Marije Goudriaan

Arm swing in human walking: What is their drive?

Although previous research has studied arm swing during walking, to date, it remains unclear what the contribution of passive dynamics versus active muscle control to arm swing is. In this study, we measured arm swing kinematics with 3D-motion analysis. We used a musculoskeletal model in OpenSim and generated dynamic simulations of walking with and without upper limb muscle excitations. We then compared arm swing amplitude and relative phase during both simulations to verify the extent to which passive dynamics contribute to arm swing. The results confirm that passive dynamics are partly responsible for arm swing during walking. However, without muscle activity, passive swing amplitude and relative phase decrease significantly (both p<0.05), the latter inducing a more in-phase swing pattern of the arms. Therefore, we conclude that muscle activity is needed to increase arm swing amplitude and modify relative phase during human walking to obtain an out-phase movement relative to the legs.

Repeatability of muscle synergies within and between days for typically developing children and children with cerebral palsy

Muscle synergies are typically calculated from electromyographic (EMG) signals using nonnegative matrix factorization. Synergies identify weighted groups of muscles that are commonly activated together during a task, such as walking. Synergy analysis has become an emerging tool to evaluate neuromuscular control; however, the repeatability of synergies between trials and days has not been evaluated. The goal of this study was to evaluate the repeatability of synergy complexity and structure in unimpaired individuals and individuals with cerebral palsy (CP). EMG data were collected from eight lower-limb muscles during gait for six typically developing (TD) children and five children with CP on two separate days, over three walking speeds. To evaluate synergy complexity, we calculated the total variance accounted for by one synergy (tVAF1). On a given day, the average range in tVAF1 between gait cycles was 18.2% for TD and 19.1% for CP. The average standard deviation in tVAF1 between gait cycles was 4.9% for TD and 5.0% for CP. Average tVAF1 calculated across gait cycles was not significantly different between days for TD or CP participants. Comparing synergy structure, the average (standard deviation) within day correlation coefficients of synergy weights for two or more synergies were 0.89 (0.15) for TD and 0.88 (0.15) for CP. Between days, the average correlation coefficient of synergy weights for two or more synergies was greater than 0.89 for TD and 0.74 for CP. These results demonstrate that synergy complexity and structure averaged over multiple gait cycles are repeatable between days in both TD and CP groups.

Children with Spastic Cerebral Palsy Experience Difficulties Adjusting Their Gait Pattern to Weight Added to the Waist, While Typically Developing Children Do Not

The prevalence of childhood overweight and obesity is increasing in the last decades, also in children with Cerebral Palsy (CP). Even though it has been established that an increase in weight can have important negative effects on gait in healthy adults and children, it has not been investigated what the effect is of an increase in body weight on the characteristics of gait in children with CP. In CP, pre and post three-dimensional gait analyses are performed to assess the effectiveness of an intervention. As a considerable amount of time can elapse between these measurements, and the effect of an alteration in the body weight is not taken into consideration, this effect of increased body weight is of specific importance. Thirty children with the predominantly spastic type of CP and 15 typically developing (TD) children were enrolled (age 3–15 years). All children underwent three-dimensional gait analysis with weight-free (baseline) and weighted (10% of the body weight added around their waist) trials. Numerous gait parameters showed a different response to the added weight for TD and CP children. TD children increased walking velocity, step- and stride length, and decreased double support duration with a slightly earlier timing of foot-off, while the opposite was found in CP. Similarly, increased ranges of motion at the pelvis (coronal plane) and hip (all planes), higher joint angular velocities at the hip and ankle, as well as increased moments and powers at the hip, knee and ankle were observed for TD children, while CP children did not change or even showed decreases in the respective measures in response to walking with added weight. Further, while TD children increased their gastrocnemius EMG amplitude during weighted walking, CP children slightly decreased their gastrocnemius EMG amplitude. As such, an increase in weight has a significant effect on the gait pattern in CP children. Clinical gait analysts should therefore take into account the negative effects of increased weight during pre–post measurements to avoid misinterpretation of treatment results. Overweight and obesity in CP should be counteracted or prevented as the increased weight has detrimental effects on the gait pattern.

