Inelastic behaviors, such as softening, a progressive decrease in modulus before failure, occur in tendon and are important aspects in degeneration and tendinopathy. These inelastic behaviors are generally attributed to two potential mechanisms: plastic deformation and damage. However, it is not clear which is primarily responsible. In this study, we evaluated these potential mechanisms of tendon inelasticity by using a recently developed reactive inelasticity model (RIE), which is a structurally inspired continuum mechanics framework that models tissue inelasticity based on the molecular bond kinetics. Using RIE, we formulated two material models, one specific to plastic deformation and the other to damage. The models were independently fit to published macroscale experimental tensile tests of rat tail tendons. We quantified the inelastic effects and compared the performance of the two models in fitting the mechanical response during loading, relaxation, unloading, and reloading phases. Additionally, we validated the models by using the resulting fit parameters to predict an independent set of experimental stress–strain curves from ramp-to-failure tests. Overall, the models were both successful in fitting the experiments and predicting the validation data. However, the results did not strongly favor one mechanism over the other. As a result, to distinguish between plastic deformation and damage, different experimental protocols will be needed. Nevertheless, these findings suggest the potential of RIE as a comprehensive framework for studying tendon inelastic behaviors.

References

1.
Cook
,
J. L.
, and
Purdam
,
C. R.
,
2009
, “
Is Tendon Pathology a Continuum? A Pathology Model to Explain the Clinical Presentation of Load-Induced Tendinopathy
,”
Br. J. Sports Med.
,
43
(
6
), pp.
409
416
.
2.
Maganaris
,
C. N.
,
Chatzistergos
,
P.
,
Reeves
,
N. D.
, and
Narici
,
M. V.
,
2017
, “
Quantification of Internal Stress-Strain Fields in Human Tendon: Unraveling the Mechanisms That Underlie Regional Tendon Adaptations and Mal-Adaptations to Mechanical Loading and the Effectiveness of Therapeutic Eccentric Exercise
,”
8
, p.
91
.
3.
Diani
,
J.
,
Fayolle
,
B.
, and
Gilormini
,
P.
,
2009
, “
A Review on the Mullins Effect
,”
45
, pp.
601
612
.
4.
Maiti
,
A.
,
Small
,
W.
,
Gee
,
R. H.
,
Weisgraber
,
T. H.
,
Chinn
,
S. C.
,
Wilson
,
T. S.
, and
Maxwell
,
R. S.
,
2014
, “
Mullins Effect in a Filled Elastomer Under Uniaxial Tension
,”
Phys. Rev. E
,
89
(
1
), p.
012602
.
5.
Peloquin
,
J. M.
,
Santare
,
M. H.
, and
Elliott
,
D. M.
,
2016
, “
Advances in Quantification of Meniscus Tensile Mechanics Including Nonlinearity, Yield, and Failure
,”
ASME J. Biomech. Eng.
,
138
(
2
), p.
021002
.
6.
Provenzano
,
P. P.
,
Heisey
,
D.
,
Hayashi
,
K.
,
Lakes
,
R.
, and
Vanderby
,
R.
,
2002
, “
Subfailure Damage in Ligament: A Structural and Cellular Evaluation
,”
J. Appl. Physiol.
,
92
(
1
), pp.
362
371
.
7.
Legerlotz
,
K.
,
Riley
,
G. P.
, and
Screen
,
H. R.
,
2010
, “
Specimen Dimensions Influence the Measurement of Material Properties in Tendon Fascicles
,”
J. Biomech.
,
43
(
12
), pp.
2274
2280
.
8.
Safa
,
B. N.
,
Meadows
,
K. D.
,
Szczesny
,
S. E.
, and
Elliott
,
D. M.
,
2017
, “
Exposure to Buffer Solution Alters Tendon Hydration and Mechanics
,”
J. Biomech.
,
61
, pp.
18
25
.
9.
Alastrué
,
V.
,
Peña
,
E.
,
Martínez
,
M. A.
, and
Doblaré
,
M.
,
2008
, “
Experimental Study and Constitutive Modelling of the Passive Mechanical Properties of the Ovine Infrarenal Vena Cava Tissue
,”
J. Biomech.
,
41
(
14
), pp.
3038
3045
.
