Modelling of some biological materials using continuum mechanics

Continuum mechanics provides a mathematical framework for modelling the physical stresses experienced by a material. Recent studies show that physical stresses play an important role in a wide variety of biological processes, including dermal wound healing, soft tissue growth and morphogenesis. Thus, continuum mechanics is a useful mathematical tool for modelling a range of biological phenomena. Unfortunately, classical continuum mechanics is of limited use in biomechanical problems. As cells refashion the �bres that make up a soft tissue, they sometimes alter the tissue's fundamental mechanical structure. Advanced mathematical techniques are needed in order to accurately describe this sort of biological `plasticity'. A number of such techniques have been proposed by previous researchers. However, models that incorporate biological plasticity tend to be very complicated. Furthermore, these models are often di�cult to apply and/or interpret, making them of limited practical use. One alternative approach is to ignore biological plasticity and use classical continuum mechanics. For example, most mechanochemical models of dermal wound healing assume that the skin behaves as a linear viscoelastic solid. Our analysis indicates that this assumption leads to physically unrealistic results. In this thesis we present a novel and practical approach to modelling biological plasticity. Our principal aim is to combine the simplicity of classical linear models with the sophistication of plasticity theory. To achieve this, we perform a careful mathematical analysis of the concept of a `zero stress state'. This leads us to a formal de�nition of strain that is appropriate for materials that undergo internal remodelling. Next, we consider the evolution of the zero stress state over time. We develop a novel theory of `morphoelasticity' that can be used to describe how the zero stress state changes in response to growth and remodelling. Importantly, our work yields an intuitive and internally consistent way of modelling anisotropic growth. Furthermore, we are able to use our theory of morphoelasticity to develop evolution equations for elastic strain. We also present some applications of our theory. For example, we show that morphoelasticity can be used to obtain a constitutive law for a Maxwell viscoelastic uid that is valid at large deformation gradients. Similarly, we analyse a morphoelastic model of the stress-dependent growth of a tumour spheroid. This work leads to the prediction that a tumour spheroid will always be in a state of radial compression and circumferential tension. Finally, we conclude by presenting a novel mechanochemical model of dermal wound healing that takes into account the plasticity of the healing skin.

[1]  J. Sherratt,et al.  Theoretical models of wound healing: past successes and future challenges. , 2002, Comptes rendus biologies.

[2]  A. Singer,et al.  Management of local burn wounds in the ED. , 2007, The American journal of emergency medicine.

[3]  Jay D. Humphrey,et al.  Review Paper: Continuum biomechanics of soft biological tissues , 2003, Proceedings of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[4]  V. Lubarda,et al.  Symmetrization of the growth deformation and velocity gradients in residually stressed biomaterials , 2004 .

[5]  Athanasios C. Antoulas,et al.  Approximation of Large-Scale Dynamical Systems , 2005, Advances in Design and Control.

[6]  R T Tranquillo,et al.  The fibroblast-populated collagen microsphere assay of cell traction force--Part 2: Measurement of the cell traction parameter. , 1995, Journal of biomechanical engineering.

[7]  F. Grinnell,et al.  Contraction of hydrated collagen gels by fibroblasts: evidence for two mechanisms by which collagen fibrils are stabilized. , 1987, Collagen and related research.

[8]  G. Genin,et al.  Cellular and Matrix Contributions to Tissue Construct Stiffness Increase with Cellular Concentration , 2006, Annals of Biomedical Engineering.

[9]  G. Oster,et al.  Cell traction models for generating pattern and form in morphogenesis , 1984, Journal of mathematical biology.

[10]  T. N. Stevenson,et al.  Fluid Mechanics , 2021, Nature.

[11]  Donald E. Carlson,et al.  On the derivative of the square root of a tensor and Guo's rate theorems , 1984 .

[12]  R. Kessin,et al.  Dictyostelium: Cell Motility and the Cytoskeleton , 2001 .

[13]  En-Jui Lee Elastic-Plastic Deformation at Finite Strains , 1969 .

[14]  G I Zahalak,et al.  A cell-based constitutive relation for bio-artificial tissues. , 2000, Biophysical journal.

[15]  S C Cowin,et al.  Strain or deformation rate dependent finite growth in soft tissues. , 1996, Journal of biomechanics.

