Abstract
The material properties of multipotent mesenchymal tissue change dramatically during the differentiation process associated with skeletal regeneration. Using a mechanobiological tissue differentiation concept, and homogeneous and isotropic simplifications of a fiber-reinforced poroelastic model of soft skeletal tissues, we have developed a mathematical approach for describing time-dependent material property changes during the formation of cartilage, fibrocartilage, and fibrous tissue under various loading histories. In this approach, intermittently imposed fluid pressure and tensile strain regulate proteoglycan synthesis and collagen fibrillogenesis, assembly, cross-linking, and alignment to cause changes in tissue permeability (k), compressive aggregate modulus (H A), and tensile elastic modulus (E). In our isotropic model, k represents the permeability in the least permeable direction (perpendicular to the fibers) and E represents the tensile elastic modulus in the stiffest direction (parallel to the fibers). Cyclic fluid pressure causes an increase in proteoglycan synthesis, resulting in a decrease in k and increase in H A caused by the hydrophilic nature and large size of the aggregating proteoglycans. It further causes a slight increase in E owing to the stiffness added by newly synthesized type II collagen. Tensile strain increases the density, size, alignment, and cross-linking of collagen fibers thereby increasing E while also decreasing k as a result of an increased flow path length. The Poisson's ratio of the solid matrix, ν s, is assumed to remain constant (near zero) for all soft tissues. Implementing a computer algorithm based on these concepts, we simulate progressive changes in material properties for differentiating tissues. Beginning with initial values of E=0.05 MPa, H A=0 MPa, and k=1×10–13 m4/Ns for multipotent mesenchymal tissue, we predict final values of E=11 MPa, H A=1 MPa, and k=4.8×10–15 m4/Ns for articular cartilage, E=339 MPa, H A=1 MPa, and k=9.5×10–16 m4/Ns for fibrocartilage, and E=1,000 MPa, H A=0 MPa, and k=7.5×10–16 m4/Ns for fibrous tissue. These final values are consistent with the values reported by other investigators and the time-dependent acquisition of these values is consistent with current knowledge of the differentiation process.
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References
Akizuki S, Mow VC, Müller F, Pita JC, Howell DS, Manicourt DH (1986) 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
Armstrong CG, Lai WM, Mow VC (1984) An analysis of the unconfined compression of articular cartilage. J Biomech Eng 106:165–173
Ateshian GA, Lai WM, Zhu WB, Mow VC (1994) An asymptotic solution for the contact of two biphasic cartilage layers. J Biomech 27:1347–1360
Ateshian GA, Warden WH, Kim JJ, Grelsamer RP, Mow VC (1997) Finite deformation biphasic material properties of bovine articular cartilage from confined compression experiments. J Biomech 30:1157–1164
Athanasiou KA, Agarwal A, Dzida FJ (1994) Comparative study of the intrinsic mechanical properties of the human acetabular and femoral head cartilage. J Orthop Res 12:340–349.
Athanasiou KA, Rosenwasser MP, Buckwalter JA, Malinin TI, Mow VC (1991) Interspecies comparisons of in situ intrinsic mechanical properties of distal femoral cartilage. J Orthop Res 9:330–340
Atkinson TS, Haut RC, Altiero NJ (1997) A poroelastic model that predicts some phenomenological responses of ligaments and tendons. J Biomech Eng 119:400–405
Beynnon B, Howe JG, Pope MH, Johnson RJ, Fleming BC (1992) The measurement of anterior cruciate ligament strain in vivo. Int Orthop 16:1–12
Biot M (1941) General theory of three-dimensional consolidation. J Appl Phys 12:155–164
Biot M (1955) Theory of elasticity and consolidation for a porous anisotropic solid. J Appl Phys 26:182–185
Brown TD, Singerman RJ (1986) Experimental determination of the linear biphasic constitutive coefficients of human fetal proximal femoral chondroepiphysis. J Biomech 19:597–605
Carter DR, Beaupré GS (2001) Skeletal tissue regeneration. In: Skeletal function and form: mechanobiology of skeletal development, aging and regeneration. Cambridge University Press, Cambridge
Carter DR, Beaupré, GS, Giori NJ, Helms JA (1998) Mechanobiology of skeletal regeneration. Clin Orthop Relat Res 331(355 Suppl):S41–S55
Carter DR, Giori N (1991) Effect of mechanical stress on tissue differentiation in the bony implant bed. In: Davies J (ed) The bone–biomaterial interface. University of Toronto Press, Toronto, pp 367–379
