Skip to main content
Log in

A variational homogenization approach applied to the multiscale analysis of the viscoelastic behavior of tendon fascicles

  • Original Article
  • Published:
Continuum Mechanics and Thermodynamics Aims and scope Submit manuscript

Abstract

This work presents a variational homogenization approach based on representative volume elements (RVE) in order to investigate the macro- and microviscoelastic behavior of tendon fascicles. A three-dimensional hexagonal–helicoidal finite element RVE is proposed to properly account for the morphology of tendon fascicles observed in serial block-face scanning electron microscopy. Two material phases (collagen fibers and cells) comprising three finite strain variational viscoelastic models (fibrils, matrix of fibers and cells) compose the proposed multiscale model. The material parameters of the micromechanical models were identified with the aid of atomic force microscopy experiments extracted from the literature. A set of multiscale simulations of tensile tests under physiological strain amplitudes were performed, providing the following results. Firstly, numerical predictions corroborate experimental findings: collagen fibrils are the main load-bearing structures of tendons; the cellular matrix contributes neither to the stiffness nor to the energy dissipation of tendons. Secondly, the model brings insights about microscale mechanics of tendon fascicles not completely understood: prediction of uncoiling of fibers during axial loads which may explain the large apparent Poisson ratios and fluid loss, and significant strain localization in cells, which may lead to important mechanotransduction mechanisms. Moreover, the distribution of dissipated power became available, pointing out the fibrils as the main source of dissipation of fascicles under high macroscopic strain rates and during the unloading phase in cyclic regimes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Svensson, R.B., Hassenkam, T., Grant, C.A., Peter Magnusson, S.: Tensile properties of human collagen fibrils and fascicles are insensitive to environmental salts. Biophys. J. 99(12), 4020–4027 (2010). ISSN 00063495

    Article  ADS  Google Scholar 

  2. Vergari, C., Pourcelot, P., Holden, L., Ravary-Plumioën, B., Gerard, G., Laugier, P., Mitton, D., Crevier-Denoix, N.: True stress and Poisson’s ratio of tendons during loading. J. Biomech. 44(4), 719–724 (2011). ISSN 00219290

    Article  Google Scholar 

  3. Chernak, L.A., Thelen, D.G.: Tendon motion and strain patterns evaluated with two-dimensional ultrasound elastography. J. Biomech. 45(15), 2618–2623 (2012)

    Article  Google Scholar 

  4. Reese, S.P., Weiss, J.: Tendon fascicles exhibit a linear correlation between poisson’s ratio and force during uniaxial stress relaxation. J. Biomech. Eng. 135(3), 34501 (2013). ISSN 1528-8951

    Article  Google Scholar 

  5. Böl, M., Ehret, A.E., Leichsenring, K., Ernst, M.: Tissue-scale anisotropy and compressibility of tendon in semi-confined compression tests. J. Biomech. 48(6), 1092–1098 (2015)

    Article  Google Scholar 

  6. Lynch, H.A., Johannessen, W., Wu, J.P., Jawa, A., Elliott, D.M.: Effect of fiber orientation and strain rate on nonlinear tendon tensile properties. J. Biomech. Eng. 125, 726–731 (2003)

    Article  Google Scholar 

  7. Ahmadzadeh, H., Freedman, B.R., Connizzo, B.K., Soslowsky, L.J., Shenoy, V.B.: Micromechanical poroelastic finite element and shear-lag models of tendon predict large strain dependent Poisson’s ratios and fluid expulsion under tensile loading. Acta Biomaterialia 22, 83–91 (2014)

    Article  Google Scholar 

  8. Kannus, P.: Structure of the tendon connective tissue. Scand. J. Med. Sci. Sports 10(6), 312–320 (2000)

    Article  Google Scholar 

  9. Franchi, M., Trirè, A., Quaranta, M., Orsini, E., Ottani, V.: Collagen structure of tendon relates to function. TheScientificWorldJournal 7, 404–420 (2007)

