Abstract

This paper is concerned with proposing a suitable structurally motivated strain energy function, denoted by Weelastinnetwork, for modeling the deformation of the elastin network within the aortic valve (AV) tissue. The AV elastin network is the main noncollagenous load-bearing component of the valve matrix, and therefore, in the context of continuum-based modeling of the AV, the Weelastinnetwork strain energy function would essentially serve to model the contribution of the “isotropic matrix.” To date, such a function has mainly been considered as either a generic neo-Hookean term or a general exponential function. In this paper, we take advantage of the established structural analogy between the network of elastin chains and the freely jointed molecular chain networks to customize a structurally motivated Weelastinnetwork function on this basis. The ensuing stress–strain (force-stretch) relationships are thus derived and fitted to the experimental data points reported by (Vesely, 1998, “The Role of Elastin in Aortic Valve Mechanics,” J. Biomech., 31, pp. 115–123) for intact AV elastin network specimens under uniaxial tension. The fitting results are then compared with those of the neo-Hookean and the general exponential models, as the frequently used models in the literature, as well as the “Arruda–Boyce” model as the gold standard of the network chain models. It is shown that our proposed Weelastinnetwork function, together with the general exponential and the Arruda–Boyce models provide excellent fits to the data, with R2 values in excess of 0.98, while the neo-Hookean function is entirely inadequate for modeling the AV elastin network. However, the general exponential function may not be amenable to rigorous interpretation, as there is no structural meaning attached to the model. It is also shown that the parameters estimated by the Arruda–Boyce model are not mathematically and structurally valid, despite providing very good fits. We thus conclude that our proposed strain energy function Weelastinnetwork is the preferred choice for modeling the behavior of the AV elastin network and thereby the isotropic matrix. This function may therefore be superimposed onto that of the anisotropic collagen fibers family in order to develop a structurally motivated continuum-based model for the AV.

References

1.
Holzapfel
,
G. A.
,
Gasser
,
T. C.
, and
Ogden
,
R. W.
,
2000
, “
A New Constitutive Framework for Arterial Wall Mechanics and a Comparative Study of Material Models
,”
J. Elasticity
,
61
(1–3), pp.
1
48
.
2.
Anssari-Benam
,
A.
,
Bucchi
,
A.
,
Screen
,
H. R. C.
, and
Evans
,
S. L.
,
2017
, “
A Transverse Isotropic Viscoelastic Constitutive Model for the Aortic Valve Tissue
,”
R. Soc. Open Sci.
,
4
(
1
), p.
160585
.
3.
Freed
,
A. D.
,
Einstein
,
D. R.
, and
Vesely
,
I.
,
2005
, “
Invariant Formulation for Dispersed Transverse Isotropy in Aortic Heart Valves: An Efficient Means for Modeling Fiber Splay
,”
Biomech. Model. Mechanobiol.
,
4
(2–3), pp.
100
117
.
4.
Gasser
,
T. C.
,
Ogden
,
R. W.
, and
Holzapfel
,
G. A.
,
2006
, “
Hyperelastic Modelling of Arterial Layers With Distributed Collagen Fibre Orientation
,”
J. R. Soc. Interface
,
3
(
6
), pp.
15
35
.
5.
Holzapfel
,
G. A.
, and
Ogden
,
R. W.
,
2010
, “
Constitutive Modelling of Arteries
,”
Proc. R. Soc. A
,
466
(
2118
), pp.
1551
1597
.
6.
Holzapfel
,
G. A.
,
Niestrawska
,
J. A.
,
Ogden
,
R. W.
,
Reinisch
,
A. J.
, and
Schriefl
,
A. J.
,
2015
, “
Modelling Non-Symmetric Collagen Fibre Dispersion in Arterial Walls
,”
J. R. Soc. Interface
,
12
(
106
), p.
20150188
.
7.
Humphrey
,
J. D.
,
2003
, “
Review Paper: Continuum Biomechanics of Soft Biological Tissues
,”
Proc. R. Soc. A
,
459
(
2029
), pp.
3
46
.
8.
