Abstract
Atherosclerotic plaques can gradually develop in certain arteries. Disruption of fibrous tissue in plaques can result in plaque rupture and thromboembolism, leading to heart attacks and strokes. Collagen fibrils are important tissue building blocks and tissue strength depends on how fibrils are oriented. Fibril orientation in plaque tissue may potentially influence vulnerability to disruption. While X-ray scattering has previously been used to characterize fibril orientations in soft tissues and bones, it has never been used for characterization of human atherosclerotic plaque tissue. This study served to explore fibril orientation in specimens from human plaques using small angle X-ray scattering (SAXS). Plaque tissue was extracted from human femoral and carotid arteries, and each tissue specimen contained a region of calcified material. Three-dimensional (3D) collagen fibril orientation was determined along scan lines that started away from and then extended toward a given calcification. Fibrils were found to be oriented mainly in the circumferential direction of the plaque tissue at the majority of locations away from calcifications. However, in a number of cases, the dominant fibril direction differed near a calcification, changing from circumferential to longitudinal or thickness (radial) directions. Further study is needed to elucidate how these fibril orientations may influence plaque tissue stress–strain behavior and vulnerability to rupture.
Issue Section:
Technical Briefs
References
1.
Mackay
,
J.
, and
Mensah
,
G.
, eds., 2004
, Atlas of Heart Disease and Stroke
,
World Health Organization
,
Geneva, Switzerland
.2.
Simionescu
,
M.
, and
Sima
,
A.
, 2012
, “
Morphology of Atherosclerotic Lesions
,” Inflammation and Atherosclerosis
,
G.
Wick
and
C.
Grundtman
, eds.,
Springer
,
Vienna, Austria
, pp. 19
–37
.3.
Insull
,
W.
, 2009
, “
The Pathology of Atherosclerosis: Plaque Development and Plaque Response to Medical Treatment
,” Am. J. Med.
,
122
(1
), pp. S3
–S14
.10.1016/j.amjmed.2008.10.0134.
Hutcheson
,
J. D.
,
Goettsch
,
C.
,
Bertazzo
,
S.
,
Maldonado
,
N.
,
Ruiz
,
J. L.
,
Goh
,
W.
,
Yabusaki
,
K.
, 2016
, “
Genesis and Growth of Extracellular-Vesicle-Derived Micro Calcifications in Atherosclerotic Plaques
,” Nat. Mater.
,
15
(3
), pp. 335
–343
.10.1038/nmat45195.
Richardson
,
P.
, 2002
, “
Biomechanics of Plaque Rupture: Progress, Problems and New Frontiers
,” Ann. Biomed. Eng.
,
30
(4
), pp. 524
–536
.10.1114/1.14827816.
Carr
,
S.
,
Farb
,
A.
,
Pearce
,
W.
,
Virmani
,
R.
, and
Yao
,
J.
, 1996
, “
Atherosclerotic Plaque Rupture in Symptomatic Carotid Artery Stenosis
,” J. Vasc. Surg.
,
23
(5
), pp. 755
–766
.10.1016/S0741-5214(96)70237-97.
Fratzl
,
P.
, 2008
, “
Collagen: Structure and Mechanics, an Introduction
,” Collagen Structure and Mechanics
,
P.
Fratzl
, ed.,
Springer
,
New York
, pp. 1
–12
.8.
Chen
,
H.
, and
Kassab
,
G.
, 2016
, “
Microstructure-Based Biomechanics of Coronary Arteries in Health and Disease
,” J. Biomech.
,
49
(12
), pp. 2548
–2559
.10.1016/j.jbiomech.2016.03.0239.
Holzapfel
,
G.
, 2008
, “
Collagen in Arterial Walls: Biomechanical Aspects
,” Collagen Structure and Mechanics
,
P.
Fratzl
, ed.,
Springer
,
New York
, pp. 285
–324
.10.
Whelan
,
A.
,
Duffy
,
J.
,
Gaul
,
R. T.
,
O'Reilly
,
D.
,
Nolan
,
D. R.
,
Gunning
,
P.
,
Lally
,
C.
, and
Murphy
,
B. P.
, 2019
, “
Collagen Fibre Orientation and Dispersion Govern Ultimate Tensile Strength, Stiffness and the Fatigue Performance of Bovine Pericardium
,” J. Mech. Behav. Biomed. Mater.