A new strength assessment to evaluate the association between muscle weakness and gait pathology in children with cerebral palsy

Aim The main goal of this validation study was to evaluate whether lower limb muscle weakness and plantar flexor rate of force development (RFD) related to altered gait parameters in children with cerebral palsy (CP), when weakness was assessed with maximal voluntary isometric contractions (MVICs) in a gait related test position. As a subgoal, we analyzed intra- and intertester reliability of this new strength measurement method. Methods Part 1 –Intra- and intertester reliability were determined with the intra-class correlation coefficient (ICC2,1) in 10 typical developing (TD) children (age: 5–15). We collected MVICs in four lower limb muscle groups to define maximum joint torques, as well as plantar flexor RFD. Part 2 –Validity of the strength assessment was explored by analyzing the relations of lower limb joint torques and RFD to a series of kinematic- and kinetic gait features, the GDI (gait deviation index), and the GDI-kinetic in 23 children with CP (GMFCS I-II; age: 5–15) and 23 TD children (age: 5–15) with Spearman’s rank correlation coefficients. Results Part 1 –The best reliability was found for the torque data (Nm), with the highest ICC2,1 (0.951) for knee extension strength (inter) and the lowest (0.693) for dorsiflexion strength (intra). For plantar flexor RFD, the most reliable window size was 300 milliseconds (ICC2,1: 0.828 (inter) and 0.692 (intra)). Part 2 –The children with CP were significantly weaker than the TD children (p <0.001). Weakness of the dorsiflexors and plantar flexors associated with delayed and decreased knee flexion angle during swing, respectively. No other significant correlations were found. Conclusion While our new strength assessment was reliable, intra-joint correlations between weakness, RFD, and gait deviations were low. However, we found inter-joint associations, reflected by a strong association between plantar- and dorsiflexor weakness, and decreased and delayed knee flexion angle during swing.

Gait deviations in Duchenne muscular dystrophy—Part 1. A systematic review

BACKGROUND Although prolonged ambulation is considered important in children with Duchenne muscular dystrophy (DMD), articles describing gait deviations in DMD are scarce. RESEARCH QUESTION Therefore, our research questions were the following: 1) what are the most consistently reported spatiotemporal-, kinematic-, kinetic-, and muscle activity deviations in children with DMD in literature, 2) what is the quality of the studies describing these deviations, and 3) is there need for further research? METHODS We conducted a systematic literature search for studies published before the end of June 2017 in six online databases. We created a data extraction form to define information on materials and methods and on the analyzed gait parameters for each paper included in the review. If enough information was available, we calculated standardized mean differences (SMDs). RESULTS The search yielded nine articles, but generalizability was poor. Seventy-nine parameters were analyzed by seven research groups, but they only agreed on a decrease in walking speed (minimal SMD: 1.26), stride length (1.83), step length (1.80), dorsiflexion during swing (1.43), maximal power generation at the hip (0.92), maximal knee extension torque (0.99), maximal dorsiflexion torque (-1.30), and maximal power generation at the ankle (0.92), and an increased knee range of motion (-0.82) in DMD. SIGNIFICANCE In order to keep children with DMD ambulant as long as possible, a clear understanding of their pathological gait pattern is necessary. However, gait deviations in DMD appear not well defined. Previous studies appear to be of an exploratory nature while using predefined gait parameters to assess an undirected null hypothesis. This made them prone to regional focus bias, thereby increasing the chance of a type I error. Therefore, further research is required to define the altered gait pattern in children with DMD.

Gait deviations in Duchenne muscular dystrophy—Part 2. Statistical non-parametric mapping to analyze gait deviations in children with Duchenne muscular dystrophy

