The physiological performance of trachea is highly dependent on its mechanical behavior, and therefore, the mechanical properties of its components. Mechanical characterization of trachea is key to succeed in new treatments such as tissue engineering, which requires the utilization of scaffolds which are mechanically compatible with the native human trachea. In this study, after isolating human trachea samples from brain-dead cases and proper storage, we assessed the viscoelastic properties of tracheal cartilage, smooth muscle, and connective tissue based on stress relaxation tests (at 5% and 10% strains for cartilage and 20%, 30%, and 40% for smooth muscle and connective tissue). After investigation of viscoelastic linearity, constitutive models including Prony series for linear viscoelasticity and quasi-linear viscoelastic, modified superposition, and Schapery models for nonlinear viscoelasticity were fitted to the experimental data to find the best model for each tissue. We also investigated the effect of age on the viscoelastic behavior of tracheal tissues. Based on the results, all three tissues exhibited a (nonsignificant) decrease in relaxation rate with increasing the strain, indicating viscoelastic nonlinearity which was most evident for cartilage and with the least effect for connective tissue. The three-term Prony model was selected for describing the linear viscoelasticity. Among different models, the modified superposition model was best able to capture the relaxation behavior of the three tracheal components. We observed a general (but not significant) stiffening of tracheal cartilage and connective tissue with aging. No change in the stress relaxation percentage with aging was observed. The results of this study may be useful in the design and fabrication of tracheal tissue engineering scaffolds.

References

References
1.
Grillo
,
H. C.
,
1989
, “
Notes on the Windpipe
,”
Ann. Thorac. Surg.
,
47
(
1
), pp.
9
26
.
2.
Bagnoli
,
P.
,
Acocella
,
F.
,
Di Giancamillo
,
M.
,
Fumero
,
R.
, and
Costantino
,
M. L.
,
2013
, “
Finite Element Analysis of the Mechanical Behavior of Preterm Lamb Tracheal Bifurcation During Total Liquid Ventilation
,”
J. Biomech.
,
46
(
3
), pp.
462
469
.
3.
Teng
,
Z.
,
Trabelsi
,
O.
,
Ochoa
,
I.
,
He
,
J.
,
Gillard
,
J. H.
, and
Doblare
,
M.
,
2012
, “
Anisotropic Material Behaviours of Soft Tissues in Human Trachea: An Experimental Study
,”
J. Biomech.
,
45
(
9
), pp.
1717
1723
.
4.
Roberts
,
C. R.
,
Rains
,
J. K.
,
Paré
,
P. D.
,
Walker
,
D. C.
,
Wiggs
,
B.
, and
Bert
,
J. L.
,
1998
, “
Ultrastructure and Tensile Properties of Human Tracheal Cartilage
,”
J. Biomech.
,
31
(
1
), pp.
81
86
.
5.
Pérez del Palomar
,
A.
,
Trabelsi
,
O.
,
Mena
,
A.
,
López-Villalobos
,
J. L.
,
Ginel
,
A.
, and
Doblaré
,
M.
,
2010
, “
Patient-Specific Models of Human Trachea to Predict Mechanical Consequences of Endoprosthesis Implantation
,”
Philos. Trans. R. Soc., A
,
368
(
1921
), pp.
2881
2896
.
6.
Kamm
,
R. D.
,
1999
, “
Airway Wall Mechanics
,”
Annu. Rev. Biomed. Eng.
,
1
(
1
), pp.
47
72
.
7.
Teng
,
Z.
,
Ochoa
,
I.
,
Li
,
Z.
,
Lin
,
Y.
,
Rodriguez
,
J. F.
,
Bea
,
J. A.
, and
Doblare
,
M.
,
2008
, “
Nonlinear Mechanical Property of Tracheal Cartilage: A Theoretical and Experimental Study
,”
J. Biomech.
,
41
(
9
), pp.
1995
2002
.
8.
Teng
,
Z.
,
Ochoa
,
I.
,
Li
,
Z.
,
Liao
,
Z.
,
Lin
,
Y.
, and
Doblare
,
M.
,
2009
, “
Study on Tracheal Collapsibility, Compliance, and Stress by Considering Nonlinear Mechanical Property of Cartilage
,”
Ann. Biomed. Eng.
,
37
(
11
), pp.
2380
2389
.
9.
Trabelsi
,
O.
,
del Palomar
,
A. P.
,
López-Villalobos
,
J. L.
,
Ginel
,
A.
, and
Doblaré
,
M.
,
2010
, “
Experimental Characterization and Constitutive Modeling of the Mechanical Behavior of the Human Trachea
,”
Med. Eng. Phys.
,
32
(
1
), pp.
76
82
.
10.
Murphy
,
C.
,
Kelliher
,
D.
, and
Davenport
,
J.
,
2012
, “
Shape and Material Characteristics of the Trachea in the Leatherback Sea Turtle Promote Progressive Collapse and Reinflation During Dives
,”
J. Exp. Biol.
,
215
(
Pt. 17
), pp.
3064
3071
.
11.
