Skip to main content
Log in

Reduced Parameter Formulation for Incorporating Fiber Level Viscoelasticity into Tissue Level Biomechanical Models

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Collagen is known to be a viscoelastic material and therefore is an important source of time dependent behavior in soft tissue. Though there are material models for soft tissue that rely on properties and structure of constituent collagen fibers, such models generally utilize only the elastic properties of collagen, and thus the resulting tissue level response does not possess any viscoelastic features. Here, the time dependent properties of collagen are directly incorporated into a fiber based hyperelastic model using the one dimensional theory of quasi-linear viscoelasticity within the context of a locally defined, anisotropic representation of extracellular matrix structure. The resulting model possesses seven material parameters and, using numerical and computational analysis, is shown to successfully predict many key features of soft tissue response including anisotropy, strain hardening, preconditioning, and rate independent hysteresis. A formulation is also introduced for incorporating fiber level viscoelasticity into structural models derived from a continuous representation of fiber structure.

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.

FIGURE 1.
FIGURE 2.
FIGURE 3.
FIGURE 4.
FIGURE 5.
FIGURE 6.
FIGURE 7.

Similar content being viewed by others

REFERENCES

  1. Abramowitch, S. D., S. L.-Y. Woo, T. D. Clineff, and R. E. Debski. An evaluation of the quasi-linear viscoelastic properties of the healing medial collateral ligament in a goat model. Ann. Biomed. Eng. 32(3):329–335, 2004.

    Article  PubMed  Google Scholar 

  2. Best, T. M., J. McElhaney, W. E. Garrett, and B. S. Myers. Characterization of the passive responses of live skeletal muscle using the quasi-linear theory of viscoelasticity. J. Biomech. 27:413–419, 1994.

    Article  PubMed  CAS  Google Scholar 

  3. Billiar, K. L. and M. S. Sacks. Biaxial mechanical properties of the natural and gluteraldehyde treated aortic valve cusp—Part I: Experimental results. J. Biomech. Eng. 122:23–30, 2000a.

    Article  PubMed  CAS  Google Scholar 

  4. Billiar, K. L., and M. S. Sacks. Biaxial mechanical properties of the natural and gluteraldehyde treated aortic valve cusp—Part II: A structural constitutive model. J. Biomech. Eng. 122:327–335, 2000b.

    Article  PubMed  CAS  Google Scholar 

  5. Bischoff, J. E. Static indentation of anisotropic biomaterials using axially asymmetric indenters—A computational study. J. Biomech. Eng. 126(4):498–505, 2004.

    Article  PubMed  Google Scholar 

  6. Bischoff, J. E., E. M. Arruda, and K. Grosh. Orthotropic hyperelasticity in terms of an arbitrary molecular chain model. J. Appl. Mech. 69(2):198–201, 2002a.

    Article  CAS  Google Scholar 

  7. Bischoff, J. E., E. M. Arruda, and K. Grosh. A microstructurally based orthotropic hyperelastic constitutive law. J. Appl. Mech. 69:570–579, 2002b.

    Article  CAS  Google Scholar 

  8. Bischoff, J. E., E. M. Arruda, and K. Grosh. A rheological network model for the continuum anisotropic and viscoelastic behavior of soft tissue. Biomech. Modeling Mechanobiol. 3(1):56–65, 2004.

    Article  Google Scholar 

  9. Carew, E. O., E. A. Talman, D. R. Boughnew, and I. Vesely. Quasi-linear viscoelastic theory applied to internal shearing of porcine aortic valve leaflets. J. Biomech. Eng. 121:386–392, 1999.

    Article  PubMed  CAS  Google Scholar 

  10. Decraemer, W. F., M. A. Maes, V. J. Vanhuyse, and P. Vanpeperstraete. A non-linear viscoelastic constitutive equation for soft biological tissues, based upon a structural model. J. Biomech. 13:559–564, 1980.

    Article  PubMed  CAS  Google Scholar 

  11. Doehring, T. C., E. O. Carew, and I. Vesely. The effect of strain rate on the viscoelastic response of aortic valve tissue: A direct fit approach. Ann. Biomed. Eng. 32(2):223–232, 2004.

    Article  PubMed  Google Scholar 

  12. Fung, Y. C. Stress-strain-history relations of soft tissues in simple elongation. In: Biomechanics: Its Foundations and Objectives, edited by Y. C. Fung, N. Perrone, and M. Anliker. Englewood Cliffs, Prentice-Hall, 1972.

  13. Fung, Y. C. Biomechanics: Mechanical Properties of Living Tissues, 2nd ed. New York: Springer-Verlag, Inc., 1993.

  14. Gutsmann, T., G. E. Fantner, J. H. Kindt, M. Venturone, S. Danielsen, and P. K. Hansma. Force spectroscopy of collagen fibers to investigate their mechanical properties and structural organization. Biophys. J. 86:3186–3193, 2004.

