Katherine M. Steele

Muscle contributions to support and progression during single-limb stance in crouch gait

Pathological movement patterns like crouch gait are characterized by abnormal kinematics and muscle activations that alter how muscles support the body weight during walking. Individual muscles are often the target of interventions to improve crouch gait, yet the roles of individual muscles during crouch gait remain unknown. The goal of this study was to examine how muscles contribute to mass center accelerations and joint angular accelerations during single-limb stance in crouch gait, and compare these contributions to unimpaired gait. Subject-specific dynamic simulations were created for ten children who walked in a mild crouch gait and had no previous surgeries. The simulations were analyzed to determine the acceleration of the mass center and angular accelerations of the hip, knee, and ankle generated by individual muscles. The results of this analysis indicate that children walking in crouch gait have less passive skeletal support of body weight and utilize substantially higher muscle forces to walk than unimpaired individuals. Crouch gait relies on the same muscles as unimpaired gait to accelerate the mass center upward, including the soleus, vasti, gastrocnemius, gluteus medius, rectus femoris, and gluteus maximus. However, during crouch gait, these muscles are active throughout single-limb stance, in contrast to the modulation of muscle forces seen during single-limb stance in an unimpaired gait. Subjects walking in crouch gait rely more on proximal muscles, including the gluteus medius and hamstrings, to accelerate the mass center forward during single-limb stance than subjects with an unimpaired gait.

Compressive Tibiofemoral Force during Crouch Gait

Crouch gait, a common walking pattern in individuals with cerebral palsy, is characterized by excessive flexion of the hip and knee. Many subjects with crouch gait experience knee pain, perhaps because of elevated muscle forces and joint loading. The goal of this study was to examine how muscle forces and compressive tibiofemoral force change with the increasing knee flexion associated with crouch gait. Muscle forces and tibiofemoral force were estimated for three unimpaired children and nine children with cerebral palsy who walked with varying degrees of knee flexion. We scaled a generic musculoskeletal model to each subject and used the model to estimate muscle forces and compressive tibiofemoral forces during walking. Mild crouch gait (minimum knee flexion 20-35°) produced a peak compressive tibiofemoral force similar to unimpaired walking; however, severe crouch gait (minimum knee flexion>50°) increased the peak force to greater than 6 times body-weight, more than double the load experienced during unimpaired gait. This increase in compressive tibiofemoral force was primarily due to increases in quadriceps force during crouch gait, which increased quadratically with average stance phase knee flexion (i.e., crouch severity). Increased quadriceps force contributes to larger tibiofemoral and patellofemoral loading which may contribute to knee pain in individuals with crouch gait.

Can strength training predictably improve gait kinematics? A pilot study on the effects of hip and knee extensor strengthening on lower-extremity alignment in cerebral palsy.

Background Computer simulations have demonstrated that excessive hip and knee flexion during gait, as frequently seen in ambulatory children with cerebral palsy (CP), can reduce the ability of muscles to provide antigravity support and increase the tendency of hip muscles to internally rotate the thigh. These findings suggest that therapies for improving upright posture during gait also may reduce excessive internal rotation. Objective The goal of this study was to determine whether strength training can diminish the degree of crouched, internally rotated gait in children with spastic diplegic CP. Design This was a pilot prospective clinical trial. Methods Eight children with CP participated in an 8-week progressive resistance exercise program, with 3-dimensional gait analysis and isokinetic testing performed before and after the program. Secondary measures included passive range of motion, the Ashworth Scale, and the PedsQL CP Module. To identify factors that may have influenced outcome, individual and subgroup data were examined for patterns of change within and across variables. Results Strength (force-generating capacity) increased significantly in the left hip extensors, with smaller, nonsignificant mean increases in the other 3 extensor muscle groups, yet kinematic and functional outcomes were inconsistent. The first reported subject-specific computer simulations of crouch gait were created for one child who showed substantial benefit to examine the factors that may have contributed to this outcome. Limitations The sample was small, with wide variability in outcomes. Conclusions Strength training may improve walking function and alignment in some patients for whom weakness is a major contributor to their gait deficits. However, in other patients, it may produce no change or even undesired outcomes. Given the variability of outcomes in this and other strengthening studies in CP, analytical approaches to determine the sources of variability are needed to better identify those individuals who are most likely to benefit from strengthening.

