Abstract
This study investigated the effect of collagen fiber tortuosity distribution on the biomechanical failure and prefailure properties of arterial wall tissue. An in-silico model of the arterial wall was developed using data obtained from combined multiphoton microscopy imaging and uni-axial tensile testing. Layer-dependent properties were prescribed for collagen, elastin, and ground substance. Collagen fibers were modeled as discrete anisotropic elements, while elastin and ground substance were modeled as homogeneous isotropic components. Our parametric analysis, using a finite element approach, revealed that different parameters of collagen fibers tortuosity distribution significantly influence both prefailure and failure biomechanical properties. Increased fiber tortuosity improved the tissue strength whereas the dispersion in the tortuosity distribution reduced it. This study provides novel insights into the structural-mechanical interdependencies in arterial walls, offering potential targets for clinical assessments and therapeutic interventions aimed at mitigating rupture risks.
Issue Section:
Research Papers
References
1.
Hutson
, H. N.
, Marohl
, T.
, Anderson
, M.
, Eliceiri
, K.
, Campagnola
, P.
, and Masters
, K. S.
, 2016
, “Calcific Aortic Valve Disease Is Associated With Layer-Specific Alterations in Collagen Architecture
,” PLoS One
, 11
(9
), p. e0163858
.10.1371/journal.pone.01638582.
Panwar
, P.
, Butler
, G. S.
, Jamroz
, A.
, Azizi
, P.
, Overall
, C. M.
, and Brömme
, D.
, 2018
, “Aging-Associated Modifications of Collagen Affect Its Degradation by Matrix Metalloproteinases
,” Matrix Biol.
, 65
, pp. 30
–44
.10.1016/j.matbio.2017.06.0043.
Omens
, J. H.
, Miller
, T. R.
, and Covell
, J. W.
, 1997
, “Relationship Between Passive Tissue Strain and Collagen Uncoiling During Healing of Infarcted Myocardium
,” Cardiovasc. Res.
, 33
(2
), pp. 351
–358
.10.1016/S0008-6363(96)00206-44.
Monson
, K. L.
, Converse
, M. I.
, and Manley
, G. T.
, 2019
, “Cerebral Blood Vessel Damage in Traumatic Brain Injury
,” Clin. Biomech.
, 64
, pp. 98
–113
.10.1016/j.clinbiomech.2018.02.0115.
Signorelli
, F.
, Sela
, S.
, Gesualdo
, L.
, Chevrel
, S.
, Tollet
, F.
, Pailler-Mattei
, C.
, Tacconi
, L.
, Turjman
, F.
, Vacca
, A.
, and Schul
, D. B.
, 2018
, “Hemodynamic Stress, Inflammation, and Intracranial Aneurysm Development and Rupture: A Systematic Review
,” World Neurosurg.
, 115
, pp. 234
–244
.10.1016/j.wneu.2018.04.1436.
Kelly
, P. J.
, Stein
, J.
, Shafqat
, S.
, Eskey
, C.
, Doherty
, D.
, Chang
, Y.
, Kurina
, A.
, and Furie
, K. L.
, 2001
, “Functional Recovery After Rehabilitation for Cerebellar Stroke.
,” Stroke
, 32
(2
), pp. 530
–534
.10.1161/01.STR.32.2.5307.
Burns
, J. D.
, and Brown
, R. D.
, Jr., 2009
, “Treatment of Unruptured Intracranial Aneurysms: Surgery, Coiling, or Nothing?
,” Curr. Neurol. Neurosci. Rep.
, 9
(1
), pp. 6
–12
.10.1007/s11910-009-0002-08.
Wiebers
, D. O.
, 2003
, “Unruptured Intracranial Aneurysms: Natural History, Clinical Outcome, and Risks of Surgical and Endovascular Treatment
,” Lancet
, 362
(9378
), pp. 103
–110
.10.1016/S0140-6736(03)13860-39.
Juvela
, S.
, Poussa
, K.
, Lehto
, H.
, and Porras
, M.
, 2013
, “Natural History of Unruptured Intracranial Aneurysms: A Long-Term Follow-Up Study
,” Stroke
, 44
(9
), pp. 2414
–2421
.10.1161/STROKEAHA.113.00183810.
Broderick
, J. P.
, Brown
, R. D.
, Jr, Sauerbeck
, L.
, Hornung
, R.
, Huston
, J.
, III, Woo
, D.
, Anderson
, C.
, Rouleau
, G.
, Kleindorfer
, D.
