A tissue's microstructure determines its failure properties at larger length scales, however, the specific relationship between microstructure and macroscopic failure in native and engineered soft tissues (such as capsular ligaments, aortic aneurysms, or vascular grafts) has proven elusive. In this study, variations in the microscale fiber alignment in collagen gel tissue analogs were modeled in order to understand their effects on macroscale damage and failure outcomes. The study employed a multiscale finite-element (FE) model for damage and failure in collagen-based materials. The model relied on microstructural representative volume elements (RVEs) that consisted of stochastically-generated networks of discrete type-I collagen fibers. Fiber alignment was varied within RVEs and between layers of RVEs in a macroscopic FE model of a notched dogbone geometry. The macroscale stretch and the microscale response of fibers for each of the differently aligned cases were compared as the dogbone was uniaxially extended to failure. Networks with greater fiber alignment parallel to the direction of extension failed at smaller strains (with a 6–22% reduction in the Green strain at failure), however, at greater grip forces (a 28–60% increase) than networks with fibers aligned perpendicular to the extension. Alternating layers of crisscrossed network alignments (aligned ±45 deg to the direction of extension) failed at smaller strains but at greater grip forces than those created using one fiber alignment type. In summary, variations in microscale structure via fiber alignment produced different macroscale failure trends. To conclude, these findings may be significant in the realm of tissue engineering and in soft tissue biomechanics.

References

1.
Anssari-Benam
,
A.
,
Gupta
,
H. S.
, and
Screen
,
H. R.
,
2012
, “
Strain Transfer Through the Aortic Valve
,”
ASME J. Biomech. Eng.
,
134
(
6
), p.
061003
.10.1115/1.4006812
2.
Quinn
,
K. P.
, and
Winkelstein
,
B. A.
,
2011
, “
Detection of Altered Collagen Fiber Alignment in the Cervical Facet Capsule After Whiplash-Like Joint Retraction
,”
Ann. Biomed. Eng.
,
39
(
8
), pp.
2163
2173
.10.1007/s10439-011-0316-3
3.
Keyes
,
J. T.
,
Haskett
,
D. G.
,
Utzinger
,
U.
,
Azhar
,
M.
, and
Van de Geest
,
J. P.
,
2011
, “
Adaptation of a Planar Microbiaxial Optomechanical Device for the Tubular Biaxial Microstructural and Macroscopic Characterization of Small Vascular Tissues
,”
ASME J. Biomech. Eng.
,
133
(
7
), p.
075001
.10.1115/1.4004495
4.
Ritter
,
M. C.
,
Jesudason
,
R.
,
Majumdar
,
A.
,
Stamenović
,
D.
,
Buczek-Thomas
,
J. A.
,
Stone
,
P. J.
,
Nugent
,
M. A.
, and
Suki
,
B.
,
2009
, “
A Zipper Network Model of the Failure Mechanics of Extracellular Matrices
,”
Proc. Natl. Acad. Sci.
,
106
(
4
), pp.
1081
1086
.10.1073/pnas.0808414106
5.
Ayturk
,
U. M.
,
Gadomski
,
B.
,
Schuldt
,
D.
,
Patel
,
V.
, and
Puttlitz
,
C. M.
,
2012
, “
Modeling Degenerative Disk Disease in the Lumbar Spine: A Combined Experimental, Constitutive, and Computational Approach
,”
ASME J. Biomech. Eng.
,
134
(
10
), p.
101003
.10.1115/1.4007632
6.
Kao
,
P. H.
,
Lammers
,
S.
,
Tian
,
L.
,
Hunter
,
K.
,
Stenmark
,
K. R.
,
Shandas
,
R.
, and
Qi
,
H. J.
,
2011
, “
A Microstructurally-Driven Model for Pulmonary Artery Tissue
,”
ASME J. Biomech. Eng.
,
133
(
5
), p.
051002
.10.1115/1.4002698
7.
Hamed
,
E.
,
Jasiuk
,
I.
,
Yoo
,
A.
,
Lee
,
Y.
, and
Liszka
,
T.
,
2012
, “
Multi-Scale Modelling of Elastic Moduli of Trabecular Bone
,”
J. R. Soc., Interface
,
9
(
72
), pp.
1654
1673
.10.1098/rsif.2011.0814
8.
Hadi
,
M. F.
,
Sander
,
E. A.
,
Ruberti
,
J. W.
, and
Barocas
,
V. H.
,
2012
, “
Simulated Remodeling of Loaded Collagen Networks via Strain-Dependent Enzymatic Degradation and Constant-Rate Fiber Growth
,”
Mech. Mater.
,
44
, pp.
