Constitutive modeling of coronary arterial media--comparison of three model classes.

Accurate modeling of arterial elasticity is imperative for predicting pulsatile blood flow and transport to the periphery, and for evaluating the mechanical microenvironment of the vessel wall. The goal of the present study is to compare a recently developed structural model of porcine left anterior descending artery media to two commonly used typical representatives of phenomenological and structure-motivated invariant-based models, in terms of the number of model parameters, model descriptive and predictive powers, and requisite different test protocols for reliable parameter estimation. The three models were compared against 3D data of radial inflation, axial extension, and twist tests. Also checked are the models predictive capabilities to response data not used for estimation, including both tests outside the range of estimation database, as well as protocols of a different nature. The results show that the descriptive estimation error (model fit to estimation database), measured by the sum of squared residuals (SSE) between full 3D data and model predictions, was about twice as low for the structural (4.58%) model compared to the other two (9.71 and 8.99% for the phenomenological and structure-motivated models, respectively). Similar SSE ratios were obtained for the predictive capabilities. Prediction SSE at high stretch based on estimation of two low stretches yielded an SSE value of 2.81% for the structural model, and 10.54% and 7.87% for the phenomenological and structure-motivated models, respectively. For the prediction of twist from inflation-extension data, SSE values for the torsional stiffness was 1.76% for the structural model and 39.62 and 2.77% for the phenomenological and structure-motivated models. The required number of model parameters for the structural model is four, whereas the phenomenological model requires six to nine and the structure-motivated has four parameters. These results suggest that modeling based on the tissue structural features improves model reliability in describing given data and in predicting the tissue general response.

[1]  G S Kassab,et al.  Shear modulus of porcine coronary artery: contributions of media and adventitia. , 2003, American journal of physiology. Heart and circulatory physiology.

[2]  Gerhard A Holzapfel,et al.  Comparison of a multi-layer structural model for arterial walls with a fung-type model, and issues of material stability. , 2004, Journal of biomechanical engineering.

[3]  Y. Fung,et al.  Strain distribution in small blood vessels with zero-stress state taken into consideration. , 1992, The American journal of physiology.

[4]  K. Wasano,et al.  Tridimensional architecture of elastic tissue in the rat aorta and femoral artery--a scanning electron microscope study. , 1983, Journal of electron microscopy.

[5]  Gerard A Ateshian,et al.  Heterogeneous transmural proteoglycan distribution provides a mechanism for regulating residual stresses in the aorta. , 2008, American journal of physiology. Heart and circulatory physiology.

[6]  Y C Fung,et al.  Compressibility and constitutive equation of arterial wall in radial compression experiments. , 1984, Journal of biomechanics.

[7]  Y. Lanir,et al.  Effect of osmolarity on the zero-stress state and mechanical properties of aorta. , 2007, American journal of physiology. Heart and circulatory physiology.

[8]  M. Epstein,et al.  Cardiovascular Solid Mechanics: Cells, Tissues, and Organs , 2002 .

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

[10]  Hilmi Demiray,et al.  A layered cylindrical shell model for an aorta , 1991 .

[11]  Y. Lanir,et al.  Three-dimensional mechanical properties of porcine coronary arteries: a validated two-layer model. , 2006, American journal of physiology. Heart and circulatory physiology.

[12]  Michael S Sacks,et al.  Incorporation of experimentally-derived fiber orientation into a structural constitutive model for planar collagenous tissues. , 2003, Journal of biomechanical engineering.

[13]  Y Lanir,et al.  Plausibility of structural constitutive equations for swelling tissues--implications of the C-N and S-E conditions. , 1996, Journal of biomechanical engineering.

[14]  Nikos Stergiopulos,et al.  A constitutive formulation of arterial mechanics including vascular smooth muscle tone. , 2004, American journal of physiology. Heart and circulatory physiology.

[15]  Y. Fung,et al.  Pseudoelasticity of arteries and the choice of its mathematical expression. , 1979, The American journal of physiology.

[16]  Y C Fung,et al.  Residual strain in rat left ventricle. , 1990, Circulation research.

[17]  Yoram Lanir,et al.  Micro and macro rheology of planar tissues. , 2009, Biomaterials.

[18]  Gerhard Sommer,et al.  Determination of layer-specific mechanical properties of human coronary arteries with nonatherosclerotic intimal thickening and related constitutive modeling. , 2005, American journal of physiology. Heart and circulatory physiology.

[19]  M.S. Sacks,et al.  A Structural Constitutive Model for the Native Pulmonary Valve , 2004, The 26th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[20]  Ghassan S Kassab,et al.  Biaxial incremental homeostatic elastic moduli of coronary artery: two-layer model. , 2004, American journal of physiology. Heart and circulatory physiology.

[21]  Y Lanir Structure-function relations in mammalian tendon: the effect of geometrical nonuniformity. , 1978, Journal of bioengineering.

[22]  Ghassan S Kassab,et al.  Biaxial elastic material properties of porcine coronary media and adventitia. , 2005, American journal of physiology. Heart and circulatory physiology.

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

[24]  R. Vito,et al.  Blood vessel constitutive models-1995-2002. , 2003, Annual review of biomedical engineering.

[25]  S Glagov,et al.  Nature of Species Differences in the Medial Distribution of Aortic Vasa Vasorum in Mammals , 1967, Circulation research.

