An extensive multiaxial experimental campaign on the monotonic, time- and history-dependent mechanical response of bovine Glisson's capsule (GC) is presented. Reproducible characteristics were observed such as J-shaped curves in uniaxial and biaxial configurations, large lateral contraction, cyclic tension softening, large tension relaxation, and moderate creep strain accumulation. The substantial influence of the reference state selection on the kinematic response and the tension versus stretch curves is demonstrated and discussed. The parameters of a large-strain viscoelastic constitutive model were determined based on the data of uniaxial tension relaxation experiments. The model is shown to well predict the uniaxial and biaxial viscoelastic responses in all other configurations. GC, the corresponding model, and the experimental protocols are proposed as a useful basis for future studies on the relation between microstructure and tissue functionality and on the factors influencing the mechanical response of soft collagenous membranes.

References

1.
Kuntz
,
E.
, and
Kuntz
,
H.-D.
,
2006
,
Hepatology, Principles and Practice: History, Morphology, Biochemistry, Diagnostics, Clinic, Therapy
,
Springer Science & Business Media
,
Berlin, Germany
.
2.
Schünke
,
M.
,
Schulte
,
E.
, and
Schumacher
,
U.
,
2007
,
THIEME Atlas of Anatomy: Neck and Internal Organs
,
Thieme
,
Stuttgart, Germany
.
3.
Arnold
,
G.
,
Gressner
,
A.
, and
Clahsen
,
H.
,
1976
, “
Experimental Studies of the Historheology of the Liver Capsule (experimentelle untersuchungen zur historheologie der leberkapsel)
,”
Anat. Anz.
,
142
(
3
), pp.
180
191
.
4.
Snedeker
,
J.
,
Niederer
,
P.
,
Schmidlin
,
F.
,
Farshad
,
M.
,
Demetropoulos
,
C.
,
Lee
,
J.
, and
Yang
,
K.
,
2005
, “
Strain-Rate Dependent Material Properties of the Porcine and Human Kidney Capsule
,”
J. Biomech.
,
38
(
5
), pp.
1011
1021
.
5.
Stingl
,
J.
,
Báca
,
V.
,
Cech
,
P.
,
Kovanda
,
J.
,
Kovandová
,
H.
,
Mandys
,
V.
,
Rejmontová
,
J.
, and
Sosna
,
B.
,
2002
, “
Morphology and Some Biomechanical Properties of Human Liver and Spleen
,”
Surg. Radiol. Anat.
,
24
(
5
), pp.
285
289
.
6.
Tamura
,
A.
,
Omori
,
K.
,
Miki
,
K.
,
Lee
,
J.
,
Yang
,
K.
, and
King
,
A.
,
2002
, “
Mechanical Characterization of Porcine Abdominal Organs
,”
Stapp Car Crash J.
,
46
, pp.
55
69
.
7.
Brunon
,
A.
,
Bruyère-Garnier
,
K.
, and
Coret
,
M.
,
2010
, “
Mechanical Characterization of Liver Capsule Through Uniaxial Quasi-Static Tensile Tests Until Failure
,”
J. Biomech.
,
43
(
11
), pp.
2221
2227
.
8.
Tinkoff
,
G.
,
Esposito
,
T.
,
Reed
,
J.
,
Kilgo
,
P.
,
Fildes
,
J.
,
Pasquale
,
M.
, and
Meredith
,
J.
,
2008
, “
American Association for the Surgery of Trauma Organ Injury Scale I: Spleen, Liver, and Kidney, Validation Based on the National Trauma Data Bank
,”
J. Am. Coll. Surg.
,
207
(
5
), pp.
646
655
.
9.
Hollenstein
,
M.
,
2011
, “
Mechanics of the Human Liver: Experiments and Modeling
,” Ph.D. thesis, ETH-Zürich, Zürich, Switzerland.
10.
Umale
,
S.
,
Chatelin
,
S.
,
Bourdet
,
N.
,
Deck
,
C.
,
Diana
,
M.
,
Dhumane
,
P.
,
Soler
,
L.
,
Marescaux
,
J.
, and
Willinger
,
R.
,
2011
, “
Experimental In Vitro Mechanical Characterization of Porcine Glisson's Capsule and Hepatic Veins
,”
J. Biomech.
,
44
(
9
), pp.
1678
1683
.
11.
Gressner
,
A.
,
Clahsen
,
H.
,
Arnold
,
G.
, and
Fessel
,
H.
,
1977
, “
Biomechanical Investigations of the Liver Capsule (biomechanische untersuchungen der leberkapsel)
,”
Res. Exp. Med.