[16]  Adam Morecki Biomechanics of Motion , 1980 .

[17]  Pawel Herzyk,et al.  Phenotypic responses to mechanical stress in fibroblasts from tendon, cornea and skin. , 2006, The Biochemical journal.

[18]  B. Hinz,et al.  Myofibroblasts and mechano-regulation of connective tissue remodelling , 2002, Nature Reviews Molecular Cell Biology.

[19]  Andreas Karlsson,et al.  Matrix Analysis for Statistics , 2007, Technometrics.

[20]  C. Gans,et al.  Biomechanics: Motion, Flow, Stress, and Growth , 1990 .

[21]  Ben-yu Guo,et al.  Analytic solutions of the Fisher equation , 1991 .

[22]  P. Tracqui,et al.  Modelling Biological Gel Contraction by Cells: Mechanocellular Formulation and Cell Traction Force Quantification , 1997, Acta biotheoretica.

[23]  Frederick Grinnell,et al.  Fibroblast mechanics in 3D collagen matrices. , 2007, Advanced drug delivery reviews.

[24]  D. L. Sean McElwain,et al.  A Mixture Theory for the Genesis of Residual Stresses in Growing Tissues I: A General Formulation , 2005, SIAM J. Appl. Math..

[25]  W. Claycomb,et al.  Effect of mechanical loading on three-dimensional cultures of embryonic stem cell-derived cardiomyocytes. , 2008, Tissue engineering. Part A.

[26]  P K Maini,et al.  Spatio-temporal patterns in a mechanical model for mesenchymal morphogenesis , 1995, Journal of mathematical biology.

[27]  Patrick Perré,et al.  A Physical and Mechanical Model Able to Predict the Stress Field in Wood over a Wide Range of Drying Conditions , 2004 .

[28]  Patrick Perré,et al.  A large displacement formulation for anisotropic constitutive laws , 1999 .

[29]  R F Kallman,et al.  Migration and internalization of cells and polystyrene microsphere in tumor cell spheroids. , 1982, Experimental cell research.

[30]  Frederick Grinnell,et al.  Fibroblasts, myofibroblasts, and wound contraction , 1994, The Journal of cell biology.

[31]  S. Chien,et al.  Tumor cell cycle arrest induced by shear stress: Roles of integrins and Smad , 2008, Proceedings of the National Academy of Sciences.

[32]  D. Greenhalgh,et al.  The role of apoptosis in wound healing. , 1998, The international journal of biochemistry & cell biology.

[33]  A. McCulloch,et al.  Stress-dependent finite growth in soft elastic tissues. , 1994, Journal of biomechanics.

[34]  D. McGrouther,et al.  Keloid disease: clinical relevance of single versus multiple site scars. , 2005, British journal of plastic surgery.

[35]  J A Sherratt,et al.  A mathematical model for fibro-proliferative wound healing disorders. , 1996, Bulletin of mathematical biology.

[36]  Yubin Shi,et al.  Mechanical load initiates hypertrophic scar formation through decreased cellular apoptosis , 2007, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[37]  L O,et al.  A Mechanochemical Model for Adult Dermal Wound Contraction and the Permanence of the Contracted Tissue Displacement Profile , 1995 .

[38]  K. Krafts Tissue repair , 2010, Organogenesis.

[39]  R. Tranquillo,et al.  Temporal variations in cell migration and traction during fibroblast-mediated gel compaction. , 2003, Biophysical Journal.

[40]  Elliot L Elson,et al.  Thin bio-artificial tissues in plane stress: the relationship between cell and tissue strain, and an improved constitutive model. , 2005, Biophysical journal.

[41]  Extensions of the Jordan-Brouwer separation theorem and its converse , 1952 .

[42]  Raphael C. Lee,et al.  Prevention and treatment of excessive dermal scarring. , 2004, Journal of the National Medical Association.

[43]  R. Bird Dynamics of Polymeric Liquids , 1977 .

[44]  R. Tranquillo,et al.  Confined compression of a tissue-equivalent: collagen fibril and cell alignment in response to anisotropic strain. , 2002, Journal of biomechanical engineering.

[45]  W Matthew Petroll,et al.  Direct, dynamic assessment of cell-matrix interactions inside fibrillar collagen lattices. , 2003, Cell motility and the cytoskeleton.

