Mechanical and failure mechanisms of descending thoracic aorta: implications for health and disease
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Citation
Abstract
Structural organization of the extracellular matrix components of the aorta is critical to its loading-bearing capacity and homeostasis. Aortic elastic fibers form concentric lamellar layers with a closely interwoven three-dimensional network of collagen and elastic fibers in the narrow interlamellar space. Aging and cardiovascular diseases are closely associated with disrupted microstructural organization, integrity, as well as altered mechanical and failure properties of the aortic wall. The overall goal of this research is to advance the current understanding of the mechanical and failure mechanisms of human descending thoracic aorta and provide insights for aortic remodeling during aging and disease progression using integrated biomechanical testing, imaging, and computational modeling approaches.
Biaxial tensile tests revealed anisotropic stiffening of the aortic wall with aging with a more drastic stiffening behavior in the longitudinal direction. A newly developed constitutive model considering collagen crosslinking suggested that collagen crosslinking has an increasing contribution to the stress-stretch behavior and elastic energy storage in aortic senescence. The aorta relies on interlamellar structural components, mainly elastic and collagen fibers, for maintaining its structural and mechanical integrity. Our study using peeling and direct tension tests demonstrated that elastic and collagen fibers both play an important role in bonding of the arterial wall, while collagen fibers dominate the interlamellar stiffness, strength and toughness. Our study further reveals that the interlamellar strength and toughness both increase due to nonenzymatic glycation, which is in accordance with the reported inverse relation between diabetes and a reduced risk of aortic dissection. On the other hand, however, our study showed decreasing interlamellar bonding toughness of the medial layer of human descending thoracic aorta with aging. Avalanches and power-law behavior in dissection propagation was found for all age groups investigated. Finite element simulations incorporating discrete interlamellar collagen fibers successfully recapitulates the power-law behavior and points to prominent structural alterations in interlamellar collagen fibers with aging including reduced fiber density and higher degree of dispersion.
In aging and diseases, changes to the extracellular matrix microstructure can trigger a cascade of effects on tissue and cellular function. The knowledge gained from this research provide insights into the microstructural mechanisms in determining the physiological and failure properties of aorta and will potentially generate clinical impact on the developments of new diagnostics and interventions.