The purpose of this study is to investigate the effects of preconditioning on the deformation response of planar tissues measured by inflation tests. The inflation response of test specimens, including the bovine cornea, bovine and porcine sclera, and human skin, exhibited a negligible evolving deformation response when subjected to repeated pressure loading with recovery periods between cycles. Tissues obtained complete recovery to the reference state, and strain contours across the entire specimen were nearly identical at the maximum pressure of each load cycle. This repeatability was obtained regardless of strain history. These results suggest that negligible permanent change was induced in the microstructure by inflation testing. Additionally, we present data illustrating that a lack of a recovery period can result in an evolving deformation response to repeated loading that is commonly attributed to preconditioning. These results suggest that the commonly observed effects of preconditioning may be avoided by experimental design for planar tissues characterized by long collagen fibers arranged in the plane of the tissue. Specifically, if the test is designed to fully fix the specimen boundary during loading, adequate recovery periods are allowed after each load cycle, and loads are limited to avoid damage, preconditioning effects may be avoided for planar tissues.

References

References
1.
Fung
,
Y. C. B.
,
1973
, “
Biorheology of Soft Tissues
,”
Biorheology
,
10
(
2
), pp.
139
155
.
2.
Fung
,
Y. C.
,
1993
,
Mechanical Properties of Living Tissues
,
Springer
,
New York
.
3.
Munoz
,
M. J.
,
Bea
,
J. A.
,
Rodriguez
,
J. F.
,
Ochoa
,
I.
,
Grasa
,
J.
,
Perez del Palomar
,
A.
,
Zaragoza
,
P.
,
Osta
,
R.
, and
Doblare
,
M.
,
2008
, “
An Experimental Study of the Mouse Skin Behaviour: Damage and Inelastic Aspects
,”
J. Biomech.
,
41
(
1
), pp.
93
99
.10.1016/j.jbiomech.2007.07.013
4.
Zeng
,
Y.
,
Liu
,
Y.
,
Xu
,
C.
,
Xu
,
X.
,
Xu
,
H.
, and
Sun
,
G.
,
2004
, “
Biomechanical Properties of Skin In Vitro for Different Expansion Methods
,”
Clin. Biomech.
,
19
(
8
), pp.
853
857
.10.1016/j.clinbiomech.2004.05.009
5.
Lee
,
M.
,
Fung
,
Y. C.
,
Shabetai
,
R.
, and
LeWinter
,
M. M.
,
1987
, “
Biaxial Mechanical Properties of Human Pericardium and Canine Comparisons
,”
Am. J. Physiol. Heart Circ. Physiol.
,
253
(
1
), pp.
H75
H82
.
6.
Provenzano
,
P.
,
Lakes
,
R.
,
Keenan
,
T.
, and
Vanderby
,
R.
, Jr.
,
2001
, “
Nonlinear Ligament Viscoelasticity
,”
Ann. Biomed. Eng.
,
29
(
10
), pp.
908
914
.10.1114/1.1408926
7.
Cheng
,
S.
,
Clarke
,
E. C.
, and
Bilston
,
L. E.
,
2009
, “
The Effects of Preconditioning Strain on Measured Tissue Properties
,”
J. Biomech.
,
42
(
9
), pp.
1360
1362
.10.1016/j.jbiomech.2009.03.023
8.
Lanir
,
Y.
, and
Fung
,
Y. C.
,
1974
, “
Two Dimensional Mechanical Properties of Rabbit Skin. I. Experimental System
,”
J. Biomech.
,
7
(
1
), pp.
29
34
.10.1016/0021-9290(74)90067-0
9.
Samani
,
A.
,
Bishop
,
J.
,
Luginbuhl
,
C.
, and
Plewes
,
D. B.
,
2003
, “
Measuring the Elastic Modulus of Ex Vivo Small Tissue Samples
,”
Phys. Med. Biol.
,
48
(
14
), pp.
2183
2198
.10.1088/0031-9155/48/14/310
10.
Marquez
,
J. P.
,
Legant
,
W.
,
Lam
,
V.
,
Cayemberg
,
A.