,
90
, pp. 54
–60
.10.1016/j.jmbbm.2018.09.03811.
Libby
,
P.
, 2013
, “
Collagenases and Cracks in the Plaque
,” J. Clin. Invest.
,
123
(8
), pp. 3201
–3203
.10.1172/JCI6752612.
Adiguzel
,
E.
,
Ahmad
,
P.
,
Franco
,
C.
, and
Bendeck
,
M.
, 2009
, “
Collagens in the Progression and Complications of Atherosclerosis
,” Vasc. Med.
,
14
(1
), pp. 73
–89
.10.1177/1358863X0809480113.
Douglas
,
G.
,
Brown
,
A.
,
Gillard
,
J.
,
Bennett
,
M.
,
Sutcliffe
,
M.
, and
Teng
,
Z.
, 2017
, “
Impact of Fiber Structure on the Material Stability and Rupture Mechanisms of Coronary Atherosclerotic Plaque
,” Ann. Biomed. Eng.
,
45
(6
), pp. 1462
–1474
.10.1007/s10439-017-1827-314.
Holzapfel
,
G.
,
Mulvihill
,
J.
,
Cunnane
,
E.
, and
Walsh
,
M.
, 2014
, “
Computational Approaches for Analyzing the Mechanics of Atherosclerotic Plaques: A Review
,” J. Biomech.
,
47
(4
), pp. 859
–869
.10.1016/j.jbiomech.2014.01.01115.
Akyildiz
,
A.
,
Speelman
,
L.
,
Nieuwstadt
,
H.
,
van Brummelen
,
H.
,
Virmani
,
R.
,
van der Lugt
,
A.
,
van der Steen
,
A.
,
Wentzel
,
J.
, and
Gijsen
,
F.
, 2016
, “
The Effects of Plaque Morphology and Material Properties on Peak Cap Stress in Human Coronary Arteries
,” Comput. Methods Biomech. Biomed. Eng.
,
19
(7
), pp. 771
–779
.10.1080/10255842.2015.106209116.
Costopoulos
,
C.
,
Huang
,
Y.
,
Brown
,
A.
,
Calvert
,
P.
,
Hoole
,
S.
,
West
,
N.
,
Gillard
,
J.
,
Teng
,
Z.
, and
Bennett
,
M.
, 2017
, “
Plaque Rupture in Coronary Atherosclerosis Is Associated With Increased Plaque Structural Stress
,” JACC Cardiovasc. Imaging
,
10
(12
), pp. 1472
–1483
.10.1016/j.jcmg.2017.04.01717.
Noble
,
C.
,
Carlson
,
K.
,
Neumann
,
E.
,
Dragomir-Daescu
,
D.
,
Erdemir
,
A.
,
Lerman
,
A.
, and
Young
,
M.
, 2020
, “
Patient Specific Characterization of Artery and Plaque Material Properties in Peripheral Artery Disease
,” J. Mech. Behav. Biomed. Mater.
,
101
, p. 103453
.10.1016/j.jmbbm.2019.10345318.
Nandalur
,
K. R.
,
Baskurt
,
E.
,
Hagspiel
,
K. D.
,
Phillips
,
C. D.
, and
Kramer
,
C. M.
, 2005
, “
Calcified Carotid Atherosclerotic Plaque Is Associated Less With Ischemic Symptoms Than in Noncalcified Plaques on MDCT
,” Am. J. Roentgenol.
,
184
(1
), pp. 295
–298
.10.2214/ajr.184.1.0184029519.
Shaalan
,
W. E.
,
Cheng
,
H.
,
Gewertz
,
B.
,
McKinsey
,
J. F.
,
Schwartz
,
L. B.
,
Katz
,
D.
,
Cao
,
D.
,
Desai
,
T.
,
Glagov
,
S.
, and
Bassiouny
,
H. S.
, 2004
, “
Degree of Carotid Plaque Calcification in Relation to Symptomatic Outcome and Plaque Inflammation
,” J. Vasc. Surg.
,
40
(2
), pp. 262
–269
.10.1016/j.jvs.2004.04.02520.
Kwee
,
R.
