journal article·2025-06Open access

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

Ricardo J. Andrade, Apolline Racapé, Mar Hernández-Secorún, Ha-Hien-Phuong Ngo, Alice Lemoine, Nicolas Etaix, Thomas Frappart, Christophe Fraschini, Jean-Luc Gennisson, Antoine Nordez

Acta Biomaterialia· Volume 199

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.
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Research context

OpenAlex topics: Ultrasound Imaging and Elastography · Body Composition Measurement Techniques · Elasticity and Material Modeling

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References (82)

Show source-provided references
1. Skeletal muscle: a brief review of structure and function10.1007/s00223-014-9915-y ↗
2. The basement membrane/Basal lamina of skeletal muscle10.1074/jbc.R200027200 ↗
3. The structure and role of intramuscular connective tissue in muscle function10.3389/fphys.2020.00495 ↗
4. On the anisotropy of skeletal muscle tissue under compression10.1016/j.actbio.2014.03.003 ↗
5. Structure and function of the skeletal muscle extracellular matrix10.1002/mus.22094 ↗
6. Intravital imaging reveals ghost fibers as architectural units guiding myogenic progenitors during regeneration10.1016/j.stem.2015.11.005 ↗
7. Cellular biomechanics in skeletal muscle regeneration10.1016/bs.ctdb.2017.08.007 ↗
8. Actomyosin meshwork mechanosensing enables tissue shape to orient cell force10.1038/ncomms15014 ↗
9. Tension and force-resistant attachment are essential for myofibrillogenesis in Drosophila flight muscle10.1016/j.cub.2014.02.032 ↗
10. Transversely isotropic tensile material properties of skeletal muscle tissue10.1016/j.jmbbm.2009.03.004 ↗
11. Skeletal muscle mechanics: questions, problems and possible solutions10.1186/s12984-017-0310-6 ↗
12. The short range stiffness of active mammalian muscle and its effect on mechanical properties10.1113/jphysiol.1974.sp010613 ↗
13. Biochemical and structural basis of the passive mechanical properties of whole skeletal muscle10.1113/JP280867 ↗
14. Skeletal muscle mechanics, energetics and plasticity10.1186/s12984-017-0318-y ↗
15. The stiffness of living tissues and its implications for tissue engineering10.1038/s41578-019-0169-1 ↗
16. Porous biomaterial scaffolds for skeletal muscle tissue engineering10.3389/fbioe.2023.1245897 ↗
17. Design and analysis of tissue engineering scaffolds that mimic soft tissue mechanical anisotropy10.1016/j.biomaterials.2006.02.024 ↗
18. Biomimetic hierarchically arranged nanofibrous structures resembling the architecture and the passive mechanical properties of skeletal muscles: a step forward toward artificial muscle10.3389/fbioe.2020.00767 ↗
19. Tissue engineering of skeletal muscle, tendons and nerves: a review of manufacturing strategies to meet structural and functional requirements
20. Supersonic shear imaging: a new technique for soft tissue elasticity mapping10.1109/TUFFC.2004.1295425 ↗
21. Shear wave elasticity imaging: a new ultrasonic technology of medical diagnostics10.1016/S0301-5629(98)00110-0 ↗
22. Ultrasound elastography: principles and techniques10.1016/j.diii.2013.01.022 ↗
23. Mechanics of ultrasound elastography10.1098/rspa.2016.0841 ↗
24. Elastography assessment of Liver fibrosis: society of Radiologists in Ultrasound Consensus Conference Statement10.1148/radiol.2015150619 ↗
25. Detection of breast cancer with addition of annual screening ultrasound or a single screening MRI to mammography in women with elevated breast cancer risk10.1001/jama.2012.388 ↗
26. On the elasticity of transverse isotropic soft tissues (L)10.1121/1.3559681 ↗
27. Anisotropy in ultrasound shear wave elastography: an add-on to muscles characterization10.3389/fphys.2022.1000612 ↗
28. Tractable calculation of the Green’s tensor for shear wave propagation in an incompressible, transversely isotropic material10.1088/1361-6560/ab5c2d ↗
29. Finite element modeling of impulsive excitation and shear wave propagation in an incompressible, transversely isotropic medium10.1016/j.jbiomech.2013.09.008 ↗
30. On the elasticity of transverse isotropic soft tissues (L)10.1121/1.3559681 ↗
31. In plane quantification of in vivo muscle elastic anisotropy factor by steered ultrasound pushing beams10.1088/1361-6560/ad21a0 ↗
32. Analysis of multiple shear wave modes in a nonlinear soft solid: experiments and finite element simulations with a tilted acoustic radiation force10.1016/j.jmbbm.2020.103754 ↗
33. In vivo assessment of shear modulus along the fibers of pennate muscle during passive lengthening and contraction using steered ultrasound push beams
34. Coherent plane-wave compounding for very high frame rate ultrasonography and transient elastography10.1109/TUFFC.2009.1067 ↗
35. In plane quantification of in vivo muscle elastic anisotropy factor by steered ultrasound pushing beams10.1088/1361-6560/ad21a0 ↗
36. Specular beamforming10.1109/TUFFC.2017.2709038 ↗
37. The variance of quantitative estimates in shear wave imaging: theory and experiments10.1109/TUFFC.2012.2472 ↗
38. An axial velocity estimator for ultrasound blood flow imaging, based on a full evaluation of the Doppler equation by means of a two-dimensional autocorrelation approach10.1109/58.393110 ↗
39. Anisotropy in ultrasound shear wave elastography: an add-on to muscles characterization10.3389/fphys.2022.1000612 ↗
40. Tractable calculation of the Green’s tensor for shear wave propagation in an incompressible, transversely isotropic material10.1088/1361-6560/ab5c2d ↗