The number and choice of muscles impact the results of muscle synergy analyses

One theory for how humans control movement is that muscles are activated in weighted groups or synergies. Studies have shown that electromyography (EMG) from a variety of tasks can be described by a low-dimensional space thought to reflect synergies. These studies use algorithms, such as nonnegative matrix factorization, to identify synergies from EMG. Due to experimental constraints, EMG can rarely be taken from all muscles involved in a task. However, it is unclear if the choice of muscles included in the analysis impacts estimated synergies. The aim of our study was to evaluate the impact of the number and choice of muscles on synergy analyses. We used a musculoskeletal model to calculate muscle activations required to perform an isometric upper-extremity task. Synergies calculated from the activations from the musculoskeletal model were similar to a prior experimental study. To evaluate the impact of the number of muscles included in the analysis, we randomly selected subsets of between 5 and 29 muscles and compared the similarity of the synergies calculated from each subset to a master set of synergies calculated from all muscles. We determined that the structure of synergies is dependent upon the number and choice of muscles included in the analysis. When five muscles were included in the analysis, the similarity of the synergies to the master set was only 0.57 ± 0.54; however, the similarity improved to over 0.8 with more than ten muscles. We identified two methods, selecting dominant muscles from the master set or selecting muscles with the largest maximum isometric force, which significantly improved similarity to the master set and can help guide future experimental design. Analyses that included a small subset of muscles also over-estimated the variance accounted for (VAF) by the synergies compared to an analysis with all muscles. Thus, researchers should use caution using VAF to evaluate synergies when EMG is measured from a small subset of muscles.

Muscle synergies and complexity of neuromuscular control during gait in cerebral palsy

Individuals with cerebral palsy (CP) have impaired movement due to a brain injury near birth. Understanding how neuromuscular control is altered in CP can provide insight into pathological movement. We sought to determine if individuals with CP demonstrate reduced complexity of neuromuscular control during gait compared with unimpaired individuals and if changes in control are related to functional ability.

How much muscle strength is required to walk in a crouch gait

Muscle weakness is commonly cited as a cause of crouch gait in individuals with cerebral palsy; however, outcomes after strength training are variable and mechanisms by which muscle weakness may contribute to crouch gait are unclear. Understanding how much muscle strength is required to walk in a crouch gait compared to an unimpaired gait may provide insight into how muscle weakness contributes to crouch gait and assist in the design of strength training programs. The goal of this study was to examine how much muscle groups could be weakened before crouch gait becomes impossible. To investigate this question, we first created muscle-driven simulations of gait for three typically developing children and six children with cerebral palsy who walked with varying degrees of crouch severity. We then simulated muscle weakness by systematically reducing the maximum isometric force of each muscle group until the simulation could no longer reproduce each subjects gait. This analysis indicated that moderate crouch gait required significantly more knee extensor strength than unimpaired gait. In contrast, moderate crouch gait required significantly less hip abductor strength than unimpaired gait, and mild crouch gait required significantly less ankle plantarflexor strength than unimpaired gait. The reduced strength required from the hip abductors and ankle plantarflexors during crouch gait suggests that weakness of these muscle groups may contribute to crouch gait and that these muscle groups are potential targets for strength training.

Muscle contributions to vertical and fore-aft accelerations are altered in subjects with crouch gait

The goals of this study were to determine if the muscle contributions to vertical and fore-aft acceleration of the mass center differ between crouch gait and unimpaired gait and if these muscle contributions change with crouch severity. Examining muscle contributions to mass center acceleration provides insight into the roles of individual muscles during gait and can provide guidance for treatment planning. We calculated vertical and fore-aft accelerations using musculoskeletal simulations of typically developing children and children with cerebral palsy and crouch gait. Analysis of these simulations revealed that during unimpaired gait the quadriceps produce large upward and backward accelerations during early stance, whereas the ankle plantarflexors produce large upward and forward accelerations later in stance. In contrast, during crouch gait, the quadriceps and ankle plantarflexors produce large, opposing fore-aft accelerations throughout stance. The quadriceps force required to accelerate the mass center upward was significantly larger in crouch gait than in unimpaired gait and increased with crouch severity. The gluteus medius accelerated the mass center upward during midstance in unimpaired gait; however, during crouch gait the upward acceleration produced by the gluteus medius was significantly reduced. During unimpaired gait the quadriceps and ankle plantarflexors accelerate the mass center at different times, efficiently modulating fore-aft accelerations. However, during crouch gait, the quadriceps and ankle plantarflexors produce fore-aft accelerations at the same time and the opposing fore-aft accelerations generated by these muscles contribute to the inefficiency of crouch gait.

