The Simultaneous Model-Based Estimation of Joint, Muscle, and Tendon Stiffness is Highly Sensitive to the Tendon Force-Strain Relationship.

OBJECTIVE: Accurate estimation of stiffness across anatomical levels (i.e., joint, muscle, and tendon) in vivo has long been a challenge in biomechanics. Recent advances in electromyography (EMG)-driven musculoskeletal modeling have allowed the non-invasive estimation of stiffness during dynamic joint rotations. Nevertheless, validation has been limited to the joint level due to a lack of simultaneous in vivo experimental measurements of muscle and tendon stiffness. METHODS: With a focus on the triceps surae, we employed a novel perturbation-based experimental technique informed by dynamometry and ultrasonography to derive reference stiffness at the joint, muscle, and tendon levels simultaneously. Here, we propose a new EMG-driven model-based approach that does not require external joint perturbation, nor ultrasonography, to estimate multi-level stiffness. We present a novel set of closed-form equations that enables the person-specific tuning of musculoskeletal parameters dictating biological stiffness, including passive force-length relationships in modeled muscles and tendons. RESULTS: Calibrated EMG-driven musculoskeletal models estimated the reference data with average normalized root-mean-square error ≈ 20%. Moreover, only when calibrated tendons were approximately four times more compliant than typically modeled, our approach could estimate multi-level reference stiffness. CONCLUSION: EMG-driven musculoskeletal models can be calibrated on a larger set of reference data to provide more realistic values for the biomechanical variables across multiple anatomical levels. Moreover, the tendon models that are typically used in musculoskeletal modeling are too stiff. SIGNIFICANCE: Calibrated musculoskeletal models informed by experimental measurements give access to an augmented range of biomechanical variables that might not be easily measured with sensors alone.

At matched loads, aging does not alter ankle, muscle, or tendon stiffness.

Older adults have difficulty maintaining balance when faced with postural disturbances, a task that is influenced by the stiffness of the triceps surae and Achilles tendon. Age-related changes in Achilles tendon stiffness have been reported at matched levels of effort, but measures typically have not been made at matched loads, which is important due to age-dependent changes in strength. Moreover, age-dependent changes in muscle stiffness have yet to be tested. Here, we investigate how age alters muscle and tendon stiffness and their influence on ankle stiffness. We hypothesized that age-related changes in muscle and tendon contribute to reduced ankle stiffness in older adults and evaluated this hypothesis when either load or effort were matched. We used B-mode ultrasound with joint-level perturbations to quantify ankle, muscle, and tendon stiffness across a range of loads and efforts in seventeen healthy younger and older adults. At matched loads, there was no significant difference in ankle, muscle, or tendon stiffness between groups (all p>0.13). However, at matched effort, older adults exhibited a significant decrease in ankle (27%; p=0.008), muscle (37%; p=0.02), and tendon stiffness (22%; p=0.03) at 30% of maximum effort. This is consistent with our finding that older adults were 36% weaker than younger adults in plantarflexion (p=0.004). Together these results indicate that, at the loads tested in this study, there are no age-dependent changes in the mechanical properties of muscle or tendon, only differences in strength that result in altered ankle, muscle, and tendon stiffness at matched levels of effort.

Non-linear properties of the Achilles tendon determine ankle impedance over a broad range of activations in humans.

Regulating ankle mechanics is essential for controlled interactions with the environment and rejecting unexpected disturbances. Ankle mechanics can be quantified by impedance, the dynamic relationship between an imposed displacement and the torque generated in response. Ankle impedance in the sagittal plane depends strongly on the triceps surae and Achilles tendon, but their relative contributions remain unknown. It is commonly assumed that ankle impedance is controlled by changing muscle activation and, thereby, muscle impedance, but this ignores that tendon impedance also changes with activation-induced loading. Thus, we sought to determine the relative contributions from the triceps surae and Achilles tendon during conditions relevant to postural control. We used a novel technique that combines B-mode ultrasound imaging with joint-level perturbations to quantify ankle, muscle and tendon impedance simultaneously across activation levels from 0% to 30% of maximum voluntary contraction. We found that muscle and tendon stiffness, the static component of impedance, increased with voluntary plantarflexion contractions, but that muscle stiffness exceeded tendon stiffness at very low loads (21±7 N). Above these loads, corresponding to 1.3% of maximal strength for an average participant in our study, ankle stiffness was determined predominately by Achilles tendon stiffness. At approximately 20% MVC for an average participant, ankle stiffness was 4 times more sensitive to changes in tendon stiffness than to changes in muscle stiffness. We provide the first empirical evidence demonstrating that the nervous system, through changes in muscle activations, leverages the non-linear properties of the Achilles tendon to increase ankle stiffness during postural conditions.