10.
Li
,
W.
,
2016
, “
Damage Models for Soft Tissues: A Survey
,”
J. Med. Biol. Eng.
,
36
(
3
), pp.
285
307
.
11.
Fleming
,
B. C.
,
Hulstyn
,
M. J.
,
Oksendahl
,
H. L.
, and
Fadale
,
P. D.
,
2005
, “
Ligament Injury, Reconstruction and Osteoarthritis
,”
Curr. Opin. Orthop.
,
16
, pp.
354
362
.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1948850/
12.
Cook
,
J. L.
,
Rio
,
E.
,
Purdam
,
C. R.
, and
Docking
,
S. I.
,
2016
, “
Revisiting the Continuum Model of Tendon Pathology: What Is Its Merit in Clinical Practice and Research?
,”
Br. J. Sports Med.
,
50
, pp.
354
362
.
13.
Abrahams
,
M.
,
1967
, “
Mechanical Behaviour of Tendon In Vitro—A Preliminary Report
,”
Med. Biol. Eng.
,
5
(
5
), pp.
433
443
.
14.
Sverdlik
,
A.
, and
Lanir
,
Y.
,
2002
, “
Time-Dependent Mechanical Behavior of Sheep Digital Tendons, Including the Effects of Preconditioning
,”
ASME J. Biomech. Eng.
,
124
(
1
), pp.
78
84
.
15.
Rigby
,
B. J.
,
1964
, “
Effect of Cyclic Extension on the Physical Properties of Tendon Collagen and Its Possible Relation to Biological Ageing of Collagen
,”
Nature
,
202
(
4937
), pp.
1072
1074
.
16.
Duenwald-Kuehl
,
S.
,
Lakes
,
R.
, and
Vanderby
,
R. J.
,
2012
, “
Strain-Induced Damage Reduces Echo Intensity Changes in Tendon During Loading
,”
J. Biomech.
,
45
(
9
), pp.
1607
1611
.
17.
Natali
,
A.
,
Pavan
,
P.
,
Carniel
,
E.
,
Lucisano
,
M.
, and
Taglialavoro
,
G.
,
2005
, “
Anisotropic Elasto-Damage Constitutive Model for the Biomechanical Analysis of Tendons
,”
Med. Eng. Phys.
,
27
(
3
), pp.
209
214
.
18.
Lee
,
A. H.
,
Szczesny
,
S. E.
,
Santare
,
M. H.
, and
Elliott
,
D. M.
,
2017
, “
Investigating Mechanisms of Tendon Damage by Measuring Multi-Scale Recovery Following Tensile Loading
,”
Acta Biomater.
,
57
, pp.
363
372
.
19.
Veres
,
S. P.
, and
Lee
,
J. M.
,
2012
, “
Designed to Fail: A Novel Mode of Collagen Fibril Disruption and Its Relevance to Tissue Toughness
,”
Biophys. J.
,
102
(
12
), pp.
2876
2884
.
20.
Zitnay
,
J. L.
,
Li
,
Y.
,
Qin
,
Z.
,
San
,
B. H.
,
Depalle
,
B.
,
Reese
,
S. P.
,
Buehler
,
M. J.
,
Yu
,
S. M.
, and
Weiss
,
J. A.
,
2017
, “
Molecular Level Detection and Localization of Mechanical Damage in Collagen Enabled by Collagen Hybridizing Peptides
,”
Nat. Commun.
,
8
, p.
14913
.
21.
Liu
,
Y.
,
Ballarini
,
R.
, and
Eppell
,
S. J.
,
2016
, “
Tension Tests on Mammalian Collagen Fibrils
,”
Interface Focus
,
6
(
1
), p.
20150080
.
22.
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
.
23.
Safa
,
B. N.
,
Santare
,
M. H.
, and
Elliott
,
D. M.
,
2018
, “
A Reactive Inelasticity Theoretical Framework for Modeling Viscoelasticity, Plastic Deformation, and Damage in Musculoskeletal Soft Tissue
,”
ASME J. Biomech. Eng.
,
141
(2), p. 021005.
24.
Ateshian
,
G. A.
,
2015
, “
Viscoelasticity Using Reactive Constrained Solid Mixtures
,”
J. Biomech.
,
48
(
6
), pp.
