lower limb muscle fatigue during walking in children with cerebral palsy. Dev Med Child Neurol 2019;61: 212–8. 2. Unnithan VB, Dowling JJ, Frost G, Bar-Or O. Role of

cocontraction in the O2 cost of walking in children

with cerebral palsy. Med Sci Sports Exerc 1996; 28: 1498–504.

3. Unnithan VB, Dowling JJ, Frost G, Volpe Ayub B, Bar-Or O. Cocontraction and phasic activity during GAIT in children with cerebral palsy. Electromyogr Clin Neurophysiol 1996;36: 487–94.

4. Martın Lorenzo T, Rocon E, Martınez Caballero I, Ramırez Barragan A, Lerma Lara S. Prolonged stretching of the ankle plantarflexors elicits muscle-tendon

adapta-tions relevant to ankle gait kinetics in children with spas-tic cerebral palsy. Med Hypotheses 2017;109: 65–9. 5. Maltais DB, Pierrynowski MR, Galea VA, Matsuzaka A,

Bar-Or O. Habitual physical activity levels are associ-ated with biomechanical walking economy in children with cerebral palsy. Am J Phys Med Rehabil 2005;84: 36–45.

Effect of ankle–foot orthoses on motor performance in cerebral

palsy

MARC DEGELAEN

Physiotherapy, Free University Brussels, Brussels, Belgium. doi: 10.1111/dmcn.14069

This commentary is on the original article by Ries and Schwartz on pages 219–225 of this issue.

People with cerebral palsy (CP) show a great variety in their clinical needs. A wide array of treatment modalities is therefore necessary to address these needs, and this includes optimizing any individual’s motor function. Clinical out-comes can also be very varied. Assessment of what we do and how we achieve our goals is part and parcel of manage-ment. Attempting to establish treatment efficacy of ankle– foot orthosis for a very inclusive population of children with CP without taking sound account of the heterogeneity of the condition may be misleading. It would also be decep-tive to generalize findings to a wider population based on highly selected groups. Ankle–foot orthosis is one among many options and should always be only a part of a com-prehensive management plan. Establishing the efficacy of one type of orthotic device in different children (e.g. with bilateral spastic CP) is very challenging indeed. Moreover, there are different types of orthoses. The effects of wearing ankle–foot orthoses go well beyond providing more stability at the ankle joint. Orthoses also influence trunk motion and

alter body segment coordination.1,2 Reorganization of

movement and posture including adaptation and compensa-tions depends on every individual’s potential and needs. For example, individuals presenting with crouch gait may show different motor performance and capabilities owing to the severity of spasticity and lack of mobility.3

Ries et al.4 provide important results with respect to average change in minimum knee flexion during stance in groups of children with bilateral spastic CP who wear either solid ankle–foot orthoses (SAFO) or ground reaction ankle–foot orthoses (GRAFO) as part of their prescribed management. SAFO are designed to control dynamic equi-nus and the subtalar joint. They have been traditionally used with a view to decrease equinus and prevent ankle plantar flexor contractures. GRAFO are constructed to minimize knee flexion during the stance phase thanks to the ground reaction force. They were developed for chil-dren with bilateral spastic CP who walk with excessive knee flexion and ankle dorsiflexion during the stance phase (crouch gait). GRAFO need to be adjusted individually to control the position of the ground reaction force vector in relation to the knee joint. Ries et al. show that both SAFO and GRAFO can improve crouch gait without any clear difference in average change in minimum knee flexion dur-ing stance. They also demonstrate the importance of a

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