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Research Papers

Failure of the Porcine Ascending Aorta: Multidirectional Experiments and a Unifying Microstructural Model

[+] Author and Article Information
Colleen M. Witzenburg, Rohit Y. Dhume

Department of Mechanical Engineering,
University of Minnesota,
Minneapolis, MN 55455

Sachin B. Shah, Christopher E. Korenczuk, Hallie P. Wagner, Patrick W. Alford

Department of Biomedical Engineering,
University of Minnesota,
Minneapolis, MN 55455

Victor H. Barocas

Department of Biomedical Engineering,
University of Minnesota,
7-105 Nils Hasselmo Hall,
312 Church Street SE,
Minneapolis, MN 55455
e-mail: baroc001@umn.edu

1Corresponding author.

Manuscript received May 8, 2016; final manuscript received October 30, 2016; published online January 23, 2017. Assoc. Editor: Hai-Chao Han.

J Biomech Eng 139(3), 031005 (Jan 23, 2017) (14 pages) Paper No: BIO-16-1186; doi: 10.1115/1.4035264 History: Received May 08, 2016; Revised October 30, 2016

The ascending thoracic aorta is poorly understood mechanically, especially its risk of dissection. To make better predictions of dissection risk, more information about the multidimensional failure behavior of the tissue is needed, and this information must be incorporated into an appropriate theoretical/computational model. Toward the creation of such a model, uniaxial, equibiaxial, peel, and shear lap tests were performed on healthy porcine ascending aorta samples. Uniaxial and equibiaxial tests showed anisotropy with greater stiffness and strength in the circumferential direction. Shear lap tests showed catastrophic failure at shear stresses (150–200 kPa) much lower than uniaxial tests (750–2500 kPa), consistent with the low peel tension (∼60 mN/mm). A novel multiscale computational model, including both prefailure and failure mechanics of the aorta, was developed. The microstructural part of the model included contributions from a collagen-reinforced elastin sheet and interlamellar connections representing fibrillin and smooth muscle. Components were represented as nonlinear fibers that failed at a critical stretch. Multiscale simulations of the different experiments were performed, and the model, appropriately specified, agreed well with all experimental data, representing a uniquely complete structure-based description of aorta mechanics. In addition, our experiments and model demonstrate the very low strength of the aorta in radial shear, suggesting an important possible mechanism for aortic dissection.

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Figures

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Fig. 1

The ascending thoracic aorta. (a) Illustration of the heart with the ascending aorta highlighted [3], (b) Geometry and coordinate system describing the ascending aorta, and (c) The three-dimensional stress tensor for the aorta, marked to show how different testing modes were used to target specific stress components.

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Fig. 2

Specimen dissection. (a) Porcine aortic arch with ascending aortic ring removed. The white star represents a marker used to keep track of tissue sample orientation. (b) The ring was cut open along its superior edge and laid flat with the intimal surface up and the axial, Z, and circumferential, θ, directions along the vertical and horizontal directions, respectively. Axial and circumferential directions are shown with black arrows. (c) Schematic showing a typical sectioning and testing plan for an ascending aortic specimen.

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Fig. 3

Schematics of all mechanical tests. (a) Uniaxial test: samples were cut and mounted such that the direction of pull corresponded with either the axial or circumferential orientation of the vessel. (b) Equibiaxial test: samples were cut and mounted such that the directions of pull corresponded with the axial and circumferential orientations of the vessel. (c) Peel test: samples were cut and mounted such that the vertical direction corresponded with either the axial or circumferential orientation of the vessel. (d) Lap test: samples were cut and mounted such that the direction of pull corresponded with either the axial or circumferential orientation of the vessel; dotted black line indicates overlap length.

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Fig. 4

Multiscale model based on aortic media structure. (a) Hematoxylin and eosin stain shows smooth muscle cell nuclei (dark purple) and elastic lamina (pink). (b) Masson's trichrome stain shows collagen (blue) within the lamina and smooth muscle (red). (c) Verhoeff–Van Gieson shows elastin (black/purple). (d) A microstructural model based on the histology contains a layer of elastin (red) reinforced by collagen fibers (black). The collagen fibers are aligned preferentially in the circumferential direction, and the elastin sheet is isotropic. Lamellae are connected by interlamellar connections (green) representing the combined contribution of fibrillin and smooth muscle. The interlamellar connections are aligned primarily in the radial direction but also have some preference for circumferential alignment to match smooth muscle alignment in vivo. (e) An RVE with eight gauss points. (f) FE geometry showing a uniaxial shaped sample (equibiaxial, lap, and peel geometries were also used).

