Simultaneous measurement of tensile and shear elasticity and anisotropy in human skeletal muscle tissue using steered ultrasound shear waves.

Abstract

Load-bearing skeletal muscle tissues are reinforced by intricate networks of protein fibers aligned in preferential orientations, imparting direction-dependent mechanical properties (anisotropy). Characterizing this anisotropy in vivo is essential for understanding both normal and pathological muscle function, as well as structural integrity. However, current noninvasive techniques are limited in their ability to accurately measure the mechanical properties of anisotropic tissues such as skeletal muscle. Here, we used an innovative angle-resolved ultrasound elastography method, recently developed by our team, to simultaneously quantify tensile and shear elasticity and anisotropy, enabling comprehensive assessment of muscle biomechanics. We fully characterized the mechanical properties of the biceps brachii in fourteen healthy young adults under passive and active axial loadings, revealing distinct shear and tensile mechanical behaviors both along and across muscle fibers. Notably, tensile and shear moduli along the main fiber orientation were found to be uncoupled, while cross-muscle fiber measurements exhibited a consistent modulus ratio of 3.4 ± 0.2, regardless of axial loading conditions or intensities. These findings highlight the anisotropic nature of skeletal muscle and provide valuable insights into its in vivo mechanical behavior. Both shear and tensile anisotropy increased with muscle axial physiological loading, indicating that our method is sensitive to changes in anisotropic tissue mechanics. Lastly, we demonstrated that angle-resolved ultrasound shear wave elastography provides direct estimates of shear and tensile properties, offering significant promise for clinical applications, including neuromuscular disease diagnostics and monitoring, biomechanical modeling for predicting tissue responses to loading and therapies, and tissue engineering. STATEMENT OF SIGNIFICANCE: : Conventional ultrasound shear wave elastography techniques overlook the anisotropy of skeletal muscles, leading to incomplete tissue mechanical characterization. In this study, we leveraged an innovative angle-resolved elastography method to assess tensile and shear elasticity, along with their anisotropic factors, of human muscle in vivo. For the first time, we reveal the intricate relationships between tensile and shear elasticities during active and passive physiological loading. This technique enhances our understanding of muscle mechanics and has promising clinical implications for muscle health and neuromuscular disease management, where tissue structural and mechanical properties are often altered. Additionally, it could help in developing constitutive models for muscle tissue and contribute to the design of tissue-engineered materials.