Turnover of fibrillar collagen in soft biological tissue with application to the expansion of abdominal aortic aneurysms

A better understanding of the inherent properties of vascular tissue to adapt to its mechanical environment is crucial to improve the predictability of biomechanical simulations. Fibrillar collagen in the vascular wall plays a central role in tissue adaptation owing to its relatively short lifetime. Pathological alterations of collagen turnover may fail to result in homeostasis and could be responsible for abdominal aortic aneurysm (AAA) growth at later stages of the disease. For this reason our previously reported multiscale constitutive framework (Martufi, G. & Gasser, T. C. 2011 J. Biomech. 44, 2544–2550 (doi:10.1016/j.jbiomech.2011.07.015)) has been enriched by a collagen turnover model. Specifically, the framework's collagen fibril level allowed a sound integration of vascular wall biology, and the impact of collagen turnover on the macroscopic properties of AAAs was studied. To this end, model parameters were taken from the literature and/or estimated from clinical follow-up data of AAAs (on average 50.7 mm-large). Likewise, the in vivo stretch of the AAA wall was set, such that 10 per cent of collagen fibres were engaged. Results showed that the stretch spectrum, at which collagen fibrils are deposed, is the most influential parameter, i.e. it determines whether the vascular geometry grows, shrinks or remains stable over time. Most importantly, collagen turnover also had a remarkable impact on the macroscopic stress field. It avoided high stress gradients across the vessel wall, thus predicted a physiologically reasonable stress field. Although the constitutive model could be successfully calibrated to match the growth of small AAAs, a rigorous validation against experimental data is crucial to further explore the model's descriptive and predictive capabilities.

[1]  Martin Kroon,et al.  A theoretical model for fibroblast-controlled growth of saccular cerebral aneurysms. , 2009, Journal of theoretical biology.

[2]  J. Humphrey,et al.  Importance of initial aortic properties on the evolving regional anisotropy, stiffness and wall thickness of human abdominal aortic aneurysms , 2012, Journal of The Royal Society Interface.

[3]  N. Sasaki,et al.  Elongation mechanism of collagen fibrils and force-strain relations of tendon at each level of structural hierarchy. , 1996, Journal of biomechanics.

[4]  J Swedenborg,et al.  Biomechanical rupture risk assessment of abdominal aortic aneurysms: model complexity versus predictability of finite element simulations. , 2010, European journal of vascular and endovascular surgery : the official journal of the European Society for Vascular Surgery.

[5]  Jonathan P Vande Geest,et al.  Biomechanical properties of ruptured versus electively repaired abdominal aortic aneurysm wall tissue. , 2006, Journal of vascular surgery.

[6]  Gerard Pasterkamp,et al.  Increased collagen turnover is only partly associated with collagen fiber deposition in the arterial response to injury. , 2004, Cardiovascular research.

[7]  S A Wickline,et al.  Decreased vascular smooth muscle cell density in medial degeneration of human abdominal aortic aneurysms. , 1997, The American journal of pathology.

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

[9]  M M Thompson,et al.  A review of biological factors implicated in abdominal aortic aneurysm rupture. , 2005, European journal of vascular and endovascular surgery : the official journal of the European Society for Vascular Surgery.

[10]  H. L. Cox The elasticity and strength of paper and other fibrous materials , 1952 .

[11]  K. J. Grande-Allen,et al.  Effects of static and cyclic loading in regulating extracellular matrix synthesis by cardiovascular cells. , 2006, Cardiovascular research.

[12]  J. S. Yao,et al.  Collagen types and matrix protein content in human abdominal aortic aneurysms. , 1989, Journal of vascular surgery.

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

[14]  W H Baker,et al.  Elastolytic and collagenolytic studies of arteries. Implications for the mechanical properties of aneurysms. , 1984, Archives of surgery.

[15]  B. Strauss,et al.  In vivo collagen turnover following experimental balloon angioplasty injury and the role of matrix metalloproteinases. , 1996, Circulation research.

[16]  Per Eriksson,et al.  Influence of intraluminal thrombus on structural and cellular composition of abdominal aortic aneurysm wall. , 2003, Journal of vascular surgery.

[17]  Y Ventikos,et al.  Modelling evolution and the evolving mechanical environment of saccular cerebral aneurysms , 2011, Biomechanics and modeling in mechanobiology.

[18]  T Christian Gasser,et al.  A constitutive model for vascular tissue that integrates fibril, fiber and continuum levels with application to the isotropic and passive properties of the infrarenal aorta. , 2011, Journal of biomechanics.

