Abstract
Degeneration of the lumbar spine, and especially how that degeneration may lead to pain, remains poorly understood. In particular, the mechanics of the facet capsular ligament may contribute to low back pain, but the mechanical changes that occur in this ligament with spinal degeneration are unknown. Additionally, the highly nonlinear, heterogeneous, and anisotropic nature of the facet capsular ligament makes understanding mechanical changes more difficult. Clinically, magnetic resonance imaging (MRI)-based signs of degeneration in the facet joint and the intervertebral disc (IVD) correlate. Therefore, this study examined how the nonlinear, heterogeneous mechanics of the facet capsular ligament change with degeneration of the lumbar spine as characterized using MRI. Cadaveric human spines were imaged via MRI, and the L2-L5 facet joints and IVDs were scored using the Fujiwara and Pfirrmann grading systems. Then, the facet capsular ligament was isolated and biaxially loaded. The nonlinear mechanical properties of the ligament were obtained using a nonlinear generalized anisotropic inverse mechanics analysis (nGAIM). Then a Holzapfel–Gasser–Ogden (HGO) model was fit to the stress–strain data obtained from nGAIM. The facet capsular ligament is stiffer and more anisotropic at larger Pfirrmann grades and higher Fujiwara scores than at lower grades and scores. Analysis of ligament heterogeneity showed all tissues are highly heterogeneous, but no distinct spatial patterns of heterogeneity were found. These results show that degeneration of the lumbar spine including the facet capsular ligament appears to be occurring as a whole joint phenomenon and advance our understanding of lumbar spine degeneration.
Issue Section:
Research Papers
References
1.
Breivik
,
H.
,
Collett
,
B.
,
Ventafridda
,
V.
,
Cohen
,
R.
, and
Gallacher
,
D.
, 2006
, “
Survey of Chronic Pain in Europe: Prevalence, Impact on Daily Life, and Treatment
,” Eur. J. Pain
,
10
(4
), pp. 287
–287
.10.1016/j.ejpain.2005.06.0092.
Ita
,
M. E.
,
Zhang
,
S.
,
Holsgrove
,
T. P.
,
Kartha
,
S.
, and
Winkelstein
,
B. A.
, 2017
, “
The Physiological Basis of Cervical Facet-Mediated Persistent Pain: Basic Science and Clinical Challenges
,” J. Orthop. Sports Phys. Ther.
,
47
(7
), pp. 450
–461
.10.2519/jospt.2017.72553.
Falco
,
F. J. E.
,
Manchikanti
,
L.
,
Datta
,
S.
,
Sehgal
,
N.
,
Geffert
,
S.
,
Onyewu
,
O.
,
Singh
,
V.
,
Bryce
,
D. A.
,
Benyamin
,
R. M.
,
Simopoulos
,
T. T.
,
Vallejo
,
R.
,
Gua
,
S.
,
Ward
,
S. P.
, and
Hirsch
,
J. A.
, 2012
, “
An Update of the Systematic Assessment of the Diagnostic Accuracy of Lumbar Facet Joint Nerve Blocks
,” Pain Phys.
,
6;15
(6;12
), pp. E869
–E907
.10.36076/ppj.2012/15/E8694.
Perolat
,
R.
,
Kastler
,
A.
,
Nicot
,
B.
,
Pellat
,
J. M.
,
Tahon
,
F.
,
Attye
,
A.
,
Heck
,
O.
,
Boubagra
,
K.
,
Grand
,
S.
, and
Krainik
,
A.
, 2018
, “
Facet Joint Syndrome: From Diagnosis to Interventional Management
,” Insights Imag.
,
9
(5
), pp. 773
–789
.10.1007/s13244-018-0638-x5.
Bermel
,
E. A.
,
Barocas
,
V. H.
, and
Ellingson
,
A. M.
, 2018
, “
The Role of the Facet Capsular Ligament in Providing Spinal Stability
,” Comput. Methods Biomech Biomed Eng.
,
21
(13
), pp. 712
–721
.10.1080/10255842.2018.15143926.
Ellingson
,
A. M.
,
Shaw
,
M. N.
,
Giambini
,
H.
