Abstract

Aortic aneurysms are inherently unpredictable. One can never be sure whether any given aneurysm may rupture or dissect. Clinically, the criteria for surgical intervention are based on size and growth rate, but it remains difficult to identify a high-risk aneurysm, which may require intervention before the cutoff criteria, versus an aneurysm than can be treated safely by more conservative measures. In this work, we created a computational microstructural model of a medial lamellar unit (MLU) incorporating (1) growth and remodeling laws applied directly to discrete, individual fibers, (2) separate but interacting fiber networks for collagen, elastin, and smooth muscle, (3) active and passive smooth-muscle cell mechanics, and (4) failure mechanics for all three fiber types. The MLU model was then used to study different pathologies and microstructural anomalies that may play a role in vascular growth and failure. Our model recapitulated many aspects of arterial remodeling under hypertension with no underlying genetic syndrome including remodeling dynamics, tissue mechanics, and failure. Syndromic effects (smooth muscle cell (SMC) dysfunction or elastin fragmentation) drastically changed the simulated remodeling process, tissue behavior, and tissue strength. Different underlying pathologies were able to produce similarly dilatated vessels with different failure properties, providing a partial explanation for the imperfect nature of aneurysm size as a predictor of outcome.

References

1.
Milewicz
,
D. M.
,
Guo
,
D.-C.
,
Tran-Fadulu
,
V.
,
Lafont
,
A. L.
,
Papke
,
C. L.
,
Inamoto
,
S.
,
Kwartler
,
C. S.
, and
Pannu
,
H.
,
2008
, “
Genetic Basis of Thoracic Aortic Aneurysms and Dissections: Focus on Smooth Muscle Cell Contractile Dysfunction
,”
Annu. Rev. Genomics Hum. Genet.
,
9
(
1
), pp.
283
302
.10.1146/annurev.genom.8.080706.092303
2.
National Center for Chronic Disease Prevention and Health Promotion, Division for Heart Disease and Stroke Prevention, 2019, “
Aortic Aneurysm
,” CDC, Atlanta, GA, accessed Mar. 9, 2020, https://www.cdc.gov/heartdisease/aortic_aneurysm.htm
3.
O'Connell
,
M.
,
Murthy
,
S.
,
Phan
,
S.
,
Xu
,
C.
,
Buchanan
,
J.
,
Spilker
,
R.
,
Dalman
,
R.
,
Zarins
,
C.
,
Denk
,
W.
, and
Taylor
,
C.
,
2008
, “
The Three-Dimensional Micro- and Nanostructure of the Aortic Medial Lamellar Unit Measured Using 3D Confocal and Electron Microscopy Imaging
,”
Matrix Biol.
,
27
(
3
), pp.
171
181
.10.1016/j.matbio.2007.10.008
4.
Humphrey
,
J. D.
,
2002
,
Cardiovascular Solid Mechanics
,
Springer
,
New York
.
5.
Treuting
,
P. M.
,
Dintzis
,
S. M.
, and
Montine
,
K. S.
,
2012
,
Comparative Anatomy and Histology
,
Elsevier
, San Diego, CA.
6.
Wheeler
,
J. B.
,
Mukherjee
,
R.
,
Stroud
,
R. E.
,
Jones
,
J. A.
, and
Ikonomidis
,
J. S.
,
2015
, “
Relation of Murine Thoracic Aortic Structural and Cellular Changes With Aging to Passive and Active Mechanical Properties
,”
J. Am. Heart Assoc.
, 4(3), pp.
1
9
.10.1161/JAHA.114.001744
7.
Wagenseil
,
J. E.
, and
Mecham
,
R. P.
,
2012
, “
Elastin in Large Artery Stiffness and Hypertension
,”
J. Cardiovasc. Transl. Res.
,
5
(
3
), pp.
264
273
.10.1007/s12265-012-9349-8
8.
Aaron
,
B. B.
, and
Gosline
,
J. M.
,
1981
, “
Elastin as a Random-Network Elastomer: A Mechanical and Optical Analysis of Single Elastin Fibers
,”
Biopolymers
,
20
(
6
), pp.