[46]  L. Gibson,et al.  Contractile forces generated by articular chondrocytes in collagen-glycosaminoglycan matrices. , 2004, Biomaterials.

[47]  Keith Harding,et al.  Science, medicine and the future: healing chronic wounds. , 2002, BMJ.

[48]  Giulio Gabbiani,et al.  Perspective Article: Tissue repair, contraction, and the myofibroblast , 2005, Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society.

[49]  R K Jain,et al.  Compatibility and the genesis of residual stress by volumetric growth , 1996, Journal of mathematical biology.

[50]  R F Kallman,et al.  Effect of cytochalasin B, nocodazole and irradiation on migration and internalization of cells and microspheres in tumor cell spheroids. , 1986, Experimental cell research.

[51]  W. Eaglstein,et al.  THE PIG AS A MODEL FOR HUMAN WOUND HEALING , 2001, Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society.

[52]  Davide Carlo Ambrosi,et al.  Stress-Modulated Growth , 2007 .

[53]  T. Krieg,et al.  Interactions of fibroblasts with the extracellular matrix: implications for the understanding of fibrosis , 2004, Springer Seminars in Immunopathology.

[54]  J A Sherratt,et al.  Mathematical modelling of extracellular matrix dynamics using discrete cells: fiber orientation and tissue regeneration. , 1999, Journal of theoretical biology.

[55]  D. Ambrosi,et al.  Growth and dissipation in biological tissues , 2007 .

[56]  P N Watton,et al.  A mathematical model for the growth of the abdominal aortic aneurysm , 2004, Biomechanics and modeling in mechanobiology.

[57]  Y. Fung,et al.  Residual Stress in Arteries , 1986 .

[58]  Robert T. Tranquillo,et al.  Fibroblast‐populated collagen microsphere assay of cell traction force: Part 1. Continuum model , 1993 .

[59]  J A Sherratt,et al.  Keratinocyte growth factor signalling: a mathematical model of dermal-epidermal interaction in epidermal wound healing. , 2000, Mathematical biosciences.

[60]  Elliot L Elson,et al.  The relationship between cell and tissue strain in three-dimensional bio-artificial tissues. , 2005, Biophysical journal.

[61]  Mark Taylor,et al.  Bone remodelling inside a cemented resurfaced femoral head. , 2006, Clinical biomechanics.

[62]  H. Anton,et al.  Contemporary Linear Algebra , 2002 .

[63]  L. Taber Biomechanics of Growth, Remodeling, and Morphogenesis , 1995 .

[64]  Alan Wells,et al.  Extracellular matrix signaling through growth factor receptors during wound healing , 2004, Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society.

[65]  Victor H Barocas,et al.  Deterministic material-based averaging theory model of collagen gel micromechanics. , 2007, Journal of biomechanical engineering.

[66]  A. Desmoulière,et al.  Mechanical forces induce scar remodeling. Study in non-pressure-treated versus pressure-treated hypertrophic scars. , 1999, The American journal of pathology.

[67]  Jesse A Berlin,et al.  Diabetic neuropathic foot ulcers: predicting which ones will not heal. , 2003, The American journal of medicine.

[68]  Heng Xiao,et al.  Elastoplasticity beyond small deformations , 2006 .

[69]  John A. Pedersen,et al.  Mechanobiology in the Third Dimension , 2005, Annals of Biomedical Engineering.

[70]  Ben D MacArthur,et al.  Residual stress generation and necrosis formation in multi-cell tumour spheroids , 2004, Journal of mathematical biology.

[71]  V. Lubarda Constitutive theories based on the multiplicative decomposition of deformation gradient: Thermoelasticity, elastoplasticity, and biomechanics , 2004 .

[72]  A. Drozdov,et al.  A model for the volumetric growth of a soft tissue , 1997 .

[73]  Giuseppe Saccomandi,et al.  Topics in finite elasticity , 2001 .

[74]  S. V. Sotirchos,et al.  Mathematical modelling of microenvironment and growth in EMT6/Ro multicellular tumour spheroids , 1992, Cell proliferation.

[75]  Victor H Barocas,et al.  Microstructural mechanics of collagen gels in confined compression: poroelasticity, viscoelasticity, and collapse. , 2004, Journal of biomechanical engineering.