Simultaneous Quantification of Ankle, Muscle, and Tendon Impedance in Humans.

OBJECTIVE: Regulating the impedance of our joints is essential for the effective control of posture and movement. The impedance of a joint is governed mainly by the mechanical properties of the muscle-tendon units spanning it. Many studies have quantified the net impedance of joints but not the specific contributions from the muscles and tendons. The inability to quantify both muscle and tendon impedance limits the ability to determine the causes underlying altered movement control associated with aging, neuromuscular injury, and other conditions that have different effects on muscle and tendon properties. Therefore, we developed a technique to quantify joint, muscle, and tendon impedance simultaneously and evaluated this technique at the human ankle. METHODS: We used a single degree of freedom actuator to deliver pseudorandom rotations to the ankle while measuring the corresponding torques. We simultaneously measured the displacement of the medial gastrocnemius muscle-tendon junction with B-mode ultrasound. From these experimental measurements, we were able to estimate ankle, muscle, and tendon impedance using non-parametric system identification. RESULTS: We validated our estimates by comparing them to previously reported measurements of muscle and tendon stiffness, the position-dependent component of impedance, to demonstrate that our technique generates reliable estimates of these properties. CONCLUSION: Our approach can be used to clarify the respective contributions from the muscle and tendon to the net mechanics of a joint. SIGNIFICANCE: This is a critical step forward in the ultimate goal of understanding how muscles and tendons govern ankle impedance during posture and movement.

Simultaneous in vivo Estimation of Muscle, Tendon, and Ankle Impedance.

Appropriate regulation of joint impedance is required to successfully navigate our environment. Joint impedance is strongly dependent upon the mechanical properties of the muscles and tendons spanning it. While the impedance of the joint has been well characterized, methods to determine the individual contribution from the muscles and tendons are limited. This is a crucial gap as muscle and tendon impedance can be selectively altered by aging, pathology, or injury. Therefore, we developed an innovative in vivo method that allows for the simultaneous quantification of joint, muscle, and tendon impedance. Stochastic perturbations of ankle angle were applied while a B-mode ultrasound was used to image the displacement of the medial gastrocnemius muscle-tendon junction. Non-parametric system identification was used to quantify ankle impedance and the frequency response function between ankle rotations and muscle-tendon junction displacements. The latter represents, when scaled by Achilles tendon moment arm, the ratio between the net musculotendon impedance and the impedance of the muscle, a relationship we refer to as the impedance ratio. Muscle and tendon impedance can be calculated from these experimental estimates. The ability to simultaneously quantify joint, muscle, and tendon impedance will provide a clearer understanding their respective roles in our ability to navigate our environment, and how changes in those roles may contribute to functional impairments.

Ultrasound Shear Wave Velocity Varies Across Anatomical Region in Ex Vivo Bovine Ovaries.

The physical properties of the ovarian extracellular matrix (ECM) regulate the function of ovarian cells, specifically the ability of the ovary to maintain a quiescent primordial follicle pool while allowing a subset of follicles to grow and mature in the estrous cycle. Design of a long-term, cycling artificial ovary has been hindered by the limited information regarding the mechanical properties of the ovary. In particular, differences in the mechanical properties of the two ovarian compartments, the cortex and medulla, have never been quantified. Shear wave (SW) ultrasound elastography is an imaging modality that enables assessment of material properties, such as the mechanical properties, based on the velocity of SWs, and visualization of internal anatomy, when coupled with B-mode ultrasound. We used SW ultrasound elastography to assess whole, ex vivo bovine ovaries. We demonstrated, for the first time, a difference in mechanical properties, as inferred from SW velocity, between the cortex and medulla, as measured along the length (cortex: 2.57 ± 0.53 m/s, medulla: 2.87 ± 0.77 m/s, p < 0.0001) and width (cortex: 2.99 ± 0.81 m/s, medulla: 3.24 ± 0.97 m/s, p < 0.05) and that the spatial distribution and magnitude of SW velocity vary between these two anatomical planes. This work contributes to a larger body of literature assessing the mechanical properties of the ovary and related cells and specialized ECMs and will enable the rational design of biomimetic tissue engineered models and durable bioprostheses. Impact Statement Shear wave (SW) ultrasound elastography can be used to simultaneously assess the material properties and tissue structures when accompanied with B-mode ultrasound. We report a quantitative difference in mechanical properties, as inferred from SW velocity, between the cortex and medulla, with SW velocity being 11.4% and 8.4% higher in the medulla than the cortex when measured along the length and width, respectively. This investigation into the spatial and temporal variation in SW velocity in bovine ovaries will encourage and improve design of more biomimetic scaffolds for ovarian tissue engineering.

