Abstract

The understanding of strain rate-dependent mechanical properties of the skin is important for accurate prediction of its biomechanics under different loading conditions. This study investigated the effect of strain rate, i.e., 0.025/s (low), 0.5/s (medium), and 1.25/s (high), ranging in the physiological loading rate of connective tissue, on the stress-relaxation response of the porcine dermis. Results show that in the initial phase of the relaxation, the value of stress relaxation (extent of relaxation) was found higher for high strain rate. However, the equilibrium stress was found strain rate independent. A Mooney–Rivlin-based five-term quasi-linear viscoelastic (QLV) model was proposed to determine the effect of strain rate on the stress-relaxation behavior of the porcine dermis. The value of relaxation modulus G1 and G2 were found higher for the high strain rate, whereas the reverse trend was observed for G3, G4, and G5. Moreover, the value of time constants τ1,τ2,τ3τ4, and τ5 were found higher for low strain rate. Statistical analysis shows no significant difference in the values of G5, τ4, and τ5 among the three strain rates. The proposed model was found capable to fit the stress-relaxation response of skin with great accuracy, e.g., root-mean-squared-error (RMSE) value equal to 0.015 ± 0.00012 MPa. Moreover, this hyper-viscoelastic model can be utilized: to quantify the effects of age and diseases on the skin; to simulate the stresses on sutures during large wound closure and impact loading.

References

1.
Pissarenko
,
A.
,
Yang
,
W.
,
Quan
,
H.
,
Brown
,
K. A.
,
Williams
,
A.
,
Proud
,
W. G.
, and
Meyers
,
M. A.
,
2019
, “
Tensile Behavior and Structural Characterization of Pig Dermis
,”
Acta Biomater.
,
86
, pp.
77
95
.10.1016/j.actbio.2019.01.023
2.
Wilkes
,
G. L.
,
Brown
,
I. A.
, and
Wildnauer
,
R. H.
,
1973
, “
The Biomechanical Properties of Skin
,”
CRC Crit. Rev. Bioeng.
,
1
(
4
), pp.
453
95
.
3.
Hsu
,
S.
,
Jamieson
,
A. M.
, and
Blackwell
,
J.
,
1994
, “
Viscoelastic Studies of Extracellular Matrix Interactions in a Model Native Collagen Gel System
,”
Biorheology
,
31
(
1
), pp.
21
36
.10.3233/BIR-1994-31103
4.
Crichton
,
M. L.
,
Chen
,
X.
,
Huang
,
H.
, and
Kendall
,
M.
,
2013
, “
Elastic Modulus and Viscoelastic Properties of Full Thickness Skin Characterised at Micro Scales
,”
Biomaterials
,
34
(
8
), pp.
2087
2097
.10.1016/j.biomaterials.2012.11.035
5.
Liu
,
F.
,
Li
,
C.
,
Liu
,
S.
,
Genin
,
G. M.
,
Huang
,
G.
,
Lu
,
T.
, and
Xu
,
F.
,
2015
, “
Effect of Viscoelasticity on Skin Pain Sensation
,”
Theor. Appl. Mech. Lett. [Internet]
,
5
(
6
), pp.
222
226
.10.1016/j.taml.2015.11.002
6.
Jee
,
T.
, and
Komvopoulos
,
K.
,
2014
, “
Skin Viscoelasticity Studied In Vitro by Microprobe-Based Techniques
,”
J. Biomech.
,
47
(
2
), pp.
553
559
.10.1016/j.jbiomech.2013.10.006
7.
Ottenio
,
M.
,
Tran
,
D.
,
Annaidh
,
A. N.
,
Gilchrist
,
M. D.
, and
Bruyère
,
K.
,
2015
, “
Strain Rate and Anisotropy Effects on the Tensile Failure Characteristics of Human Skin
,”
J. Mech. Behav. Biomed. Mater.
,
41
, pp.
241
250
.10.1016/j.jmbbm.2014.10.006
8.
Remache
,
D.
,
Caliez
,
M.
,
Gratton
,
M.
, and
Dos Santos
,
S.
,
2018
, “
The Effects of Cyclic Tensile and Stress-Relaxation Tests on Porcine Skin
,”
J. Mech. Behav. Biomed. Mater.
,
77
, pp.
242
249
.10.1016/j.jmbbm.2017.09.009
9.
Sherman
,
V. R.
,
Tang
,
Y.
,
Zhao
,
S.
,
Yang
,
W.
, and
Meyers
,
M. A.
,
2017
, “
Structural Characterization and Viscoelastic Constitutive Modeling of Skin
,”
Acta Biomater.