72
82
.10.1016/j.mechmat.2011.07.003
9.
Wang
,
C. W.
, and
Sastry
,
A. M.
,
2000
, “
Structure, Mechanics and Failure of Stochastic Fibrous Networks—Part II: Network Simulations and Application
,”
ASME J. Eng. Mater. Technol.
,
122
, pp.
460
469
.10.1115/1.1288768
10.
Zhang
,
B.
,
Yang
,
Z.
,
Wu
,
Y.
, and
Sun.
,
H.
,
2010
, “
Hierarchical Multiscale Modeling of Failure in Unidirectional Fiber-Reinforced Plastic Matrix Composite
,”
Mater. Des.
,
31
(
5
), pp.
2312
2318
.10.1016/j.matdes.2009.12.009
11.
Lee
,
D. J.
, and
Winkelstein
,
B. A.
,
2012
, “
The Failure Response of the Human Cervical Facet Capsular Ligament During Facet Joint Retraction
,”
J. Biomech.
,
45
(
14
), pp.
2325
2329
.10.1016/j.jbiomech.2012.07.015
12.
Raghavan
,
M. L.
,
Hanaoka
,
M. M.
,
Kratzberg
,
J. A.
,
Higuchi
,
M. D. L.
, and
Da Silva
,
E. S.
,
2011
, “
Biomechanical Failure Properties and Microstructural Content of Ruptured and Unruptured Abdominal Aortic Aneurysms
,”
J. Biomech.
,
44
(
13
), pp.
2501
2507
.10.1016/j.jbiomech.2011.06.004
13.
Volokh
,
K.
, and
Vorp
,
D.
,
2008
, “
A Model of Growth and Rupture of Abdominal Aortic Aneurysm
,”
J. Biomech.
,
41
(
5
), pp.
1015
1021
.10.1016/j.jbiomech.2007.12.014
14.
Drilling
,
S.
,
Gaumer
,
J.
, and
Lannutti
,
J.
,
2009
, “
Fabrication of Burst Pressure Competent Vascular Grafts via Electrospinning: Effects of Microstructure
,”
J. Biomed. Mater. Res. Part A
,
88
(
4
), pp.
923
934
.10.1002/jbm.a.31926
15.
Hang
,
F.
, and
Barber
,
A. H.
,
2011
, “
Nano-Mechanical Properties of Individual Mineralized Collagen Fibrils From Bone Tissue
,”
J. R. Soc., Interface
,
8
(
57
), pp.
500
505
.10.1098/rsif.2010.0413
16.
Ito
,
S.
,
Ingenito
,
E. P.
,
Brewer
,
K. K.
,
Black
,
L. D.
,
Parameswaran
,
H.
,
Lutchen
,
K. R.
, and
Suki
,
B.
,
2005
, “
Mechanics, Nonlinearity, and Failure Strength of Lung Tissue in a Mouse Model of Emphysema: Possible Role of Collagen Remodeling
,”
J. Appl. Physiol.
,
98
(
2
), pp.
503
511
.10.1152/japplphysiol.00590.2004
17.
D'Amore
,
A.
,
Stella
,
J. A.
,
Wagner
,
W. R.
, and
Sacks
,
M. S.
,
2010
, “
Characterization of the Complete Fiber Network Topology of Planar Fibrous Tissues and Scaffolds
,”
Biomaterials
,
31
(
20
), pp.
5345
5354
.10.1016/j.biomaterials.2010.03.052
18.
Christian Gasser
,
T.
,
2011
, “
An Irreversible Constitutive Model for Fibrous Soft Biological Tissue: A 3-D Microfiber Approach With Demonstrative Application to Abdominal Aortic Aneurysms
,”
Acta Biomater.
,
7
(
6
), pp.
2457
2466
.10.1016/j.actbio.2011.02.015
19.
Nerurkar
,
N. L.
,
Elliott
,
D. M.
, and
Mauck
,
R. L.
,
2010
, “
Mechanical Design Criteria for Intervertebral Disc Tissue Engineering
,”
J. Biomech.
,
43
(
6
), pp.
1017
1030
.10.1016/j.jbiomech.2009.12.001
20.
Hadi
,
M. F.
,
Sander
,
E. A.
, and
Barocas
,
V. H.
,
2012
, “
Multiscale Model Predicts Tissue-Level Failure From Collagen Fiber-Level Damage
,”
ASME J. Biomech. Eng.
,
134
(
9
), p.
091005
.10.1115/1.4007097
21.
Chandran
,
P. L.
, and
Barocas
,
V. H.
,
2007
, “
Deterministic Material-Based Averaging Theory Model of Collagen Gel Micromechanics
,”
ASME J. Biomech. Eng.
