Abstract

In light of the correlation between chronic back pain and intervertebral disc (IVD) degeneration, this literature review seeks to illustrate the importance of the hydraulic response across the nucleus pulposus (NP)-annulus fibrosus (AF) interface, by synthesizing current information regarding injurious biomechanics of the spine, stemming from axial compression. Damage to vertebrae, endplates (EPs), the NP, and the AF, can all arise from axial compression, depending on the segment's posture, the manner in which it is loaded, and the physiological state of tissue. Therefore, this movement pattern was selected to illustrate the importance of the bracing effect of a pressurized NP on the AF, and how injuries interrupting support to the AF may contribute to IVD degeneration.

References

1.
Global Burden of Disease Study 2013 Collaborators,
2017
, “
Global, Regional, and National Incidence, Prevalence, and Years Lived With Disability for 328 Diseases and Injuries for 195 Countries, 1990–2016: A Systematic Analysis for the Global Burden of Disease Study 2016
,”
Lancet
,
390
(
10100
), pp.
1211
1259
. 10.1016/S0140-6736(17)32154-2
2.
Global Burden of Disease Study 2013 Collaborators,
2015
, “
Global, Regional, and National Incidence, Prevalence, and Years Lived With Disability for 301 Acute and Chronic Diseases and Injuries in 188 Countries, 1990–2013: A Systematic Analysis for the Global Burden of Disease Study 2013
,”
Lancet
386
(
9995
), pp.
743
800
.10.1016/S0140-6736(15)60692-4
3.
McCann
,
M. R.
, and
Séguin
,
C. A.
,
2016
, “
Notochord Cells in Intervertebral Disc Development and Degeneration
,”
J. Dev. Biol.
,
4
(
1
), p.
3
.10.3390/jdb4010003
4.
Pattappa
,
G.
,
Li
,
Z.
,
Peroglio
,
M.
,
Wismer
,
N.
,
Alini
,
M.
, and
Grad
,
S.
,
2012
, “
Diversity of Intervertebral Disc Cells: Phenotype and Function
,”
J. Anat.
,
221
(
6
), pp.
480
496
.10.1111/j.1469-7580.2012.01521.x
5.
Smith
,
L. J.
,
Nerurkar
,
N. L.
,
Choi
,
K.-S.
,
Harfe
,
B. D.
, and
Elliott
,
D. M.
,
2011
, “
Degeneration and Regeneration of the Intervertebral Disc: Lessons From Development
,”
Dis. Models Mech.
,
4
(
1
), pp.
31
41
. 10.1242/dmm.006403
6.
Risbud
,
M. V.
,
Schaer
,
T. P.
, and
Shapiro
,
I. M.
,
2010
, “
Toward an Understanding of the Role of Notochordal Cells in the Adult Intervertebral Disc: From Discord to Accord
,”
Dev. Dyn.
,
239
(
8
), pp.
2141
2148
.10.1002/dvdy.22350
7.
Boxberger
,
J. I.
,
Orlansky
,
A. S.
,
Sen
,
S.
, and
Elliott
,
D. M.
,
2009
, “
Reduced Nucleus Pulposus Glycosaminoglycan Content Alters Intervertebral Disc Dynamic Viscoelastic Mechanics
,”
J. Biomech.
,
42
(
12
), pp.
1941
1946
.10.1016/j.jbiomech.2009.05.008
8.
Boxberger
,
J. I.
,
Sen
,
S.
,
Yerramalli
,
C. S.
, and
Elliott
,
D. M.
,
2006
, “
Nucleus Pulposus Glycosaminoglycan Content is Correlated With Axial Mechanics in Rat Lumbar Motion Segments
,”
J. Orthop. Res.
,
24
(
9
), pp.
1906
1915
.10.1002/jor.20221
9.
Johannessen
,
W.
, and
Elliott
,
D. M.
,
2005
, “
Effects of Degeneration on the Biphasic Material Properties of Human Nucleus Pulposus in Confined Compression
,”
Spine
,
30
(
24
), pp.
E724
E729
.10.1097/01.brs.0000192236.92867.15
10.
Myers
,
E. R.
, and
Wilson
,
S. E.
,
1997
, “
Biomechanics of Osteoporosis and Vertebral Fracture
,”
Spine
,
22
(
Suppl. 24
), pp.
25S
31S
.10.1097/00007632-199712151-00005
11.
Osterhoff
,
G.
,
Morgan
,
E. F.
,
Shefelbine
,
S. J.
,
Karim
,
L.
,
McNamara
,
L. M.
, and
Augat
,
P.
,
2016
, “
Bone Mechanical Properties and Changes With Osteoporosis
,”
Injury
,
47
, pp.
S11
S20
.10.1016/S0020-1383(16)47003-8
12.
Mc Donnell
,
P.
,
Mc Hugh
,
P. E.
, and
O' Mahoney
,
D.
,
2007
, “
Vertebral Osteoporosis and Trabecular Bone Quality
,”
Ann. Biomed. Eng.
,
35
(
2
), pp.
170
189
.10.1007/s10439-006-9239-9
13.
Ritzel
,
H.
,
Amling
,
M.
,
Pösl
,
M.
,
Hahn
,
M.
, and
Delling
,
G.
,
1997
, “
The Thickness of Human Vertebral Cortical Bone and Its Changes in Aging and Osteoporosis: A Histomorphometric Analysis of the Complete Spinal Column From Thirty-Seven Autopsy Specimens
,”
J. Bone Miner. Res.
,
12
(
1
), pp.
89
95
.10.1359/jbmr.1997.12.1.89
14.
Morton
,
J. J.
,
Bennison
,
M.
,
Brent Lievers
,
W.
,
Waldman
,
S. D.
, and
Pilkey
,
A. K.
,
2018
, “
Failure Behaviour of Rat Vertebrae Determined Through Simultaneous Compression Testing and Micro-CT Imaging
,”
J. Mech. Behav. Biomed. Mater.
,
79
, pp.
73
82
.10.1016/j.jmbbm.2017.11.021
15.
Kennedy
,
O. D.
,
Brennan
,
O.
,
Rackard
,
S. M.
,
O'Brien
,
F. J.
,
Taylor
,
D.
, and
Clive Lee
,
T.
,
2009
, “
Variation of Trabecular Microarchitectural Parameters in Cranial, Caudal and Mid‐Vertebral Regions of the Ovine L3 Vertebra
,”
J. Anat.
,
214
(
5
), pp.
729
735
.10.1111/j.1469-7580.2009.01054.x
16.
Wojnar
,
L. K.
,
Gądek-Moszczak
,
A.
, and
Pietraszek
,
J.
,
2019
, “
On the Role of Histomorphometric (Stereological) Microstructure Parameters in the Prediction of Vertebrae Compression Strength
,”
Image Anal. Stereol.
,
38
(
1
), pp.
63
73
. 10.5566/ias.2028
17.
Ogurkowska
,
M. B.
, and
Błaszczyk
,
A.
,
2018
, “
Variation in Human Vertebral Body Strength for Vertebral Body Samples From Different Locations in Segments L1–L5
,”
Clin. Biomech.
,
60
, pp.
66
75
.10.1016/j.clinbiomech.2018.10.008
18.
Rho
,
Y.-J.
,
Choe
,
W. J.
, and
Chun
,
Y. I.
,
2012
, “
Risk Factors Predicting the New Symptomatic Vertebral Compression Fractures After Percutaneous Vertebroplasty or Kyphoplasty
,”
Eur. Spine J.
,
21
(
5
), pp.
905
911
.10.1007/s00586-011-2099-5
19.
Kim
,
M.-H.
,
Lee
,
A. S.
,
Min
,
S.-H.
, and
Yoon
,
S.-H.
,
2011
, “
Risk Factors of New Compression Fractures in Adjacent Vertebrae After Percutaneous Vertebroplasty
,”
Asian Spine J.
,
5
(
3
), p.
180
10.4184/asj.2011.5.3.180
20.
Roux
,
J.-P.
,
Wegrzyn
,
J.
,
Arlot
,
M. E.
,
Guyen
,
O.
,
Delmas
,
P. D.
,
Chapurlat
,
R.
, and
Bouxsein
,
M. L.
,
2010
, “
Contribution of Trabecular and Cortical Components to Biomechanical Behavior of Human Vertebrae: An Ex Vivo Study
,”
J. Bone Miner. Res.
,
25
(
2
), pp.
356
361
.10.1359/jbmr.090803
21.
Hulme
,
P. A.
,
Boyd
,
S. K.
, and
Ferguson
,
S. J.
,
2007
, “
Regional Variation in Vertebral Bone Morphology and Its Contribution to Vertebral Fracture Strength
,”
Bone
,
41
(
6
), pp.
946
957
.10.1016/j.bone.2007.08.019
22.
Renau
,
A.
,
Farrerons
,
J.
,
Yoldi
,
B.
,
Gil
,
J.
,
Proubasta
,
I.
,
Llauger
,
J.
,
Gonzalez Oliván
,
J.
, and
Planell
,
J.
