Laura C. Slane

Non-uniform in vivo deformations of the human Achilles tendon during walking.

The free Achilles tendon (AT) consists of distinct fascicles arising from each of the triceps surae muscles that may give rise to non-uniform behavior during functional tasks such as walking. Here, we estimated in vivo deformations of the human AT during walking using simultaneous ultrasound and motion capture measurements. Ten subjects walked at three speeds (0.75, 1.00, and 1.25 m/s) on a force-measuring treadmill. A custom orthotic secured a linear array transducer in two locations: (1) the distal lateral gastrocnemius muscle-tendon junction and (2) the free AT, on average centered 6 cm superior to calcaneal insertion. We used motion capture to record lower extremity kinematics and the position and orientation of the ultrasound transducer. A 2D ultrasound elastography algorithm tracked superficial and deep tissue displacements within the free AT. We estimated AT elongation (i.e., change in length) relative to the calcaneal insertion by transforming the orthotic, transducer, and calcaneus kinematics into a common reference frame. Superficial and deep regions of the free AT underwent significantly different longitudinal displacements and elongations during walking. For example, we found that the superficial AT exhibited 16-29% greater peak elongation than the deep AT during the stance phase of walking (p < 0.01). Moreover, superficial-deep AT tissue deformations became less uniform with faster walking speed (p < 0.01). Non-uniform deformations of the free AT, which could reflect inter-fascicle sliding, may enable the gastrocnemius and soleus muscles to transmit their forces independently while allowing unique kinematic behavior at the muscle fiber level.

Spatial variations in Achilles tendon shear wave speed

Supersonic shear imaging (SSI) is an ultrasound imaging modality that can provide insight into tissue mechanics by measuring shear wave propagation speed, a property that depends on tissue elasticity. SSI has previously been used to characterize the increase in Achilles tendon shear wave speed that occurs with loading, an effect attributable to the strain-stiffening behavior of the tissue. However, little is known about how shear wave speed varies spatially, which is important, given the anatomical variation that occurs between the calcaneus insertion and the gastrocnemius musculotendon junction. The purpose of this study was to investigate spatial variations in shear wave speed along medial and lateral paths of the Achilles tendon for three different ankle postures: resting ankle angle (R, i.e. neutral), plantarflexed (P; R - 15°), and dorsiflexed (D; R+15°). We observed significant spatial and posture variations in tendon shear wave speed in ten healthy young adults. Shear wave speeds in the Achilles free tendon averaged 12 ± 1.2m/s in a resting position, but decreased to 7.2 ± 1.8m/s with passive plantarflexion. Distal tendon shear wave speeds often reached the maximum tracking limit (16.3m/s) of the system when the ankle was in the passively dorsiflexed posture (+15° from R). At a fixed posture, shear wave speeds decreased significantly from the free tendon to the gastrocnemius musculotendon junction, with slightly higher speeds measured on the medial side than on the lateral side. Shear wave speeds were only weakly correlated with the thickness and depth of the tendon, suggesting that the distal-to-proximal variations may reflect greater compliance in the aponeurosis relative to the free tendon. The results highlight the importance of considering both limb posture and transducer positioning when using SSI for biomechanical and clinical assessments of the Achilles tendon.

Non-uniform displacements within the Achilles tendon observed during passive and eccentric loading

The goal of this study was to investigate Achilles tendon tissue displacement patterns under passive and eccentric loading conditions. Nine healthy young adults were positioned prone on an examination table with their foot secured to a rotating footplate aligned with the ankle. Subjects cyclically rotated their ankle over a 25° range of motion at 0.5 Hz. An inertial load geared to the footplate induced eccentric plantarflexor contractions with dorsiflexion. Passive cyclic ankle motion was also performed over the same angular range of motion. An ultrasound transducer positioned over the distal Achilles tendon was used to collect radiofrequency (RF) images at 70 frames/s. Two-dimensional ultrasound elastographic analysis of the RF data was used to track tendon tissue displacements throughout the cyclic motion. Non-uniform tissue displacement patterns were observed in all trials, with the deeper portions of the Achilles tendon consistently exhibiting larger displacements than the superficial tendon (average of 0.9-2.6mm larger). Relative to the passive condition, eccentric loading consistently induced smaller tissue displacements in all tendon regions, except for the superficial tendon in a flexed knee posture. Significantly greater overall tissue displacement was observed in a more extended knee posture (30°) relative to a flexed knee posture (90°). These spatial- and posture-dependent displacement patterns suggest that the tendon undergoes non-uniform deformation under in vivo loading conditions. Such behavior could reflect relative sliding between the distinct tendon fascicles that arise from the gastrocnemius and soleus muscles.