, 2010
, “
Systematic Review on the Association Between Calcification in Carotid Plaques and Clinical Ischemic Symptoms
,” J. Vasc. Surg.
,
51
(4
), pp. 1015
–1025
.10.1016/j.jvs.2009.08.07221.
Wahlgren
,
C.
,
Zheng
,
W.
,
Shaalan
,
W.
,
Tang
,
J.
, and
Bassiouny
,
H.
, 2009
, “
Human Carotid Plaque Calcification and Vulnerability
,” Cerebrovasc. Dis.
,
27
(2
), pp. 193
–200
.10.1159/00018920422.
Prabhakaran
,
S.
,
Singh
,
R.
,
Zhou
,
X.
,
Ramas
,
R.
,
Sacco
,
R. L.
, and
Rundek
,
T.
, 2007
, “
Presence of Calcified Carotid Plaque Predicts Vascular Events: The Northern Manhattan Study
,” Atherosclerosis
,
195
(1
), pp. e197
–e201
.10.1016/j.atherosclerosis.2007.03.04423.
Kan
,
Y.
,
He
,
W.
,
Ning
,
B.
,
Li
,
H.
,
Wei
,
S.
, and
Yu
,
T.
, 2019
, “
The Correlation Between Calcification in Carotid Plaque and Stroke: Calcification May Be a Risk Factor for Stroke
,” Int. J. Clin. Exp. Pathol.
,
12
(3
), pp. 750
–758
.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC694518624.
Wenk
,
J.
,
Papadopoulos
,
P.
, and
Zohdi
,
T.
, 2010
, “
Numerical Modeling of Stress in Stenotic Arteries With Microcalcifications in a Micromechanical Approximation
,” ASME J. Biomech. Eng.
,
132
(9
), p. 091001.
10.1115/1.400135125.
Wong
,
K.
,
Thavornpattanapong
,
P.
,
Cheung
,
S.
,
Sun
,
Z.
, and
Tu
,
J.
, 2012
, “
Effect of Calcification on the Mechanical Stability of Plaque Based on a Three-Dimensional Carotid Bifurcation Model
,” BMC Cardiovasc. Disord.
,
12
, p. 7
.10.1186/1471-2261-12-726.
Kelly-Arnold
,
A.
,
Maldonado
,
N.
,
Laudier
,
D.
,
Aikawa
,
E.
,
Cardoso
,
L.
, and
Weinbaum
,
S.
, 2013
, “
Revised Microcalcification Hypothesis for Fibrous Cap Rupture in Human Coronary Arteries
,” Proc. Natl. Acad. Sci. U. S. A.
,
110
(26
), pp. 10741
–10746
.10.1073/pnas.130881411027.
Barrett
,
H.
,
Van der Heiden
,
K.
,
Farrell
,
E.
,
Gijsen
,
F.
, and
Akyildiz
,
A.
, 2019
, “
Calcifications in Atherosclerotic Plaques and Impact on Plaque Biomechanics
,” J. Biomech.
,
87
, pp. 1
–12
.10.1016/j.jbiomech.2019.03.00528.
Streeter
,
I.
, and
de Leeuw
,
N.
, 2011
, “
A Molecular Dynamics Study of the Interprotein Interactions in Collagen Fibrils
,” Soft Matter
,
7
(7
), pp. 3373
–3382
.10.1039/c0sm01192d29.
He
,
B.
, 2018
, Two-Dimensional X-Ray Diffraction
,
Wiley
,
Hoboken, NJ
.30.
Burger
,
C.
,
Hsiao
,
B.
, and
Chu
,
B.
, 2010
, “
Preferred Orientation in Polymer Fiber Scattering
,” Polym. Rev.
,
50
(1
), pp. 91
–111
.10.1080/1558372090350349431.
Pabisch
,
S.
,
Wagermaier
,
W.
,
Zander
,
T.
,
Li
,
C.
, and
Fratzl
,
P.
, 2013
, “
Imaging the Nanostructure of Bone and Dentin Through Small- and Wide-Angle X-Ray Scattering
,” Methods Enzymol.
,
532
, pp. 391
–413
.10.1016/B978-0-12-416617-2.00018-732.
Schmid
,
F.
,
Sommer
,
G.
,
Rappolt
,
M.
,
Schulze-Bauer
,
C. A. J.
,
Regitnig
,
P.