1247
1260
.10.1002/bip.1981.360200611
9.
Mouw
,
J. K.
,
Ou
,
G.
, and
Weaver
,
V. M.
,
2014
, “
Extracellular Matrix Assembly: A Multiscale Deconstruction
,”
Nat. Rev. Mol. Cell Biol.
,
15
(
12
), pp.
771
785
.10.1038/nrm3902
10.
Nissen
,
R.
,
Cardinale
,
G. J.
, and
Udenfriend
,
S.
,
1978
, “
Increased Turnover of Arterial Collagen in Hypertensive Rats
,”
Proc. Natl. Acad. Sci. U. S. A.
,
75
(
1
), pp.
451
453
.10.1073/pnas.75.1.451
11.
Revenko
,
I.
,
Sommer
,
F.
,
Minh
,
D. T.
,
Garrone
,
R.
, and
Franc
,
J.-M.
,
1994
, “
Atomic Force Microscopy Study of the Collagen Fibre Structure
,”
Biol. Cell
,
80
(
1
), pp.
67
69
.10.1016/0248-4900(94)90019-1
12.
Flynn
,
B. P.
,
Bhole
,
A. P.
,
Saeidi
,
N.
,
Liles
,
M.
,
Dimarzio
,
C. A.
, and
Ruberti
,
J. W.
,
2010
, “
Mechanical Strain Stabilizes Reconstituted Collagen Fibrils Against Enzymatic Degradation by Mammalian Collagenase Matrix Metalloproteinase 8 (MMP-8)
,”
PLoS One
,
5
(
8
), p.
e12337
.10.1371/journal.pone.0012337
13.
Ruberti
,
J. W.
, and
Hallab
,
N. J.
,
2005
, “
Strain-Controlled Enzymatic Cleavage of Collagen in Loaded Matrix
,”
Biochem. Biophys. Res. Commun.
,
336
(
2
), pp.
483
489
.10.1016/j.bbrc.2005.08.128
14.
Flynn
,
B. P.
,
Tilburey
,
G. E.
, and
Ruberti
,
J. W.
,
2013
, “
Highly Sensitive Single-Fibril Erosion Assay Demonstrates Mechanochemical Switch in Native Collagen Fibrils
,”
Biomech. Model. Mechanobiol.
,
12
(
2
), pp.
291
300
.10.1007/s10237-012-0399-2
15.
Martyn
,
C.
, and
Greenwald
,
S.
,
1997
, “
Impaired Synthesis of Elastin in Walls of Aorta and Large Conduit Arteries During Early Development as an Initiating Event in Pathogenesis of Systemic Hypertension
,”
Lancet
,
350
(
9082
), pp.
953
955
.10.1016/S0140-6736(96)10508-0
16.
Win
,
Z.
,
Buksa
,
J. M.
,
Steucke
,
K. E.
,
Gant Luxton
,
G. W.
,
Barocas
,
V. H.
, and
Alford
,
P. W.
,
2017
, “
Cellular Microbiaxial Stretching to Measure a Single-Cell Strain Energy Density Function
,”
J. Biomech. Eng.
,
139
(
7
), p.
071006
.10.1115/1.4036440
17.
Steucke
,
K. E.
,
Win
,
Z.
,
Stemler
,
T. R.
,
Walsh
,
E. E.
,
Hall
,
J. L.
, and
Alford
,
P. W.
,
2017
, “
Empirically Determined Vascular Smooth Muscle Cell Mechano-Adaptation Law
,”
ASME J. Biomech. Eng.
,
139
(
7
), p. 071005.10.1115/1.4036454
18.
Vorp
,
D. A.
,
Tsamis
,
A.
, and
Krawiec
,
J. T.
,
2013
, “
Elastin and Collagen Fibre Microstructure of the Human Aorta in Ageing and Disease: A Review
,”
J. Royal Soc. Interface
, 10(83), pp.
1
22
.10.1098/rsif.2012.1004
19.