,
2004
, “
Yield Point in Prediction of Compressive Behavior of Lumbar Vertebral Body by Dual-Energy X-Ray Absorptiometry
,”
J. Clin. Densitom.
,
7
(
4
), pp.
382
389
.10.1385/JCD:7:4:382
23.
Ochia
,
R. S.
,
Tencer
,
A. F.
, and
Ching
,
R. P.
,
2003
, “
Effect of Loading Rate on Endplate and Vertebral Body Strength in Human Lumbar Vertebrae
,”
J. Biomech.
,
36
(
12
), pp.
1875
1881
.10.1016/S0021-9290(03)00211-2
24.
Cheng
,
W.-C.
,
Yang
,
R.-S.
,
Huey-Jen Hsu
,
S.
,
Chieng
,
P.-U.
, and
Tsai
,
K.-S.
,
2001
, “
Effects of Gender and Age Differences on the Distribution of Bone Content in the Third Lumbar Vertebra
,”
Spine
,
26
(
8
), pp.
964
968
.10.1097/00007632-200104150-00023
25.
Huber
,
G.
,
Nagel
,
K.
,
Skrzypiec
,
D. M.
,
Klein
,
A.
,
Püschel
,
K.
, and
Morlock
,
M. M.
,
2016
, “
A Description of Spinal Fatigue Strength
,”
J. Biomech.
,
49
(
6
), pp.
875
880
.10.1016/j.jbiomech.2016.01.041
26.
Fields
,
A. J.
,
Lee
,
G. L.
,
Sherry Liu
,
X.
,
Jekir
,
M. G.
,
Edward Guo
,
X.
, and
Keaveny
,
T. M.
,
2011
, “
Influence of Vertical Trabeculae on the Compressive Strength of the Human Vertebra
,”
J. Bone Miner. Res.
,
26
(
2
), pp.
263
269
.10.1002/jbmr.207
27.
Smit
,
T. H.
,
Odgaard
,
A.
, and
Schneider
,
E.
,
1997
, “
Structure and Function of Vertebral Trabecular Bone
,”
Spine
,
22
(
24
), pp.
2823
2833
.10.1097/00007632-199712150-00005
28.
Wegrzyn
,
J.
,
Roux
,
J.-P.
,
Arlot
,
M. E.
,
Boutroy
,
S.
,
Vilayphiou
,
N.
,
Guyen
,
O.
,
Delmas
,
P. D.
,
Chapurlat
,
R.
, and
Bouxsein
,
M. L.
,
2010
, “
Role of Trabecular Microarchitecture and Its Heterogeneity Parameters in the Mechanical Behavior of Ex Vivo Human L3 Vertebrae
,”
J. Bone Miner. Res.
,
25
(
11
), pp.
2324
2331
.10.1002/jbmr.164
29.
Buckley
,
J. M.
,
Kuo
,
C. C.
,
Cheng
,
L. C.
,
Loo
,
K.
,
Motherway
,
J.
,
Slyfield
,
C.
,
Deviren
,
V.
, and
Ames
,
C.
,
2009
, “
Relative Strength of Thoracic Vertebrae in Axial Compression Versus Flexion
,”
Spine J.
,
9
(
6
), pp.
478
485
.10.1016/j.spinee.2009.02.010
30.
Stokes
,
I. A.
,
1987
, “
Surface Strain on Human Intervertebral Discs
,”
J. Orthop. Res.
,
5
(
3
), pp.
348
355
.10.1002/jor.1100050306
31.
Bachu
,
G. S.
, and
Gordon
,
V. A.
,
1979
, “
Calculation of the Strength of Vertebrae Under Sagittal Compression
,”
Mech. Compos. Mater.
,
15
(
1
), pp.
100
105
.10.1007/BF00604967
32.
Oravec
,
D.
,
Kim
,
W.
,
Flynn
,
M. J.
, and
Yeni
,
Y. N.
,
2018
, “
The Relationship of Whole Human Vertebral Body Creep to Geometric, Microstructural, and Material Properties
,”
J. Biomech.
,
73
, pp.
92
98
.10.1016/j.jbiomech.2018.03.021
33.
Pollintine
,
P.
,
Luo
,
J.
,
Offa-Jones
,
B.
,
Dolan
,
P.
, and
Adams
,
M. A.
,
2009
, “
Bone Creep Can Cause Progressive Vertebral Deformity
,”
Bone
,
45
(
3
), pp.
466
472
.10.1016/j.bone.2009.05.015
34.
MacLean
,
J. J.
,
Owen
,
J. P.
, and
Iatridis
,
J. C.
,
2007
, “
Role of Endplates in Contributing to Compression Behaviors of Motion Segments and Intervertebral Discs
,”
J. Biomech.
,
40
(
1
), pp.
55
63
.10.1016/j.jbiomech.2005.11.013
35.
Yamamoto
,
E.
,
Paul Crawford
,
R.
,
Chan
,
D. D.
, and
Keaveny
,
T. M.
,
2006
, “
Development of Residual Strains in Human Vertebral Trabecular Bone After Prolonged Static and Cyclic Loading at Low Load Levels
,”
J. Biomech.
,
39
(
10
), pp.
1812
1818
.10.1016/j.jbiomech.2005.05.017
36.
Zhao
,
F.-D.
,
Pollintine
,
P.
,
Hole
,
B. D.
,
Adams
,
M. A.
, and
Dolan
,
P.
,
2009
, “
Vertebral Fractures Usually Affect the Cranial Endplate Because It is Thinner and Supported by Less-Dense Trabecular Bone
,”
Bone
,
44
(
2
), pp.
372
379
.10.1016/j.bone.2008.10.048
37.
Jackman
,
T. M.
,
Hussein
,
A. I.
,
Curtiss
,
C.
,
Fein
,
P. M.
,
Camp
,
A.
,
De Barros
,
L.
, and
Morgan
,
E. F.
,
2016
, “
Quantitative, 3D Visualization of the Initiation and Progression of Vertebral Fractures Under Compression and Anterior Flexion
,”
J. Bone Miner. Res.
,
31
(
4
), pp.
777
788
.10.1002/jbmr.2749
38.
Jackman
,
T. M.
,
Hussein
,
A. I.
,
Adams
,
A. M.
,
Makhnejia
,
K. K.
, and
Morgan
,
E. F.
,
2014
, “
Endplate Deflection is a Defining Feature of Vertebral Fracture and is Associated With Properties of the Underlying Trabecular Bone
,”
J. Orthop. Res.
,
32
(
7
), pp.
880
886
.10.1002/jor.22620
39.
Hussein
,
A. I.
,
Jackman
,
T. M.
,
Morgan
,
S. R.
,
Barest
,
G. D.
, and
Morgan
,
E. F.
,
2013
, “
The Intravertebral Distribution of Bone Density: Correspondence to Intervertebral Disc Health and Implications for Vertebral Strength
,”
Osteoporosis Int.
,
24
(
12
), pp.
3021
3030
.10.1007/s00198-013-2417-3
40.
Gunning
,
J. L.
,
Callaghan
,
J. P.
, and
McGill
,
S. M.
,
2001
, “
Spinal Posture and Prior Loading History Modulate Compressive Strength and Type of Failure in the Spine: A Biomechanical Study Using a Porcine Cervical Spine Model
,”
Clin. Biomech.
,
16
(
6
), pp.
471
480
.10.1016/S0268-0033(01)00032-8
41.
Sapiee
,
N. H.
,
Thambyah
,
A.
,
Robertson
,
P. A.
, and
Broom
,
N. D.
,
2019
, “
Sagittal Alignment With Downward Slope of the Lower Lumbar Motion Segment Influences Its Modes of Failure in Direct Compression: A Mechanical and Microstructural Investigation
,”
Spine
,
44
(
16
), pp.
1118
1128
.10.1097/BRS.0000000000003018
42.
Cotterill
,
P. C.
,
Kostuik
,
J. P.
,
Wilson
,
J. A.
,
Fernie
,
G. R.
, and
Maki
,
B. E.
,
1987
, “
Production of a Reproducible Spinal Burst Fracture for Use in Biomechanical Testing
,”
J. Orthop. Res.
,
5
(
3
), pp.
462
465
.10.1002/jor.1100050319
43.
Panjabi
,
M. M.
,
Hoffman
,
H.
,
Kato
,
Y.
, and
Cholewicki
,
J.
,
2000
, “
Superiority of Incremental Trauma Approach in Experimental Burst Fracture Studies
,”
Clin. Biomech.
,
15
(
2
), pp.
73
78
.10.1016/S0268-0033(99)00048-0
44.
Jones
,
H. L.
,
Crawley
,
A. L.
,
Noble
,
P. C.
,
Schoenfeld
,
A. J.
, and
Weiner
,
B. K.
,
2011
, “
A Novel Method for the Reproducible Production of Thoracolumbar Burst Fractures in Human Cadaveric Specimens
,”
Spine J.
,
11
(
5
), pp.
447
451
.10.1016/j.spinee.2011.03.021
45.
Tsai
,
K.-H.
,
Chang
,
G.-L.
, and
Lin
,
R.-M.