,
53
, pp.
460
469
.10.1016/j.actbio.2017.02.011
10.
Liu
,
Z.
, and
Yeung
,
K.
,
2008
, “
The Preconditioning and Stress Relaxation of Skin Tissue
,”
J. Biomed. Pharm. Eng.
,
2
(
1
), pp.
22
28
.https://www3.ntu.edu.sg/bmerc/contents/JBPE/J002/JBPE%202(1)%2022-28.pdf
11.
Legerlotz
,
K.
,
Riley
,
G. P.
, 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
.10.1016/j.actbio.2013.02.028
12.
Lawless
,
B. M.
,
Sadeghi
,
H.
,
Temple
,
D. K.
,
Dhaliwal
,
H.
,
Espino
,
D. M.
, and
Hukins
,
D.
,
2017
, “
Viscoelasticity of Articular Cartilage: Analysing the Effect of Induced Stress and the Restraint of Bone in a Dynamic Environment
,”
J. Mech. Behav. Biomed. Mater.
,
75
, pp.
293
301
.10.1016/j.jmbbm.2017.07.040
13.
Kang
,
G.
, and
Wu
,
X.
,
2011
, “
Ratchetting of Porcine Skin Under Uniaxial Cyclic Loading
,”
J. Mech. Behav. Biomed. Mater.
,
4
(
3
), pp.
498
506
.10.1016/j.jmbbm.2010.12.015
14.
Screen HRC,
2008
, “
Investigating Load Relaxation Mechanics in Tendon
,”
J. Mech. Behav. Biomed. Mater.
,
1
(
1
), pp.
51
58
.10.1016/j.jmbbm.2007.03.002
15.
Abramowitch
,
S. D.
, and
Woo
,
S.-Y.
,
2004
, “
An Improved Method to Analyze the Stress Relaxation of Ligaments Following a Finite Ramp Time Based on the Quasi-Linear Viscoelastic Theory
,”
ASME J. Biomech. Eng.
,
126
(
1
), pp.
92
97
.10.1115/1.1645528
16.
Troyer
,
K. L.
,
Estep
,
D. J.
, and
Puttlitz
,
C. M.
,
2012
, “
Viscoelastic Effects During Loading Play an Integral Role in Soft Tissue Mechanics
,”
Acta Biomater.
,
8
(
1
), pp.
234
243
.10.1016/j.actbio.2011.07.035
17.
Sorvari
,
J.
,
Malinen
,
M.
, and
Hämäläinen
,
J.
,
2006
, “
Finite Ramp Time Correction Method for Non-Linear Viscoelastic Material Model
,”
Int. J. Non Linear Mech.
,
41
(
9
), pp.
1050
1056
.10.1016/j.ijnonlinmec.2006.10.015
18.
Toms
,
S. R.
,
Dakin
,
G. J.
,
Lemons
,
J. E.
, and
Eberhardt
,
A. W.
,
2002
, “
Quasi-Linear Viscoelastic Behavior of the Human Periodontal Ligament
,”
J. Biomech.
,
35
(
10
), pp.
1411
1415
.10.1016/S0021-9290(02)00166-5
19.
De Pascalis
,
R.
,
Abrahams
,
I. D.
, and
Parnell
,
W. J.
,
2014
, “
On Nonlinear Viscoelastic Deformations: A Reappraisal of Fung's Quasi-Linear Viscoelastic Model
,”
Proc. R. Soc. A Math. Phys. Eng. Sci.
,
470
(
2166
), p.
20140058
.10.1098/rspa.2014.0058
20.
Quirinia
,
A.
, and
Viidik
,
A.
,
1991
, “
Freezing for Postmortal Storage Influences the Biomechanical Properties of Linear Skin Wounds
,”
J. Biomech.
,
24
(
9
), pp.
819
823
.10.1016/0021-9290(91)90307-9
21.
O'Leary
,
S. A.
,
Doyle
,
B. J.
, and
McGloughlin
,
T. M.
,
2014
, “
The Impact of Long Term Freezing on the Mechanical Properties of Porcine Aortic Tissue
,”
J. Mech. Behav. Biomed. Mater.
,
37
, pp.
165
173
.10.1016/j.jmbbm.2014.04.015
22.
Bancelin
,
S.
,
Lynch
,
B.
,
Bonod-Bidaud
,
C.
,
Ducourthial
,
G.
,
Psilodimitrakopoulos
,
S.
,
Dokládal
,
P.
,
Allain
,
J.-M.
,
Schanne-Klein
,
M.-C.
, and
Ruggiero
,
F.
,.
