Abstract

Cartilage loading is important in both structural and biological contexts, with overloading known to cause osteoarthritis (OA). Cellular metabolism, which can be evaluated through the relative measures of glycolysis and oxidative phosphorylation, is important in disease processes across tissues. Details of structural damage coupled with cellular metabolism in cartilage have not been evaluated. Therefore, the aim of this study was to characterize the time- and location-dependent metabolic response to traumatic impact loading in articular cartilage. Cartilage samples from porcine femoral condyles underwent a single traumatic injury that created cracks in most samples. Before and up to 30 min after loading, samples underwent optical metabolic imaging. Optical metabolic imaging measures the fluorescent intensity of byproducts of the two metabolic pathways, flavin adenine dinucleotide for oxidative phosphorylation and nicotinamide adenine dinucleotide ± phosphate for glycolysis, as well as the redox ratio between them. Images were taken at varied distances from the center of the impact. Shortly after impact, fluorescence intensity in both channels decreased, while redox ratio was unchanged. The most dramatic metabolic response was measured closest to the impact center, with suppressed fluorescence in both channels relative to baseline. Redox ratio varied nonlinearly as a function of distance from the impact. Finally, both lower and higher magnitude loading reduced flavin adenine dinucleotide fluorescence, whereas reduced nicotinamide adenine dinucleotide ± phosphate fluorescence was associated only with low strain loads and high contact pressure loads, respectively. In conclusion, this study performed novel analysis of metabolic activity following induction of cartilage damage and demonstrated time-, distance-, and load-dependent response to traumatic impact loading.

References

References
1.
Murphy
,
L.
, and
Helmick
,
C. G.
,
2012
, “
The Impact of Osteoarthritis in the United States: A Population-Health Perspective
,”
Am. J. Nurs.
,
112
(
3
), pp.
13
19
.https://nursing.ceconnection.com/ovidfiles/00000446-201203001-00003.pdf
2.
Zhang
,
Y.
, and
Jordan
,
J. M.
,
2008
, “
Epidemiology of Osteoarthritis
,”
Rheum. Dis. Clin. North Am.
,
34
(
3
), pp.
515
529
.10.1016/j.rdc.2008.05.007
3.
Sangha
,
O.
,
2000
, “
Epidemiology of Rheumatic Fever
,”
Br. Soc. Rheumatol.
,
39
(
Suppl_2
), pp.
3
12
.10.1093/rheumatology/39.suppl_2.3
4.
Vina
,
E. R.
, and
Kwoh
,
C. K.
,
2018
, “
Epidemiology of Osteoarthritis: Literature Update
,”
Curr. Opin. Rheumatol.
, 30(2), pp. 160–167. 10.1097/BOR.0000000000000479
5.
Juhakoski
,
R.
,
Heliövaara
,
M.
,
Impivaara
,
O.
,
Kröger
,
H.
,
Knekt
,
P.
,
Lauren
,
H.
, and
Arokoski
,
J. P. A.
,
2008
, “
Risk Factors for the Development of Hip Osteoarthritis: A Population-Based Prospective Study
,”
Rheumatology (Oxford
),
48
(
1
), pp.
83
–8
7
.10.1093/rheumatology/ken427
6.
Brown
,
T. D.
,
Johnston
,
R. C.
,
Saltzman
,
C. L.
,
Marsh
,
J. L.
, and
Buckwalter
,
J. A.
,
2006
, “
Posttraumatic Osteoarthritis: A First Estimate of Incidence, Prevalence, and Burden of Disease
,”
J. Orthop. Trauma
,
20
(
10
), pp.
739
744
.10.1097/01.bot.0000246468.80635.ef
7.
Ferkel
,
R. D.
, and
Chams
,
R. N.
,
2007
, “
Chronic Lateral Instability: Arthroscopic Findings and Long-Term Results
,”
Foot Ankle Int.
,
28
(
1
), pp.
24
31
.10.3113/FAI.2007.0005
8.
Takao
,
M.
,
Uchio
,
Y.
,
Naito
,
K.
,
Fukazawa
,
I.
, and
Ochi
,
M.
,
2005
, “
Arthroscopic Assessment for Intra-Articular Disorders in Residual Ankle Disability After Sprain
,”
Am. J. Sports Med.
,
33
(
5
), pp.
686
–6
92
.10.1177/0363546504270566
9.
Randall
,
D.