, et al., 2009
, “Greater Rupture Risk for Familial as Compared to Sporadic Unruptured Intracranial Aneurysms
,” Stroke
, 40
(6
), pp. 1952
–1957
.10.1161/STROKEAHA.108.54257111.
Sacks
, M. S.
, 2003
, “Incorporation of Experimentally-Derived Fiber Orientation Into a Structural Constitutive Model for Planar Collagenous Tissues
,” ASME J. Biomech. Eng.
, 125
(2
), pp. 280
–287
.10.1115/1.154450812.
Chen
, H.
, Slipchenko
, M. N.
, Liu
, Y.
, Zhao
, X.
, Cheng
, J.-X.
, Lanir
, Y.
, and Kassab
, G. S.
, 2013
, “Biaxial Deformation of Collagen and Elastin Fibers in Coronary Adventitia
,” J. Appl. Physiol.
, 115
(11
), pp. 1683
–1693
.10.1152/japplphysiol.00601.201313.
Chow
, M.-J.
, Turcotte
, R.
, Lin
, C. P.
, and Zhang
, Y.
, 2014
, “Arterial Extracellular Matrix: A Mechanobiological Study of the Contributions and Interactions of Elastin and Collagen
,” Biophys. J.
, 106
(12
), pp. 2684
–2692
.10.1016/j.bpj.2014.05.01414.
Elhamian
, S.
, et al., 2014
, “The Effect of Collagen Fibers Volume Fraction on the Mechanical Properties of Articular Cartilage by Micromechanics Models.
,” Perfusion
, 30
(7
), pp. 1
–9
.10.1177/026765911454794215.
Gasser
, T. C.
, Gallinetti
, S.
, Xing
, X.
, Forsell
, C.
, Swedenborg
, J.
, and Roy
, J.
, 2012
, “Spatial Orientation of Collagen Fibers in the Abdominal Aortic Aneurysm's Wall and Its Relation to Wall Mechanics
,” Acta Biomater.
, 8
(8
), pp. 3091
–3103
.10.1016/j.actbio.2012.04.04416.
Horgan
, C. O.
, and Murphy
, J. G.
, 2017
, “Fiber Orientation Effects in Simple Shearing of Fibrous Soft Tissues
,” J. Biomech.
, 64
, pp. 131
–135
.10.1016/j.jbiomech.2017.09.01817.
Zimmerman
, S. D.
, McCormick
, R. J.
, Vadlamudi
, R. K.
, and Thomas
, D. P.
, 1993
, “Age and Training Alter Collagen Characteristics in Fast- and Slow-Twitch Rat Limb Muscle
,” J. Appl. Physiol. (1985)
, 75
(4
), pp. 1670
–1674
.10.1152/jappl.1993.75.4.167018.
Niestrawska
, J. A.
, Pukaluk
, A.
, Babu
, A. R.
, and Holzapfel
, G. A.
, 2022
, “Differences in Collagen Fiber Diameter and Waviness Between Healthy and Aneurysmal Abdominal Aortas.
,” Microsc. Microanal.
, pp. 1
–15
.10.1017/S143192762200062919.
Niestrawska
, J. A.
, Regitnig
, P.
, Viertler
, C.
, Cohnert
, T. U.
, Babu
, A. R.
, and Holzapfel
, G. A.
, 2019
, “The Role of Tissue Remodeling in Mechanics and Pathogenesis of Abdominal Aortic Aneurysms
,” Acta Biomater.
, 88
, pp. 149
–161
.10.1016/j.actbio.2019.01.07020.
Niestrawska
, J. A.
, Viertler
, C.
, Regitnig
, P.
, Cohnert
, T. U.
, Sommer
, G.
, and Holzapfel
, G. A.
, 2016
, “Microstructure and Mechanics of Healthy and Aneurysmatic Abdominal Aortas: Experimental Analysis and Modelling
,” J. R. Soc. Interface
, 13
(124
), p. 20160620
.10.1098/rsif.2016.062021.
Faiyaz‐Ul‐Haque
, M.
, Mubarak
, M.
, AbdulWahab
, A.
, AlRikabi
, A. C.
, Alsaeed
, A. H.
, Al‐Otaiby
, M.
, Nawaz
, Z.
, Zaidi
, S. H. E.
, and Basit
, S.
, 2022
, “Ultrastructure Abnormalities of Collagen and Elastin in Arab Patients With Arterial Tortuosity Syndrome
,” J. Cutaneous Pathol.
, 49
(7
), pp. 618
–622
.10.1111/cup.1422822.
