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      Role of smooth muscle activation in the static and dynamic mechanical characterization of human aortas

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          Significance

          The rupture of aortic aneurysms causes around 10,000 deaths each year in the United States. Prosthetic tubes for aortic repair present a large mismatch of mechanical properties with the natural aorta, which has negative consequences for perfusion. This motivates research into the mechanical characterization of human aortas to develop a new generation of mechanically compatible aortic grafts. Experimental data and a suitable material model for human aortas with vascular smooth muscle (VSM) activation are not available. Hence, the present study provides experimental data that are needed. These data made it possible to develop a precise structure-based model of active aortic tissue. The results show the importance of VSM activation on the static and dynamic mechanical response of human aortas.

          Abstract

          Experimental data and a suitable material model for human aortas with smooth muscle activation are not available in the literature despite the need for developing advanced grafts; the present study closes this gap. Mechanical characterization of human descending thoracic aortas was performed with and without vascular smooth muscle (VSM) activation. Specimens were taken from 13 heart-beating donors. The aortic segments were cooled in Belzer UW solution during transport and tested within a few hours after explantation. VSM activation was achieved through the use of potassium depolarization and noradrenaline as vasoactive agents. In addition to isometric activation experiments, the quasistatic passive and active stress–strain curves were obtained for circumferential and longitudinal strips of the aortic material. This characterization made it possible to create an original mechanical model of the active aortic material that accurately fits the experimental data. The dynamic mechanical characterization was executed using cyclic strain at different frequencies of physiological interest. An initial prestretch, which corresponded to the physiological conditions, was applied before cyclic loading. Dynamic tests made it possible to identify the differences in the viscoelastic behavior of the passive and active tissue. This work illustrates the importance of VSM activation for the static and dynamic mechanical response of human aortas. Most importantly, this study provides material data and a material model for the development of a future generation of active aortic grafts that mimic natural behavior and help regulate blood pressure.

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          Most cited references43

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          Vascular Smooth Muscle Cells and Arterial Stiffening: Relevance in Development, Aging, and Disease.

          The cushioning function of large arteries encompasses distension during systole and recoil during diastole which transforms pulsatile flow into a steady flow in the microcirculation. Arterial stiffness, the inverse of distensibility, has been implicated in various etiologies of chronic common and monogenic cardiovascular diseases and is a major cause of morbidity and mortality globally. The first components that contribute to arterial stiffening are extracellular matrix (ECM) proteins that support the mechanical load, while the second important components are vascular smooth muscle cells (VSMCs), which not only regulate actomyosin interactions for contraction but mediate also mechanotransduction in cell-ECM homeostasis. Eventually, VSMC plasticity and signaling in both conductance and resistance arteries are highly relevant to the physiology of normal and early vascular aging. This review summarizes current concepts of central pressure and tensile pulsatile circumferential stress as key mechanical determinants of arterial wall remodeling, cell-ECM interactions depending mainly on the architecture of cytoskeletal proteins and focal adhesion, the large/small arteries cross-talk that gives rise to target organ damage, and inflammatory pathways leading to calcification or atherosclerosis. We further speculate on the contribution of cellular stiffness along the arterial tree to vascular wall stiffness. In addition, this review provides the latest advances in the identification of gene variants affecting arterial stiffening. Now that important hemodynamic and molecular mechanisms of arterial stiffness have been elucidated, and the complex interplay between ECM, cells, and sensors identified, further research should study their potential to halt or to reverse the development of arterial stiffness.
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            Hyperelastic modelling of arterial layers with distributed collagen fibre orientations.