,
Burggren
,
W.
, and
French
,
K.
,
2002
,
Eckert Animal Physiology: Mechanisms and Adaptations
,
W.H. Freeman and Company
, New York. 
10.
Martin
,
J. A.
,
Martini
,
A.
,
Molinari
,
A.
,
Morgan
,
W.
,
Ramalingam
,
W.
,
Buckwalter
,
J. A.
, and
McKinley
,
T. O.
,
2012
, “
Mitochondrial Electron Transport and Glycolysis Are Coupled in Articular Cartilage
,”
Osteoarthritis Cartilage
,
20
(
4
), pp.
323
–32
9
.10.1016/j.joca.2012.01.003
11.
Blanco
,
F. J.
,
López-Armada
,
M. J.
, and
Maneiro
,
E.
,
2004
, “
Mitochondrial Dysfunction in Osteoarthritis
,”
Mitochondrion
,
4
(
5–6
), pp.
715
728
.10.1016/j.mito.2004.07.022
12.
Coleman
,
M. C.
,
Ramakrishnan
,
P. S.
,
Brouillette
,
M. J.
, and
Martin
,
J. A.
,
2016
, “
Injurious Loading of Articular Cartilage Compromises Chondrocyte Respiratory Function
,”
Arthritis Rheumatol.
,
68
(
3
), pp.
662
671
.10.1002/art.39460
13.
Zignego
,
D. L.
,
Hilmer
,
J. K.
, and
June
,
R. K.
,
2015
, “
Mechanotransduction in Primary Human Osteoarthritic Chondrocytes is Mediated by Metabolism of Energy, Lipids, and Amino Acids
,”
J. Biomech.
,
48
(
16
), pp.
4253
4261
.10.1016/j.jbiomech.2015.10.038
14.
Jutila
,
A. A.
,
Zignego
,
D. L.
,
Hwang
,
B. K.
,
Hilmer
,
J. K.
,
Hamerly
,
T.
,
Minor
,
C. A.
,
Walk
,
S. T.
, and
June
,
R. K.
,
2014
, “
Candidate Mediators of Chondrocyte Mechanotransduction Via Targeted and Untargeted Metabolomic Measurements
,”
Arch. Biochem. Biophys.
,
545
, pp.
116
123
.10.1016/j.abb.2014.01.011
15.
Jutila
,
A. A.
,
Zignego
,
D. L.
,
Schell
,
W. J.
, and
June
,
R. K.
,
2015
, “
Encapsulation of Chondrocytes in High-Stiffness Agarose Microenvironments for In Vitro Modeling of Osteoarthritis Mechanotransduction
,”
Ann. Biomed. Eng.
,
43
(
5
), pp.
1132
1144
.10.1007/s10439-014-1183-5
16.
Adams
,
S. B.
,
Setton
,
L. A.
,
Kensicki
,
E.
,
Bolognesi
,
M. P.
,
Toth
,
A. P.
, and
Nettles
,
D. L.
,
2012
, “
Global Metabolic Profiling of Human Osteoarthritic Synovium
,”
Osteoarthritis Cartilage
,
20
(
1
), pp.
64
67
.10.1016/j.joca.2011.10.010
17.
Jurvelin
,
J.
,
Helminen
,
H. J.
,
Lauritsalo
,
S.
,
Kiviranta
,
I.
,
Säämänen
,
A.-M.
,
Paukkonen
,
K.
, and
Tammi
,
M.
,
1985
, “
Influences of Joint Immobilization and Running Exercise on Articular Cartilage Surfaces of Young Rabbits: A Semiquantitative Stereomicroscopic and Scanning Electron Microscopic Study
,”
Acta Anat. (Basel)
,
122
(
1
), pp.
62
68
.10.1159/000145984
18.
Videman
,
T.
,
1982
, “
The Effect of Running on the Osteoarthritic Joint: An Experimental Matched-Pair Study With Rabbits
,”
Rheumatol. Rehabil.
,
XXI
(
1
), pp.
1
8
.10.1093/rheumatology/21.1.1
19.
Palmoski
,
M. J.
, and
Brandt
,
K. D.
,
1981
, “
Running Inhibits the Reversal of Atrophic Changes in Canine Knee Cartilage After Removal of a Leg Cast
,”
Arthritis Rheum.
,
24
(
11
), pp.
1329
1337
.10.1002/art.1780241101
20.