,
Elson
,
E.
, and
Wakatsuki
,
T.
,
2009
, “
High-Throughput Measurements of Hydrogel Tissue Construct Mechanics
,”
Tissue Eng.
,
15
(
2
), pp.
181
190
.10.1089/ten.tec.2008.0347
11.
Nava
,
A.
,
Mazza
,
E.
,
Haefner
,
O.
, and
Bajka
,
M.
,
2004
,
Experimental Observation and Modelling of Preconditioning in Soft Biological Tissues
, Vol.
3078
,
(Lecture Notes in Computer Science)
,
Springer, New York
.
12.
Stammen
,
J. A.
,
Williams
,
S.
,
Ku
,
D. N.
, and
Guldberg
,
R. E.
,
2001
, “
Mechanical Properties of a Novel PVA Hydrogel in Shear and Unconfined Compression
,”
Biomaterials
,
22
(
8
), pp.
799
806
.10.1016/S0142-9612(00)00242-8
13.
Liu
,
Z.
, and
Yeung
,
K.
,
2006
, “
On Preconditioning and Stress Relaxation Behavior of Fresh Swine Skin in Different Fibre Direction
,”
ICBPE 2006 - Proceedings of the 2006 International Conference on Biomedical and Pharmaceutical Engineering
, pp.
221
226
.
14.
Sacks
,
M. S.
,
2000
, “
Biaxial Mechanical Evaluation of Planar Biological Materials
,”
J, Elast.
,
61
(
1-3
), pp.
199
246
.10.1023/A:1010917028671
15.
Lanir
,
Y.
, and
Fung
,
Y. C.
,
1974
, “
Two Dimensional Mechanical Properties of Rabbit Skin. II. Experimental Results
,”
J. Biomech.
,
7
(
2
), pp.
171
182
.10.1016/0021-9290(74)90058-X
16.
Boyce
,
B. L.
,
Jones
,
R. E.
,
Nguyen
,
T. D.
, and
Grazier
,
J. M.
,
2007
, “
Stress-Controlled Viscoelastic Tensile Response of Bovine Cornea
,”
J. Biomech.
,
40
(
11
), pp.
2367
2376
.10.1016/j.jbiomech.2006.12.001
17.
Girard
,
M.
,
Suh
,
J. F.
,
Hart
,
R. T.
,
Burgoyne
,
C. F.
, and
Downs
,
J. C.
,
2007
, “
Effects of Storage Time on the Mechanical Properties of Rabbit Peripapillary Sclera After Enucleation
,”
Curr. Eye Res.
,
32
(
5
), pp.
465
470
.10.1080/02713680701273792
18.
Lari
,
D.
,
Schultz
,
D.
,
Wang
,
A.
,
Lee
,
O.
, and
Stewart
,
J.
,
2011
, “
Scleral Mechanics: Comparing Whole Globe Inflation and Uniaxial Testing
,”
Exp. Eye Res.
,
94
, pp.
128
135
.10.1016/j.exer.2011.11.017
19.
Schatzmann
,
L.
,
Brunner
,
P.
, and
Staubli
,
H. U.
,
1998
, “
Effect of Cyclic Preconditioning on the Tensile Properties of Human Quadriceps Tendons and Patellar Ligaments
,”
Knee Surg. Sports Traumatol. Arthrosc.
,
6
(
Suppl. 1
), pp.
S56
S61
.10.1007/s001670050224
20.
Carew
,
E. O.
,
Garg
,
A.
,
Barber
,
J. E.
, and
Vesely
,
I.
,
2004
, “
Stress Relaxation Preconditioning of Porcine Aortic Valves
,”
Ann. Biomed. Eng.
,
32
(
4
), pp.
563
572
.10.1023/B:ABME.0000019176.49650.19
21.
Eshel
,
H.
, and
Lanir
,
Y.
,
2001
, “
Effects of Strain Level and Proteoglycan Depletion on Preconditioning and Viscoelastic Responses of Rat Dorsal Skin
,”
Ann. Biomed. Eng.
,
29
(
2
), pp.
