Predicting the mechanical behavior of the intervertebral disk (IVD) in health and in disease requires accurate spatial mapping of its compressive mechanical properties. Previous studies confirmed that residual strains in the annulus fibrosus (AF) of the IVD, which result from nonuniform extracellular matrix deposition in response to in vivo loads, vary by anatomical regions (anterior, posterior, and lateral) and zones (inner, middle, and outer). We hypothesized that as the AF is composed of a nonlinear, anisotropic, viscoelastic material, the state of residual strain in the transverse plane would influence the apparent values of axial compressive properties. To test this hypothesis, axial creep indentation tests were performed, using a 1.6 mm spherical probe, at nine different anatomical locations on bovine caudal AFs in both the intact (residual strain present) and strain relieved states. The results showed a shift toward increased spatial homogeneity in all measured parameters, particularly instantaneous strain. This shift was not observed in control AFs, which were tested twice in the intact state. Our results confirm that time-dependent axial compressive properties of the AF are sensitive to the state of residual strain in the transverse plane, to a degree that is likely to affect whole disk behavior.

References

References
1.
Freburger
,
J. K.
,
Holmes
,
G. M.
,
Agans
,
R. P.
,
Jackman
,
A. M.
,
Darter
,
J. D.
,
Wallace
,
A. S.
,
Castel
,
L. D.
,
Kalsbeek
,
W. D.
, and
Carey
,
T. S.
,
2009
, “
The Rising Prevalence of Chronic Low Back Pain
,”
Arch. Intern. Med.
,
169
(
3
), pp.
251
258
.
2.
Masuda
,
K.
,
Aota
,
Y.
,
Muehleman
,
C.
,
Imai
,
Y.
,
Okuma
,
M.
,
Thonar
,
E. J.
,
Andersson
,
G. B.
, and
An
,
H. S.
,
2005
, “
A Novel Rabbit Model of Mild, Reproducible Disc Degeneration by an Anulus Needle Puncture: Correlation Between the Degree of Disc Injury and Radiological and Histological Appearances of Disc Degeneration
,”
Spine
,
30
(
1
), pp.
5
14
.
3.
Kaigle
,
A. M.
,
Holm
,
S. H.
, and
Hansson
,
T. H.
,
1997
, “
1997 Volvo Award Winner in Biomechanical Studies. Kinematic Behavior of the Porcine Lumbar Spine: A Chronic Lesion Model
,”
Spine
,
22
(
24
), pp.
2796
2806
.
4.
Marchand
,
F.
, and
Ahmed
,
A. M.
,
1990
, “
Investigation of the Laminate Structure of Lumbar Disc Anulus Fibrosus
,”
Spine
,
15
(
5
), pp.
402
410
.
5.
Mader
,
K. T.
,
Peeters
,
M.
,
Detiger
,
S. E.
,
Helder
,
M. N.
,
Smit
,
T. H.
,
Le Maitre
,
C. L.
, and
Sammon
,
C.
,
2016
, “
Investigation of Intervertebral Disc Degeneration Using Multivariate FTIR Spectroscopic Imaging
,”
Faraday Discuss.
,
187
, pp.
393
414
.
6.
Perie
,
D.
,
Korda
,
D.
, and
Iatridis
,
J. C.
,
2005
, “
Confined Compression Experiments on Bovine Nucleus Pulposus and Annulus Fibrosus: Sensitivity of the Experiment in the Determination of Compressive Modulus and Hydraulic Permeability
,”
J. Biomech.
,
38
(
11
), pp.
2164
2171
.
7.
Wang
,
P.
,
Yang
,
L.
, and
Hsieh
,
A. H.
,
2011
, “
Nucleus Pulposus Cell Response to Confined and Unconfined Compression Implicates Mechanoregulation by Fluid Shear Stress
,”
Ann. Biomed. Eng.
,
39
(
3
), pp.
1101
1111
.
8.
Recuerda
,
M.
,
Cote
,
S. P.
,
Villemure
,
I.
, and
Perie
,
D.
,
2011
, “
Influence of Experimental Protocols on the Mechanical Properties of the Intervertebral Disc in Unconfined Compression
,”
ASME J. Biomech. Eng.
,
133
(
7
), p.
071006
.
9.
Ellingson
,
A. M.
, and
Nuckley
,
D. J.
,
2012
, “
Intervertebral Disc Viscoelastic Parameters and Residual Mechanics Spatially Quantified Using a Hybrid Confined/In Situ Indentation Method
,”
J. Biomech.
,
45
(
3
), pp.
491
496
.
10.
Umehara
,
S.
,
Tadano
,
S.
,
Abumi
,
K.
,
Katagiri
,
K.
,
Kaneda
,
K.
, and
Ukai
,
T.
