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Research Papers

Contribution of Collagen Fiber Undulation to Regional Biomechanical Properties Along Porcine Thoracic Aorta

[+] Author and Article Information
Shahrokh Zeinali-Davarani, Yunjie Wang, Ming-Jay Chow

Department of Mechanical Engineering,
Boston University,
Boston, MA 02215

Raphaël Turcotte

Department of Biomedical Engineering,
Boston University,
Boston, MA 02215
Advanced Microscopy Program,
Center for Systems Biology
and Wellman Center for Photomedicine,
Massachusetts General Hospital,
Harvard Medical School,
Boston, MA 02114

Yanhang Zhang

Department of Mechanical Engineering,
Boston University,
Boston, MA 02215
Department of Biomedical Engineering,
Boston University,
Boston, MA 02215
e-mail: yanhang@bu.edu

1Corresponding author.

Manuscript received August 13, 2014; final manuscript received December 24, 2014; published online February 20, 2015. Assoc. Editor: Hai-Chao Han.

J Biomech Eng 137(5), 051001 (May 01, 2015) (10 pages) Paper No: BIO-14-1394; doi: 10.1115/1.4029637 History: Received August 13, 2014; Revised December 24, 2014; Online February 20, 2015

As major extracellular matrix components, elastin, and collagen play crucial roles in regulating the mechanical properties of the aortic wall and, thus, the normal cardiovascular function. The mechanical properties of aorta, known to vary with age and multitude of diseases as well as the proximity to the heart, have been attributed to the variations in the content and architecture of wall constituents. This study is focused on the role of layer-specific collagen undulation in the variation of mechanical properties along the porcine descending thoracic aorta. Planar biaxial tensile tests are performed to characterize the hyperelastic anisotropic mechanical behavior of tissues dissected from four locations along the thoracic aorta. Multiphoton microscopy is used to image the associated regional microstructure. Exponential-based and recruitment-based constitutive models are used to account for the observed mechanical behavior while considering the aortic wall as a composite of two layers with independent properties. An elevated stiffness is observed in distal regions compared to proximal regions of thoracic aorta, consistent with sharper and earlier collagen recruitment estimated for medial and adventitial layers in the models. Multiphoton images further support our prediction that higher stiffness in distal regions is associated with less undulation in collagen fibers. Recruitment-based models further reveal that regardless of the location, collagen in the media is recruited from the onset of stretching, whereas adventitial collagen starts to engage with a delay. A parameter sensitivity analysis is performed to discriminate between the models in terms of the confidence in the estimated model parameters.

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Figures

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Fig. 1

Representative stress–stretch responses for proximal ((a) and (b)) and distal ((c) and (d)) regions of thoracic aorta in the longitudinal and circumferential directions using biaxial loading protocols: fl:fc = 1:2, 2:3, 1:1, 3:2, 2:1 (fl:fc is the ratio of tensions applied in the longitudinal and circumferential directions). The curves estimated using model B are shown as solid lines while the model response predicted for the equibiaxial tension protocol (fl:fc = 1:1) are shown as dashed lines.

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Fig. 2

Average longitudinal (a) and circumferential (b) tangent modulus at multiple locations (proximal, midproximal, mid-distal, and distal) along the descending thoracic aorta

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Fig. 3

Recruitment distribution densities estimated for medial and adventitial collagen fibers in the proximal ((a) and (c)) and distal ((b) and (d)) thoracic aorta using models B (top panels) and C (bottom panels)

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Fig. 4

Three-dimensional contour plots of strain energy stored in media and adventitia given the estimated parameters of model B for proximal ((a) and (b)) and distal ((c) and (d)) regions of Artery 2

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Fig. 5

Sensitivity coefficients of longitudinal and circumferential stress with respect to the constitutive parameters associated with collagen for model A ((a) and (b)), model B ((c) and (d)), and model C ((e) and (f))

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Fig. 6

Representative SHG images of collagen in media and adventitia and 2PEF images of elastin in media of proximal (left column) and distal (right column) regions of thoracic aortas. Adventitial collagen fibers are highly undulated in the proximal region compared to the distal region while there is no obvious difference in medial elastin and collagen waviness between proximal and distal region (images 360 × 360 μm).

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Fig. 7

Mean and standard deviation of adventitial collagen fibers straightness measured at proximal and distal regions (p < 0.05)

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