941
947
.
25.
Andrews
,
R. D.
,
Tobolsky
,
A. V.
, and
Hanson
,
E. E.
,
1946
, “
The Theory of Permanent Set at Elevated Temperatures in Natural and Synthetic Rubber Vulcanizates
,”
J. Appl. Phys.
,
17
(
5
), pp.
352
361
.
26.
Huntley
,
H.
,
Wineman
,
A.
, and
Rajagopal
,
K.
,
1997
, “
Stress Softening, Strain Localization and Permanent Set in the Circumferential Shear of an Incompressible Elastomeric Cylinder
,”
IMA J. Appl. Math.
,
59
(
3
), pp.
309
338
.
27.
Wineman
,
A.
,
2009
, “
On the Mechanics of Elastomers Undergoing Scission and Cross-Linking
,”
Int. J. Adv. Eng. Sci. Appl. Math.
,
1
(
2–3
), pp.
123
131
.
28.
Duenwald
,
S. E.
,
Vanderby
,
R.
, and
Lakes
,
R. S.
,
2010
, “
Stress Relaxation and Recovery in Tendon and Ligament: Experiment and Modeling
,”
Biorheology
,
47
(
1
), pp.
1
14
.
29.
Raz
,
E.
,
Einat
,
R.
,
Lanir
,
Y.
, and
Yoram
,
L.
,
2009
, “
Recruitment Viscoelasticity of the Tendon
,”
ASME J. Biomech. Eng.
,
131
(
11
), p.
111008
.
30.
Yin
,
L.
, and
Elliott
,
D. M.
,
2004
, “
A Biphasic and Transversely Isotropic Mechanical Model for Tendon: Application to Mouse Tail Fascicles in Uniaxial Tension
,”
J. Biomech.
,
37
(
6
), pp.
907
916
.
31.
Zhang
,
W.
, and
Sacks
,
M. S.
,
2017
, “
Modeling the Response of Exogenously Crosslinked Tissue to Cyclic Loading: The Effects of Permanent Set
,”
J. Mech. Behav. Biomed. Mater.
,
75
, pp.
336
350
.
32.
Tonge
,
T. K.
,
Ruberti
,
J. W.
, and
Nguyen
,
T. D.
,
2015
, “
Micromechanical Modeling Study of Mechanical Inhibition of Enzymatic Degradation of Collagen Tissues
,”
Biophys. J.
,
109
(
12
), pp.
2689
2700
.
33.
Duenwald-Kuehl
,
S.
,
Kondratko
,
J.
,
Lakes
,
R. S.
, and
Vanderby
,
R. J.
,
2012
, “
Damage Mechanics of Porcine Flexor Tendon: Mechanical Evaluation and Modeling
,”
Ann. Biomed. Eng.
,
40
(
8
), pp.
1692
1707
.
34.
Guo
,
Z.
, and
De Vita
,
R.
,
2009
, “
Probabilistic Constitutive Law for Damage in Ligaments
,”
Med. Eng. Phys.
,
31
(
9
), pp.
1104
1109
.
35.
Nims
,
R. J.
,
Durney
,
K. M.
,
Cigan
,
A. D.
,
Dusséaux
,
A.
,
Hung
,
C. T.
, and
Ateshian
,
G. A.
,
2016
, “
Continuum Theory of Fibrous Tissue Damage Mechanics Using Bond Kinetics: Application to Cartilage Tissue Engineering
,”
Interface Focus
,
6
(
1
), p.
20150063
.
36.
Fereidoonnezhad
,
B.
,
Naghdabadi
,
R.
, and
Holzapfel
,
G.
,
2016
, “
Stress Softening and Permanent Deformation in Human Aortas: Continuum and Computational Modeling With Application to Arterial Clamping
,”
J. Mech. Behav. Biomed. Mater.
,
61
, pp.
600
616
.
37.
Maher
,
E.
,
Creane
,
A.
,
Lally
,
C.
, and
Kelly
,
D. J.
,
2012
, “
An Anisotropic Inelastic Constitutive Model to Describe Stress Softening and Permanent Deformation in Arterial Tissue
,”
J. Mech. Behav. Biomed. Mater.
,
12
, pp.
