Skip to main content

Mixture Theory for Modeling Biological Tissues: Illustrations from Articular Cartilage

  • Chapter
  • First Online:

Part of the book series: Studies in Mechanobiology, Tissue Engineering and Biomaterials ((SMTEB,volume 20))

Abstract

Mixture theory has been used for modeling hydrated biological tissues for several decades. This chapter reviews the basic foundation of mixture theory as applied to biphasic mixtures consisting of a porous-permeable deformable solid matrix and an interstitial fluid. Canonical problems of permeation, confined compression, and unconfined compression are analyzed from theory and compared to prior experimental measurements on articular cartilage, with an emphasis on studies that provide validations of theoretical predictions. A brief overview is also provided of the application of mixture theory to solute transport, reactive kinetics, and growth and remodeling.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   139.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   179.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Notes

  1. 1.

    Mow and Lai were this author’s doctoral advisors and mentors, starting in 1986.

References

  • Akizuki, S., Mow, V.C., Müller, F., Pita, J.C., Howell, D.S., Manicourt, D.H.: Tensile properties of human knee joint cartilage: I. Influence of ionic conditions, weight bearing, and fibrillation on the tensile modulus. J. Orthop. Res. 4, 379–392 (1986)

    Article  Google Scholar 

  • Albro, M.B., Chahine, N.O., Caligaris, M., Wei, V.I., Likhitpanichkul, M., Ng, K.W., Hung, C.T., Ateshian, G.A.: Osmotic loading of spherical gels: a biomimetic study of hindered transport in the cell protoplasm. J. Biomech. Eng. 129, 503–510 (2007)

    Article  Google Scholar 

  • Albro, M.B., Chahine, N.O., Li, R., Yeager, K., Hung, C.T., Ateshian, G.A.: Dynamic loading of deformable porous media can induce active solute transport. J. Biomech. 41, 3152–3157 (2008)

    Article  Google Scholar 

  • Albro, M.B., Petersen, L.E., Li, R., Hung, C.T., Ateshian, G.A.: Influence of the partitioning of osmolytes by the cytoplasm on the passive response of cells to osmotic loading. Biophys. J. 97, 2886–2893 (2009)

    Article  Google Scholar 

  • Albro, M.B., Li, R., Banerjee, R.E., Hung, C.T., Ateshian, G.A.: Validation of theoretical framework explaining active solute uptake in dynamically loaded porous media. J. Biomech. 43, 2267–2273 (2010)

    Article  Google Scholar 

  • Albro, M.B., Banerjee, R.E., Li, R., Oungoulian, S.R., Chen, B., del Palomar, A.P., Hung, C.T., Ateshian, G.A.: Dynamic loading of immature epiphyseal cartilage pumps nutrients out of vascular canals. J. Biomech. 44, 1654–1659 (2011)

    Article  Google Scholar 

  • Ambrosi, D., Ateshian, G.A., Arruda, E.M., Cowin, S.C., Dumais, J., Goriely, A., Holzapfel, G.A., Humphrey, J.D., Kemkemer, R., Kuhl, E., Olberding, J.E., Taber, L.A., Garikipati, K.: Perspectives on biological growth and remodeling. J. Mech. Phys. Solids 59, 863–883 (2011)

    Article  MathSciNet  MATH  Google Scholar 

  • Armstrong, C.G., Lai, W.M., Mow, V.C.: An analysis to unconfined compression of articular cartilage. J. Biomech. Eng. 106, 165–173 (1984)

    Article  Google Scholar 

  • Armstrong, C.G., Mow, V.C.: Variations in the intrinsic mechanical properties of human articular cartilage with age, degeneration, and water content. J. Bone Joint Surg. Am. 64, 88–94 (1982)

    Google Scholar 

  • Ateshian, G.A.: On the theory of reactive mixtures for modeling biological growth. Biomech. Model. Mechanobiol. 6, 423–445 (2007)