,
171
(
2
), pp.
191
199
.
12.
Arnold
,
G.
,
Gressner
,
A.
,
Clahsen
,
H.
, and
Krönchen
,
A.
,
1977
, “
On the Biomechanical Function of the Liver Capsule
,”
Experientia
,
33
(
8
), pp.
1089
1091
.
13.
Brunon
,
A.
,
Bruyère-Garnier
,
K.
, and
Coret
,
M.
,
2011
, “
Characterization of the Nonlinear Behaviour and the Failure of Human Liver Capsule Through Inflation Tests
,”
J. Mech. Behav. Biomed. Mater.
,
4
(
8
), pp.
1572
1581
.
14.
Jayyosi
,
C.
,
Coret
,
M.
, and
Bruyère-Garnier
,
K.
,
2013
, “
Imaging of the Human Glisson's Capsule by Two-Photon Excitation Microscopy and Mechanical Characterisation by Uniaxial Tensile Tests
,”
Comput. Methods Biomech. Biomed. Eng.
,
16
(
Suppl. 1
), pp.
282
283
.
15.
Jayyosi
,
C.
,
Fargier
,
G.
,
Coret
,
M.
, and
Bruyere-Garnier
,
K.
,
2014
, “
Photobleaching as a Tool to Measure the Local Strain Field in Fibrous Membranes of Connective Tissues
,”
Acta Biomater.
,
10
(
6
), pp.
2591
2601
.
16.
Carter
,
F.
,
Frank
,
T.
,
Davies
,
P.
,
McLean
,
D.
, and
Cuschieri
,
A.
,
2001
, “
Measurements and Modelling of the Compliance of Human and Porcine Organs
,”
Med. Image Anal.
,
5
(
4
), pp.
231
236
.
17.
Ottensmeyer
,
M.
,
2002
, “
Tempest 1-D: An Instrument for Measuring Solid Organ Soft Tissue Properties
,”
Exp. Tech.
,
26
(
3
), pp.
48
50
.
18.
Samur
,
E.
,
Sedef
,
M.
,
Basdogan
,
C.
,
Avtan
,
L.
, and
Duzgun
,
O.
,
2007
, “
A Robotic Indenter for Minimally Invasive Measurement and Characterization of Soft Tissue Response
,”
Med. Image Anal.
,
11
(
4
), pp.
361
373
.
19.
Nava
,
A.
,
Mazza
,
E.
,
Furrer
,
M.
,
Villiger
,
P.
, and
Reinhart
,
W.
,
2008
, “
In Vivo Mechanical Characterization of Human Liver
,”
Med. Image Anal.
,
12
(
2
), pp.
203
216
.
20.
Mazza
,
E.
,
Nava
,
A.
,
Hahnloser
,
D.
,
Jochum
,
W.
, and
Bajka
,
M.
,
2007
, “
The Mechanical Response of Human Liver and Its Relation to Histology: An In Vivo Study
,”
Med. Image Anal.
,
11
(
6
), pp.
663
672
.
21.
Buerzle
,
W.
,
2014
, “
Mechanical Characterization and Modeling of Human Fetal Membrane Tissue
,”
Ph.D. thesis
, ETH-Zürich, Zürich, Switzerland.
22.
Mauri
,
A.
,
Perrini
,
M.
,
Ehret
,
A.
,
De Focatiis
,
D.
, and
Mazza
,
E.
,
2015
, “
Time-Dependent Mechanical Behavior of Human Amnion: Macroscopic and Microscopic Characterization
,”
Acta Biomater.
,
11
(
1
), pp.
314
323
.
23.
Perrini
,
M.
,
Mauri
,
A.
,
Ehret
,
A.
,
Ochsenbein-Kölble
,
N.
,
Zimmermann
,
R.
,
Ehrbar
,
M.
, and
Mazza
,
E.
,
2015
, “
Mechanical and Microstructural Investigation of the Cyclic Behavior of Human Amnion
,”
ASME J. Biomech. Eng.
,
137
(
6
), p.
061010
.
24.
Ohtani
,
O.
,
1988
, “
Three-Dimensional Organization of the Collagen Fibrillar Framework of the Human and Rat Livers
,”
Arch. Histol. Cytol.
,
51
(
5
), pp.
473
488
.
25.
Martinez-Hernandez
,
A.
, and
Amenta
,
P.
,
1993
, “
The Hepatic Extracellular Matrix. I. Components and Distribution in Normal Liver
,”
Virchows Arch. A: Pathol. Anat. Histol.
,
423
(
1
), pp.
1
11
.