Consequences of biomechanically constrained tasks in the design and interpretation of synergy analyses

Matrix factorization algorithms are commonly used to analyze muscle activity and provide insight into neuromuscular control. These algorithms identify low-dimensional subspaces, commonly referred to as synergies, which can describe variation in muscle activity during a task. Synergies are often interpreted as reflecting underlying neural control; however, it is unclear how these analyses are influenced by biomechanical and task constraints, which can also lead to low-dimensional patterns of muscle activation. The aim of this study was to evaluate whether commonly used algorithms and experimental methods can accurately identify synergy-based control strategies. This was accomplished by evaluating synergies from five common matrix factorization algorithms using muscle activations calculated from 1) a biomechanically constrained task using a musculoskeletal model and 2) without task constraints using random synergy activations. Algorithm performance was assessed by calculating the similarity between estimated synergies and those imposed during the simulations; similarities ranged from 0 (random chance) to 1 (perfect similarity). Although some of the algorithms could accurately estimate specified synergies without biomechanical or task constraints (similarity >0.7), with these constraints the similarity of estimated synergies decreased significantly (0.3-0.4). The ability of these algorithms to accurately identify synergies was negatively impacted by correlation of synergy activations, which are increased when substantial biomechanical or task constraints are present. Increased variability in synergy activations, which can be captured using robust experimental paradigms that include natural variability in motor activation patterns, improved identification accuracy but did not completely overcome effects of biomechanical and task constraints. These results demonstrate that a biomechanically constrained task can reduce the accuracy of estimated synergies and highlight the importance of using experimental protocols with physiological variability to improve synergy analyses.

Use of shear wave ultrasound elastography to quantify muscle properties in cerebral palsy.

BACKGROUND Individuals with cerebral palsy tend to have altered muscle architecture and composition, but little is known about the muscle material properties, specifically stiffness. Shear wave ultrasound elastography allows shear wave speed, which is related to stiffness, to be measured in vivo in individual muscles. Our aim was to evaluate the material properties, specifically stiffness, as measured by shear wave speed of the medial gastrocnemius and tibialis anterior muscles in children with hemiplegic cerebral palsy across a range of ankle torques and positions, and fascicle strains. METHOD Shear wave speed was measured bilaterally in the medial gastrocnemius and tibialis anterior over a range of ankle positions and torques using shear wave ultrasound elastography in eight individuals with hemiplegic cerebral palsy. B-mode ultrasound was used to measure muscle thickness and fascicle strain. RESULTS Shear waves traveled faster in the medial gastrocnemius and tibialis anterior of the more-affected limb by 14% (P=0.024) and 20% (P=0.03), respectively, when the ankle was at 90°. Shear wave speed in the medial gastrocnemius increased as the ankle moved from plantarflexion to dorsiflexion (less affected: r(2)=0.82, P<0.001; more-affected: r(2)=0.69, P<0.001) and as ankle torque increased (less affected: r(2)=0.56, P<0.001; more-affected: r(2)=0.45, P<0.001). In addition, shear wave speed was strongly correlated with fascicle strain (less affected: r(2)=0.63, P<0.001; more-affected: r(2)=0.53, P<0.001). INTERPRETATION The higher shear wave speed in the more-affected limb of individuals with cerebral palsy indicates greater muscle stiffness, and demonstrates the clinical potential of shear wave elastography as a non-invasive tool for investigating mechanisms of altered muscle properties and informing diagnosis and treatment.

Characteristics associated with improved knee extension after strength training for individuals with cerebral palsy and crouch gait

Muscle weakness may contribute to crouch gait in individuals with cerebral palsy, and some individuals participate in strength training programs to improve crouch gait. Unfortunately, improvements in muscle strength and gait are inconsistent after completing strength training programs. The purpose of this study was to examine changes in knee extensor strength and knee extension angle during walking after strength training in individuals with cerebral palsy who walk in crouch gait and to determine subject characteristics associated with these changes. A literature review was performed of studies published since January 2000 that included strength training, three-dimensional motion analysis, and knee extensor strength measurements for individuals with cerebral palsy. Three studies met these criteria and individual subject data was obtained from the authors for thirty crouch gait subjects. Univariate regression analyses were performed to determine which of ten physical examination and motor performance variables were associated with changes in strength and knee extension during gait. Change in knee extensor strength ranged from a 25% decrease to a 215% increase, and change in minimum knee flexion angle during gait ranged from an improvement of 9° more knee extension to 15° more knee flexion. Individuals without hamstring spasticity had greater improvement in knee extension after strength training. Hamstring spasticity was associated with an undesired increase in knee flexion during walking. Subject-specific factors such as hamstring spasticity may be useful for predicting which subjects will benefit from strength training to improve crouch gait.