Interlamellar shear may play an important role in the homeostasis and degeneration of the intervertebral disk. Accurately modeling the shear behavior of the interlamellar compartment would enhance the study of its mechanobiology. In this study, physical experiments were utilized to describe interlamellar shear and define a constitutive model, which was implemented into a finite element analysis. Ovine annulus fibrosus (AF) specimens from three locations within the intervertebral disk (lateral, outer anterior, and inner anterior) were subjected to in vitro mechanical shear testing. The local shear stress–stretch relationship was described for the lamellae and across the interlamellar layer of the AF. A hyperelastic constitutive model was defined for interlamellar and lamellar materials at each location tested. The constitutive models were incorporated into a finite element model of a block of AF, which modeled the interlamellar and lamellar layers using a continuum description. The global shear behavior of the AF was compared between the finite element model and physical experiments. The shear moduli at the initial and final regions of the stress–strain curve were greater within the lamellae than across the interlamellar layer. The difference between interlamellar and lamellar shear was greater at the outer anterior AF than at the inner anterior region. The finite element model was shown to accurately predict the global shear behavior or the AF. Future studies incorporating finite element analysis of the interlamellar compartment may be useful for predicting its physiological mechanical behavior to inform the study of its mechanobiology.

References

1.
Parker
,
S. L.
,
Xu
,
R.
,
McGirt
,
M. J.
,
Witham
,
T. F.
,
Long
,
D. M.
, and
Bydon
A.
,
2010
, “
Long-Term Back Pain After a Single-Level Discectomy for Radiculopathy: Incidence and Health Care Cost Analysis
,”
J. Neurosurg. Spine
,
12
(
2
), pp.
178
182
.10.3171/2009.9.SPINE09410
2.
Sherman
,
J.
,
Cauthen
,
J.
,
Schoenberg
,
D.
,
Burns
,
M.
,
Reaven
,
N. L.
, and
Griffith
,
S. L.
,
2010
, “
Economic Impact of Improving Outcomes of Lumbar Discectomy
,”
Spine J.
,
10
(
2
), pp.
108
116
.10.1016/j.spinee.2009.08.453
3.
Iatridis
,
J. C.
,
Nicoll
,
S. B.
,
Michalek
,
A. J.
,
Walter
,
B. A.
, and
Gupta
,
M. S.
,
2013
, “
Role of Biomechanics in Intervertebral Disc Degeneration and Regenerative Therapies: What Needs Repairing in the Disc and What Are Promising Biomaterials for Its Repair?
Spine J.
,
13
(
3
), pp.
243
262
.10.1016/j.spinee.2012.12.002
4.
Driscoll
,
T. P.
,
Nakasone
,
R. H.
,
Szczesny
,
S. E.
,
Elliott
,
D. M.
, and
Mauck
,
R. L.
,
2013
, “
Biaxial Mechanics and Inter-Lamellar Shearing of Stem-Cell Seeded Electrospun Angle-Ply Laminates for Annulus Fibrosus Tissue Engineering
,”
J. Orthop. Res.
,
31
, pp.
864
870
.10.1002/jor.22312
5.
Bowles
,
R. D.
,
Williams
,
R. M.
,
Zipfel
,
W. R.
, and
Bonassar
,
L. J.
,
2010
, “
Self-Assembly of Aligned Tissue-Engineered Annulus Fibrosus and Intervertebral Disc Composite via Collagen Gel Contraction
,”
Tissue Eng. A
,
16
(
4
), pp.
1339
1348
.10.1089/ten.tea.2009.0442
6.
Yu
,
J.
,
Tirlapur
,
U.
,
Fairbank
,
J.
,
Handford
,
P.
,
Roberts
,
S.
,
Winlove
,
C. P.
,
Cui
,
Z.
, and
Urban
,
J.
,
2007
, “
Microfibrils, Elasin Fibres and Collagen Fibres in the Human Intervertebral Disc and Bovine Tail Disc
,”
J. Anat.
,
210
(
4
), pp.
460
471
.10.1111/j.1469-7580.2007.00707.x
7.
Melrose
,
J.
,
Smaith
,
S. M.
,
Appleyard
,
R. C.
, and
Little
,
C. B.
,
2008
, “
Aggrecan, Versican and Type VI Collagen Are Components of Annular Translamellar Crossbridges in the Intervertebral Disc
,”
Eur. Spine J.