, and
An
,
K.-N.
, 2016
, “
Comparative Role of Disc Degeneration and Ligament Failure on Functional Mechanics of the Lumbar Spine
,” Comput. Methods Biomech. Biomed. Eng.
,
19
(9
), pp. 1009
–1018
.10.1080/10255842.2015.10885247.
Little
,
J. S.
, and
Khalsa
,
P. S.
, 2005
, “
Material Properties of the Lumbar Facet Joint Capsule
,” ASME J. Biomech. Eng.
,
127
(1
), pp. 15
–24
.10.1115/1.18353488.
Naserkhaki
,
S.
,
Arjmand
,
N.
,
Shirazi-Adl
,
A.
,
Farahmand
,
F.
, and
El-Rich
,
M.
, 2018
, “
Effects of Eight Different Ligament Property Datasets on Biomechanics of a Lumbar L4-L5 Finite Element Model
,” J. Biomech.
,
70
(2018
), pp. 33
–42
.10.1016/j.jbiomech.2017.05.0039.
Sharma
,
M.
,
Langrana
,
N. A.
, and
Rodriguez
,
J.
, 1995
, “
Role of Ligaments and Facets in Lumbar Spinal Stability
,” Spine (Phila. Pa. 1976)
,
20
(8
), pp. 887
–900
.10.1097/00007632-199504150-0000310.
Intolo
,
P.
,
Milosavljevic
,
S.
,
Baxter
,
D. G.
,
Carman
,
A. B.
,
Pal
,
P.
, and
Munn
,
J.
, 2009
, “
The Effect of Age on Lumbar Range of Motion: A Systematic Review
,” Man. Ther.
,
14
(6
), pp. 596
–604
.10.1016/j.math.2009.08.00611.
Farshad
,
M.
,
Aichmair
,
A.
,
Götschi
,
T.
,
Senteler
,
M.
, and
Urbanschitz
,
L.
, 2021
, “
How is Spinal Range of Motion Affected by Disc- and Facet Degeneration and Spinopelvic Anatomy?
,” North Am. Spine Soc. J.
,
7
, p. 100076
.10.1016/j.xnsj.2021.10007612.
Ellingson
,
A. M.
, and
Nuckley
,
D. J.
, 2015
, “
Altered Helical Axis Patterns of the Lumbar Spine Indicate Increased Instability With Disc Degeneration
,” J. Biomech.
,
48
(2
), pp. 361
–369
.10.1016/j.jbiomech.2014.11.01013.
Mimura
,
M.
,
Panjabi
,
M. M.
,
Oxland
,
T. R.
,
Crisco
,
J. J.
,
Yamamoto
,
I.
, and
Vasavada
,
A.
, 1994
, “
Disc Degeneration Affects the Multidirectional Flexibility of the Lumbar Spine
,” Spine (Phila. Pa. 1976)
,
19
(12
), pp. 1371
–1380
.10.1097/00007632-199406000-0001114.
Kettler
,
A.
,
Rohlmann
,
F.
,
Ring
,
C.
,
Mack
,
C.
, and
Wilke
,
H. J.
, 2011
, “
Do Early Stages of Lumbar Intervertebral Disc Degeneration Really Cause Instability? Evaluation of an In Vitro Database
,” Eur. Spine J.
,
20
(4
), pp. 578
–584
.10.1007/s00586-010-1635-z15.
Cornaz
,
F.
,
Widmer
,
J.
,
Farshad-Amacker
,
N. A.
,
Spirig
,
J. M.
,
Snedeker
,
J. G.
, and
Farshad
,
M.
, 2021
, “
Intervertebral Disc Degeneration Relates to Biomechanical Changes of Spinal Ligaments
,” Spine J.
, 21(8), pp. 1
–9
.10.1016/j.spinee.2021.04.01616.
Pfirrmann
,
C. W. A.
,
Metzdorf
,
A.
,
Zanetti
,
M.
,
Hodler
,
J.
, and
Boos
,
N.