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Fig. 5

Uniaxial extension to failure. (a) First Piola-Kirchhoff (PK1) stress versus grip stretch for circumferentially (n = 11) and axially (n = 11) orientated samples (dots, mean ±95% CI). Error bars are only shown for stretch levels up to the point at which the first sample failed. The final dot shows the average stretch and stress at tissue failure, and the dashed rectangle indicates the 95% confidence intervals of stretch and stress at failure. The red lines show the model results for PK1 stress as a function of grip stretch. (b) PK1 stress distributions along the axis of applied deformation for both the circumferentially (Sθθ) and axially (Szz) aligned simulations, accompanied by an enlarged view of a network with the upper interlamellar connections removed to make the collagen and elastin visible. (c) Fraction of failed fibers of each type in the simulated experiment. Because the collagen fibers are preferentially aligned in the circumferential direction, more of the failed fibers were collagen for the circumferentially aligned simulation, whereas for the axially aligned simulation more of the failed fibers were interlamellar connections (I.C. = interlamellar connections).

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Fig. 6

Equibiaxial extension. (a) Mean PK1 stress as a function of grip stretch (dots) for equibiaxial extension. The 95% CI was 30–35% of the measured value but was omitted from the figure to improve visual clarity. The red lines show the model results for PK1 stress versus grip stretch. (b) Circumferential (Sθθ) and axial (Szz) PK1 stress distributions predicted by the model. (c) Enlarged view of a micronetwork with the upper interlamellar connections removed to make the collagen and elastin visible.

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Fig. 7

Peel to failure. (a) Peel tension versus grip stretch for both circumferentially and axially oriented samples (dots, mean ± 95% CI). The red lines indicate the model results. (b) PK1 stress (Srr) distributions along the axis of applied deformation for both the circumferentially and axially aligned simulations, accompanied by an enlarged view of a network with the upper interlamellar connections removed to make the collagen and elastin visible.

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Fig. 8

Kinematics of the shear lap test. (a) Displacement of a representative shear lap sample, adjusted to zero displacement at the center. (b) Strain of the representative sample in the xy-direction. (c) Dotted line showing overlap surface edge and vectors with normal and tangential directions. (d) Average strain on the overlap surface edge for both axially (n = 15) and circumferentially (n = 19) oriented samples. Error bars indicate 95% confidence intervals. +p < 0.10, ++p < 0.05, and +++p < 0.01.

Grahic Jump Location
Fig. 9

Shear lap failure. (a) PK1 stress versus grip stretch for circumferentially (n = 28) and axially (n = 26) orientated samples (dots, mean ±95% CI). Error bars are only shown for stretch levels up to the point at which the first sample failed. The final dot shows the average stretch and stress at tissue failure and the dashed rectangle indicates the 95% confidence intervals of stretch and stress at failure. The red lines show the model results. (b) Shear stress distributions along the axis of applied deformation for both the circumferentially (Srθ) and axially (Srz) aligned simulations, accompanied by an enlarged view of a network with the upper interlamellar connections removed to make the collagen and elastin visible. (c) Fraction of failed fibers of each type in the simulated experiment (I.C. = interlamellar connections).

Grahic Jump Location
Fig. 10

Summary of experimental and model results. (a) Experimental and model failure PK1 stress (Sθθ and Szz) in uniaxial tension tests for samples oriented circumferentially and axially. (b) Experimental and model failure tension in peel tests for samples oriented circumferentially and axially. (c) Experimental and model failure shear stress (Srθ and Srz) in shear lap tests for samples oriented circumferentially and axially. All the experimental data show mean ±95% CI. (d) The model showed failure at a stretch ratio of 3.1 with a tangent modulus of 58 kPa in the region prior to failure, comparing well to MacLean's reported tangent modulus of 61 kPa.

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