,
17
(
2
), pp.
314
324
.10.1007/s00586-007-0538-0
8.
Bruehlmann
,
S. B.
,
Rattner
,
J. B.
,
Matyas
,
J. R.
, and
Duncan
.
N. A.
,
2002
, “
Regional Variations in the Cellular Matrix of the Annulus Fibrosus of the Intervertebral Disc
,”
J. Anat.
,
201
(
2
), pp.
159
171
.10.1046/j.1469-7580.2002.00080.x
9.
Pezowicz
,
C. A.
,
Robertson
,
P. A.
, and
Broom
,
N. D.
,
2006
, “
The Structural Basis of Interlamellar Cohesion in the Intervertebral Disc Wall
,”
J. Anat.
,
208
, pp.
317
330
.10.1111/j.1469-7580.2006.00536.x
10.
Schollum
,
M. L.
,
Robertson
,
P. A.
, and
Broom
,
N. D.
,
2008
, “
ISSLS Prize Winner: Microstructure and Mechanical Disruption of the Lumbar Disc Annulus: Part I: A Microscopic Investigation of the Translamellar Bridging Network
,”
Spine
,
33
(
25
), pp.
2702
2710
.10.1097/BRS.0b013e31817bb92c
11.
Nerurkar
,
N. L.
,
Baker
,
B. M.
,
Sen
,
S.
,
Wible
,
E. E.
,
Elliott
,
D. M.
, and
Mauck
,
R. L.
,
2009
, “
Nanofibrous Biologic Laminates Replicate the Form and Function of the Annulus Fibrosus
,”
Nat. Mater.
,
8
, pp.
986
992
.10.1038/nmat2558
12.
Nerurkar
,
N. L.
,
Mauck
,
R. L.
, and
Elliott
,
D. M.
,
2011
, “
Modeling Interlamellar Interactions in Angle-Ply Biologic Laminates for Annulus Fibrosus Tissue Engineering
,”
Biomech. Model. Mechanobiol.
,
10
, pp.
973
984
.10.1007/s10237-011-0288-0
13.
Fagan
,
M. J.
,
Julian
,
S.
, and
Mohsen
,
A. M.
, “
Finite Element Analysis in Spine Research
,”
J. Eng. Med.
,
216
(
5
), pp.
281
298
.10.1243/09544110260216568
14.
Galbusera
,
F.
,
Wilke
,
H. J.
,
Brayda-Bruno
,
M.
,
Costa
,
F.
, and
Fornari
,
M.
,
2013
, “
Influence of Sagittal Balance on Spinal Lumbar Loads: A Numerical Approach
,”
Clin. Biomech.
,
28
(
4
), pp.
370
377
.10.1016/j.clinbiomech.2013.02.006
15.
Webster
,
D.
,
Wirth
,
A.
,
van Lenthe
,
G. H.
, and
Muller
,
R.
,
2012
, “
Experimental and Finite Element Analysis of the Mouse Caudal Vertebrae Loading Model: Prediction of Cortical and Trabecular Bone Aadaptation
,”
Biomech. Model. Mechanobiol.
,
11
, pp.
221
230
.10.1007/s10237-011-0305-3
16.
Tchako
,
A.
, and
Sadegh
,
A.
,
2009
, “
A Cervical Spine Model to Predict Injury Scenarios and Clinical Instability
,”
Sports Biomech.
,
8
(
1
), pp.
78
95
.10.1080/14763140802630006
17.
Woldtvedt
,
D. J.
,
Womack
,
W.
,
Gadomski
,
B. C.
,
Schuldt
,
D.
, and
Puttlitz
,
C. M.
,
2011
, “
Finite Element Lumbar Spine Facet Contact Parameter Predictions are Affected by the Cartilage Thickness Distribution and Initial Joint Gap Size
,”
ASME J. Biomech. Eng.
,
133
(
6
), p.
061009
.10.1115/1.4004287
18.
Ayturk
,
U. M.
,
Gadomski
,
B.
,
Schuldt
,
D.
,
Patel
,
V.