Muscle material properties in passive and active stroke-impaired muscle.

Stroke survivors routinely experience long-term motor and sensory impairments. In parallel with neurological changes, material properties of muscles in the impaired limbs, such as muscle stiffness, may also change progressively. However, these stiffness measures are routinely derived from individual joint stiffness, representing whole muscle groups. Here, we use shear wave (SW) ultrasound elastography to measure SW velocity, as a surrogate measure of stiffness, to quantify material properties in individual muscles. Accordingly, the purpose of this study was to compare muscle material properties of the bicep brachii in stroke survivors and in age-matched control subjects by measuring SW velocity at rest and different voluntary activation levels. Our main findings show that at rest, the SW velocity was on average 41% greater in the paretic muscle compared the contralateral non-paretic muscle. The mean passive SW velocity across all subjects were 2.34 ±â€¯0.41 m/s for the non-paretic side, 3.30 ±â€¯1.20 m/s for the paretic side, and 2.24 ±â€¯0.18 for controls. SW velocity was significantly different in muscles of the paretic and non-paretic side (p < 0.001), but not between muscles of the non-paretic and controls (p = 0.47). As voluntary activation increased, SW velocity increased non-linearly, with an average power fit of r2 = 0.83 ±â€¯0.09 for the non-paretic side, r2 = 0.61 ±â€¯0.24 for the paretic side, and r2 = 0.24 ±â€¯0.15 for the healthy age-matched controls. In active muscle (10, 25, 50, 75, 100% maximum voluntary contraction), there was no significant difference in SW velocity between the non-paretic, paretic, and control muscles. These findings suggest that stroke-impaired muscles have potentially altered muscle material properties, specifically stiffness, and that passive and active stiffness may contribute differently to total muscle stiffness.

The Relationship Between Volitional Activation and Muscle Properties in Incomplete Spinal Cord Injury.

Purpose: Following a motor incomplete spinal cord injury (iSCI), there is decreased volitional activation and changes in composition, architecture, and stiffness of affected muscles. We investigated the relationship between muscle properties and volitional activation. Methods: The relationship between central activation ratio (CAR), maximum volitional torque (MVT), and muscle properties was assessed in the gastrocnemius of 6 participants with iSCI. Results: No significant relationship was found between CAR and muscle properties, while a significant relationship was found between CAR and MVT. Conclusion: Our findings suggest there may be no relationship between volitional activation and muscle; thus, certain patients with iSCI may benefit from therapies targeted at neural control.

Passive material properties of stroke-impaired plantarflexor and dorsiflexor muscles.

BACKGROUND: Following a stroke, intrinsic muscle properties such as stiffness may be altered, which is accompanied by increased spasticity and contractures. Previously, quantification of muscle stiffness has been based off of indirect measurements. Using shear wave ultrasound elastography, direct measurements of muscle material properties can be made. METHODS: Our aim was to evaluate material properties, specifically passive stiffness, using shear wave ultrasound elastography across a range of muscle lengths, in the medial gastrocnemius and the tibialis anterior in chronic stroke survivors. FINDINGS: Our main results show significant increases of 27.7% and 26.9% in shear wave velocity of stroke-impaired medial gastrocnemius compared to the unimpaired contralateral side at 90° ankle angle (P=0.033) and 15° plantarflexion (P=0.001), respectively. However, no significant difference was found in the tibialis anterior between the two sides. Relatively weak correlations were found between SW velocity in the medial gastrocnemius and joint stiffness for both the non-paretic (ρ=0.384, P=0.001), and paretic side (ρ=0.363, P=0.002). Additionally, muscle stiffness estimates of stroke-impaired tibialis anterior from joint torque and angle measurements were significantly greater by 23.1% (P=0.033) than the unimpaired contralateral side. However, no significant difference was found in the medial gastrocnemius. INTERPRETATION: These results indicate that there are non-uniform changes in passive stiffness of stroke-impaired muscle. Therefore, muscles need to be evaluated individually to assess alterations. Additionally, interpretation of joint-based calculations of muscle stiffness should be made cautiously. Having the ability to non-invasively assess muscle stiffness adaptations in vivo would aid in prognosis, evaluation, and treatment following a stroke.