26.
Porto
,
L.
,
Chevallier
,
M.
,
Peyrol
,
S.
,
Guerret
,
S.
, and
Grimaud
,
J.-A.
,
1990
, “
Elastin in Human, Baboon, and Mouse Liver: An Immunohistochemical and Immunoelectron Microscopic Study
,”
Anat. Rec.
,
228
(
4
), pp.
392
404
.
27.
Rauterberg
,
J.
,
Voss
,
B.
,
Pott
,
P. D. G.
, and
Gerlach
,
U.
,
1981
, “
Connective Tissue Components of the Normal and Fibrotic Liver
,”
Klin. Wochenschr.
,
59
(
14
), pp.
767
779
.
28.
Stenman
,
S.
, and
Vaheri
,
A.
,
1978
, “
Distribution of a Major Connective Tissue Protein, Fibronectin, in Normal Human Tissues
,”
J. Exp. Med.
,
147
(
4
), pp.
1054
1064
.
29.
Lee
,
J.
,
Kim
,
S.
,
Kwack
,
S.
,
Kim
,
C.
,
Moon
,
T.
,
Lee
,
S.
,
Cho
,
M.
,
Kang
,
D.
, and
Kim
,
G.
,
2008
, “
Hepatic Capsular and Subcapsular Pathologic Conditions: Demonstration With CT and MR Imaging
,”
Radiographics
,
28
(
5
), pp.
1307
1323
.
30.
Jayyosi
,
C.
,
Coret
,
M.
, and
Bruyère-Garnier
,
K.
,
2016
, “
Characterizing Liver Capsule Microstructure Via In Situ Bulge Test Coupled With Multiphoton Imaging
,”
J. Mech. Behav. Biomed. Mater.
,
54
, pp.
229
243
.
31.
Buerzle
,
W.
,
Haller
,
C.
,
Jabareen
,
M.
,
Egger
,
J.
,
Mallik
,
A.
,
Ochsenbein-Koelble
,
N.
,
Ehrbar
,
M.
, and
Mazza
,
E.
,
2013
, “
Multiaxial Mechanical Behavior of Human Fetal Membranes and Its Relationship to Microstructure
,”
Biomech. Model. Mechanobiol.
,
12
(
4
), pp.
747
762
.
32.
Hopf
,
R.
,
Bernardi
,
L.
,
Menze
,
J.
,
Zündel
,
M.
,
Mazza
,
E.
, and
Ehret
,
A.
,
2016
, “
Experimental and Theoretical Analyses of the Age-Dependent Large-Strain Behavior of Sylgard 184 (10:1) Silicone Elastomer
,”
J. Mech. Behav. Biomed. Mater.
,
60
, pp.
425
437
.
33.
Mauri
,
A.
,
Ehret
,
A.
,
Perrini
,
M.
,
Maake
,
C.
,
Ochsenbein-Koelble
,
N.
,
Ehrbar
,
M.
,
Oyen
,
M.
, and
Mazza
,
E.
,
2015
, “
Deformation Mechanisms of Human Amnion: Quantitative Studies Based on Second Harmonic Generation Microscopy
,”
J. Biomech.
,
48
(
9
), pp.
1606
1613
.
34.
Hollenstein
,
M.
,
Nava
,
A.
,
Valtorta
,
D.
,
Snedeker
,
J.
, and
Mazza
,
E.
,
2006
, “
Mechanical Characterization of the Liver Capsule and Parenchyma
,”
Biomedical Simulation
(Lecture Notes in Computer Science, Vol.
4072
),
Springer-Verlag
,
Berlin, Germany
, pp.
150
158
.
35.
Mauri
,
A.
,
Ehret
,
A.
,
De Focatiis
,
D. S. A.
, and
Mazza
,
E.
, “
A Model for the Compressible, Viscoelastic Behavior of Human Amnion Addressing Tissue Variability Through a Single Parameter
,”
Biomech. Model. Mechanobiol
, epub.
36.
Rubin
,
M.
, and
Bodner
,
S.
,
2002
, “
A Three-Dimensional Nonlinear Model for Dissipative Response of Soft Tissue
,”
Int. J. Solids Struct.
,
39
(
19
), pp.
5081
5099
.
37.
Rubin
,
M.
, and
Papes
,
O.
,
2011
, “
Advantages of Formulating Evolution Equations for Elastic-Viscoplastic Materials in Terms of the Velocity Gradient Instead of the Spin Tensor
,”
J. Mech. Mater. Struct.
,
6
(
1–4
), pp.
529
543
.
38.
Hollenstein
,
M.
