Achilles Tendon Loading during Running Estimated Via Shear Wave Tensiometry: A Step Toward Wearable Kinetic Analysis.

PURPOSE: Understanding muscle-tendon forces (e.g., triceps surae and Achilles tendon) during locomotion may aid in the assessment of human performance, injury risk, and rehabilitation progress. Shear wave tensiometry is a noninvasive technique for assessing in vivo tendon forces that has been recently adapted to a wearable technology. However, previous laboratory-based and outdoor tensiometry studies have not evaluated running. This study was undertaken to assess the capacity for shear wave tensiometry to produce valid measures of Achilles tendon loading during running at a range of speeds. METHODS: Participants walked (1.34 m·s -1 ) and ran (2.68, 3.35, and 4.47 m·s -1 ) on an instrumented treadmill while shear wave tensiometers recorded Achilles tendon wave speeds simultaneously with whole-body kinematic and ground reaction force data. A simple isometric task allowed for the participant-specific conversion of Achilles tendon wave speeds to forces. Achilles tendon forces were compared with ankle torque measures obtained independently via inverse dynamics analyses. Differences in Achilles tendon wave speed, Achilles tendon force, and ankle torque across walking and running speeds were analyzed with linear mixed-effects models. RESULTS: Achilles tendon wave speed, Achilles tendon force, and ankle torque exhibited similar temporal patterns across the stance phase of walking and running. Significant monotonic increases in peak Achilles tendon wave speed (56.0-83.8 m·s -1 ), Achilles tendon force (44.0-98.7 N·kg -1 ), and ankle torque (1.72-3.68 N·m·(kg -1 )) were observed with increasing locomotion speed (1.34-4.47 m·s -1 ). Tensiometry estimates of peak Achilles tendon force during running (8.2-10.1 body weights) were within the range of those estimated previously via indirect methods. CONCLUSIONS: These results set the stage for using tensiometry to evaluate Achilles tendon loading during unobstructed athletic movements, such as running, performed in the field.

A hierarchical clustering approach for examining the relationship between pelvis-proximal femur geometry and bone stress injury in runners.

Bone stress injury (BSI) risk in runners is multifactorial and not well understood. Unsupervised machine learning approaches can potentially elucidate risk factors for BSI by identifying groups of similar runners within a population which differ in BSI incidence. Here, a hierarchical clustering approach is used to identify groups of collegiate cross country runners based on 2-dimensional frontal plane pelvis and proximal femur geometry, which was extracted from dual-energy X-ray absorptiometry scans and dimensionally reduced by principal component analysis. Seven distinct groups were identified using the cluster tree, with the initial split being highly related to female-male differences. Visual inspection revealed clear differences between groups in pelvis and proximal femur geometry, and groups were found to differ in lower body BSI incidence during the subsequent academic year (Rand index = 0.53; adjusted Rand index = 0.07). Linear models showed between-cluster differences in visually identified geometric measures. Geometric measures were aggregated into a pelvis shape factor based on trends with BSI incidence, and the resulting shape factor was significantly different between clusters (p < 0.001). Lower shape factor values, corresponding with lower pelvis height and ischial span, and greater iliac span and trochanteric span, appeared to be related to increased BSI incidence. This trend was dominated by the effect observed across clusters of male runners, indicating that geometric effects may be more relevant to BSI risk in males, or that other factors masked the relationship in females. More broadly, this work outlines a methodological approach for distilling complex geometric differences into simple metrics that relate to injury risk.

A trained neural network model accurately predicts Achilles tendon stress during walking and running based on shear wave propagation.

Shear wave tensiometry is a noninvasive technique for measuring tendon loading during activity based on the speed of a shear wave traveling along the tendon. Shear wave speed has been shown to modulate with axial stress, but calibration is required to obtain absolute measures of tendon loading. However, the current technique only makes use of wave speed, whereas other characteristics of the wave (e.g., amplitude, frequency content) may also vary with tendon loading. It is possible that these data could be used in addition to wave speed to circumvent the need for calibration. Given the potential complex relationships to tendon loading, and the lack of an analytical model to guide the use of these data, it is sensible to use a machine learning approach. Here, we used an ensemble neural network approach to predict inverse dynamics estimates of Achilles tendon stress from shear wave tensiometry data collected in a prior study. Neural network-predicted stresses were highly correlated with stance phase inverse dynamics estimates for walking (R2 = 0.89 ± 0.06) and running (R2 = 0.87 ± 0.11) data reserved for neural network model testing and not included in model training. Additionally, error between neural network-predicted and inverse dynamics-estimated stress was reasonable (walking: RMSD = 11 ± 2% of peak load; running: 25 ± 14%). Results of this pilot analysis suggest that a machine learning approach could reduce the reliance of shear wave tensiometry on calibration and expand its usability in many settings.