The Use of 2D Ultrasound Elastography for Measuring Tendon Motion and Strain

The goal of the current study was to investigate the fidelity of a 2D ultrasound elastography method for the measurement of tendon motion and strain. Ultrasound phantoms and ex vivo porcine flexor tendons were cyclically stretched to 4% strain while cine ultrasound radiofrequency (RF) data and video data were simultaneously collected. 2D ultrasound elastography was used to estimate tissue motion and strain from RF data, and surface tissue motion and strain were separately estimated using digital image correlation (DIC). There were strong correlations (R(2)>0.97) between DIC and RF measurements of phantom displacement and strain, and good agreement in estimates of peak phantom strain (DIC: 3.5±0.2%; RF: 3.7±0.1%). For tendon, elastographic estimates of displacement profiles also correlated well with DIC measurements (R(2)>0.92), and exhibited similar estimated peak tendon strain (DIC: 2.6±1.4%; RF: 2.2±1.3%). Elastographic tracking with B-Mode images tended to under-predict peak strain for both the phantom and tendon. This study demonstrates the capacity to use quantitative elastographic techniques to measure tendon displacement and strain within an ultrasound image window. The approach may be extendible to in vivo use on humans, which would allow for the non-invasive analysis of tendon deformation in both normal and pathological states.

Achilles tendon displacement patterns during passive stretch and eccentric loading are altered in middle-aged adults

The purpose of this study was to investigate middle-age effects on Achilles displacement patterns under passive stretch and eccentric loading. Healthy young (24.1 ± 1.4 years, n = 9) and middle-aged (49.0 ± 3.1 years, n = 9) adults were positioned prone and the ankle was cyclically dorsiflexed (0.5 Hz, 25° range) during passive stretch and active lengthening. Achilles displacements were tracked in cine ultrasound using 2D speckle tracking. Displacements were found to be non-uniform, with mid and deep portions of the tendon displacing more than superficial portions. However, the degree of non-uniformity was significantly reduced in middle-aged adults, suggesting a potential age-related reduction in inter-fascicle sliding or a shift in loading sharing between plantarflexors. Eccentric loading reduced displacement magnitudes, likely reflecting distal tendon stretch induced via active muscle contractions. Changes in tendon displacement with active loading were greater in middle-aged adults, which could reflect greater tendon compliance. The observed age-related changes in Achilles tendon behavior may have implications for both plantarflexor performance and injury risk.

A 3D model of the Achilles tendon to determine the mechanisms underlying nonuniform tendon displacements

The Achilles is the thickest tendon in the body and is the primary elastic energy-storing component during running. The form and function of the human Achilles is complex: twisted structure, intratendinous interactions, and differential motor control from the triceps surae muscles make Achilles behavior difficult to intuit. Recent in vivo imaging of the Achilles has revealed nonuniform displacement patterns that are not fully understood and may result from complex architecture and musculotendon interactions. In order to understand which features of the Achilles tendon give rise to the nonuniform deformations observed in vivo, we used computational modeling to predict the mechanical contributions from different features of the tendon. The aims of this study are to: (i) build a novel computational model of the Achilles tendon based on ultrashort echo time MRI, (ii) compare simulated displacements with published in vivo ultrasound measures of displacement, and (iii) use the model to elucidate the effects of tendon twisting, intratendon sliding, retrocalcaneal insertion, and differential muscle forces on tendon deformation. Intratendon sliding and differential muscle forces were found to be the largest factors contributing to displacement nonuniformity between tendon regions. Elimination of intratendon sliding or muscle forces reduced displacement nonuniformity by 96% and 85%, respectively, while elimination of tendon twist and the retrocalcaneal insertion reduced displacement nonuniformity by only 35% and 3%. These results suggest that changes in the complex internal structure of the tendon alter the interaction between muscle forces and tendon behavior and therefore may have important implications on muscle function during movement.

