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Multiscale Contrasts Between the Right and Left Ventricle Biomechanics in Healthy Adult Sheep and Translational Implications

Cardiac biomechanics play a significant role in the progression of structural heart diseases (SHDs). SHDs alter baseline myocardial biomechanics leading to single or bi-ventricular dysfunction. But therapies for left ventricle (LV) failure patients do not always work well for right ventricle (RV) fa...

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Autores principales: Liu, Wenqiang, Nguyen-Truong, Michael, LeBar, Kristen, Labus, Kevin M., Gray, Elisabeth, Ahern, Matt, Neelakantan, Sunder, Avazmohammadi, Reza, McGilvray, Kirk C., Puttlitz, Christian M., Wang, Zhijie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9068898/
https://www.ncbi.nlm.nih.gov/pubmed/35528212
http://dx.doi.org/10.3389/fbioe.2022.857638
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author Liu, Wenqiang
Nguyen-Truong, Michael
LeBar, Kristen
Labus, Kevin M.
Gray, Elisabeth
Ahern, Matt
Neelakantan, Sunder
Avazmohammadi, Reza
McGilvray, Kirk C.
Puttlitz, Christian M.
Wang, Zhijie
author_facet Liu, Wenqiang
Nguyen-Truong, Michael
LeBar, Kristen
Labus, Kevin M.
Gray, Elisabeth
Ahern, Matt
Neelakantan, Sunder
Avazmohammadi, Reza
McGilvray, Kirk C.
Puttlitz, Christian M.
Wang, Zhijie
author_sort Liu, Wenqiang
collection PubMed
description Cardiac biomechanics play a significant role in the progression of structural heart diseases (SHDs). SHDs alter baseline myocardial biomechanics leading to single or bi-ventricular dysfunction. But therapies for left ventricle (LV) failure patients do not always work well for right ventricle (RV) failure patients. This is partly because the basic knowledge of baseline contrasts between the RV and LV biomechanics remains elusive with limited discrepant findings. The aim of the study was to investigate the multiscale contrasts between LV and RV biomechanics in large animal species. We hypothesize that the adult healthy LV and RV have distinct passive anisotropic biomechanical properties. Ex vivo biaxial tests were performed in fresh sheep hearts. Histology and immunohistochemistry were performed to measure tissue collagen. The experimental data were then fitted to a Fung type model and a structurally informed model, separately. We found that the LV was stiffer in the longitudinal (outflow tract) than circumferential direction, whereas the RV showed the opposite anisotropic behavior. The anisotropic parameter K from the Fung type model accurately captured contrasting anisotropic behaviors in the LV and RV. When comparing the elasticity in the same direction, the LV was stiffer than the RV longitudinally and the RV was stiffer than the LV circumferentially, suggesting different filling patterns of these ventricles during diastole. Results from the structurally informed model suggest potentially stiffer collagen fibers in the LV than RV, demanding further investigation. Finally, type III collagen content was correlated with the low-strain elastic moduli in both ventricles. In summary, our findings provide fundamental biomechanical differences between the chambers. These results provide valuable insights for guiding cardiac tissue engineering and regenerative studies to implement chamber-specific matrix mechanics, which is particularly critical for identifying biomechanical mechanisms of diseases or mechanical regulation of therapeutic responses. In addition, our results serve as a benchmark for image-based inverse modeling technologies to non-invasively estimate myocardial properties in the RV and LV.
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spelling pubmed-90688982022-05-05 Multiscale Contrasts Between the Right and Left Ventricle Biomechanics in Healthy Adult Sheep and Translational Implications Liu, Wenqiang Nguyen-Truong, Michael LeBar, Kristen Labus, Kevin M. Gray, Elisabeth Ahern, Matt Neelakantan, Sunder Avazmohammadi, Reza McGilvray, Kirk C. Puttlitz, Christian M. Wang, Zhijie Front Bioeng Biotechnol Bioengineering and Biotechnology Cardiac biomechanics play a significant role in the progression of structural heart diseases (SHDs). SHDs alter baseline myocardial biomechanics leading to single or bi-ventricular dysfunction. But therapies for left ventricle (LV) failure patients do not always work well for right ventricle (RV) failure patients. This is partly because the basic knowledge of baseline contrasts between the RV and LV biomechanics remains elusive with limited discrepant findings. The aim of the study was to investigate the multiscale contrasts between LV and RV biomechanics in large animal species. We hypothesize that the adult healthy LV and RV have distinct passive anisotropic biomechanical properties. Ex vivo biaxial tests were performed in fresh sheep hearts. Histology and immunohistochemistry were performed to measure tissue collagen. The experimental data were then fitted to a Fung type model and a structurally informed model, separately. We found that the LV was stiffer in the longitudinal (outflow tract) than circumferential direction, whereas the RV showed the opposite anisotropic behavior. The anisotropic parameter K from the Fung type model accurately captured contrasting anisotropic behaviors in the LV and RV. When comparing the elasticity in the same direction, the LV was stiffer than the RV longitudinally and the RV was stiffer than the LV circumferentially, suggesting different filling patterns of these ventricles during diastole. Results from the structurally informed model suggest potentially stiffer collagen fibers in the LV than RV, demanding further investigation. Finally, type III collagen content was correlated with the low-strain elastic moduli in both ventricles. In summary, our findings provide fundamental biomechanical differences between the chambers. These results provide valuable insights for guiding cardiac tissue engineering and regenerative studies to implement chamber-specific matrix mechanics, which is particularly critical for identifying biomechanical mechanisms of diseases or mechanical regulation of therapeutic responses. In addition, our results serve as a benchmark for image-based inverse modeling technologies to non-invasively estimate myocardial properties in the RV and LV. Frontiers Media S.A. 2022-04-21 /pmc/articles/PMC9068898/ /pubmed/35528212 http://dx.doi.org/10.3389/fbioe.2022.857638 Text en Copyright © 2022 Liu, Nguyen-Truong, LeBar, Labus, Gray, Ahern, Neelakantan, Avazmohammadi, McGilvray, Puttlitz and Wang. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Bioengineering and Biotechnology
Liu, Wenqiang
Nguyen-Truong, Michael
LeBar, Kristen
Labus, Kevin M.
Gray, Elisabeth
Ahern, Matt
Neelakantan, Sunder
Avazmohammadi, Reza
McGilvray, Kirk C.
Puttlitz, Christian M.
Wang, Zhijie
Multiscale Contrasts Between the Right and Left Ventricle Biomechanics in Healthy Adult Sheep and Translational Implications
title Multiscale Contrasts Between the Right and Left Ventricle Biomechanics in Healthy Adult Sheep and Translational Implications
title_full Multiscale Contrasts Between the Right and Left Ventricle Biomechanics in Healthy Adult Sheep and Translational Implications
title_fullStr Multiscale Contrasts Between the Right and Left Ventricle Biomechanics in Healthy Adult Sheep and Translational Implications
title_full_unstemmed Multiscale Contrasts Between the Right and Left Ventricle Biomechanics in Healthy Adult Sheep and Translational Implications
title_short Multiscale Contrasts Between the Right and Left Ventricle Biomechanics in Healthy Adult Sheep and Translational Implications
title_sort multiscale contrasts between the right and left ventricle biomechanics in healthy adult sheep and translational implications
topic Bioengineering and Biotechnology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9068898/
https://www.ncbi.nlm.nih.gov/pubmed/35528212
http://dx.doi.org/10.3389/fbioe.2022.857638
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