American Society of Biomechanics Clinical Biomechanics Award 2021: Redistribution of muscle-tendon work in children with cerebral palsy who walk in crouch.

BACKGROUND: Previous study showed the triceps surae exhibits spring-like behavior about the ankle during walking in children with cerebral palsy. Thus, the work generated by the triceps surae is diminished relative to typically developing children. This study investigated whether the quadriceps offset the lack of triceps surae work production in children with cerebral palsy who walk in crouch. METHODS: Seven children with cerebral palsy (8-16 yrs) and 14 typically developing controls (8-17 yrs) walked overground at their preferred speed in a motion analysis laboratory. Shear wave tensiometers were used to track patellar and Achilles tendon loading throughout the gait cycle. Tendon force measures were coupled with muscle-tendon kinematic estimates to characterize the net work generated by the quadriceps and triceps surae about the knee and ankle, respectively. FINDINGS: Children with cerebral palsy generated significantly less triceps surae work when compared to controls (P < 0.001). The reverse was true at the knee. Children with cerebral palsy generated positive net work from the quadriceps about the knee, which exceeded the net quadriceps work generated by controls (P = 0.028). INTERPRETATION: There was a marked difference in functional behavior of the triceps surae and quadriceps in children with cerebral palsy who walk in crouch. In particular, the triceps surae of children with cerebral palsy exhibited spring-like behavior about the ankle while the quadriceps exhibited more motor-like behavior about the knee. This redistribution in work could partly be associated with the elevated energetic cost of walking in children with cerebral palsy and is relevant to consider when planning treatments to correct crouch gait.

A hierarchical clustering approach for examining potential risk factors for bone stress injury in runners.

Bone stress injuries (BSI) are overuse injuries that commonly occur in runners. BSI risk is multifactorial and not well understood. Unsupervised machine learning approaches can potentially elucidate risk factors for BSI by looking for groups of similar runners within a population that differ in BSI incidence. Here, a hierarchical clustering approach is used to identify groups of collegiate cross country runners (32 females, 21 males) based on healthy pre-season running (4.47 m·s-1) gait data which were aggregated and dimensionally reduced by principal component analysis. Five distinct groups were identified using the cluster tree. Visual inspection revealed clear differences between groups in kinematics and kinetics, and linear mixed effects models showed between-group differences in metrics potentially related to BSI risk. The groups also differed in BSI incidence during the subsequent academic year (Rand index = 0.49; adjusted Rand index = -0.02). Groups ranged from those including runners spending less time contacting the ground and generating higher peak ground reaction forces and joint moments to those including runners spending more time on the ground with lower loads. The former groups showed higher BSI incidence, indicating that short stance phases and high peak loads may be risk factors for BSI. Since ground contact duration may itself account for differences in peak loading metrics, we hypothesize that the percentage of time a runner is in contact with the ground may be a useful metric to include in machine learning models for predicting BSI risk.

Atypical triceps surae force and work patterns underlying gait in children with cerebral palsy.

The purpose of this study was to quantitatively assess Achilles tendon mechanical behavior during gait in children with cerebral palsy (CP). We used a newly designed noninvasive sensor to measure Achilles tendon force in 11 children with CP (4F, 8-16 years old) and 15 typically developing children (controls) (9F, 8-17 years old) during overground walking. Mechanical work loop plots (force-displacement plots) were generated by combining muscle-tendon kinetics, kinematics, and EMG activity to evaluate the Achilles tendon work generated about the ankle. Work loop patterns in children with CP were substantially different than those seen in controls. Notably, children with CP showed significantly diminished work production at their preferred speed compared to controls at their preferred speed and slower speeds. Despite testing a heterogeneous population of children with CP, we observed a homogenous spring-like muscle-tendon behavior in these participants. This is in contrast with control participants who used their plantar flexors like a motor during gait. Statement of Clinical Significance: These data demonstrate the potential for using skin-mounted sensors to objectively evaluate muscle contributions to work production in pathological gait.

Normative Achilles and patellar tendon shear wave speeds and loading patterns during walking in typically developing children.

