Digital image correlation-based point-wise inverse characterization of heterogeneous material properties of gallbladder in vitro

Continuing advances in mechanobiology reveal more and more that many cell types, especially those responsible for establishing, maintaining, remodelling or repairing extracellular matrix, are extremely sensitive to their local mechanical environment. Indeed, it appears that they fashion the extracellular matrix so as to promote a ‘mechanical homeostasis’. A natural corollary, therefore, is that cells will try to offset complexities in geometry and applied loads with heterogeneous material properties in order to render their local environment mechanobiologically favourable. There is a pressing need, therefore, for hybrid experimental–computational methods in biomechanics that can quantify such heterogeneities. In this paper, we present an approach that combines experimental information on full-field surface geometry and deformations with a membrane-based point-wise inverse method to infer full-field mechanical properties for soft tissues that exhibit nonlinear behaviours under finite deformations. To illustrate the potential utility of this new approach, we present the first quantification of regional mechanical properties of an excised but intact gallbladder, a thin-walled, sac-like organ that plays a fundamental role in normal digestion. The gallbladder was inflated to a maximum local stretch of 120% in eight pressure increments; at each pressure pause, the entire three-dimensional surface was optically extracted, and from which the surface strains were computed. Wall stresses in each state were predicted from the deformed geometry and the applied pressure using an inverse elastostatic method. The elastic properties of the gallbladder tissue were then characterized locally using point-wise stress–strain data. The gallbladder was found to be highly heterogeneous, with drastically different stiffness between the hepatic and the serosal sides. The identified material model was validated through forward finite-element analysis; both the configurations and the local stress–strain patterns were well reproduced.

[1]  S. Govindjee,et al.  Computational methods for inverse finite elastostatics , 1996 .

[2]  Jia Lu,et al.  Characterizing heterogeneous properties of cerebral aneurysms with unknown stress-free geometry: a precursor to in vivo identification. , 2011, Journal of biomechanical engineering.

[3]  M. L. Raghavan,et al.  Inverse method of stress analysis for cerebral aneurysms , 2008, Biomechanics and modeling in mechanobiology.

[4]  J D Humphrey,et al.  Novel optical system for in vitro quantification of full surface strain fields in small arteries: I. Theory and design , 2011, Computer methods in biomechanics and biomedical engineering.

[5]  Hubert W. Schreier,et al.  Image Correlation for Shape, Motion and Deformation Measurements: Basic Concepts,Theory and Applications , 2009 .

[6]  Shouhua Hu,et al.  A Shell-Based Inverse Approach of Stress Analysis in Intracranial Aneurysms , 2013, Annals of Biomedical Engineering.

[7]  R. Ogden,et al.  Anisotropic behaviour of human gallbladder walls. , 2013, Journal of the mechanical behavior of biomedical materials.

[8]  R. Ogden,et al.  A quasi-nonlinear analysis of the anisotropic behaviour of human gallbladder wall. , 2012, Journal of biomechanical engineering.

[9]  Jia Lu,et al.  Pointwise Identification of Elastic Properties in Nonlinear Hyperelastic Membranes―Part I: Theoretical and Computational Developments , 2009 .

[10]  Jia Lu,et al.  Patient-Specific Wall Stress Analysis in Cerebral Aneurysms Using Inverse Shell Model , 2010, Annals of Biomedical Engineering.

[11]  Michael A. Sutton,et al.  Error Assessment in Stereo-based Deformation Measurements , 2011 .

[12]  M. Beatty A class of universal relations for constrained, isotropic elastic materials , 1989 .

[13]  J D Humphrey,et al.  An improved panoramic digital image correlation method for vascular strain analysis and material characterization. , 2013, Journal of the mechanical behavior of biomedical materials.

[14]  M. L. Raghavan,et al.  Inverse elastostatic stress analysis in pre-deformed biological structures: Demonstration using abdominal aortic aneurysms. , 2007, Journal of biomechanics.

[15]  Jay D. Humphrey,et al.  Multiaxial Mechanical Behavior of Human Saccular Aneurysms , 2001 .

[16]  Karol Miller,et al.  On the prospect of patient-specific biomechanics without patient-specific properties of tissues. , 2013, Journal of the mechanical behavior of biomedical materials.

[17]  Katia Genovese,et al.  Regional Finite Strains in an Angiotensin-II Induced Mouse Model of Dissecting Abdominal Aortic Aneurysms , 2012 .

[18]  Jia Lu,et al.  Identifying heterogeneous anisotropic properties in cerebral aneurysms: a pointwise approach , 2011, Biomechanics and modeling in mechanobiology.

[19]  J. Humphrey Vascular Adaptation and Mechanical Homeostasis at Tissue, Cellular, and Sub-cellular Levels , 2007, Cell Biochemistry and Biophysics.

[20]  M. L. Raghavan,et al.  Computational method of inverse elastostatics for anisotropic hyperelastic solids , 2007 .

[21]  Sophia Mã ¶ ller,et al.  Biomechanics — Mechanical properties of living tissue , 1982 .

[22]  S. Govindjee,et al.  Computational methods for inverse de-formations in quasi-incompressible nite elasticity , 1998 .

[23]  J. D. Humphrey,et al.  Finite Element Based Predictions of Preferred Material Symmetries in Saccular Aneurysms , 1999, Annals of Biomedical Engineering.

[24]  M. Grédiac,et al.  Assessment of Digital Image Correlation Measurement Errors: Methodology and Results , 2009 .

[25]  Jia Lu,et al.  Inverse formulation for geometrically exact stress resultant shells , 2008 .

[26]  Jia Lu,et al.  Pointwise Identification of Elastic Properties in Nonlinear Hyperelastic Membranes—Part II: Experimental Validation , 2009 .

[27]  Padmanabhan Seshaiyer,et al.  A sub-domain inverse finite element characterization of hyperelastic membranes including soft tissues. , 2003, Journal of biomechanical engineering.

[28]  J D Humphrey,et al.  Novel optical system for in vitro quantification of full surface strain fields in small arteries: II. Correction for refraction and illustrative results , 2011, Computer methods in biomechanics and biomedical engineering.

[29]  Frederick H. Silver,et al.  Mechanosensing and Mechanochemical Transduction in Extracellular Matrix , 2006 .