, and
Puttlitz
,
C. M.
,
2012
, “
Modeling Degenerative Disk Disease in the Lumbar Spine: A Combined Experimental, Constitutive, and Computational Approach
,”
ASME J. Biomech. Eng.
,
134
(10), p.
101003
.10.1115/1.4007632
19.
Wagner
,
D. R.
, and
Lotz
,
J. C.
,
2004
, “
Theoretical Model and Experimental Results for the Nonlinear Elastic Behavior of Human Annulus Fibrosus
,”
J. Orthop. Res.
,
22
, pp.
901
909
.10.1016/j.orthres.2003.12.012
20.
Guerin
,
H. L.
, and
Elliott
,
D. M.
,
2007
, “
Quantifying the Contributions of Structure to Annulus Fibrosus Mechanical Function Using a Nonlinear, Anisotropic, Hyperelastic Model
,”
J. Orthop. Res.
,
25
, pp.
508
516
.10.1002/jor.20324
21.
Wu, H.-C. and Yao, R.-F., 1976, “Mechanical Behavior of the Human Annulus Fibrosus,” J. Biomech., 9, pp. 1–7.
22.
Costi
,
J. J.
,
Stokes
,
I. A.
,
Gardner-Morse
,
M.
,
Laible
,
J. P.
,
Scoffone
,
H. M.
, and
Iatridis
,
J. C.
,
2007
, “
Direct Measurement of Intervertebral Disc Maximum Shear Strain in Six Degrees of Freedom: Motions That Place Disc Tissue at Risk of Injury
,”
J. Biomech.
,
40
, pp.
2457
2466
.10.1016/j.jbiomech.2006.11.006
23.
Iatridis
,
J. C.
,
Kumar
,
S.
,
Foster
,
R. J.
,
Weidenbaum
,
M.
, and
Mow
,
V. C.
,
1999
, “
Shear Mechanical Properties of Human Lumbar Annulus Fibrosus
,”
J. Orthop. Res.
,
17
, pp.
732
737
.10.1002/jor.1100170517
24.
Gregory
,
D. E.
,
Veldhuis
,
J. H.
,
Horst
,
C.
,
Brodland
,
G. W.
, and
Callaghan
,
J. P.
,
2011
, “
Novel Lap Test Determines the Mechanics of Delamination Between Annular Lamellae of the Intervertebral Disc
,”
J. Biomech.
,
44
, pp.
97
102
.10.1016/j.jbiomech.2010.08.031
25.
Spencer
,
A. J. M.
,
1984
,
Continuum Theory of the Mechanics of Fibre-Reinforced Composites
.
Springer-Verlag
,
New York, NY
.
26.
Michalek
,
A. J.
,
Buckley
,
M. R.
,
Bonassar
,
L. J.
,
Cohen
,
I.
, and
Iatridis
,
J. C.
,
2009
, “
Measurement of Local Strains in Intervertebral Disc Annulus Fibrosus Tissue Under Dynamic Shear: Contributions of Matrix Fiber Orientation and Elastin Content
,”
J. Biomech.
,
42
, pp.
2279
2285
.10.1016/j.jbiomech.2009.06.047
27.
Han
,
W. M.
,
Nernurkar
,
N. L.
,
Smith
,
L. J.
,
Jacobs
,
N. T.
,
Mauck
,
R. L.
, and
Elliott
,
D. M.
,
2012
, “
Multi-Scale Structural and Tensile Mechanical Response of Annulus Fibrosus to Osmotic Loading
,”
Ann. Biomed. Eng.
,
40
(
7
), pp.
1610
1621
.10.1007/s10439-012-0525-4
28.
Romgens
,
A. M.
,
Donkelaar
,
C. C.
, and
Ito
,
K.
,
2013
, “
Contribution of Collagen Fibers to the Compressive Stiffness of Cartilaginous Tissues
,”
Biomech. Model. Mechanobiol
, 12(6), pp. 1221–1231.
29.
Iatridis
,
J. C.
,
MacLean
,
J. J.
,
O'Brien
,
M.
, and
Stokes
, I
. A. F.
,
2007
, “
Measurement of Proteoglycan and Water Content Distribution in Human Lumbar Intervertebral Discs
,”
Spine
,
32
(
14
), pp.
1493
1497
.10.1097/BRS.0b013e318067dd3f
30.