    Article  Google Scholar 

  • Ateshian, G.A.: Viscoelasticity using reactive constrained solid mixtures. J. Biomech. 48, 941–947 (2015)

    Article  Google Scholar 

  • Ateshian, G.A., Humphrey, J.D.: Continuum mixture models of biological growth and remodeling: past successes and future opportunities. Annu. Rev. Biomed. Eng. 14, 97–111 (2012)

    Article  Google Scholar 

  • Ateshian, G.A., Ricken, T.: Multigenerational interstitial growth of biological tissues. Biomech. Model. Mechanobiol. 9, 689–702 (2010)

    Article  Google Scholar 

  • Ateshian, G.A., Warden, W.H., Kim, J.J., Grelsamer, R.P., Mow, V.C.: Finite deformation biphasic material properties of bovine articular cartilage from confined compression experiments. J. Biomech. 30, 1157–1164 (1997)

    Article  Google Scholar 

  • Ateshian, G.A., Likhitpanichkul, M., Hung, C.T.: A mixture theory analysis for passive transport in osmotic loading of cells. J. Biomech. 39, 464–475 (2006)

    Article  Google Scholar 

  • Ateshian, G.A., Maas, S., Weiss, J.A.: Finite element algorithm for frictionless contact of porous permeable media under finite deformation and sliding. J. Biomech. Eng. 132(061), 006 (2010)

    Google Scholar 

  • Ateshian, G.A., Albro, M.B., Maas, S., Weiss, J.A.: Finite element implementation of mechanochemical phenomena in neutral deformable porous media under finite deformation. J. Biomech. Eng. 133(081), 005 (2011)

    Google Scholar 

  • Ateshian, G.A., Maas, S., Weiss, J.A.: Solute transport across a contact interface in deformable porous media. J. Biomech. 45, 1023–1027 (2012)

    Article  Google Scholar 

  • Ateshian, G.A., Maas, S., Weiss, J.A.: Multiphasic finite element framework for modeling hydrated mixtures with multiple neutral and charged solutes. J. Biomech. Eng. 135(111), 001 (2013)

    Google Scholar 

  • Ateshian, G.A., Nims, R.J., Maas, S., Weiss, J.A.: Computational modeling of chemical reactions and interstitial growth and remodeling involving charged solutes and solid-bound molecules. Biomech. Model. Mechanobiol. 13, 1105–1120 (2014)

    Article  Google Scholar 

  • Azeloglu, E.U., Albro, M.B., Thimmappa, V.A., Ateshian, G.A., Costa, K.D.: Heterogeneous transmural proteoglycan distribution provides a mechanism for regulating residual stresses in the aorta. Am. J. Physiol. Heart Circ. Physiol. 294, H1197–1205 (2008)

    Article  Google Scholar 

  • Bachrach, N.M., Mow, V.C., Guilak, F.: Incompressibility of the solid matrix of articular cartilage under high hydrostatic pressures. J. Biomech. 31, 445–451 (1998)

    Article  Google Scholar 

  • Bayliss, M.T., Urban, J.P., Johnstone, B., Holm, S.: In vitro method for measuring synthesis rates in the intervertebral disc. J. Orthop. Res. 4, 10–17 (1986)

    Article  Google Scholar 

  • Bedford, A., Drumheller, D.S.: Recent advances theories of immiscible and structured mixtures. Int. J. Eng. Sci. 21, 863–960 (1983)

    Article  MathSciNet  MATH  Google Scholar 

  • Biot, M.A.: General theory of three-dimensional consolidation. J. Appl. Phys. 12, 155–164 (1941)

    Article  MATH  Google Scholar 

  • Boer, R.D.: Highlights in the historical development of the porous media theory: toward a consistent macroscopic theory. Appl. Mech. Rev. 49, 201–262 (1996)

    Article  Google Scholar 

  • Bowen, R.M.: Thermochemistry of reacting materials. J. Chem. Phys. 49, 1625–1637 (1968)

