The Metabolic Cost of Walking Balance Control and Adaptation in Young Adults.

Shawn Ahuja and Jason R. Franz

Background: Our aim was to quantify the role of metabolic energy cost in governing neuromuscular adaptation to prolonged exposure to optical flow walking balance perturbations in young adults. Research Question: We hypothesized that metabolic cost would increase at the onset of balance perturbations in a manner consistent with wider and shorter steps and increased step-to-step variability. We also hypothesized that metabolic cost would decrease with prolonged exposure in a manner consistent with a return of step width and step length to values seen during normal, unperturbed walking. Methods: Healthy young adults (n=18) walked on a treadmill while viewing a virtual hallway. Optical flow balance perturbations were introduced over a 10-minute interval during a 20-minute walking bout while measuring step kinematics and metabolic energy cost. For all outcome measures, we computed average values during the following four time periods of interest: Pre (minutes 3-5), Early Perturbation (minutes 5-7), Late Perturbation (minutes 13-15), and Post (minutes 18-20). A repeated-measures ANOVA tested for main effects of time, following by post-hoc pairwise comparisons. Results: With the onset of perturbations, participants walked with 3% shorter, 17% wider, and 53-73% more variable steps. These changes were accompanied by a significant 12% increase in net metabolic power compared to walking normally. With prolonged exposure to perturbations, step width and step length tended toward values seen during normal, unperturbed walking – changes accompanied by a 5% reduction in metabolic power (p-values≤0.05). Significance: Our study reveals that the adoption of generalized anticipatory control at the onset of optical flow balance perturbations and the subsequent shift to task-specific reactive control following prolonged exposure have meaningful metabolic consequences. Moreover, our findings suggest that metabolic energy cost may shape the strategies we use to adapt walking balance in response to perturbations.

Our lab had a wonderful time attending our regional ASB meeting here at UNC Chapel Hill. Really inclusive meeting with especially great opportunities for undergraduate biomechanists. Our triangle-area ASB student chapter was well represented as well! Congratulations to Ricky Pimentel, Andy Shelton, Mandy Munsch, Jordan Feldman, and Ellie McTaggart for their terrific presentations.

Our laboratory was recently awarded two pilot grants from the UNC Thurston Arthritis Research Center (TARC). The awards will accelerate new interdisciplinary lines of research into: (i) the association between muscle action, inflammatory biomarkers, and cartilage loading during walking in people with osteoarthritis, and (ii) precision medicine approaches for individualized gait retraining to mitigate osteoarthritis. Our team science approach formally integrates biomedical engineering, exercise and sport science, orthopaedics, and rheumatology, allergy and immunology. Thanks for the support!

Our Applied Biomechanics Laboratory was notified this summer that two laboratory members were selected as the two finalists for the 2021 Journal of Biomechanics Award at this year’s American Society of Biomechanics (ASB) meeting. Both finalists, BME Senior Callum J. Funk (Exploring the functional boundaries and metabolism of triceps surae force-length relations during walking) and UNC Medical Student Shawn Ahuja (The metabolic cost of walking balance control and adaptation in young adults) were invited to deliver a podium presentation at the annual virtual meeting in August. In the conference’s closing ceremony, it was announced that Funk had won the prestigious Award.

The Journal of Biomechanics Award recognizes substantive and conceptually novel mechanics approaches explaining how biological systems function. It is one of the highest honors at the ASB conference. Many Congratulations to Funk and his coauthors (BME post-doc Rebecca Krupenevich, Georgia Tech faculty Gregory Sawicki, and senior author Jason Franz), as well as to finalist Shawn Ahuja for delivering exceptional presentations!

Age-related differences in calf muscle recruitment strategies in the time-frequency domain during walking as a function of task demand

