A Pilot Study on Linking Tissue Mechanics with Load-Dependent Collagen Microstructures in Porcine Tricuspid Valve Leaflets

The tricuspid valve (TV) is composed of three leaflets that coapt during systole to prevent deoxygenated blood from re-entering the right atrium. The connection between the TV leaflets’ microstructure and the tissue-level mechanical responses has yet to be fully understood in the TV biomechanics soc...

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Main Authors: Luke T. Hudson, Samuel V. Jett, Katherine E. Kramer, Devin W. Laurence, Colton J. Ross, Rheal A. Towner, Ryan Baumwart, Ki Moo Lim, Arshid Mir, Harold M. Burkhart, Yi Wu, Chung-Hao Lee
Format: Article
Language:English
Published: MDPI AG 2020-06-01
Series:Bioengineering
Subjects:
Online Access:https://www.mdpi.com/2306-5354/7/2/60
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language English
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author Luke T. Hudson
Samuel V. Jett
Katherine E. Kramer
Devin W. Laurence
Colton J. Ross
Rheal A. Towner
Ryan Baumwart
Ki Moo Lim
Arshid Mir
Harold M. Burkhart
Yi Wu
Chung-Hao Lee
spellingShingle Luke T. Hudson
Samuel V. Jett
Katherine E. Kramer
Devin W. Laurence
Colton J. Ross
Rheal A. Towner
Ryan Baumwart
Ki Moo Lim
Arshid Mir
Harold M. Burkhart
Yi Wu
Chung-Hao Lee
A Pilot Study on Linking Tissue Mechanics with Load-Dependent Collagen Microstructures in Porcine Tricuspid Valve Leaflets
Bioengineering
tricuspid regurgitation
biaxial mechanical testing
polarized spatial frequency domain imaging
spatial alignment
collagen fiber reorientation
material anisotropy
author_facet Luke T. Hudson
Samuel V. Jett
Katherine E. Kramer
Devin W. Laurence
Colton J. Ross
Rheal A. Towner
Ryan Baumwart
Ki Moo Lim
Arshid Mir
Harold M. Burkhart
Yi Wu
Chung-Hao Lee
author_sort Luke T. Hudson
title A Pilot Study on Linking Tissue Mechanics with Load-Dependent Collagen Microstructures in Porcine Tricuspid Valve Leaflets
title_short A Pilot Study on Linking Tissue Mechanics with Load-Dependent Collagen Microstructures in Porcine Tricuspid Valve Leaflets
title_full A Pilot Study on Linking Tissue Mechanics with Load-Dependent Collagen Microstructures in Porcine Tricuspid Valve Leaflets
title_fullStr A Pilot Study on Linking Tissue Mechanics with Load-Dependent Collagen Microstructures in Porcine Tricuspid Valve Leaflets
title_full_unstemmed A Pilot Study on Linking Tissue Mechanics with Load-Dependent Collagen Microstructures in Porcine Tricuspid Valve Leaflets
title_sort pilot study on linking tissue mechanics with load-dependent collagen microstructures in porcine tricuspid valve leaflets
publisher MDPI AG
series Bioengineering
issn 2306-5354
publishDate 2020-06-01
description The tricuspid valve (TV) is composed of three leaflets that coapt during systole to prevent deoxygenated blood from re-entering the right atrium. The connection between the TV leaflets’ microstructure and the tissue-level mechanical responses has yet to be fully understood in the TV biomechanics society. This pilot study sought to examine the load-dependent collagen fiber architecture of the three TV leaflets, by employing a multiscale, combined experimental approach that utilizes tissue-level biaxial mechanical characterizations, micro-level collagen fiber quantification, and histological analysis. Our results showed that the three TV leaflets displayed greater extensibility in the tissues’ radial direction than in the circumferential direction, consistently under different applied biaxial tensions. Additionally, collagen fibers reoriented towards the direction of the larger applied load, with the largest changes in the alignment of the collagen fibers under radially-dominant loading. Moreover, collagen fibers in the belly region of the TV leaflets were found to experience greater reorientations compared to the tissue region closer to the TV annulus. Furthermore, histological examinations of the TV leaflets displayed significant regional variation in constituent mass fraction, highlighting the heterogeneous collagen microstructure. The combined experimental approach presented in this work enables the connection of tissue mechanics, collagen fiber microstructure, and morphology for the TV leaflets. This experimental methodology also provides a new research platform for future developments, such as multiscale models for the TVs, and the design of bioprosthetic heart valves that could better mimic the mechanical, microstructural, and morphological characteristics of the native tricuspid valve leaflets.