BACKGROUND Prolonged ambulation is considered important in children with Duchenne muscular dystrophy (DMD). However, previous studies analyzing DMD gait were sensitive to false positive outcomes, caused by uncorrected multiple comparisons, regional focus bias, and inter-component covariance bias. Also, while muscle weakness is often suggested to be the main cause for the altered gait pattern in DMD, this was never verified. RESEARCH QUESTION Our research question was twofold: 1) are we able to confirm the sagittal kinematic and kinetic gait alterations described in a previous review with statistical non-parametric mapping (SnPM)? And 2) are these gait deviations related to lower limb weakness? METHODS We compared gait kinematics and kinetics of 15 children with DMD and 15 typical developing (TD) children (5-17 years), with a two sample Hotellings T2 test and post-hoc two-tailed, two-sample t-test. We used canonical correlation analyses to study the relationship between weakness and altered gait parameters. For all analyses, α-level was corrected for multiple comparisons, resulting in α = 0.005. RESULTS We only found one of the previously reported kinematic deviations: the children with DMD had an increased knee flexion angle during swing (p = 0.0006). Observed gait deviations that were not reported in the review were an increased hip flexion angle during stance (p = 0.0009) and swing (p = 0.0001), altered combined knee and ankle torques (p = 0.0002), and decreased power absorption during stance (p = 0.0001). No relationships between weakness and these gait deviations were found. SIGNIFICANCE We were not able to replicate the gait deviations in DMD previously reported in literature, thus DMD gait remains undefined. Further, weakness does not seem to be linearly related to altered gait features. The progressive nature of the disease requires larger study populations and longitudinal analyses to gain more insight into DMD gait and its underlying causes.

The influence of maximum isometric muscle force scaling on estimated muscle forces from musculoskeletal models of children with cerebral palsy

BACKGROUND Musculoskeletal models do not include patient-specific muscle forces but rely on a scaled generic model, with muscle forces left unscaled in most cases. However, to use musculoskeletal simulations to inform clinical decision-making in children with cerebral palsy (CP), inclusion of subject-specific muscle forces is of utmost importance in order to represent each childs compensation mechanisms introduced through muscle weakness. RESEARCH AIM The aims of this study were to (i) evaluate if maximum isometric muscle forces (MIMF) in musculoskeletal models of children with CP can be scaled based on strength measurements obtained with a hand-held-dynamometer (HHD), (ii) evaluate the impact of the HHD based scaling approach and previously published MIMF scaling methods on computed muscle forces during gait, and (iii) compare maximum muscle forces during gait between CP and typically developing (TD) children. METHODS Strength and motion capture data of six CP and motion capture data of six TD children were collected. The HHD measurements to obtain hip, knee and ankle muscle strength were simulated in OpenSim and used to modify MIMF of the 2392-OpenSim model. These muscle forces were compared to the MIMF scaled on the childs body mass and a scaling approach, which included the body mass and muscle-tendon lengths. OpenSim was used to calculate peak muscle forces during gait. RESULTS Ankle muscle strength was insufficient to reproduce joint moments during walking when MIMF were scaled based on HHD. During gait, peak hip and knee extensor muscle forces were higher and peak ankle dorsi-flexor forces were lower in CP compared to TD participants. SIGNIFICANCE HHD measurements can be used to scale MIMF for the hip and knee muscle groups but underestimate the force capacity of the ankle muscle groups during walking. Muscle-tendon-length and mass based scaling methods affected muscle activations but had little influence on peak muscle forces during gait.BACKGROUND Musculoskeletal models do not include patient-specific muscle forces but rely on a scaled generic model, with muscle forces left unscaled in most cases. However, to use musculoskeletal simulations to inform clinical decision-making in children with cerebral palsy (CP), inclusion of subject-specific muscle forces is of utmost importance in order to represent each childs compensation mechanisms introduced through muscle weakness. RESEARCH AIM The aims of this study were to (i) evaluate if maximum isometric muscle forces (MIMF) in musculoskeletal models of children with CP can be scaled based on strength measurements obtained with a hand-held-dynamometer (HHD), (ii) evaluate the impact of the HHD based scaling approach and previously published MIMF scaling methods on computed muscle forces during gait, and (iii) compare maximum muscle forces during gait between CP and typically developing (TD) children. METHODS Strength and motion capture data of six CP and motion capture data of six TD children were collected. The HHD measurements to obtain hip, knee and ankle muscle strength were simulated in OpenSim and used to modify MIMF of the 2392-OpenSim model. These muscle forces were compared to the MIMF scaled on the childs body mass and a scaling approach, which included the body mass and muscle-tendon lengths. OpenSim was used to calculate peak muscle forces during gait. RESULTS Ankle muscle strength was insufficient to reproduce joint moments during walking when MIMF were scaled based on HHD. During gait, peak hip and knee extensor muscle forces were higher and peak ankle dorsi-flexor forces were lower in CP compared to TD participants. SIGNIFICANCE HHD measurements can be used to scale MIMF for the hip and knee muscle groups but underestimate the force capacity of the ankle muscle groups during walking. Muscle-tendon-length and mass based scaling methods affected muscle activations but had little influence on peak muscle forces during gait.

