The objective of this study was to develop a nonlinear and anisotropic three-dimensional mathematical model of tendon behavior in which the structural components of fibers, matrix, and fiber-matrix interactions are explicitly incorporated and to use this model to infer the contributions of these structures to tendon mechanical behavior. We hypothesized that this model would show that: (i) tendon mechanical behavior is not solely governed by the isotropic matrix and fiber stretch, but is also influenced by fiber-matrix interactions; and (ii) shear fiber-matrix interaction terms will better describe tendon mechanical behavior than bulk fiber-matrix interaction terms. Model versions that did and did not include fiber-matrix interaction terms were applied to experimental tendon stress-strain data in longitudinal and transverse orientations, and the R2 goodness-of-fit was evaluated. This study showed that models that included fiber-matrix interaction terms improved the fit to longitudinal data (RToe2=0.88,RLin2=0.94) over models that only included isotropic matrix and fiber stretch terms (RToe2=0.36,RLin2=0.84). Shear fiber-matrix interaction terms proved to be responsible for the best fit to data and to contribute to stress-strain nonlinearity. The mathematical model of tendon behavior developed in this study showed that fiber-matrix interactions are an important contributor to tendon behavior. The more complete characterization of mechanical behavior afforded by this mathematical model can lead to an improved understanding of structure-function relationships in soft tissues and, ultimately, to the development of tissue-engineered therapies for injury or degeneration.

1.
Fung
,
Y. C.
, 1967, “
Elasticity of Soft Tissues in Simple Elongation
,”
Am. J. Physiol.
0002-9513,
213
(
6
), pp.
1532
1544
.
2.
Fung
,
Y. C.
, 1972,
Biomechanics: Its Foundations and Objectives
,
Y. C.
Fung
,
M.
Anliker
, and
N.
Perrone
eds.,
Prentice-Hall
, Englewood Cliffs, NJ.
3.
Decraemer
,
W. F.
,
Maes
,
M. A.
, and
Vanhuyse
,
V. J.
, 1980, “
An Elastic Stress-Strain Relation for Soft Biological Tissues Based on a Structural Model
,”
J. Biomech.
0021-9290,
13
(
6
), pp.
463
468
.
4.
Hurschler
,
C.
,
Loitz-Ramage
,
B.
, and
Vanderby
,
R.
, Jr.
, 1997, “
A Structurally Based Stress-Stretch Relationship for Tendon and Ligament
,”
ASME J. Biomech. Eng.
0148-0731,
119
(
4
), pp.
392
399
.
5.
Hurschler
,
C.
,
Provenzano
,
P. P.
, and
Vanderby
,
R.
, 2003, “
Application of a Probabilistic Microstructural Model to Determine Reference Length and Toe-to-Linear Region Transition in Fibrous Connective Tissue
,”
ASME J. Biomech. Eng.
0148-0731,
125
, pp.
415
422
.
6.
Kastelic
,
J.
,
Pally
,
I.
, and
Baer
,
E.
, 1980, “
A Structural Mechanical Model for Tendon Crimping
,”
J. Biomech.
0021-9290,
13
, pp.
887
893
.
7.
Kwan
,
M. K.
, and
Woo
,
S. L.
, 1989, “
A Structural Model to Describe the Nonlinear Stress-Strain Behavior for Parallel-Fibered Collagenous Tissues
,”
ASME J. Biomech. Eng.
0148-0731,
111
(
4
), pp.
361
363
.
8.
Lanir
,
Y.
, 1979, “
A Structural Theory for the Homogeneous Biaxial Stress-Strain Relationships in Flat Collagenous Tissues
,”
J. Biomech.
0021-9290,
12
(
6
), pp.
423
436
.
9.
Elliott
,
D. M.
, and
Setton
,
L. A.
, 2000, “
A Linear Material Model for Fiber-Induced Anisotropy of the Anulus Fibrosus
,”
ASME J. Biomech. Eng.
0148-0731,
122
(
2
), pp.
173
179
.
10.
Elliott
,
D. M.
, and
Setton
,
L. A.
, 2001, “
Anisotropic and Inhomogeneous Tensile Behavior of the Human Anulus Fibrosus: Experimental Measurement and Material Model Predictions
,”
ASME J. Biomech. Eng.
0148-0731,
123
(
3
), pp.
256
263
.
11.
Humphrey
,
J. D.
, and
Yin
,
F. C.
, 1987, “
A New Constitutive Formulation for Characterizing the Mechanical Behavior of Soft Tissues
,”
Biophys. J.
0006-3495,
52
(
4
), pp.
563
570
.
12.
Humphrey
,
J. D.
,
Strumpf
,
R. K.
, and
Yin
,
F. C.
, 1990, “
Determination of a Constitutive Relation for Passive Myocardium: I. A New Functional Form
,”
ASME J. Biomech. Eng.
0148-0731,
112
(
3
), pp.
333
339
.
13.
