Reduced Achilles tendon stiffness disrupts calf muscle neuromechanics in elderly gait (Review article)

Rebecca L. Krupenevich, Owen N. Beck, Gregory S. Sawicki, Jason R. Franz

Abstract. Older adults walk slower and with higher metabolic energy expenditure than young adults. We hypothesize that age-related declines in Achilles tendon stiffness increase the metabolic cost of walking due to less economical calf muscle contractions and increased proximal joint work. This viewpoint may motivate interventions to restore ankle muscle-tendon stiffness, improve walking mechanics, and reduce metabolic cost in older adults.

Summary: Age-related declines in Achilles tendon stiffness increase the metabolic cost of walking due to less economical calf muscle contractions and increased proximal joint work.

Mandy Munsch, third year BME PhD candidate, has received an NIH National Research Service Award from the National Institute of Arthritis and Musculoskeletal and Skin Diseases. The award will fund her project titled “Effects of anterior cruciate ligament reconstruction on the association between quadriceps muscle dynamics, knee joint biomechanics, and articular cartilage loading during walking.” The research will evaluate how systematic changes in quadriceps activation and knee joint biomechanics affect cartilage contact forces and will improve our understanding of osteoarthritis development following knee joint injuries. Mandy will be advised by Dr. Jason Franz, Associate Professor in BME, and co-advised by Dr. Brian Pietrosimone, Associate Professor from UNC’s Department of Exercise and Sports Science.

Congratulations on this prestigious early career recognition!

Automated Analysis of Medial Gastrocnemius Muscle-Tendon Junction Displacements During Isolated Contractions and Walking Using Deep Neural Networks.

Rebecca L. Krupenevich, Callum J. Funk, Jason R. Franz

Abstract

Background and objective: Direct measurement of muscle-tendon junction (MTJ) position is important for understanding dynamic tendon behavior and muscle-tendon interaction in healthy and pathological populations. Traditionally, obtaining MTJ position during functional activities is accomplished by manually tracking the position of the MTJ in cine B-mode ultrasound images – a laborious and time-consuming process. Recent advances in deep learning have facilitated the availability of user-friendly open-source software packages for automated tracking. However, these software packages were originally intended for animal pose estimation and have not been widely tested on ultrasound images. Therefore, the purpose of this paper was to evaluate the efficacy of deep neural networks to accurately track medial gastrocnemius MTJ positions in cine B-mode ultrasound images across tasks spanning controlled loading during isolated contractions to physiological loading during treadmill walking.

Methods: Cine B-mode ultrasound images of the medial gastrocnemius MTJ were collected from 15 subjects (6M/9F, 23 yr, 71.9 kg, 1.8 m) during treadmill walking at 1.25 m/s and during maximal voluntary isometric plantarflexor contractions (MVICs). Five deep neural networks were trained using 480 manually labeled images, defined as the ground truth, collected during walking, and were then used to predict MTJ position in images from novel subjects 1) during walking (novel-subject), and 2) during MVICs (novel-condition).

Results: We found an average mean absolute error of 1.26±1.30 mm and 2.61±3.31 mm between the ground truth and predicted MTJ positions in the novel-subject and novel-condition evaluations, respectively.

Conclusions: Our results provide support for the use of open-source software for creating deep neural networks to reliably track MTJ positions in B-mode ultrasound images. We believe this approach to MTJ position tracking is an accessible and time-saving solution, with broad applications for many fields, such as rehabilitation or clinical diagnostics.

Open source access to computational resources supported by this paper can be found here.

The metabolic and mechanical consequences of altered propulsive force generation in walking.

