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Published in final edited form as: Gait Posture. 2022 Oct 18;99:1–8. doi: 10.1016/j.gaitpost.2022.10.010

Independently ambulatory children with spina bifida experience near-typical knee and ankle joint moments and forces during walking

Marissa R Lee a, Jennifer L Hicks b, Tishya A L Wren c, Scott L Delp a,b
PMCID: PMC9772073  NIHMSID: NIHMS1854603  PMID: 36283301

Abstract

Background:

Spina bifida, a neurological defect, can result in lower-limb muscle weakness. Altered ambulation and reduced musculoskeletal loading can yield decreased bone strength in individuals with spina bifida, yet individuals who remain ambulatory can exhibit normal bone outcomes.

Research question:

During walking, how do lower-limb joint kinematics and moments and tibial forces in independently ambulatory children with spina bifida differ from those of children with typical development?

Methods:

We retrospectively analyzed data from 16 independently ambulatory children with spina bifida and 16 children with typical development and confirmed that tibial bone strength was similar between the two groups. Plantar flexor muscle strength was measured by manual muscle testing, and 14 of the children with spina bifida wore activity monitors for an average of 5 days. We estimated tibial forces at the knee and ankle using motion capture data and musculoskeletal simulations. We used Statistical Parametric Mapping t-tests to compare lower-limb joint kinematic and kinetic waveforms between the groups with spina bifida and typical development. Within the group with spina bifida, we examined relationships between plantar flexor muscle strength and peak tibial forces by calculating Spearman correlations.

Results:

Activity monitors from the children with spina bifida reported typical daily steps (9656 [SD 3095]). Despite slower walking speeds (p=0.004) and altered lower-body kinematics (p<0.001), children with spina bifida had knee and ankle joint moments and forces similar to those of children with typical development, with no detectable differences during stance. Plantar flexor muscle weakness was associated with increased compressive knee force (p=0.002) and shear ankle force (p=0.009).

Significance:

High-functioning, independently ambulatory children with spina bifida exhibited near-typical tibial bone strength and near-typical step counts and tibial load magnitudes. Our results suggest that the tibial forces in this group are of sufficient magnitudes to support the development of normal tibial bone strength.

Keywords: spina bifida, myelomeningocele, musculoskeletal simulation, joint moment, joint force, bone

Introduction

Spina bifida is a neurological birth defect resulting from incomplete closure of the spinal column in early fetal development. In many cases, insufficient protection causes damage to the spinal cord and nerves. As a result, muscles in the lower extremities can be weakened or paralyzed. With increasing severity, spina bifida weakens the plantar flexor, gluteal, and quadriceps muscles [1]. In the US, approximately 166,000 individuals live with spina bifida [2]. Worldwide, it occurs in 2 to 8 of every 1000 live births [3].

Children with spina bifida have diminished motor abilities [4] and spend less time being active [5] than peers with typical development, in part due to lower-limb muscle weakness. These activity differences are hypothesized to contribute to the population’s increased risk of osteoporosis and low-energy fracture in lower-extremity weight-bearing long bones [6–9]. These increased risks are not constant across the population with spina bifida. With increasing ambulation and function, individuals with spina bifida have better bone health, including improved bone strength properties in the tibia [9,10] and femoral neck [11], increased tibia bone mass and volume [12], more normal tibial development [13], and lower risk for bone fracture [8]. In studying bone outcomes in individuals with spina bifida, it is important to understand why individuals with higher levels of function and ambulation demonstrate better bone health. This understanding will provide insight into how we might preserve bone health in this population.

Bone accrual and maintenance are influenced by mechanical loading. Dynamic loads drive bone adaptation, with loading magnitude generally regarded as more important than number of load cycles [14]. Insufficient mechanical stimulation of the bone yields bone resorption and lower bone strength [15]. Challenges in directly measuring joint forces have limited our ability to quantitatively understand bone loading. Fortunately, advances in musculoskeletal simulation enable joint force estimation [16–19].