Collins
,
M. J.
,
Dev
,
V.
,
Strauss
,
B. H.
,
Fedak
,
P. W. M.
, and
Butany
,
J.
,
2008
, “
Variation in the Histopathological Features of Patients With Ascending Aortic Aneurysms: A Study of 111 Surgically Excised Cases
,”
J. Clin. Pathol.
,
61
(
4
), pp.
519
523
.10.1136/jcp.2006.046250
20.
Bellini
,
C.
,
Bersi
,
M. R.
,
Caulk
,
A. W.
,
Ferruzzi
,
J.
,
Milewicz
,
D. M.
,
Ramirez
,
F.
,
Rifkin
,
D. B.
,
Tellides
,
G.
,
Yanagisawa
,
H.
, and
Humphrey
,
J. D.
,
2017
, “
Comparison of 10 Murine Models Reveals a Distinct Biomechanical Phenotype in Thoracic Aortic Aneurysms
,”
J. R. Soc. Interface
,
14
(
130
), p.
20161036
.10.1098/rsif.2016.1036
21.
Fung
,
Y. C.
, and
Liu
,
S. Q.
,
1995
, “
Determination of the Mechanical Properties of the Different Layers of Blood Vessels In Vivo
,”
Proc. Natl. Acad. Sci. U. S. A.
,
92
(
6
), pp.
2169
2173
.10.1073/pnas.92.6.2169
22.
Fung
,
Y. C.
, and
Liu
,
S. Q.
, 1989, “
Change of Residual Strains in Arteries Due to Hypertrophy Caused by Aortic Constriction
,”
Circ. Res.
, 65(5), pp.
1340
1349
.10.1161/01.res.65.5.1340
23.
Liu
,
S. Q.
, and
Fung
,
Y. C.
,
1989
, “
Relationship Between Hypertension, Hypertrophy, and Opening Angle of Zero-Stress State of Arteries Following Aortic Constriction
,”
ASME J. Biomech. Eng.
,
111
(
4
), pp.
325
335
.10.1115/1.3168386
24.
Jackson
,
Z. S.
,
Gotlieb
,
A. I.
, and
Langille
,
B. L.
,
2002
, “
Wall Tissue Remodeling Regulates Longitudinal Tension in Arteries
,”
Circ. Res.
,
90
(
8
), pp.
918
925
.10.1161/01.RES.0000016481.87703.CC
25.
Matsumoto
,
T.
, and
Hayashi
,
K.
,
1996
, “
Stress and Strain Distribution in Hypertensive and Normotensive Rat Aorta Considering Residual Strain
,”
ASME J. Biomech. Eng.
,
118
(
1
), pp.
62
73
.10.1115/1.2795947
26.
Bendeck
,
M. P.
, and
Langille
,
B. L.
,
1991
, “
Rapid Accumulation of Elastin and Collagen in the Aortas of Sheep in the Immediate Perinatal Period
,”
Circ. Res.
,
69
(
4
), pp.
1165
1169
.10.1161/01.RES.69.4.1165
27.
Skalak
,
R.
,
Dasgupta
,
G.
,
Moss
,
M.
,
Otten
,
E.
,
Dullemeijer
,
P.
, and
Vilmann
,
H.
,
1982
, “
Analytical Description of Growth
,”
J. Theor. Biol.
,
94
(
3
), pp.
555
577
.10.1016/0022-5193(82)90301-0
28.
Rodriguez
,
E. K.
,
Hoger
,
A.
, and
McCulloch
,
A. D.
,
1994
, “
Stress-Dependent Finite Growth in Soft Elastic Tissues
,”
J. Biomech.
,
27
(
4
), pp.
455
467
.10.1016/0021-9290(94)90021-3
29.
Alford
,
P. W.
, and
Taber
,
L. A.
,
2008
, “
Computational Study of Growth and Remodelling in the Aortic Arch
,”
Comput. Methods Biomech. Biomed. Eng.
,
11
(
5
), pp.
525
538
.10.1080/10255840801930710
30.