Tsamis
, A.
, Krawiec
, J. T.
, and Vorp
, D. A.
, 2013
, “Elastin and Collagen Fibre Microstructure of the Human Aorta in Ageing and Disease: A Review
,” J. R. Soc. Interface
, 10
(83
), p. 20121004
.10.1098/rsif.2012.100423.
Saeidi
, S.
, Kainz
, M. P.
, Dalbosco
, M.
, Terzano
, M.
, and Holzapfel
, G. A.
, 2023
, “Histology-Informed Multiscale Modeling of Human Brain White Matter
,” Sci. Rep.
, 13
(1
), p. 19641
.10.1038/s41598-023-46600-324.
Lee
, P.-Y.
, Fryc
, G.
, Gnalian
, J.
, Wang
, B.
, Hua
, Y.
, Waxman
, S.
, Zhong
, F.
, Yang
, B.
, and Sigal
, I. A.
, 2024
, “Direct Measurements of Collagen Fiber Recruitment in the Posterior Pole of the Eye
,” Acta Biomater.
, 173
, pp. 135
–147
.10.1016/j.actbio.2023.11.01325.
Hill
, M. R.
, Duan
, X.
, Gibson
, G. A.
, Watkins
, S.
, and Robertson
, A. M.
, 2012
, “A Theoretical and Non-Destructive Experimental Approach for Direct Inclusion of Measured Collagen Orientation and Recruitment Into Mechanical Models of the Artery Wall
,” J. Biomech.
, 45
(5
), pp. 762
–771
.10.1016/j.jbiomech.2011.11.01626.
Weisbecker
, H.
, Unterberger
, M. J.
, and Holzapfel
, G. A.
, 2015
, “Constitutive Modelling of Arteries Considering Fibre Recruitment and Three-Dimensional Fibre Distribution
,” J. R. Soc. Interface
, 12
(105
), p. 20150111
.10.1098/rsif.2015.011127.
Dalbosco
, M.
, Carniel
, T. A.
, Fancello
, E. A.
, and Holzapfel
, G. A.
, 2021
, “Multiscale Numerical Analyses of Arterial Tissue With Embedded Elements in the Finite Strain Regime
,” Comput. Methods Appl. Mech. Eng.
, 381
, p. 113844
.10.1016/j.cma.2021.11384428.
Fortunato
, R. N.
, Robertson
, A. M.
, Sang
, C.
, Duan
, X.
, and Maiti
, S.
, 2021
, “Effect of Macro-Calcification on the Failure Mechanics of Intracranial Aneurysmal Wall Tissue
,” Exp. Mech.
, 61
(1
), pp. 5
–18
.10.1007/s11340-020-00657-729.
Bleiler
, C.
, and Röhrle
, O.
, 2022
, “Strain Measures and Energies for Crimped Fibres and Novel Analytical Expressions for Fibre Populations: Ingredients for Structural Fibre Network Models
,” J. Elasticity
, 150
(2
), pp. 401
–448
.10.1007/s10659-022-09920-530.
Thunes
, J. R.
, Phillippi
, J. A.
, Gleason
, T. G.
, Vorp
, D. A.
, and Maiti
, S.
, 2018
, “Structural Modeling Reveals Microstructure-Strength Relationship for Human Ascending Thoracic Aorta
,” J. Biomech.
, 71
, pp. 84
–93
.10.1016/j.jbiomech.2018.01.03731.
Li
, K.
, and Holzapfel
, G. A.
, 2019
, “Multiscale Modeling of Fiber Recruitment and Damage With a Discrete Fiber Dispersion Method
,” J. Mech. Phys. Solids
, 126
, pp. 226
–244
.10.1016/j.jmps.2019.01.02232.
Rolf-Pissarczyk
, M.
, Li
, K.
, Fleischmann
, D.
, and Holzapfel
, G. A.
, 2021
, “A Discrete Approach for Modeling Degraded Elastic Fibers in Aortic Dissection
,” Comput. Methods Appl. Mech. Eng.
, 373
, p. 113511
.10.1016/j.cma.2020.11351133.
Thunes
, J. R.
, Pal
, S.
, Fortunato
, R. N.
, Phillippi
, J. A.
, Gleason
, T. G.
, Vorp
, D. A.
, and Maiti
, S.
, 2016
, “A Structural Finite Element Model for Lamellar Unit of Aortic Media Indicates Heterogeneous Stress Field After Collagen Recruitment
,” J. Biomech.
, 49
(9
), pp. 1562
–1569
.10.1016/j.jbiomech.2016.03.03434.