In this study, we investigated joint loads during walking gait in high-functioning, independently ambulatory children with spina bifida. Walking is a daily activity that is impacted by spina bifida, and altered gait patterns affect joint loading. For example, lower-limb joint loads can be reduced with slower walking [18] or when smaller muscle forces are generated [19]. To investigate these issues, we sought to answer two questions: 1) How do lower-limb joint kinematics and moments and tibial forces during gait differ between independently ambulatory children with spina bifida and children with typical development? 2) Are there relationships between muscle strength and tibial forces in independently ambulatory children with spina bifida? By exploring these questions, we hope to understand bone loading during walking and how joint forces relate to muscle strength in high-functioning children with spina bifida. Our results provide insight into how daily mechanical loading relates to bone health in this population.

Methods

Data Collection

Data for this study were previously collected at Children’s Hospital Los Angeles [9,12]. This dataset contains demographic, step count, physical exam, computed tomography, and gait data of 83 ambulatory children with spina bifida and 179 children with typical development. The current analysis included only participants who could walk independently and barefoot, without orthoses or walking aids like crutches, and who had at least one complete gait cycle of kinematic and kinetic walking data (three consecutive force plate strikes, with a single foot contacting each plate).

Sixteen independent ambulators with spina bifida (mean age 10.4, standard deviation [SD] 2.7 years old, 8 female / 8 male) and 16 age- and sex-matched individuals with typical development were included (Table 1). The group with spina bifida comprised 11 individuals with myelomeningocele and 5 with lipomyelomeningocele. Using the Dias functional classification of myelomeningocele [1], physical therapists classified 2 individuals with spina bifida with high sacral functional levels and 14 with low sacral functional levels. For each included individual with spina bifida, an individual with typical development was matched such that the sexes were the same and the ages were as close as available. No significant differences (p≥0.868) in age, height, weight, or body mass index (BMI) existed between the groups with spina bifida and typical development. Written informed assent and consent were obtained from all participants and their guardians. All study procedures were approved by our institutional review boards.

Table 1. Group characteristics.

Mean (standard deviation) demographic characteristics and tibia bone strength measures within the groups with typical development and spina bifida and p-values of a Welch’s t-test between groups.

Typical development (n=16) Spina bifida (n=16) p
Age (years) 10.6 (2.3) 10.4 (2.7) 0.893
Height (cm) 140 (14) 141 (18) 0.920
Weight (kg) 41 (17) 42 (21) 0.939
BMI (kg/m2) 20.2 (5.6) 19.9 (5.3) 0.868
Sex 8F / 8M 8F / 8M --
Proximal cross-sectional area (mm2) 847 (206) 897 (293) 0.590
Proximal cancellous bone density (mg/cm3) 165 (41) 114 (36) **0.001
Distal cross-sectional area (mm2) 648 (166) 618 (190) 0.651
Distal cancellous bone density (mg/cm3) 161 (39) 145 (35) 0.258
Midshaft cortical bone area (mm2) 229 (61) 227 (89) 0.926
Midshaft cross-sectional area (mm2) 294 (72) 296 (105) 0.946
Midshaft cortical thickness (mm) 5.1 (0.8) 5.0 (1.1) 0.656
Midshaft cortical bone density (mg/cm3) 1001 (48) 1022 (61) 0.288
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BMI=body mass index;

**

p<0.01

Bone strength outcomes for all participants were calculated from quantitative computed tomography scans of each participant’s tibias. Image acquisition and processing procedures are described in a previous study [9]. Of eight bone properties measured, only cancellous bone density at the proximal tibia (p=0.001) was significantly lower (p<0.05) in the group with spina bifida than in the group with typical development (Table 1).

Individuals with spina bifida underwent exams with a physical therapist. Plantar flexor muscle strength was evaluated using a standard manual muscle test (0–5 scale [20]). Among participants with spina bifida, 14 of 16 wore StepWatch activity monitors (Modus, Edmonds, WA) for 1–9 (mean 5, median 6) days. Average steps per day were calculated for each participant.

