Research article

Multiscale modeling of skeletal muscle to explore its passive mechanical properties and experiments verification


  • Received: 21 August 2021 Accepted: 18 November 2021 Published: 02 December 2021
  • The research of the mechanical properties of skeletal muscle has never stopped, whether in experimental tests or simulations of passive mechanical properties. To investigate the effect of biomechanical properties of micro-components and geometric structure of muscle fibers on macroscopic mechanical behavior, in this manuscript, we establish a multiscale model where constitutive models are proposed for fibers and the extracellular matrix, respectively. Besides, based on the assumption that the fiber cross-section can be expressed by Voronoi polygons, we optimize the Voronoi polygons as curved-edge Voronoi polygons to compare the effects of the two cross-sections on macroscopic mechanical properties. Finally, the macroscopic stress response is obtained through the numerical homogenization method. To verify the effectiveness of the multi-scale model, we measure the mechanical response of skeletal muscles in the in-plane shear, longitudinal shear, and tensions, including along the fiber direction and perpendicular to the fiber direction. Compared with experimental data, the simulation results show that this multiscale framework predicts both the tension response and the shear response of skeletal muscle accurately. The root mean squared error (RMSE) is 0.0035 MPa in the tension along the fiber direction; The RMSE is 0.011254 MPa in the tension perpendicular to the fiber direction; The RMSE is 0.000602 MPa in the in-plane shear; The RMSE was 0.00085 MPa in the longitudinal shear. Finally, we obtained the influence of the component constitutive model and muscle fiber cross-section on the macroscopic mechanical behavior of skeletal muscle. In terms of the tension perpendicular to the fiber direction, the curved-edge Voronoi polygons achieve the result closer to the experimental data than the Voronoi polygons. Skeletal muscle mechanics experiments verify the effectiveness of our multiscale model. The comparison results of experiments and simulations prove that our model can accurately capture the tension and shear behavior of skeletal muscle.

    Citation: Fengjie Liu, Monan Wang, Yuzheng Ma. Multiscale modeling of skeletal muscle to explore its passive mechanical properties and experiments verification[J]. Mathematical Biosciences and Engineering, 2022, 19(2): 1251-1279. doi: 10.3934/mbe.2022058

    Related Papers:

  • The research of the mechanical properties of skeletal muscle has never stopped, whether in experimental tests or simulations of passive mechanical properties. To investigate the effect of biomechanical properties of micro-components and geometric structure of muscle fibers on macroscopic mechanical behavior, in this manuscript, we establish a multiscale model where constitutive models are proposed for fibers and the extracellular matrix, respectively. Besides, based on the assumption that the fiber cross-section can be expressed by Voronoi polygons, we optimize the Voronoi polygons as curved-edge Voronoi polygons to compare the effects of the two cross-sections on macroscopic mechanical properties. Finally, the macroscopic stress response is obtained through the numerical homogenization method. To verify the effectiveness of the multi-scale model, we measure the mechanical response of skeletal muscles in the in-plane shear, longitudinal shear, and tensions, including along the fiber direction and perpendicular to the fiber direction. Compared with experimental data, the simulation results show that this multiscale framework predicts both the tension response and the shear response of skeletal muscle accurately. The root mean squared error (RMSE) is 0.0035 MPa in the tension along the fiber direction; The RMSE is 0.011254 MPa in the tension perpendicular to the fiber direction; The RMSE is 0.000602 MPa in the in-plane shear; The RMSE was 0.00085 MPa in the longitudinal shear. Finally, we obtained the influence of the component constitutive model and muscle fiber cross-section on the macroscopic mechanical behavior of skeletal muscle. In terms of the tension perpendicular to the fiber direction, the curved-edge Voronoi polygons achieve the result closer to the experimental data than the Voronoi polygons. Skeletal muscle mechanics experiments verify the effectiveness of our multiscale model. The comparison results of experiments and simulations prove that our model can accurately capture the tension and shear behavior of skeletal muscle.



