Relationship of spasticity to knee angular velocity and motion during gait in cerebral palsy

Abstract

This study investigated the effects of spasticity in the hamstrings and quadriceps muscles on gait parameters including temporal spatial measures, knee position, excursion and angular velocity in 25 children with spastic diplegic cerebral palsy (CP) as compared to 17 age-matched peers. While subjects were instructed to relax, an isokinetic device alternately flexed and extended the left knee at one of the three constant velocities 30°/s, 60°/s and 120°/s, while surface electromyography (EMG) electrodes over the biceps femoris and the rectus femoris recorded muscle activity. Patients then participated in 3D gait analysis at a self-selected speed. Results showed that, those with CP who exhibited heightened stretch responses (spasticity) in both muscles, had significantly slower knee angular velocities during the swing phase of gait as compared to those with and without CP who did not exhibit stretch responses at the joint and the tested speeds. The measured amount (torque) of the resistance to passive flexion or extension was not related to gait parameters in subjects with CP; however, the rate of change in resistance torque per unit angle change (stiffness) at the fastest test speed of 120°/s showed weak to moderate relationships with knee angular velocity and motion during gait. For the subset of seven patients with CP who subsequently underwent a selective dorsal rhizotomy, knee angular extension and flexion velocity increased post-operatively, suggesting some degree of causality between spasticity and movement speed.

Introduction

Due to the multi-dimensional nature of the motor disorder in spastic cerebral palsy (CP), several factors interact to produce gait limitations in these patients. Motor coordination during walking and other motor tasks may be compromised by ‘negative’ features, such as restrictions in muscle length, reduced strength, poor selective control and by the ‘positive’ sign of spasticity. Patients with spastic CP, by definition, have increased velocity-dependent resistance to passive stretch, presumed to interfere with active motion. Spasticity may be focal (a single or only a few joints) or generalized (multiple joints). It has been proposed that children with CP are constrained in movement speed by spasticity, in that they ‘avoid’ or are prevented from achieving faster velocities so as not to elicit a stretch response [1]. While spasticity, when present, clearly interferes with passive muscle stretch in the relaxed state, the precise role of spasticity in disrupting voluntary or active motion remains a topic of considerable debate and clinical importance.

A stretch response is a normal protective mechanism that occurs when a resting muscle is lengthened rapidly or forcefully. A person is considered to have ‘spasticity’, when the threshold for this response is lowered and can be elicited much more readily, even on passive examination. The force and speed of a manual evaluation, such as performed when administering the Ashworth test for grading spasticity, typically underestimates those conditions which would likely produce stretch responses in persons with intact neuromotor systems. On the other hand, instrumented systems, which can accelerate quickly and can safely move the joint at more rapid speeds are able to detect stretch responses in persons both with and without spasticity. The former group is often distinguishable by the slow speeds at which these responses have been shown to occur [2].

For decades, spasticity was considered to be the primary culprit in producing the motor deficit in cerebral palsy. While scientific evidence has failed to confirm this strong presumed link and suggests that spasticity has a more modest or perhaps even negligible effect on motor function [3], interventions aimed at alleviating spasticity such as selective dorsal rhizotomy, intra-thecal baclofen pump implantation and botulinum toxin injections, are still frequently prescribed. Conflicting reports on the role of spasticity during active movement have been noted in the literature for decades and no consensus or resolution has yet been reached.

Similar to the goals of this study, Norton et al. [4] specifically examined the relationship between spasticity at the knee and gait speed in 15 adults with hemiplegia, 10 in whom the deficiency was due to a cerebrovascular accident and five, who had sustained a head injury. Their measure of spasticity was the area under the smoothed and rectified electromyography (EMG) curve of the antagonist muscle during passive knee flexion and extension in a sinusoidal (changing velocity) and ramp (constant velocity) condition and they correlated these values with the fastest voluntary walking speed of the patients. None of the correlation values reached significance, although the authors felt that a trend was evident between flexor muscle spasticity and gait speed that might have reached significance with a greater number of patients with more homogeneous disorders. Sahrmann and Norton [3] in a later study relating spasticity in the elbow musculature to rapid alternating movements find more conclusively that spasticity was related to movement speed in the upper extremity. In this study, a relationship was only found between elbow flexor, but not extensor, spasticity and the speed of movement. Ada and co-workers [5] compared the magnitude of stretch responses at the ankle during passive (patient relaxed) and active (patient attempting movement) conditions in patients with strokes compared to neurologically normal controls. They found that two-thirds of the patient group had heightened stretch responses during passive lengthening with none of the controls showing stretch responses. The patient group did not show higher levels of antagonistic resistance than controls during the active condition, leading these authors to conclude that spasticity has little to do with impairing muscle activation during gait.