,
Holzapfel
,
G. A.
,
Laggner
,
P.
, and
Amenitsch
,
H.
, 2005
, “
In-Situ Tensile Testing of Human Aortas by Time-Resolved Small-Angle X-Ray Scattering
,” J. Synchrotron Radiat.
,
12
(6
), pp. 727
–733
.10.1107/S090904950501254933.
Purslow
,
P. P.
,
Wess
,
T. J.
, and
Hukins
,
D. W.
, 1998
, “
Collagen Orientation and Molecular Spacing During Creep and Stress-Relaxation in Soft Connective Tissues
,” J. Exp. Biol.
,
201
(1
), pp. 135
–142
.10.1242/jeb.201.1.13534.
Wells
,
H.
,
Sizeland
,
K.
,
Kirby
,
N.
,
Hawley
,
A.
,
Mudie
,
S.
, and
Haverkamp
,
R.
, 2015
, “
Collagen Fibril Structure and Strength in Acellular Dermal Matrix Materials of Bovine, Porcine, and Human Origin
,” ACS Biomater. Sci. Eng.
,
1
(10
), pp. 1026
–1038
.10.1021/acsbiomaterials.5b0031035.
Daxer
,
A.
, and
Fratzl
,
P.
, 1997
, “
Collagen Fibril Orientation in the Human Corneal Stroma and Its Implication in Keratoconus
,” Invest. Ophthalmol. Visual Sci.
,
38
(1
), pp. 121
–129
.https://www.pubmed.ncbi.nlm.nih.gov/900863736.
Meek
,
K.
, and
Boote
,
C.
, 2009
, “
The Use of X-Ray Scattering Techniques to Quantify the Orientation and Distribution of Collagen in the Corneal Stroma
,” Prog. Retinal Eye Res.
,
28
(5
), pp. 369
–392
.10.1016/j.preteyeres.2009.06.00537.
Pijanka
,
J. K.
,
Abass
,
A.
,
Sorensen
,
T.
,
Elsheikh
,
A.
, and
Boote
,
C.
, 2013
, “
A Wide-Angle X-Ray Diffraction Method for Quantifying Collagen Orientation Across Large Tissue Areas: Application to the Human Eyeball Coat
,” J. Appl. Crystallogr.
,
46
(5
), pp. 1481
–1489
.10.1107/S002188981302235838.
Liao
,
J.
,
Yang
,
L.
,
Grashow
,
J.
, and
Sacks
,
M.
, 2005
, “
Molecular Orientation of Collagen Intact Planar Connective Tissues Under Biaxial Stretch
,” Acta Biomater.
,
1
(1
), pp. 45
–54
.10.1016/j.actbio.2004.09.00739.
Sizeland
,
K. H.
,
Wells
,
H. C.
,
Higgins
,
J.
,
Cunanan
,
C. M.
,
Kirby
,
N.
,
Hawley
,
A.
,
Mudie
,
S. T.
, and
Haverkamp
,
R. G.
, 2014
, “
Age Dependent Differences in Collagen Alignment of Glutaraldehyde Fixed Bovine Pericardium
,” BioMed. Res. Int.
,
2014
, pp. 189
–197
.10.1155/2014/18919740.
Liao
,
J.
,
Yang
,
L.
,
Grashow
,
J.
, and
Sacks
,
M.
, 2007
, “
The Relation Between Collagen Fibril Kinematics and Mechanical Properties in the Mitral Valve Anterior Leaflet
,” ASME J. Biomech. Eng.
,
129
(1
), pp. 78
–87
.10.1115/1.240118641.
Hadian
,
M.
,
Corcoran
,
B.
,
Han
,
R.
,
Grossmann
,
J.
, and
Bradshaw
,
J.
, 2007
, “
Collagen Organization in Canine Myxomatous Mitral Valve Disease: An X-Ray Diffraction Study
,” Bipohys. J.
,
93
(7
), pp. 2472
–2476
.10.1529/biophysj.107.10784742.
Lee
,
C.-H.
,
Zhang
,
W.
,
Liao
,
J.
,
Carruthers
,
C. A.
,
Sacks
,
J. I.
, and
Sacks
,
M. S.
, 2015
, “
On the Presence of the Affine Fibril and Fiber Kinematics in the Mitral Valve Anterior Leaflet
,” Biophys. J.