2015
, “
Ex Vivo Multiscale Quantitation of Skin Biomechanics in Wild-Type and Genetically-Modified Mice Using Multiphoton Microscopy
,”
Sci. Rep.
,
5
(
1
), p.
17635
.10.1038/srep17635
23.
Woo
,
S.-Y.
,
Orlando
,
C. A.
,
Camp
,
J. F.
, and
Akeson
,
W. H.
,
1986
, “
Effects of Postmortem Storage by Freezing on Ligament Tensile Behavior
,”
J. Biomech.
,
19
(
5
), pp.
399
404
.10.1016/0021-9290(86)90016-3
24.
Arumugam
,
V.
,
Naresh
,
M. D.
, and
Sanjeevi
,
R.
,
1994
, “
Effect of Strain Rate on the Fracture Behaviour of Skin
,”
J. Biosci.
,
19
(
3
), pp.
307
313
.10.1007/BF02716820
25.
Duenwald
,
S. E.
,
Vanderby
,
R.
, and
Lakes
,
R. S.
,
2009
, “
Constitutive Equations for Ligament and Other Soft Tissue: Evaluation by Experiment
,”
Acta Mech.
,
205
(
1–4
), pp.
23
33
.10.1007/s00707-009-0161-8
26.
Fung
,
Y.
,
2013
,
Biomechanics: Mechanical Properties of Living Tissues
,
Springer Science & Business Media
, New York.
27.
Funk
,
J. R.
,
Hall
,
G. W.
,
Crandall
,
J. R.
, and
Pilkey
,
W. D.
,
2000
, “
Linear and Quasi-Linear Viscoelastic Characterization of Ankle Ligaments
,”
ASME J. Biomech. Eng.
,
122
(
1
), pp.
15
22
.10.1115/1.429623
28.
Khajehsaeid
,
H.
,
Arghavani
,
J.
,
Naghdabadi
,
R.
, and
Sohrabpour
,
S.
,
2014
, “
A Visco-Hyperelastic Constitutive Model for Rubber-Like Materials: A Rate-Dependent Relaxation Time Scheme
,”
Int. J. Eng. Sci.
,
79
, pp.
44
58
.10.1016/j.ijengsci.2014.03.001
29.
Holzapfel
,
G. A.
,
2002
, “
Nonlinear Solid Mechanics: A Continuum Approach for Engineering Science
,”
Meccanica
,
37
(
4/5
), pp.
489
490
.10.1023/A:1020843529530
30.
Ott
,
R. L.
, and
Longnecker
,
M. T.
,
2015
,
An Introduction to Statistical Methods and Data Analysis
,
Nelson Education
, Pacific Grove, CA.
31.
Sihota
,
P.
,
Yadav
,
R. N.
,
Dhiman
,
V.
,
Bhadada
,
S. K.
,
Mehandia
,
V.
, and
Kumar
,
N.
,
2019
, “
Investigation of Diabetic Patient's Fingernail Quality to Monitor Type 2 Diabetes Induced Tissue Damage
,”
Sci. Rep.
,
9
(
1
), p.
3193
.10.1038/s41598-019-39951-3
32.
Cua
,
A. B.
,
Wilhelm
,
K.-P.
, and
Maibach
,
H. I.
,
1990
, “
Elastic Properties of Human Skin: Relation to Age, Sex, and Anatomical Region
,”
Arch. Dermatol. Res.
,
282
(
5
), pp.
283
288
.10.1007/BF00375720
33.
Anssari-Benam
,
A.
,
Screen
,
H. R. C.
, and
Bucchi
,
A.
,
2019
, “
Insights Into the Micromechanics of Stress-Relaxation and Creep Behaviours in the Aortic Valve
,”
J. Mech. Behav. Biomed. Mater.
,
93
, pp.
230
245
.10.1016/j.jmbbm.2019.02.011
34.
Gupta
,
H. S.
,
Seto
,
J.
,
Krauss
,
S.
,
Boesecke
,
P.
, and
Screen
,
H. R. C.
, and
Screen HRC
,
2010
, “
In Situ Multi-Level Analysis of Viscoelastic Deformation Mechanisms in Tendon Collagen
,”
J. Struct. Biol.
,
169
(
2
), pp.
183
191
.10.1016/j.jsb.2009.10.002
35.
Emile
,
O.
,
Le Floch
,
A.
, and
Vollrath
,
F.
,
2007
, “
Time-Resolved Torsional Relaxation of Spider Draglines by an Optical Technique
,”
Phys. Rev. Lett.
,
98
(
16
), p.
167402
.10.1103/PhysRevLett.98.167402
You do not currently have access to this content.