    Article  Google Scholar 

  • Bowen, R.M.: Theory of mixtures. In: Eringen, A.C. (ed.) Continuum Physics, vol. III, pp. 1–127. Academic Press, New York (1976)

    Chapter  Google Scholar 

  • Bowen, R.M.: Incompressible pourous media models by use of theory of mixture. Int. J. Eng. Sci. 18, 1129–1148 (1980)

    Article  MATH  Google Scholar 

  • Brown, T.D., Singerman, R.J.: Experimental determination of the linear biphasic constitutive coefficients of human fetal proximal femoral chondroepiphysis. J. Biomech. 19, 597–605 (1986)

    Article  Google Scholar 

  • Bryant, M.R., McDonnell, P.J.: A triphasic analysis of corneal swelling and hydration control. J. Biomech. Eng. 120, 370–381 (1998)

    Article  Google Scholar 

  • Bursać, P.M., Obitz, T.W., Eisenberg, S.R., Stamenović, D.: Confined and unconfined stress relaxation of cartilage: appropriateness of a transversely isotropic analysis. J. Biomech. 32, 1125–1130 (1999)

    Article  Google Scholar 

  • Chahine, N.O., Wang, C.C.B., Hung, C.T., Ateshian, G.A.: Anisotropic strain-dependent material properties of bovine articular cartilage in the transitional range from tension to compression. J. Biomech. 37, 1251–1261 (2004)

    Article  Google Scholar 

  • Chahine, N.O., Albro, M.B., Lima, E.G., Wei, V.I., Dubois, C.R., Hung, C.T., Ateshian, G.A.: Effect of dynamic loading on the transport of solutes into agarose hydrogels. Biophys. J. 97, 968–975 (2009)

    Article  Google Scholar 

  • Cohen, B., Lai, W.M., Mow, V.C.: A transversely isotropic biphasic model for unconfined compression of growth plate and chondroepiphysis. J. Biomech. Eng. 120, 491–496 (1998)

    Article  Google Scholar 

  • Coleman, B.D., Noll, W.: The thermodynamics of elastic materials with heat conduction and viscosity. Arch. Ration. Mech. Anal. 13, 167–178 (1963)

    Article  MathSciNet  MATH  Google Scholar 

  • Cowin, S.C.: The specific growth rates of tissues: a review and a re-evaluation. J. Biomech. Eng. 133(041), 001 (2011)

    Google Scholar 

  • Cowin, S.C., Hegedus, D.H.: Bone remodelling I: theory of adaptive elasticity. J. Elasticity 6, 313–326 (1976)

    Article  MathSciNet  MATH  Google Scholar 

  • Curnier, A., He, Q.-C., Zysset, P.: Conewise linear elastic materials. J. Elast. 37, 1–38 (1995)

    Article  MathSciNet  MATH  Google Scholar 

  • Deen, W.: Hindered transport of large molecules in liquid-filled pores. AIChE J 33, 1409–1425 (1987)

    Article  Google Scholar 

  • Eringen, A., Ingram, J.: Continuum theory of chemically reacting media - 1. Int. J. Eng. Sci. 3, 197–212 (1965)

    Article  Google Scholar 

  • Gailani, G., Benalla, M., Mahamud, R., Cowin, S.C., Cardoso, L.: Experimental determination of the permeability in the lacunar-canalicular porosity of bone. J. Biomech. Eng. 131(101), 007 (2009)

    Google Scholar 

  • Gu, W.Y., Lai, W.M., Mow, V.C.: Transport of fluid and ions through a porous-permeable charged-hydrated tissue, and streaming potential data on normal bovine articular cartilage. J. Biomech. 26, 709–723 (1993)

    Article  Google Scholar 

  • Gu, W.Y., Lai, W.M., Mow, V.C.: A mixture theory for charged-hydrated soft tissues containing multi-electrolytes: Passive transport and swelling behaviors. J. Biomech. Eng. 120, 169–180 (1998)