Carter DR, Loboa Polefka EG, Beaupré GS (2000) Mechanical influences on skeletal regeneration. In: Human biomechanics and injury prevention. Springer-Verlag, Berlin Heidelberg New York, pp 129–136
Chen CT, Malkus DS, Vanderby R, Jr (1998) A fiber matrix model for interstitial fluid flow and permeability in ligaments and tendons. Biorheology 35:103–118
Claes LE, Heigele CA (1999) Magnitudes of local stress and strain along bony surfaces predict the course and type of fracture healing. J Biomech 32:255–266
Derwin KA, Soslowsky LJ, Green WD, Elder SH (1994) A new optical system for the determination of deformations and strains: calibration characteristics and experimental results. J Biomech 27:1277–1285
Elliott DM, Guilak F, Vail TP, Wang JY, Setton LA (1999) Tensile properties of articular cartilage are altered by meniscectomy in a canine model of osteoarthritis. J Orthop Res 17:503–508
Evanko SP, Vogel KG (1990) Ultrastructure and proteoglycan composition in the developing fibrocartilaginous region of bovine tendon. Matrix 10:420–436
Giori NJ, Beaupré GS, Carter DR (1993) Cellular shape and pressure may mediate mechanical control of tissue composition in tendons. J Orthop Res 11:581–591
Giori NJ, Ryd L, Carter DR (1995) Mechanical influences on tissue differentiation at bone-cement interfaces. J Arthrop 10:514–522
Gu WY, Mao XG, Foster RJ, Weidenbaum M, Mow VC, Rawlins BA (1999) The anisotropic hydraulic permeability of human lumbar anulus fibrosus. Influence of age, degeneration, direction, and water content. Spine 24:2449–2455
Haridas B, Butler D, Malaviya P, Awad H, Boivin G, Smith F (1998) In vivo stresses correlate with cellular morphology in the fibrocartilage-rich region of the rabbit flexor tendon. In: Proceedings of the 44th Annual Meeting, Orthopaedic Research Society, New Orleans,La.
Higginson GR, Snaith JE (1979) The mechanical stiffness of articular cartilage in confined oscillating compression. Eng Med 8:11–14
Hodge WA, Carlson KL, Fijan RS, Burgess RG, Riley PO, Harris WH, Mann RW (1989) Contact pressures from an instrumented hip endoprosthesis. J Bone Joint Surg Am 71:1378–1386.
Howard PS, Kucich U, Taliwal R, Korostoff JM (1998) Mechanical forces alter extracellular matrix synthesis by human periodontal ligament fibroblasts. J Periodont Res 33:500–508
Huiskes R, van Driel W, Prendergast P, Soballe K (1997) A biomechanical regulatory model for periprosthetic fibrous-tissue differentiation. J Mater Sci Mater Med 8:785–788
Ilizarov GA (1989) The tension–stress effect on the genesis and growth of tissues. Part I. The influence of stability of fixation and soft-tissue preservation. Clin Orthop 238:249–281
Joshi MD, Suh JK, Marui T, Woo SL (1995) Interspecies variation of compressive biomechanical properties of the meniscus. J Biomed Mater Res 29:823–828
Jurvelin JS, Buschmann MD, Hunziker EB (1997) Optical and mechanical determination of Poisson's ratio of adult bovine humeral articular cartilage. J Biomech 30:235–241
Kember NF, Sissons HA (1976) Quantitative histology of the human growth plate. J Bone Joint Surg Br 58:426–435
Klein-Nulend J, Veldhuijzen JP, van de Stadt RJ, van Kampen GP, Kuijer R, Burger EH (1987) Influence of intermittent compressive force on proteoglycan content in calcifying growth plate cartilage in vitro. J Biol Chem 262: 15490–15495
Lai W, Mow V (1980) Drag-induced compression of articular cartilage during a permeation experiment. Biorheology 17:111–123
Levenston M, Frank E, Grodzinsky A (1998) Variationally derived 3-field finite element formulations for quasistatic poroelastic analysis of hydrated biological tissues. Comput Meth Appl Mech Eng 156:231–246
Li LP, Buschmann MD, Shirazi-Adl A (2000) A fibril reinforced nonhomogeneous poroelastic model for articular cartilage: inhomogeneous response in unconfined compression. J Biomech 33:1533–1541
Li LP, Soulhat J, Buschmann MD, Shirazi-Adl A (1999) Nonlinear analysis of cartilage in unconfined ramp compression using a fibril reinforced poroelastic model. Clin Biomech 14:673–682
Liu GT, Lavery LA, Schenck RC, Jr, Lanctot DR, Zhu CF, Athanasiou KA (1997) Human articular cartilage biomechanics of the second metatarsal intermediate cuneiform joint. J Foot Ankle Surg 36:367–374
Loboa E, Beaupré G, Carter D (2001) Mechanobiology of initial pseudarthrosis formation with oblique fractures. J Orthop Res 19:1067–1072
Mansour JM, Mow VC (1976) The permeability of articular cartilage under compressive strain and at high pressures. J Bone Joint Surg Am 58:509–516
Maroudas A, Muir H, Wingham J (1969) The correlation of fixed negative charge with glycosaminoglycan content of human articular cartilage. Biochim Biophys Acta 177:492–500