[19]  P N Watton,et al.  Evolving mechanical properties of a model of abdominal aortic aneurysm , 2009, Biomechanics and modeling in mechanobiology.

[20]  K Y Volokh,et al.  A model of growth and rupture of abdominal aortic aneurysm. , 2008, Journal of biomechanics.

[21]  T. Christian Gasser,et al.  An Integrated Fluid-Chemical Model Toward Modeling the Formation of Intra-Luminal Thrombus in Abdominal Aortic Aneurysms , 2012, Front. Physio..

[22]  L. Soslowsky,et al.  Influence of decorin and biglycan on mechanical properties of multiple tendons in knockout mice. , 2005, Journal of biomechanical engineering.

[23]  J. Scott,et al.  Tendon response to tensile stress: an ultrastructural investigation of collagen:proteoglycan interactions in stressed tendon. , 1995, Journal of anatomy.

[24]  F Radice,et al.  Alteration of elastin, collagen and their cross-links in abdominal aortic aneurysms. , 2002, European journal of vascular and endovascular surgery : the official journal of the European Society for Vascular Surgery.

[25]  K. Angquist,et al.  Proteolysis of the abdominal aortic aneurysm wall and the association with rupture. , 2002, European journal of vascular and endovascular surgery : the official journal of the European Society for Vascular Surgery.

[26]  D. Carey,et al.  Control of growth and differentiation of vascular cells by extracellular matrix proteins. , 1991, Annual review of physiology.

[27]  Jun Liao,et al.  A structural basis for the size-related mechanical properties of mitral valve chordae tendineae. , 2003, Journal of biomechanics.

[28]  R I Bashey,et al.  Changes in collagen biosynthesis, types, and mechanics of aorta in hypertensive rats. , 1989, The Journal of laboratory and clinical medicine.

[29]  A. Redaelli,et al.  Estimation of the binding force of the collagen molecule-decorin core protein complex in collagen fibril. , 2005, Journal of biomechanics.

[30]  A. Kelly Interface effects and the work of fracture of a fibrous composite , 1970, Proceedings of the Royal Society of London. A. Mathematical and Physical Sciences.

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

[32]  J. Snedeker,et al.  Equivalent stiffness after glycosaminoglycan depletion in tendon--an ultra-structural finite element model and corresponding experiments. , 2011, Journal of theoretical biology.

[33]  R. Armentano,et al.  Assessment of elastin and collagen contribution to aortic elasticity in conscious dogs. , 1991, The American journal of physiology.

[34]  C. Miehe,et al.  Aspects of the formulation and finite element implementation of large strain isotropic elasticity , 1994 .

[35]  D. Vorp,et al.  The effects of aneurysm on the biaxial mechanical behavior of human abdominal aorta. , 2006, Journal of biomechanics.

[36]  G. Upchurch,et al.  Abdominal aortic aneurysm. , 2006, American family physician.

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

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

[39]  J. C. Simo,et al.  Quasi-incompressible finite elasticity in principal stretches. Continuum basis and numerical algorithms , 1991 .

[40]  Jay D. Humphrey,et al.  Structure, Mechanical Properties, and Mechanics of Intracranial Saccular Aneurysms , 2000 .

[41]  J D Humphrey,et al.  A theoretical model of enlarging intracranial fusiform aneurysms. , 2006, Journal of biomechanical engineering.

[42]  S Mantero,et al.  Possible role of decorin glycosaminoglycans in fibril to fibril force transfer in relative mature tendons--a computational study from molecular to microstructural level. , 2003, Journal of biomechanics.

[43]  T Christian Gasser,et al.  Nonlinear elasticity of biological tissues with statistical fibre orientation , 2010, Journal of The Royal Society Interface.

[44]  Jay D. Humphrey,et al.  A CONSTRAINED MIXTURE MODEL FOR GROWTH AND REMODELING OF SOFT TISSUES , 2002 .

[45]  M. Barnes,et al.  Collagens in atherosclerosis. , 1985, Collagen and related research.

[46]  P. Hoskins,et al.  The relationship between abdominal aortic aneurysm distensibility and serum markers of elastin and collagen metabolism. , 2001, European journal of vascular and endovascular surgery : the official journal of the European Society for Vascular Surgery.

[47]  J. Humphrey Cardiovascular solid mechanics , 2002 .

[48]  Simon G. Thompson,et al.  Abdominal Aortic Aneurysm Expansion: Risk Factors and Time Intervals for Surveillance , 2004, Circulation.