BACKGROUND: Motion analysis is commonly used to evaluate joint kinetics in children with cerebral palsy who exhibit gait disorders. However, one cannot readily infer muscle-tendon forces from joint kinetics. This study investigates the use of shear wave tensiometry to characterize Achilles and patellar tendon forces during gait. RESEARCH QUESTION: How do Achilles and patellar tendon wave speed and loading modulate with walking speed in typically developing children? METHODS: Twelve typically developing children (9-16 years old) walked on an instrumented treadmill with shear wave tensiometers over their Achilles (n = 11) and patellar (n = 9) tendons. Wave speeds were recorded at five leg length-normalized walking speeds (very slow to very fast). Achilles and patellar tendon moment arms were measured with synchronized ultrasound and motion capture. The tendon wave speed-load relationship was calibrated at the typical walking speed and used to estimate tendon loading at other walking speeds. RESULTS: Characteristic Achilles and patellar tendon wave speed trajectories exhibited two peaks over a gait cycle. Peak Achilles tendon force closely aligned with peak ankle plantarflexor moment during pushoff, though force exhibited less modulation with walking speed. A second peak in late swing Achilles loading, which was not evident from the ankle moment, increased significantly with walking speed (p < 0.001). The two peaks in patellar tendon loading occurred at 12 ± 1% and 68 ± 6% of the gait cycle, matching the timing of peak knee extension moment in early stance and early swing. Both patellar tendon load peaks increased significantly with walking speed (p < 0.05). SIGNIFICANCE: This is the first study to use shear wave tensiometry to characterize Achilles and patellar tendon loading during gait in children. These data could serve as a normative comparison when using tensiometry to identify abnormal tendon loading patterns in individuals who exhibit equinus and/or crouch gait.

Shear Wave Tensiometry Reveals an Age-Related Deficit in Triceps Surae Work at Slow and Fast Walking Speeds.

Prior studies have observed an age-related decline in net ankle power and work at faster walking speeds. However, the underlying changes in muscle-tendon behavior are not well-understood, and are challenging to infer from joint level analyses. This study used shear wave tensiometry to investigate the modulation of force and work done by the triceps surae across walking speeds. Fourteen healthy young (7F/7M, 26 ± 5 years) and older (7F/7M, 67 ± 5 years) adults were tested. Subjects walked on an instrumented treadmill at four walking speeds (0.75, 1.00, 1.25, and 1.50 m/s) while lower extremity kinematics and Achilles tendon shear wave speeds were collected. Subject-specific calibrations were used to compute Achilles tendon force from wave speed. Excursions of the soleus and gastrocnemius muscle-tendon units were computed from the kinematic data and subject-specific measures of the Achilles tendon moment arm. Work loop plots were then used to assess effective muscle-tendon stiffness during lengthening, and positive, negative, and net work production during stance. Two-way mixed ANOVAs were used to evaluate the effects of age group and walking speed on each outcome measure. Tendon loading during muscle-tendon lengthening (effective stiffness) did not differ between age groups, but did vary with speed. The soleus became effectively stiffer with increasing speed while the gastrocnemius became effectively more compliant. There was a marked age-related deficit in net soleus (-66% on average) and gastrocnemius (-36%) work across all walking speeds. We did not observe an age-speed interaction effect on net work production. These results suggest the age-related deficit in triceps surae output in walking is pervasive across speed, and hence seemingly not linked to absolute mechanical demands of the task.

Achilles Tendon Morphology Is Related to Triceps Surae Muscle Size and Peak Plantarflexion Torques During Walking in Young but Not Older Adults.

The interaction of the triceps surae muscles and the Achilles tendon is critical in producing the ankle plantarflexion torque required for human walking. Deficits in plantarflexor output are a hallmark of reduced mobility in older adults and are likely associated with changes in the triceps surae muscles that occur with age. Structural differences between young and older adults have been observed in the Achilles tendon and in the triceps surae muscles. However, less is known about how age-related differences in muscle and tendon morphology correspond with each other and, furthermore, how those morphology differences correlate with age-related deficits in function. The goal of this work was to investigate whether there is a correlation between age-related differences in triceps surae muscle size and Achilles tendon cross-sectional area (CSA) and whether either is predictive of ankle plantarflexion torque during walking. We used magnetic resonance imaging (MRI) to measure triceps surae muscle volumes and tendon CSAs in young (n = 14, age: 26 ± 4 years) and older (n = 7, age: 66 ± 5 years) adults, and we determined peak plantarflexion torques during treadmill walking. We found that individual muscle volumes as a percentage of the total triceps surae volume did not differ between young and older adults, though muscle volumes per body size (normalized by the product of height and mass) were smaller in older adults. Achilles tendon CSA was correlated with body size and muscle volumes in young adults but not in older adults. The ratio of tendon CSA to total triceps surae muscle volume was significantly greater in older adults. Peak ankle plantarflexion torque during walking correlated with body size and triceps surae volume in young and older adults but was correlated with tendon CSA only in the young adults. Structure-function relationships that seem to exist between the Achilles tendon and the triceps surae muscles in young adults are no longer evident in all older adults. Understanding mechanisms that determine altered Achilles tendon CSA in older adults may provide insight into age-related changes in function.