    Article  Google Scholar 

  10. Thorpe, C.T., Birch, H.L., Clegg, P.D., Screen, H.R.C.: Tendon physiology and mechanical behavior: structure-function relationships. In: Gomes, M.E., Reis, R.L., Rodrigues, M.T. (eds.) Tendon Regeneration: Understanding Tissue Physiology and Development to Engineer Functional Substitutes, Chap. 1, pp. 3–39. Elsevier Academic Press, Cambridge (2015)

    Chapter  Google Scholar 

  11. Svensson, R.B., Hassenkam, T., Hansen, P., Peter Magnusson, S.: Viscoelastic behavior of discrete human collagen fibrils. J Mech Behav Biomed Mater 3(1), 112–115 (2010b)

    Article  Google Scholar 

  12. Shen, Z.L., Kahn, H., Ballarini, R., Eppell, S.J.: Viscoelastic properties of isolated collagen fibrils. Biophys J 100(12), 3008–3015 (2011)

    Article  Google Scholar 

  13. Yang, L., van der Werf, K.O., Dijkstra, P.J., Feijen, J., Bennink, M.L.: Micromechanical analysis of native and cross-linked collagen type I fibrils supports the existence of microfibrils. J Mech Behav Biomed Mater 6, 148–158 (2012)

    Article  Google Scholar 

  14. Blanco, P.J., Sanchez, P.J., de Souza Neto, E.A., Feijo, R.A.: Variational Foundations and generalized unified theory of RVE-based multiscale models. Arch Comput Methods Eng 23(2), 191–253 (2014). ISSN 18861784

    Article  MathSciNet  MATH  Google Scholar 

  15. de Souza Neto, E., Blanco, P.J., Sánchez, P.J., Feijóo, R.: An RVE-based multiscale theory of solids with micro-scale inertia and body force effects. Mech Mater 80, 136–144 (2015)

    Article  Google Scholar 

  16. Lanir, Y.: Multi-scale structural modeling of soft tissues mechanics and mechanobiology. J Elast 129(1–2), 7–48 (2017). https://doi.org/10.1007/s10659-016-9607-0. ISSN 15732681

    Article  MathSciNet  MATH  Google Scholar 

  17. Fang, F., Lake, S.P.: Modelling approaches for evaluating multiscale tendon mechanics. Interface Focus, 6 (2016)

  18. Marino, M., Vairo, G.: Stress and strain localization in stretched collagenous tissues via a multiscale modelling approach. Comput. Methods Biomech. Biomed. Eng. 1–20 (2012)

  19. Herchenhan, A., Kalson, N.S., Holmes, D.F., Hill, P., Kadler, K.E., Margetts, L.: Tenocyte contraction induces crimp formation in tendon-like tissue. Biomech. Model. Mechanobiol. 11(3–4), 449–459 (2012)

    Article  Google Scholar 

  20. Fallah, A., Ahmadian, M.T., Firozbakhsh, K., Aghdam, M.M.: Micromechanics and constitutive modeling of connective soft tissues. J. Mech. Behav. Biomed. Mater. 60, 157–176 (2016). https://doi.org/10.1016/j.jmbbm.2015.12.029

    Article  Google Scholar 

  21. Ganghoffer, J.F., Laurent, C., Maurice, G., Rahouadj, R., Wang, X.: Nonlinear viscous behavior of the tendon’s fascicles from the homogenization of viscoelastic collagen fibers. Eur. J. Mech. A/Solids 59, 265–279 (2016). https://doi.org/10.1016/j.euromechsol.2016.04.006

    Article  ADS  MathSciNet  MATH  Google Scholar 

  22. Ortiz, M., Stainier, L.: The variational formulation of viscoplastic constitutive updates. Comput. Methods Appl. Mech. Eng. 7825(98), 419–444 (1999)

    Article  ADS  MathSciNet  MATH  Google Scholar 

  23. Fancello, E., Ponthot, J.-P., Stainier, L.: A variational formulation of constitutive models and updates in non-linear finite viscoelasticity. Int. J. Numer. Methods Eng. 65(11), 1831–1864 (2006)

    Article  MATH  Google Scholar 

  24. Mosler, J., Bruhns, O.T.: On the implementation of rate-independent standard dissipative solids at finite strain—Variational constitutive updates. Comput. Methods Appl. Mech. Eng. 199(9–12), 417–429 (2010)