,
1997
, “
Differences in Mechanical Response Between Fractured and Non-Fractured Spines Under High-Speed Impact
,”
Clin. Biomech.
,
12
(
7–8
), pp.
445
451
.10.1016/S0268-0033(97)00022-3
46.
Ivancic
,
P. C.
,
2013
, “
Hybrid Cadaveric/Surrogate Model of Thoracolumbar Spine Injury Due to Simulated Fall From Height
,”
Accid. Anal. Prev.
,
59
, pp.
185
191
.10.1016/j.aap.2013.05.024
47.
Parkinson
,
R. J.
, and
Callaghan
,
J. P.
,
2007
, “
Can Periods of Static Loading Be Used to Enhance the Resistance of the Spine to Cumulative Compression?
,”
J. Biomech.
,
40
(
13
), pp.
2944
2952
.10.1016/j.jbiomech.2007.02.007
48.
Germaneau
,
A.
,
M.
,
Saget
,
S.
,
D'Houtaud
,
T.
,
Vandeuvre
,
P.
,
Doumalin
,
J.
-
C.
,
Dupré
,
F.
,
Hesser
,
F.
,
Brémand
,
P.
,
Maxy
,
P.
, and
Rigoard
,
2014
, “
A Novel Experimental Strategy for the Production of Thoracolumbar Burst Fractures Coupled With a Biomechanical Analysis by Using Non-Invasive Optical Methods
,”
Strain
,
50
(
5
), pp.
381
388
.10.1111/str.12079
49.
Keaveny
,
T. M.
,
Wachtel
,
E. F.
, and
Kopperdahl
,
D. L.
,
1999
, “
Mechanical Behavior of Human Trabecular Bone After Overloading
,”
J. Orthop. Res.
,
17
(
3
), pp.
346
353
.10.1002/jor.1100170308
50.
Wilcox
,
R. K.
,
Allen
,
D. J.
,
Hall
,
R. M.
,
Limb
,
D.
,
Barton
,
D. C.
, and
Dickson
,
R. A.
,
2004
, “
A Dynamic Investigation of the Burst Fracture Process Using a Combined Experimental and Finite Element Approach
,”
Eur. Spine J.
,
13
(
6
), pp.
481
488
.10.1007/s00586-003-0625-9
51.
Hongo
,
M.
,
Abe
,
E.
,
Shimada
,
Y.
,
Murai
,
H.
,
Ishikawa
,
N.
, and
Sato
,
K.
,
1999
, “
Surface Strain Distribution on Thoracic and Lumbar Vertebrae Under Axial Compression: The Role in Burst Fractures
,”
Spine
,
24
(
12
), pp.
1197
1202
.10.1097/00007632-199906150-00005
52.
Yang
,
H.
,
Jekir
,
M. G.
,
Davis
,
M. W.
, and
Keaveny
,
T. M.
,
2016
, “
Effective Modulus of the Human Intervertebral Disc and Its Effect on Vertebral Bone Stress
,”
J. Biomech.
,
49
(
7
), pp.
1134
1140
.10.1016/j.jbiomech.2016.02.045
53.
Baranto
,
A.
,
Ekström
,
L.
,
Hellström
,
M.
,
Lundin
,
O.
,
Holm
,
S.
, and
Swärd
,
L.
,
2005
, “
Fracture Patterns of the Adolescent Porcine Spine: An Experimental Loading Study in Bending-Compression
,”
Spine
,
30
(
1
), pp.
75
82
.10.1097/00007632-200501010-00014
54.
Alkalay
,
R. N.
,
Vader
,
D.
, and
Hackney
,
D.
,
2015
, “
The Degenerative State of the Intervertebral Disk Independently Predicts the Failure of Human Lumbar Spine to High Rate Loading: An Experimental Study
,”
Clin. Biomech.
,
30
(
2
), pp.
211
218
.10.1016/j.clinbiomech.2014.09.016
55.
Adams
,
M. A.
,
Pollintine
,
P.
,
Tobias
,
J. H.
,
Wakley
,
G. K.
, and
Dolan
,
P.
,
2006
, “
Intervertebral Disc Degeneration Can Predispose to Anterior Vertebral Fractures in the Thoracolumbar Spine
,”
J. Bone Miner. Res.
,
21
(
9
), pp.
1409
1416
.10.1359/jbmr.060609
56.
Pollintine
,
P.
,
Dolan
,
P.
,
Tobias
,
J. H.
, and
Adams
,
M. A.
,
2004
, “
Intervertebral Disc Degeneration Can Lead to “Stress-Shielding” of the Anterior Vertebral Body: A Cause of Osteoporotic Vertebral Fracture?
,”
Spine
,
29
(
7
), pp.
774
782
.10.1097/01.BRS.0000119401.23006.D2
57.
Fazzalari
,
N. L.
,
Manthey
,
B.
, and
Parkinson
,
I. H.
,
2001
, “
Intervertebral Disc Disorganisation and Its Relationship to Age Adjusted Vertebral Body Morphometry and Vertebral Bone Architecture
,”
Anat. Rec.
,
262
(
3
), pp.
331
339
.10.1002/1097-0185(20010301)262:3<331::AID-AR1044>3.0.CO;2-H
58.
O'Callaghan
,
P.
,
Szarko
,
M.
,
Wang
,
Y.
, and
Luo
,
J.
,
2018
, “
Effects of Bone Damage on Creep Behaviours of Human Vertebral Trabeculae
,”
Bone
,
106
, pp.
204
210
.10.1016/j.bone.2017.10.022
59.
Rodrigues
,
S. A.
,
Wade
,
K. R.
,
Thambyah
,
A.
, and
Broom
,
N. D.
,
2012
, “
Micromechanics of Annulus–End Plate Integration in the Intervertebral Disc
,”
Spine J.
,
12
(
2
), pp.
143
150
.10.1016/j.spinee.2012.01.003
60.
Dudli
,
S.
,
Enns-Bray
,
W.
,
Pauchard
,
Y.
,
Römmeler
,
A.
,
Fields
,
A. J.
,
Ferguson
,
S. J.
, and
Helgason
,
B.
,
2018
, “
Larger Vertebral Endplate Concavities Cause Higher Failure Load and Work at Failure Under High-Rate Impact Loading of Rabbit Spinal Explants
,”
J. Mech. Behav. Biomed. Mater.
,
80
, pp.
104
110
.10.1016/j.jmbbm.2018.01.019
61.
Fields
,
A. J.
,
Lee
,
G. L.
, and
Keaveny
,
T. M.
,
2010
, “
Mechanisms of Initial Endplate Failure in the Human Vertebral Body
,”
J. Biomech.
,
43
(
16
), pp.
3126
3131
.10.1016/j.jbiomech.2010.08.002
62.
Allan
,
D. G.
,
Russell
,
G. G.
,
Moreau
,
M. J.
,
Raso
,
V. J.
, and
Budney
,
D.
,
1990
, “
Vertebral End‐Plate Failure in Porcine‐and Bovine Models of Spinal Fracture Instrumentation
,”
J. Orthop. Res.
,
8
(
1
), pp.
154
156
.10.1002/jor.1100080121
63.
Lundin
,
O.
,
Ekström
,
L.
,
Hellström
,
M.
,
Holm
,
S.
, and
Swärd
,
L.
,
2000
, “
Exposure of the Porcine Spine to Mechanical Compression: Differences in Injury Pattern Between Adolescents and Adults
,”
Eur. Spine J.
,
9
(
6
), pp.
466
471
.10.1007/s005860000164
64.
Yingling
,
V. R.
,
Callaghan
,
J. P.
, and
McGill
,
S. M.
,
1999
, “
The Porcine Cervical Spine as a Model of the Human Lumbar Spine: An Anatomical, Geometric, and Functional Comparison
,”
Clin. Spine Surg.
,
12
(
5
), pp.
415
423
.https://europepmc.org/article/med/10549707
65.
Lundin
,
O.
,
Ekström
,
L.
,
Hellström
,
M.
,
Holm
,
S.
, and
Swärd
,
L.
,
1998
, “
Injuries in the Adolescent Porcine Spine Exposed to Mechanical Compression
,”
Spine
,
23
(
23
), pp.
2574
2579
.10.1097/00007632-199812010-00012
66.
Karlsson
,
L.
,
Lundin
,
O.
,
Ekström
,
L.
,
Hansson
,
T.
, and
Swärd
,
L.
,
1998
, “
Injuries in Adolescent Spine Exposed to Compressive Loads: An Experimental Cadaveric Study
,”
J. Spinal Disord.
,
11
(
6
), pp.
501
507
.10.1097/00002517-199812000-00009
67.
Aufdermaur
,
M.
,
1974
, “
Spinal Injuries in Juveniles: Necropsy Findings in Twelve Cases
,”
J. Bone Jt. Surg., Br.
,
56
(
3
), pp.
513
519
.10.1302/0301-620X.56B3.513
68.
Perey
,
O.
,
1957
, “
Fracture of the Vertebral End-Plate in the Lumbar Spine: An Experimental Biomechanical Investigation
,”
Acta Orthop. Scand.
,
28
(
Suppl. 25
), pp.