    加载中


    [1] R. L. Lieber, E. Runesson, F. Einarsson, J. Friden, Inferior mechanical properties of spastic muscle bundles due to hypertrophic but compromised extracellular matrix material, Muscle Nerve., 28 (2003), 464–471. doi: 10.1002/mus.10446. doi: 10.1002/mus.10446
    [2] B. Sharafi, S. S. Blemker, A micromechanical model of skeletal muscle to explore the effects of fiber and fascicle geometry, J. Biomech., 43 (2010), 3207–3213. doi: 10.1016/j.jbiomech.2010.07.020. doi: 10.1016/j.jbiomech.2010.07.020
    [3] B. Pierrat, J. G. Murphy, D. B. MacManus, M. D. Gilchrist, Finite element implementation of a new model of slight compressibility for transversely isotropic materials, Comput. Methods Biomech. Biomed. Eng., 19 (2016), 745–758. doi: 10.1080/10255842.2015.1061513. doi: 10.1080/10255842.2015.1061513
    [4] M. D. Gilchrist, J. G. Murphy, W. Parnell, B. Pierrat, Modelling the slight compressibility of anisotropic soft tissue, Int. J. Solids Struct., 51 (2014), 3857–3865. doi: 10.1016/j.ijsolstr.2014.06.018. doi: 10.1016/j.ijsolstr.2014.06.018
    [5] M. Böl, Micromechanical modelling of skeletal muscles: from the single fibre to the whole muscle, Arch. Appl. Mech., 80 (2010), 557–567. doi: 10.1007/s00419-009-0378-y. doi: 10.1007/s00419-009-0378-y
    [6] T. Heidlauf, O. Röhrle, Modeling the chemoelectromechanical behavior of skeletal muscle using the parallel open-source software library OpenCMISS, Comput. Math. Methods Med., 2013 (2013), 517287. doi: 10.1155/2013/517287. doi: 10.1155/2013/517287
    [7] A. E. Ehret, M. Böl, M. Itskov, A continuum constitutive model for the active behaviour of skeletal muscle, J. Mech. Phys. Solids, 59 (2011), 625–636. doi: 10.1016/j.jmps.2010.12.008. doi: 10.1016/j.jmps.2010.12.008
    [8] S. S. Blemker, P. M. Pinsky, S. L. Delp, A 3D model of muscle reveals the causes of nonuniform strains in the biceps brachii, J. Biomech., 38 (2005), 657–665. doi: 10.1016/j.jbiomech.2004.04.009. doi: 10.1016/j.jbiomech.2004.04.009
    [9] G. Chagnon, M. Rebouah, D. Favier, Hyperelastic energy densities for soft biological tissues: a review, J. Elast., 120 (2015), 129–160. doi: 10.1007/s10659-014-9508-z. doi: 10.1007/s10659-014-9508-z
    [10] M. Böl, S. Reese, Micromechanical modelling of skeletal muscles based on the finite element method, Comput. Methods Biomech. Biomed. Eng., 11 (2008), 489–504. doi: 10.1080/10255840701771750. doi: 10.1080/10255840701771750
    [11] P. Kanouté, D. P. Boso, J. L. Chaboche, B. A. Schrefler, Multiscale methods for composites: a review, Arch. Comput. Methods Eng., 16 (2009), 31–75. doi: 10.1007/s11831-008-9028-8. doi: 10.1007/s11831-008-9028-8
    [12] C. Bleiler, P. P. Castaneda, O. Rohrle, A microstructurally-based, multi-scale, continuum-mechanical model for the passive behaviour of skeletal muscle tissue, J. Mech. Behav. Biomed. Mater., 97 (2019), 171–186. doi: 10.1016/j.jmbbm.2019.05.012. doi: 10.1016/j.jmbbm.2019.05.012
    [13] M. Böl, R. Iyer, J. Dittmann, M. Garces-Schroder, A. Dietzel, Investigating the passive mechanical behaviour of skeletal muscle fibres: Micromechanical experiments and Bayesian hierarchical modelling, Acta Biomater., 92 (2019), 277–289. doi: 10.1016/j.actbio.2019.05.015. doi: 10.1016/j.actbio.2019.05.015
    [14] G. A. Holzapfel, Biomechanics of Soft Tissue, Cambridge: Academic Press, 2001.