, 2001
, “
Magnetic Resonance Classification of Lumbar Intervertebral Disc Degeneration
,” Spine (Phila. Pa. 1976)
,
26
(17
), pp. 1873
–1878
.10.1097/00007632-200109010-0001117.
Jamaludin
,
A.
,
Lootus
,
M.
,
Kadir
,
T.
,
Zisserman
,
A.
,
Urban
,
J.
,
Battié
,
M. C.
,
Fairbank
,
J.
, and
McCall
,
I.
, The Genodisc Consortium
2017
, “
Automation of Reading of Radiological Features From Magnetic Resonance Images (MRIs) of the Lumbar Spine Without Human Intervention is Comparable With an Expert Radiologist
,” Eur. Spine J.
,
26
(5
), pp. 1374
–1383
.10.1007/s00586-017-4956-318.
Fujiwara
,
A.
,
Tamai
,
K.
,
Yamato
,
M.
,
An
,
H. S.
,
Yoshida
,
H.
,
Saotome
,
K.
, and
Kurihashi
,
A.
, 1999
, “
The Relationship Between Facet Joint Osteoarthritis and Disc Degeneration of the Lumbar Spine: An MRI Study
,” Eur. Spine J.
,
8
(5
), pp. 396
–401
.10.1007/s00586005019319.
Fujiwara
,
A.
,
Lim
,
T. H.
,
An
,
H. S.
,
Tanaka
,
N.
,
Jeon
,
C. H.
,
Andersson
,
G. B. J.
, and
Haughton
,
V. M.
, 2000
, “
The Effect of Disc Degeneration and Facet Joint Osteoarthritis on the Segmental Flexibility of the Lumbar Spine
,” Spine (Phila. Pa. 1976)
,
25
(23
), pp. 3036
–3044
.10.1097/00007632-200012010-0001120.
Hawellek
,
T.
,
Hubert
,
J.
,
Hischke
,
S.
,
Rolvien
,
T.
,
Krause
,
M.
,
Püschel
,
K.
,
Rüther
,
W.
, and
Niemeier
,
A.
, 2017
, “
Microcalcification of Lumbar Spine Intervertebral Discs and Facet Joints is Associated With Cartilage Degeneration, but Differs in Prevalence and Its Relation to Age
,” J. Orthop. Res.
,
35
(12
), pp. 2692
–2699
.10.1002/jor.2359121.
Li
,
J.
,
Muehleman
,
C.
,
Abe
,
Y.
, and
Masuda
,
K.
, 2011
, “
Prevalence of Facet Joint Degeneration in Association With Intervertebral Joint Degeneration in a Sample of Organ Donors
,” J. Orthop. Res.
,
29
(8
), pp. 1267
–1274
.10.1002/jor.2138722.
Iida
,
T.
,
Abumi
,
K.
,
Kotani
,
Y.
, and
Kaneda
,
K.
, 2002
, “
Effects of Aging and Spinal Degeneration on Mechanical Properties of Lumbar Supraspinous and Interspinous Ligaments
,” Spine J.
,
2
(2
), pp. 95
–100
.10.1016/S1529-9430(02)00142-023.
Claeson
,
A. A.
, and
Barocas
,
V. H.
, 2017
, “
Planar Biaxial Extension of the Lumbar Facet Capsular Ligament Reveals Significant in-Plane Shear Forces
,” J. Mech. Behav. Biomed. Mater.
,
65
, pp. 127
–136
.10.1016/j.jmbbm.2016.08.01924.
Zhang
,
S.
,
Singh
,
S.
, and
Winkelstein
,
B. A.
, 2017
, “
Collagen Organization Regulates Stretch-Initiated Pain-Related Neuronal Signals In Vitro: Implications for Structure–Function Relationships in Innervated Ligaments
,” J. Orthop. Res.
,
36
(2
), pp. 770
–777
.10.1002/jor.2365725.
Zarei
,
V.
,
Liu
,
C. J.
,
Claeson
,
A. A.
,
Akkin
,
T.
, and
Barocas
,
V. H.
, 2017
, “
Image-Based Multiscale Mechanical Modeling Shows the Importance of Structural Heterogeneity in the Human Lumbar Facet Capsular Ligament
,” Biomech. Model. Mechanobiol.