,
Jabareen
,
M.
, and
Rubin
,
M.
,
2013
, “
Modeling a Smooth Elastic-Inelastic Transition With a Strongly Objective Numerical Integrator Needing No Iteration
,”
Comput. Mech.
,
52
(
3
), pp.
649
667
.
39.
Buerzle
,
W.
, and
Mazza
,
E.
,
2013
, “
On the Deformation Behavior of Human Amnion
,”
J. Biomech.
,
46
(
11
), pp.
1777
1783
.
40.
Vader
,
D.
,
Kabla
,
A.
,
Weitz
,
D.
, and
Mahadevan
,
L.
,
2009
, “
Strain-Induced Alignment in Collagen Gels
,”
PLoS One
,
4
(
6
), p.
e5902
.
41.
Lake
,
S.
, and
Barocas
,
V.
,
2011
, “
Mechanical and Structural Contribution of Non-Fibrillar Matrix in Uniaxial Tension: A Collagen-Agarose Co-Gel Model
,”
Ann. Biomed. Eng.
,
39
(
7
), pp.
1891
1903
.
42.
Lynch
,
H.
,
Johannessen
,
W.
,
Wu
,
J.
,
Jawa
,
A.
, and
Elliott
,
D.
,
2003
, “
Effect of Fiber Orientation and Strain Rate on the Nonlinear Uniaxial Tensile Material Properties of Tendon
,”
ASME J. Biomech. Eng.
,
125
(
5
), pp.
726
731
.
43.
Hewitt
,
J.
,
Guilak
,
F.
,
Glisson
,
R.
, and
Parker Vail
,
T.
,
2001
, “
Regional Material Properties of the Human Hip Joint Capsule Ligaments
,”
J. Orthop. Res.
,
19
(
3
), pp.
359
364
.
44.
Jayyosi
,
C.
,
2015
, “
Mechanical and Microstructural Characterization of Glisson's Capsule Behavior up to Failure, for the Prediction of Human Hepatic Tissues Injury Risk
,” Ph.D. thesis, IFSTTAR, Grenoble, France.
45.
Umale
,
S.
,
Deck
,
C.
,
Bourdet
,
N.
,
Dhumane
,
P.
,
Soler
,
L.
,
Marescaux
,
J.
, and
Willinger
,
R.
,
2012
, “
Experimental Mechanical Characterization of Abdominal Organs: Liver, Kidney & Spleen
,”
J. Mech. Behav. Biomed. Mater.
,
17
, pp.
22
33
.
46.
Itskov
,
M.
,
Ehret
,
A.
, and
Mavrilas
,
D.
,
2006
, “
A Polyconvex Anisotropic Strain-Energy Function for Soft Collagenous Tissues
,”
Biomech. Model. Mechanobiol.
,
5
(
1
), pp.
17
26
.
47.
Sacks
,
M.
, and
Chuong
,
C.
,
1998
, “
Orthotropic Mechanical Properties of Chemically Treated Bovine Pericardium
,”
Ann. Biomed. Eng.
,
26
(
5
), pp.
892
902
.
48.
Sacks
,
M.
,
Chuong
,
C.
, and
More
,
R.
,
1994
, “
Collagen Fiber Architecture of Bovine Pericardium
,”
ASAIO J.
,
40
(
3
), pp.
M632
M637
.
49.
Mavrilas
,
D.
,
Sinouris
,
E.
,
Vynios
,
D.
, and
Papageorgakopoulou
,
N.
,
2005
, “
Dynamic Mechanical Characteristics of Intact and Structurally Modified Bovine Pericardial Tissues
,”
J. Biomech.
,
38
(
4
), pp.
761
768
.
50.
Boyce
,
B.
,
Jones
,
R.
,
Nguyen
,
T.
, and
Grazier
,
J.
,
2007
, “
Stress-Controlled Viscoelastic Tensile Response of Bovine Cornea
,”
J. Biomech.
,
40
(
11
), pp.
2367
2376
.
51.
Woo
,
S.-Y.
,
Gomez
,
M.
, and
Akeson
,
W.
,
1981
, “
The Time and History-Dependent Viscoelastic Properties of the Canine Medial Collateral Ligament
,”
ASME J. Biomech. Eng.
,
103
(
4
), pp.
293
298
.
52.
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
.
53.
Sung
,
H.-W.
,
Chang
,
Y.
,
Chiu
,
C.-T.
,
Chen
,
C.-N.
, and
Liang
,
H.-C.