    [15] R. Kuravi, K. Leichsenring, M. Böl, A. E. Ehret, 3D finite element models from serial section histology of skeletal muscle tissue-The role of micro-architecture on mechanical behaviour, J. Mech. Behav. Biomed. Mater., 113 (2021), 104109. doi: 10.1016/j.jmbbm.2020.104109. doi: 10.1016/j.jmbbm.2020.104109
    [16] G. A. Holzapfel, T. C. Gasser, R. W. Ogden, A new constitutive framework for arterial wall mechanics and a comparative study of material models, J. Elast., 61 (2000), 1–48. doi: 10.1023/a:1010835316564. doi: 10.1023/a:1010835316564
    [17] L. A. Spyrou, S. Brisard, K. Danas, Multiscale modeling of skeletal muscle tissues based on analytical and numerical homogenization, J. Mech. Behav. Biomed. Mater., 92 (2019), 97–117. doi: 10.1016/j.jmbbm.2018.12.030. doi: 10.1016/j.jmbbm.2018.12.030
    [18] L. A. Spyrou, M. Agoras, K. Danas, A homogenization model of the Voigt type for skeletal muscle, J. Theor. Biol., 414 (2017), 50–61. doi: 10.1016/j.jtbi.2016.11.018. doi: 10.1016/j.jtbi.2016.11.018
    [19] K. M. Virgilio, K. S. Martin, S. M. Peirce, S. S. Blemker, Multiscale models of skeletal muscle reveal the complex effects of muscular dystrophy on tissue mechanics and damage susceptibility, Interface Focus, 5 (2015), 20140080. doi: 10.1098/rsfs.2014.0080. doi: 10.1098/rsfs.2014.0080
    [20] O. Rohrle, U. S. Yavuz, T. Klotz, F. Negro, T. Heidlauf, Multiscale modeling of the neuromuscular system: Coupling neurophysiology and skeletal muscle mechanics, Wiley Interdiscip. Rev. Syst. Biol., 11 (2019), e1457. doi: 10.1002/wsbm.1457. doi: 10.1002/wsbm.1457
    [21] F. L. Jiménez, Modeling of soft composites under three-dimensional loading, Compos. Pt. B-Eng., 59 (2014), 173–180. doi: 10.1016/j.compositesb.2013.11.020. doi: 10.1016/j.compositesb.2013.11.020
    [22] M. Rintoul, S. Torquato, Reconstruction of the structure of dispersions, J. Colloid Interface Sci., 186 (1997), 467–476. doi: 10.1006/jcis.1996.4675. doi: 10.1006/jcis.1996.4675
    [23] G. A. Holzapfel, J. A. Niestrawska, R. W. Ogden, A. J. Reinisch, A. J. Schriefl, Modelling non-symmetric collagen fibre dispersion in arterial walls, J. R. Soc. Interface, 12 (2015), 20150188. doi: 10.1098/rsif.2015.0188. doi: 10.1098/rsif.2015.0188
    [24] K. Li, G. A. Holzapfel, Multiscale modeling of fiber recruitment and damage with a discrete fiber dispersion method, J. Mech. Phys. Solids, 126 (2019), 226–244. doi: 10.1016/j.jmps.2019.01.022. doi: 10.1016/j.jmps.2019.01.022
    [25] K. Li, R. W. Ogden, G. A. Holzapfel, A discrete fibre dispersion method for excluding fibres under compression in the modelling of fibrous tissues, J. R. Soc. Interface, 15 (2018), 20170766. doi: 10.1098/rsif.2017.0766. doi: 10.1098/rsif.2017.0766
    [26] D. H. Cortes, S. P. Lake, J. A. Kadlowec, L. J. Soslowsky, D. M. Elliott, Characterizing the mechanical contribution of fiber angular distribution in connective tissue: comparison of two modeling approaches, Biomech. Model Mechanobiol., 9 (2010), 651–658. doi: 10.1007/s10237-010-0194-x. doi: 10.1007/s10237-010-0194-x
    [27] P. A. Huijing, Muscle as a collagen fiber reinforced composite: a review of force transmission in muscle and whole limb, J. Biomech., 32 (1999), 329–345. doi: 10.1016/S0021-9290(98)00186-9. doi: 10.1016/S0021-9290(98)00186-9
    [28] M. N. Wang, F. J. Liu, A compressible anisotropic hyperelastic model with I5 and I7 strain invariants, Comput. Methods Biomech. Biomed. Eng., 23 (2020), 1277–1286. doi: 10.1080/10255842.2020.1795839. doi: 10.1080/10255842.2020.1795839