Noah L. Pieper,  Sidney T. Baudendistel, Chris J. Hass, Gabriela B. Diaz, Rebecca L. Krupenevich, Jason R. Franz

Abstract. Older adults walk with greater metabolic energy consumption than younger for reasons that are not well understood. We suspect that a distal-to-proximal redistribution of leg muscle demand, from muscles spanning the ankle to those spanning the hip, contributes to greater metabolic energy costs. Recently, we found that when younger adults using biofeedback target smaller than normal peak propulsive forces (F_P), they do so via a similar redistribution of leg muscle demand during walking. This alludes to an experimental paradigm that emulates characteristics of elderly gait independent of other age-related changes relevant to metabolic energy cost.  Thus, our purpose was to quantify the metabolic and limb- and joint-level mechanical energy costs associated with modulating propulsive forces during walking in younger adults.  Walking with larger F_P increased net metabolic power by 47% (main effect, p=0.001), which was accompanied by small but relatively uniform increases in hip, knee, and ankle joint power and which correlated with total joint power (R²=0.151, p=0.019). Walking with smaller F_P increased net metabolic power by 58% (main effect, p<0.001), which was accompanied by higher step frequencies and increased total joint power due to disproportionate increases in hip joint power. Increases in hip joint power when targeting smaller than normal F_P accounted for more than 65% of the variance in the measured changes in net metabolic power. Our findings suggest that walking with a diminished push-off exacts a metabolic penalty because of higher step frequencies and more total limb work due to an increased demand on proximal leg muscles.

Muscle metabolic energy costs while modifying propulsive force generation during walking.

Ricky R. Pimentel, Noah L. Pieper, Billy H. Clark, Jason R. Franz.

Computer Methods in Biomechanics and Biomedical Engineering.

Abstract. We pose that an age-related increase in the metabolic cost of walking arises in part from a redistribution of joint power where muscles spanning the hip compensate for insufficient ankle push-off and smaller peak propulsive forces (F_P). Young adults elicit a similar redistribution when walking with smaller F_P via biofeedback. We used targeted F_P biofeedback and musculoskeletal models to estimate the metabolic costs of operating lower limb muscles in young adults walking across a range of F_P. Our simulations support the theory of distal-to-proximal redistribution of joint power as a determinant of increased metabolic cost in older adults during walking.

We are very proud to congratulate Billy Clark for successfully defending his PhD dissertation, titled “Interaction between triceps surae muscles and the Achilles tendon in young and older adults: mechanisms and functional consequences”. Outstanding job! We also thank the wonderful support of his committee members, Drs. Xiaogang Hu (UNC/NCSU BME), Mike Lewek (UNC PT), Kate Saul (NCSU MAE), and Eric Ryan (UNC EXSS). Billy will be starting a position as a post-doc in the Department of Ecology and Evolutionary Biology at Browne University working under the mentorship of Dr. Tom Roberts. Big things ahead!!

The effects of a 6-week horizontal impeding force gait training protocol on push-off intensity in older adults

Conway KA, Crudup KL, Lewek MD, Franz JR

Abstract. Aging and many gait pathologies are often characterized by deficits in push-off intensity (i.e., propulsive ground reaction forces and peak ankle moment and power output) during walking. Unfortunately, conventional interventions such as progressive resistance training, designed to enhance calf muscle mechanical output, generally fail to translate strength gains to functional improvements in habitual push-off intensity. Methods: Horizontal impeding forces applied to the body’s center of mass systematically augment the mechanical output required from muscle-tendon units spanning the ankle during the push-off phase of walking, which could convey long-term benefits via training. Therefore, the purpose of this study was to investigate the preliminary efficacy of a 6-week horizontal impeding force training paradigm on improving habitual push-off intensity in 11 healthy but not physically active older adults (age: 76±4 years, 6F/5M). Results: We found that older adults significantly (p<0.05) increased measures of isometric strength by 18%, maximum walking speed by 10%, and 6-minute walk test distance by 9% as a result of horizontal impeding force training. As a more clinically significant contribution of this work, we found that those subjects also increased habitual peak ankle moment and peak ankle power during push-off following training by a significant 10% and 15%, respectively (p≤0.036). Conclusions: We conclude that the use of horizontal impeding forces in older adults improves their maximum muscular and walking capacities while encouraging access to newfound strength gains, thereby improving habitual push-off intensity during walking.

Imaging and simulation of inter-muscular differences in triceps surae contributions to forward propulsion during walking.

Clark WH, Pimentel RE, Franz JR.