    Article  PubMed  CAS  Google Scholar 

  15. Haut, R. C., and R. W. Little. A constitutive equation for collagen fibers. J. Biomech. 5:423–430, 1972.

    Article  PubMed  CAS  Google Scholar 

  16. Holzapfel, G. A., and T. C. Gasser. A viscoelastic model for fiber-reinforced composites at finite strains: Continuum basis, computational aspects and applications. Comp. Methods Appl. Mech. Eng. 190:4379–4403, 2001.

    Article  Google Scholar 

  17. Johnson, G. A., D. M. Tramaglini, R. E. Levine, K. Ohno, N.-Y. Choi, and S. L. Y. Woo. Tensile and viscoelastic properties of human patellar tendon. J. Orthopaed. Res. 12:796–803, 1994.

    Article  CAS  Google Scholar 

  18. Kwan, M. K., T. H. C. Lin, and S. L. Y. Woo. On the viscoelastic properties of the anteromedial bundle of the anterior cruciate ligament. J. Biomech. 26(4/5):447–452, 1993.

    Article  PubMed  CAS  Google Scholar 

  19. Lanir, Y. A structural theory for the homogeneous biaxial stress-strain relationships in flat collagenous tissues. J. Biomech. 12:423–426, 1979.

    Article  PubMed  CAS  Google Scholar 

  20. Lanir, Y. A microstructural model for the rheology of mammalian tendon. J. Biomech. 102:332–339, 1980.

    Article  CAS  Google Scholar 

  21. Lanir, Y. Constitutive equations for fibrous connective tissues. J. Biomech. 16(1):1–12, 1983

    Article  PubMed  CAS  Google Scholar 

  22. Limbert, G., and J. Middleton. A transversely isotropic viscohyperelastic material—Application to the modeling of biological soft connective tissues. Int. J. Solids Struct. 41:4237–4260, 2004.

    Article  Google Scholar 

  23. Nagatomi, J., D. C. Gloeckner, M. B. Chancellor, W. C. DeGroat, and M. S. Sacks. Changes in the biaxial viscoelastic response of the urinary bladder following spinal cord injury. Ann. Biomed. Eng. 32(10):1409–1419, 2004.

    Article  PubMed  Google Scholar 

  24. Pioletti, D. P., and L. R. Rakotomanana. Non-linear viscoelastic laws for soft biological tissues. Eur. J. Mech. A/Solids 19:749–759, 2000.

    Article  Google Scholar 

  25. Provenzano, P., R. Lakes, T. Keenan, and R. Vanderby, Jr. Nonlinear ligament viscoelasticity. Ann. Biomed. Eng. 29:908–914, 2001.

    Article  PubMed  CAS  Google Scholar 

  26. Puso, M. A., and J. A. Weiss. Finite element implementation of anisotropic quasi-linear viscoelasticity using a discrete spectrum approximation. J. Biomech. Eng. 120:62–70, 1998.

    Article  PubMed  CAS  Google Scholar 

  27. Rubin, M. B., S. R. Bodner. A three-dimensional nonlinear model for dissipative response of soft tissue. Int. J. Solids Struc. 39:5081–5099, 2002.

    Article  Google Scholar 

  28. Sacks, M. S. Biaxial mechanical evaluation of planar biological materials. J. Elast. 61:199–246, 2000.

    Article  Google Scholar 

  29. Sacks, M. S. Incorporation of experimentally-derived fiber orientation into a structural constitutive model for planar collagenous tissues. J. Biomech. Eng. 125:280–287, 2003.

    Article  PubMed  Google Scholar 

  30. Sverdlik, A., and Y. Lanir. Time-dependent mechanical behavior of sheep digital tendons, including the effects of preconditioning. J. Biomech. Eng. 124:78–84, 2002.

    Article  PubMed  CAS  Google Scholar 

  31. Thornton, G. M., C. B. Frank, and N. G. Shrive. Ligament creep behavior can be predicted from stress relaxation by incorporating fiber recruitment. J. Rheol. 45(2):493–507, 2001.

    Article  CAS  Google Scholar 

  32. Woo, S. L. Y., M. A. Gomez, and W. H. Akeson. The time and history-dependent viscoelastic properties of canine medial collateral ligament. J. Biomech. Eng. 103:293–298, 1981.

    PubMed  CAS  Google Scholar 

Download references

ACKNOWLEDGMENT

The author gratefully acknowledges the work of Mr. Jing Lu in acquiring the experimental data presented in this paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jeffrey E. Bischoff.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bischoff, J.E. Reduced Parameter Formulation for Incorporating Fiber Level Viscoelasticity into Tissue Level Biomechanical Models. Ann Biomed Eng 34, 1164–1172 (2006). https://doi.org/10.1007/s10439-006-9124-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-006-9124-6

Keywords

Navigation