164
172
.10.1114/1.1349697
22.
Carew
,
E. O.
,
Barber
,
J. E.
, and
Vesely
,
I.
,
2000
, “
Role of Preconditioning and Recovery Time in Repeated Testing of Aortic Valve Tissues: Validation Through Quasilinear Viscoelastic Theory
,”
Ann. Biomed. Eng.
,
28
(
9
), pp.
1093
1100
.10.1114/1.1310221
23.
Lokshin
,
O.
, and
Lanir
,
Y.
,
2009
, “
Viscoelasticity and Preconditioning of Rat Skin Under Uniaxial Stretch: Microstructural Constitutive Characterization
,”
ASME J. Biomech. Eng.
,
131
(
3
), p.
031009
.10.1115/1.3049479
24.
Graf
,
B. K.
,
Vanderby
, Jr.,
R.
,
Ulm
,
M. J.
,
Rogalski
,
R. P.
, and
Thielke
,
R. J.
,
1994
, “
Effect of Preconditioning on the Viscoelastic Response of Primate Patellar Tendon
,”
Arthroscopy
,
10
(
1
), pp.
90
96
.10.1016/S0749-8063(05)80298-1
25.
Viidik
,
A
.,
1973
, “
Functional Properties of Collagenous Tissues
,”
Int. Rev. Connect Tissue Res.
,
6
, pp.
127
215
.
26.
Tower
,
T. T.
,
Neidert
,
M. R.
, and
Tranquillo
,
R. T.
,
2002
, “
Fiber Alignment Imaging During Mechanical Testing of Soft Tissues
,”
Ann. Biomed. Eng.
,
30
(
10
), pp.
1221
1233
.10.1114/1.1527047
27.
Quinn
,
K. P.
, and
Winkelstein
,
B. A.
,
2011
, “
Preconditioning Is Correlated With Altered Collagen Fiber Alignment in Ligament
,”
ASME J. Biomech. Eng.
,
133
(
6
), p.
064506
.10.1115/1.4004205
28.
Gregersen
,
H.
,
Emery
,
J. L.
, and
Mcculloch
,
A. D.
,
1998
, “
History-Dependent Mechanical Behavior of Guinea-Pig Small Intestine
,”
Ann. Biomed. Eng.
,
26
(
5
), pp.
850
858
.10.1114/1.109
29.
Emery
,
J. L.
,
Omens
,
J. H.
, and
McCulloch
,
A. D.
,
1997
, “
Strain Softening in Rat Left Ventricular Myocardium
,”
ASME J. Biomech. Eng.
,
119
(
1
), pp.
6
12
.10.1115/1.2796067
30.
Myers
,
K. M.
,
Coudrillier
,
B.
,
Boyce
,
B. L.
, and
Nguyen
,
T. D.
,
2010
, “
The Inflation Response of the Posterior Bovine Sclera
,”
Acta Biomater.
,
6
(
11
), pp.
4327
4335
.10.1016/j.actbio.2010.06.007
31.
Coudrillier
,
B.
,
Tian
,
J.
,
Alexander
,
S.
,
Myers
,
K. M.
,
Quigley
,
H. A.
, and
Nguyen
,
T. D.
,
2012
, “
Biomechanics of the Human Posterior Sclera: Age- and Glaucoma-Related Changes Measured Using Inflation Testing
,”
Invest. Ophthalmol. Vis. Sci.
,
53
(
4
), pp.
1714
1728
.10.1167/iovs.11-8009
32.
Tonge
,
T. K.
,
Atlan
,
L. S.
,
Voo
,
L. M.
, and
Nguyen
,
T. D.
,
2013
, “
Full-Field Bulge Test for Planar Anisotropic Tissues: Part I—Experimental Methods Applied to Human Skin Tissue
,”
Acta Biomater.
,
9
(
4
), pp.
5913
5925
.10.1016/j.actbio.2012.11.035
33.
Coudrillier
,
B.
,
Boote
,
C.
,
Quigley
,
H. A.
, and
Nguyen
,
T. D.
,
2012
, “
Scleral Anisotropy and Its Effects on the Mechanical Response of the Optic Nerve Head
,”
Biomech. Model. Mechanobiol.