Taber
,
L. A.
,
1998
, “
A Model for Aortic Growth Based on Fluid Shear and Fiber Stresses
,”
ASME J. Biomech. Eng.
,
120
(
3
), pp.
348
354
.10.1115/1.2798001
31.
Humphrey
,
J. D.
, and
Rajagopal
,
K. R.
,
2002
, “
A Constrained Mixture Model for Growth and Remodelling of Soft Tissues
,”
Math. Model. Methods Appl. Sci.
,
12
(
03
), pp.
407
430
.10.1142/S0218202502001714
32.
Ateshian
,
G. A.
, and
Humphrey
,
J. D.
,
2012
, “
Continuum Mixture Models of Biological Growth and Remodeling: Past Successes and Future Opportunities
,”
Annu. Rev. Biomed. Eng.
,
14
(
1
), pp.
97
111
.10.1146/annurev-bioeng-071910-124726
33.
Kuhl
,
E.
, and
Holzapfel
,
G. A.
,
2007
, “
A Continuum Model for Remodeling in Living Structures
,”
J. Mater. Sci.
,
42
(
21
), pp.
8811
8823
.10.1007/s10853-007-1917-y
34.
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/s10237-006-0049-7
35.
Picu
,
R. C.
,
2011
, “
Mechanics of Random Fiber Networks—A Review
,”
Soft Matter
,
7
(
15
), pp.
6768
6785
.10.1039/c1sm05022b
36.
Green
,
E. M.
,
Mansfield
,
J. C.
,
Bell
,
J. S.
, and
Winlove
,
C. P.
,
2014
, “
The Structure and Micromechanics of Elastic Tissue
,”
Interface Focus
,
4
(
2
), p.
20130058
.10.1098/rsfs.2013.0058
37.
Fornieri
,
C.
,
Quaglino
,
D.
, Jr
,., and
Mori
,
G.
,
1992
, “
Role of the Exracellular Matrix in Age-Related Modifications of the Rat Aorta
,”
Art. Thromb.
,
12
(
9
), pp.
1008
1016
.10.1161/01.ATV.12.9.1008
38.
Alford
,
P. W.
,
Humphrey
,
J. D.
, and
Taber
,
L. A.
,
2008
, “
Growth and Remodelling in a Thick-Walled Artery Model: Effects of Spatial Variations in Wall Constituents
,”
Biomech. Model. Mechanobiol.
,
7
(
4
), pp.
245
262
.10.1007/s10237-007-0101-2
39.
Freed
,
A. D.
, and
Doehring
,
T. C.
,
2005
, “
Elastic Model for Crimped Collagen Fibrils
,”
ASME J. Biomech. Eng.
,
127
(
4
), pp.
587
593
.10.1115/1.1934145
40.
Holmes
,
K. C.
,
Popp
,
D.
,
Gebhard
,
W.
, and
Kabsch
,
W.
,
1990
, “
Atomic Model of the Actin Filament
,”
Nature
,
347
(
6288
), pp.
44
49
.10.1038/347044a0
41.
Rachev
,
A.
, and
Hayashi
,
K.
,
1999
, “Theoretical Study of the Effects of Vascular Smooth Muscle Contraction on Strain and Stress Distributions in Arteries,”
Annals BME.
, 27, pp.
459
468
.10.1114/1.191
42.
Shen
,
Z. L.
,
Dodge
,
M. R.
,
Kahn
,
H.
,
Ballarini
,
R.
, and
Eppell
,
S. J.
,
2008
, “
Stress-Strain Experiments on Individual Collagen Fibrils
,”
Biophys. J.
,
95
(
8
), pp.
3956
3963
.10.1529/biophysj.107.124602
43.
Buehler
,
M. J.
,
2008
, “
Nanomechanics of Collagen Fibrils Under Varying Cross-Link Densities: Atomistic and Continuum Studies
,”
J. Mech. Behav. Biomed. Mater.
,
1
(
1
), pp.
59
67
.10.1016/j.jmbbm.2007.04.001
44.
Gosline
,
J.
,
Lillie
,
M.
,
Carrington
,
E.