,
16
(4
), pp. 1425
–1438
.10.1007/s10237-017-0896-426.
Ban
,
E.
,
Zhang
,
S.
,
Zarei
,
V.
,
Barocas
,
V. H.
,
Winkelstein
,
B. A.
, and
Picu
,
C. R.
, 2017
, “
Collagen Organization in Facet Capsular Ligaments Varies With Spinal Region and With Ligament Deformation
,” ASME J. Biomech. Eng.
,
139
(7
), p. 071009
.10.1115/1.403601927.
Claeson
,
A. A.
,
Yeh
,
Y. J.
,
Black
,
A. J.
,
Akkin
,
T.
, and
Barocas
,
V. H.
, 2015
, “
Marker-Free Tracking of Facet Capsule Motion Using Polarization-Sensitive Optical Coherence Tomography
,” Ann. Biomed. Eng.
,
43
(12
), pp. 2953
–2966
.10.1007/s10439-015-1349-928.
Middendorf
,
J. M.
,
Ita
,
M. E.
,
Winkelstein
,
B. A.
, and
Barocas
,
V. H.
, 2021
, “Local Tissue Heterogeneity May Modulate Neuronal Responses Via Altered Axon Strain Fields: Insights About Innervated Joint Capsules From a Computational Model,” Biomech. Model. Mechanobiol.
,
20
(6
), pp. 2269
–2285
.10.1007/s10237-021-01506-929.
Raghupathy
,
R.
, and
Barocas
,
V. H.
, 2010
, “
Generalized Anisotropic Inverse Mechanics for Soft Tissues
,” ASME J. Biomech. Eng.
,
132
(8
), p. 081006
.10.1115/1.400125730.
Raghupathy
,
R.
,
Witzenburg
,
C.
,
Lake
,
S. P.
,
Sander
,
E. A.
, and
Barocas
,
V. H.
, 2011
, “
Identification of Regional Mechanical Anisotropy in Soft Tissue Analogs
,” ASME J. Biomech. Eng.
,
133
(9
), p. 091011
.10.1115/1.400517031.
Witzenburg
,
C. M.
,
Dhume
,
R. Y.
,
Lake
,
S. P.
, and
Barocas
,
V. H.
, 2016
, “
Automatic Segmentation of Mechanically Inhomogeneous Tissues Based on Deformation Gradient Jump
,” IEEE Trans. Med. Imag.
,
35
(1
), pp. 29
–41
.10.1109/TMI.2015.245331632.
Witzenburg
,
C. M.
, and
Barocas
,
V. H.
, 2016
, “
A Nonlinear Anisotropic Inverse Method for Computational Dissection of Inhomogeneous Planar Tissues
,” Comput. Methods Biomech. Biomed. Eng.
,
19
(15
), pp. 1630
–1646
.10.1080/10255842.2016.117615433.
Raghupathy
,
R.
, 2011
, “Form From Function: Generalized Anisotropic Inverse Mechanics for Soft Tissues,” Doctoral thesis
, University of Minnesota Digital Conservancy.https://hdl.handle.net/11299/11628634.
Raghupathy
,
R.
,
Barocas
,
V. H.
, 2022
, “
Robust Image Correlation Based Strain Calculator for Tissue Systems
,” University of Minnesota, Minneapolis, MN, accessed Dec. 15, 2022, https://license.umn.edu/product/robust-image-correlation-based-strain-calculator-for-tissue-systems35.
Shih
,
E. D.
,
Provenzano
,
P. P.
,
Witzenburg
,
C. M.
,
Barocas
,
V. H.
,
Grande
,
A. W.
, and
Alford
,
P. W.
, 2022
, “
Characterizing Tissue Remodeling and Mechanical Heterogeneity in Cerebral Aneurysms
,” Methods Vasc. Biol.
,
59
(1
), pp. 34
–42
.10.1159/00051969436.
Holzapfel
,
G. A.
,
Gasser
,
T. C.
, and
Ogden
,
R. W.
, 2000
, “
A New Constitutive Framework for Arterial Wall Mechanics and a Comparative Study of Material Models
,” J. Elast.