Costantino
,
M. L.
,
Bagnoli
,
P.
,
Dini
,
G.
,
Fiore
,
G. B.
,
Soncini
,
M.
,
Corno
,
C.
,
Acocella
,
F.
, and
Colombi
,
R.
,
2004
, “
A Numerical and Experimental Study of Compliance and Collapsibility of Preterm Lamb Tracheae
,”
J. Biomech.
,
37
(
12
), pp.
1837
1847
.
12.
Rains
,
J. K.
,
Bert
,
J. L.
,
Roberts
,
C. R.
, and
Paré
,
P. D.
,
1992
, “
Mechanical Properties of Human Tracheal Cartilage
,”
J. Appl. Physiol.
,
72
(
1
), pp.
219
225
.
13.
Bagnoli
,
P.
,
Cozzi
,
B.
,
Zaffora
,
A.
,
Acocella
,
F.
,
Fumero
,
R.
, and
Costantino
,
M. L.
,
2011
, “
Experimental and Computational Biomechanical Characterisation of the Tracheo-Bronchial Tree of the Bottlenose Dolphin (Tursiops Truncatus) During Diving
,”
J. Biomech.
,
44
(
6
), pp.
1040
1045
.
14.
Safshekan
,
F.
,
Tafazzoli-Shadpour
,
M.
,
Abdouss
,
M.
, and
Shadmehr
,
M. B.
,
2016
, “
Mechanical Characterization and Constitutive Modeling of Human Trachea: Age and Gender Dependency
,”
Materials
,
9
(
6
), p.
456
.
15.
Malvè
,
M.
,
del Palomar
,
A. P.
,
Chandra
,
S.
,
López-Villalobos
,
J. L.
,
Finol
,
E. A.
,
Ginel
,
A.
, and
Doblaré
,
M.
,
2011
, “
FSI Analysis of a Human Trachea Before and After Prosthesis Implantation
,”
ASME J. Biomech. Eng.
,
133
(
7
), p.
071003
.
16.
Purslow
,
P. P.
,
Wess
,
T. J.
, and
Hukins
,
D. W.
,
1998
, “
Collagen Orientation and Molecular Spacing During Creep and Stress-Relaxation in Soft Connective Tissues
,”
J. Exp. Biol.
,
201
(
Pt. 1
), pp.
135
142
.http://jeb.biologists.org/content/201/1/135.short
17.
Mak
,
A. F.
,
1986
, “
The Apparent Viscoelastic Behavior of Articular Cartilage—The Contributions From the Intrinsic Matrix Viscoelasticity and Interstitial Fluid Flows
,”
ASME J. Biomech. Eng.
,
108
(
2
), pp.
123
130
.
18.
Lujan
,
T. J.
,
Underwood
,
C. J.
,
Jacobs
,
N. T.
, and
Weiss
,
J. A.
,
2009
, “
Contribution of Glycosaminoglycans to Viscoelastic Tensile Behavior of Human Ligament
,”
J. Appl. Physiol.
,
106
(
2
), pp.
423
431
.
19.
Palacio-Torralba
,
J.
,
Hammer
,
S.
,
Good
,
D. W.
,
Alan McNeill
,
S.
,
Stewart
,
G. D.
,
Reuben
,
R. L.
, and
Chen
,
Y.
,
2015
, “
Quantitative Diagnostics of Soft Tissue Through Viscoelastic Characterization Using Time-Based Instrumented Palpation
,”
J. Mech. Behav. Biomed. Mater.
,
41
, pp.
149
160
.
20.
Cone
,
R. A.
,
2009
, “
Barrier Properties of Mucus
,”
Adv. Drug Delivery Rev.
,
61
(
2
), pp.
75
85
.
21.
Satpathi
,
D. K.
,
Rathish Kumar
,
B. V.
, and
Chandra
,
P.
,
2003
, “
Unsteady-State Laminar Flow of Viscoelastic Gel and Air in a Channel: Application to Mucus Transport in a Cough Machine Simulating Trachea
,”
Math. Comput. Model.
,
38
(
1–2
), pp.
63
75
.
22.
Bansil
,
R.
, and
Turner
,
B. S.
,
2006
, “
Mucin Structure, Aggregation, Physiological Functions and Biomedical Applications
,”
Curr. Opin. Colloid Interface Sci.
,
11
(
2–3
), pp.
164
170
.
23.
Bhutani
,
V. K.
, and
Shaffer
,
T. H.
,
1982
, “
Time-Dependent Tracheal Deformation in Fetal, Neonatal, and Adult Rabbits
,”
Pediatr. Res.
,
16
(
10
), pp.
830
833
.
24.
Aljuri
,
N.
,
Venegas
,
J. G.
, and
Freitag
,
L.
,
2006
, “
Viscoelasticity of the Trachea and Its Effects on Flow Limitation
,”
J. Appl. Physiol.
,
100
(
2
), pp.
384
389
.
25.
Provenzano
,
P. P.
,
Lakes
,
R. S.
,
Corr
,
D. T.
, and
Vanderby
,
R.
, Jr.
