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Clark WH and Franz JR, Triceps surae muscle-subtendon interaction differs between young and older adults. Connective Tissue Research. *Invited, Special Issue on Aging.

Abstract. Mechanical power generated via triceps surae muscle-tendon interaction during walking is largely responsible for the total power needed to walk. This interaction is made complex by the biological architecture of the Achilles tendon, which consists of distinct bundles of tendon fascicles, known as “subtendons”, arising from the lateral and medial gastrocnemius (GAS) and soleus (SOL) muscles. Comparative data and our own in vivo evidence allude to a reduced capacity for sliding between adjacent subtendons compromising the Achilles tendon in old age. This is functionally important, as subtendon sliding could facilitate independent actuation between individual triceps surae muscles, perhaps augmenting contributions to trunk support and forward propulsion. Recently, we revealed that length change differences between the GAS and SOL of young adults positively correlated with non-uniform subtendon tissue displacement patterns. Here, we investigated aging effects on triceps surae muscle-subtendon interaction using dual-probe ultrasound imaging during a series of ramped isometric contractions. We hypothesized that, compared to young adults, older adults would have more uniform subtendon tissue displacements that are accompanied by anatomically consistent differences in GAS versus SOL muscle length change behavior. Our findings fully supported our hypotheses. Older adults had more uniform subtendon tissue displacements that extended to anatomically consistent and potentially unfavorable changes in muscle contractile behavior – evidenced by smaller differences between GAS and SOL peak shortening during isometric force generation. These findings provide an important biomechanical basis for previously reported correlations between more uniform Achilles subtendon behavior and reduced ankle moment generation during waking in older adults.

Conway KA and Franz JR. Increasing the propulsive demands of walking to their maximum elucidates functionally limiting impairments in older adult gait. Journal of Aging and Physical Activity (In press).

Abstract. We elucidated functional limitations in older adult gait by increasing horizontal impeding forces and walking speed to their maximums compared to dynamometry and to data from their young counterparts. Specifically, we investigated which determinants of push-off intensity represent genuine functionally limiting impairments in older adult gait versus locomotor changes that simply present as age-related deficits in walking performance. We found that older adults walked at their preferred speed with hallmark deficits in push-off intensity. These subjects were fully capable of overcoming deficits in propulsive ground reaction force, trailing limb positive work, trailing leg and hip extension, and ankle power generation when the propulsive demands of walking were increased to maximum. Of the outcomes tested, age-related deficits in ankle moment emerged as the lone genuine functionally limiting impairment in older adults. Distinguishing genuine functional limitations from age-related differences masquerading as limitations represents a critical step toward the development and prescription of effective interventions.

Browne MG and Franz JR. Ankle power biofeedback attenuates the distal-to-proximal redistribution in older adults. Gait & Posture (In press).

Abstract:

Background: Compared to young adults, older adults walk slower, with shorter strides, and with a characteristic decrease in ankle power output. Seemingly in response, older adults rely more than young on hip power output, a phenomenon known as a distal-to-proximal redistribution. Nevertheless, older adults can increase ankle power to walk faster or uphill, revealing a translationally important gap in our understanding.

Research Question: Our purpose was to implement a novel ankle power biofeedback paradigm to encourage favorable biomechanical adaptations (i.e. reverse the distal-redistribution) during habitual speed walking in older adults.

Methods: 10 healthy older adults walked at their preferred speeds while real-time visual biofeedback provided target increases and decreases of 10 and 20% different from preferred ankle power. We evaluated the effect of changes in ankle power on joint kinetics, kinematics, and propulsive ground reaction forces. Pre and post overground walking speed assessments evaluated the effect of increased ankle power recall on walking speed.

Results: Biofeedback systematically elicited changes in ankle power; increasing and decreasing ankle power by 14% and 17% when targeting ±20% different from preferred, respectively. We observed a significant negative correlation between ankle power and hip extensor work. Older adults relied more heavily on changes in ankle angular velocity than ankle moment to modulate ankle power. Lastly, older adults walked almost 11% faster when recalling increased ankle power overground.

Significance: Older adults are capable of increasing ankle power through targeted ankle power biofeedback – effects that are accompanied by diminished hip power output and a reversal of the distal-to-proximal redistribution. The associated increase in preferred walking speed during recall suggests a functional benefit to increased ankle power output via transfer to overground walking. Further, our mechanistic insights allude to translational success using ankle angular velocity as a surrogate to modulate ankle power through biofeedback.