,
Guerette
,
P.
,
Ortlepp
,
C.
, and
Savage
,
K.
,
2002
, “
Elastic Proteins: Biological Roles and Mechanical Properties
,”
Phil. Trans. R. Soc. Lond. B.
, 3(57). pp.
121
132
.10.1098/rstb.2001.1022
45.
Ateshian
,
G. A.
,
Rajan
,
V.
,
Chahine
,
N. O.
,
Canal
,
C. E.
, and
Hung
,
C. T.
,
2009
, “
Modeling the Matrix of Articular Cartilage Using a Continuous Fiber Angular Distribution Predicts Many Observed Phenomena
,”
ASME J. Biomech. Eng.
,
131
(
6
), p.
061003
.10.1115/1.3118773
46.
Nolan
,
D. R.
, and
McGarry
,
J. P.
,
2016
, “
On the Compressibility of Arterial Tissue
,”
Ann. Biomed. Eng.
,
44
(
4
), pp.
993
1007
.10.1007/s10439-015-1417-1
47.
Chandran
,
P. L.
, and
Barocas
,
V. H.
,
2006
, “
Affine Versus Non-Affine Fibril Kinematics in Collagen Networks: Theoretical Studies of Network Behavior
,”
ASME J. Biomech. Eng.
,
128
(
2
), pp.
259
270
.10.1115/1.2165699
48.
Stylianopoulos
,
T.
, and
Barocas
,
V. H.
,
2007
, “
Volume-Averaging Theory for the Study of the Mechanics of Collagen Networks
,”
Comput. Methods Appl. Mech. Eng.
,
196
(
31–32
), pp.
2981
2990
.10.1016/j.cma.2006.06.019
49.
Guennebaud
,
G.
, and
Jacob
,
B.
,
2010
, “
Eigen V3
,” Online, accessed Mar. 9, 2020, http://www.eigen.tuxfamily.org/
50.
Jia
,
Z.
, and
Nguyen
,
T. D.
,
2019
, “
A Micromechanical Model for the Growth of Collagenous Tissues Under Mechanics-Mediated Collagen Deposition and Degradation
,”
J. Mech. Behav. Biomed. Mater.
,
98
, pp.
96
107
.10.1016/j.jmbbm.2019.06.004
51.
Witzenburg
,
C. M.
,
Dhume
,
R. Y.
,
Shah
,
S. B.
,
Korenczuk
,
C. E.
,
Wagner
,
H. P.
,
Alford
,
P. W.
, and
Barocas
,
V. H.
,
2017
, “
Failure of the Porcine Ascending Aorta: Multidirectional Experiments and a Unifying Microstructural Model
,”
ASME J. Biomech. Eng.
,
139
(
3
), p.
031005
.10.1115/1.4035264
52.
Korenczuk
,
C. E.
,
Votava
,
L. E.
,
Dhume
,
R. Y.
,
Kizilski
,
S. B.
,
Brown
,
G. E.
,
Narain
,
R.
, and
Barocas
,
V. H.
,
2017
, “
Isotropic Failure Criteria Are Not Appropriate for Anisotropic Fibrous Biological Tissues
,”
ASME J. Biomech. Eng.
, 139(7), p. 071008.10.1115/1.4036316
53.
Sherifova
,
S.
, and
Holzapfel
,
G. A.
,
2019
, “
Biomechanics of Aortic Wall Failure With a Focus on Dissection and Aneurysm: A Review
,”
Acta Biomater.
,
99
, pp.
1
17
.10.1016/j.actbio.2019.08.017
54.
Tong
,
J.
,
Cheng
,
Y.
, and
Holzapfel
,
G. A.
,
2016
, “
Mechanical Assessment of Arterial Dissection in Health and Disease: Advancements and Challenges
,”
J. Biomech.
,
49
(
12
), pp.
2366
2373
.10.1016/j.jbiomech.2016.02.009
55.
Sommer
,
G.
,
Sherifova
,
S.