    Article  Google Scholar 

  • Gu, W.Y., Mao, X.G., Foster, R.J., Weidenbaum, M., Mow, V.C., Rawlins, B.A.: The anisotropic hydraulic permeability of human lumbar anulus fibrosus. influence of age, degeneration, direction, and water content. Spine (Phila Pa 1976) 24, 2449–2455 (1999)

    Google Scholar 

  • Harrison, R.G., Massaro, T.A.: Water flux through porcine aortic tissue due to a hydrostatic pressure gradient. Atherosclerosis 24, 363–367 (1976)

    Article  Google Scholar 

  • Holmes, M.: A theoretical analysis for determining the nonlinear hydraulic permeability of a soft tissue from a permeation experiment. Bull. Math. Biol. 47, 669–683 (1985)

    Article  Google Scholar 

  • Holmes, M.H., Mow, V.C.: The nonlinear characteristics of soft gels and hydrated connective tissues in ultrafiltration. J. Biomech. 23, 1145–1156 (1990)

    Article  Google Scholar 

  • Holmes, M.H., Lai, W.M., Mow, V.C.: Singular perturbation analysis of the nonlinear, flow-dependent compressive stress relaxation behavior of articular cartilage. J. Biomech. Eng. 107, 206–218 (1985)

    Article  Google Scholar 

  • Huang, C.-Y., Stankiewicz, A., Ateshian, G.A., Mow, V.C.: Anisotropy, inhomogeneity, and tension-compression nonlinearity of human glenohumeral cartilage in finite deformation. J. Biomech. 38, 799–809 (2005)

    Article  Google Scholar 

  • Humphrey, J.D., Rajagopal, K.R.: A constrained mixture model for growth and remodeling of soft tissues. Math. Model. Meth. Appl. Sci. 12, 407–430 (2002)

    Article  MathSciNet  MATH  Google Scholar 

  • Jurvelin, J., Buschmann, M., Hunziker, E.: Mechanical anisotropy of the human knee articular cartilage in compression. Proc Inst Mech Eng Part H: J Eng Med 217, 215–219 (2003)

    Article  Google Scholar 

  • Kempson, G.E., Freeman, M.A., Swanson, S.A.: Tensile properties of articular cartilage. Nature 220, 1127–1128 (1968)

    Article  Google Scholar 

  • Kenyon, D.E.: Transient filtration in a porous elastic cylinder. J. Appl. Mech. 43, 594–598 (1976)

    Article  Google Scholar 

  • Kwan, M.K., Lai, W.M., Mow, V.C.: A finite deformation theory for cartilage and other soft hydrated connective tissues-I. Equilib. Results J. Biomech. 23, 145–155 (1990)

    Google Scholar 

  • Lai, W.M., Mow, V.C., Roth, V.: Effects of nonlinear strain-dependent permeability and rate of compression on the stress behavior of articular cartilage. J. Biomech. Eng. 103, 61–66 (1981)

    Article  Google Scholar 

  • Lai, W.M., Hou, J.S., Mow, V.C.: A triphasic theory for the swelling and deformation behaviors of articular cartilage. J. Biomech. Eng. 113, 245–258 (1991)

    Article  Google Scholar 

  • Lai, W.M., Mow, V.C., Sun, D.D., Ateshian, G.A.: On the electric potentials inside a charged soft hydrated biological tissue: Streaming potential versus diffusion potential. J. Biomech. Eng. 122, 336–346 (2000)

    Article  Google Scholar 

  • Lanir, Y.: A structural theory for the homogeneous biaxial stress-strain relationships in flat collagenous tissues. J. Biomech. 12, 423–436 (1979)

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Li, L.P., Soulhat, J., Buschmann, M.D., Shirazi-Adl, A.: Nonlinear analysis of cartilage in unconfined ramp compression using a fibril reinforced poroelastic model. Clin. Biomech. (Bristol, Avon) 14, 673–682 (1999)