[76]  L. Gibson,et al.  Fibroblast contractile force is independent of the stiffness which resists the contraction. , 2002, Experimental cell research.

[77]  Anne Hoger,et al.  Residual stress in an elastic body: a theory for small strains and arbitrary rotations , 1993 .

[78]  David G Baer,et al.  Soft tissue wounds and principles of healing. , 2007, Emergency medicine clinics of North America.

[79]  J. Pearson,et al.  Expansions at small Reynolds numbers for the flow past a sphere and a circular cylinder , 1957, Journal of Fluid Mechanics.

[80]  Vlado A. Lubarda,et al.  On the mechanics of solids with a growing mass , 2002 .

[81]  R T Tranquillo,et al.  An anisotropic biphasic theory of tissue-equivalent mechanics: the interplay among cell traction, fibrillar network deformation, fibril alignment, and cell contact guidance. , 1997, Journal of biomechanical engineering.

[82]  D L S McElwain,et al.  A history of the study of solid tumour growth: The contribution of mathematical modelling , 2004, Bulletin of mathematical biology.

[83]  F. Hirche,et al.  Fibroblasts in Mechanically Stressed Collagen Lattices Assume a “Synthetic” Phenotype* , 2001, The Journal of Biological Chemistry.

[84]  H. D. Cavanagh,et al.  Effect of Cell Migration on the Maintenance of Tension on a Collagen Matrix , 2004, Annals of Biomedical Engineering.

[85]  Leila Cuttle,et al.  A porcine deep dermal partial thickness burn model with hypertrophic scarring. , 2006, Burns : journal of the International Society for Burn Injuries.

[86]  F. Grinnell,et al.  Transforming growth factor beta stimulates fibroblast-collagen matrix contraction by different mechanisms in mechanically loaded and unloaded matrices. , 2002, Experimental cell research.

[87]  J. Humphrey Continuum biomechanics of soft biological tissues , 2003 .

[88]  A. Spencer Continuum Mechanics , 1967, Nature.

[89]  V. Moulin,et al.  Epidermis promotes dermal fibrosis: role in the pathogenesis of hypertrophic scars , 2005, The Journal of pathology.

[90]  H M Byrne,et al.  A model of wound-healing angiogenesis in soft tissue. , 1996, Mathematical biosciences.

[91]  A. Desmoulière,et al.  Apoptosis mediates the decrease in cellularity during the transition between granulation tissue and scar. , 1995, The American journal of pathology.

[92]  F. Grinnell,et al.  Fibroblast adhesion on collagen substrata in the presence and absence of plasma fibronectin. , 1981, Journal of cell science.

[93]  Paul Martin,et al.  Wound Healing--Aiming for Perfect Skin Regeneration , 1997, Science.

[94]  F. Silver,et al.  Mechanobiology of force transduction in dermal tissue , 2003, Skin research and technology : official journal of International Society for Bioengineering and the Skin (ISBS) [and] International Society for Digital Imaging of Skin (ISDIS) [and] International Society for Skin Imaging.

[95]  H M Byrne,et al.  A mathematical model of the stress induced during avascular tumour growth , 2000, Journal of mathematical biology.

[96]  A. Klarbring,et al.  On compatible strain with reference to biomechanics of soft tissues , 2005 .

[97]  R. Darling Differential forms and connections , 1994 .

[98]  S. Jonathan Chapman,et al.  Mathematical Models of Avascular Tumor Growth , 2007, SIAM Rev..

[99]  Robert A. Brown,et al.  The origins and regulation of tissue tension: identification of collagen tension-fixation process in vitro. , 2006, Experimental cell research.

[100]  J. Murray,et al.  A MECHANICAL MODEL FOR FIBROBLAST-DRIVEN WOUND HEALING , 1995 .

[101]  R. Gorenflo,et al.  Analytical properties and applications of the Wright function , 2007, math-ph/0701069.

[102]  H M Byrne,et al.  On the rôle of angiogenesis in wound healing , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[103]  C. Cobbold The role of nitric oxide in the formation of keloid and hypertrophic lesions. , 2001, Medical hypotheses.

[104]  R. C. Lee,et al.  The problem scar. , 1998, Clinics in plastic surgery.