,
129
(
2
), pp.
137
147
.10.1115/1.2472369
22.
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
23.
Barber
,
C. B.
,
Dobkin
,
D. P.
, and
Huhdanpaa
,
H.
,
1996
, “
The Quickhull Algorithm for Convex Hulls
,”
ACM Trans. Math. Softw.
,
22
(
4
), pp.
469
483
.10.1145/235815.235821
24.
Billiar
,
K. L.
, and
Sacks
,
M. S.
,
2000
, “
Biaxial Mechanical Properties of the Native and Glutaraldehyde-Treated Aortic Valve Cusp—Part II: A Structural Constitutive Model
,”
ASME J. Biomech. Eng.
,
122
(
4
), p.
327
.10.1115/1.1287158
25.
Sander
,
E. A.
,
Stylianopoulos
,
T.
,
Tranquillo
,
R. T.
, and
Barocas
,
V. H.
,
2009
, “
Image-Based Multiscale Modeling Predicts Tissue-Level and Network-Level Fiber Reorganization in Stretched Cell-Compacted Collagen Gels
,”
Proc. Natl. Acad. Sci.
,
106
(
42
), pp.
17675
17680
.10.1073/pnas.0903716106
26.
Lai
,
V. K.
,
Lake
,
S. P.
,
Frey
,
C. R.
,
Tranquillo
,
R. T.
, and
Barocas
,
V. H.
,
2012
, “
Mechanical Behavior of Collagen-Fibrin Co-Gels Reflects Transition From Series to Parallel Interactions With Increasing Collagen Content
,”
ASME J. Biomech. Eng.
,
134
(
1
), p.
011004
.10.1115/1.4005544
27.
Lake
,
S. P.
,
Hadi
,
M. F.
,
Lai
,
V. K.
, and
Barocas
,
V. H.
,
2012
, “
Mechanics of a Fiber Network Within a Non-Fibrillar Matrix: Model and Comparison With Collagen-Agarose Co-Gels
,”
Ann. Biomed. Eng.
,
40
(
10
), pp.
2111
2121
.10.1007/s10439-012-0584-6
28.
Sander
,
E. A.
, and
Barocas
,
V. H.
,
2009
, “
Comparison of 2D Fiber Network Orientation Measurement Methods
,”
J. Biomed. Mater. Res. Part A
,
88
(
2
), pp.
322
331
.10.1002/jbm.a.31847
29.
Sander
,
E. A.
,
Stylianopoulos
,
T.
,
Tranquillo
,
R. T.
, and
Barocas
,
V. H.
,
2009
, “
Image-Based Biomechanics of Collagen-Based Tissue Equivalents: Multiscale Models Compared to Fiber Alignment Predicted by Polarimetric Imaging
,”
IEEE Eng. Med. Biol. Mag.
,
28
(
3
), pp.
10
18
.10.1109/MEMB.2009.932486
30.
Nerurkar
,
N. L.
,
Baker
,
B. M.
,
Sen
,
S.
,
Wible
,
E. E.
,
Elliott
,
D. M.
, and
Mauck
,
R. L.
,
2009
, “
Nanofibrous Biologic Laminates Replicate the Form and Function of the Annulus Fibrosus
,”
Nature Mater.
,
8
(
12
), pp.
986
992
.10.1038/nmat2558
31.
Nerurkar
,
N. L.
,
Elliott
,
D. M.
, and
Mauck
,
R. L.
,
2007
, “
Mechanics of Oriented Electrospun Nanofibrous Scaffolds for Annulus Fibrosus Tissue Engineering
,”
J. Orthop. Res.
,
25
(
8
), pp.
1018
1028
.10.1002/jor.20384
32.
Lake
,
S. P.
,
Miller
,
K. S.
,
Elliott
,
D. M.
, and
Soslowsky
,
L. J.
,
2009
, “
Effect of Fiber Distribution and Realignment on the Nonlinear and Inhomogeneous Mechanical Properties of Human Supraspinatus Tendon Under Longitudinal Tensile Loading
,”
J. Orthop. Res.
,
27
(
12
), pp.
1596
1602
.10.1002/jor.20938
33.
Cummings
,
C. L.
,
Gawlitta
,
D.
,
Nerem
,
R. M.
, and
Stegemann
,
J. P.
,
2004
, “
Properties of Engineered Vascular Constructs Made From Collagen, Fibrin, and Collagen–Fibrin Mixtures
,”
Biomaterials
,
25
(
17
), pp.
3699
3706
.10.1016/j.biomaterials.2003.10.073
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