, pp.
1
23
. 10.1007/s10237-012-0455-y
34.
Boyce
,
B. L.
,
Grazier
,
J. M.
,
Jones
,
R. E.
, and
Nguyen
,
T. D.
,
2008
, “
Full-Field Deformation of Bovine Cornea Under Constrained Inflation Conditions
,”
Biomaterials
,
29
(
28
), pp.
3896
3904
.10.1016/j.biomaterials.2008.06.011
35.
Tonge
,
T. K.
,
Voo
,
L. M.
, and
Nguyen
,
T. D.
,
2013
, “
Full-Field Bulge Test for Planar Anisotropic Tissues: Part II—A Thin Shell Method for Determining Material Parameters and Comparison of Two Distributed Fiber Modeling Approaches
,”
Acta Biomater.
,
9
(
4
), pp.
5926
5942
.10.1016/j.actbio.2012.11.034
36.
Ning
,
J.
,
Xu
,
S.
,
Wang
,
Y.
,
Lessner
,
S. M.
,
Sutton
,
M. A.
,
Anderson
,
K.
, and
Bischoff
,
J. E.
,
2010
, “
Deformation Measurements and Material Property Estimation of Mouse Carotid Artery Using a Microstructure-Based Constitutive Model
,”
ASME J. Biomech. Eng.
,
132
(
12
), p.
121010
.10.1115/1.4002700
37.
Meyer
,
C. A.
,
Bertrand
,
E.
,
Boiron
,
O.
, and
Deplano
,
V.
,
2011
, “
Stereoscopically Observed Deformations of a Compliant Abdominal Aortic Aneurysm Model
,”
ASME J. Biomech. Eng.
,
133
(
11
), p.
111004
.10.1115/1.4005416
38.
Soons
,
J.
,
Lava
,
P.
,
Debruyne
,
D.
, and
Dirckx
,
J.
,
2012
, “
Full-Field Optical Deformation Measurement in Biomechanics: Digital Speckle Pattern Interferometry and 3D Digital Image Correlation Applied to Bird Beaks
,”
J. Mech. Behav. Biomed. Mater.
,
14
, pp.
186
191
.10.1016/j.jmbbm.2012.05.004
39.
Hu
,
Z.
,
Xie
,
H.
,
Lu
,
J.
,
Wang
,
H.
, and
Zhu
,
J.
,
2011
, “
Error Evaluation Technique for Three-Dimensional Digital Image Correlation
,”
Appl. Opt.
,
50
(
33
), pp.
6239
6247
.10.1364/AO.50.006239
40.
Ke
,
X.-D.
,
Schreier
,
H.
,
Sutton
,
M.
, and
Wang
,
Y.
,
2011
, “
Error Assessment in Stereo-Based Deformation Measurements
,”
Exp. Mech.
,
51
(
4
), pp.
423
441
.10.1007/s11340-010-9450-3
41.
Fazzini
,
M.
,
Mistou
,
S.
,
Dalverny
,
O.
, and
Robert
,
L.
,
2010
, “
Study of Image Characteristics on Digital Image Correlation Error Assessment
,”
Opt. Lasers Eng.
,
48
(
3
), pp.
335
339
.10.1016/j.optlaseng.2009.10.012
42.
Sutton
,
M.
,
Ke
,
X.
,
Lessner
,
S.
,
Goldbach
,
M.
,
Yost
,
M.
,
Zhao
,
F.
, and
Schreier
,
H.
,
2008
, “
Strain Field Measurements on Mouse Carotid Arteries Using Microscopic Three-Dimensional Digital Image Correlation
,”
J. Biomed. Mater. Res., Part A
,
84
(
1
), pp.
178
190
.10.1002/jbm.a.31268
43.
Schreier
,
H.
,
Garcia
,
D.
, and
Sutton
,
M.
,
2004
, “
Advances in Light Microscope Stereo Vision
,”
Exp. Mech.
,
44
(
3
), pp.
278
288
.10.1007/BF02427894
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