[105]  C. Please,et al.  Tumour dynamics and necrosis: surface tension and stability. , 2001, IMA journal of mathematics applied in medicine and biology.

[106]  J A Sherratt,et al.  Mathematical modelling of nitric oxide activity in wound healing can explain keloid and hypertrophic scarring. , 2000, Journal of theoretical biology.

[107]  Y C Fung,et al.  Change of Residual Strains in Arteries due to Hypertrophy Caused by Aortic Constriction , 1989, Circulation research.

[108]  Joel E. Cohen,et al.  Mathematics Is Biology's Next Microscope, Only Better; Biology Is Mathematics' Next Physics, Only Better , 2004, PLoS biology.

[109]  P. Klemera,et al.  Visco-elastic response of human skin and aging , 2002, Journal of the American Aging Association.

[110]  S Ramtani,et al.  Mechanical modelling of cell/ECM and cell/cell interactions during the contraction of a fibroblast-populated collagen microsphere: theory and model simulation. , 2004, Journal of biomechanics.

[111]  L. Gibson,et al.  Fibroblast contraction of a collagen-GAG matrix. , 2001, Biomaterials.

[112]  Alain Goriely,et al.  Growth and instability in elastic tissues , 2005 .

[113]  K. Harding,et al.  Clinical review Science , medicine , and the future Healing chronic wounds , 2005 .

[114]  P. Maini,et al.  A mathematical model for the capillary endothelial cell-extracellular matrix interactions in wound-healing angiogenesis. , 1997, IMA journal of mathematics applied in medicine and biology.

[115]  F. Silver,et al.  Viscoelastic properties of human skin and processed dermis , 2001, Skin research and technology : official journal of International Society for Bioengineering and the Skin (ISBS) [and] International Society for Digital Imaging of Skin (ISDIS) [and] International Society for Skin Imaging.

[116]  J. Murray,et al.  Mechanistic model of wound contraction. , 1993, The Journal of surgical research.

[117]  Alain Goriely,et al.  Elastic Growth Models , 2008 .

[118]  J A Sherratt,et al.  Mathematical modelling of anisotropy in fibrous connective tissue. , 1999, Mathematical biosciences.

[119]  Shubhada Sankararaman,et al.  Cells, tissues and disease: Principles of general pathology , 1997 .

[120]  Jing-zi Li,et al.  Connective tissue growth factor stimulates renal cortical myofibroblast‐like cell proliferation and matrix protein production , 2008, Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society.

[121]  R. Compans,et al.  EFFECT OF CYTOCHALASIN B ON THE , 1979 .

[122]  Lisa Macintyre,et al.  Pressure garments for use in the treatment of hypertrophic scars--a review of the problems associated with their use. , 2006, Burns : journal of the International Society for Burn Injuries.

[123]  D Ambrosi,et al.  The role of stress in the growth of a multicell spheroid , 2004, Journal of mathematical biology.

[124]  G. Chejfec Robbins Pathologic Basis of Disease , 2009 .

[125]  G. Oster,et al.  Mechanical aspects of mesenchymal morphogenesis. , 1983, Journal of embryology and experimental morphology.

[126]  B. Coulomb,et al.  Cutaneous Wound Healing: Myofibroblastic Differentiation and in Vitro Models , 2003, The international journal of lower extremity wounds.

[127]  D A Weitz,et al.  Measuring the mechanical stress induced by an expanding multicellular tumor system: a case study. , 2003 .

[128]  F.M.F. Simões,et al.  A framework for deformation, generalized diffusion, mass transfer and growth in multi-species multi-phase biological tissues , 2005 .

[129]  G. J. Pettet,et al.  The migration of cells in multicell tumor spheroids , 2001, Bulletin of mathematical biology.

[130]  L. E. Malvern Introduction to the mechanics of a continuous medium , 1969 .

[131]  A Bayat,et al.  Genetic susceptibility to keloid disease and transforming growth factor beta 2 polymorphisms. , 2002, British journal of plastic surgery.

[132]  E Bell,et al.  Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[133]  R. Tranquillo,et al.  Estimation of cell traction and migration in an isometric cell traction assay , 1999 .

[134]  Renato Perucchio,et al.  Modeling Heart Development , 2000 .