9
19
.
38.
Peña
,
E.
,
2014
, “
Computational Aspects of the Numerical Modelling of Softening, Damage and Permanent Set in Soft Biological Tissues
,”
Comput. Struct.
,
130
, pp.
57
72
.
39.
Peña
,
E.
,
Calvo
,
B.
,
Martínez
,
M. A.
, and
Doblaré
,
M.
,
2007
, “
An Anisotropic Visco-Hyperelastic Model for Ligaments at Finite Strains. Formulation and Computational Aspects
,”
Int. J. Solids Struct.
,
44
(
3–4
), pp.
760
778
.
40.
Szczesny
,
S. E.
,
Edelstein
,
R. S.
, and
Elliott
,
D. M.
,
2014
, “
DTAF Dye Concentrations Commonly Used to Measure Microscale Deformations in Biological Tissues Alter Tissue Mechanics
,”
PLoS One
,
9
(
6
), p.
e99588
.
41.
Kachanov
,
L. M.
,
1986
,
Introduction to Continuum Damage Mechanics
, Vol.
79
,
Springer Science & Business Media
,
Dordrecht, The Netherlands
.
42.
Lemaitre
,
J.
,
1984
, “
How to Use Damage Mechanics
,”
Nucl. Eng. Des.
,
80
(
2
), pp.
233
245
.
43.
Chaboche
,
J. L.
,
1987
, “
Continuum Damage Mechanics: Present State and Future Trends
,”
Nucl. Eng. Des.
,
105
(
1
), pp.
19
33
.
44.
Provenzano
,
P. P.
, and
Vanderby
,
R.
,
2006
, “
Collagen Fibril Morphology and Organization: Implications for Force Transmission in Ligament and Tendon
,”
Matrix Biol.
,
25
(
2
), pp.
71
84
.
45.
Woo
,
S. L.
,
Johnson
,
G. A.
, and
Smith
,
B. A.
,
1993
, “
Mathematical Modeling of Ligaments and Tendons
,”
ASME J. Biomech. Eng.
,
115
(
4B
), pp.
468
473
.
46.
Reese
,
S. P.
, and
Weiss
,
J. A.
,
2013
, “
Tendon Fascicles Exhibit a Linear Correlation Between Poisson's Ratio and Force During Uniaxial Stress Relaxation
,”
ASME J. Biomech. Eng.
,
135
(
3
), p.
34501
.
47.
Wang
,
X. T.
, and
Ker
,
R. F.
,
1995
, “
Creep Rupture of Wallaby Tail Tendons
,”
J. Exp. Biol.
,
198
(
Pt. 3
), pp.
831
845
.https://www.ncbi.nlm.nih.gov/pubmed/?term=9244804
48.
Andarawis-Puri
,
N.
, and
Flatow
,
E. L.
,
2011
, “
Tendon Fatigue in Response to Mechanical Loading
,”
J. Musculoskeletal Neuronal Interact.
,
11
(
2
), pp.
106
114
.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4408766/?tool=pmcentrez&report=abstract
49.
Safa
,
B. N.
,
2018
, “
ReactiveBond
,” accessed May 23, 2019, https://github.com/BabakNSafa/ReactiveBond/
50.
Johansson
,
J.
, and
Forsell
,
C.
,
2016
, “
Evaluation of Parallel Coordinates: Overview, Categorization and Guidelines for Future Research
,”
IEEE Trans. Vis. Comput. Graph.
,
22
(
1
), pp.
579
588
.
51.
Wren
,
T. A.
,
Yerby
,
S. A.
,
Beaupré
,
G. S.
, and
Carter
,
D. R.
,
2001
, “
Mechanical Properties of the Human Achilles Tendon
,”
Clin. Biomech.
,
16
(
3
), pp.
245
251
.
52.
Henninger
,
H. B.
,
Valdez
,
W. R.
,
Scott
,
S. A.
, and
Weiss
,
J. A.
,
2015
, “
Elastin Governs the Mechanical Response of Medial Collateral Ligament Under Shear and Transverse Tensile Loading
,”
Acta Biomater.
,
25
, pp.
304
312
.
53.
Redaelli
,
A.
,
Vesentini
,
S.
,
Soncini
,
M.
,
Vena
,
P.