Overground gait data of participants walking barefoot and without assistance at self-selected speeds were obtained for 1 to 5 gait cycles per participant (mean 2.1, median 2). Data from every complete gait cycle of kinematic and kinetic walking data (three consecutive force plate strikes, with a single foot contacting each plate) were included. Ground reaction forces were acquired at 2520 Hz through three consecutive floor-embedded force plates (AMTI, Watertown, MA) and were filtered at 6 Hz. Marker data of the torso and lower extremities were acquired at 120 Hz by an 8-camera motion capture system (Vicon, Oxford, UK), following the Plug-in-Gait model, with thigh markers replaced by patella markers [21].

Musculoskeletal Simulation

We estimated joint kinematics, moments, and forces using OpenSim 4.1 [22,23]. We first scaled a generic musculoskeletal model, using marker data from a static trial, to match the size of each participant. The generic model was based on the full-body model developed by Rajagopal et al. [24] and modified by Uhlrich et al. [25]. Arms in the model were fixed to the torso, since arm marker data were not collected. We scaled peak isometric muscle forces to each participant using the mass-height-volume relationship estimated by Handsfield et al. [24,26]. Using OpenSim’s Inverse Kinematics tool, we calculated joint kinematics. Across gait cycles, average marker root mean square (RMS) error was 1.1 (SD 0.2) cm, and maximum marker error was 3.5 (SD 0.4) cm, within recommended accuracy [27]. We filtered kinematics at 6 Hz.

To reduce dynamic inconsistencies in the experimental data, we used the Residual Reduction Algorithm [22]. RMS and peak residual forces were 1.6% (SD 0.6%) and 3.5% (SD 1.7%) of the maximum ground reaction force magnitude, respectively, within the recommended limit of 5% [27]. RMS and peak residual moments were 1.7% (SD 0.4%) and 3.7% (SD 1.2%) of the center of mass height times maximum ground reaction force magnitude, respectively. These moment discrepancies are greater than the 1% recommended discrepancy, likely because the arms were fixed to the torsos of our models [27,28].

We estimated muscle forces using the static optimization algorithm developed and described by Uhlrich et al. [25]. This algorithm minimizes the sum of squared muscle activations and accounts for active and passive muscle forces. It also approximates tendon compliance by solving a musculotendon equilibrium equation at each time step [25]. Using OpenSim’s Joint Reaction Analysis, we summed intersegmental resultant forces and muscle forces to estimate tibial forces. These tibial forces comprised compressive and shear forces on the tibia at the knee and ankle joints.

Musculoskeletal Simulation Evaluation

To evaluate the ability of our simulations to represent muscle activity, we qualitatively compared simulation muscle activation estimates to electromyography (EMG) recordings in a separate group of independently ambulatory participants. We performed this comparison with a separate group, comprising 1 participant with typical development and 6 participants with spina bifida, because EMG data were not collected in the primary cohort. Bone strength measures were not collected for this separate group. Overground walking EMG recordings from the gastrocnemius medialis, tibialis anterior, semitendinosus, rectus femoris, and vastus lateralis were acquired at 2400 Hz, band-pass filtered between 50 and 500 Hz, rectified, low-pass filtered at 7.5 Hz, and scaled such that peak EMG signals matched peak simulated activations.

We qualitatively compared muscle activations computed using static optimization and EMG signals to determine if major features of experimental EMG were represented in our simulations (Supplementary Figure 1). EMG recordings and simulated muscle activity both indicated gastrocnemius activity in late stance; tibialis anterior activity in early stance and swing; semitendinosus activity in early stance and late swing; and vastus lateralis activity in early stance. EMG recordings indicated that rectus femoris activation timing varied by participant. In general, simulated muscle activity indicated rectus femoris activity in late stance and early swing. Peak static optimization activation estimates of the gastrocnemius medialis tended to decrease with plantar flexor muscle strengths.

Statistical Analysis

We compared walking speed, estimated by average center of mass velocity from the gait simulations, between the groups with spina bifida and typical development using Welch’s t-test.