    [29] C. O. Horgan, J. G. Murphy, On the fiber stretch in shearing deformations of fibrous soft materials, J. Elast., 133 (2018), 253–259. doi: 10.1007/s10659-018-9678-1. doi: 10.1007/s10659-018-9678-1
    [30] C. O. Horgan, J. G. Murphy, A constitutive model for fibre-matrix interaction in fibre-reinforced hyperelastic materials, Appl. Eng. Sci., 2020. doi: 10.1016/j.apples.2020.100008. doi: 10.1016/j.apples.2020.100008
    [31] M. Böl, A. E. Ehret, K. Leichsenring, C. Weichert, R. Kruse, On the anisotropy of skeletal muscle tissue under compression, Acta Biomater., 10 (2015), 3225–3234. doi: 10.1016/j.actbio.2014.03.003. doi: 10.1016/j.actbio.2014.03.003
    [32] S. Kohn, K. Leichsenring, R. Kuravi, A. E. Ehret, M. Böl, Direct measurement of the direction-dependent mechanical behaviour of skeletal muscle extracellular matrix, Acta Biomater., 122 (2021), 249–262. doi: 10.1016/j.actbio.2020.12.050. doi: 10.1016/j.actbio.2020.12.050
    [33] J. Gindre, M. Takaza, K. M. Moerman, C. K. Simms, A structural model of passive skeletal muscle shows two reinforcement processes in resisting deformation, J. Mech. Behav. Biomed. Mater., 22 (2013), 84–94. doi: 10.1016/j.jmbbm.2013.02.007. doi: 10.1016/j.jmbbm.2013.02.007
    [34] P. P. Purslow, The extracellular matrix of skeletal and cardiac muscle, Collagen: Struct. Mech., (2008), 325–357. doi: 10.1007/978-0-387-73906-9_12 doi: 10.1007/978-0-387-73906-9_12
    [35] G. A. Holzapfel, Nonlinear solid mechanics: A continuum approach for engineering, Meccanica, 37 (2002), 489–490. doi: 10.1023/A:1020843529530. doi: 10.1023/A:1020843529530
    [36] L. R. Smith, L. H. Fowlergerace, R. L. Lieber, Muscle extracellular matrix applies a transverse stress on fibers with axial strain, J. Biomech., 44 (2011), 1618. doi: 10.1016/j.jbiomech.2011.03.009. doi: 10.1016/j.jbiomech.2011.03.009
    [37] Y. Feng, S. Qiu, X. Xia, S. Ji, C. H. Lee, A computational study of invariant I5 in a nearly incompressible transversely isotropic model for white matter, J. Biomech., 57 (2017), 146–151. doi: 10.1016/j.jbiomech.2017.03.025. doi: 10.1016/j.jbiomech.2017.03.025
    [38] J. G. Murphy, Transversely isotropic biological, soft tissue must be modelled using both anisotropic invariants, Eur. J. Mech. A-Solids., 42 (2013), 90–96. doi: 10.1016/j.euromechsol.2013.04.003. doi: 10.1016/j.euromechsol.2013.04.003
    [39] Y. Feng, R. J. Okamoto, R. Namani, G. M. Genin, P. V. Bayly, Measurements of mechanical anisotropy in brain tissue and implications for transversely isotropic material models of white matter, J. Mech. Behav. Biomed. Mater., 23 (2013), 117–132. doi: 10.1016/j.jmbbm.2013.04.007. doi: 10.1016/j.jmbbm.2013.04.007
    [40] P. P. Purslow, The structure and role of intramuscular connective tissue in muscle function, Front Physiol., 11 (2020), 495. doi: 10.3389/fphys.2020.00495. doi: 10.3389/fphys.2020.00495
    [41] N. Narayanan, S. Calve, Extracellular matrix at the muscle endon interface: functional roles, techniques to explore and implications for regenerative medicine, Connect. Tissue Res., 62 (2021), 53–71. doi: 10.1080/03008207.2020.1814263. doi: 10.1080/03008207.2020.1814263
    [42] M. Kjær, Role of extracellular matrix in adaptation of tendon and skeletal muscle tomechanical loading, Physiol. Rev., 84 (2004), 649–698. doi: 10.1152/physrev.00031.2003. doi: 10.1152/physrev.00031.2003