,
108
(8
), pp. 2074
–2087
.10.1016/j.bpj.2015.03.01943.
Bunk
,
O.
,
Bech
,
M.
,
Jensen
,
T. H.
,
Feidenhans'l
,
R.
,
Binderup
,
T.
,
Menzel
,
A.
, and
Pfeiffer
,
F.
, 2009
, “
Multimodal X-Ray Scatter Imaging
,” New J. Phys.
,
11
(12
), p. 123016
.10.1088/1367-2630/11/12/12301644.
Moger
,
C.
,
Barrett
,
R.
,
Bleuet
,
P.
,
Bradley
,
D.
,
Ellis
,
R.
,
Green
,
E.
,
Knapp
,
K.
,
Muthuvelu
,
P.
, and
Winlove
,
C.
, 2007
, “
Regional Variations of Collagen Orientation in Normal and Diseased Articular Cartilage and Subchondral Bone Determined Using Small Angle X-Ray Scattering (SAXS)
,” Osteoarthritis Cartilage
,
15
(6
), pp. 682
–687
.10.1016/j.joca.2006.12.00645.
Inamdar
,
S.
,
Knight
,
D.
,
Terrill
,
N.
,
Karunaratne
,
A.
,
Cacho-Nerin
,
F.
,
Knight
,
M.
, and
Gupta
,
H.
, 2017
, “
The Secret Life of Collagen: Temporal Changes in Nanoscale Fibrillar Pre-Strain and Molecular Organization During Physiological Loading of Cartilage
,” ACS Nano
,
11
(10
), pp. 9728
–9737
.10.1021/acsnano.7b0056346.
Fratzl
,
P.
,
Schreiber
,
S.
, and
Boyde
,
A.
, 1996
, “
Characterization of Bone Mineral Crystals in Horse Radius by Small-Angle X-Ray Scattering
,” Calcif. Tissue Int.
,
58
(5
), pp. 341
–346
.10.1007/BF0250938347.
Wagermaier
,
W.
,
Gupta
,
H.
,
Gourrier
,
A.
,
Paris
,
O.
,
Roschger
,
P.
,
Burghammer
,
M.
,
Riekel
,
C.
, and
Fratzl
,
P.
, 2007
, “
Scanning Texture Analysis of Lamellar Bone Using Microbeam Synchrotron X-Ray Radiation
,” J. Appl. Crystallogr.
,
40
(1
), pp. 115
–120
.10.1107/S002188980604488848.
Liu
,
Y.
,
Manjubala
,
I.
,
Roschger
,
P.
,
Schell
,
H.
,
Duda
,
G.
, and
Fratzl
,
P.
, 2010
, “
Mineral Crystal Alignment in Mineralized Fracture Callus Determined by 3D Small-Angle Scattering
,” J. Phys.: Conf. Ser.
,
247
(1
), p. 012031
.10.1088/1742-6596/247/1/01203149.
Seidel
,
R.
,
Gourrier
,
A.
,
Kerschnitzki
,
M.
,
Burghammer
,
M.
,
Fratzl
,
P.
,
Gupta
,
H. S.
, and
Wagermaier
,
W.
, 2012
, “
Synchrotron 3D SAXS Analysis of Bone Nanostructure
,” Bioinspired, Biomimetic Nanobiomater.
,
1
(2
), pp. 123
–132
.10.1680/bbn.11.0001450.
Granke
,
M.
,
Gourrier
,
A.
,
Rupin
,
F.
,
Raum
,
K.
,
Peyrin
,
F.
,
Burghammer
,
M.
,
Saied
,
A.
, and
Laugier
,
P.
, 2013
, “
Microfibril Orientation Dominated the Micro Elastic Properties of Human Bone Tissue at the Lamellar Length Scale
,” PLoS One
,
8
(3
), p. e58043
.10.1371/journal.pone.005804351.
Georgiadis
,
M.
,
Guizar-Sicairos
,
M.
,
Zwahlen
,
A.
,
Trüssel
,
A. J.
,
Bunk
,
O.
,
Müller
,
R.
, and
Schneider
,
P.