,
Oberwalder
,
P. J.
,
Dapunt
,
O. E.
,
Ursomanno
,
P. A.
,
DeAnda
,
A.
,
Griffith
,
B. E.
, and
Holzapfel
,
G. A.
,
2016
, “
Mechanical Strength of Aneurysmatic and Dissected Human Thoracic Aortas at Different Shear Loading Modes
,”
J. Biomech.
,
49
(
12
), pp.
2374
2382
.10.1016/j.jbiomech.2016.02.042
56.
Kim
,
J. H.
,
Avril
,
S.
,
Duprey
,
A.
, and
Favre
,
J. P.
,
2012
, “
Experimental Characterization of Rupture in Human Aortic Aneurysms Using a Full-Field Measurement Technique
,”
Biomech. Model. Mechanobiol.
,
11
(
6
), pp.
841
853
.10.1007/s10237-011-0356-5
57.
Vorp
,
D. A.
, and
Vande Geest
,
J. P.
,
2005
, “
Biomechanical Determinants of Abdominal Aortic Aneurysm Rupture
,”
Arterioscler. Thromb. Vasc. Biol.
,
25
(
8
), pp.
1558
1566
.10.1161/01.ATV.0000174129.77391.55
58.
Saleh
,
F. H.
, and
Jurjus
,
A. R.
,
2001
, “
A Comparative Study of Morphological Changes in Spontaneously Hypertensive Rats and Normotensive Wistar Kyoto Rats Treated With an Angiotensin‐Converting Enzyme Inhibitor or a Calcium‐Channel Blocker
,”
J. Pathol.
,
193
(
3
), pp.
415
420
.10.1002/1096-9896
59.
Benetos
,
A.
,
Lacolley
,
P.
, and
Safar
,
M. E.
,
1997
, “
Prevention of Aortic Fibrosis by Spironolactone in Spontaneously Hypertensive Rats
,”
Arterioscler. Thromb. Vasc. Biol.
,
17
(
6
), pp.
1152
1156
.10.1161/01.ATV.17.6.1152
60.
Koffi
,
I.
,
Lacolley
,
P.
,
Kirchengaast
,
M.
,
Pomiès
,
J. P.
,
Laurent
,
S.
, and
Benetos
,
A.
,
1998
, “
Prevention of Arterial Structural Alterations With Verapamil and Trandolapril and Consequences for Mechanical Properties in Spontaneously Hypertensive Rats
,”
Eur. J. Pharmacol.
,
361
(
1
), pp.
51
60
.10.1016/S0014-2999(98)00691-8
61.
Matsumoto
,
T.
, and
Hayashi
,
K.
,
1994
, “
Mechanical and Dimensional Adaptation of Rat Aorta to Hypertension
,”
ASME J. Biomech. Eng.
,
116
(
3
), pp.
278
283
.10.1115/1.2895731
62.
Bézie
,
Y.
,
Lamaziè
,
J.-M. D.
,
Laurent
,
S.
,
Challande
,
P.
,
Cunha
,
R. S.
,
Bonnet
,
J.
, and
Lacolley
,
P.
,
1998
, Fibronectin Expression and Aortic Wall Elastic Modulus in Spontaneously Hypertensive Rats,
Arterioscler. Thromb. Vasc. Biol.
, 18(7), pp.
1027
1034
.10.1161/01.atv.18.7.1027
63.
Karsaj
,
I.
, and
Humphrey
,
J. D.
,
2012
, “
A Multilayered Wall Model of Arterial Growth and Remodeling
,”
Mech. Mater.
,
44
, pp.
110
119
.10.1016/j.mechmat.2011.05.006
64.
Perrucci
,
G. L.
,
Rurali
,
E.
,
Gowran
,
A.
,
Pini
,
A.
,
Antona
,
C.
,
Chiesa
,
R.
,
Pompilio
,
G.
, and
Nigro
,
P.
,
2017
, “
Vascular Smooth Muscle Cells in Marfan Syndrome Aneurysm: The Broken Bricks in the Aortic Wall
,”
Cell. Mol. Life Sci.
,
74
(
2
), pp.