[135]  G. Sohie,et al.  Generalization of the matrix inversion lemma , 1986, Proceedings of the IEEE.

[136]  Ali Nekouzadeh,et al.  Incremental Mechanics of Collagen Gels: New Experiments and a New Viscoelastic Model , 2003, Annals of Biomedical Engineering.

[137]  R. Ogden,et al.  A New Constitutive Framework for Arterial Wall Mechanics and a Comparative Study of Material Models , 2000 .

[138]  Andreas Menzel,et al.  Modelling of anisotropic growth in biological tissues , 2005 .

[139]  Alain Goriely,et al.  Differential growth and instability in elastic shells. , 2005, Physical review letters.

[140]  K. Rajagopal,et al.  Review of the uses and modeling of bitumen from ancient to modern times , 2003 .

[141]  A. Hoger The constitutive equation for finite deformations of a transversely isotropic hyperelastic material with residual stress , 1993 .

[142]  F. Grinnell,et al.  Studies on the mechanism of hydrated collagen gel reorganization by human skin fibroblasts. , 1985, Journal of cell science.

[143]  F. Grinnell,et al.  Fibroblast-collagen-matrix contraction: growth-factor signalling and mechanical loading. , 2000, Trends in cell biology.

[144]  T. Krieg,et al.  Regulation of connective tissue homeostasis in the skin by mechanical forces. , 2004, Clinical and experimental rheumatology.

[145]  H. Greenspan Models for the Growth of a Solid Tumor by Diffusion , 1972 .

[146]  D. McElwain,et al.  A linear-elastic model of anisotropic tumour growth , 2004, European Journal of Applied Mathematics.

[147]  Y. Verma,et al.  Imaging growth dynamics of tumour spheroids using optical coherence tomography , 2007, Biotechnology Letters.

[148]  M. Abercrombie,et al.  Fibroblasts , 1978, Journal of clinical pathology. Supplement.

[149]  R. Tranquillo,et al.  A novel implantable collagen gel assay for fibroblast traction and proliferation during wound healing. , 2002, The Journal of surgical research.

[150]  Mark Eastwood,et al.  Quantitative analysis of collagen gel contractile forces generated by dermal fibroblasts and the relationship to cell morphology , 1996, Journal of cellular physiology.

[151]  A. Ghahary,et al.  Myofibroblasts and Apoptosis in Human Hypertrophic Scars: The Effect of Interferon- α2b: 14. , 2001 .

[152]  Stephen M. Klisch,et al.  A Theory of Volumetric Growth for Compressible Elastic Biological Materials , 2001 .

[153]  C. F. Curtiss,et al.  Dynamics of Polymeric Liquids, Volume 1: Fluid Mechanics , 1987 .

[154]  James D. Murray Dermal Wound Healing , 1993 .

[155]  E. Hofer,et al.  Simulation of Fracture Healing Using Cellular Automata : Influence of Operation Conditions on Healing Result in External Fixation , 2005 .

[156]  A. Menzel,et al.  Modelling of anisotropic growth in biological tissues. A new approach and computational aspects. , 2005, Biomechanics and modeling in mechanobiology.

[157]  H. Othmer,et al.  A HYBRID MODEL FOR TUMOR SPHEROID GROWTH IN VITRO I: THEORETICAL DEVELOPMENT AND EARLY RESULTS , 2007 .

[158]  Frederick Grinnell,et al.  Fibroblast biology in three-dimensional collagen matrices. , 2003, Trends in cell biology.

[159]  R. Hill The mathematical theory of plasticity , 1950 .

[160]  A. Roberts,et al.  Scarring Occurs at a Critical Depth of Skin Injury: Precise Measurement in a Graduated Dermal Scratch in Human Volunteers , 2007, Plastic and reconstructive surgery.

[161]  Thibault Lemaire,et al.  Mécanotransduction du remodelage osseux : rôle des fissures à la périphérie des ostéons , 2008 .

[162]  J A Sherratt,et al.  Spatially varying equilibria of mechanical models: application to dermal wound contraction. , 1998, Mathematical biosciences.

[163]  Geoffrey C Gurtner,et al.  Topical vascular endothelial growth factor accelerates diabetic wound healing through increased angiogenesis and by mobilizing and recruiting bone marrow-derived cells. , 2004, The American journal of pathology.