topic tricuspid regurgitation
biaxial mechanical testing
polarized spatial frequency domain imaging
spatial alignment
collagen fiber reorientation
material anisotropy
url https://www.mdpi.com/2306-5354/7/2/60
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spelling doaj-6f844b49f8a54bbaa09dc9495d5aecf92020-11-25T02:51:51ZengMDPI AGBioengineering2306-53542020-06-017606010.3390/bioengineering7020060A Pilot Study on Linking Tissue Mechanics with Load-Dependent Collagen Microstructures in Porcine Tricuspid Valve LeafletsLuke T. Hudson0Samuel V. Jett1Katherine E. Kramer2Devin W. Laurence3Colton J. Ross4Rheal A. Towner5Ryan Baumwart6Ki Moo Lim7Arshid Mir8Harold M. Burkhart9Yi Wu10Chung-Hao Lee11Biomechanics and Biomaterials Design Laboratory (BBDL), School of Aerospace and Mechanical Engineering, The University of Oklahoma, Norman, OK 73019, USABiomechanics and Biomaterials Design Laboratory (BBDL), School of Aerospace and Mechanical Engineering, The University of Oklahoma, Norman, OK 73019, USABiomechanics and Biomaterials Design Laboratory (BBDL), School of Aerospace and Mechanical Engineering, The University of Oklahoma, Norman, OK 73019, USABiomechanics and Biomaterials Design Laboratory (BBDL), School of Aerospace and Mechanical Engineering, The University of Oklahoma, Norman, OK 73019, USABiomechanics and Biomaterials Design Laboratory (BBDL), School of Aerospace and Mechanical Engineering, The University of Oklahoma, Norman, OK 73019, USAAdvanced Magnetic Resonance Center, MS 60, Oklahoma Medical Research Foundation, Oklahoma City, OK 73104, USADepartment of Veterinary Clinical Sciences, College of Veterinary Medicine, Washington State University, Pullman, WA 99164, USADepartment of Medical IT Convergence Engineering, Kumoh National Institute of Technology, Gumi, Gyeongbuk 39177, KoreaDivision of Pediatric Cardiology, Department of Pediatrics, The University of Oklahoma Health Sciences Center, Oklahoma City, OK 73104, USADivision of Cardiothoracic Surgery, Department of Surgery, The University of Oklahoma Health Sciences Center, Oklahoma City, OK 73104, USABiomechanics and Biomaterials Design Laboratory (BBDL), School of Aerospace and Mechanical Engineering, The University of Oklahoma, Norman, OK 73019, USABiomechanics and Biomaterials Design Laboratory (BBDL), School of Aerospace and Mechanical Engineering, The University of Oklahoma, Norman, OK 73019, USAThe tricuspid valve (TV) is composed of three leaflets that coapt during systole to prevent deoxygenated blood from re-entering the right atrium. The connection between the TV leaflets’ microstructure and the tissue-level mechanical responses has yet to be fully understood in the TV biomechanics society. This pilot study sought to examine the load-dependent collagen fiber architecture of the three TV leaflets, by employing a multiscale, combined experimental approach that utilizes tissue-level biaxial mechanical characterizations, micro-level collagen fiber quantification, and histological analysis. Our results showed that the three TV leaflets displayed greater extensibility in the tissues’ radial direction than in the circumferential direction, consistently under different applied biaxial tensions. Additionally, collagen fibers reoriented towards the direction of the larger applied load, with the largest changes in the alignment of the collagen fibers under radially-dominant loading. Moreover, collagen fibers in the belly region of the TV leaflets were found to experience greater reorientations compared to the tissue region closer to the TV annulus. Furthermore, histological examinations of the TV leaflets displayed significant regional variation in constituent mass fraction, highlighting the heterogeneous collagen microstructure. The combined experimental approach presented in this work enables the connection of tissue mechanics, collagen fiber microstructure, and morphology for the TV leaflets. This experimental methodology also provides a new research platform for future developments, such as multiscale models for the TVs, and the design of bioprosthetic heart valves that could better mimic the mechanical, microstructural, and morphological characteristics of the native tricuspid valve leaflets.https://www.mdpi.com/2306-5354/7/2/60tricuspid regurgitationbiaxial mechanical testingpolarized spatial frequency domain imagingspatial alignmentcollagen fiber reorientationmaterial anisotropy