1
101
.10.3109/ort.1957.28.suppl-25.01
69.
Brown
,
S. H.
,
Gregory
,
D. E.
, and
McGill
,
S. M.
,
2008
, “
Vertebral End-Plate Fractures as a Result of High Rate Pressure Loading in the Nucleus of the Young Adult Porcine Spine
,”
J. Biomech.
,
41
(
1
), pp.
122
127
.10.1016/j.jbiomech.2007.07.005
70.
Snow
,
C. R.
,
Harvey-Burgess
,
M.
,
Laird
,
B.
,
Brown
,
S. H.
, and
Gregory
,
D. E.
,
2018
, “
Pressure-Induced End-Plate Fracture in the Porcine Spine: Is the Annulus Fibrosus Susceptible to Damage?
,”
Eur. Spine J.
,
27
(
8
), pp.
1767
1774
.10.1007/s00586-017-5428-5
71.
Fields
,
A. J.
,
Ballatori
,
A.
,
Liebenberg
,
E. C.
, and
Lotz
,
J. C.
,
2018
, “
Contribution of the Endplates to Disc Degeneration
,”
Curr. Mol. Biol. Rep.
,
4
(
4
), pp.
151
160
.10.1007/s40610-018-0105-y
72.
Teraguchi
,
M.
,
Yoshimura
,
N.
,
Hashizume
,
H.
,
Muraki
,
S.
,
Yamada
,
H.
,
Oka
,
H.
,
Minamide
,
A.
,
Nakagawa
,
H.
,
Ishimoto
,
Y.
,
Nagata
,
K.
,
Kagotani
,
R.
,
Tanaka
,
S.
,
Kawaguchi
,
H.
,
Nakamura
,
K.
,
Akune
,
T.
, and
Yoshida
,
M.
,.
2015
, “
The Association of Combination of Disc Degeneration, End Plate Signal Change, and Schmorl Node With Low Back Pain in a Large Population Study: The Wakayama Spine Study
,”
Spine J.
,
15
(
4
), pp.
622
628
.10.1016/j.spinee.2014.11.012
73.
Dudli
,
S.
,
Haschtmann
,
D.
, and
Ferguson
,
S. J.
,
2012
, “
Fracture of the Vertebral Endplates, but Not Equienergetic Impact Load, Promotes Disc Degeneration In Vitro
,”
J. Orthop. Res.
,
30
(
5
), pp.
809
816
.10.1002/jor.21573
74.
Wang
,
Y.
,
Videman
,
T.
, and
Battié
,
M. C.
,
2012
, “
ISSLS Prize Winner: Lumbar Vertebral Endplate Lesions Associations With Disc Degeneration and Back Pain History
,”
Spine
,
37
(
17
), pp.
1490
1496
.10.1097/BRS.0b013e3182608ac4
75.
Hadjipavlou
,
A. G.
,
Tzermiadianos
,
M. N.
,
Bogduk
,
N.
, and
Zindrick
,
M. R.
,
2008
, “
The Pathophysiology of Disc Degeneration: A Critical Review
,”
J. Bone Jt. Surg., Br.
,
90
(
10
), pp.
1261
1270
.10.1302/0301-620X.90B10.20910
76.
Adams
,
M. A.
,
Freeman
,
B. J.
,
Morrison
,
H. P.
,
Nelson
,
I. W.
, and
Dolan
,
P.
,
2000
, “
Mechanical Initiation of Intervertebral Disc Degeneration
,”
Spine
,
25
(
13
), pp.
1625
1636
.10.1097/00007632-200007010-00005
77.
Przybyla
,
A.
,
Pollintine
,
P.
,
Bedzinski
,
R.
, and
Adams
,
M. A.
,
2006
, “
Outer Annulus Tears Have Less Effect Than Endplate Fracture on Stress Distributions Inside Intervertebral Discs: Relevance to Disc Degeneration
,”
Clin. Biomech.
,
21
(
10
), pp.
1013
1019
.10.1016/j.clinbiomech.2006.07.003
78.
Pye
,
S. R.
,
Reid
,
D. M.
,
Lunt
,
M.
,
Adams
,
J. E.
,
Silman
,
A. J.
, and
O'Neill
,
T. W.
,
2007
, “
Lumbar Disc Degeneration: Association Between Osteophytes, End-Plate Sclerosis and Disc Space Narrowing
,”
Ann. Rheum. Dis.
,
66
(
3
), pp.
330
333
.10.1136/ard.2006.052522
79.
Malandrino
,
A.
,
Noailly
,
J.
, and
Lacroix
,
D.
,
2014
, “
Numerical Exploration of the Combined Effect of Nutrient Supply, Tissue Condition and Deformation in the Intervertebral Disc
,”
J. Biomech.
,
47
(
6
), pp.
1520
1525
.10.1016/j.jbiomech.2014.02.004
80.
Arpinar
,
V. E.
,
Rand
,
S. D.
,
Klein
,
A. P.
,
Maiman
,
D. J.
, and
Tugan Muftuler
,
L.
,
2015
, “
Changes in Perfusion and Diffusion in the Endplate Regions of Degenerating Intervertebral Discs: A DCE-MRI Study
,”
Eur. Spine J.
,
24
(
11
), pp.
2458
2467
.10.1007/s00586-015-4172-y
81.
Rodriguez
,
A. G.
,
Rodriguez‐Soto
,
A. E.
,
Burghardt
,
A. J.
,
Berven
,
S.
,
Majumdar
,
S.
, and
Lotz
,
J. C.
,
2012
, “
Morphology of the Human Vertebral Endplate
,”
J. Orthop. Res.
,
30
(
2
), pp.
280
287
.10.1002/jor.21513
82.
Roberts
,
S.
,
Urban
,
J. P.
,
Evans
,
H.
, and
Eisenstein
,
S. M.
,
1996
, “
Transport Properties of the Human Cartilage Endplate in Relation to Its Composition and Calcification
,”
Spine
,
21
(
4
), pp.
415
420
.10.1097/00007632-199602150-00003
83.
Kim
,
K.-W.
,
Lim
,
T.-H.
,
Kim
,
J. G.
,
Jeong
,
S.-T.
,
Masuda
,
K.
, and
An
,
H. S.
,
2003
, “
The Origin of Chondrocytes in the Nucleus Pulposus and Histologic Findings Associated With the Transition of a Notochordal Nucleus Pulposus to a Fibrocartilaginous Nucleus Pulposus in Intact Rabbit Intervertebral Discs
,”
Spine
,
28
(
10
), pp.
982
990
.10.1097/01.BRS.0000061986.03886.4F
84.
Kim
,
K.-W.
,
Ha
,
K.-Y.
,
Park
,
J.-B.
,
Woo
,
Y.-K.
,
Chung
,
H.-N.
, and
An
,
H. S.
,
2005
, “
Expressions of Membrane-Type I Matrix Metalloproteinase, Ki-67 Protein, and Type II Collagen by Chondrocytes Migrating From Cartilage Endplate Into Nucleus Pulposus in Rat Intervertebral Discs: A Cartilage Endplate-Fracture Model Using an Intervertebral Disc Organ Culture
,”
Spine
,
30
(
12
), pp.
1373
1378
. 10.1097/01.brs.0000166155.48168.0e
85.
Kim
,
K.-W.
,
Ha
,
K.-Y.
,
Lee
,
J.-S.
,
Nam
,
S.-W.
,
Woo
,
Y.-K.
,
Lim
,
T.-H.
, and
An
,
H. S.
,
2009
, “
Notochordal Cells Stimulate Migration of Cartilage End Plate Chondrocytes of the Intervertebral Disc in In Vitro Cell Migration Assays
,”
Spine J.
,
9
(
4
), pp.
323
329
.10.1016/j.spinee.2008.05.003
86.
Morales
,
T. I.
,
2007
, “
Chondrocyte Moves: Clever Strategies?
,”
Osteoarthritis Cartilage
,
15
(
8
), pp.
861
871
.10.1016/j.joca.2007.02.022
87.
Dudli
,
S.
,
Ferguson
,
S. J.
, and
Haschtmann
,
D.
,
2014
, “
Severity and Pattern of Post-Traumatic Intervertebral Disc Degeneration Depend on the Type of Injury
,”
Spine J.
,
14
(
7
), pp.
1256
1264
.10.1016/j.spinee.2013.07.488
88.
Urban
,
J. P. G.
,
Roberts
,
S.
, and
Ralphs
,
J. R.
,
2000
, “
The Nucleus of the Intervertebral Disc From Development to Degeneration
,”
Am. Zool.
,
40
(
1
), pp.
53
61
.10.1093/icb/40.1.53
89.
Iatridis
,
J. C.
,
Setton
,
L. A.
,
Weidenbaum
,
M.
, and
Mow
,
V. C.
,
1997
, “
Alterations in the Mechanical Behavior of the Human Lumbar Nucleus Pulposus With Degeneration and Aging
,”
J. Orthop. Res.
,
15
(
2
), pp.
318
322
.10.1002/jor.1100150224
90.
Adams
,
M. A.
,
McNally
,
D. S.
, and
Dolan
,
P.