Calibration of the shear wave speed-stress relationship in in situ Achilles tendons using cadaveric simulations of gait and isometric contraction.

It has been shown that shear wave speed is directly dependent on axial stress in ex vivo tendons. Hence, a wave speed sensor could be used to track tendon loading during movement. However, adjacent soft tissues and varying joint postures may affect the wave speed-load relationship for intact tendons. The purpose of this study was to determine whether the proportional relationship between squared wave speed and stress holds for in situ cadaveric Achilles tendons, to evaluate whether this relationship is affected by joint angle, and to assess potential calibration techniques. Achilles tendon wave speed and loading were simultaneously measured during cadaveric simulations of gait and isometric contractions performed in a robotic gait simulator. Squared wave speed and axial stress were highly correlated during isometric contraction at all ankle postures (R2avg = 0.98) and during simulations of gait (R2avg = 0.92). Ankle plantarflexion angle did not have a consistent effect on the constant of proportionality (p = 0.217), but there was a significant specimen-angle interaction effect (p < 0.001). Wave speed-based predictions of tendon stress were most accurate (average RMS error = 11% of maximum stress) when calibrating to isometric contractions performed in a dorsiflexed posture that resembled the posture at peak Achilles loading during gait. The results presented here show that the linear relationship between tendon stress and squared shear wave speed holds for a case resembling in vivo conditions, and that calibration during an isometric task can yield accurate predictions of tendon loading during a functional task.

Achilles tendon loading is lower in older adults than young adults across a broad range of walking speeds.

The purpose of this study was to investigate age-related differences in Achilles tendon loading during gait. Fourteen young (7F/7M, 26 ± 5 years) and older (7F/7M, 67 ± 5 years) adults without current neurological or orthopaedic impairment participated. Shear wave tensiometry was used to measure tendon stress by tracking Achilles tendon wave speed. The wave speed-stress relationship was calibrated using simultaneously collected tensiometer and force plate measures during a standing sway task. Tendon stress was computed from the force plate measures using subject-specific ultrasound measures of tendon moment arm and cross-sectional area. All subjects exhibited a highly linear relationship between wave speed squared and tendon stress (mean R2 > 0.9), with no significant age-group differences in tensiometer calibration parameters. Tendon wave speed was monitored during treadmill walking at four speeds (0.75, 1.00, 1.25, and 1.50 m/s) and used to compute the stress experienced by the tendon. Relative to young adults, older adults exhibited 22% lower peak tendon wave speeds. Peak tendon stress during push-off in older adults (24.8 MPa) was 32% less than that in the young adults (36.7 MPa) (p = 0.01). There was a moderate increase (+11%) in peak tendon stress across both groups when increasing speed from 0.75 to 1.50 m/s (main effect of speed, p = 0.01). Peak tendon loading during late swing did not differ between age groups (mean 3.8 MPa in young and 4.2 MPa in older adults). These age-related alterations in tendon tissue loading may affect the mechanobiological stimuli underlying tissue remodeling and thereby alter the propensity for tendon injury and disease.

Achilles tendon shear wave speed tracks the dynamic modulation of standing balance.

Standing balance performance is often characterized by sway, as measured via fluctuations of the center of pressure (COP) under the feet. For example, COP metrics can effectively delineate changes in balance under altered sensory conditions. However, COP is a global metric of whole-body dynamics and thus does not necessarily lend insight into the underlying musculotendon control. We have previously shown that shear wave tensiometers can track wave speeds in tendon as a surrogate measure of the load transmitted by the muscle-tendon unit. The purpose of this study was to investigate whether shear wave metrics have sufficient sensitivity to track subtle variations in Achilles tendon loading that correspond with postural sway. Sixteen healthy young adults (26 ± 5 years) stood for 10 s with their eyes open and closed. We simultaneously recorded COP under the feet and shear wave speed in the right Achilles tendon. We found that Achilles tendon shear wave speed closely tracked (r > 0.95) dynamic fluctuations of the COP in the anteroposterior direction. Achilles tendon wave speed fluctuations significantly increased during standing with eyes closed, mirroring increases in COP fluctuations. These results demonstrate that tendon wave speed can track the subtle variations in Achilles tendon loading that modulate COP in standing. Hence, shear wave tensiometry exhibits the sensitivity to investigate the muscular control of quiet standing, and may also be useful for investigating other fine motor and force steadiness tasks.