,
1996
, “
Effects of Degeneration on the Elastic Modulus Distribution in the Lumbar Intervertebral Disc
,”
Spine
,
21
(
7
), pp.
811
819
.
11.
Vergari
,
C.
,
Rouch
,
P.
,
Dubois
,
G.
,
Bonneau
,
D.
,
Dubousset
,
J.
,
Tanter
,
M.
,
Gennisson
,
J. L.
, and
Skalli
,
W.
,
2014
, “
Non-Invasive Biomechanical Characterization of Intervertebral Discs by Shear Wave Ultrasound Elastography: A Feasibility Study
,”
Eur. Radiol.
,
24
(
12
), pp.
3210
3216
.
12.
Gomez
,
F. S.
,
Lorza
,
R. L.
,
Bobadilla
,
M. C.
, and
Garcia
,
R. E.
,
2017
, “
Improving the Process of Adjusting the Parameters of Finite Element Models of Healthy Human Intervertebral Discs by the Multi-Response Surface Method
,”
Materials
,
10
(
10
), p. E1116.
13.
Newell
,
N.
,
Grigoriadis
,
G.
,
Christou
,
A.
,
Carpanen
,
D.
, and
Masouros
,
S. D.
,
2017
, “
Material Properties of Bovine Intervertebral Discs Across Strain Rates
,”
J. Mech. Behav. Biomed. Mater.
,
65
, pp.
824
830
.
14.
Lee
,
C. H.
,
Landham
,
P. R.
,
Eastell
,
R.
,
Adams
,
M. A.
,
Dolan
,
P.
, and
Yang
,
L.
,
2017
, “
Development and Validation of a Subject-Specific Finite Element Model of the Functional Spinal Unit to Predict Vertebral Strength
,”
Proc. Inst. Mech. Eng. H
,
231
(
9
), pp.
821
830
.
15.
Guo
,
Z.
,
Shi
,
X.
,
Peng
,
X.
, and
Caner
,
F.
,
2012
, “
Fibre-Matrix Interaction in the Human Annulus Fibrosus
,”
J. Mech. Behav. Biomed. Mater.
,
5
(
1
), pp.
193
205
.
16.
Klisch
,
S. M.
, and
Lotz
,
J. C.
,
1999
, “
Application of a Fiber-Reinforced Continuum Theory to Multiple Deformations of the Annulus Fibrosus
,”
J. Biomech.
,
32
(
10
), pp.
1027
1036
.
17.
O'Connell
,
G. D.
,
Sen
,
S.
, and
Elliott
,
D. M.
,
2012
, “
Human Annulus Fibrosus Material Properties From Biaxial Testing and Constitutive Modeling Are Altered With Degeneration
,”
Biomech. Model. Mechanobiol.
,
11
(
3–4
), pp.
493
503
.
18.
Jacobs
,
N. T.
,
Cortes
,
D. H.
,
Peloquin
,
J. M.
,
Vresilovic
,
E. J.
, and
Elliott
,
D. M.
,
2014
, “
Validation and Application of an Intervertebral Disc Finite Element Model Utilizing Independently Constructed Tissue-Level Constitutive Formulations That Are Nonlinear, Anisotropic, and Time-Dependent
,”
J. Biomech.
,
47
(
11
), pp.
2540
2546
.
19.
Laible
,
J. P.
,
Pflaster
,
D. S.
,
Krag
,
M. H.
,
Simon
,
B. R.
, and
Haugh
,
L. D.
,
1993
, “
A Poroelastic-Swelling Finite Element Model With Application to the Intervertebral Disc
,”
Spine
,
18
(
5
), pp.
659
670
.
20.
Schroeder
,
Y.
,
Huyghe
,
J. M.
,
van Donkelaar
,
C. C.
, and
Ito
,
K.
,
2010
, “
A Biochemical/Biophysical 3D FE Intervertebral Disc Model
,”
Biomech. Model. Mechanobiol.
,
9
(
5
), pp.
641
650
.
21.
Duclos
,
S. E.
, and
Michalek
,
A. J.
,
2017
, “
Residual Strains in the Intervertebral Disc Annulus Fibrosus Suggest Complex Tissue Remodeling in Response to In-Vivo Loading
,”
J. Mech. Behav. Biomed. Mater.
,
68
, pp.
232
238
.
22.
Mengoni
,
M.
,
Kayode
,
O.
,
Sikora
,
S. N. F.
,
Zapata-Cornelio
,
F. Y.
,
Gregory
,
D. E.
, and
Wilcox
,
R. K.
,
2017
, “
Annulus Fibrosus Functional Extrafibrillar and Fibrous Mechanical Behaviour: Experimental and Computational Characterisation
,”
R. Soc. Open Sci.
,
4
(
8
), p.
170807
.
23.
