Adaptive Remodeling in the Elastase-Induced Rabbit Aneurysms
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SP ISS: EXPERIMENTAL ADVANCES IN CARDIOVASCULAR BIOMECHANICS
Adaptive Remodeling in the Elastase-Induced Rabbit Aneurysms C. Sang 1 & D.F. Kallmes 2 & R. Kadirvel 2 & M.J. Durka 1 & Y.-H. Ding 2 & D. Dai 2 & S.C. Watkins 3 & A.M. Robertson 1 Received: 5 February 2020 / Accepted: 29 September 2020 # Society for Experimental Mechanics 2020
Abstract Background Rupture of brain aneurysms is associated with high fatality and morbidity rates. Through remodeling of the collagen matrix, many aneurysms can remain unruptured for decades, despite an enlarging and evolving geometry. Objective Our objective was to explore this adaptive remodeling for the first time in an elastase induced aneurysm model in rabbits. Methods Saccular aneurysms were created in 22 New Zealand white rabbits and remodeling was assessed in tissue harvested 2, 4, 8 and 12 weeks after creation. Results The intramural principal stress ratio doubled after aneurysm creation due to increased longitudinal loads, triggering a remodeling response. A distinct wall layer with multi-directional collagen fibers developed between the media and adventitia as early as 2 weeks, and in all cases by 4 weeks with an average thickness of 50.6 ± 14.3 μm. Collagen fibers in this layer were multi-directional (AI = 0.56 ± 0.15) with low tortuosity (1.08 ± 0.02) compared with adjacent circumferentially aligned medial fibers (AI = 0.78 ± 0.12) and highly tortuous adventitial fibers (1.22 ± 0.03). A second phase of remodeling replaced circumferentially aligned fibers in the inner media with longitudinal fibers. A structurally motivated constitutive model with both remodeling modes was introduced along with methodology for determining material parameters from mechanical testing and multiphoton imaging. Conclusions A new mechanism was identified by which aneurysm walls can rapidly adapt to changes in load, ensuring the structural integrity of the aneurysm until a slower process of medial reorganization occurs. The rabbit model can be used to evaluate therapies to increase aneurysm wall stability. Keywords Cerebral aneurysm . Animal model . Collagen remodeling . Axial loading . Constitutive modeling
Introduction An intracranial aneurysm (IA) is an enlargement in the wall of a cerebral artery that is generally saccular in shape, though the geometry can be quite irregular [1]. Rupture of IAs is estimated to occur at a rate of 1.3% per year [2] and can cause subarachnoid hemorrhage with an associated mortality rate of 40–65% [3]. * A. M. Robertson [email protected] C. Sang [email protected] 1
Department of Mechanical Engineering and Materials Science, University of Pittsburgh, 3700 O’Hara Street, Pittsburgh, PA 15261, USA
2
Department of Radiology, Mayo Clinic, Rochester, MN, USA
3
Center for Biologic Imaging, University of Pittsburgh, Pittsburgh, PA, USA
Current treatments for IAs are largely aimed at isolating the aneurysm wall from the circulation through treatments that include placement of mechanical clips across the aneurysm neck, insertion of coils into the aneurysm sac a
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