We scaled internal joint moments by body mass and normalized joint forces by body weight. For each participant with spina bifida, we analyzed only the leg with weaker plantar flexor muscle strength. If both legs were equally affected, and for participants with typical development, we analyzed the leg with more available gait cycles. For each selected limb, we extracted and averaged gait waveforms (lower-limb joint kinematics and moments, ground reaction forces, and tibial compressive and shear forces at the knee and ankle) across gait cycles.

To determine how lower-limb gait waveforms differed between independently ambulatory children with spina bifida and children with typical development, we compared average gait waveforms using Statistical Parametric Mapping (SPM) unpaired t-tests. This technique [29] enables the comparison of the means of two groups of continuous waveforms and identification of periods of difference in the gait cycle. It has previously been used to identify differences in walking gait patterns in children with cerebral palsy [30].

To determine if relationships exist between muscle strength and tibial forces, we calculated the Spearman correlation between plantar flexor muscle strength and peak tibial forces. Manual muscle test scores involving + or − were replaced with ±0.33 adjustments (e.g., 3+ re-coded as 3.33, 3− re-coded as 2.67).

Statistical tests were evaluated with a significance level of 0.05. Statistical analyses were conducted in Python 3 (Natick, MA, USA).

Data and custom simulation and analysis scripts are available on SimTK at: https://simtk.org/projects/sb_force.

Results

Walking Activity and Speed

Activity monitors worn by 14 participants with spina bifida reported 9656 (SD 3095) average daily steps.

Average walking speed, estimated by average center of mass velocity from the gait simulations, was slower (p=0.004) in the group with spina bifida (1.1 [SD 0.1] m/s) than in the group with typical development (1.3 [SD 0.1] m/s).

Gait Waveforms

The group with spina bifida exhibited significantly more ankle dorsiflexion in the second half of stance and less plantarflexion at toe-off (p<0.001) and significantly less knee flexion at toe-off (p=0.032) compared to the group with typical development. Hip flexion, adduction, and rotation angles did not differ significantly between groups. Greater variances in joint kinematics among participants with spina bifida were observed across the gait cycle at the hip, knee, and ankle (Figure 1).

Figure 1. Group joint kinematic waveforms.

Figure 1.

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Mean ± one standard deviation joint kinematics across the gait cycle for participants in the groups with typical development (black) and spina bifida (red). The light gray regions represent the swing phase of the gait cycle. Bars underneath the curves reflect significant difference results from the SPM t-tests (*p<0.05, ***p<0.001).

Few statistically significant differences in joint moments were identified between groups (Figure 2). Differences in hip extension moments (p=0.025), hip abduction moments (p=0.040), and knee extension moments (p=0.037) occurred only in swing and for periods less than 4% of the gait cycle. Significant differences were found in hip rotation moments in mid-stance (p<0.001). As with kinematics, joint moment variances were greater in the group with spina bifida than in the group with typical development. Ankle power was significantly lower in the group with spina bifida (p<0.05) for short periods of late stance and swing (Supplementary Figure 2a).

Figure 2. Group joint moment waveforms.

Figure 2.

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Mean ± one standard deviation joint moments across the gait cycle for participants in the groups with typical development (black) and spina bifida (red). Joint moments are scaled by body mass. The light gray regions represent the swing phase of the gait cycle. Bars underneath the curves reflect significant difference results from the SPM t-tests (*p<0.05, ***p<0.001).

No differences between the two groups were detected in mean ground reaction forces (Figure 3) or in shear, compressive, or total tibial forces at the knee and ankle (Figure 4).

Figure 3. Group ground reaction force waveforms.

Figure 3.

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Mean ± one standard deviation ground reaction forces (GRFs) across the gait cycle for participants in the groups with typical development (black) and spina bifida (red). GRFs are expressed in terms of number of body weights (xBW). The light gray regions represent the swing phase of the gait cycle. No significant differences were detected between groups.

Figure 4. Group joint force waveforms.

Figure 4.

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Mean ± one standard deviation tibial forces across the gait cycle for participants in the groups with typical development (black) and spina bifida (red). Forces are expressed in terms of number of body weights (xBW). The light gray regions represent the swing phase of the gait cycle. No significant differences were detected between groups.