Congratulations to Michael Browne on successfully defending his dissertation, titled “Biofeedback to modulate push-off intensity in older adults: implications at the muscle, joint, limb, and whole-body levels.” Nice work, Dr. Browne!!

Clark WH and Franz JR. Activation-dependent changes in soleus length-tension behavior augment ankle joint quasi-stiffness. Journal of Applied Biomechanics (In press).

Abstract. The triceps surae muscle-tendon units are important in governing walking performance, acting to regulate mechanical behavior of the ankle through interaction between active muscle and passive elastic structures. Ankle joint quasi-stiffness (the slope of the relation between ankle moment and ankle rotation, k_A), is a useful aggregate measure of this mechanical behavior. However, the role of muscle activation and length-tension behavior in augmenting k_A remains unclear. Here, 10 subjects completed eccentric isokinetic contractions at rest and at two soleus activation levels (25% and 75% isometric voluntary contraction – IVC) prescribed using electromyographic biofeedback. Ultrasound imaging quantified activation-dependent modulation of soleus muscle length-tension behavior and its role in augmenting k_A. We found that soleus muscle stiffness (k_M) and k_A exhibit non-linear relations with muscle activation and were both more sensitive to the onset of activation than to subsequent increases in activation. Our findings also suggest that k_A can be modulated via activation through changes in soleus muscle length-tension behavior. However, this modulation is more complex than previously appreciated – reflecting interaction between active muscle and passive elastic tissues. Our findings may have implications for understanding normal and pathological ankle joint function and the design of impedance-based prostheses.

Waanders JB, Hortobágyi T, Murgia A, DeVita P, Franz JR. Advanced age redistributes positive but not negative leg joint work during walking. Medicine & Science in Sports & Exercise (In press).

Abstract. 

Introduction: Advanced age brings a distal-to-proximal redistribution of positive joint work during walking that is relevant to walking performance and economy. It is unclear whether negative joint work is similarly redistributed in old age. Negative work can affect positive work through elastic energy return in gait. We determined the effects of age, walking speed, and grade on positive and negative joint work in young and older adults.

Methods: Bilateral ground reaction force and marker data were collected from healthy young (age 22.5 years, n=18) and older (age 76.0 years, n=22) adults walking on a split-belt instrumented treadmill at 1.1, 1.4, and 1.7 m/s at each of three grades (0, 10, and -10%). Subjects also performed maximal voluntary eccentric, isometric, and concentric contractions for the knee extensors (120, 90, 0°/s) and plantarflexors (90, 30, 0°/s).

Results: Compared to young adults, older adults exhibited a distal-to-proximal redistribution of positive leg joint work during level (p<0.001) and uphill (p<0.001) walking, with larger differences at faster walking speeds. However, the distribution of negative joint work was unaffected by age during level (p=0.150) and downhill (p=0.350) walking. Finally, the age-related loss of maximal voluntary knee extensor (p<0.001) and plantarflexor (p=0.001) strength was lower during an eccentric contraction vs. concentric contraction for the knee extensors (p<0.001) but not for the plantarflexors (p=0.320).

Conclusion: The distal-to-proximal redistribution of positive joint work during level and uphill walking is absent for negative joint work during level and downhill walking. Exercise prescription should focus on improving ankle muscle function while preserving knee muscle function in older adults trying to maintain their independence.

Franz JR, Khanchandani A, McKenney H, Clark WH. Ankle rotation and muscle loading effects on the calcaneal tendon moment arm: an in vivo imaging and modeling study. Annals of Biomedical Engineering (In press).

 

Abstract. In this combined in vivo and computational modeling study, we tested the central hypothesis that ankle joint rotation and triceps surae muscle loading have independent and combinatory effects on the calcaneal (i.e., Achilles) tendon moment arm (CTma) that are not fully captured in contemporary musculoskeletal models of human movement. We used motion capture guided ultrasound imaging to estimate instantaneous variations in the CTma during a series of isometric and isotonic contractions compared to predictions from scaled, lower extremity computational models. As hypothesized, we found that muscle loading: (i) independently increased the CTma by up to 8% and (ii) attenuated the effects of ankle joint rotation, the latter likely through changes in tendon slack and tendon curvature. Neglecting the effects of triceps surae muscle loading in lower extremity models led to an underestimation of the CTma, on average, particularly in plantarflexion when those effects were most prominent. We also found little agreement between in vivo estimates and model predictions on an individual subject by subject basis, alluding to unaccounted for variation in anatomical morphology and thus fundamental limitations in model scaling. Together, these findings contribute to improving our understanding of the physiology of ankle moment and power generation and novel opportunities for model development.