,
1996
, “
Stress' Distributions Inside Intervertebral Discs: The Effects of Age and Degeneration
,”
J. Bone Jt. Surg., Br.
,
78
(
6
), pp.
965
972
.10.1302/0301-620X.78B6.0780965
91.
Antoniou
,
J.
,
Steffen
,
T.
,
Nelson
,
F.
,
Winterbottom
,
N.
,
Hollander
,
A. P.
,
Poole
,
R. A.
,
Aebi
,
M.
, and
Alini
,
M.
,
1996
, “
The Human Lumbar Intervertebral Disc: Evidence for Changes in the Biosynthesis and Denaturation of the Extracellular Matrix With Growth, Maturation, Ageing, and Degeneration
,”
J. Clin. Invest.
,
98
(
4
), pp.
996
1003
.10.1172/JCI118884
92.
Osti
,
O. L.
,
Vernon-Roberts
,
B.
,
Moore
,
R.
, and
Fraser
,
R. D.
,
1992
, “
Annular Tears and Disc Degeneration in the Lumbar Spine. A Post-Mortem Study of 135 Discs
,”
J. Bone Jt. Surg., Br.
,
74
(
5
), pp.
678
682
.10.1302/0301-620X.74B5.1388173
93.
Sive
,
J. I.
,
Baird
,
P.
,
Jeziorsk
,
M.
,
Watkins
,
A.
,
Hoyland
,
J. A.
, and
Freemont
,
A. J.
,
2002
, “
Expression of Chondrocyte Markers by Cells of Normal and Degenerate Intervertebral Discs
,”
Mol. Pathol.
,
55
(
2
), pp.
91
97
.10.1136/mp.55.2.91
94.
Iatridis
,
J. C.
,
Weidenbaum
,
M.
,
Setton
,
L. A.
, and
Mow
,
V. C.
,
1996
, “
Is the Nucleus Pulposus a Solid or a Fluid? Mechanical Behaviors of the Nucleus Pulposus of the Human Intervertebral Disc
,”
Spine
,
21
(
10
), pp.
1174
1184
.10.1097/00007632-199605150-00009
95.
Wang
,
F.
,
Zhang
,
C.
,
Sinkemani
,
A.
,
Shi
,
R.
,
Xie
,
Z.-Y.
,
Chen
,
L.
,
Mao
,
L.
, and
Wu
,
X.-T.
,
2019
, “
A Histocytological and Radiological Overview of the Natural History of Intervertebral Disk: From Embryonic Formation to Age-Related Degeneration
,”
Eur. Spine J.
,
28
(
4
), pp.
633
648
.10.1007/s00586-019-05903-8
96.
Risbud
,
M. V.
, and
Shapiro
,
I. M.
,
2011
, “
Notochordal Cells in the Adult Intervertebral Disc: New Perspective on an Old Question
,”
Crit. Rev. Eukaryotic Gene Expression
,
21
(
1
), pp.
29
41
.10.1615/CritRevEukarGeneExpr.v21.i1.30
97.
McCann
,
M. R.
,
Tamplin
,
O. J.
,
Rossant
,
J.
, and
Séguin
,
C. A.
,
2012
, “
Tracing Notochord-Derived Cells Using a Noto-Cre Mouse: Implications for Intervertebral Disc Development
,”
Dis. Models Mech.
,
5
(
1
), pp.
73
82
. 10.1242/dmm.008128
98.
Kerr
,
G. J.
,
Veras
,
M. A.
,
Kim
,
M. K. M.
, and
Séguin
,
C. A.
,
2017
, “
Decoding the Intervertebral Disc: Unravelling the Complexities of Cell Phenotypes and Pathways Associated With Degeneration and Mechanotransduction
,”
Seminars in Cell & Developmental Biology
, Vol.
62
,
Academic Press
,
Cambridge, MA
, pp.
94
103
.
99.
Bedore
,
J.
,
Leask
,
A.
, and
Séguin
,
C. A.
,
2014
, “
Targeting the Extracellular Matrix: Matricellular Proteins Regulate Cell–Extracellular Matrix Communication Within Distinct Niches of the Intervertebral Disc
,”
Matrix Biol.
,
37
, pp.
124
130
.10.1016/j.matbio.2014.05.005
100.
Poiraudeau
,
S.
,
Monteiro
,
I.
,
Anract
,
P.
,
Blanchard
,
O.
,
Revel
,
M.
, and
Corvol
,
M. T.
,
1999
, “
Phenotypic Characteristics of Rabbit Intervertebral Disc Cells: Comparison With Cartilage Cells From the Same Animals
,”
Spine
,
24
(
9
), pp.
837
844
.10.1097/00007632-199905010-00002
101.
Hunter
,
C. J.
,
Bianchi
,
S.
,
Cheng
,
P.
, and
Muldrew
,
K.
,
2007
, “
Osmoregulatory Function of Large Vacuoles Found in Notochordal Cells of the Intervertebral Disc
,”
Mol. Cell. Biomech.
,
4
(
4
), pp.
227
237
.https://pubmed.ncbi.nlm.nih.gov/18437919/
102.
Alini
,
M.
,
Eisenstein
,
S. M.
,
Ito
,
K.
,
Little
,
C.
,
Annette Kettler
,
A.
,
Masuda
,
K.
,
Melrose
,
J.
,
Ralphs
,
J.
,
Stokes
,
I.
, and
Wilke
,
H. J.
,
2008
, “
Are Animal Models Useful for Studying Human Disc Disorders/Degeneration?
,”
Eur. Spine J.
,
17
(
1
), pp.
2
19
.10.1007/s00586-007-0414-y
103.
Hunter
,
C. J.
,
Matyas
,
J. R.
, and
Duncan
,
N. A.
,
2004
, “
Cytomorphology of Notochordal and Chondrocytic Cells From the Nucleus Pulposus: A Species Comparison
,”
J. Anat.
,
205
(
5
), pp.
357
362
.10.1111/j.0021-8782.2004.00352.x
104.
Hunter
,
C. J.
,
Matyas
,
J. R.
, and
Duncan
,
N. A.
,
2003
, “
The Notochordal Cell in the Nucleus Pulposus: A Review in the Context of Tissue Engineering
,”
Tissue Eng.
,
9
(
4
), pp.
667
677
.10.1089/107632703768247368
105.
Malko
,
J. A.
,
Hutton
,
W. C.
, and
Fajman
,
W. A.
,
1999
, “
An In Vivo Magnetic Resonance Imaging Study of Changes in the Volume (and Fluid Content) of the Lumbar Intervertebral Discs During a Simulated Diurnal Load Cycle
,”
Spine
,
24
(
10
), pp.
1015
1022
.10.1097/00007632-199905150-00016
106.
Kingsley
,
M. I.
,
D'Silva
,
L. A.
,
Jennings
,
C.
,
Humphries
,
B.
,
Dalbo
,
V. J.
, and
Scanlan
,
A. T.
,
2012
, “
Moderate-Intensity Running Causes Intervertebral Disc Compression in Young Adults
,”
Med. Sci. Sports Exercise
,
44
(
11
), pp.
2199
204
.10.1249/MSS.0b013e318260dbc1
107.
Ahrens
,
S. F.
,
1994
, “
The Effect of Age on Intervertebral Disc Compression During Running
,”
J. Orthop. Sports Phys. Ther.
,
20
(
1
), pp.
17
21
.10.2519/jospt.1994.20.1.17
108.
Carrigg
,
S. Y.
, and
Hillemeyer
,
L. E.
,
1992
, “
The Effect of Running-Induced Intervertebral Disc Compression on Thoracolumbar Vertebral Column Mobility in Young, Healthy Males
,”
J. Orthop. Sports Phys. Ther.
,
16
(
1
), pp.
19
24
.10.2519/jospt.1992.16.1.19
109.
Ghiss
,
M.
,
Giannesini
,
B.
,
Tropiano
,
P.
,
Tourki
,
Z.
, and
Boiron
,
O.
,
2016
, “
Quantitative MRI Water Content Mapping of Porcine Intervertebral Disc During Uniaxial Compression
,”
Comput. Methods Biomech. Biomed. Eng.
,
19
(
10
), pp.
1079
1088
.10.1080/10255842.2015.1101072
110.
Velísková
,
P.
,
Bashkuev
,
M.
,
Shirazi-Adl
,
A.
, and
Schmidt
,
H.
,
2018
, “
Computational Study of the Role of Fluid Content and Flow on the Lumbar Disc Response in Cyclic Compression: Replication of In Vitro and In Vivo Conditions
,”
J. Biomech.
,
70
, pp.
16
25
.10.1016/j.jbiomech.2017.10.032
111.
Schmidt
,
H.
,
Shirazi-Adl
,
A.
,
Schilling
,
C.
, and
Dreischarf
,
M.
,
2016
, “
Preload Substantially Influences the Intervertebral Disc Stiffness in Loading–Unloading Cycles of Compression
,”
J. Biomech.
,
49
(
9
), pp.
1926
1932
.10.1016/j.jbiomech.2016.05.006
112.
van der Veen
,
A. J.
,
Mullender
,
M. G.
,
Kingma
,
I.