Shear Wave Predictions of Achilles Tendon Loading during Human Walking.

The evaluation of in vivo muscle-tendon loads is fundamental to understanding the actuation of normal and pathological human walking. However, conventional techniques for measuring muscle-tendon loads in the human body are too invasive for use in gait analysis. Here, we demonstrate the use of noninvasive measures of shear wave propagation as a proxy for Achilles tendon loading during walking. Twelve healthy young adults performed isometric ankle plantarflexion on a dynamometer. Achilles tendon wave speed, tendon moment arms, tendon cross-sectional area and ankle torque were measured. We first showed that the linear relationship between tendon stress and wave speed squared can be calibrated from isometric tasks. There was no significant effect of knee angle, ankle angle or loading rate on the subject-specific calibrations. Calibrated shear wave tensiometers were used to estimate Achilles tendon loading when walking at speeds ranging from 1 to 2 m/s. Peak tendon stresses during pushoff increased from 41 to 48 MPa as walking speed was increased, and were comparable to estimates from inverse dynamics. The tensiometers also detected Achilles tendon loading of 4 to 7 MPa in late swing. Late swing tendon loading was not discernible in the inverse dynamics estimates, but did coincide with passive stretch of the gastrocnemius muscle-tendon units. This study demonstrates the capacity to use calibrated shear wave tensiometers to evaluate tendon loading in locomotor tasks. Such technology could prove beneficial for identifying the muscle actions that underlie subject-specific movement patterns.

Calibration of the shear wave speed-stress relationship in ex vivo tendons.

It has recently been shown that shear wave speed in tendons is directly dependent on axial stress. Hence, wave speed could be used to infer tendon load provided that the wave speed-stress relationship can be calibrated and remains robust across loading conditions. The purpose of this study was to investigate the effects of loading rate and fluid immersion on the wave speed-stress relationship in ex vivo tendons, and to assess potential calibration techniques. Tendon wave speed and axial stress were measured in 20 porcine digital flexor tendons during cyclic (0.5, 1.0 and 2.0 Hz) or static axial loading. Squared wave speed was highly correlated to stress (r2avg = 0.98) and was insensitive to loading rate (p = 0.57). The constant of proportionality is the effective density, which reflects the density of the tendon tissue and additional effective mass added by the adjacent fluid. Effective densities of tendons vibrating in a saline bath averaged 1680 kg/m3 and added mass effects caused wave speeds to be 22% lower on average in a saline bath than in air. The root-mean-square error between predicted and measured stress was 0.67 MPa (6.7% of maximum stress) when using tendon-specific calibration parameters. These errors increased to 1.31 MPa (13.1% of maximum stress) when calibrating based on group-compiled data from ten tendons. These results support the feasibility of calculating absolute tendon stresses from wave speed squared based on linear calibration relationships.

Gauging force by tapping tendons.

Muscles are the actuators that drive human movement. However, despite many decades of work, we still cannot readily assess the forces that muscles transmit during human movement. Direct measurements of muscle-tendon loads are invasive and modeling approaches require many assumptions. Here, we introduce a non-invasive approach to assess tendon loads by tracking vibrational behavior. We first show that the speed of shear wave propagation in tendon increases with the square root of axial stress. We then introduce a remarkably simple shear wave tensiometer that uses micron-scale taps and skin-mounted accelerometers to track tendon wave speeds in vivo. Tendon wave speeds are shown to modulate in phase with active joint torques during isometric exertions, walking, and running. The capacity to non-invasively assess muscle-tendon loading can provide new insights into the motor control and biomechanics underlying movement, and could lead to enhanced clinical treatment of musculoskeletal injuries and diseases.

In Vivo Measures of Shear Wave Speed as a Predictor of Tendon Elasticity and Strength.

The purpose of this study was to assess the potential for ultrasound shear wave elastography (SWE) to measure tissue elasticity and ultimate stress in both intact and healing tendons. The lateral gastrocnemius (Achilles) tendons of 41 New Zealand white rabbits were surgically severed and repaired with growth factor coated sutures. SWE imaging was used to measure shear wave speed (SWS) in both the medial and lateral tendons pre-surgery, and at 2 and 4 wk post-surgery. Rabbits were euthanized at 4 wk, and both medial and lateral tendons underwent mechanical testing to failure. SWS significantly (p < 0.001) decreased an average of 17% between the intact and post-surgical state across all tendons. SWS was significantly (p < 0.001) correlated with both the tendon elastic modulus (r = 0.52) and ultimate stress (r = 0.58). Thus, ultrasound SWE is a potentially promising non-invasive technology for quantitatively assessing the mechanical integrity of pre-operative and post-operative tendons.