Constitutive modeling of ascending thoracic aortic aneurysms using microstructural parameters

Abstract

Ascending thoracic aortic aneurysm (ATAA) has been associated with diminished biomechanical strength and disruption in the collagen fiber microarchitecture. Additionally, the congenital bicuspid aortic valve (BAV) leads to a distinct extracellular matrix structure that may be related to ATAA development at an earlier age than degenerative aneurysms arising in patients with the morphological normal tricuspid aortic valve (TAV). The purpose of this study was to model the fiber-reinforced mechanical response of ATAA specimens from patients with either BAV or TAV. This was achieved by combining image-analysis derived parameters of collagen fiber dispersion and alignment with tensile testing data. Then, numerical simulations were performed to assess the role of anisotropic constitutive formulation on the wall stress distribution of aneurysmal aorta. Results indicate that both BAV ATAA and TAV ATAA have altered collagen fiber architecture in the medial plane of experimentally-dissected aortic tissues when compared to normal ascending aortic specimens. The study findings highlight that differences in the collagen fiber distribution mostly influences the resulting wall stress distribution rather than the peak stress. We conclude that fiber-reinforced constitutive modeling that takes into account the collagen fiber defect inherent to the aneurysmal ascending aorta is paramount for accurate finite element predictions and ultimately for biomechanical-based indicators to reliably distinguish the more from the less 'malignant' ATAAs.

Keywords: Aortic aneurysm; Aortic failure; Bicuspid aortic valve; Extracellular matrix; Finite element.

Fig 1

(A) Example of multi-photon microscopy images (stack of 120 μm) of elastin (green) and collagen (red) fibers in the medial dissected plane of non-aneurysmal aorta, BAV ATAA and TAV ATAA in both ADV-DEL and INT-DEL layers; (B) processed image with small arrows in blue that follow the direction of collagen fibers and (C) histogram of fiber angle

Fig 2

(A) Fiber angle for ADV-DEL (black squares) and INT-DEL (white squares) halves obtained by multi-photon imaging analysis, * significantly different from ADV-DEL non-aneurysmal aorta (P<.05); (B) orientation index for ADV-DEL (black squares) and INT-DEL (white squares) layers, ** significantly different from INT-DEL non-aneurysmal aorta (P<.05)

Fig 3

Uniaxial stress-stretch responses for ADV-DEL and INT-DEL layers in CIRC (solid line) and LONG (dot line) orientations of non-aneurysmal aorta (top row), BAV ATAA (middle row) and TAV ATAA (bottom row); labels indicate specimens obtained from same tissue

Fig 4

Representative fitting curve and corresponding stress-stretch data for ADV-DEL and INT-DEL layers of BAV ATAA (top row) and TAV ATAA (bottom row)

Fig 5

Comparison of maximum principal stress in both ADV-DEL (right models) and INT-DEL (left models) for both BAV ATAA and TAV ATAA simulations utilizing the anisotropic, fiber-reinforced structural model with structural parameters quantified by multi-photon imaging analysis; the black arrows indicate local maxima of wall stress

Fig 6

Comparison of maximum principal stress in the ADV-DEL of both BAV ATAA and TAV ATAA simulations utilizing isotropic material properties (left models) and anisotropic material properties (right models); the black arrows indicate local maxima of wall stress

Fig 7

Distribution of maximum principal stress in TAV ATAA obtained with all five Gasser-Ogden-Holzapfel parameters derived from the macroscopic mechanical response of ADV-DEL halves; note that there is no appreciable difference in the wall stress distribution obtained with multi-photon derived parameters (see Fig 5).