Middle-aged adults exhibit altered spatial variations in Achilles tendon wave speed

The purpose of this study was to investigate spatial variations in measured wave speed in the relaxed and stretched Achilles tendons of young and middle-aged adults. Wave speed was measured from the distal Achilles tendon, soleus aponeurosis, medial gastrocnemius aponeurosis and medial gastrocnemius muscle in healthy young (n = 15, aged 25   ±   4 years) and middle-aged (n = 10, aged 49   ±   4 years) adults in resting, dorsiflexed and plantarflexed postures. In both age groups, Achilles tendon wave speed decreased proximally, with the lowest wave speed measured in the gastrocnemius aponeurosis. Measured wave speed increased with passive dorsiflexion, reflecting the strain-stiffening behavior of tendons. There were no significant aging effects on wave speed in the free tendon or soleus aponeurosis. However, a significant, inverse relationship between gastrocnemius aponeurosis wave speed and age was observed in the dorsiflexed posture. We also observed significantly lower wave speeds in the gastrocnemius muscles of middle-aged adults when compared with young adults. These results suggest that Achilles tendon compliance increases in a distal-to-proximal pattern, with middle-aged adults exhibiting greater compliance in the distal gastrocnemius muscle and tendinous structures. An age-related change in the spatial variation in Achilles tendon compliance could affect localized tissue deformation patterns and injury potential within the triceps surae muscle-tendon units.

Evidence of patellar tendon buckling during passive knee extension

PURPOSE The purpose of this study was to investigate and describe buckling of the patellar tendon. METHODS Healthy young adults (28±4years, 10F/10M) underwent passive knee flexion/extension during the simultaneous measurement of knee angle and collection of cine ultrasound from the patellar tendon. Patellar tendon buckling was observed visually in ultrasound images, and the corresponding knee angle at which evidence of buckling disappeared was identified. RESULTS All subjects showed evidence of distal buckling which occurred on average at 23±8° flexion. Proximal buckling was only observed in fourteen subjects (10F/4M) at an average of 15±8°. Buckling patterns varied between subjects, but with high within-subject consistency. Buckling magnitude increased with age (p=0.03) and decreased with more weekly exercise (p=0.02). DISCUSSION The patellar tendon exhibited significant buckling in knee extension suggesting that buckling is a component of healthy knee function. Like tendon crimp, buckling may serve as a protective mechanism, allowing the tissue to unwrinkle prior to undergoing pure strain. The links between increased buckling magnitude and both age and reduced activity suggest that excessive buckling may be maladaptive, though future work is necessary to elucidate this relationship. Buckling is relevant to consider when estimating tendon length, as buckling can lead to significant underestimation of resting length and thus overestimation of strain. CONCLUSION This study demonstrates the complexity of tendon behavior even in healthy adults undergoing passive motion, suggesting that buckling may be relevant to an improved understanding of tendon health and pathology.

Non-uniform Deformation of the Patellar Tendon During Passive Knee Flexion

The purpose of this study was to evaluate localized patterns of patellar tendon deformation during passive knee flexion. Ultrasound radiofrequency data were collected from the patellar tendons of 20 healthy young adults during knee flexion over a range of motion of 50°-90° of flexion. A speckle tracking approach was used to compute proximal and distal tendon displacements and elongations. Nonuniform tissue displacements were visible in the proximal tendon (P < .001), with the deep tendon undergoing more distal displacement than the superficial tendon. In the distal tendon, more uniform tendon motion was observed. Spatial variations in percent elongation were also observed, but these varied along the length of the tendon (P < .002), with the proximal tendon remaining fairly isometric while the distal tendon underwent slight elongation. These results suggest that even during passive flexion the tendon undergoes complex patterns of deformation. Proximal tendon nonuniformity may arise from its complex anatomy where the deep tendon inserts onto the patella and the superficial tendon extends to the quadriceps tendon. Such heterogeneity is not captured in whole tendon average assessments, emphasizing the relevance of considering localized tendon mechanics, which may be key to understanding tendon behavior and precursors to injury and disease.

The challenges of measuring in vivo knee collateral ligament strains using ultrasound

Ultrasound-based methods have shown promise in their ability to characterize non-uniform deformations in large energy-storing tendons such as the Achilles and patellar tendons, yet applications to other areas of the body have been largely unexplored. The noninvasive quantification of collateral ligament strain could provide an important clinical metric of knee frontal plane stability, which is relevant in ligament injury and for measuring outcomes following total knee arthroplasty. In this pilot cadaveric experiment, we investigated the possibility of measuring collateral ligament strain with our previously validated speckle-tracking approach, but encountered a number of challenges during both data acquisition and processing. Given the clinical interest in this type of tool, and the fact that this is a developing area of research, the goal of this article is to transparently describe this pilot study, both in terms of methods and results, while also identifying specific challenges to this work and areas for future study. Some challenges faced relate generally to speckle-tracking of soft tissues (e.g. the limitations of using a 2D imaging modality to characterize 3D motion), while others are specific to this application (e.g. the small size and complex anatomy of the collateral ligaments). This work illustrates a clear need for additional studies, particularly relating to the collection of ground-truth data and more thorough validation work. These steps will be critical prior to the translation of ultrasound-based measures of collateral ligament strains into the clinic.