[26]  Y. Lanir Mechanisms of residual stress in soft tissues. , 2009, Journal of biomechanical engineering.

[27]  Michael S Sacks,et al.  A structural model for the flexural mechanics of nonwoven tissue engineering scaffolds. , 2006, Journal of biomechanical engineering.

[28]  Y C Fung,et al.  New experiments on shear modulus of elasticity of arteries. , 1994, The American journal of physiology.

[29]  W. von Maltzahn,et al.  Experimental measurements of elastic properties of media and adventitia of bovine carotid arteries. , 1984, Journal of biomechanics.

[30]  A. C. Burton,et al.  The reason for the shape of the distensibility curves of arteries. , 1957, Canadian journal of biochemistry and physiology.

[31]  Laura E. Niklason,et al.  An Ultrastructural Analysis of Collagen in Tissue Engineered Arteries , 2007, Annals of Biomedical Engineering.

[32]  W. Wiemer,et al.  Elastic properties of arteries: a nonlinear two-layer cylindrical model. , 1981, Journal of biomechanics.

[33]  B. Helwig,et al.  Central Tempol alters basal sympathetic nerve discharge and attenuates sympathetic excitation to central ANG II. , 2004, American journal of physiology. Heart and circulatory physiology.

[34]  Y Lanir,et al.  Time-dependent mechanical behavior of sheep digital tendons, including the effects of preconditioning. , 2002, Journal of biomechanical engineering.

[35]  A Rachev,et al.  Experimental investigation of the distribution of residual strains in the artery wall. , 1997, Journal of biomechanical engineering.

[36]  R N Vaishnav,et al.  Compressibility of the Arterial Wall , 1968, Circulation research.

[37]  R. Ogden,et al.  Hyperelastic modelling of arterial layers with distributed collagen fibre orientations , 2006, Journal of The Royal Society Interface.

[38]  M. Sacks,et al.  A method to quantify the fiber kinematics of planar tissues under biaxial stretch. , 1997, Journal of biomechanics.

[39]  S. Glagov,et al.  Transmural Organization of the Arterial Media: The Lamellar Unit Revisited , 1985, Arteriosclerosis.

[40]  S Glagov,et al.  Structural integration of the arterial wall. I. Relationships and attachments of medial smooth muscle cells in normally distended and hyperdistended aortas. , 1979, Laboratory investigation; a journal of technical methods and pathology.

[41]  Y. Lanir Constitutive equations for fibrous connective tissues. , 1983, Journal of biomechanics.

[42]  Charles A. Taylor,et al.  The three-dimensional micro- and nanostructure of the aortic medial lamellar unit measured using 3D confocal and electron microscopy imaging. , 2008, Matrix Biology.

[43]  Y. Lanir,et al.  Experimentally validated microstructural 3D constitutive model of coronary arterial media. , 2011, Journal of biomechanical engineering.

[44]  Ghassan S Kassab,et al.  The mathematical formulation of a generalized Hooke's law for blood vessels. , 2007, Biomaterials.

[45]  Yoram Lanir,et al.  Viscoelasticity and preconditioning of rat skin under uniaxial stretch: microstructural constitutive characterization. , 2009, Journal of biomechanical engineering.

[46]  Y Lanir,et al.  A structural theory for the homogeneous biaxial stress-strain relationships in flat collagenous tissues. , 1979, Journal of biomechanics.

[47]  Y C Fung,et al.  On residual stresses in arteries. , 1986, Journal of biomechanical engineering.

[48]  Y. C. Fung,et al.  What are the residual stresses doing in our blood vessels? , 2006, Annals of Biomedical Engineering.

[49]  Takehiko Azuma,et al.  A RHEOLOGICAL APPROACH TO THE ARCHTECTURE OF ARTERIAL WALLS , 1971 .

[50]  Y. Fung,et al.  Biomechanics: Mechanical Properties of Living Tissues , 1981 .

[51]  G. Holzapfel,et al.  A structural model for the viscoelastic behavior of arterial walls: Continuum formulation and finite element analysis , 2002 .

[52]  E. Nevo,et al.  Structural finite deformation model of the left ventricle during diastole and systole. , 1989, Journal of biomechanical engineering.

[53]  J D Humphrey,et al.  Mechanics of the arterial wall: review and directions. , 1995, Critical reviews in biomedical engineering.

[54]  S Oka,et al.  Mechanical equilibrium of blood vessel walls. , 1971, The American journal of physiology.

[55]  Y C Fung,et al.  Three-dimensional stress distribution in arteries. , 1983, Journal of biomechanical engineering.

[56]  S Oka,et al.  Physical theory of tension in thick-walled blood vessels in equilibrium. , 1970, Biorheology.

[57]  K. Takamizawa,et al.  Strain energy density function and uniform strain hypothesis for arterial mechanics. , 1987, Journal of biomechanics.

[58]  P. Dobrin,et al.  Finite deformation analysis of the relaxed and contracted dog carotid artery. , 1971, Microvascular research.

[59]  G A Holzapfel,et al.  Determination of constitutive equations for human arteries from clinical data. , 2003, Journal of biomechanics.

[60]  I. Sheinman,et al.  Structural three-dimensional constitutive law for the passive myocardium. , 1988, Journal of biomechanical engineering.