Plantar Flexor Muscle Strength and Tibial Forces

Plantar flexor muscle strength was negatively correlated with compressive knee force (ρ=−0.71, p=0.002) and shear ankle force (ρ=−0.63, p=0.009) in the group with spina bifida (Figure 5). The three participants with the lowest plantar flexor muscle strength exhibited peak compressive knee forces and peak shear ankle forces greater than those exhibited by participants with typical development (mean ± two standard deviations). Correlations excluding these three participants were not significant (p>0.106). These three participants with the lowest plantar flexor muscle strength walked at an average speed (1.2 m/s) similar to that of the rest of the group with spina bifida (1.1 m/s). They also walked with more hip flexion and knee flexion during stance, less knee flexion during swing, and more hip abduction and ankle dorsiflexion throughout the gait cycle (Supplementary Figure 3). Ankle power in this group was low (Supplementary Figure 2b).

Figure 5. Peak joint force and plantar flexor muscle strength correlations.

Figure 5.

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Forces are expressed in terms of number of body weights (xBW). Each data point represents the analyzed limb of a single participant. Each gray band represents the peak joint force mean ± two standard deviations of participants in the group with typical development. Spearman’s ρ was calculated for each relationship.

Discussion

On average, children with spina bifida with near-typical bone health demonstrated near-typical lower-limb joint moments and forces, despite walking at slower speeds with altered lower-limb kinematics. We observed greater kinematic and kinetic variability across the gait cycle within the group with spina bifida. Variability in peak shear and compressive joint forces could be explained in part by differences associated with plantar flexor muscle weakness. Our results suggest that the tibial forces in independently ambulatory children with spina bifida are of sufficient magnitudes to support the development of normal tibial bone strength and that children with weak plantar flexor muscles may undergo high joint loading.

Joint Kinematics & Moments

Previous studies have presented qualitative comparisons of joint kinematic and moment waveforms between groups with spina bifida and typical development [31,32]. In this study, we additionally analyzed continuous differences across the gait cycle using SPM t-tests. These tests enable identification of statistically significant periods of difference.

Independently ambulatory participants with spina bifida demonstrated near-typical kinematics on average. The main difference between groups occurred in ankle angles. Our findings of more ankle dorsiflexion and less ankle plantarflexion during walking are consistent with the plantar flexor muscle weakness associated with spina bifida and with previous findings [31].

Despite lower-limb kinematic differences, the group with spina bifida demonstrated near-typical joint moments. Gutierrez et al. [32] qualitatively compared joint moments among groups with typical development and varying levels of spina bifida. Our finding of lower hip external rotation moment in stance is consistent with their findings. They also reported lower hip abduction and ankle plantarflexion moments during stance and lower knee flexion moment in late stance. These differences, consistent with the weak hip abductor and plantar flexor muscles present in children with spina bifida, are supported by trends in our data, but we did not detect statistically significant differences in our high-functioning study group.

Average walking speed was slower than typical in the group with spina bifida. Schwartz et al. [33] reported joint kinematic and moment changes associated with walking speed in children with typical development. The directions of the trends we observed in our analyses align with those associated with decreased walking speed. Notably, however, the differences we observed between groups were greater than the reported changes due to slower walking speed alone.

Tibial Forces & Bone Health

On average, our simulations estimated typical shear and compressive tibial forces in the group with spina bifida. This group also exhibited typical numbers of daily loading cycles (steps per day). The daily steps recorded on activity monitors worn by participants with spina bifida (9656 [SD 3095] steps) were comparable to those previously reported from 7 children with typical development who underwent the same activity monitoring protocol (9589 [SD 3322] steps [34]). Our findings of near-typical tibial forces and loading cycles, combined with the near-typical tibial bone health observed (Table 1), suggest that this group undergoes daily loading patterns sufficient to develop normal tibial bone strength. In general, this independently ambulatory population’s low risk for osteoporosis and fracture may result from near-typical mechanical loading patterns.