Holzapfel
,
G. A.
,
2006
, “
Determination of Material Models for Arterial Walls From Uniaxial Extension Tests and Histological Structure
,”
J. Theor. Biol.
,
238
(
2
), pp.
290
302
.
9.
Anssari-Benam
,
A.
,
Bader
,
D. L.
, and
Screen
,
H. R. C.
,
2011
, “
A Combined Experimental and Modelling Approach to Aortic Valve Viscoelasticity in Tensile Deformation
,”
J. Mater. Sci. Mater. Med.
,
22
(
2
), pp.
253
262
.
10.
Anssari-Benam
,
A.
,
Barber
,
A. H.
, and
Bucchi
,
A.
,
2016
, “
Evaluation of Bioprosthetic Heart Valve Failure Using a Matrix-Fibril Shear Stress Transfer Approach
,”
J. Mater. Sci. Mater. Med.
,
27
(
2
), p.
42
.
11.
Vesely
,
I.
,
1997
, “
The Role of Elastin in Aortic Valve Mechanics
,”
J. Biomech.
,
31
(2), pp.
115
123
.
12.
Weinberg
,
E. J.
, and
Kaazempur-Mofrad
,
M. R.
,
2005
, “
On the Constitutive Models for Heart Valve Leaflet Mechanics
,”
Cardiovasc. Eng.
,
5
(
1
), pp.
37
43
.
13.
Weinberg
,
E. J.
, and
Kaazempur Mofrad
,
M. R.
,
2007
, “
Transient, Three-Dimensional, Multiscale Simulations of the Human Aortic Valve
,”
Cardiovasc. Eng.
,
7
(
4
), pp.
140
155
.
14.
Weinberg
,
E. J.
,
Shahmirzadi
,
D.
, and
Kaazempur Mofrad
,
M. R.
,
2010
, “
On the Multiscale Modeling of Heart Valve Biomechanics in Health and Disease
,”
Biomech. Model. Mechanobiol.
,
9
(
4
), pp.
373
387
.
15.
Bischoff
,
J. E.
,
Arruda
,
E. M.
, and
Grosh
,
K.
,
2002
, “
Orthotropic Hyperelasticity in Terms of an Arbitrary Molecular Chain Model
,”
J. Appl. Mech.
,
69
(
2
), pp.
198
201
.
16.
Kuhl
,
E.
,
Garikipati
,
K.
,
Arruda
,
E. M.
, and
Grosh
,
K.
,
2005
, “
Remodeling of Biological Tissue: Mechanically Induced Reorientation of a Transversely Isotropic Chain Network
,”
J. Mech. Phys. Solids
,
53
(
7
), pp.
1552
1573
.
17.
Zhang
,
Y.
,
Dunn
,
M. L.
,
Drexler
,
E. S.
,
McCowan
,
C. N.
,
Slifka
,
A. J.
,
Ivy
,
D. D.
, and
Shandas
,
R.
,
2005
, “
A Microstructural Hyperelastic Model of Pulmonary Arteries Under Normo- and Hypertensive Conditions
,”
Ann. Biomed. Eng.
,
33
(
8
), pp.
1042
1052
.
18.
Arruda
,
E. M.
, and
Boyce
,
M. C.
,
1993
, “
A Three-Dimensional Constitutive Model for the Large Stretch Behavior of Rubber Elastic Materials
,”
J. Mech. Phys. Solids
,
41
(
2
), pp.
389
412
.
19.
Lewinsohn
,
A. D.
,
Anssari-Benham
,
A.
,
Lee
,
D. A.
,
Taylor
,
P. M.
,
Chester
,
A. H.
,
Yacoub
,
M. H.
, and
Screen
,
H. R. C.
,
2011
, “
Anisotropic Strain Transfer Through the Aortic Valve and Its Relevance to the Cellular Mechanical Environment
,”
Proc. Inst. Mech. Eng. H
,
225
(
8
), pp.
821
830
.
20.
Rock
,
C. A.
,
Han
,
L.
, and
Doehring
,
T. C.
,
2014
, “
Complex Collagen Fiber and Membrane Morphologies of the Whole Porcine Aortic Valve
,”
PLoS One
,
9
(
1
), p.
e86087
.