Meroi EA, Natali AN (1989) A numerical approach to the biomechanical analysis of bone fracture healing. J Biomed Eng 11:390–397
Mikic B, Carter DR (1995) Bone strain gage data and theoretical models of functional adaptation. J Biomech 28:465–469
Mow VC, Gibbs MC, Lai WM, Zhu WB, Athanasiou KA (1989) Biphasic indentation of articular cartilage—II. A numerical algorithm and an experimental study. J Biomech 22:853–861
Mow VC, Holmes MH, Lai WM (1984) Fluid transport and mechanical properties of articular cartilage: a review. J Biomech 17:377–394
Mow VC, Kuei SC, Lai WM, Armstrong CG (1980) Biphasic creep and stress relaxation of articular cartilage in compression? Theory and experiments. J Biomech Eng 102:73–84
Mow VC, Zhu W, Ratcliffe A (1991) Structure and function of articular cartilage and meniscus. In: Mow VC, Hayes WC (eds) Basic orthopaedic biomechanics. Raven Press, New York, pp 143–198
Pauwels F (1980) Biomechanics of the locomotor apparatus : contributions on the functional anatomy of the locomotor apparatus. Springer-Verlag, Berlin Heidelberg New York
Perren S, Cordey J (1980) The concept of interfragmentary strain. In: Uhthoff HK (ed) Current concepts of internal fixation of fractures. Springer-Verlag, New York Berlin Heidelberg, pp 63–77
Prendergast PJ, Huiskes R, Søballe K (1997) ESB Research Award 1996. Biophysical stimuli on cells during tissue differentiation at implant interfaces. J Biomech 30:539–548
Proctor CS, Schmidt MB, Whipple RR, Kelly MA, Mow VC (1989) Material properties of the normal medial bovine meniscus. J Orthop Res 7:771–782
Rockwood CA, Green DP, Bucholz RW (1991) Rockwood and Green's fractures in adults. Lippincott, Philadelphia, Pa.
Roth V, Mow VC (1980) The intrinsic tensile behavior of the matrix of bovine articular cartilage and its variation with age. J Bone Joint Surg Am 62:1102–1117
Roughley PJ, Lee ER (1994) Cartilage proteoglycans: structure and potential functions. Microsc Res Technol 28:385–397
Smith RL, Rusk SF, Ellison BE, Wessells P, Tsuchiya K, Carter DR, Caler WE, Sandell LJ, Schurman DJ (1996) In vitro stimulation of articular chondrocyte mRNA and extracellular matrix synthesis by hydrostatic pressure. J Orthop Res 14:53–60
Soltz MA, Ateshian GA (1998) Experimental verification and theoretical prediction of cartilage interstitial fluid pressurization at an impermeable contact interface in confined compression. J Biomech 31:927–934
Soltz MA, Ateshian GA (2000) Interstitial fluid pressurization during confined compression cyclical loading of articular cartilage. Ann Biomed Eng 28:150–159
Soulhat J, Buschmann MD, Shirazi-Adl A (1999) A fibril-network-reinforced biphasic model of cartilage in unconfined compression. J Biomech Eng 121:340–347
Spilker RL, Donzelli PS, Mow VC (1992) A transversely isotropic biphasic finite element model of the meniscus. J Biomech 25:1027–1045
Tissakht M, Ahmed AM (1995) Tensile stress–strain characteristics of the human meniscal material. J Biomech 28:411–422
Vogel KG, Ordög A, Pogány G, Oláh J (1993) Proteoglycans in the compressed region of human tibialis posterior tendon and in ligaments. J Orthop Res 11:68–77
Weiss J, Maakestad B, Nisbet J (2000) The permeability of human medial collateral ligament. In: Proceedings of the 46th Annual Meeting, Orthopaedic Research Society, Orlando, Fl.
Wren TA, Beaupré GS, Carter DR (1998) A model for loading-dependent growth, development, and adaptation of tendons and ligaments. J Biomech 31:107–114
Wren TA, Beaupré GS, Carter DR (2000) Mechanobiology of tendon adaptation to compressive loading through fibrocartilaginous metaplasia. J Rehabil Res Dev 37:135–143
Wren TA, Carter DR (1998) A microstructural model for the tensile constitutive and failure behavior of soft skeletal connective tissues. J Biomech Eng 120:55–61
Yamamoto N, Hayashi K, Kuriyama H, Ohno K, Yasuda K, Kaneda K (1992) Mechanical properties of the rabbit patellar tendon. J Biomech Eng 114: 332–337
Acknowledgements
We would like to thank Jay Henderson, Sandra Shefelbine, and Dr. R. Lane Smith for their helpful suggestions. Support for this work was provided by VA Merit Review project A501–4RA.
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Loboa, E.G., Wren, T.A.L., Beaupré, G.S. et al. Mechanobiology of soft skeletal tissue differentiation—a computational approach of a fiber-reinforced poroelastic model based on homogeneous and isotropic simplifications. Biomech Model Mechanobiol 2, 83–96 (2003). https://doi.org/10.1007/s10237-003-0030-7
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DOI: https://doi.org/10.1007/s10237-003-0030-7