A computational model for collagen fibre remodelling in the arterial wall.

As the interaction between tissue adaptation and the mechanical condition within tissues is complex, mathematical models are desired to study this interrelation. In this study, a mathematical model is presented to investigate the interplay between collagen architecture and mechanical loading conditions in the arterial wall. It is assumed that the collagen fibres align along preferred directions, situated in between the principal stretch directions. The predicted fibre directions represent symmetrically arranged helices and agree qualitatively with morphometric data from literature. At the luminal side of the arterial wall, the fibres are oriented more circumferentially than at the outer side. The discrete transition of the fibre orientation at the media-adventitia interface can be explained by accounting for the different reference configurations of both layers. The predicted pressure-radius relations resemble experimentally measured sigma-shaped curves. As there is a strong coupling between the collagen architecture and the mechanical loading condition within the tissue, we expect that the presented model for collagen remodelling is useful to gain further insight into the processes involved in vascular adaptation, such as growth and smooth muscle tone adaptation.

[1]  Jonathon Howard,et al.  Slow local movements of collagen fibers by fibroblasts drive the rapid global self-organization of collagen gels , 2002, The Journal of cell biology.

[2]  N. Stergiopulos,et al.  Geometrical, functional, and histomorphometric adaptation of rat carotid artery in induced hypertension. , 2003, Journal of biomechanics.

[3]  J D Humphrey,et al.  Remodeling of a collagenous tissue at fixed lengths. , 1999, Journal of biomechanical engineering.

[4]  T Matsumoto,et al.  Mechanical and dimensional adaptation of rat aorta to hypertension. , 1994, Journal of biomechanical engineering.

[5]  C. William Hall,et al.  Biomedical Engineering II Recent Developments , 1983 .

[6]  David N. Ku,et al.  Arterial Wall Adaptation under Elevated Longitudinal Stretch in Organ Culture , 2003, Annals of Biomedical Engineering.

[7]  B L Langille,et al.  Arterial remodeling: relation to hemodynamics. , 1996, Canadian journal of physiology and pharmacology.

[8]  A Rachev,et al.  Theoretical study of the effect of stress-dependent remodeling on arterial geometry under hypertensive conditions. , 1997, Journal of biomechanics.

[9]  Partap S. Khalsa,et al.  Human Lumbar Spine Creep during Cyclic and Static Flexion: Creep Rate, Biomechanics, and Facet Joint Capsule Strain , 2005, Annals of Biomedical Engineering.

[10]  Jacques M. Huyghe,et al.  Finite Element Model of Mechanically Induced Collagen Fiber Synthesis and Degradation in the Aortic Valve , 2003, Annals of Biomedical Engineering.

[11]  Victor H. Barocas,et al.  A finite element solution for the anisotropic biphasic theory of tissue- equivalent mechanics , 1997 .

[12]  Johannes A. G. Rhodin,et al.  Architecture of the Vessel Wall , 1980 .

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

[14]  L. Taber A model for aortic growth based on fluid shear and fiber stresses. , 1998, Journal of biomechanical engineering.

[15]  A Rachev,et al.  Theoretical study of dynamics of arterial wall remodeling in response to changes in blood pressure. , 1996, Journal of biomechanics.

[16]  F. Iuorno Effect of mechanical forces on growth and matrix protein synthesis in the in vitro pulmonary artery , 1996 .

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

[18]  Robert A. Brown,et al.  Mechanical loading regulates protease production by fibroblasts in three‐dimensional collagen substrates , 2000, Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society.

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

[20]  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.

[21]  F. Plum Handbook of Physiology. , 1960 .

[22]  R. Nerem,et al.  Tissue engineering a blood vessel: Regulation of vascular biology by mechanical stresses , 1994, Journal of cellular biochemistry.

[23]  T. Borg,et al.  Collagen expression in mechanically stimulated cardiac fibroblasts. , 1991, Circulation research.

[24]  A. Sadegh,et al.  An evolutionary Wolff's law for trabecular architecture. , 1992, Journal of biomechanical engineering.

[25]  Avrum I. Gotlieb,et al.  Wall Tissue Remodeling Regulates Longitudinal Tension in Arteries , 2002, Circulation research.

[26]  P. Canham,et al.  Contrasting structure of the saphenous vein and internal mammary artery used as coronary bypass vessels. , 1997, Cardiovascular research.

[27]  Christopher J. O’Callaghan,et al.  Mechanical Strain–Induced Extracellular Matrix Production by Human Vascular Smooth Muscle Cells: Role of TGF-&bgr;1 , 2000, Hypertension.

[28]  P. Maini,et al.  Biological implications of a discrete mathematical model for collagen deposition and alignment in dermal wound repair. , 2000, IMA journal of mathematics applied in medicine and biology.

[29]  M. Rekhter,et al.  Effect of mechanical forces on growth and matrix protein synthesis in the in vitro pulmonary artery. Analysis of the role of individual cell types. , 1995, Circulation research.