Li
, D.
, and Robertson
, A. M.
, 2009
, “A Structural Multi-Mechanism Damage Model for Cerebral Arterial Tissue
,” ASME J. Biomech. Eng.
, 131
(10
), p. 101013
.10.1115/1.320255935.
Li
, D.
, Robertson
, A. M.
, Lin
, G.
, and Lovell
, M.
, 2012
, “Finite Element Modeling of Cerebral Angioplasty Using a Structural Multi‐Mechanism Anisotropic Damage Model
,” Int. J. Numer. Methods Eng.
, 92
(5
), pp. 457
–474
.10.1002/nme.434236.
Teng
, Z.
, Tang
, D.
, Zheng
, J.
, Woodard
, P. K.
, and Hoffman
, A. H.
, 2009
, “An Experimental Study on the Ultimate Strength of the Adventitia and Media of Human Atherosclerotic Carotid Arteries in Circumferential and Axial Directions
,” J. Biomech.
, 42
(15
), pp. 2535
–2539
.10.1016/j.jbiomech.2009.07.00937.
Schneider
, C. A.
, Rasband
, W. S.
, and Eliceiri
, K. W.
, 2012
, “NIH Image to ImageJ: 25 Years of Image Analysis
,” Nat. Methods
, 9
(7
), pp. 671
–675
.10.1038/nmeth.208938.
Robertson
, A. M.
, Duan
, X.
, Aziz
, K. M.
, Hill
, M. R.
, Watkins
, S. C.
, and Cebral
, J. R.
, 2015
, “Diversity in the Strength and Structure of Unruptured Cerebral Aneurysms
,” Ann. Biomed. Eng.
, 43
(7
), pp. 1502
–1515
.10.1007/s10439-015-1252-439.
Bredfeldt
, J. S.
, Liu
, Y.
, Pehlke
, C. A.
, Conklin
, M. W.
, Szulczewski
, J. M.
, Inman
, D. R.
, Keely
, P. J.
, Nowak
, R. D.
, Mackie
, T. R.
, and Eliceiri
, K. W.
, 2014
, “Computational Segmentation of Collagen Fibers From Second-Harmonic Generation Images of Breast Cancer
,” J. Biomed. Opt.
, 19
(1
), p. 016007
.10.1117/1.JBO.19.1.01600740.
Hill
, M.
, 2012
, “A Novel Approach for Combining Biomechanical and Micro-Structural Analyses to Assess the Mechanical and Damage Properties of the Artery Wall
,” Doctoral dissertation
, University of Pittsburgh
, Pittsburgh, PA.http://d-scholarship.pitt.edu/id/eprint/1047341.
Miyazaki
, H.
, and Hayashi
, K.
, 1999
, “Tensile Tests of Collagen Fibers Obtained From the Rabbit Patellar Tendon
,” Biomed. Microdev.
, 2
(2
), pp. 151
–157
.10.1023/A:100995380565842.
Cheng
, F.
, Birder
, L. A.
, Kullmann
, F. A.
, Hornsby
, J.
, Watton
, P. N.
, Watkins
, S.
, Thompson
, M.
, and Robertson
, A. M.
, 2018
, “Layer-Dependent Role of Collagen Recruitment During Loading of the Rat Bladder Wall
,” Biomech. Model. Mechanobiol.
, 17
(2
), pp. 403
–417
.10.1007/s10237-017-0968-543.
Gosline
, J.
, Lillie
, M.
, Carrington
, E.
, Guerette
, P.
, Ortlepp
, C.
, and Savage
, K.
, 2002
, “Elastic Proteins: Biological Roles and Mechanical Properties
,” Philos. Trans. R. Soc. London B: Biol. Sci.
, 357
(1418
), pp. 121
–132
.10.1098/rstb.2001.102244.
Lillie
, M. A.
, and Gosline
, J. M.
, 2007
, “Mechanical Properties of Elastin Along the Thoracic Aorta in the Pig
,” J. Biomech.
, 40
(10
), pp. 2214
–2221
.10.1016/j.jbiomech.2006.10.02545.
Burton
, A. C.
, 1954
, “Relation of Structure to Function of the Tissues of the Wall of Blood Vessels
,” Physiol. Rev.
, 34
(4
), pp. 619
–642
.10.1152/physrev.1954.34.4.61946.
Fonck
, E.
, Prod'hom
, G.
, Roy
, S.
, Augsburger
, L.
, Rüfenacht
, D. A.
, and Stergiopulos
, N.