Crenna [6] proposed that the potential effect of spasticity on active motion was dependent on the type of movement being performed, irrespective of its velocity. In studies on CP gait, he noted that abnormal stretch responses were more easily elicited during lengthening contractions around the time of ground contact than at other points in the cycle, and he hypothesized that this may occur because floor contact is a critical event that may be more dependent on supraspinal rather than peripheral control. He further suggested that disruptions in movement in other parts of the cycle may be attributable to weakness, co-contraction or passive muscle properties, rather than to heightened stretch responses.

Knutsson and co-workers [7] agreed spasticity could impair voluntary movement if the spastic muscle was lengthening. They showed clear differences in the amount and velocity-dependence of restraint from a spastic antagonist during concentric action of the agonist versus eccentric action of that same agonist, when the spastic antagonist was shortening. They also pointed out that the ability of the agonist to produce force, independent of antagonist restraint, was concurrently disrupted in patients with spasticity, and that both impairments worsened with increasing the velocity. Similar findings of relatively greater concentric compared to eccentric weakness and greater antagonist resistance at faster test velocities have been reported in CP [8]. Sinkjaer [9] proposed that movement is disrupted in patients with ankle spasticity in part, because they lack modulation of reflexes during gait as seen in healthy controls. He further noted that passive stiffness is increased in these same patients, also contributing to the motor deficit.

While some of these findings seem to indicate that treatment of spasticity is unwarranted or would be only marginally effective if the goal of the intervention is to improve movement, others suggest the possibility that therapeutic intervention aimed at reducing spasticity and/or an increasing muscle strength may improve the ability to perform movements, particularly at faster speeds. However, many of these specific causal relationships have not been verified.

Patients with cerebral palsy have reduced gait velocity at free and fast speeds that is in proportion to their level of neurological involvement [10], [11]. Stride lengths are restricted and cadence is often increased. Angular velocity at the hip, knee and ankle, normalized by stride time to remove the effects of cadence, has been shown to be reduced in a group of patients with CP compared to normal [12]. Kinematic parameters also differ in these patients and for reasons beyond diminished velocity alone. Specifically at the knee joint, two kinematic patterns have been identified in this population, which have been presumed to be directly related to spastic responses in the hamstrings and quadriceps muscle groups. The first is ‘crouch’ gait which is characterized by excessive knee flexion at initial contact and during mid-stance when the knee typically reaches its maximum extension during the gait cycle. Inability to fully extend the knee disrupts the normal plantar-flexion knee extension couple and necessitates increased muscular effort to sustain this posture. Muscle tightness, compromised ambulatory ability with age and growth and long term joint deterioration may also ensue if this pattern persists. A second prevalent pattern is ‘stiff-knee’ gait in which total knee excursion is limited, particularly peak knee flexion during swing. In contrast to crouch, the functional implications of this pattern are primarily seen in swing with a disruption of foot clearance that can affect the smoothness and stability of the gait pattern. The etiologies of these knee patterns remain incompletely understood despite multiple hypotheses. Strengthening programs targeting these and other muscles can lead to significant improvements in temporal spatial and kinematic parameters in these patients, inferring some degree of causality [13]. Restricted muscle length at the knee and adjacent joints has also been shown to produce or exacerbate these and other kinematic abnormalities [14].

The primary purpose of this investigation was to examine the relationship of heightened stretch responses (spasticity) in the quadriceps and hamstrings muscles as detected during passive motion, to gait parameters including knee angular velocity, which reaches its maximum values during swing, and knee position and excursion throughout the gait cycle. Using an instrumented measure in combination with electromyography that can more precisely identify the presence and magnitude of stretch responses, we sub-grouped the children with CP and hypothesized that the group of children with stretch responses at relatively slow velocities would show differences in gait from children with CP who did not exhibit stretch responses at these velocities. All children with CP were expected to show differences from age-matched peers, but these were projected to be more pronounced in the ‘spastic’ sub-groups. More specifically we proposed that (1) peak knee extension velocity would be slowest in swing for those with hamstrings stretch responses and peak knee flexion velocity in swing would be least in those with quadriceps stretch responses, (2) hamstring spasticity would specifically limit stride length and knee extension, and (3) quadriceps spasticity would specifically limit total excursion and maximum flexion achieved in gait.

Causal relationships were explored in a limited subset of these patients who subsequently underwent selective dorsal rhizotomy to provide greater insights on the specific effects of reducing spasticity on gait. Selective dorsal rhizotomy has been shown to predictably reduce spasticity without a measurable effect on muscle strength [15] or isolated motor control [16] in the short term. Therefore, this intervention provides an opportunity to evaluate the causal effects of spasticity on movement speed with the hypothesis that knee joint angular velocity would increase after SDR.