,
van
,
J. H.
, and
Smit
,
T. H.
,.
2008
, “
Contribution of Vertebral Bodies, Endplates, and Intervertebral Discs to the Compression Creep of Spinal Motion Segments
,”
J. Biomech.
,
41
(
6
), pp.
1260
1268
.10.1016/j.jbiomech.2008.01.010
113.
Ménard
,
A. ‐L.
,
Grimard
,
G.
,
Massol
,
E.
,
Londono
,
I.
,
Moldovan
,
F.
, and
Villemure
,
I.
,
2016
, “
Static and Dynamic Compression Application and Removal on the Intervertebral Discs of Growing Rats
,”
J. Orthop. Res.
,
34
(
2
), pp.
290
298
.10.1002/jor.22991
114.
Stokes
,
I. A.
,
McBride
,
C.
,
Aronsson
,
D. D.
, and
Roughley
,
P. J.
,
2011
, “
Intervertebral Disc Changes With Angulation, Compression and Reduced Mobility Simulating Altered Mechanical Environment in Scoliosis
,”
Eur. Spine J.
,
20
(
10
), pp.
1735
1744
.10.1007/s00586-011-1868-5
115.
Nakamura
,
T.
,
Iribe
,
T.
,
Asou
,
Y.
,
Miyairi
,
H.
,
Ikegami
,
K.
, and
Takakuda
,
K.
,
2009
, “
Effects of Compressive Loading on Biomechanical Properties of Disc and Peripheral Tissue in a Rat Tail Model
,”
Eur. Spine J.
,
18
(
11
), pp.
1595
1603
.10.1007/s00586-009-1078-6
116.
Lotz
,
J. C.
, and
Chin
,
J. R.
,
2000
, “
Intervertebral Disc Cell Death is Dependent on the Magnitude and Duration of Spinal Loading
,”
Spine
,
25
(
12
), pp.
1477
1483
.10.1097/00007632-200006150-00005
117.
Iatridis
,
J. C.
,
Mente
,
P. L.
,
Stokes
,
I. A.
,
Aronsson
,
D. D.
, and
Alini
,
M.
,
1999
, “
Compression-Induced Changes in Intervertebral Disc Properties in a Rat Tail Model
,”
Spine
,
24
(
10
), pp.
996
1002
.10.1097/00007632-199905150-00013
118.
Ching
,
C. T.
,
Chow
,
D. H.
,
Yao
,
F. Y.
, and
Holmes
,
A. D.
,
2003
, “
The Effect of Cyclic Compression on the Mechanical Properties of the Inter-Vertebral Disc: An In Vivo Study in a Rat Tail Model
,”
Clin. Biomech.
,
18
(
3
), pp.
182
189
.10.1016/S0268-0033(02)00188-2
119.
Ching
,
C. T.
,
Chow
,
D. H.
,
Yao
,
F. Y.
, and
Holmes
,
A. D.
,
2004
, “
Changes in Nuclear Composition Following Cyclic Compression of the Intervertebral Disc in an In Vivo Rat-Tail Model
,”
Med. Eng. Phys.
,
26
(
7
), pp.
587
594
. 10.1016/j.medengphy.2004.03.006
120.
MacLean
,
J. J.
,
Lee
,
C. R.
,
Alini
,
M.
, and
Iatridis
,
J. C.
,
2004
, “
Anabolic and Catabolic mRNA Levels of the Intervertebral Disc Vary With the Magnitude and Frequency of In Vivo Dynamic Compression
,”
J. Orthop. Res.
,
22
(
6
), pp.
1193
1200
.10.1016/j.orthres.2004.04.004
121.
MacLean
,
J. J.
,
Lee
,
C. R.
,
Grad
,
S.
,
Ito
,
K.
,
Alini
,
M.
, and
Iatridis
,
J. C.
,
2003
, “
Effects of Immobilization and Dynamic Compression on Intervertebral Disc Cell Gene Expression In Vivo
,”
Spine
,
28
(
10
), pp.
973
981
.10.1097/01.BRS.0000061985.15849.A9
122.
Wuertz
,
K.
,
Godburn
,
K.
,
MacLean
,
J. J.
,
Barbir
,
A.
,
Donnelly
,
J. S.
,
Roughley
,
P. J.
,
Alini
,
M.
, and
Iatridis
,
J. C.
,
2009
, “
In Vivo Remodeling of Intervertebral Discs in Response to Short‐and Long‐Term Dynamic Compression
,”
J. Orthop. Res.
,
27
(
9
), pp.
1235
1242
.10.1002/jor.20867
123.
MacLean
,
J. J.
,
Lee
,
C. R.
,
Alini
,
M.
, and
Iatridis
,
J. C.
,
2005
, “
The Effects of Short‐Term Load Duration on Anabolic and Catabolic Gene Expression in the Rat Tail Intervertebral Disc
,”
J. Orthop. Res.
,
23
(
5
), pp.
1120
1127
.10.1016/j.orthres.2005.01.020
124.
Iatridis
,
J. C.
,
MacLean
,
J. J.
,
Roughley
,
P. J.
, and
Alini
,
M.
,
2006
, “
Effects of Mechanical Loading on Intervertebral Disc Metabolism In Vivo
,”
J. Bone Jt. Surg.
,
88
(
2
), p.
41
46
.10.2106/JBJS.E.01407
125.
Yan
,
Z.
,
Pan
,
Y.
,
Wang
,
S.
,
Cheng
,
M.
,
Kong
,
H.
,
Sun
,
C.
,
Hu
,
K.
,
Chen
,
T.
,
Dong
,
Q.
, and
Chen
,
J.
,
2017
, “
Static Compression Induces ECM Remodeling and Integrin α2β1 Expression and Signaling in a Rat Tail Caudal Intervertebral Disc Degeneration Model
,”
Spine
,
42
(
8
), pp.
E448
E458
.10.1097/BRS.0000000000001856
126.
Gao
,
X.
,
Zhu
,
Q.
, and
Gu
,
W.
,
2016
, “
Prediction of Glycosaminoglycan Synthesis in Intervertebral Disc Under Mechanical Loading
,”
J. Biomech.
,
49
(
13
), pp.
2655
2661
.10.1016/j.jbiomech.2016.05.028
127.
Korecki
,
C. L.
,
MacLean
,
J. J.
, and
Iatridis
,
J. C.
,
2008
, “
Dynamic Compression Effects on Intervertebral Disc Mechanics and Biology
,”
Spine
,
33
(
13
), pp.
1403
1409
.10.1097/BRS.0b013e318175cae7
128.
Wang
,
D.-L.
,
Jiang
,
S.-D.
, and
Dai
,
L.-Y.
,
2007
, “
Biologic Response of the Intervertebral Disc to Static and Dynamic Compression In Vitro
,”
Spine
,
32
(
23
), pp.
2521
2528
.10.1097/BRS.0b013e318158cb61
129.
Hutton
,
W. C.
,
Elmer
,
W. A.
,
Boden
,
S. D.
,
Hyon
,
S.
,
Toribatake
,
Y.
,
Tomita
,
K.
, and
Hair
,
G. A.
,
1999
, “
The Effect of Hydrostatic Pressure on Intervertebral Disc Metabolism
,”
Spine
,
24
(
15
), pp.
1507
1515
.10.1097/00007632-199908010-00002
130.
Handa
,
T.
,
Ishihara
,
H.
,
Ohshima
,
H.
,
Osada
,
R.
,
Tsuji
,
H.
, and
Obata
,
K.
,
1997
, “
Effects of Hydrostatic Pressure on Matrix Synthesis and Matrix Metalloproteinase Production in the Human Lumbar Intervertebral Disc
,”
Spine
,
22
(
10
), pp.
1085
1091
.10.1097/00007632-199705150-00006
131.
Zhu
,
L.-G.
,
Feng
,
M.-S.
,
Zhan
,
J.-W.
,
Zhang
,
P.
, and
Yu
,
J.
,
2016
, “
Effect of Static Load on the Nucleus Pulposus of Rabbit Intervertebral Disc Motion Segment in Ex Vivo Organ Culture
,”
Chin. Med. J.
,
129
(
19
), p.
2338
.10.4103/0366-6999.190666
132.
Kasra
,
M.
,
Goel
,
V.
,
Martin
,
J.
,
Wang
,
S.‐T.
,
Choi
,
W.
, and
Buckwalter
,
J.
,
2003
, “
Effect of Dynamic Hydrostatic Pressure on Rabbit Intervertebral Disc Cells
,”
J. Orthop. Res.
,
21
(
4
), pp.
597
603
.10.1016/S0736-0266(03)00027-5
133.
Hutton
,
W. C.
,
Elmer
,
W. A.
,
Bryce
,
L. M.
,
Kozlowska
,
E. E.
,
Boden
,
S. D.
, and
Kozlowski
,
M.
,
2001
, “
Do the Intervertebral Disc Cells Respond to Different Levels of Hydrostatic Pressure?
,”
Clin. Biomech.
,
16
(
9
), pp.