Hoon Kim and Jason R. Franz

ABSTRACT

Activation of the plantar flexors is critical in governing ankle push-off power during walking, which decreases due to age. However, electromyographic (EMG) signal amplitude alone are unable to fully characterize motor unit recruitment during functional activity.  Although not yet studied in walking, EMG frequency content may also vary due to age-related differences in muscle morphology and neural signaling. Our purpose was to quantify plantar flexor activation differences in the time-frequency domain between young and older adults during walking across a range of speeds and with and without horizontal aiding and impeding forces. Ten healthy young (24.0±3.4 years) and older adults (73.7±3.9 years) walked at three speeds and walked with horizontal aiding and impeding force while muscle activations of soleus (SOL) and gastrocnemius (GAS) were recorded. The EMG signals were decomposed in the time-frequency domain with wavelet transformation. Principal component analyses extracted principal components (PC) and PC scores. Compared to young adults, we observed that GAS activation in older adults: 1) was lower across all frequency ranges during midstance and in slow to middle frequency ranges during push-off, independent of walking speed, and 2) shifted to slower frequencies with earlier timing as walking speed increased. Our results implicate GAS time-frequency content, and its morphological and neural origins, as a potential determinant of hallmark ankle push-off deficits due to aging, particularly at faster walking speeds. Rehabilitation specialists may attempt to restore GAS intensity across all frequency ranges during mid to late stance while avoiding disproportionate increases in slower frequencies during early stance.

The Effects of Triceps Surae Muscle Stimulation on Localized Achilles Subtendon Tissue Displacements

Nathan L. Lehr, William H. Clark, Michael D. Lewek, Jason R. Franz

Abstract. The triceps surae muscle tendon unit is comprised of the lateral and medial gastrocnemius (MG) and soleus (SOL) muscles and three in series elastic “subtendons” that form the Achilles tendon. Comparative literature and our own in vivo evidence suggests that sliding between adjacent subtendons may facilitate independent muscle actuation. We aim to more clearly define the relation between individual muscle activation and subtendon tissue displacements. Here, during fixed-end contractions, electrical muscle stimulation controlled the magnitude of force transmitted via individual triceps surae muscles while ultrasound imaging recorded resultant subtendon tissue displacements. We hypothesized that MG and SOL stimulation would elicit larger displacements in their associated subtendon. 10 young adults completed 4 experimental activations at 3 ankle angles (-20°, 0°, 20°) with knee flexed to approximately 20°: MG stimulation (STIM_MG), SOL stimulation (STIM_SOL), combined stimulation, and volitional contraction. At 20° plantarflexion, STIM_SOL elicited 49% larger tendon non-uniformity (SOL – MG subtendon tissue displacement) than that of STIM_MG (p=0.004). For STIM_SOL, a one-way post-hoc ANOVA revealed a significant main effect of ankle angle (p=0.009) on Achilles tendon non-uniformity. However, peak tendon non-uniformity decreased by an average of 61% from plantarflexion to dorsiflexion, likely due to an increase in passive tension. Our results suggest that localized tissue displacements within the Achilles tendon respond in anatomically consistent ways to differential patterns of triceps surae muscle activation, but these relations are highly susceptible to ankle angle. This in vivo evidence points to at least some mechanical independence in actuation between the human triceps surae muscle-subtendon units.

Effects of age and locomotor demand on foot mechanics during walking.

Rebecca L. Krupenevich, Samuel F. Ray, Howard E. Kashefsky, Kota Z. Takahashi, Jason R. Franz

Abstract. Older adults exhibit reductions in trailing leg push-off power that are often attributed to deficits in plantarflexor force-generating capacity. However, growing evidence suggests that the foot may also contribute to push-off power during walking. Thus, age-related changes in foot structure and function may contribute to altered foot mechanics and ultimately reduced push-off power. The purpose of this paper was to quantify age-related differences in foot mechanical work during walking across a range of speeds and, at a single fixed speed with varied demands for trailing leg push-off.  9 young and 10 older adults walked at 1.0, 1.2, and 1.4 m/s, and at 1.2 m/s with an aiding or impeding horizontal pulling force equal to 5% BW. We calculated foot work in Visual3D using a unified deformable foot model, accounting for contributions of structures distal to the hindfoot’s center-of-mass. Older adults walked while performing less positive foot work and more negative net foot work (p<0.05). Further, we found that the effect of age on mechanical work performed by the foot and the ankle-foot complex increased with increased locomotor demand (p<0.05). Our findings suggest that during walking, age-related differences in foot mechanics may contribute to reduced push-off intensity via greater energy loss from distal foot structures, particularly during walking tasks with a greater demand for foot power generation. These findings are the first step in understanding the role of the foot in push-off power deficits in older adults and may serve as a roadmap for developing future low-cost mobility interventions.

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.