,
61
(1/3
), pp. 1
–48
.10.1023/A:101083531656437.
Maas
,
S. A.
,
Ellis
,
B. J.
,
Ateshian
,
G. A.
, and
Weiss
,
J. A.
, 2012
, “
FEBio: Finite Elements for Biomechanics
,” ASME J. Biomech. Eng.
,
134
(1
), p. 011005
.10.1115/1.400569438.
Flynn
,
B. P.
,
Bhole
,
A. P.
,
Saeidi
,
N.
,
Liles
,
M.
,
Dimarzio
,
C. A.
, and
Ruberti
,
J. W.
, 2010
, “
Mechanical Strain Stabilizes Reconstituted Collagen Fibrils Against Enzymatic Degradation by Mammalian Collagenase Matrix Metalloproteinase 8 (MMP-8)
,” PLoS One
,
5
(8
), p. e12337
.10.1371/journal.pone.001233739.
Luetkemeyer
,
C. M.
,
Scheven
,
U.
,
Estrada
,
J. B.
, and
Arruda
,
E. M.
, 2021
, “
Constitutive Modeling of the Anterior Cruciate Ligament Bundles and Patellar Tendon With Full-Field Methods
,” J. Mech. Phys. Solids
,
156
, p. 104577
.10.1016/j.jmps.2021.10457740.
Peña
,
E.
,
Calvo
,
B.
,
Martínez
,
M. A.
,
Palanca
,
D.
, and
Doblaré
,
M.
, 2005
, “
Finite Element Analysis of the Effect of Meniscal Tears and Meniscectomies on Human Knee Biomechanics
,” Clin. Biomech.
,
20
(5
), pp. 498
–507
.10.1016/j.clinbiomech.2005.01.00941.
Sadeqi
,
S.
,
Summers
,
R.
,
Erbulut
,
D. U.
, and
Goel
,
V. K.
, 2021
, “
Optimization of Material Coefficients in the Holzapfel-Gasser-Ogden Material Model for the Main Four Ligaments of the Knee Joint-A Finite Element Study
,” Appl. Math.
,
12
(12
), pp. 1166
–1188
.10.4236/am.2021.121207542.
Weiss
,
J. A.
, and
Gardiner
,
J. C.
, 2001
, “
Computational Modeling of Ligament Mechanics
,” Crit. Rev. Biomed. Eng.
,
29
(3
), pp. 303
–371
.10.1615/CritRevBiomedEng.v29.i3.2043.
Simon
,
P.
,
Espinoza
,
A. A.
,
Andersson
,
G. B. J.
,
An
,
H. S.
, and
Inoue
,
N.
, 2012
, “
In Vivo Topographic Analysis of Lumbar Facet Joint Space Width Distribution in Healthy and Symptomatic Subjects
,” Spine (Phila. Pa. 1976)
,
37
(12
), pp. 1058
–1064
.10.1097/BRS.0b013e3182552ec944.
Yamabe
,
D.
,
Murakami
,
H.
,
Chokan
,
K.
,
Endo
,
H.
,
Oikawa
,
R.
,
Sawamura
,
S.
, and
Doita
,
M.
, 2017
, “
Evaluation of Water Content in Lumbar Intervertebral Discs and Facet Joints Before and After Physiological Loading Using T2 Mapping MRI
,” Spine (Phila. Pa. 1976)
,
42
(24
), pp. E1423
–E1428
.10.1097/BRS.000000000000220445.
Bermel
,
E. A.
,
Thakral
,
S.
,
Claeson
,
A. A.
,
Ellingson
,
A. M.
, and
Barocas
,
V. H.
, 2020
, “
Asymmetric in-Plane Shear Behavior of Isolated Cadaveric Lumbar Facet Capsular Ligaments: Implications for Subject Specific Biomechanical Models
,” J. Biomech.
,
105
, p. 109814
.10.1016/j.jbiomech.2020.10981446.
Eubanks
,
J. D.
,
Lee
,
M. J.
,
Cassinelli
,
E.