, 2015
, “
3D Scanning SAXS: A Novel Method for the Assessment of Bone Ultrastructure Orientation
,” Bone
,
71
, pp. 42
–52
.10.1016/j.bone.2014.10.00252.
Liebi
,
M.
,
Georgiadis
,
M.
,
Menzel
,
A.
,
Schneider
,
P.
,
Kohlbrecher
,
J.
,
Bunk
,
O.
, and
Guizar-Sicairos
,
M.
, 2015
, “
Nanostructure Surveys of Macroscopic Specimens by Small-Angle Scattering Tensor Tomography
,” Nature
,
527
(7578
), pp. 349
–352
.10.1038/nature1605653.
Schaff
,
F.
,
Bech
,
M.
,
Zaslansky
,
P.
,
Jud
,
C.
,
Liebi
,
M.
,
Guizar-Sicairos
,
M.
, and
Pfeiffer
,
F.
, 2015
, “
Six Dimensional Real and Reciprocal Space Small-Angle X-Ray Scattering Tomography
,” Nature
,
527
(7578
), pp. 353
–356
.10.1038/nature1606054.
Gray
,
H.
, 1959
, Anatomy of the Human Body
,
Lea & Febiger
,
Philadelphia, PA
.55.
Laclaustra
,
M.
,
Casasnovas
,
J.
,
Fernandez-Ortiz
,
A.
,
Fuster
,
V.
,
León-Latre
,
M.
,
Jiménez-Borreguero
,
L.
,
Pocovi
,
M.
, 2016
, “
Femoral and Carotid Subclinical Atherosclerosis Association With Risk Factors and Coronary Calcium: The AWHS Study
,” J. Am. Coll. Cardiol.
,
67
(11
), pp. 1263
–1274
.10.1016/j.jacc.2015.12.05656.
McDermott
,
M.
,
Liu
,
K.
,
Carroll
,
T.
,
Tian
,
L.
,
Ferrucci
,
L.
,
Li
,
D.
,
Carr
,
J.
, 2011
, “
Superficial Femoral Artery Plaque and Functional Performance in Peripheral Arterial Disease: Walking and Leg Circulation Study (WALCS III)
,” JACC: Cardiovasc. Imaging
,
4
(7
), pp. 730
–739
.10.1016/j.jcmg.2011.04.00957.
McDermott
,
M.
,
Carroll
,
T.
,
Kibbe
,
M.
,
Kramer
,
C.
,
Liu
,
K.
,
Guralnik
,
J.
,
Keeling
,
A.
, 2013
, “
Proximal Superficial Femoral Artery Occlusion, Collateral Vessels, and Walking Performance in Peripheral Artery Disease
,” JACC: Cardiovasc. Imaging
,
6
(6
), pp. 687
–694
.10.1016/j.jcmg.2012.10.02458.
Blanton
,
T. N.
,
Huang
,
T. C.
,
Toraya
,
H.
,
Hubbard
,
C. R.
,
Robie
,
S. B.
,
Louër
,
D.
,
Göbel
,
H. E.
,
Will
,
G.
,
Gilles
,
R.
, and
Raftery
,
T.
, 1995
, “
JCPDS—International Centre for Diffraction Data Round Robin Study of Silver Behenate. A Possible Low-Angle X-Ray Diffraction Calibration Standard
,” Powder Diffr.
,
10
(2
), pp. 91
–95
.10.1017/S088571560001442159.
Deymier-Black
,
A.
,
Almer
,
J.
,
Stock
,
S.
, and
Dunand
,
D.
, 2012
, “
Variability in the Elastic Properties of Bovine Dentin at Multiple Length Scales
,” J. Mech. Behav. Biomed. Mater.
,
5
(1
), pp. 71
–81
.10.1016/j.jmbbm.2011.08.00560.
Hubbell
,
J.
, and
Seltzer
,
S.
, 1995
, “
Tables of X-Ray Mass Attenuation Coefficients and Mass Energy-Absorption Coefficients from1 keV to 20 MeV for Elements Z = 1 to 92 and 48 Additional Substances of Dosimetric Interest
,” National Institute of Standards and Technology
, Gaithersburg, MD, Database No. 126.https://www.nist.gov/publications/tables-x-ray-mass-attenuation-coefficients-and-mass-energyabsorption-coefficients-1-061.
Alavi
,
S.