Michalek
,
A. J.
,
Gardner-Morse
,
M. G.
, and
Iatridis
,
J. C.
,
2012
, “
Large Residual Strains Are Present in the Intervertebral Disc Annulus Fibrosus in the Unloaded State
,”
J. Biomech.
,
45
(
7
), pp.
1227
1231
.
24.
Athanasiou
,
K. A.
,
Rosenwasser
,
M. P.
,
Buckwalter
,
J. A.
,
Malinin
,
T. I.
, and
Mow
,
V. C.
,
1991
, “
Interspecies Comparisons of In Situ Intrinsic Mechanical Properties of Distal Femoral Cartilage
,”
J. Orthop. Res.
,
9
(
3
), pp.
330
340
.
25.
Moore
,
A. C.
,
DeLucca
,
J. F.
,
Elliott
,
D. M.
, and
Burris
,
D. L.
,
2016
, “
Quantifying Cartilage Contact Modulus, Tension Modulus, and Permeability With Hertzian Biphasic Creep
,”
ASME J. Tribol.
,
138
(
4
), pp.
414051
414057
.
26.
Michalek
,
A. J.
,
Kuxhaus
,
L.
,
Jaremczuk
,
D.
, and
Zaino
,
N. L.
,
2018
, “
Proteoglycans Contribute Locally to Swelling, but Globally to Compressive Mechanics, in Intact Cervine Medial Meniscus
,”
J. Biomech.
,
74
, pp.
86
91
.
27.
Sweigart
,
M. A.
,
Zhu
,
C. F.
,
Burt
,
D. M.
,
DeHoll
,
P. D.
,
Agrawal
,
C. M.
,
Clanton
,
T. O.
, and
Athanasiou
,
K. A.
,
2004
, “
Intraspecies and Interspecies Comparison of the Compressive Properties of the Medial Meniscus
,”
Ann. Biomed. Eng.
,
32
(
11
), pp.
1569
1579
.
28.
Nohava
,
J.
,
Swain
,
M.
,
Lang
,
S. J.
,
Maier
,
P.
,
Heinzelmann
,
S.
,
Reinhard
,
T.
, and
Eberwein
,
P.
,
2018
, “
Instrumented Indentation for Determination of Mechanical Properties of Human Cornea After Ultraviolet-A Crosslinking
,”
J. Biomed. Mater. Res. A
,
106
(
5
), pp.
1413
1420
.
29.
Caner
,
F. C.
,
Guo
,
Z.
,
Moran
,
B.
,
Bazant
,
Z. P.
, and
Carol
,
I.
,
2007
, “
Hyperelastic Anisotropic Microplane Constitutive Model for Annulus Fibrosus
,”
ASME J. Biomech. Eng.
,
129
(
5
), pp.
632
641
.
30.
Hollingsworth
,
N. T.
, and
Wagner
,
D. R.
,
2011
, “
Modeling Shear Behavior of the Annulus Fibrosus
,”
J. Mech. Behav. Biomed. Mater.
,
4
(
7
), pp.
1103
1114
.
31.
Mooney
,
M.
,
1940
, “
A Theory of Large Elastic Deformation
,”
J. Appl. Phys.
,
11
(
9
), pp.
582
592
.
32.
Demers
,
C. N.
,
Antoniou
,
J.
, and
Mwale
,
F.
,
2004
, “
Value and Limitations of Using the Bovine Tail as a Model for the Human Lumbar Spine
,”
Spine
,
29
(
24
), pp.
2793
2799
.
33.
Latridis
,
J. C.
,
Setton
,
L. A.
,
Foster
,
R. J.
,
Rawlins
,
B. A.
,
Weidenbaum
,
M.
, and
Mow
,
V. C.
,
1998
, “
Degeneration Affects the Anisotropic and Nonlinear Behaviors of Human Anulus Fibrosus in Compression
,”
J. Biomech.
,
31
(
6
), pp.
535
544
.
34.
O'Connell
,
G. D.
,
Vresilovic
,
E. J.
, and
Elliott
,
D. M.
,
2007
, “
Comparison of Animals Used in Disc Research to Human Lumbar Disc Geometry
,”
Spine
,
32
(
3
), pp.
328
333
.
35.
Michalek
,
A. J.
, and
Iatridis
,
J. C.
,
2012
, “
Height and Torsional Stiffness Are Most Sensitive to Annular Injury in Large Animal Intervertebral Discs
,”
Spine J.
,
12
(
5
), pp.
425
432
.
36.
Campana
,
S.
,
Charpail
,
E.
,
de Guise
,
J. A.
,
Rillardon
,
L.
,
Skalli
,
W.
, and
Mitton
,
D.
,
2011
, “
Relationships Between Viscoelastic Properties of Lumbar Intervertebral Disc and Degeneration Grade Assessed by MRI
,”
J. Mech. Behav. Biomed. Mater.
,
4
(
4
), pp.
593
599
.
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