Growth instabilities and folding in tubular organs: A variational method in non-linear elasticity☆

Abstract Morphoelastic theories have demonstrated that elastic instabilities can occur during the growth of soft materials, initiating the transition toward complex patterns. Within the framework of non-linear elasticity, the theory of incremental elastic deformations is classically employed for solving stability problems with finite strains. In this work, we define a variational method to study the bifurcation of growing cylinders with circular section. Accounting for a constant axial pre-stretch, we define a set of canonical transformations in mixed polar coordinates, providing a locally isochoric mapping. Introducing a generating function to derive an implicit gradient form of the mixed variables, the incompressibility constraint for the elastic deformation is solved exactly. The canonical representation allows to transform a generic boundary value problem, characterized by conservative body forces and surface traction loads, into a completely variational formulation. The proposed variational method gives a straightforward derivation of the linear stability analysis, which would otherwise require lengthy manipulations on the governing incremental equations. The definition of a generating function can also account for the presence of local singularities in the elastic solution. Bifurcation analysis is performed for few constrained growth problems of biomechanical interests, such as the mucosal folding of tubular tissues and surface instabilities in tumor growth. In a concluding section, the theoretical results are discussed for clarifying how anisotropy, residual strains and external constraints can affect the stability properties of soft tissues in growth and remodeling processes.

[1]  Thomas Lecuit,et al.  Orchestrating size and shape during morphogenesis , 2007, Nature.

[2]  Pasquale Ciarletta,et al.  Swelling instability of surface-attached gels as a model of soft tissue growth under geometric constraints , 2010 .

[3]  R. Ogden Non-Linear Elastic Deformations , 1984 .

[4]  Alain Goriely,et al.  Circumferential buckling instability of a growing cylindrical tube , 2011 .

[5]  José Carlos Goulart de Siqueira,et al.  Differential Equations , 1919, Nature.

[6]  B. Shraiman,et al.  Mechanical feedback as a possible regulator of tissue growth. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[7]  R. Ogden,et al.  On Surface Waves and Deformations in a Pre-stressed Incompressible Elastic Solid , 1990 .

[8]  Pasquale Ciarletta,et al.  Morphogenesis of thin hyperelastic plates: A constitutive theory of biological growth in the Föppl-von Kármán limit , 2009 .

[9]  I. Müller,et al.  3 Non-linear Elasticity , 2004 .

[10]  Gerhard A. Holzapfel,et al.  Modelling the layer-specific three-dimensional residual stresses in arteries, with an application to the human aorta , 2010, Journal of The Royal Society Interface.

[11]  M. Biot Surface instability of rubber in compression , 1963 .

[12]  P Ciarletta,et al.  The radial growth phase of malignant melanoma: multi-phase modelling, numerical simulations and linear stability analysis , 2011, Journal of The Royal Society Interface.

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

[14]  Silvestro Micera,et al.  Hyperelastic Model of Anisotropic Fiber Reinforcements within Intestinal Walls for Applications in Medical Robotics , 2009, Int. J. Robotics Res..

[15]  J. W. Humberston Classical mechanics , 1980, Nature.

[16]  Luigi Preziosi,et al.  The insight of mixtures theory for growth and remodeling , 2010 .

[17]  M. Labouesse,et al.  Tissue morphogenesis: how multiple cells cooperate to generate a tissue. , 2010, Current opinion in cell biology.

[18]  Ray W. Ogden,et al.  On the incremental equations in non-linear elasticity — II. Bifurcation of pressurized spherical shells , 1978 .

[19]  J. Dervaux,et al.  Buckling condensation in constrained growth , 2011 .

[20]  M. Destrade,et al.  Asymptotic results for bifurcations in pure bending of rubber blocks , 2008, 0811.4022.

[21]  Arezki Boudaoud,et al.  Multiple-length-scale elastic instability mimics parametric resonance of nonlinear oscillators , 2010, 1006.2404.

[22]  R D Kamm,et al.  On the mechanism of mucosal folding in normal and asthmatic airways. , 1997, Journal of applied physiology.

[23]  R. Hayward,et al.  Dynamic display of biomolecular patterns through an elastic creasing instability of stimuli-responsive hydrogels. , 2010, Nature materials.

[24]  R. Ogden Nonlinear Elasticity: Elements of the Theory of Finite Elasticity , 2001 .

[25]  J. P. Paul,et al.  Biomechanics , 1966 .

[26]  P Ciarletta,et al.  Continuum model of epithelial morphogenesis during Caenorhabditis elegans embryonic elongation , 2009, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[27]  H. Frieboes,et al.  Nonlinear modelling of cancer: bridging the gap between cells and tumours , 2010, Nonlinearity.

[28]  Ray W. Ogden,et al.  Bifurcation of inflated circular cylinders of elastic material under axial loading—II. Exact theory for thick-walled tubes , 1979 .

[29]  P. Podio-Guidugli A variational approach to live loadings in finite elasticity , 1988 .

[30]  R. Ogden,et al.  On deforming a sector of a circular cylindrical tube into an intact tube: Existence, uniqueness, and stability , 2010, 1301.5117.

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

[32]  On the eversion of compressible elastic cylinders , 1997 .

[33]  M. J. Sewell,et al.  Maximum and minimum principles , 1989, The Mathematical Gazette.

[34]  R. Ogden,et al.  On the incremental equations in non-linear elasticity — I. Membrane theory , 1978 .

[35]  R. Knops On Bateman's exercise , 2005 .

[36]  P. Howarth,et al.  Airway wall remodelling in asthma. , 1997, Thorax.

[37]  Constantin Carathéodory,et al.  Calculus of variations and partial differential equations of the first order , 1965 .

[38]  Alan N. Gent,et al.  Elastic instabilities in rubber , 2005 .

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

[40]  L. Preziosi,et al.  Multiphase models of tumour growth , 2008 .

[41]  Flexure and compression of incompressible elastic plates , 1999 .

[42]  Y C Fung,et al.  Strain distribution in the layered wall of the esophagus. , 1999, Journal of biomechanical engineering.

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

[44]  M. J. Sewell,et al.  Anatomy of the canonical transformation , 1993, Philosophical Transactions of the Royal Society of London. Series A: Physical and Engineering Sciences.

[45]  M. M. Carroll,et al.  Generating functions for plane or axisymmetric isochoric deformations , 1984 .

[46]  P Ciarletta,et al.  Contour instabilities in early tumor growth models. , 2011, Physical review letters.

[47]  Alan N. Gent,et al.  Surface Instabilities in Compressed or Bent Rubber Blocks , 1999 .

[48]  M. M. Carroll A representation theorem for volume-preserving transformations , 2004 .

[49]  Xi-Qiao Feng,et al.  Growth and surface folding of esophageal mucosa: a biomechanical model. , 2011, Journal of biomechanics.

[50]  Larry A Taber,et al.  Towards a unified theory for morphomechanics , 2009, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.