    Article  ADS  MathSciNet  MATH  Google Scholar 

  25. Vassoler, J.M., Reips, L., Fancello, E.A.: A variational framework for fiber-reinforced viscoelastic soft tissues. Int. J. Numer. Methods Eng. 89(13), 1691–1706 (2012)

    Article  MathSciNet  MATH  Google Scholar 

  26. Kalson, N.S., Lu, Y., Taylor, S.H., Starborg, T., Holmes, D.F., Kadler, K.E.: A structure-based extracellular matrix expansion mechanism of fibrous tissue growth. eLife, 4 (2015). ISSN 2050-084X

  27. Aifantis, K.E., Shrivastava, S., Odegard, G.M.: Transverse mechanical properties of collagen fibers from nanoindentation. J. Mater. Sci.: Mater. Med. 22(6), 1375–1381 (2011)

    Google Scholar 

  28. Haga, H., Sasaki, S., Kawabata, K., Ito, E., Ushiki, T., Sambongi, T.: Elasticity mapping of living fibroblasts by AFM and immunofluorescence observation of the cytoskeleton. Ultramicroscopy 82, 253–258 (2000). ISSN 03043991

    Article  Google Scholar 

  29. Sirghi, L., Ponti, J., Broggi, F., Rossi, F.: Probing elasticity and adhesion of live cells by atomic force microscopy indentation. Eur. Biophys. J. 37(6), 935–945 (2008). ISSN 01757571

    Article  Google Scholar 

  30. Raman, A., Trigueros, S., Cartagena, A., Stevenson, P.Z., Susilo, M., Nauman, E., Antoranz Contera, S.: Mapping nanomechanical properties of live cells using multi-harmonic atomic force microscopy. Nat. Nanotechnol. 6(12), 809–814 (2011)

    Article  ADS  Google Scholar 

  31. Nawaz, S., Sánchez, P., Bodensiek, K., Li, S., Simons, M., Schaap, I.A.T.: Cell visco-elasticity measured with AFM and optical trapping at sub-micrometer deformations. PLoS ONE 7(9), (2012). ISSN 19326203

  32. Hecht, F.M., Rheinlaender, J., Schierbaum, N., Goldmann, W.H., Fabry, B., Schäffer, T.E.: Imaging viscoelastic properties of live cells by AFM: power-law rheology on the nanoscale. Soft Matter 11(23), 4584–4591 (2015). ISSN 1744-6848

    Article  ADS  Google Scholar 

  33. Thorpe, C.T., Udeze, C.P., Birch, H.L., Clegg, P.D., Screen, H.R.C.: Specialization of tendon mechanical properties results from interfascicular differences. J. R. Soc. Interface 9(July), 3108–3117 (2012)

    Article  Google Scholar 

  34. de Aro, A.A., de Campos Vidal, B., Rosa Pimentel, E.: Biochemical and anisotropical properties of tendons. Micron 43(2–3), 205–214 (2012)

    Google Scholar 

  35. Starborg, T., Kalson, N.S., Lu, Y., Mironov, A., Cootes, T.F., Holmes, D.F., Kadler, K.E.: Using transmission electron microscopy and 3View to determine collagen fibril size and three-dimensional organization. Nat. Protoc. 8(7), 1433–48 (2013). ISSN 1750-2799

    Article  Google Scholar 

  36. Provenzano, P.P., Vanderby, R.: Collagen fibril morphology and organization: implications for force transmission in ligament and tendon. Matrix Biol. 25(2), 71–84 (2006). ISSN 0945053X

    Article  Google Scholar 

  37. Buehler, M.J.: Nature designs tough collagen: explaining the nanostructure of collagen fibrils. Proc. Nat. Acad. Sci. USA 103, 12285–12290 (2006)

    Article  ADS  Google Scholar 

  38. Svensson, R.B., Mulder, H., Kovanen, V., Peter Magnusson, S.: Fracture mechanics of collagen fibrils: influence of natural cross-links. Biophys. J. 104(11), 2476–2484 (2013)