21.
Elias-Zuniga
,
A.
, and
Beatty
,
M. F.
,
2002
, “
Constitutive Equations for Amended Non-Gaussian Network Models of Rubber Elasticity
,”
Int. J. Eng. Sci.
,
40
(
20
), pp.
2265
2294
.
22.
Scott
,
M.
, and
Vesely
,
I.
,
1995
, “
Aortic Valve Cusps Microstructure: The Role of Elastin
,”
Ann. Thorac. Surg.
,
60
(
2
), pp.
S391
S394
.
23.
Tseng
,
H.
, and
Grande-Allen
,
K. J.
,
2011
, “
Elastic Fibers in the Aortic Valve Spongiosa: A Fresh Perspective on its Structure and Role in Overall Tissue Function
,”
Acta Biomater.
,
7
(
5
), pp.
2101
2108
.
24.
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
.
25.
James
,
H. M.
, and
Guth
,
E.
,
1943
, “
Theory of the Elastic Properties of Rubber
,”
J. Chem. Phys.
,
11
(
10
), pp.
455
481
.
26.
Treloar
,
L. R. G.
,
1954
, “
The Photoelastic Properties of Short-Chain Molecular Networks
,”
Trans. Faraday Soc.
,
50
, pp.
881
896
.
27.
Anssari-Benam
,
A.
,
Viola
,
G.
, and
Korakianitis
,
T.
,
2010
, “
Thermodynamic Effects of Linear Dissipative Small Deformations
,”
J. Therm. Anal. Calorim.
,
100
(
3
), pp.
941
947
.
28.
Beatty
,
M. F.
,
2003
, “
An Average-Stretch Full-Network Model for Rubber Elasticity
,”
J. Elasticity
,
70
(1–3), pp.
65
86
.
29.
Miehe
,
C.
,
Göktepe
,
S.
, and
Lulei
,
F.
,
2004
, “
A Micro-Macro Approach to Rubber-Like Materials—Part I: The Non-Affine Micro-Sphere Model of Rubber Elasticity
,”
J. Mech. Phys. Solids
,
52
(
11
), pp.
2617
2660
.
30.
Boyce
,
M. C.
, and
Arruda
,
E. M.
,
2000
, “
Constitutive Models of Rubber Elasticity: A Review
,”
Rubber Chem. Technol.
,
73
(
3
), pp.
504
523
.
31.
Anssari-Benam
,
A.
,
Gupta
,
H. S.
, and
Screen
,
H. R. C.
,
2012
, “
Strain Transfer Through the Aortic Valve
,”
ASME J. Biomech. Eng.
,
134
(
6
), p.
061003
.
32.
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
.
33.
Jayyosi
,
C.
,
Affagard
,
J. S.
,
Ducourthial
,
G.
,
Bonod-Bidaud
,
C.
,
Lynch
,
B.
,
Bancelin
,
S.
,
Ruggiero
,
F.
,
Schanne-Klein
,
M. C.
,
Allain
,
J. M.
,
Bruyère-Garnier
,
K.
, and
Coret
,
M.
,
2017
, “
Affine Kinematics in Planar Fibrous Connective Tissues: An Experimental Investigation
,”
Biomech. Model Mechanobiol.
,
16
(
4
), pp.
1459
1473
.
34.
Cohen
,
A.
,
1991
, “
A Padé Approximant to the Inverse Langevin Function
,”
Rheol. Acta
,
30
(
3
), pp.
270
273
.
35.
Billiar
,
K. L.
, and
Sacks
,
M. S.
,
2000
, “
Biaxial Mechanical Properties of the Natural and Glutaraldehyde Treated Aortic Valve Cusp—Part II: A Structural Constitutive Model
,”
ASME J. Biomech. Eng.
,
122
(
4
), pp.
327
335
.
36.
Zou
,
Y.
, and
Zhang
,
Y.
,
2009
, “
An Experimental and Theoretical Study on the Anisotropy of Elastin Network
,”
Ann. Biomed. Eng.
,
37
(
8
), pp.
1572
1583
.
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