728
734
.10.1016/S0268-0033(01)00080-8
134.
Ishihara
,
H.
,
McNally
,
D. S.
,
Urban
,
J. P.
, and
Hall
,
A. C.
,
1996
, “
Effects of Hydrostatic Pressure on Matrix Synthesis in Different Regions of the Intervertebral Disk
,”
J. Appl. Physiol.
,
80
(
3
), pp.
839
846
.10.1152/jappl.1996.80.3.839
135.
Chen
,
J.
,
Yan
,
W.
, and
Setton
,
L. A.
,
2004
, “
Static Compression Induces Zonal-Specific Changes in Gene Expression for Extracellular Matrix and Cytoskeletal Proteins in Intervertebral Disc Cells In Vitro
,”
Matrix Biol.
,
22
(
7
), pp.
573
583
.10.1016/j.matbio.2003.11.008
136.
Chen
,
S.
,
Lv
,
X.
,
Hu
,
B.
,
Shao
,
Z.
,
Wang
,
B.
,
Ma
,
K.
,
Lin
,
H.
, and
Cui
,
M.
,
2017
, “
RIPK1/RIPK3/MLKL-Mediated Necroptosis Contributes to Compression-Induced Rat Nucleus Pulposus Cells Death
,”
Apoptosis
,
22
(
5
), pp.
626
638
.10.1007/s10495-017-1358-2
137.
Ma
,
K.-G.
,
Shao
,
Z.-W.
,
Yang
,
S.-H.
,
Wang
,
J.
,
Wang
,
B.-C.
,
Xiong
,
L.-M.
,
Wu
,
Q.
, and
Chen
,
S.-F.
,
2013
, “
Autophagy is Activated in Compression-Induced Cell Degeneration and is Mediated by Reactive Oxygen Species in Nucleus Pulposus Cells Exposed to Compression
,”
Osteoarthritis Cartilage
,
21
(
12
), pp.
2030
2038
.10.1016/j.joca.2013.10.002
138.
Farrell
,
M.
, and
Riches
,
P.
,
2012
, “
The Poisson's Ratio of the Nucleus Pulposus is Strain Dependent
,”
18th Congress of the European Society of Biomechanics
, Lisbon, Portugal, July
1
4
.10.1016/S0021-9290(12)70567-5
139.
Klein
,
J. A.
,
Hickey
,
D. S.
, and
Hukins
,
D. W. L.
,
1983
, “
Radial Bulging of the Annulus Fibrosus During Compression of the Intervertebral Disc
,”
J. Biomech.
,
16
(
3
), pp.
211
217
.10.1016/0021-9290(83)90128-8
140.
Li
,
J.
,
Liu
,
C.
,
Guo
,
Q.
,
Yang
,
H.
, and
Li
,
B.
,
2014
, “
Regional Variations in the Cellular, Biochemical, and Biomechanical Characteristics of Rabbit Annulus Fibrosus
,”
PLoS One
,
9
(
3
), p.
e91799
.10.1371/journal.pone.0091799
141.
Markolf
,
K. L.
, and
Morris
,
J. M.
,
1974
, “
The Structural Components of the Intervertebral Disc: A Study of Their Contributions to the Ability of the Disc to Withstand Compressive Forces
,”
J. Bone Jt. Surg.
,
56
(
4
), pp.
675
687
.10.2106/00004623-197456040-00003
142.
Balkovec
,
C.
,
Vernengo
,
A. J.
, and
McGill
,
S. M.
,
2016
, “
Disc Height Loss and Restoration Via Injectable Hydrogel Influences Adjacent Segment Mechanics In-Vitro
,”
Clin. Biomech.
,
36
, pp.
1
7
.10.1016/j.clinbiomech.2016.05.004
143.
Zhou
,
Z.
,
Gao
,
M.
,
Wei
,
F.
,
Liang
,
J.
,
Deng
,
W.
,
Dai
,
X.
,
Zhou
,
G.
, and
Zou
,
X.
,
2014
, “
Shock Absorbing Function Study on Denucleated Intervertebral Disc With or Without Hydrogel Injection Through Static and Dynamic Biomechanical Tests In Vitro
,”
BioMed Res. Int.
,
2014
, pp.
1
7
.10.1155/2014/461724
144.
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
.10.1016/j.jbiomech.2012.01.042
145.
Meakin
,
J. R.
, and
Hukins
,
D. W. L.
,
2000
, “
Effect of Removing the Nucleus Pulposus on the Deformation of the Annulus Fibrosus During Compression of the Intervertebral Disc
,”
J. Biomech.
,
33
(
5
), pp.
575
580
.10.1016/S0021-9290(99)00215-8
146.
O'Connell
,
G. D.
,
Malhotra
,
N. R.
,
Vresilovic
,
E. J.
, and
Elliott
,
D. M.
,
2011
, “
The Effect of Discectomy and the Dependence on Degeneration of Human Intervertebral Disc Strain in Axial Compression
,”
Spine
,
36
(
21
), p.
1765
.10.1097/BRS.0b013e318216752f
147.
O'Connell
,
G. D.
,
Vresilovic
,
E. J.
, and
Elliott
,
D. M.
,
2011
, “
Human Intervertebral Disc Internal Strain in Compression: The Effect of Disc Region, Loading Position, and Degeneration
,”
J. Orthop. Res.
,
29
(
4
), pp.
547
555
. 10.1002/jor.21232
148.
Adams
,
M. A.
,
Dolan
,
P.
, and
McNally
,
D. S.
,
2009
, “
The Internal Mechanical Functioning of Intervertebral Discs and Articular Cartilage, and Its Relevance to Matrix Biology
,”
Matrix Biol.
,
28
(
7
), pp.
384
389
.10.1016/j.matbio.2009.06.004
149.
Stefanakis
,
M.
,
Luo
,
J.
,
Pollintine
,
P.
,
Dolan
,
P.
, and
Adams
,
M. A.
,
2014
, “
ISSLS Prize Winner: Mechanical Influences in Progressive Intervertebral Disc Degeneration
,”
Spine
,
39
(
17
), pp.
1365
1372
.10.1097/BRS.0000000000000389
150.
Dolan
,
P.
,
Luo
,
J.
,
Pollintine
,
P.
,
Landham
,
P. R.
,
Stefanakis
,
M.
, and
Adams
,
M. A.
,
2013
, “
Intervertebral Disc Decompression Following Endplate Damage: Implications for Disc Degeneration Depend on Spinal Level and Age
,”
Spine
,
38
(
17
), pp.
1473
1481
.10.1097/BRS.0b013e318290f3cc
151.
Malandrino
,
A.
,
Planell
,
J. A.
, and
Lacroix
,
D.
,
2009
, “
Statistical Factorial Analysis on the Poroelastic Material Properties Sensitivity of the Lumbar Intervertebral Disc Under Compression, Flexion and Axial Rotation
,”
J. Biomech.
,
42
(
16
), pp.
2780
2788
.10.1016/j.jbiomech.2009.07.039
152.
Römgens
,
A. M.
,
Van 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
.10.1007/s10237-013-0477-0
153.
Cortes
,
D. H.
, and
Elliott
,
D. M.
,
2012
, “
Extra-Fibrillar Matrix Mechanics of Annulus Fibrosus in Tension and Compression
,”
Biomech. Model. Mechanobiol.
,
11
(
6
), pp.
781
790
.10.1007/s10237-011-0351-x
154.
Michalek
,
A. J.
,
Buckley
,
M. R.
,
Bonassar
,
L. J.
,
Cohen
,
I.
, and
Iatridis
,
J. C.
,
2010
, “
The Effects of Needle Puncture Injury on Microscale Shear Strain in the Intervertebral Disc Annulus Fibrosus
,”
Spine J.
,
10
(
12
), pp.
1098
1105
.10.1016/j.spinee.2010.09.015
155.
Iatridis
,
J. C.
, and
Ap Gwynn
,
I.
,
2004
, “
Mechanisms for Mechanical Damage in the Intervertebral Disc Annulus Fibrosus
,”
J. Biomech.
,
37
(
8
), pp.
1165
1175
.10.1016/j.jbiomech.2003.12.026
156.
Adam
,
C.
,
Rouch
,
P.
, and
Skalli
,
W.
,
2015
, “
Inter-Lamellar Shear Resistance Confers Compressive Stiffness in the Intervertebral Disc: An Image-Based Modelling Study on the Bovine Caudal Disc
,”
J. Biomech.
,
48
(
16
), pp.
4303
4308
.10.1016/j.jbiomech.2015.10.041
157.
Gardner‐Morse
,
M. G.
, and
Stokes
,
I. A.
,
2003
, “
Physiological Axial Compressive Preloads Increase Motion Segment Stiffness, Linearity and Hysteresis in All Six Degrees of Freedom for Small Displacements About the Neutral Posture
,”
J. Orthop. Res.
,
21
(
3
), pp.
547
552
.10.1016/S0736-0266(02)00199-7
158.
Fujita
,
Y.