While we did not detect differences in the group means of the tibial forces, we did observe larger variation within the group with spina bifida. Variabilities may be partially attributable to variations in the intersegmental resultant forces but are likely most reflective of differences in muscle forces over the gait cycle, since muscles are the major contributing forces to joint forces [35]. Given this high variability, while on average independently ambulatory children with spina bifida do not have atypical loading or bone strength, altered loading may still be present for some individuals with spina bifida.

Our investigations of the relationships between muscle strength and joint forces identified that weaker plantar flexor muscles were significantly correlated with greater peak compressive knee and shear ankle forces. Of particular note are the increased forces experienced by the participants with spina bifida with the weakest plantar flexor muscles, likely associated with crouch gait. The increased compressive knee forces in this group are consistent with previous findings of children with crouch gait [17] and likely reflect increased activations of the quadriceps muscles (Supplementary Figure 4). The increased shear ankle forces may be related to the increased ankle dorsiflexion in late stance. These elevated compressive knee and shear ankle forces could lead to fracture [36] and osteoarthritis [37]. Special attention should be paid to high-functioning individuals with spina bifida who have weak plantar flexor muscles, as they may undergo atypical joint forces. Further study is required to understand the impact of these increased forces.

We used manual muscle tests to measure plantar flexor muscle strength. Manual muscle testing may underestimate the dynamic force capacity of plantar flexor muscles [38]. However, we found that simulated activations of the plantar flexor muscles generally aligned with manual muscle test scores. In particular, participants with the lowest manual muscle test scores exhibited low peak dynamic plantar flexor forces (Supplementary Figures 4 and 5).

Our gait simulations relied on scaled generic musculoskeletal models, since we did not have images of the full lower limbs. Personalized musculoskeletal geometries were not accounted for, which may impact the accuracy of our estimated tibial forces [39,40]. An important area of future research is to determine for which studies personalized musculoskeletal modeling significantly influences scientific conclusions.

While we found that plantar flexor muscle strength was associated with tibial forces, we did not detect (p>0.3) significant correlations between plantar flexor muscle strength and bone strength measures. Our study included only highly functional, independently ambulatory children with spina bifida and is limited by its sample size. Given the small sample, that we did not detect significant differences in many of our tests does not indicate that we would not detect differences in a study with a larger, more diverse sample. Previous work has demonstrated that bone health disparities between individuals with spina bifida and individuals with typical development increase with puberty [9] and disparities in function [10–13]. Including older independent ambulators with spina bifida, as well as a group of individuals with spina bifida with a greater range of functional abilities, will be critical to understanding how bone loading differs among individuals with spina bifida and relates to bone health. Future studies should also investigate joint forces beyond walking gait and in other free-living activities.

We conclude that on average, young, high-functioning individuals with spina bifida undergo near-typical knee and ankle joint moments and forces. These loads are of sufficient magnitudes to support the near-typical tibial bone health observed in this group.

Supplementary Material

Supplementary Figures

Acknowledgements

Funding:

This work was supported by the National Institutes of Health [grant numbers 5R01HD059826, P41EB027060]; the Inventec Stanford Graduate Fellowship, Stanford, CA; and the Catalyst for Collaborative Solutions, Stanford, CA. The study sponsors had no involvement in the study design; in the collection, analysis, or interpretation of data; in the writing of the manuscript; or in the decision to submit the manuscript for publication.

Our thanks to the team members of the Children’s Hospital Los Angeles John C. Wilson, Jr. Motion and Sports Analysis Laboratory for their collection and sharing of the data and to Scott Uhlrich and Carmichael Ong for their simulation expertise.

Footnotes

Ethics approval and consent to participate statement

This study was conducted with the approvals of the Children’s Hospital Los Angeles and Stanford Institutional Review Boards. Written informed assent and consent were obtained from all participants and their guardians.

Data statement

The data and code supporting the conclusions of this study are available on SimTK at: https://simtk.org/projects/sb_force.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary Figures
NIHMS1854603-supplement-Supplementary_Figures.pdf (518.2KB, pdf)

Data Availability Statement

The data and code supporting the conclusions of this study are available on SimTK at: https://simtk.org/projects/sb_force.

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