, and
Ahn
,
N. U.
, 2007
, “
Does Lumbar Facet Arthrosis Precede Disc Degeneration? A Postmortem Study
,” Clin. Orthop. Relat. Res.
,
464
(464
), pp. 184
–189
.10.1097/BLO.0b013e3181583d4e47.
Suri
,
P.
,
Miyakoshi
,
A.
,
Hunter
,
D. J.
,
Jarvik
,
J. G.
,
Rainville
,
J.
,
Guermazi
,
A.
,
Li
,
L.
, and
Katz
,
J. N.
, 2011
, “
Does Lumbar Spinal Degeneration Begin With the Anterior Structures? A Study of the Observed Epidemiology in a Community-Based Population
,” BMC Musculoskelet. Disord.
,
12
(1
), p. 202
.10.1186/1471-2474-12-20248.
Diamant
,
J.
,
Keller
,
A.
,
Baer
,
E.
,
Litt
,
M.
, and
Arridge
,
R. G.
, 1972
, “
Collagen; Ultrastructure and Its Relation to Mechanical Properties as a Function of Ageing
,” Proc. R. Soc. London. Ser. B. Biol. Sci.
,
180
(60
), pp. 293
–315
.10.1098/rspb.1972.001949.
De Bastiani
,
G.
,
De La Côrte
,
F. D.
,
Brass
,
K. E.
,
Cantarelli
,
C.
,
Dau
,
S.
,
Kommers
,
G. D.
,
Da Silva
,
T. M.
, and
Da Silva Azevedo
,
M.
, 2018
, “
Histochemistry of Equine Damaged Tendons, Ligaments and Articular Cartilage
,” Acta Sci. Vet.
,
46
(1
), p. 8
.10.22456/1679-9216.8937550.
Legerlotz
,
K.
,
Dorn
,
J.
,
Richter
,
J.
,
Rausch
,
M.
, and
Leupin
,
O.
, 2014
, “
Age-Dependent Regulation of Tendon Crimp Structure, Cell Length and Gap Width With Strain
,” Acta Biomater.
,
10
(10
), pp. 4447
–4455
.10.1016/j.actbio.2014.05.02951.
Zarei
,
V.
,
Zhang
,
S.
,
Winkelstein
,
B. A.
, and
Barocas
,
V. H.
, 2017
, “
Tissue Loading and Microstructure Regulate the Deformation of Embedded Nerve Fibres: Predictions From Single-Scale and Multiscale Simulations
,” J. R. Soc. Interface
,
14
(135
), pp. 1
–11
.10.1098/rsif.2017.032652.
Quinn
,
K. P.
, and
Winkelstein
,
B. A.
, 2011
, “
Detection of Altered Collagen Fiber Alignment in the Cervical Facet Capsule After Whiplash-Like Joint Retraction
,” Ann. Biomed. Eng.
,
39
(8
), pp. 2163
–2173
.10.1007/s10439-011-0316-353.
Yahia
,
L. H.
, and
Garzon
,
S.
, 1993
, “
Structure on the Capsular Ligaments of the Facet Joints
,” Ann. Anat.
,
175
(2
), pp. 185
–188
.10.1016/S0940-9602(11)80179-254.
Sharma
,
P.
, and
Maffulli
,
N.
, 2006
, “
Biology of Tendon Injury: Healing, Modeling and Remodeling
,” J. Musculoskelet. Neruonal. Interact.
,
6
(2
), pp. 181
–190
.https://pubmed.ncbi.nlm.nih.gov/16849830/55.
Yang
,
Y.
,
Rupani
,
A.
,
Weightman
,
A.
,
Wimpenny
,
I.
,
Bagnaninchi
,
P.
, and
Ahearne
,
M.
, 2011
, “
The Study of Optical Properties and Proteoglycan Content of Tendons by PS-OCT
,” Dyn. Fluctuat. Biomed. Photonics VIII
,
7898
, p. 789808
.10.1117/12.87711356.
Lopez
,
S. G.
, and
Bonassar
,
L. J.
, 2022
, “
The Role of SLRPs and Large Aggregating Proteoglycans in Collagen Fibrillogenesis, Extracellular Matrix Assembly, and Mechanical Function of Fibrocartilage
,” Connect. Tissue Res.