267
277
.10.1007/s00018-016-2324-9
65.
Guo
,
D. C.
,
Pannu
,
H.
,
Tran-Fadulu
,
V.
,
Papke
,
C. L.
,
Yu
,
R. K.
,
Avidan
,
N.
,
Bourgeois
,
S.
,
Estrera
,
A. L.
,
Safi
,
H. J.
,
Sparks
,
E.
,
Amor
,
D.
,
Ades
,
L.
,
McConnell
,
V.
,
Willoughby
,
C. E.
,
Abuelo
,
D.
,
Willing
,
M.
,
Lewis
,
R. A.
,
Kim
,
D. H.
,
Scherer
,
S.
,
Tung
,
P. P.
,
Ahn
,
C.
,
Buja
,
L. M.
,
Raman
,
C. S.
,
Shete
,
S. S.
, and
Milewicz
,
D. M.
,
2007
, “
Mutations in Smooth Muscle α-Actin (ACTA2) Lead to Thoracic Aortic Aneurysms and Dissections
,”
Nat. Genet.
,
39
(
12
), pp.
1488
1493
.10.1038/ng.2007.6
66.
Deogekar
,
S.
, and
Picu
,
R. C.
,
2018
, “
On the Strength of Random Fiber Networks
,”
J. Mech. Phys. Solids
,
116
, pp.
1
16
.10.1016/j.jmps.2018.03.026
67.
Lederle
,
F. A.
,
Wilson
,
S. E.
,
Johnson
,
G. R.
,
Reinke
,
D. B.
,
Littooy
,
F. N.
,
Acher
,
C. W.
,
Messina
,
L. M.
,
Ballard
,
D. J.
, and
Ansel
,
H. J.
,
1995
, “
Variability in Measurement of Abdominal Aortic Aneurysms
,”
J. Vasc. Surg.
, 21(6), pp.
945
952
.10.1016/s0741-5214(95)70222-9
68.
Wilmink
,
A. B. M.
,
Forshaw
,
M.
,
Quick
,
C. R. G.
,
Hubbard
,
C. S.
, and
Day
,
N. E.
,
2002
, “
Accuracy of Serial Screening for Abdominal Aortic Aneurysms by Ultrasound
,”
J. Med. Screen.
,
9
(
3
), pp.
125
127
.10.1136/jms.9.3.125
69.
Nardi
,
P.
, and
Ruvolo
,
G.
,
2016
, “
Current Indications to Surgical Repair of the Aneurysms of Ascending Aorta
,”
J. Vasc. Endovasc. Surg.
,
1
(
2
).10.21767/2573-4482.100009
70.
Hayashi
,
K.
, and
Sugimoto
,
T.
,
2007
, “
Biomechanical Response of Arterial Wall to DOCA-Salt Hypertension in Growing and Middle-Aged Rats
,”
J. Biomech.
,
40
(
7
), pp.
1583
1593
.10.1016/j.jbiomech.2006.07.021
71.
Van Gorp
,
A. W.
,
Van Ingen Schenau
,
D. S.
,
Hoeks
,
A. P. G.
,
Struijker Boudier
,
H. A. J.
,
Reneman
,
R. S.
, and
De Mey
,
J. G. R.
,
1995
, “
Aortic Wall Properties in Normotensive and Hypertensive Rats of Various Ages In Vivo
,”
Hypertension
,
26
(
2
), pp.
363
368
.10.1161/01.HYP.26.2.363
72.
Marque
,
V.
,
Kieffer
,
P.
,
Atkinson
,
J.
, and
Lartaud-Idjouadiene
,
I.
,
1999
, “
Elastic Properties and Composition of the Aortic Wall in Old Spontaneously Hypertensive Rats
,”
Hypertension
,
34
(
3
), pp.
415
422
.10.1161/01.HYP.34.3.415
73.
Hayashi
,
K.
, and
Shimizu
,
E.
,
2016
, “
Composition of Connective Tissues and Morphometry of Vascular Smooth Muscle in Arterial Wall of DOCA-Salt Hypertensive Rats—In Relation With Arterial Remodeling
,”
J. Biomech.
,
49
(
7
), pp.