,
Mantero
,
S.
, and
Montevecchi
,
F. M.
,
2003
, “
Possible Role of Decorin Glycosaminoglycans in Fibril to Fibril Force Transfer in Relative Mature Tendons—A Computational Study From Molecular to Microstructural Level
,”
J. Biomech.
,
36
(
10
), pp.
1555
1569
.
54.
Fang
,
F.
, and
Lake
,
S. P.
,
2016
, “
Multiscale Mechanical Integrity of Human Supraspinatus Tendon in Shear After Elastin Depletion
,”
J. Mech. Behav. Biomed. Mater.
,
63
, pp.
443
455
.
55.
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
.
56.
Freedman
,
B. R.
,
Gordon
,
J. A.
, and
Castro
,
L. J.
,
2019
, “
The Achilles Tendon: Fundamental Properties and Mechanisms Governing Healing
,”
Muscles Ligaments Tendons J.
,
4
(
2
), pp.
245
55
.
57.
Snedeker
,
J. G.
, and
Foolen
,
J.
,
2017
, “
Tendon Injury and Repair—A Perspective on the Basic Mechanisms of Tendon Disease and Future Clinical Therapy
,”
Acta Biomater.
,
63
, pp.
18
36
.
58.
Babaei
,
B.
,
Velasquez-Mao
,
A. J.
,
Thomopoulos
,
S.
,
Elson
,
E. L.
,
Abramowitch
,
S. D.
, and
Genin
,
G. M.
,
2017
, “
Discrete Quasi-Linear Viscoelastic Damping Analysis of Connective Tissues, and the Biomechanics of Stretching
,”
J. Mech. Behav. Biomed. Mater.
,
69
, pp.
193
202
.
59.
Puso
,
M. A.
, and
Weiss
,
J. A.
,
1998
, “
Finite Element Implementation of Anisotropic Quasi-Linear Viscoelasticity Using a Discrete Spectrum Approximation
,”
ASME J. Biomech. Eng.
,
120
(
1
), pp.
62
70
.
60.
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
), p.
280
.
61.
Szczesny
,
S. E.
, and
Elliott
,
D. M.
,
2014
, “
Incorporating Plasticity of the Interfibrillar Matrix in Shear Lag Models Is Necessary to Replicate the Multiscale Mechanics of Tendon Fascicles
,”
J. Mech. Behav. Biomed. Mater.
,
40
, pp.
325
338
.
62.
Ban
,
E.
,
Barocas
,
V. H.
,
Shephard
,
M. S.
, and
Picu
,
C. R.
,
2016
, “
Softening in Random Networks of Non-Identical Beams
,”
J. Mech. Phys. Solids
,
87
, pp.
38
50
.
63.
Simo
,
J. C.
, and
Ju
,
J. W.
,
1987
, “
Strain- and Stress-Based Continuum Damage model—I: Formulation
,”
Int. J. Solids Struct.
,
23
(
7
), pp.
821
840
.
64.
Voyiadjis
,
G. Z.
, and
Kattan
,
P. I.
,
2009
, “
A Comparative Study of Damage Variables in Continuum Damage Mechanics
,”
Int. J. Damage Mech.
,
18
(
4
), pp.
315
340
.
65.
Connizzo
,
B. K.
, and
Grodzinsky
,
A. J.
,
2017
, “
Tendon Exhibits Complex Poroelastic Behavior at the Nanoscale as Revealed by High-Frequency AFM-Based Rheology
,”
J. Biomech.
,
54
, pp.
11
18
.
66.
Huang
,
C. Y.
,
Mow
,
V. C.
, and
Ateshian
,
G. A.
,
2001
, “
The Role of Flow-Independent Viscoelasticity in the Biphasic Tensile and Compressive Responses of Articular Cartilage
,”
ASME J. Biomech. Eng.
,
123
(
5
), pp.
410
417
.
67.
Iatridis
,
J. C.
,
Wu
,
J.
,
Yandow
,
J. A.
, and
Langevin
,
H. M.
,
2003
, “
Subcutaneous Tissue Mechanical a Is Linear and Viscoelastic Under Uniaxial Tension
,”
Connect. Tissue Res.
,
44
(
5
), pp.
208
217
.
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