,
1999
, “
Crosslinking Characteristics and Mechanical Properties of a Bovine Pericardium Fixed With a Naturally Occurring Crosslinking Agent
,”
J. Biomed. Mater. Res.
,
47
(
2
), pp.
116
126
.
54.
Ehret
,
A.
,
Hollenstein
,
M.
,
Mazza
,
E.
, and
Itskov
,
M.
,
2012
, “
Porcine Dermis in Uniaxial Cyclic Loading: Sample Preparation, Experimental Results and Modeling
,”
J. Mech. Mater. Struct.
,
6
(
7–8
), pp.
1125
1135
.
55.
Thornton
,
G.
,
Oliynyk
,
A.
,
Frank
,
C.
, and
Shrive
,
N.
,
1997
, “
Ligament Creep Cannot Be Predicted From Stress Relaxation at Low Stress: A Biomechanical Study of the Rabbit Medial Collateral Ligament
,”
J. Orthop. Res.
,
15
(
5
), pp.
652
656
.
56.
Provenzano
,
P.
,
Lakes
,
R.
,
Keenan
,
T.
, and
Vanderby
,
R.
, Jr.
,
2001
, “
Nonlinear Ligament Viscoelasticity
,”
Ann. Biomed. Eng.
,
29
(
10
), pp.
908
914
.
57.
Liao
,
J.
,
Yang
,
L.
,
Grashow
,
J.
, and
Sacks
,
M.
,
2007
, “
The Relation Between Collagen Fibril Kinematics and Mechanical Properties in the Mitral Valve Anterior Leaflet
,”
ASME J. Biomech. Eng.
,
129
(
1
), pp.
78
87
.
58.
Grashow
,
J.
,
Sacks
,
M.
,
Liao
,
J.
, and
Yoganathan
,
A.
,
2006
, “
Planar Biaxial Creep and Stress Relaxation of the Mitral Valve Anterior Leaflet
,”
Ann. Biomed. Eng.
,
34
(
10
), pp.
1509
1518
.
59.
Purslow
,
P.
,
Wess
,
T.
, and
Hukins
,
D.
,
1998
, “
Collagen Orientation and Molecular Spacing During Creep and Stress-Relaxation in Soft Connective Tissues
,”
J. Exp. Biol.
,
201
(
1
), pp.
135
142
.
60.
Screen
,
H.
,
Seto
,
J.
,
Krauss
,
S.
,
Boesecke
,
P.
, and
Gupta
,
H.
,
2011
, “
Extrafibrillar Diffusion and Intrafibrillar Swelling at the Nanoscale Are Associated With Stress Relaxation in the Soft Collagenous Matrix Tissue of Tendons
,”
Soft Matter
,
7
(
23
), pp.
11243
11251
.
61.
Svensson
,
R.
,
Hassenkam
,
T.
,
Hansen
,
P.
, and
Peter Magnusson
,
S.
,
2010
, “
Viscoelastic Behavior of Discrete Human Collagen Fibrils
,”
J. Mech. Behav. Biomed. Mater.
,
3
(
1
), pp.
112
115
.
62.
Thornton
,
G.
,
Frank
,
C.
, and
Shrive
,
N.
,
2001
, “
Ligament Creep Behavior Can Be Predicted From Stress Relaxation by Incorporating Fiber Recruitment
,”
J. Rheol.
,
45
(
2
), pp.
493
507
.
63.
Screen
,
H.
,
2008
, “
Investigating Load Relaxation Mechanics in Tendon
,”
J. Mech. Behav. Biomed. Mater.
,
1
(
1
), pp.
51
58
.
64.
Sopakayang
,
R.
,
De Vita
,
R.
,
Kwansa
,
A.
, and
Freeman
,
J.
,
2012
, “
Elastic and Viscoelastic Properties of a Type I Collagen Fiber
,”
J. Theor. Biol.
,
293
, pp.
197
205
.
65.
Raischel
,
F.
,
Kun
,
F.
, and
Herrmann
,
H.
,
2006
, “
Failure Process of a Bundle of Plastic Fibers
,”
Phys. Rev. E
,
73
(
6
), p.
066101
.
66.
Guo
,
Z.
, and
De Vita
,
R.
,
2009
, “
Probabilistic Constitutive Law for Damage in Ligaments
,”
Med. Eng. Phys.
,
31
(
9
), pp.
1104
1109
.
67.
Legerlotz
,
K.
,
Riley
,
G.
, and
Screen
,
H.
,
2013
, “
Gag Depletion Increases the Stress-Relaxation Response of Tendon Fascicles, but Does Not Influence Recovery
,”
Acta Biomater.
,
9
(
6
), pp.
6860
6866
.
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