Abstract. Forward propulsion during the push-off phase of walking is largely governed at the ankle by differential neuromechanical contributions from the biarticular medial (MG) and lateral gastrocnemii (LG) and the uniarticular soleus (SOL). However, the relative contribution of these individual muscles to forward propulsion is equivocal, with important implications for the design and control of wearable assistive devices and for targeted therapeutics. The aim of this study was to evaluate the agreement between empirical and model-predicted triceps surae contributions to forward propulsion during walking using conditions that systematically manipulated both walking speed and the mechanical demand for forward propulsion at a fixed speed – through the use of aiding and impeding forces. Ten young adults (age: 24.1 ± 3.6 years, 6M/4F) participated. We found that muscle-specific responses derived from experimental measurements (i.e., activation and fascicle behavior) were consistent with those derived from musculoskeletal simulations (i.e., muscle force and positive mechanical work) within the same subjects. In vivo, compared to walking normally, only LG muscle activation was affected by both aiding and impeding forces. Similarly, increased propulsive demand elicited greater relative fascicle shortening in the MG but not the SOL. In silico, only MG and LG force and positive mechanical work increased significantly to meet the increased demands for forward propulsion. By combining electromyography, ultrasound imaging, and musculoskeletal modeling in the same subjects, our cumulative findings suggest that the biarticular gastrocnemius muscles play a more significant role than the uniarticular soleus in governing changes in forward propulsion during the mid to late stance phase of walking.

The effects of knee extensor moment biofeedback on gait biomechanics and quadriceps contractile behavior

Munsch AE, Pietrosimone B, Franz JR

Abstract. Individuals with knee joint pathologies exhibit quadriceps dysfunction that, during walking, manifests as smaller peak knee extensor moment (pKEM) and reduced knee flexion excursion. These changes persist despite muscle strengthening and may alter stance phase knee joint loading considered relevant to osteoarthritis risk. Novel rehabilitation strategies that more directly augment quadriceps mechanical output during functional movements are needed to reduce this risk. As an important first step, we tested the efficacy of real-time biofeedback during walking to prescribe changes of ±20% and ±40% of normal walking pKEM values in 11 uninjured young adults. We simultaneously recorded knee joint kinematics, ground reaction forces, and, via ultrasound, vastus lateralis (VL) fascicle length change behavior. Participants successfully responded to real-time biofeedback and averaged up to 55% larger and 51% smaller than normal pKEM values with concomitant and potentially favorable changes in knee flexion excursion. While the VL muscle-tendon unit (MTU) lengthened, VL fascicles accommodated weight acceptance during walking largely through isometric, or even slight concentric, rather than eccentric action as is commonly presumed. Targeted pKEM biofeedback may be a useful rehabilitative and/or scientific tool to elicit desirable changes in knee joint biomechanics considered relevant to the development of osteoarthritis.

Older adults overcome reduced triceps surae structural stiffness to preserve ankle joint quasi-stiffness during walking.

Krupenevich RL, Clark WH, Sawicki GS, Franz JR.

Abstract. Ankle joint quasi-stiffness is an aggregate measure of the interaction between triceps surae muscle stiffness and Achilles tendon stiffness. This interaction may be altered due to age-related changes in the structural properties and functional behavior of the Achilles tendon and triceps surae muscles. We hypothesized that, due to a more compliant Achilles’ tendon, older adults would exhibit lower ankle joint quasi-stiffness than young adults, during walking and during isolated contractions at matched triceps surae muscle activations. We also hypothesized that, independent of age, triceps surae muscle stiffness and ankle joint quasi-stiffness would increase with triceps surae muscle activation. We used conventional gait analysis in one experiment and, in another, electromyographic biofeedback and in vivo ultrasound imaging applied during isolated contractions. We found no difference in ankle joint quasi-stiffness between young and older adults during walking. Conversely, we found that: (i) young and older adults modulated ankle joint quasi-stiffness via activation-dependent changes in triceps surae muscle length-tension behavior, and (ii) at matched activation, older adults exhibited lower ankle joint quasi-stiffness than young adults. Despite age-related reductions during isolated contractions, ankle joint quasi-stiffness was maintained in older adults during walking – which may be governed via activation-mediated increases in muscle stiffness.