    [43] V. Kovanen, Intramuscular extracellular matrix: Complex environment of muscle cells, Exercise Sport Sci. Rev., 30 (2002), 20–25. doi: 10.1097/00003677-200201000-00005. doi: 10.1097/00003677-200201000-00005
    [44] K. Gelse, E. Poschl, T. Aigner, Collagens-structure, function, and biosynthesis, Adv. Drug Del. Rev., 55 (2003), 1531–1546. doi: 10.1016/j.addr.2003.08.002. doi: 10.1016/j.addr.2003.08.002
    [45] C. Suchocki, Finite element implementation of slightly compressible and incompressible first invariant-based hyperelasticity: theory, coding, exemplary problems, J. Theor. Appl. Mech., 55 (2017), 787–800. doi: 10.15632/jtam-pl.55.3.787. doi: 10.15632/jtam-pl.55.3.787
    [46] C. Suchocki, A finite element implementation of Knowles stored-energy function: theory, coding and applications, Arch. Mech. Eng., 58 (2011), 319–346. doi: 10.2478/v10180-011-0021-7. doi: 10.2478/v10180-011-0021-7
    [47] A. R. Gillies, R. L. Lieber, Structure and function of the skeletal muscle extracellular matrix, Muscle Nerve., 44 (2011), 318–331. doi: 10.1002/mus.22094. doi: 10.1002/mus.22094
    [48] A. Mbiakop, A. Constantinescu, K. Danas, An analytical model for porous single crystals with ellipsoidal voids, J. Mech. Phys. Solids, 84 (2015), 436–467. doi: 10.1016/j.jmps.2015.07.011. doi: 10.1016/j.jmps.2015.07.011
    [49] J. C. Michel, H. Moulinec, P. Suquet, Effective properties of composite materials with periodic microstructure: a computational approach, Comput. Methods Appl. Mech. Eng., 172 (1999), 109–143. doi: 10.1016/S0045-7825(98)00227-8. doi: 10.1016/S0045-7825(98)00227-8
    [50] Z. Xia, Y. Zhang, F. Ellyin, A unified periodical boundary conditions for representative volume elements of composites and applications, Int. J. Solids Struct., 40 (2003), 1907–1921. doi: 10.1016/s0020-7683(03)00024-6. doi: 10.1016/s0020-7683(03)00024-6
    [51] S. L. Omairey, P. D. Dunning, S. Sriramula, Development of an ABAQUS plugin tool for periodic RVE homogenisation, Eng. Comput., 35 (2018), 567–577. doi: 10.1007/s00366-018-0616-4. doi: 10.1007/s00366-018-0616-4
    [52] D. A. Morrow, T. L. H. Donahue, G. M. Odegard, K. R. Kaufman, Transversely isotropic tensile material properties of skeletal muscle tissue, J. Mech. Behav. Biomed. Mater., 3 (2010), 124–129. doi: 10.1016/j.jmbbm.2009.03.004. doi: 10.1016/j.jmbbm.2009.03.004
    [53] M. V. Loocke, C. G. Lyons, C. K. Simms, A validated model of passive muscle in compression, J. Biomech., 39 (2006), 2999–3009. doi: 10.1016/j.jbiomech.2005.10.016. doi: 10.1016/j.jbiomech.2005.10.016
    [54] D. W. Marquardt, An algorithm for least-squares estimation of nonlinear parameters, J. Soc. Ind. App. Math., 11 (1963), 431–441. doi: 10.2307/2098941. doi: 10.2307/2098941
    [55] R. Xu, C. Bouby, H. Zahrouni, T. B. Zineb, H. Hu, M. Potier-Ferry, 3D modeling of shape memory alloy fiber reinforced composites by multiscale finite element method, Compos. Struct., 200 (2018), 408–419. doi: 10.1016/j.compstruct.2018.05.108. doi: 10.1016/j.compstruct.2018.05.108
  • Reader Comments
  • © 2022 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索

Metrics

Article views(1736) PDF downloads(132) Cited by(0)

Article outline

Figures and Tables

Figures(18)  /  Tables(6)

Other Articles By Authors

/

DownLoad:  Full-Size Img  PowerPoint
Return
Return

Catalog