, 2007
, “Effect of Elastin Degradation on Carotid Wall Mechanics as Assessed by a Constituent-Based Biomechanical Model
,” Am. J. Physiol.-Heart Circ. Physiol.
, 292
(6
), pp. H2754
–H2763
.10.1152/ajpheart.01108.200647.
Sasaki
, N.
, and Odajima
, S.
, 1996
, “Elongation Mechanism of Collagen Fibrils and Force-Strain Relations of Tendon at Each Level of Structural Hierarchy
,” J. Biomech.
, 29
(9
), pp. 1131
–1136
.10.1016/0021-9290(96)00024-348.
Korossis
, S.
, Bolland
, F.
, Southgate
, J.
, Ingham
, E.
, and Fisher
, J.
, 2009
, “Regional Biomechanical and Histological Characterisation of the Passive Porcine Urinary Bladder: Implications for Augmentation and Tissue Engineering Strategies
,” Biomaterials
, 30
(2
), pp. 266
–275
.10.1016/j.biomaterials.2008.09.03449.
He
, X.
, Auricchio
, F.
, Morganti
, S.
, and Lu
, J.
, 2021
, “Uniaxial Properties of Ascending Aortic Aneurysms in Light of Effective Stretch
,” Acta Biomater.
, 136
, pp. 306
–313
.10.1016/j.actbio.2021.09.02950.
Ricks
, T. M.
, 2012
, “A Multiscale Modeling Methodology for Composites That Includes Fiber Strength Stochastics
,” Master thesis
, Mississippi State University
, Mississippi State, MS.https://www.proquest.com/openview/ea934e308a755a2d902457ffc8a2a8c0/1?pq-origsite=gscholar&cbl=1875051.
Hariton
, I.
, deBotton
, G.
, Gasser
, T. C.
, and Holzapfel
, G. A.
, 2007
, “Stress-Driven Collagen Fiber Remodeling in Arterial Walls
,” Biomech. Model Mechanobiol.
, 6
(3
), pp. 163
–175
.10.1007/s10237-006-0049-752.
Hepworth
, D. G.
, Steven-Fountain
, A.
, Bruce
, D. M.
, and Vincent
, J. F. V.
, 2001
, “Affine Versus Non-Affine Deformation in Soft Biological Tissues, Measured by the Reorientation and Stretching of Collagen Fibres Through the Thickness of Compressed Porcine Skin
,” J. Biomech.
, 34
(3
), pp. 341
–346
.10.1016/S0021-9290(00)00183-453.
Lee
, C.-H.
, Zhang
, W.
, Liao
, J.
, Carruthers
, C. A.
, Sacks
, J. I.
, and Sacks
, M. S.
, 2015
, “On the Presence of Affine Fibril and Fiber Kinematics in the Mitral Valve Anterior Leaflet
,” Biophys. J.
, 108
(8
), pp. 2074
–2087
.10.1016/j.bpj.2015.03.01954.
Birder
, L. A.
, Wolf-Johnston
, A.
, Wein
, A. J.
, Cheng
, F.
, Grove-Sullivan
, M.
, Kanai
, A. J.
, Watson
, A. M.
, Stoltz
, D.
, Watkins
, S. C.
, et al., 2020
, “Purine Nucleoside Phosphorylase Inhibition Ameliorates Age-Associated Lower Urinary Tract Dysfunctions
,” JCI Insight
, 5
(20
), p. e140109.10.1172/jci.insight.14010955.
Lee
, K.-W.
, Gade
, P. S.
, Dong
, L.
, Zhang
, Z.
, Aral
, A. M.
, Gao
, J.
, Ding
, X.
, Stowell
, C. E. T.
, Nisar
, M. U.
, Kim
, K.
, Reinhardt
, D. P.
, Solari
, M. G.
, Gorantla
, V. S.
, Robertson
, A. M.
, and Wang
, Y.
, 2018
, “A Biodegradable Synthetic Graft for Small Arteries Matches the Performance of Autologous Vein in Rat Carotid Arteries
,” Biomaterials
, 181
, pp. 67
–80
.10.1016/j.biomaterials.2018.07.03756.
Gade
, P. S.
, 2019
, “Coupled Theoretical and Experimental Methods to Understand Growth and Remodeling of In Situ Engineered Vascular Grafts in Young and Aged Hosts,” Doctoral dissertation
, University of Pittsburgh
, Pittsburgh, PA.http://d-scholarship.pitt.edu/id/eprint/37078Copyright © 2025 by ASME
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