,
63
(3
), pp. 269
–286
.10.1080/03008207.2021.190388757.
Kim
,
J. S.
,
Ali
,
M. H.
,
Wydra
,
F.
,
Li
,
X.
,
Hamilton
,
J. L.
,
An
,
H. S.
,
Cs-Szabo
,
G.
,
Andrews
,
S.
,
Moric
,
M.
,
Xiao
,
G.
,
Wang
,
J. H. C.
,
Chen
,
D.
,
Cavanaugh
,
J. M.
, and
Im
,
H. J.
, 2015
, “
Characterization of Degenerative Human Facet Joints and Facet Joint Capsular Tissues
,” Osteoarthr. Cartil.
,
23
(12
), pp. 2242
–2251
.10.1016/j.joca.2015.06.00958.
O'Leary
,
S. A.
,
Link
,
J. M.
,
Klineberg
,
E. O.
,
Hu
,
J. C.
, and
Athanasiou
,
K. A.
, 2017
, “
Characterization of Facet Joint Cartilage Properties in the Human and Interspecies Comparisons
,” Acta Biomater.
,
54
, pp. 367
–376
.10.1016/j.actbio.2017.03.01759.
Whatley
,
B. R.
, and
Wen
,
X.
, 2012
, “
Intervertebral Disc (IVD): Structure, Degeneration, Repair and Regeneration
,” Mater. Sci. Eng. C
,
32
(2
), pp. 61
–77
.10.1016/j.msec.2011.10.01160.
Andriotis
,
O. G.
,
Desissaire
,
S.
, and
Thurner
,
P. J.
, 2018
, “
Collagen Fibrils: Nature's Highly Tunable Nonlinear Springs
,” ACS Nano
,
12
(4
), pp. 3671
–3680
.10.1021/acsnano.8b0083761.
Zhang
,
G.
,
Ezura
,
Y.
,
Chervoneva
,
I.
,
Robinson
,
P. S.
,
Beason
,
D. P.
,
Carine
,
E. T.
,
Soslowsky
,
L. J.
,
Iozzo
,
R. V.
, and
Birk
,
D. E.
, 2006
, “
Decorin Regulates Assembly of Collagen Fibrils and Acquisition of Biomechanical Properties During Tendon Development
,” J. Cell. Biochem.
,
98
(6
), pp. 1436
–1449
.10.1002/jcb.2077662.
Kalamajski
,
S.
, and
Oldberg
,
A.
, 2010
, “
The Role of Small Leucine-Rich Proteoglycans in Collagen Fibrillogenesis
,” Matrix Biol.
,
29
(4
), pp. 248
–253
.10.1016/j.matbio.2010.01.00163.
Chui
,
E. T. F.
,
Tsang
,
H. H. L.
,
Lee
,
K. H.
,
Lau
,
C. S.
,
Wong
,
C. H.
, and
Chung
,
H. Y.
, 2020
, “
MRI Inflammation of Facet and Costovertebral Joints is Associated With Restricted Spinal Mobility and Worsened Functional Status
,” Rheumatology (United Kingdom)
,
59
(9
), pp. 2591
–2602
.10.1093/rheumatology/kez64964.
Cohen
,
S. P.
, and
Raja
,
S. N.
, 2007
, “
Pathogenesis, Diagnosis, and Treatment of Lumbar Zygapophysial (Facet) Join Pain
,” Anesthesiology
,
106
(3
), pp. 591
–614
.10.1097/00000542-200703000-0002465.
Zhou
,
X.
,
Liu
,
Y.
,
Zhou
,
S.
,
Fu
,
X.-X.
,
Yu
,
X.-L.
,
Fu
,
C.-L.
,
Zhang
,
B.
, and
Dai
,
M.
, 2016
, “
The Correlation Between Radiographic and Pathologic Grading of Lumbar Facet Joint Degeneration
,” BMC Med. Imaging
,
16
(27
), pp. 1
–8
.10.1186/s12880-016-0129-9Copyright © 2023 by ASME
You do not currently have access to this content.
