The Effect of Intraocular Pressure Load Boundary on the Biomechanics of the Human Conventional Aqueous Outflow Pathway

Background: Aqueous humor outflow resistance in the trabecular meshwork (TM), juxtacanalicular connective tissue (JCT), and Schlemm’s canal (SC) endothelium of the conventional outflow pathway actively contribute to intraocular pressure (IOP) regulation. Outflow resistance is actively affected by th...

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Main Authors: Alireza Karimi, Reza Razaghi, Seyed Mohammadali Rahmati, J. Crawford Downs, Ted S. Acott, Mary J. Kelley, Ruikang K. Wang, Murray Johnstone
Format: Article
Language:English
Published: MDPI AG 2022-11-01
Series:Bioengineering
Subjects:
Online Access:https://www.mdpi.com/2306-5354/9/11/672
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author Alireza Karimi
Reza Razaghi
Seyed Mohammadali Rahmati
J. Crawford Downs
Ted S. Acott
Mary J. Kelley
Ruikang K. Wang
Murray Johnstone
author_facet Alireza Karimi
Reza Razaghi
Seyed Mohammadali Rahmati
J. Crawford Downs
Ted S. Acott
Mary J. Kelley
Ruikang K. Wang
Murray Johnstone
author_sort Alireza Karimi
collection DOAJ
description Background: Aqueous humor outflow resistance in the trabecular meshwork (TM), juxtacanalicular connective tissue (JCT), and Schlemm’s canal (SC) endothelium of the conventional outflow pathway actively contribute to intraocular pressure (IOP) regulation. Outflow resistance is actively affected by the dynamic outflow pressure gradient across the TM, JCT, and SC inner wall tissues. The resistance effect implies the presence of a fluid–structure interaction (FSI) coupling between the outflow tissues and the aqueous humor. However, the biomechanical interactions between viscoelastic outflow tissues and aqueous humor dynamics are largely unknown. Methods: A 3D microstructural finite element (FE) model of a healthy human eye TM/JCT/SC complex was constructed with elastic and viscoelastic material properties for the bulk extracellular matrix and embedded elastic cable elements. The FE models were subjected to both idealized and a physiologic IOP load boundary using the FSI method. Results: The elastic material model for both the idealized and physiologic IOP load boundary at equal IOPs showed similar stresses and strains in the outflow tissues as well as pressure in the aqueous humor. However, outflow tissues with viscoelastic material properties were sensitive to the IOP load rate, resulting in different mechanical and hydrodynamic responses in the tissues and aqueous humor. Conclusions: Transient IOP fluctuations may cause a relatively large IOP difference of ~20 mmHg in a very short time frame of ~0.1 s, resulting in a rate stiffening in the outflow tissues. Rate stiffening reduces strains and causes a rate-dependent pressure gradient across the outflow tissues. Thus, the results suggest it is necessary to use a viscoelastic material model in outflow tissues that includes the important role of IOP load rate.
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spelling doaj.art-086c1b2f973941c691d204e632894c3c2023-11-24T03:47:06ZengMDPI AGBioengineering2306-53542022-11-0191167210.3390/bioengineering9110672The Effect of Intraocular Pressure Load Boundary on the Biomechanics of the Human Conventional Aqueous Outflow PathwayAlireza Karimi0Reza Razaghi1Seyed Mohammadali Rahmati2J. Crawford Downs3Ted S. Acott4Mary J. Kelley5Ruikang K. Wang6Murray Johnstone7Department of Ophthalmology and Visual Sciences, University of Alabama at Birmingham, Birmingham, AL 35233, USADepartment of Ophthalmology and Visual Sciences, University of Alabama at Birmingham, Birmingham, AL 35233, USASchool of Biological Sciences, Georgia Institute of Technology, Atlanta, GA 30332, USADepartment of Ophthalmology and Visual Sciences, University of Alabama at Birmingham, Birmingham, AL 35233, USADepartments of Ophthalmology and Biochemistry and Molecular Biology, Casey Eye Institute, Oregon Health & Science University, Portland, OR 97239, USADepartments of Ophthalmology and Integrative Biosciences, Casey Eye Institute, Oregon Health & Science University, Portland, OR 97239, USADepartment of Ophthalmology, University of Washington, Seattle, WA 98195, USADepartment of Ophthalmology, University of Washington, Seattle, WA 98195, USABackground: Aqueous humor outflow resistance in the trabecular meshwork (TM), juxtacanalicular connective tissue (JCT), and Schlemm’s canal (SC) endothelium of the conventional outflow pathway actively contribute to intraocular pressure (IOP) regulation. Outflow resistance is actively affected by the dynamic outflow pressure gradient across the TM, JCT, and SC inner wall tissues. The resistance effect implies the presence of a fluid–structure interaction (FSI) coupling between the outflow tissues and the aqueous humor. However, the biomechanical interactions between viscoelastic outflow tissues and aqueous humor dynamics are largely unknown. Methods: A 3D microstructural finite element (FE) model of a healthy human eye TM/JCT/SC complex was constructed with elastic and viscoelastic material properties for the bulk extracellular matrix and embedded elastic cable elements. The FE models were subjected to both idealized and a physiologic IOP load boundary using the FSI method. Results: The elastic material model for both the idealized and physiologic IOP load boundary at equal IOPs showed similar stresses and strains in the outflow tissues as well as pressure in the aqueous humor. However, outflow tissues with viscoelastic material properties were sensitive to the IOP load rate, resulting in different mechanical and hydrodynamic responses in the tissues and aqueous humor. Conclusions: Transient IOP fluctuations may cause a relatively large IOP difference of ~20 mmHg in a very short time frame of ~0.1 s, resulting in a rate stiffening in the outflow tissues. Rate stiffening reduces strains and causes a rate-dependent pressure gradient across the outflow tissues. Thus, the results suggest it is necessary to use a viscoelastic material model in outflow tissues that includes the important role of IOP load rate.https://www.mdpi.com/2306-5354/9/11/672trabecular meshworkjuxtacanalicular tissueSchlemm’s canalviscoelastic material modeltransient IOP fluctuationsfluid–structure interaction
spellingShingle Alireza Karimi
Reza Razaghi
Seyed Mohammadali Rahmati
J. Crawford Downs
Ted S. Acott
Mary J. Kelley
Ruikang K. Wang
Murray Johnstone
The Effect of Intraocular Pressure Load Boundary on the Biomechanics of the Human Conventional Aqueous Outflow Pathway
Bioengineering
trabecular meshwork
juxtacanalicular tissue
Schlemm’s canal
viscoelastic material model
transient IOP fluctuations
fluid–structure interaction
title The Effect of Intraocular Pressure Load Boundary on the Biomechanics of the Human Conventional Aqueous Outflow Pathway
title_full The Effect of Intraocular Pressure Load Boundary on the Biomechanics of the Human Conventional Aqueous Outflow Pathway
title_fullStr The Effect of Intraocular Pressure Load Boundary on the Biomechanics of the Human Conventional Aqueous Outflow Pathway
title_full_unstemmed The Effect of Intraocular Pressure Load Boundary on the Biomechanics of the Human Conventional Aqueous Outflow Pathway
title_short The Effect of Intraocular Pressure Load Boundary on the Biomechanics of the Human Conventional Aqueous Outflow Pathway
title_sort effect of intraocular pressure load boundary on the biomechanics of the human conventional aqueous outflow pathway
topic trabecular meshwork
juxtacanalicular tissue
Schlemm’s canal
viscoelastic material model
transient IOP fluctuations
fluid–structure interaction
url https://www.mdpi.com/2306-5354/9/11/672
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