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Special Section: Spotlight on the Future–Imaging and Biomechanical Engineering

Strain Mapping From Four-Dimensional Ultrasound Reveals Complex Remodeling in Dissecting Murine Abdominal Aortic Aneurysms

[+] Author and Article Information
Hannah L. Cebull

Weldon School of Biomedical Engineering,
Purdue University,
206 S. Martin Jischke Drive,
West Lafayette, IN 47907
e-mail: hcebull@purdue.edu

Arvin H. Soepriatna

Weldon School of Biomedical Engineering,
Purdue University,
206 S. Martin Jischke Drive,
West Lafayette, IN 47907
e-mail: asoepria@purdue.edu

John J. Boyle

Department of Biomedical Engineering,
Washington University,
1 Brookings Drive,
St Louis, MO 63130;
Department of Orthopaedic Surgery,
Columbia University,
116th Street and Broadway,
New York, NY 10027
e-mail: john.boyle.87@gmail.com

Sean M. Rothenberger

Weldon School of Biomedical Engineering,
Purdue University,
206 S. Martin Jischke Drive,
West Lafayette, IN 47907
e-mail: srothenb@purdue.edu

Craig J. Goergen

Mem. ASME
Weldon School of Biomedical Engineering,
Purdue University,
206 S. Martin Jischke Drive,
West Lafayette, IN 47907
e-mail: cgoergen@purdue.edu

1Corresponding author.

Manuscript received May 20, 2018; final manuscript received March 2, 2019; published online April 22, 2019. Assoc. Editor: Paul Barbone.

J Biomech Eng 141(6), 060907 (Apr 22, 2019) (8 pages) Paper No: BIO-18-1241; doi: 10.1115/1.4043075 History: Received May 20, 2018; Revised March 02, 2019

Current in vivo abdominal aortic aneurysm (AAA) imaging approaches tend to focus on maximum diameter but do not measure three-dimensional (3D) vascular deformation or strain. Complex vessel geometries, heterogeneous wall compositions, and surrounding structures can all influence aortic strain. Improved understanding of complex aortic kinematics has the potential to increase our ability to predict aneurysm expansion and eventual rupture. Here, we describe a method that combines four-dimensional (4D) ultrasound and direct deformation estimation to compute in vivo 3D Green-Lagrange strain in murine angiotensin II-induced suprarenal dissecting aortic aneurysms, a commonly used small animal model. We compared heterogeneous patterns of the maximum, first-component 3D Green-Lagrange strain with vessel composition from mice with varying AAA morphologies. Intramural thrombus and focal breakage in the medial elastin significantly reduced aortic strain. Interestingly, a dissection that was not detected with high-frequency ultrasound also experienced reduced strain, suggesting medial elastin breakage that was later confirmed via histology. These results suggest that in vivo measurements of 3D strain can provide improved insight into aneurysm disease progression. While further work is needed with both preclinical animal models and human imaging studies, this initial murine study indicates that vessel strain should be considered when developing an improved metric for predicting aneurysm growth and rupture.

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Figures

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Fig. 1

A schematic representing the strain estimation process beginning with (a) 4D ultrasound acquisition, (b) and (c) direct deformation estimation to resampled image data, (d) and (e) segmentation of the vessel wall, and (f) surface mapping of strain values at peak systole. The aorta and superior mesenteric artery are outlined in the dashed line.

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Fig. 2

Representative 3D images of maximum, first-component Green-Lagrange strain (acquired baseline, day 1 post-aneurysm formation, and end of study) showed strain heterogeneity along the aortic wall. End of the study is defined as 14 days post formation for mice in the AAA group and 28 days post-pump implantation for mice in the non-AAA group. Compared to the non-AAA group which exhibited high wall strain values (M6–M8), mice that developed AAAs experienced significantly lower wall strain (M1–M5; larger than 50% growth).

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Fig. 3

Schematic representing the quantified regions in a representative vessel for AAA and non-AAA groups (a). Boxplot and corresponding histogram representation of the distribution of maximum principal Green-Lagrange strain values for each animal at baseline, day 1 post-aneurysm formation, and end of study (b) and (c). Varying minimum, maximum, and median values allow for quantitative visualization of the heterogeneity between animals and timepoints (p <0.001 between baseline, day 1, and end of study; * significant decrease, #significant increase).

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Fig. 4

Representative comparison between (a) an aneurysm with significant intramural thrombus (*) and (b) an aneurysm with a large, open false lumen. White arrows indicate the site of focal elastin breakage in the most distal sections (black). In general, higher strain is present in mice with open false lumens versus those with substantial intramural thrombus (scale bar = 0.5 mm).

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Fig. 5

Cross-sectional hematoxylin and eosin (H&E) and Movat pentachrome histological staining of the mouse aorta. Histology reveals qualitative differences in medial elastin, adventitial collagen, and newly deposited fibrin between animals. The bottom row displays corresponding maximum, first-component Green-Lagrange principal strain values at histologically matched positions (scale bar = 0.5 mm).

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