,
2002
, “
Application of Nonlinear Viscoelastic Models to Describe Ligament Behavior
,”
Biomech. Model. Mechanobiol.
,
1
(
1
), pp.
45
57
.
26.
Lakes
,
R.
,
2009
,
Viscoelastic Materials
,
1st ed.
,
Cambridge University Press
,
Cambridge, UK
.
27.
Bradshaw
,
R. D.
, and
Brinson
,
L. C.
,
1997
, “
A Sign Control Method for Fitting and Interconverting Material Functions for Linearly Viscoelastic Solids
,”
Mech. Time-Depend. Mater.
,
1
(
1
), pp.
85
108
.
28.
Fung
,
Y. C.
,
1972
, “
Stress Strain History Relations of Soft Tissues in Simple Elongation
,”
Biomechanics, Its Foundations and Objectives
,
Y. C.
Fung
,
N.
Perrone
, and
M.
Anliker
, eds.,
Prentice Hall
,
Englewood Cliffs, NJ
.
29.
Provenzano
,
P.
,
Lakes
,
R.
,
Keenan
,
T.
, and
Vanderby
,
R.
, Jr.
,
2001
, “
Nonlinear Ligament Viscoelasticity
,”
Ann. Biomed. Eng.
,
29
(
10
), pp.
908
914
.
30.
Schapery
,
R.
,
1969
, “
On the Characterization of Nonlinear Viscoelastic Materials
,”
Polym. Eng. Sci.
,
9
(
4
), pp.
295
310
.
31.
Tripathy
,
S.
, and
Berger
,
E. J.
,
2012
, “
Quasi-Linear Viscoelastic Properties of Costal Articular Cartilage
,”
Comput. Methods Biomech. Biomed. Eng.
,
15
(
5
), pp.
475
486
.
32.
Woo
,
S. L.-Y.
,
Simon
,
B. R.
,
Kuei
,
S. C.
, and
Akeson
,
W. H.
,
1980
, “
Quasi-Linear Viscoelastic Properties of Normal Articular Cartilage
,”
ASME J. Biomech. Eng.
,
102
(
2
), pp.
85
90
.
33.
Li
,
L. P.
,
Herzog
,
W.
,
Korhonen
,
R. K.
, and
Jurvelin
,
J. S.
,
2005
, “
The Role of Viscoelasticity of Collagen Fibers in Articular Cartilage: Axial Tension Versus Compression
,”
Med. Eng. Phys.
,
27
(
1
), pp.
51
57
.
34.
Wagg
,
A.
, and
Fry
,
C. H.
,
1999
, “
Visco-Elastic Properties of Isolated Detrusor Smooth Muscle
,”
Scand. J. Urol. Nephrol., Suppl.
,
201
, pp.
12
18
.
35.
Price
,
J. M.
,
Patitucci
,
P.
, and
Fung
,
Y. C.
,
1977
, “
Mechanical Properties of Taenia Coli Smooth Muscle in Spontaneous Contraction
,”
Am. J. Physiol.
,
233
(
1
), pp.
C47
C55
.http://ajpcell.physiology.org/content/233/1/C47.short
36.
Ito
,
S.
,
Majumdar
,
A.
,
Kume
,
H.
,
Shimokata
,
K.
,
Naruse
,
K.
,
Lutchen.
,
K. R.
,
Stamenovic
,
D.
, and
Suki
,
B.
,
2006
, “
Viscoelastic and Dynamic Nonlinear Properties of Airway Smooth Muscle Tissue: Roles of Mechanical Force and the Cytoskeleton
,”
Am. J. Physiol.: Lung Cell. Mol. Physiol.
,
290
(
6
), pp.
L1227
L1237
.
37.
Nemoto
,
T.
,
Kubota
,
R.
,
Murasawa
,
Y.
, and
Isogai
,
Z.
,
2012
, “
Viscoelastic Properties of the Human Dermis and Other Connective Tissues and Its Relevance to Tissue Aging and Aging–Related Disease
,”
Viscoelasticity—From Theory to Biological Applications
,
InTech
,
Rijeka, Croatia
.
38.
Li
,
L. P.
,
Buschmann
,
M. D.
, and
Shirazi-Adl
,
A.
,
2003
, “
Strain-Rate Dependent Stiffness of Articular Cartilage in Unconfined Compression
,”
ASME J. Biomech. Eng.
,
125
(
2
), pp.
161
168
.
39.
Ahsanizadeh
,
S.
, and
Li
,
L.
,
2015
, “
Strain-Rate-Dependent Non-Linear Tensile Properties of the Superficial Zone of Articular Cartilage
,”
Connect. Tissue Res.
,
56
(
6
), pp.
469
476
.
40.
Kusafuka
,
K.
,
Yamaguchi
,
A.
,
Kayano
,
T.
, and
Takemura
,
T.
,
2001
, “
Ossification of Tracheal Cartilage in Aged Humans: A Histological and Immunohistochemical Analysis
,”
J. Bone Miner. Metab.
,
19
(
3
), pp.
168
174
.
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