Lyons
,
G.
,
Eisenstein
,
S. M.
, and
Sweet
,
M. B. E.
,
1981
, “
Biochemical Changes in Intervertebral Disc Degeneration
,”
Biochim. Biophys. Acta
,
673
, pp.
443
453
.10.1016/0304-4165(81)90476-1
31.
Reid
,
J. E.
,
Meakin
,
J. R.
,
Robins
,
S. P.
,
Skakle
,
J. M. S.
, and
Hukins
,
D. W. L.
,
2002
, “
Sheep Lumbar Intervertebral Discs as Models for Human Discs
,”
Clin. Biomech.
,
17
, pp.
312
314
.10.1016/S0268-0033(02)00009-8
32.
Schmidt
,
H.
,
Heuer
,
F.
,
Simon
,
U.
,
Kettler
,
A.
,
Rohlmann
,
A.
,
Claes
,
L.
, and
Wilke
,
H. J.
,
2006
, “
Application of a New Calibration Method for a Three-Dimensional Finite Element Model of a Human Lumbar Annulus Fibrosus
,”
Clin. Biomech.
,
21
, pp.
337
344
.10.1016/j.clinbiomech.2005.12.001
33.
Lyons
,
A. S.
,
Sherman
,
B. P.
,
Puttlitz
C. M.
,
Patel
, V
.
V
.
,
Abjornson
,
C.
,
Turner
,
A. S.
,
Seim
,
H. B.
,
Burger
,
E. L.
, and
Lindley
,
E. M.
,
2011
, “
Failure of Resorbable Plates and Screws in an Ovine Model of Anterior Cervical Discectomy and Fusion
,”
Spine J.
,
11
, pp.
876
883
.10.1016/j.spinee.2011.06.016
34.
Huntington
,
C. F.
,
Murrell
,
W. D.
,
Betz
,
R. R.
,
Cole
,
B. A.
,
Clements
,
D. H.
, and
Balsara
,
R. K.
,
1998
, “
Comparison of Thoracoscopic and Open Thoracic Discectomy in a Live Ovine Model for Anterior Spinal Fusion
,”
Spine
,
23
(
15
), pp.
1699
1702
.10.1097/00007632-199808010-00016
35.
Kandziora
,
F.
,
Pflugmacher
,
R.
,
Schafer
,
J.
,
Born
,
C.
,
Duda
,
G.
,
Haas
,
N. P.
, and
Mittlmeier
,
T.
,
2001
, “
Biomechanical Comparison of Cervical Spine Interbody Fusion Cages
,”
Spine
,
26
(
17
), pp.
1850
1857
.10.1097/00007632-200109010-00007
36.
Wilke
,
H. J.
,
Kettler
A.
,
Wenger
,
K. H.
, and
Claes
,
L. E.
,
1997
, “
Anatomy of the Sheep Spine and Its Comparison to the Human Spine
,”
Anat. Rec.
,
247
, pp.
542
555
.10.1002/(SICI)1097-0185(199704)247:4<542::AID-AR13>3.0.CO;2-P
37.
Wilke
,
H. J.
,
Kettler
,
A.
, and
Claes
,
L. E.
,
1997
, “
Are Sheep Spines a Valid Biomechanical Model for Human Spines?
,”
Spine
,
22
(
20
), pp.
2365
2374
.10.1097/00007632-199710150-00009
38.
Bruehlmann
S. B.
,
Matyas
,
J. R.
, and
Duncan
,
N. A.
,
2004
, “
ISSLS Prize Winner: Collagen Fibril Sliding Governs Cell Mechanics in the Anulus Fibrosus
,”
Spine
,
29
(
23
), pp.
2612
2620
.10.1097/01.brs.0000146465.05972.56
39.
Gilbert
,
H. T. J.
,
Hoyland
,
J. A.
,
Freemont
,
A. J.
, and
Millward-Sadler
,
S. J.
,
2011
, “
The Involvement of Interleukin-1 and Interleukin-4 in the Response of Human Annulus Fibrosus Cells to Cyclic Tensile Strain: An Altered Mechanotransduction Pathway With Degeneration
,”
Arthritis Res. Ther.
,
13
(
R8
), pp.
1
13
.10.1186/ar3229
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