 

Fickey SN, Browne MG, Franz JR. Biomechanical effects of augmented ankle power output during human walking. Journal of Experimental Biology (In press).

 

 

 

Abstract. The plantarflexor muscles are critical for forward propulsion and leg swing initiation during the push-off phase of walking, serving to modulate step length and walking speed. However, reduced ankle power output is common in aging and gait pathology and is considered a root biomechanical cause of compensatory increases in hip power generation and increased metabolic energy cost. There is a critical need for mechanistic insight into the precise influence of ankle power output on patterns of mechanical power generation at the individual joint and limb levels during walking. We also posit that rehabilitative approaches to improve locomotor patterns should consider more direct means to elicit favorable changes in ankle power output. Thus, here we used real-time inverse dynamics in a visual biofeedback paradigm to test young adults’ ability to modulate ankle power output during preferred speed treadmill walking, and the effects thereof on gait kinematics and kinetics. Subjects successfully modulated peak ankle power in response to biofeedback targets designed to elicit up to ±20% of normal walking values. Increasing ankle power output alleviated mechanical power demands at the hip and propagated to increased trailing limb positive work, propulsive ground reaction forces, and step lengths. Decreasing ankle power had the opposite effects. We conclude that ankle power generation systematically influences workload placed on more proximal leg muscles, trailing leg mechanical output, and step length. Our findings also provide a promising benchmark for the application of biofeedback to restore ankle power in individuals with deficits thereof due to aging and gait pathology.

The UNC/NCSU Applied Biomechanics Laboratory, in a great example of the inter-disciplinary nature of biomedical engineering and the impact of collaborative science, was recently awarded two new research grants from the National Institutes of Health.

First, in collaboration with the UNC Division of Geriatrics and Co-PI Dr. Gregory Sawicki in the Georgia W. Woodruff School of Mechanical Engineering at Georgia Tech, we will begin work on a new five-year NIH R01 to study (1) neuromechanical explanations for the greater metabolic energy cost of walking in older adults and (2) translation of that understanding to biologically-inspired wearable robotics for preserving independent mobility in our aging population. Ultimately, we hope to use ultrasound imaging to guide optimal prescription of assistive devices to improve locomotor function in aging – an outcome that will have significant positive impact on quality of life for millions.

Second, in collaboration with Co-PI Dr. Brian Pietrosimone in the UNC Department of Exercise and Sport Science, we will begin work on a new NIH R21 to study how altered lower extremity loading affects knee joint biomechanics, joint tissue biochemistry, cartilage deformation, and quadriceps muscle contractile behavior during walking in people following ACL reconstruction. By combining real-time biofeedback, ultrasound imaging, and biochemical markers, this study will be the first to determine the acute effects of joint loading on a collection of critical factors associated with the pathogenesis of post-traumatic osteoarthritis in a relevant patient population.

We are incredibly excited to continue our work with these exceptional groups of colleagues and collaborators.

Thompson JD, Plummer P, Franz JR. Age and falls history effects on antagonist leg muscle coactivation during walking with balance perturbations. Clinical Biomechanics.

 

 

 

 

Abstract. 

Background: Inspired by a reliance on visual feedback for movement control in older age, optical flow perturbations provide a unique opportunity to study the neuromuscular mechanisms involved in walking balance control, including aging and falls history effects on the response to environmental balance challenges. Specifically, antagonist leg muscle coactivation, which increases with age during walking, is considered a neuromuscular defense against age-associated deficits in balance control. The purpose of this study was to investigate the effects of age and falls history on antagonist leg muscle coactivation during walking with and without optical flow perturbations of different amplitudes.

Methods: Eleven young adults [mean (standard deviation) age: 24.8 (4.8) years], eleven older non-fallers [75.3 (5.4) years] and eleven older fallers [age: 78 (7.6) years] participated in this study. Participants completed 2-minute walking trials while watching a speed-matched virtual hallway that, in some conditions, included mediolateral optical flow perturbations designed to elicit the visual perception of imbalance.

Findings: We first found that lower leg antagonist muscle coactivation during normal walking increased with age, independent of falls history. We also found that older but not young adults increased antagonist leg muscle coactivation in the presence of optical flow perturbations, with more pervasive effects in older adults with a history of falls.

Interpretation: Our findings allude to a greater susceptibility to optical flow perturbations in older fallers during walking, which points to a higher potential for risk of instability in more complex and dynamic everyday environments. These findings may also have broader impacts related to the design of innovative training paradigms and neuromuscular targets for falls prevention.