,
Ruiz
,
V.
,
Krasieva
,
T.
,
Botvinick
,
E.
, and
Kheradvar
,
A.
, 2013
, “
Characterizing the Collagen Fiber Orientation in Pericardial Leaflets Under Mechanical Loading Conditions
,” Ann. Biomed. Eng.
,
41
(3
), pp. 547
–561
.10.1007/s10439-012-0696-z62.
Kamma-Lorger
,
C.
,
Hayes
,
S.
,
Boote
,
C.
,
Burghammer
,
M.
,
Boulton
,
M.
, and
Meek
,
K.
, 2009
, “
Effects on Collagen Orientation in the Cornea After Trephine Injury
,” Mol. Vision
,
15
, pp. 378
–385
.https://pubmed.ncbi.nlm.nih.gov/1923463163.
Jan
,
N.
,
Grimm
,
J.
,
Tran
,
H.
,
Lathrop
,
K.
,
Wollstein
,
G.
,
Bilonick
,
R.
,
Ishikawa
,
H.
,
Kagemann
,
L.
,
Schuman
,
J.
, and
Sigal
,
I.
, 2015
, “
Polarization Microscopy for Characterizing Fiber Orientation of Ocular Tissues
,” Biomed. Opt. Express
,
6
(12
), pp. 4705
–4718
.10.1364/BOE.6.00470564.
Howat
,
W.
, and
Wilson
,
B.
, 2014
, “
Tissue Fixation and the Effect of Molecular Fixatives on Downstream Staining Procedures
,” Methods
,
70
(1
), pp. 12
–19
.10.1016/j.ymeth.2014.01.02265.
Hickey
,
D.
, and
Hukins
,
D.
, 1979
, “
Effect of Methods of Preservation on the Arrangement of Collagen Fibrils in Connective Tissue Matrices: An X-Ray Diffraction Study of Annulus Fibrosus
,” Connect. Tissue Res.
,
6
(4
), pp. 223
–228
.10.3109/0300820790915232466.
Yasui
,
T.
,
Tohno
,
Y.
, and
Araki
,
T.
, 2004
, “
Characterization of Collagen Orientation in Human Dermis by Two-Dimensional Second Harmonic Generation Polarimetry
,” Biomed. Opt.
,
9
(2
), pp. 259
–264
.10.1117/1.164411667.
Heidelbach
,
F.
,
Riekel
,
C.
, and
Wenk
,
H.
, 1999
, “
Quantitative Texture Analysis of Small Domains With Synchrotron Radiation X-Rays
,” J. Appl. Crystallogr.
,
32
(5
), pp. 841
–849
.10.1107/S002188989900499968.
Kirby
,
N. M.
,
Mudie
,
S. T.
,
Hawley
,
A. M.
,
Cookson
,
D. J.
,
Mertens
,
H. D. T.
,
Cowieson
,
N.
, and
Samardzic-Boban
,
V.
, 2013
, “
A Low-Background-Intensity Focusing Small-Angle Scattering Undulator Beamline
,” J. Appl. Crystallogr.
,
46
(6
), pp. 1670
–1680
.10.1107/S002188981302774X69.
McLean
,
J. P.
,
Gan
,
Y.
,
Lye
,
T. H.
,
Qu
,
D.
,
Lu
,
H. H.
, and
Hendon
,
C. P.
, 2019
, “
High-Speed Collagen Fiber Modeling and Orientation Quantification for Optical Coherence Tomography Imaging
,” Opt. Express
,
27
(10
), pp. 14457
–14471
.10.1364/OE.27.01445770.
Giattina
,
S.
,
Courtney
,
B.
,
Herz
,
P.
,
Harman
,
M.
,
Shortkroff
,
S.
,
Stamper
,
D.
,
Liu
,
B.
,
Fujimoto
,
J.
, and
Brezinski
,
M.
, 2006
, “
Assessment of Coronary Plaque Collagen With Polarization Sensitive Optical Coherence Tomography (PS-OCT)
,” Int. J. Cardiol.
,
107
(3
), pp. 400
–409
.10.1016/j.ijcard.2005.11.03671.
Nadkarni
,
S.
,
Pierce
,
M.
,
Park
,
B.
,
de Boer
,
J.
,
Whittaker
,
P.
