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Local variations in material and structural properties characterize murine thoracic aortic aneurysm mechanics

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Abstract

We recently developed an approach to characterize local nonlinear, anisotropic mechanical properties of murine arteries by combining biaxial extension–distension testing, panoramic digital image correlation, and an inverse method based on the principle of virtual power. This experimental–computational approach was illustrated for the normal murine abdominal aorta assuming uniform wall thickness. Here, however, we extend our prior approach by adding an optical coherence tomography (OCT) imaging system that permits local reconstructions of wall thickness. This multimodality approach is then used to characterize spatial variations of material and structural properties in ascending thoracic aortic aneurysms (aTAA) from two genetically modified mouse models (fibrillin-1 and fibulin-4 deficient) and to compare them with those from angiotensin II-infused apolipoprotein E-deficient and wild-type control ascending aortas. Local values of stored elastic energy and biaxial material stiffness, computed from spatial distributions of the best fit material parameters, varied significantly with circumferential position (inner vs. outer curvature, ventral vs. dorsal sides) across genotypes and treatments. Importantly, these data reveal an inverse relationship between material stiffness and wall thickness that underlies a general linear relationship between stiffness and wall stress across aTAAs. OCT images also revealed sites of advanced medial degeneration, which were captured by the inverse material characterization. Quantification of histological data further provided high-resolution local correlations among multiple mechanical metrics and wall microstructure. This is the first time that such structural defects and local properties have been characterized mechanically, which can better inform computational models of aortopathy that seek to predict where dissection or rupture may initiate.

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Acknowledgments

This work was supported by NIH grants R01 HL105297, R21 HL107768, and U01 HL116323 (to JDH), P01 HL134605 (to D. Rifkin), and ERC Grant ERC-2014-CoG BIOLOCHANICS (to SA).

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Correspondence to Stéphane Avril.

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Bersi, M.R., Bellini, C., Humphrey, J.D. et al. Local variations in material and structural properties characterize murine thoracic aortic aneurysm mechanics. Biomech Model Mechanobiol 18, 203–218 (2019). https://doi.org/10.1007/s10237-018-1077-9

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  • DOI: https://doi.org/10.1007/s10237-018-1077-9

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