            Constitutive relations are fundamental to the solution of problems in continuum mechanics, and are required in the study of, for example, mechanically dominated clinical interventions involving soft biological tissues. Structural continuum constitutive models of arterial layers integrate information about the tissue morphology and therefore allow investigation of the interrelation between structure and function in response to mechanical loading. Collagen fibres are key ingredients in the structure of arteries. In the media (the middle layer of the artery wall) they are arranged in two helically distributed families with a small pitch and very little dispersion in their orientation (i.e. they are aligned quite close to the circumferential direction). By contrast, in the adventitial and intimal layers, the orientation of the collagen fibres is dispersed, as shown by polarized light microscopy of stained arterial tissue. As a result, continuum models that do not account for the dispersion are not able to capture accurately the stress-strain response of these layers. The purpose of this paper, therefore, is to develop a structural continuum framework that is able to represent the dispersion of the collagen fibre orientation. This then allows the development of a new hyperelastic free-energy function that is particularly suited for representing the anisotropic elastic properties of adventitial and intimal layers of arterial walls, and is a generalization of the fibre-reinforced structural model introduced by Holzapfel & Gasser (Holzapfel & Gasser 2001 Comput. Meth. Appl. Mech. Eng. 190, 4379-4403) and Holzapfel et al. (Holzapfel et al. 2000 J. Elast. 61, 1-48). The model incorporates an additional scalar structure parameter that characterizes the dispersed collagen orientation. An efficient finite element implementation of the model is then presented and numerical examples show that the dispersion of the orientation of collagen fibres in the adventitia of human iliac arteries has a significant effect on their mechanical response.
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              Mechanisms of Vascular Smooth Muscle Contraction and the Basis for Pharmacologic Treatment of Smooth Muscle Disorders

              The smooth muscle cell directly drives the contraction of the vascular wall and hence regulates the size of the blood vessel lumen. We review here the current understanding of the molecular mechanisms by which agonists, therapeutics, and diseases regulate contractility of the vascular smooth muscle cell and we place this within the context of whole body function. We also discuss the implications for personalized medicine and highlight specific potential target molecules that may provide opportunities for the future development of new therapeutics to regulate vascular function.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc Natl Acad Sci U S A
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                12 January 2022
                18 January 2022
                12 January 2022
                : 119
                : 3
                : e2117232119
                Affiliations
                [1] aDepartment of Mechanical Engineering, McGill University , Montreal, QC H3A 0C3, Canada;
                [2] bResearch Center, Centre Hospitalier Universitaire de Montréal, Université de Montréal , Montreal, QC H2X 3E4, Canada;
                [3] cInstitute of Biomechanics, Graz University of Technology 8010 Graz, Austria;
                [4] dDepartment of Structural Engineering, Norwegian University of Science and Technology 7034 Trondheim, Norway;
                [5] eAdvanced Material Research Center, Technology Innovation Institute , Abu Dhabi, UAE
                Author notes
                1To whom correspondence may be addressed. Email: marco.amabili@ 123456mcgill.ca .

                Edited by Yonggang Huang, Northwestern University, Glencoe, IL; received September 22, 2021; accepted December 2, 2021

                Author contributions: M.A. designed research; G.F., I.D.B., F.G., A.K., and M.A. performed research; G.F., I.D.B., F.G., and M.A. analyzed data; and G.F., I.D.B., G.H., and M.A. wrote the paper.

                Author information
                https://orcid.org/0000-0002-4338-6041
                https://orcid.org/0000-0002-9666-9731
                https://orcid.org/0000-0001-8119-5775
                https://orcid.org/0000-0001-9340-4474
                Article
                202117232
                10.1073/pnas.2117232119
                8784113
                35022244
                943985fa-489b-4026-8fa5-fd2fa0fff8cf
                Copyright © 2022 the Author(s). Published by PNAS.

                This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                : 02 December 2021
                Page count
                Pages: 8
                Funding
                Funded by: Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada (NSERC) 501100000038
                Award ID: Discovery 2018-06609
                Award Recipient : Marco Amabili
                Funded by: Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada (NSERC) 501100000038
                Award ID: RTI 2019-00057
                Award Recipient : Marco Amabili
                Categories
                416
                Physical Sciences
                Engineering

                mechanical characterization,microstructural characterization,vascular smooth muscle activation,mechanical material model,human aorta

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