[49]  Seungik Baek,et al.  Medical image-based simulation of abdominal aortic aneurysm growth , 2012 .

[50]  T Christian Gasser,et al.  Spatial orientation of collagen fibers in the abdominal aortic aneurysm's wall and its relation to wall mechanics. , 2012, Acta biomaterialia.

[51]  R. Müller,et al.  Local strain measurement reveals a varied regional dependence of tensile tendon mechanics on glycosaminoglycan content. , 2009, Journal of biomechanics.

[52]  S Udenfriend,et al.  Increased turnover of arterial collagen in hypertensive rats. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[53]  J E Scott,et al.  Elasticity in extracellular matrix ‘shape modules’ of tendon, cartilage, etc. A sliding proteoglycan‐filament model , 2003, The Journal of physiology.

[54]  M J Davies,et al.  Aortic aneurysm formation: lessons from human studies and experimental models. , 1998, Circulation.

[55]  Ian Warren,et al.  Modelling for Evolution , 1999 .

[56]  R. Bank,et al.  Distinct defects in collagen microarchitecture underlie vessel-wall failure in advanced abdominal aneurysms and aneurysms in Marfan syndrome , 2009, Proceedings of the National Academy of Sciences.

[57]  Martin Kroon,et al.  A model for saccular cerebral aneurysm growth by collagen fibre remodelling. , 2007, Journal of theoretical biology.

[58]  S. Baek,et al.  Circumferential variations of mechanical behavior of the porcine thoracic aorta during the inflation test. , 2011, Journal of biomechanics.

[59]  S. Baek,et al.  An Inverse Optimization Approach Toward Testing Different Hypotheses of Vascular Homeostasis Using Image-based Models , 2011 .

[60]  N. J. A. Sloane,et al.  McLaren’s improved snub cube and other new spherical designs in three dimensions , 1996, Discret. Comput. Geom..

[61]  Martin Auer,et al.  Reconstruction and Finite Element Mesh Generation of Abdominal Aortic Aneurysms From Computerized Tomography Angiography Data With Minimal User Interactions , 2010, IEEE Transactions on Medical Imaging.

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

[63]  J. Scott Proteoglycan:collagen interactions and subfibrillar structure in collagen fibrils. Implications in the development and ageing of connective tissues. , 1990, Journal of anatomy.

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

[65]  T. Christian Gasser,et al.  An irreversible constitutive model for fibrous soft biological tissue: a 3-D microfiber approach with demonstrative application to abdominal aortic aneurysms. , 2011 .

[66]  J. Liao,et al.  Skewness angle of interfibrillar proteoglycans increases with applied load on mitral valve chordae tendineae. , 2007, Journal of biomechanics.

[67]  Yasuteru Muragaki,et al.  Stretch-Induced Collagen Synthesis in Cultured Smooth Muscle Cells from Rabbit Aortic Media and a Possible Involvement of Angiotensin II and Transforming Growth Factor-β , 1998, Journal of Vascular Research.

[68]  R. Müller,et al.  Collagen fibril morphology and mechanical properties of the Achilles tendon in two inbred mouse strains , 2010, Journal of anatomy.

[69]  T. Christian Gasser,et al.  Histo-Mechanical Modeling of the Wall of Abdominal Aorta Aneurysms , 2012 .

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

[71]  T Christian Gasser,et al.  Failure properties of intraluminal thrombus in abdominal aortic aneurysm under static and pulsating mechanical loads. , 2008, Journal of vascular surgery.

[72]  Charles A. DiMarzio,et al.  Mechanical Strain Stabilizes Reconstituted Collagen Fibrils against Enzymatic Degradation by Mammalian Collagenase Matrix Metalloproteinase 8 (MMP-8) , 2010, PloS one.

[73]  T. Christian Gasser,et al.  Blood flow and coherent vortices in the normal and aneurysmatic aortas: a fluid dynamical approach to intra-luminal thrombus formation , 2011, Journal of The Royal Society Interface.

[74]  Timothy James Wess,et al.  Collagen Fibrillar Structure and Hierarchies , 2008 .

[75]  Peter R Hoskins,et al.  The relationship between aortic wall distensibility and rupture of infrarenal abdominal aortic aneurysm. , 2003, Journal of vascular surgery.

[76]  M L Raghavan,et al.  Toward a biomechanical tool to evaluate rupture potential of abdominal aortic aneurysm: identification of a finite strain constitutive model and evaluation of its applicability. , 2000, Journal of biomechanics.