    Article  ADS  Google Scholar 

  39. Gurtin, M.E., Anand, L.: The decomposition F = FeFp, material symmetry, and plastic irrotationality for solids that are isotropic-viscoplastic or amorphous. Int. J. Plast. 21(9), 1686–1719 (2005). ISSN 07496419

    Article  MATH  Google Scholar 

  40. Nguyen, T.D., Jones, R.E., Boyce, B.L.: Modeling the anisotropic finite-deformation viscoelastic behavior of soft fiber-reinforced composites. Int. J. Solids Struct. 44, 8366–8389 (2007)

    Article  MATH  Google Scholar 

  41. Schröder, J., Neff, P.: Invariant formulaiton of hyperelastic transverse isotropy based on polyconvex free energy functions. Int. J. Solids Struct. 40(2), 401–445 (2003). ISSN 00207683

    Article  MATH  Google Scholar 

  42. Merodio, J., Ogden, R.W.: Mechanical response of fiber-reinforced incompressible non-linearly elastic solids. Int. J. Non-Linear Mech. 40(2–3), 213–227 (2005). ISSN 00207462

    Article  ADS  MATH  Google Scholar 

  43. Ehret, A.E., Itskov, M.: A polyconvex hyperelastic model for fiber-reinforced materials in application to soft tissues. J. Mater. Sci. 42(21), 8853–8863 (2007). ISSN 00222461

    Article  ADS  Google Scholar 

  44. Holzapfel, G., Ogden, R.W.: Constitutive modelling of passive myocardium: a structurally based framework for material characterization. Philos. Trans. Ser. A Math. Phys. Eng. Sci. 367(1902), 3445–75 (2009). ISSN 1364-503X

    Article  ADS  MathSciNet  MATH  Google Scholar 

  45. Balzani, D., Neff, P., Schröder, J., Holzapfel, G.: A polyconvex framework for soft biological tissues. Adjustment to experimental data. Int. J. Solids Struct. 43(20), 6052–6070 (2006). ISSN 00207683

    Article  MathSciNet  MATH  Google Scholar 

  46. de Souza Neto, E.A., Peric, D., Owen, D.R.J.: Computational methods for plasticity: Theory Appl. (2009)

  47. Gurtin, M.E., Fried, E., Anand, L.: The Mechanics and Thermodynamics of Continua. Cambridge University Press, Cambridge (2010)

    Book  Google Scholar 

  48. Carniel, T.A., Fancello, E.A.: Modeling the local viscoelastic behavior of living cells under nanoindentation tests. Latin Am. J. Solids Struct. 1–19 (2017)

  49. Vaz Jr., M., Cardoso, E.L., Stahlschmidt, J.: Particle swarm optimization and identification of inelastic material parameters. Eng. Comput. 30(7), 936–960 (2013). ISSN 0264-4401

    Article  Google Scholar 

  50. Screen, H.R.: Hierarchical approaches to understanding tendon mechanics. J. Biomech. Sci. Eng. 4(4), 481–499 (2009)

    Article  Google Scholar 

  51. Svensson, R.B., Herchenhan, A., Starborg, T., Larsen, M., Kadler, K.E., Qvortrup, K., Peter M.S.: Evidence of structurally continuous collagen fibrils in tendon. Acta Biomaterialia, 1–9 (2017)

  52. Nguyen, V.D., Béchet, E., Geuzaine, C., Noels, L.: Imposing periodic boundary condition on arbitrary meshes by polynomial interpolation. Comput. Mater. Sci. 55, 390–406 (2012). ISSN 09270256

    Article  Google Scholar 

  53. Hansen, K., Weiss, J., Barton, J.K.: Imposing periodic boundary condition on arbitrary meshes by polynomial interpolation. J. Biomech. Eng. 124(1), 72–77 (2002). ISSN 01480731

    Article  Google Scholar 

  54. Connizzo, B.K., Yannascoli, S.M., Soslowsky, L.J.: Structure–function relationships of postnatal tendon development: a parallel to healing. Matrix Biol. 32(2), 106–116 (2013)