[30]  L A Taber,et al.  Biomechanics of cardiovascular development. , 2001, Annual review of biomedical engineering.

[31]  N. Nakatsuji,et al.  Experimental manipulation of a contact guidance system in amphibian gastrulation by mechanical tension , 1984, Nature.

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

[33]  Rik Huiskes,et al.  Effects of mechanical forces on maintenance and adaptation of form in trabecular bone , 2000, Nature.

[34]  N. Stergiopulos,et al.  Short-Term Biomechanical Adaptation of the Rat Carotid to Acute Hypertension: Contribution of Smooth Muscle , 2004, Annals of Biomedical Engineering.

[35]  Jan P. Stegemann,et al.  Phenotype Modulation in Vascular Tissue Engineering Using Biochemical and Mechanical Stimulation , 2003, Annals of Biomedical Engineering.

[36]  Jacques M Huyghe,et al.  Computational analyses of mechanically induced collagen fiber remodeling in the aortic heart valve. , 2003, Journal of biomechanical engineering.

[37]  L A Taber,et al.  Theoretical study of stress-modulated growth in the aorta. , 1996, Journal of theoretical biology.

[38]  N. Simionescu,et al.  The Cardiovascular System , 1983 .

[39]  R Langer,et al.  Functional arteries grown in vitro. , 1999, Science.

[40]  Frederick J Schoen,et al.  Cardiovascular tissue engineering. , 2002, Cardiovascular pathology : the official journal of the Society for Cardiovascular Pathology.

[41]  J M Huyghe,et al.  Remodelling of continuously distributed collagen fibres in soft connective tissues. , 2003, Journal of biomechanics.

[42]  M. Sato,et al.  Change in intramural strain distribution in rat aorta due to smooth muscle contraction and relaxation. , 1996, The American journal of physiology.

[43]  R T Tranquillo,et al.  A finite element solution for the anisotropic biphasic theory of tissue-equivalent mechanics: the effect of contact guidance on isometric cell traction measurement. , 1997, Journal of biomechanical engineering.

[44]  Arthur C. Guyton,et al.  Handbook of Physiology—The Cardiovascular System , 1985 .

[45]  P. Canham,et al.  Three-dimensional collagen organization of human brain arteries at different transmural pressures. , 1995, Journal of vascular research.

[46]  R. N. Vaishnav,et al.  ESTIMATION OF RESIDUAL STRAINS IN AORTIC SEGMENTS , 1983 .

[47]  R M Nerem,et al.  Vascular tissue engineering. , 2001, Annual review of biomedical engineering.

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

[49]  F. Silver,et al.  Collagen fiber formation in repair tissue: development of strength and toughness. , 1985, Collagen and related research.

[50]  A. A. Krikanov,et al.  Composite pressure vessels with higher stiffness , 2000 .

[51]  J A Sherratt,et al.  A mathematical model for fibroblast and collagen orientation , 1998, Bulletin of mathematical biology.

[52]  S Jockenhoevel,et al.  CARDIOVASCULAR TISSUE ENGINEERING: A NEW LAMINAR FLOW CHAMBER FOR IN VITRO IMPROVEMENT OF MECHANICAL TISSUE PROPERTIES , 2000, ASAIO journal.

[53]  D. Mackenna,et al.  Role of mechanical factors in modulating cardiac fibroblast function and extracellular matrix synthesis. , 2000, Cardiovascular research.

[54]  Kozaburo Hayashi,et al.  Theoretical Study of the Effects of Vascular Smooth Muscle Contraction on Strain and Stress Distributions in Arteries , 1999, Annals of Biomedical Engineering.

[55]  Z. Galis,et al.  Mechanical stretching of human saphenous vein grafts induces expression and activation of matrix-degrading enzymes associated with vascular tissue injury and repair. , 1999, Experimental and molecular pathology.

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

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

[58]  R Langer,et al.  Morphologic and mechanical characteristics of engineered bovine arteries. , 2001, Journal of vascular surgery.

[59]  J. Bishop,et al.  Regulation of cardiovascular collagen synthesis by mechanical load. , 1999, Cardiovascular research.

[60]  R. Nerem Tissue engineering a blood vessel , 1996, Proceedings of 18th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

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

[62]  J. Meister,et al.  Model of geometrical and smooth muscle tone adaptation of carotid artery subject to step change in pressure. , 2001, American journal of physiology. Heart and circulatory physiology.

[63]  R. Nerem,et al.  Changes in organization and composition of the extracellular matrix underlying cultured endothelial cells exposed to laminar steady shear stress. , 1995, Laboratory investigation; a journal of technical methods and pathology.

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

[65]  N. Stergiopulos,et al.  Biomechanical adaptation of porcine carotid vascular smooth muscle to hypo and hypertension in vitro. , 2002, Journal of biomechanics.

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

[67]  A Rachev,et al.  A model for geometric and mechanical adaptation of arteries to sustained hypertension. , 1998, Journal of biomechanical engineering.