Interaction Between Spasticity and the Initial Response After Balance Perturbations in Children With Spastic Cerebral Palsy

Background:

Spasticity is a common impairment following an upper motor neuron lesion, such as cerebral palsy (CP). Children with CP suffer a lot from balance impairments, which will impair their participation in daily life activities. When clinically assessing spasticity, a passive muscle is stretched and spasticity is scored based on the observed resistance against this stretch. Similar muscle stretches also occur when standing balance is perturbed, as for example when standing on a departing bus or walking on uneven terrain.

Maintaining balance involves complex sensorimotor transformations to activate the muscle to produce the required balance correcting response. Sensorimotor processing refers to how the nervous system translates incoming sensory information about body motion into motor commands to activate muscles. In both healthy animals and humans, sensorimotor processes underlying reactive standing balance can be explained by delayed feedback from CoM kinematics. The sensitivity to the CoM disturbance have been shown to be relatively constant within one subject, but change with age, age-related cognitive decline, sensory deficits, and neurological impairments.

Both kinematic and muscle responses to perturbations of standing balance are impaired in children with CP. Children with CP have a higher chance of losing their balance, change to a stepping strategy at lower perturbation levels, and have increased muscle (co-)activation. However, it is unknown whether the underlying sensorimotor transformations are altered in CP and how these changes contribute to the altered balance responses observed in CP. Therefore, the first aim was to understand alterations in sensorimotor processing underlying reactive standing balance control in children with spastic CP.

The increased muscle co-activation that is observed in CP might be a functional compensation strategy to improve balance control. For example, muscle co-activation will increase joint stiffness and therefore resisting movement of the body with respect to the feet during backward translational perturbations. In this case, co-activation will help to maintain balance. However, it is not clear whether children with CP use the increased co-activation as compensation strategy to improve balance control or whether the muscle co-activation is a consequence of impaired balance control. When standing balance is perturbed using rotational perturbations, muscle co-activation will hinder balance control. Increased muscle co-activation and the following increased joint stiffness will couple body movement to platform movement resulting in body tilt. Hence, increasing joint stiffness might not be beneficial during rotational perturbations. Our second aim was to investigate whether children with CP use increased muscle co-activation as a compensation strategy to improve balance control or whether muscle co-activation causes balance control impairments by combining translational and rotational perturbations of standing balance.

Muscle stretches occur during isolated joint rotations, as clinically applied when assessing joint hyper-resistance, and during perturbations of standing balance. Children with CP respond to both isolated joint rotations and perturbations of standing with increased excitation of the stretched muscle, combined with increased agonist-antagonist co-activation. Although the striking similarities between both reactive muscle responses to muscle stretches, little is known about the relation between joint hyper-resistance and reactive balance. Therefore our third aim was to explore the relation between muscle responses to instrumented tests of joint hyper-resistance and translational and rotational perturbations of standing balance.

Methods:

Twenty children with CP and twenty age-matched typically developing (TD) children participated in this study. Children with CP were diagnosed by a neuro-pediatrician and met the following inclusion criteria: (1)aged between 5 and 17 years old; (32) Gross Motor Classification Scale I-III; (3) able to stand independently for at least 10 minutes; (4) no orthopedic/neurological surgery in the previous year; and (5) no botulinum neurotoxin injections in the previous six months.

An instrumented spasticity assessment (hereafter called isolated joint rotations) using the method described by Bar-On and colleagues was performed. Participants lay supine and were asked to relax. The lower leg was supported by a customized frame that allowed ankle rotation. A researcher applied five times a passive rotation of the ankle joint, as fast as possible from a plantar flexed position to the end range of motion towards dorsiflexion.

Reactive balance was tested on a Caren platform. Participants stood barefoot on the platform and were secured with a safety harness. Instructions were to stand upright and maintain balance without stepping unless stepping was necessary to avoid failing. The protocol consisted of six increasingly difficult perturbations levels for the backward translations and four increasingly difficult perturbation levels for the toe-up rotational perturbations. Withing each level, eight perturbations were administered. When participants stepped I more than 3 trials within a level, the participant did not continue to the next level.

Trajectories of reflective skin markers were captured by infrared Vicon Cameras and activity of the lower leg muscles (lateral gastrocnemius, medial gastrocnemius, soleus and tibialis anterior) was measured simultaneously through surface electromyography.