Non-neural Muscle Weakness Has Limited Influence on Complexity of Motor Control during Gait

Cerebral palsy (CP) and Duchenne muscular dystrophy (DMD) are neuromuscular disorders characterized by muscle weakness. Weakness in CP has neural and non-neural components, whereas in DMD, weakness can be considered as a predominantly non-neural problem. Despite the different underlying causes, weakness is a constraint for the central nervous system when controlling gait. CP demonstrates decreased complexity of motor control during gait from muscle synergy analysis, which is reflected by a higher total variance accounted for by one synergy (tVAF1). However, it remains unclear if weakness directly contributes to higher tVAF1 in CP, or whether altered tVAF1 reflects mainly neural impairments. If muscle weakness directly contributes to higher tVAF1, then tVAF1 should also be increased in DMD. To examine the etiology of increased tVAF1, muscle activity data of gluteus medius, rectus femoris, medial hamstrings, medial gastrocnemius, and tibialis anterior were measured at self-selected walking speed, and strength data from knee extensors, knee flexors, dorsiflexors and plantar flexors, were analyzed in 15 children with CP [median (IQR) age: 8.9 (2.2)], 15 boys with DMD [8.7 (3.1)], and 15 typical developing (TD) children [8.6 (2.7)]. We computed tVAF1 from 10 concatenated steps with non-negative matrix factorization, and compared tVAF1 between the three groups with a Mann-Whiney U-test. Spearmans rank correlation coefficients were used to determine if weakness in specific muscle groups contributed to altered tVAF1. No significant differences in tVAF1 were found between DMD [tVAF1: 0.60 (0.07)] and TD children [0.65 (0.07)], while tVAF1 was significantly higher in CP [(0.74 (0.09)] than in the other groups (both p < 0.005). In CP, weakness in the plantar flexors was related to higher tVAF1 (r = −0.72). In DMD, knee extensor weakness related to increased tVAF1 (r = −0.50). These results suggest that the non-neural weakness in DMD had limited influence on complexity of motor control during gait and that the higher tVAF1 in children with CP is mainly related to neural impairments caused by the brain lesion.

Associations between muscle synergies and treatment outcomes in cerebral palsy are robust across clinical centers

OBJECTIVE To determine whether patient-specific differences in motor control quantified using muscle synergy analysis were associated with changes in gait after treatment of cerebral palsy (CP) across 2 clinical centers with different treatments and clinical protocols. DESIGN Retrospective cohort study. SETTING Clinical medical center. PARTICIPANTS Center 1: children with CP (n=473) and typically developing (TD) children (n=84). Center 2: children with CP (n=163) and TD children (n=12). INTERVENTIONS Standard clinical care at each center. MAIN OUTCOME MEASURES The Dynamic Motor Control Index During Walking (walk-DMC) was computed from electromyographic data during gait using muscle synergy analysis. Regression analysis was used to evaluate whether pretreatment walking speed or kinematics, muscle synergies, treatment group, prior treatment, or age were associated with posttreatment changes in gait at both clinical centers. RESULTS Walk-DMC was significantly associated with changes in speed and kinematics after treatment with similar regression models at both centers. Children with less impaired motor control were more likely to have improvements in walking speed and gait kinematics after treatment, independent of treatment group. CONCLUSIONS Dynamic motor control evaluated with synergy analysis was associated with changes in gait after treatment at both centers, despite differences in treatments and clinical protocols. This study further supports the finding that walk-DMC provides additional information, not captured in traditional gait analysis, that may be useful for treatment planning.