,
Wagner
,
D. R.
,
Biviji
,
A. A.
,
Duncan
,
N. A.
, and
Lotz
,
J. C.
,
2000
, “
Anisotropic Shear Behavior of the Annulus Fibrosus: Effect of Harvest Site and Tissue Prestrain
,”
Med. Eng. Phys.
,
22
(
5
), pp.
349
357
.10.1016/S1350-4533(00)00053-9
159.
Newell
,
N.
,
Carpanen
,
D.
,
Evans
,
J. H.
,
Pearcy
,
M. J.
, and
Masouros
,
S. D.
,
2019
, “
Mechanical Function of the Nucleus Pulposus of the Intervertebral Disc Under High Rates of Loading
,”
Spine
,
44
(
15
), pp.
1035
1041
.10.1097/BRS.0000000000003092
160.
Veres
,
S. P.
,
Robertson
,
P. A.
, and
Broom
,
N. D.
,
2008
, “
ISSLS Prize Winner: Microstructure and Mechanical Disruption of the Lumbar Disc Annulus—Part II: How the Annulus Fails Under Hydrostatic Pressure
,”
Spine
,
33
(
25
), pp.
2711
2720
.10.1097/BRS.0b013e31817bb906
161.
Veres
,
S. P.
,
Robertson
,
P. A.
, and
Broom
,
N. D.
,
2010
, “
ISSLS Prize Winner: How Loading Rate Influences Disc Failure Mechanics: A Microstructural Assessment of Internal Disruption
,”
Spine
,
35
(
21
), pp.
1897
1908
.10.1097/BRS.0b013e3181d9b69e
162.
Veres
,
S. P.
,
Robertson
,
P. A.
, and
Broom
,
N. D.
,
2009
, “
The Morphology of Acute Disc Herniation: A Clinically Relevant Model Defining the Role of Flexion
,”
Spine
,
34
(
21
), pp.
2288
2296
.10.1097/BRS.0b013e3181a49d7e
163.
Nikkhoo
,
M.
,
Wang
,
J.-L.
,
Parnianpour
,
M.
,
El-Rich
,
M.
, and
Khalaf
,
K.
,
2018
, “
Biomechanical Response of Intact, Degenerated and Repaired Intervertebral Discs Under Impact Loading—Ex-Vivo and in-Silico Investigation
,”
J. Biomech.
,
70
, pp.
26
32
.10.1016/j.jbiomech.2018.01.026
164.
Hedman
,
T. P.
,
Chen
,
W.-P.
,
Lin
,
L.-C.
,
Lin
,
H.-J.
, and
Chuang
,
S.-Y.
,
2017
, “
Effects of Collagen Crosslink Augmentation on Mechanism of Compressive Load Sharing in Intervertebral Discs
,”
J. Med. Biol. Eng.
,
37
(
1
), pp.
94
101
.10.1007/s40846-016-0207-z
165.
Stricker
,
J.
,
Falzone
,
T.
, and
Gardel
,
M. L.
,
2010
, “
Mechanics of the F-Actin Cytoskeleton
,”
J. Biomech.
,
43
(
1
), pp.
9
14
.10.1016/j.jbiomech.2009.09.003
166.
Pritchard
,
S.
,
Erickson
,
G. R.
, and
Guilak
,
F.
,
2002
, “
Hyperosmotically Induced Volume Change and Calcium Signaling in Intervertebral Disk Cells: The Role of the Actin Cytoskeleton
,”
Biophys. J.
,
83
(
5
), pp.
2502
2510
.10.1016/S0006-3495(02)75261-2
167.
Li
,
Z.
,
Chen
,
X.
,
Sacks
,
H.
,
Yayon
,
A.
,
Alini
,
M.
, and
Grad
,
S.
,
2014
, “
Nucleus Pulposus Replacement: Hydrogel or Scaffold?—An Organ Culture Study Under Dynamic Load
,”
Global Spine J.
,
4
(
1_Suppl
.), pp.
s-0034-1376569
s-0034-1376569
.10.1055/s-0034-1376569
168.
Yang
,
X.
, and
Li
,
X.
,
2009
, “
Nucleus Pulposus Tissue Engineering: A Brief Review
,”
Eur. Spine J.
,
18
(
11
), pp.
1564
1572
.10.1007/s00586-009-1092-8
169.
Chan
,
B. P.
, and
Leong
,
K. W.
,
2008
, “
Scaffolding in Tissue Engineering: General Approaches and Tissue-Specific Considerations
,”
Eur. Spine J.
,
17
(
S4
), pp.
467
479
.10.1007/s00586-008-0745-3
170.
Halloran
,
D. O.
,
Grad
,
S.
,
Stoddart
,
M.
,
Dockery
,
P.
,
Alini
,
M.
, and
Pandit
,
A. S.
,
2008
, “
An Injectable Cross-Linked Scaffold for Nucleus Pulposus Regeneration
,”
Biomaterials
,
29
(
4
), pp.
438
447
.10.1016/j.biomaterials.2007.10.009
171.
An
,
H. S.
,
Masuda
,
K.
, and
Inoue
,
N.
,
2006
, “
Intervertebral Disc Degeneration: Biological and Biomechanical Factors
,”
J. Orthop. Sci.
,
11
(
5
), pp.
541
552
.10.1007/s00776-006-1055-4
172.
Cassinelli
,
E. H.
, and
Kang
,
J. D.
,
2000
, “
Current Understanding of Lumbar Disc Degeneration
,”
Oper. Tech. Orthop.
,
10
(
4
), pp.
254
262
.10.1016/S1048-6666(00)80025-7
173.
Azarnoosh
,
M.
,
Stoffel
,
M.
,
Quack
,
V.
,
Betsch
,
M.
,
Rath
,
B.
,
Tingart
,
M.
, and
Markert
,
B.
,
2017
, “
A Comparative Study of Mechanical Properties of Fresh and Frozen-Thawed Porcine Intervertebral Discs in a Bioreactor Environment
,”
J. Mech. Behav. Biomed. Mater.
,
69
, pp.
169
177
.10.1016/j.jmbbm.2016.12.010
174.
Dudli
,
S.
,
Haschtmann
,
D.
, and
Ferguson
,
S. J.
,
2011
, “
Prior Storage Conditions and Loading Rate Affect the In Vitro Fracture Response of Spinal Segments Under Impact Loading
,”
J. Biomech.
,
44
(
13
), pp.
2351
2355
.10.1016/j.jbiomech.2011.07.011
175.
Dhillon
,
N.
,
Bass
,
E. C.
, and
Lotz
,
J. C.
,
2001
, “
Effect of Frozen Storage on the Creep Behavior of Human Intervertebral Discs
,”
Spine
,
26
(
8
), pp.
883
888
.10.1097/00007632-200104150-00011
176.
Monaco
,
L. A.
,
DeWitte‐Orr
,
S. J.
, and
Gregory
,
D. E.
,
2016
, “
A Comparison Between Porcine, Ovine, and Bovine Intervertebral Disc Anatomy and Single Lamella Annulus Fibrosus Tensile Properties
,”
J. Morphol.
,
277
(
2
), pp.
244
251
.10.1002/jmor.20492
177.
Wilke
,
H.-J.
,
Geppert
,
J.
, and
Kienle
,
A.
,
2011
, “
Biomechanical In Vitro Evaluation of the Complete Porcine Spine in Comparison With Data of the Human Spine
,”
Eur. Spine J.
,
20
(
11
), pp.
1859
1868
.10.1007/s00586-011-1822-6
178.
Beckstein
,
J. C.
,
Sen
,
S.
,
Schaer
,
T. P.
,
Vresilovic
,
E. J.
, and
Elliott
,
D. M.
,
2008
, “
Comparison of Animal Discs Used in Disc Research to Human Lumbar Disc: Axial Compression Mechanics and Glycosaminoglycan Content
,”
Spine
,
33
(
6
), pp.
E166
E173
.10.1097/BRS.0b013e318166e001
179.
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
.10.1097/01.brs.0000253961.40910.c1
180.
Singh
,
K.
,
Masuda
,
K.
, and
An
,
H. S.
,
2005
, “
Animal Models for Human Disc Degeneration
,”
Spine J.
,
5
(
6
), pp.
S267
S279
.10.1016/j.spinee.2005.02.016
181.
McLain
,
R. F.
,
Yerby
,
S. A.
, and
Moseley
,
T. A.
,
2002
, “
Comparative Morphometry of L4 Vertebrae: Comparison of Large Animal Models for the Human Lumbar Spine
,”
Spine
,
27
(
8
), pp.
E200
E206
. 10.1097/00007632-200204150-00005
182.
Lu
,
Y.
,
Maquer
,
G.
,
Museyko
,
O.
,
Püschel
,
K.
,
Engelke
,
K.
,
Zysset
,
P.
,
Morlock
,
M.
, and
Huber
,
G.
,
2014
, “
Finite Element Analyses of Human Vertebral Bodies Embedded in Polymethylmethalcrylate or Loaded Via the Hyperelastic Intervertebral Disc Models Provide Equivalent Predictions of Experimental Strength
,”
J. Biomech.
,
47
(
10
), pp.
2512
2516
.10.1016/j.jbiomech.2014.04.015
You do not currently have access to this content.