[164]  A. Hoger,et al.  Constitutive Functions of Elastic Materials in Finite Growth and Deformation , 2000 .

[165]  N. Rashevsky,et al.  Mathematical biology , 1961, Connecticut medicine.

[166]  Frederick Grinnell,et al.  Modulation of fibroblast morphology and adhesion during collagen matrix remodeling. , 2002, Molecular biology of the cell.

[167]  H. D. Cavanagh,et al.  An in vitro force measurement assay to study the early mechanical interaction between corneal fibroblasts and collagen matrix. , 1997, Experimental cell research.

[168]  R T Tranquillo,et al.  Continuum model of fibroblast-driven wound contraction: inflammation-mediation. , 1992, Journal of theoretical biology.

[169]  Lynda F. Bonewald,et al.  Proteolysis of Latent Transforming Growth Factor-β (TGF-β)-binding Protein-1 by Osteoclasts , 2002, The Journal of Biological Chemistry.

[170]  武 田村 “Elastoplasticity Theory”(弾塑性理論) , 2010 .

[171]  P Klemera,et al.  Viscoelasticity of biological materials - measurement and practical impact on biomedicine. , 2007, Physiological research.

[172]  E Otten,et al.  Analytical description of growth. , 1982, Journal of theoretical biology.

[173]  J D Humphrey,et al.  Stress-modulated growth, residual stress, and vascular heterogeneity. , 2001, Journal of biomechanical engineering.

[174]  M. Denn ISSUES IN VISCOELASTIC FLUID MECHANICS , 1990 .

[175]  James D. Murray,et al.  Spatial pattern formation in biology: I. Dermal wound healing. II. Bacterial patterns , 1998 .

[176]  Paolo A. Netti,et al.  Solid stress inhibits the growth of multicellular tumor spheroids , 1997, Nature Biotechnology.

[177]  Jason M. Haugh,et al.  Quantitative elucidation of a distinct spatial gradient-sensing mechanism in fibroblasts , 2005, The Journal of cell biology.

[178]  C. Petrie Dynamics of polymeric liquids. Volume 1. Fluid mechanics (2nd ed) : R.B. Bird, R.C. Armstrong and O. Hassager, Wiley-Interscience, New York, NY, 1987, 649 + xxi pages, ISBN 0-471-80245-X (V.1), price US$ 69.95 , 1988 .

[179]  B. Hinz,et al.  Mechanical tension controls granulation tissue contractile activity and myofibroblast differentiation. , 2001, The American journal of pathology.

[180]  Y. Cao,et al.  TGF-beta: a fibrotic factor in wound scarring and a potential target for anti-scarring gene therapy. , 2004, Current gene therapy.

[181]  J. M. García-Aznar,et al.  On numerical modelling of growth, differentiation and damage in structural living tissues , 2006 .

[182]  Yannis F. Dafalias,et al.  Plastic spin: necessity or redundancy? , 1998 .

[183]  G F Oster,et al.  A mechanical model for mesenchymal morphogenesis , 1983, Journal of mathematical biology.

[184]  S. Ramtani,et al.  Remodeled-matrix contraction by fibroblasts: numerical investigations , 2002, Comput. Biol. Medicine.

[185]  Alain Goriely,et al.  On the definition and modeling of incremental, cumulative, and continuous growth laws in morphoelasticity , 2007, Biomechanics and modeling in mechanobiology.

[186]  Jennifer S. Park,et al.  Mechanobiology of mesenchymal stem cells and their use in cardiovascular repair. , 2007, Frontiers in bioscience : a journal and virtual library.

[187]  Richard Skalak,et al.  Growth as A Finite Displacement Field , 1981 .

[188]  F. Grinnell,et al.  Reorganization of hydrated collagen lattices by human skin fibroblasts. , 1984, Journal of cell science.

[189]  Sabine Werner,et al.  Keratinocyte-fibroblast interactions in wound healing. , 2007, The Journal of investigative dermatology.

[190]  Frederick Grinnell,et al.  Dendritic fibroblasts in three-dimensional collagen matrices. , 2003, Molecular biology of the cell.

[191]  S. O'Kane,et al.  Scar-free healing: from embryonic mechanisms to adult therapeutic intervention. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.