,
Bouma
,
B.
,
Bressner
,
J.
,
Halpern
,
E.
,
Houser
,
S.
, and
Tearney
,
G.
, 2007
, “
Measurement of Collagen and Smooth Muscle Cell Content in Atherosclerotic Plaques Using Polarization-Sensitive Optical Coherence Tomography
,” J. Am. Coll. Cardiol.
,
49
(13
), pp. 1474
–1481
.10.1016/j.jacc.2006.11.04072.
Kuo
,
W.
,
Chou
,
N.
,
Chou
,
C.
,
Lai
,
C.
,
Huang
,
H.
,
Wang
,
S.
, and
Shyu
,
J.
, 2007
, “
Polarization-Sensitive Optical Coherence Tomography for Imaging Human Atherosclerosis
,” Appl. Opt.
,
46
(13
), pp. 2520
–2527
.10.1364/AO.46.00252073.
Azinfar
,
L.
,
Ravanfar
,
M.
,
Wang
,
Y.
,
Zhang
,
K.
,
Duan
,
D.
, and
Yao
,
G.
, 2017
, “
High Resolution Imaging of the Fibrous Microstructure in Bovine Common Carotid Artery Using Optical Polarization Tractography
,” J. Biophotonics
,
10
(2
), pp. 231
–241
.10.1002/jbio.20150022974.
Akyildiz
,
A. C.
,
Chai
,
C.-K.
,
Oomens
,
C. W. J.
,
van der Lugt
,
A.
,
Baaijens
,
F. P. T.
,
Strijkers
,
G. J.
, and
Gijsen
,
F. J. H.
, 2017
, “
3D Fiber Orientation in Atherosclerotic Carotid Plaques
,” J. Struct. Biol.
,
200
(1
), pp. 28
–35
.10.1016/j.jsb.2017.08.00375.
Sacks
,
M.
,
Smith
,
D.
, and
Hiester
,
E.
, 1997
, “
A Small Angle Light Scattering Device for Planar Connective Tissue Microstructural Analysis
,” Ann. Biomed. Eng.
,
25
(4
), pp. 678
–689
.10.1007/BF0268484576.
Gaul
,
R.
,
Nolan
,
D.
, and
Lally
,
C.
, 2017
, “
Collagen Fibre Characterization in Arterial Tissue Under Load Using SALS
,” J. Mech. Behav. Biomed. Mater.
,
75
, pp. 359
–368
.10.1016/j.jmbbm.2017.07.03677.
Davis
,
L. A.
,
Stewart
,
S. E.
,
Carsten
,
C. G.
,
Snyder
,
B. A.
,
Sutton
,
M. A.
, and
Lessner
,
S. M.
, 2016
, “
Characterization of Fracture Behavior of Human Atherosclerotic Fibrous Caps Using a Miniature Single Edge Notched Tensile Test
,” Acta Biomater.
,
43
, pp. 101
–111
.10.1016/j.actbio.2016.07.02778.
Sang
,
C.
,
Maiti
,
S.
,
Fortunato
,
R.
,
Kofler
,
J.
, and
Robertson
,
A.
, 2018
, “
A Uniaxial Testing Approach for Consistent Failure in Vascular Tissues
,” ASME J. Biomech. Eng.
,
140
(6
), p. 061010
.10.1115/1.403957779.
Deymier
,
A.
,
An
,
Y.
,
Boyle
,
J.
,
Schwartz
,
A.
,
Birman
,
V.
,
Genin
,
G.
,
Thomopoulos
,
S.
, and
Barber
,
A.
, 2017
, “
Micro-Mechanical Properties of the Tendon-to-Bone Attachment
,” Acta Biomater.
,
56
, pp. 25
–35
.10.1016/j.actbio.2017.01.03780.
Barth
,
H.
,
Zimmerman
,
E.
,
Schaible
,
E.
,
Tang
,
S.
,
Alliston
,
T.
, and
Ritchie
,
R.
, 2011
, “
Characterization of the Effects of X-Ray Irradiation on the Hierarchical Structure and Mechanical Properties of Human Cortical Bone
,” Biomaterials
,
32
(34
), pp. 8892
–8904
.10.1016/j.biomaterials.2011.08.013Copyright © 2022 by ASME
You do not currently have access to this content.
