Andrade Ricardoj, Racapé Apolline, Hernández-Secorún Mar, Ngo Ha-Hien-Phuong, Lemoine Alice, Etaix Nicolas, Frappart Thomas, Fraschini Christophe, Gennisson Jean-Luc, Nordez Antoine
Nantes Université, Movement - Interactions - Performance, MIP, UR 4334, F-44000 Nantes, France.
Nantes Université, Movement - Interactions - Performance, MIP, UR 4334, F-44000 Nantes, France.
Acta Biomater. 2025 May 3. doi: 10.1016/j.actbio.2025.05.010.
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.
承重骨骼肌组织由排列成优先取向的复杂蛋白质纤维网络加强，赋予其方向依赖性的力学性能（各向异性）。在体内表征这种各向异性对于理解正常和病理肌肉功能以及结构完整性至关重要。然而，当前的非侵入性技术在准确测量诸如骨骼肌等各向异性组织的力学性能方面能力有限。在此，我们使用了我们团队最近开发的一种创新的角度分辨超声弹性成像方法，来同时量化拉伸和剪切弹性以及各向异性，从而能够全面评估肌肉生物力学。我们全面表征了14名健康年轻成年人在被动和主动轴向加载下肱二头肌的力学性能，揭示了沿肌纤维和跨肌纤维的不同剪切和拉伸力学行为。值得注意的是，发现沿主要纤维取向的拉伸模量和剪切模量是解耦的，而跨肌纤维测量显示出一致的模量比为3.4±0.2，与轴向加载条件或强度无关。这些发现突出了骨骼肌的各向异性本质，并为其体内力学行为提供了有价值的见解。剪切和拉伸各向异性均随肌肉轴向生理负荷增加，表明我们的方法对各向异性组织力学的变化敏感。最后，我们证明角度分辨超声剪切波弹性成像提供了剪切和拉伸性能的直接估计，为临床应用带来了重大前景，包括神经肌肉疾病诊断和监测、预测组织对负荷和治疗反应的生物力学建模以及组织工程。重要性声明：传统超声剪切波弹性成像技术忽略了骨骼肌的各向异性，导致组织力学表征不完整。在本研究中，我们利用一种创新的角度分辨弹性成像方法来评估人体肌肉在体内的拉伸和剪切弹性及其各向异性因素。我们首次揭示了主动和被动生理负荷期间拉伸弹性和剪切弹性之间的复杂关系。该技术增强了我们对肌肉力学的理解，并对肌肉健康和神经肌肉疾病管理具有有前景的临床意义，在这些情况下组织结构和力学性能经常发生改变。此外，它有助于开发肌肉组织的本构模型，并有助于组织工程材料的设计。