1225
1229
.10.1016/j.jbiomech.2016.02.044
74.
Seidel
,
C. L.
,
1979
, “
Aortic Actomyosin Content of Maturing Normal and Spontaneously Hypertensive Rats
,”
Am. J. Physiol. Hear. Circ. Physiol.
,
6
(
1
), pp. H34–H39.10.1152/ajpheart.1979.237.1.H34
75.
Kochova
,
P.
,
Tonar
,
Z.
,
Matejka
,
V. M.
,
Sviglerova
,
J.
,
Stengl
,
M.
, and
Kuncova
,
J.
,
2008
, “
Morphology and Mechanical Properties of the Subrenal Aorta in Normotensive and Hypertensive Rats
,”
Biomed. Pap. Med. Fac. Univ. Palacky Olomouc. Czech Repub.
,
152
(
2
), pp.
239
245
.10.5507/bp.2008.037
76.
Sommer
,
G.
,
Gasser
,
T. C.
,
Regitnig
,
P.
,
Auer
,
M.
, and
Holzapfel
,
G. A.
,
2008
, “
Dissection Properties of the Human Aortic Media: An Experimental Study
,”
ASME J. Biomech. Eng.
,
130
(
2
), p. 021007.10.1115/1.2898733
77.
Kobs
,
R. W.
,
Muvarak
,
N. E.
,
Eickhoff
,
J. C.
, and
Chesler
,
N. C.
,
2005
, “
Linked Mechanical and Biological Aspects of Remodeling in Mouse Pulmonary Arteries With Hypoxia-Induced Hypertension
,”
Am. J. Physiol. Hear. Circ. Physiol.
,
288
, pp.
1209
1217
.10.1152/ajpheart.01129.2003
78.
Golob
,
M. J.
,
Tabima
,
D. M.
,
Wolf
,
G. D.
,
Johnston
,
J. L.
,
Forouzan
,
O.
,
Mulchrone
,
A. M.
,
Kellihan
,
H. B.
,
Bates
,
M. L.
, and
Chesler
,
N. C.
,
2017
, “
Pulmonary Arterial Strain-and Remodeling-Induced Stiffening Are Differentiated in a Chronic Model of Pulmonary Hypertension
,”
J. Biomech.
, 55, pp.
92
98
.10.1016/j.jbiomech.2017.02.003
79.
Thompson
,
R. W.
,
Curci
,
J. A.
,
Ennis
,
T. L.
,
Mao
,
D.
,
Pagano
,
M. B.
, and
Pham
,
C. T.
,
2006
, “
Pathophysiology of Abdominal Aortic Aneurysms: Insights From the Elastase-Induced Model in Mice With Different Genetic Backgrounds
,”
Ann. N. Y. Acad. Sci.
,
1085
(
1
), pp.
59
73
.10.1196/annals.1383.029
80.
Le
,
V. P.
,
Knutsen
,
R. H.
,
Mecham
,
R. P.
, and
Wagenseil
,
J. E.
,
2011
, “
Decreased Aortic Diameter and Compliance Precedes Blood Pressure Increases in Postnatal Development of Elastin-Insufficient Mice
,”
Am. J. Physiol. Hear. Circ. Physiol.
,
301
(
1
), pp.
H221
H229
.10.1152/ajpheart.00119.2011
81.
Bellini
,
C.
,
Bersi
,
M. R.
,
Caulk
,
A. W.
,
Ferruzzi
,
J.
,
Milewicz
,
D. M.
,
Ramirez
,
F.
,
Rifkin
,
D. B.
,
Tellides
,
G.
,
Yanagisawa
,
H.
, and
Humphrey
,
J. D.
,
2017
, “
Comparison of 10 Murine Models Reveals a Distinct Biomechanical Phenotype in Thoracic Aortic Aneurysms - Supplemental Material
,”
J. R. Soc. Interface
,
14
(
130
), p.
20161036
.
You do not currently have access to this content.