41. Viscoelastic and anisotropic mechanical properties of in vivo muscle tissue assessed by supersonic shear imaging10.1016/j.ultrasmedbio.2010.02.013 ↗
42. Unravelling anisotropic nonlinear shear elasticity in muscles: towards a non-invasive assessment of stress in living organisms10.1016/j.jmbbm.2023.106325 ↗
43. Elastic Cherenkov effects in transversely isotropic soft materials-I: theoretical analysis, simulations and inverse method10.1016/j.jmps.2016.05.023 ↗
44. Acute changes in hamstrings musculo-articular dissipative properties induced by cyclic and static stretching10.1055/s-2007-964980 ↗
45. Development of recommendations for SEMG sensors and sensor placement procedures10.1016/S1050-6411(00)00027-4 ↗
46. Influence of passive muscle tension on electromechanical delay in humans10.1371/journal.pone.0053159 ↗
47. Muscle and joint responses during and after static stretching performed at different intensities10.1007/s00421-015-3104-1 ↗
48. Influence of low muscle activation levels on the ankle torque and muscle shear modulus during plantar flexor stretching10.1016/j.jbiomech.2019.06.018 ↗
49. One-dimensional statistical parametric mapping in Python10.1080/10255842.2010.527837 ↗
50. Anisotropic materials for skeletal-muscle-tissue engineering10.1002/adma.201600240 ↗
51. Elastography for muscle biomechanics: toward the estimation of individual muscle force10.1249/JES.0000000000000049 ↗
52. Does elasticity of Achilles tendon change after suture applications? Evaluation of repair area by acoustic radiation force impulse elastography10.1186/s13018-018-0751-z ↗
53. Changes in morphological and elastic properties of patellar tendon in athletes with unilateral patellar tendinopathy and their relationships with pain and functional disability
54. Using ultrasound shear wave elastography to characterize peripheral nerve mechanics: a systematic review on the normative reference values in healthy individuals10.14366/usg.23211 ↗
55. Does group velocity always reflect elastic modulus in shear wave elastography?10.1117/1.JBO.24.7.076003 ↗
56. In vivo assessment of shear modulus along the fibers of pennate muscle during passive lengthening and contraction using steered ultrasound push beams
57. How does tissue preparation affect skeletal muscle transverse isotropy?10.1016/j.jbiomech.2016.06.034 ↗
58. The anisotropic mechanical behaviour of passive skeletal muscle tissue subjected to large tensile strain10.1016/j.jmbbm.2012.09.001 ↗
59. Investigating passive muscle mechanics with biaxial stretch10.3389/fphys.2020.01021 ↗
60. Characterising skeletal muscle under large strain using eccentric and fourier transform-rheology10.1016/j.jbiomech.2015.08.025 ↗
61. Muscle as a collagen fiber reinforced composite: a review of force transmission in muscle and whole limb10.1016/S0021-9290(98)00186-9 ↗
62. Full characterization of in vivo muscle as an elastic, incompressible, transversely isotropic material using ultrasonic rotational 3D shear wave elasticity imaging10.1109/TMI.2021.3106278 ↗
63. Elastic Cherenkov effects in transversely isotropic soft materials-II: ex vivo and in vivo experiments10.1016/j.jmps.2016.04.028 ↗
64. Full characterization of in vivo muscle as an elastic, incompressible, transversely isotropic material using ultrasonic rotational 3D shear wave elasticity imaging10.1109/TMI.2021.3106278 ↗
65. In vivo estimation of anisotropic mechanical properties of the gastrocnemius during functional loading with MR elastography10.1088/1361-6560/acb482 ↗
66. Requirements for accurate estimation of anisotropic material parameters by magnetic resonance elastography: a computational study10.1002/mrm.26600 ↗
67. On multiscale tension-compression asymmetry in skeletal muscle10.1016/j.actbio.2022.03.034 ↗
68. Regeneration of injured skeletal muscle after the injury10.32098/mltj.04.2013.16 ↗
69. Epimuscular myofascial force transmission: a historical review and implications for new research
70. Shear wave elastography of tumour growth in a human breast cancer model with pathological correlation10.1007/s00330-013-2828-8 ↗
71. Skeletal muscle in healthy subjects versus those with GNE -related myopathy: evaluation with Shear-wave US—A pilot study10.1148/radiol.2015142212 ↗
72. Effects of Duchenne muscular dystrophy on muscle stiffness and response to electrically-induced muscle contraction: a 12-month follow-up10.1016/j.nmd.2017.01.001 ↗
73. Non-invasive assessment of muscle stiffness in patients with duchenne muscular dystrophy10.1002/mus.24445 ↗
74. Ultrasound elastography in the assessment of post-stroke muscle stiffness: a systematic review10.1186/s13244-022-01191-x ↗
75. Regulation of fibrosis in muscular dystrophy10.1016/j.matbio.2018.01.014 ↗
76. Emery · 2015
77. Engineered materials for organoid systems10.1038/s41578-019-0129-9 ↗
78. Measurement of viscoelastic properties of homogeneous soft solid using transient elastography: an inverse problem approach10.1121/1.1815075 ↗
79. A diffraction correction for storage and loss moduli imaging using radiation force based elastography10.1088/1361-6560/62/1/91 ↗
80. Acoustoelasticity in transversely isotropic soft tissues: quantification of muscle nonlinear elasticity10.1121/10.0008976 ↗
81. Acousto-elasticity of transversely isotropic incompressible soft tissues: characterization of skeletal striated muscle10.1088/1361-6560/ac0f9b ↗
82. In vivo evaluation of the elastic anisotropy of the human Achilles tendon using shear wave dispersion analysis10.1088/0031-9155/59/3/505 ↗