    Google Scholar 

  • Li, L.P., Buschmann, M.D., Shirazi-Adl, A.: A fibril reinforced nonhomogeneous poroelastic model for articular cartilage: Inhomogeneous response in unconfined compression. J. Biomech. 33, 1533–1541 (2000)

    Article  Google Scholar 

  • Maas, S.A., Ellis, B.J., Ateshian, G.A., Weiss, J.A.: FEBio: Finite elements for biomechanics. J. Biomech. Eng. 134(011), 005 (2012)

    Google Scholar 

  • Mak, A.F., Lai, W.M., Mow, V.C.: Biphasic indentation of articular cartilage-I. Theor. Anal. J. Biomech. 20, 703–714 (1987)

    Article  Google Scholar 

  • Mansour, J.M., Mow, V.C.: The permeability of articular cartilage under compressive strain and at high pressures. J. Bone Joint Surg. Am. 58, 509–516 (1976)

    Google Scholar 

  • Maroudas, A.I.: Balance between swelling pressure and collagen tension in normal and degenerate cartilage. Nature 260, 808–809 (1976)

    Article  Google Scholar 

  • Mauck, R.L., Hung, C.T., Ateshian, G.A.: Modeling of neutral solute transport in a dynamically loaded porous permeable gel: implications for articular cartilage biosynthesis and tissue engineering. J. Biomech. Eng. 125, 602–614 (2003)

    Article  Google Scholar 

  • Mow, V.C., Lai, W.M.: Recent developments in synovial joint biomechanics. SIAM Rev. 22, 275–317 (1980)

    Article  MathSciNet  MATH  Google Scholar 

  • Mow, V.C., Mansour, J.M.: The nonlinear interaction between cartilage deformation and interstitial fluid flow. J. Biomech. 10, 31–39 (1977)

    Article  Google Scholar 

  • Mow, V.C., Kuei, S.C., Lai, W.M., Armstrong, C.: Biphasic creep and stress relaxation of articular cartilage in compression: theory and experiments. J. Biomech. Eng. 102, 73–84 (1980)

    Article  Google Scholar 

  • Mow, V.C., Holmes, M.H., Lai, W.M.: Fluid transport and mechanical properties of articular cartilage: a review. J. Biomech. 17, 377–394 (1984)

    Article  Google Scholar 

  • Mow, V.C., Gibbs, M.C., Lai, W.M., Zhu, W.B., Athanasiou, K.A.: Biphasic indentation of articular cartilage-II. A numerical algorithm and an experimental study. J. Biomech. 22, 853–861 (1989)

    Article  Google Scholar 

  • Oloyede, A., Broom, N.: Is classical consolidation theory applicable to articular cartilage deformation? Clin. Biomech. (Bristol, Avon) 6, 206–212 (1991)

    Google Scholar 

  • Oloyede, A., Broom, N.: Stress-sharing between the fluid and solid components of articular cartilage under varying rates of compression. Connect. Tissue Res. 30, 127–141 (1993)

    Google Scholar 

  • Park, S., Krishnan, R., Nicoll, S.B., Ateshian, G.A.: Cartilage interstitial fluid load support in unconfined compression. J. Biomech. 36, 1785–1796 (2003)

    Article  Google Scholar 

  • Rice, J.R., Cleary, M.P.: Some basic stress diffusion solutions for fluid-saturated elastic porous media with compressible constituents. Rev. Geophys. Space Phys. 14, 227–241 (1976)

    Article  Google Scholar 

  • Schneiderman, R., Keret, D., Maroudas, A.: Effects of mechanical and osmotic pressure on the rate of glycosaminoglycan synthesis in the human adult femoral head cartilage: an in vitro study. J. Orthop. Res. 4, 393–408 (1986)

    Article  Google Scholar 

  • Soltz, M.A., Ateshian, G.A.: Experimental verification and theoretical prediction of cartilage interstitial fluid pressurization at an impermeable contact interface in confined compression. J. Biomech. 31, 927–934 (1998)