    Article  Google Scholar 

  55. Cheng, V.W.T., Screen, H.R.C.: The micro-structural strain response of tendon. J. Mater. Sci. 42(21), 8957–8965 (2007). ISSN 00222461

    Article  ADS  Google Scholar 

  56. Goh, K.L., Holmes, D.F., Lu, H.-Y., Richardson, S., Kadler, K.E., Purslow, P.P., Wess, T.J.: Ageing changes in the tensile properties of tendons: influence of collagen fibril volume fraction. J. Biomech. Eng. 130(2), 021011 (2008). ISSN 01480731

    Article  Google Scholar 

  57. Screen, H.R.C., Seto, J., Krauss, S., Boesecke, P., Gupta, H.S.: Extrafibrillar diffusion and intrafibrillar swelling at the nanoscale are associated with stress relaxation in the soft collagenous matrix tissue of tendons. Soft Matter 7(23), 11243–11251 (2011). ISSN 1744-683X

    Article  ADS  Google Scholar 

  58. Szczesny, S.E., Elliott, D.M.: Incorporating plasticity of the interfibrillar matrix in shear lag models is necessary to replicate the multiscale mechanics of tendon fascicles. J. Mech. Behav. Biomed. Mater. 40, 325–338 (2014)

    Article  Google Scholar 

  59. Legerlotz, K., Riley, G.P., Screen, H.R.C.: Specimen dimensions influence the measurement of material properties in tendon fascicles. J. Biomech. 43(12), 2274–2280 (2010)

    Article  Google Scholar 

  60. Haraldsson, B.T., Aagaard, P., Krogsgaard, M., Alkjaer, M., Magnusson, S.P.: Regoin-specific mechanical properties of the human patella tendon. J. Appl. Physiol. 98, 1006–1007 (2005)

    Article  Google Scholar 

  61. Akhtar, R., Schwarzer, N., Sherratt, M.J., Watson, R.E.B., Graham, H.K., Trafford, W., Mummery, P.M., Derby, B.: Nanoindentation of histological specimens: mapping the elastic properties of soft tissues. J. Mater. Res. 24(3), 638–646 (2009). ISSN 0884-2914

    Article  ADS  Google Scholar 

  62. Hammer, N., Huster, D., Fritsch, S., Hädrich, C., Koch, H., Schmidt, P., Sichting, F., Franz Xaver Wagner, M., Boldt, A.: Do cells contribute to tendon and ligament biomechanics? PLoS ONE (2014). ISSN 19326203. https://doi.org/10.1371/journal.pone.0105037

  63. Herbert, A., Brown, C., Rooney, P., Kearney, J., Ingham, E., Fisher, J.: Bi-linear mechanical property determination of acellular human patellar tendon grafts for use in anterior cruciate ligament replacement. J. Biomech. 49(9), 1607–1612 (2016). https://doi.org/10.1016/j.jbiomech.2016.03.041. ISSN 18732380

    Article  Google Scholar 

  64. Depalle, B., Qin, Z., Shefelbine, S.J., Buehler, M.J.: Influence of cross-link structure, density and mechanical properties in the mesoscale deformation mechanisms of collagen fibrils. J. Mech. Behav. Biomed. Mater. 1–13 (2014)

  65. Liu, Y., Ballarini, R., Eppell, S.J.: Tension tests on mammalian collagen fibrils. Interface Focus 6(1), 20150080 (2016). ISSN 2042-8898

    Article  Google Scholar 

  66. Simo, J.C., Taylor, R.L.: Consistent tangent operators for rate-independent elastoplasticity. Comput. Methods Appl. Mech. Eng. 48(1), 101–118 (1985)

    Article  ADS  MATH  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Eduardo Alberto Fancello.

Additional information

Communicated by Andreas Öchsner.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Carniel, T.A., Fancello, E.A. A variational homogenization approach applied to the multiscale analysis of the viscoelastic behavior of tendon fascicles. Continuum Mech. Thermodyn. 31, 607–626 (2019). https://doi.org/10.1007/s00161-018-0714-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00161-018-0714-y

Keywords

Navigation