Klisch
,
S. M.
, and
Lotz
,
J. C.
, 1999, “
Application of a Fiber-Reinforced Continuum Theory to Multile Deformations of the Annulus Fibrosus
,”
Ibis
0019-1019,
32
, pp.
1027
1036
.
14.
Quapp
,
K. M.
, and
Weiss
,
J. A.
, 1998, “
Material Characterization of Human Medial Collateral Ligament
,”
J. Biomech.
0021-9290,
120
(
6
), pp.
757
763
.
15.
Bruehlmann
,
S. B.
,
Matyas
,
J. R.
, and
Duncan
,
N. A.
, 2004, “
Collagen fibril sliding at the cell boundary: novel insights into extracellular matrix mechanics in the rat tail tendon
,”
Trans. Annu. Meet. \M Orthop. Res. Soc.
0149-6433,
29
, pp.
44
.
16.
Weiss
,
J. A.
,
Gardiner
,
J. C.
, and
Bonifasi-Lista
,
C.
, 2002, “
Ligament Material Behavior Is Nonlinear, Viscoelastic and Rate-Independent Under Shear Loading
,”
J. Biomech.
0021-9290,
35
(
7
), pp.
943
950
.
17.
Spencer
,
A. J. M.
, 1984,
Constitutive Theory for Strongly Anisotropic Solids
, In
Continuum Theory of the Mechanics of Fibre-Reinforced Composites
,
A. J. M.
Spencer
ed.,
Springer-Verlag
, New York, pp.
1
32
.
18.
Lynch
,
H. A.
,
Johannessen
,
W.
,
Wu
,
J. P.
,
Jawa
,
A.
, and
Elliott
,
D. M.
, 2003, “
Effect of Fiber Orientation and Strain Rate on the Nonlinear Uniaxial Tensile Material Properties of Tendon
,”
ASME J. Biomech. Eng.
0148-0731,
125
(
5
), pp.
726
731
.
19.
Ott
,
R. L.
, 1993,
An Introduction to Statistical Methods and Data Analysis
,
Duxbury Press
, Belmont, CA.
20.
Beck
,
J. V.
, and
Arnold
,
K. J.
, 1977,
Parameter Estimation in Engineering and Science
,
Wiley
, New York.
21.
Sarver
,
J. J.
,
Robinson
,
P. S.
, and
Elliott
,
D. M.
, 2003, “
Methods for Quasi-Linear Viscoelastic Modeling of Soft Tissue: Application to Incremental Stress-Relaxation Experiments
,”
ASME J. Biomech. Eng.
0148-0731,
125
(
5
), pp.
754
758
.
22.
Yamamoto
,
E.
,
Hayashi
,
K.
, and
Yamamoto
,
N.
, 2000, “
Effects of Stress Shielding on the Transverse Mechanical Properties of Rabbit Patellar Tendons
,”
ASME J. Biomech. Eng.
0148-0731,
122
(
6
), pp.
608
614
.
23.
Davison
,
P. F.
, 1989, “
The Contribution of Labile Crosslinks to the Tensile Behavior of Tendons
,”
Connect. Tissue Res.
0300-8207,
18
(
4
), pp.
293
305
.
24.
Partington
,
F. R.
, and
Wood
,
G. C.
, 1963, “
The Role of Non-Collagen Components in the Mechanical Behaviour of Tendon Fibres
,”
Biochim. Biophys. Acta
0006-3002,
69
, pp.
485
495
.
25.
Lynch
,
H. A.
, and
Elliott
,
D. M.
, 2004, “
Fiber-Matrix Interactions in a 3-D Anisotropic Strain-Energy Model of Tendon
,”
Trans. Annu. Meet. \M Orthop. Res. Soc.
0149-6433,
29
, pp.
885
.
26.
Klisch
,
S. M.
, and
Lotz
,
J. C.
, 1999, “
Application of a Fiber-Reinforced Continuum Theory to Multiple Deformations of the Annulus Fibrosus
,”
J. Biomech.
0021-9290,
32
(
10
), pp.
1027
1036
.
27.
LeRoux
,
M. A.
, and
Setton
,
L. A.
, 2002, “
Experimental and Biphasic FEM Determinations of the Material Properties and Hydraulic Permeability of the Meniscus in Tension
,”
ASME J. Biomech. Eng.
0148-0731,
124
(
3
), pp.
315
321
.
28.
Acaroglu
,
E. R.
,
Iatridis
,
J. C.
,
Setton
,
L. A.
,
Foster
,
R. J.
,
Mow
,
V. C.
, and
Weidenbaum
,
M.
, 1995, “
Degeneration and Aging Affect the Tensile Behavior of Human Lumbar Anulus Fibrosus
,”
Spine
0362-2436,
20
(
24
), pp.
2690
2701
.
29.
Humphrey
,
J. D.
, and
Yin
,
F. C.
, 1987, “
On Constitutive Relations and Finite Deformations of Passive Cardiac Tissue: I. A Pseudostrain-Energy Function
,”
ASME J. Biomech. Eng.
0148-0731,
109
(
4
), pp.
298
304
.
You do not currently have access to this content.