    Article  Google Scholar 

  • Soltz, M.A., Ateshian, G.A.: A conewise linear elasticity mixture model for the analysis of tension-compression nonlineartiy in articular cartilage. J. Biomech. Eng. 122, 576–586 (2000a)

    Article  Google Scholar 

  • Soltz, M.A., Ateshian, G.A.: Interstitial fluid pressurization during confined compression cyclical loading of articular cartilage. Ann. Biomed. Eng. 28, 150–159 (2000b)

    Article  Google Scholar 

  • Soulhat, J., Buschmann, M.D., Shirazi-Adl, A.: A fibril-network-reinforced biphasic model of cartilage in unconfined compression. J. Biomech. Eng. 121, 340–347 (1999)

    Article  Google Scholar 

  • Spilker, R.L., de Almeida, E.S., Donzelli, P.S.: Finite element methods for the biomechanics of soft hydrated tissues: nonlinear analysis and adaptive control of meshes. Crit. Rev. Biomed. Eng. 20, 279–313 (1992)

    Google Scholar 

  • Truesdell, C., Toupin, R.A.: The classical field theories. In: Flügge, S. (ed.) Encyclopedia of Physics, III(1), pp. 226–793. Springer, Berlin (1960)

    Google Scholar 

  • Vargas, C.B., Vargas, F.F., Pribyl, J.G., Blackshear, P.L.: Hydraulic conductivity of the endothelial and outer layers of the rabbit aorta. Am. J. Physiol. 236, H53–H60 (1979)

    Google Scholar 

  • Wan, W., Hansen, L., Gleason Jr., R.L.: A 3-D constrained mixture model for mechanically mediated vascular growth and remodeling. Biomech. Model. Mechanobiol. 9, 403–419 (2010)

    Article  Google Scholar 

  • Wang, C.C.B., Chahine, N.O., Hung, C.T., Ateshian, G.A.: Optical determination of anisotropic material properties of bovine articular cartilage in compression. J. Biomech. 36, 339–353 (2003)

    Article  Google Scholar 

  • Weiss, J.A., Maakestad, B.J.: Permeability of human medial collateral ligament in compression transverse to the collagen fiber direction. J. Biomech. 39, 276–283 (2006)

    Article  Google Scholar 

Download references

Acknowledgments

I would like to thank the many former and current doctoral students and fellows who labored with me over the years, performing experiments and validating the mixture models used in our investigations of biological tissues: Dr. Huiqun (Laura) Wang, Dr. William H. Warden, Dr. Michael A. Soltz, Prof. Robert L. Mauck, Prof. Chun-Yuh (Charles) Huang, Dr. Changbin Wang, Dr. Ramaswamy Krishnan, Prof. Seonghun Park, Prof. Ines M. Basalo, Prof. Nadeen O. Chahine, Dr. Michael B. Albro, Dr. Matteo M. Caligaris, Dr. Clare Canal-Guterl, Dr. Sevan R. Oungoulian, Dr. Alexander D. Cigan, Mr. Robert J. Nims, Mr. Brian K. Jones, Mr. Chieh Hou, and Ms. Krista M. Durney. I would also like to thank Dr. Albro for providing the experimental data appearing in Fig. 4, and Mr. Brandon K. Zimmerman for re-analyzing older data sets to produce Fig. 13.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gerard A. Ateshian .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Ateshian, G.A. (2017). Mixture Theory for Modeling Biological Tissues: Illustrations from Articular Cartilage. In: Holzapfel, G., Ogden, R. (eds) Biomechanics: Trends in Modeling and Simulation. Studies in Mechanobiology, Tissue Engineering and Biomaterials, vol 20. Springer, Cham. https://doi.org/10.1007/978-3-319-41475-1_1

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-41475-1_1

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-41473-7

  • Online ISBN: 978-3-319-41475-1

  • eBook Packages: EngineeringEngineering (R0)

Publish with us

Policies and ethics