Ni
,
G.-X.
,
Zhou
,
Y.-Z.
,
Chen
,
W.
,
Xu
,
L.
,
Li
,
Z.
,
Liu
,
S.-Y.
,
Lei
,
L.
, and
Zhan
,
L.-Q.
,
2016
, “
Different Responses of Articular Cartilage to Strenuous Running and Joint Immobilization
,”
Connect. Tissue Res.
,
57
(
2
), pp.
143
151
.10.3109/03008207.2015.1117457
21.
Walsh
,
S. K.
,
Skala
,
M. C.
, and
Henak
,
C. R.
,
2019
, “
Real-Time Optical Redox Imaging of Cartilage Metabolic Response to Mechanical Loading
,”
Osteoarthritis Cartilage
,
27
(
12
), pp.
1841
1850
.10.1016/j.joca.2019.08.004
22.
Lee
,
C. M.
,
Kisiday
,
J. D.
,
McIlwraith
,
C. W.
,
Grodzinsky
,
A. J.
, and
Frisbie
,
D. D.
,
2013
, “
Development of an In Vitro Model of Injury-Induced Osteoarthritis in Cartilage Explants From Compressive Overload
,”
Am. J. Vet. Res.
,
74
(
1
), pp. 40–47. 10.2460/ajvr.74.1.40
23.
Henak
,
C. R.
,
Bartell
,
L. R.
,
Cohen
,
I.
, and
Bonassar
,
L. J.
,
2017
, “
Multiscale Strain as a Predictor of Impact-Induced Fissuring in Articular Cartilage
,”
J. Biomech. Eng.
,
139
(
3
), pp.
0310041
0310048
.10.1115/1.4034994
24.
Argote
,
P. F.
,
Kaplan
,
J. T.
,
Poon
,
A.
,
Xu
,
X.
,
Cai
,
L.
,
Emery
,
N. C.
,
Pierce
,
D. M.
, and
Neu
,
C. P.
,
2019
, “
Chondrocyte Viability is Lost During High-Rate Impact Loading by Transfer of Amplified Strain, But Not Stress, to Pericellular and Cellular Regions
,”
Osteoarthritis Cartilage
, 27(12), pp.
1822
1830
.10.1016/j.joca.2019.07.018
25.
Rolauffs
,
B.
,
Kurz
,
B.
,
Felka
,
T.
,
Rothdiener
,
M.
,
Uynuk-Ool
,
T.
,
Aurich
,
M.
,
Frank
,
E.
,
Bahrs
,
C.
,
Badke
,
A.
,
Stöckle
,
U.
,
Aicher
,
W. K.
, and
Grodzinsky
,
A. J.
,
2013
, “
Stress-vs-Time Signals Allow the Prediction of Structurally Catastrophic Events During Fracturing of Immature Cartilage and Predetermine the Biomechanical, Biochemical, and Structural Impairment
,”
J. Struct. Biol.
,
183
(
3
), pp.
501
511
.10.1016/j.jsb.2013.06.011
26.
Leucht
,
F.
,
Dürselen
,
L.
,
Hogrefe
,
C.
,
Joos
,
H.
,
Reichel
,
H.
,
Schmitt
,
H.
,
Ignatius
,
A.
, and
Brenner
,
R. E.
,
2012
, “
Development of a New Biomechanically Defined Single Impact Rabbit Cartilage Trauma Model for In Vivo-Studies
,”
J. Invest. Surg.
,
25
(
4
), pp.
235
241
.10.3109/08941939.2011.630123
27.
Borrelli
,
J.
,
Zaegel
,
M. A.
,
Martinez
,
M. D.
, and
Silva
,
M. J.
,
2010
, “
Diminished Cartilage Creep Properties and Increased Trabecular Bone Density Following a Single, Sub-Fracture Impact of the Rabbit Femoral Condyle
,”
J. Orthop. Res.
,
28
(
10
), pp.
1307
1314
.10.1002/jor.21122
28.
Flachsmann
,
R.
,
Kistler
,
M.
,
Rentzios
,
A.
, and
Broom
,
N. D.
,
2006
, “
Influence of an Initiating Microsplit on the Resistance to Compression-Induced Rupture of the Articular Surface
,”
Connect. Tissue Res.
,
47
(
2
), pp.
77
84
.10.1080/03008200600584090
29.
Oakley
,
S. P.
,
Lassere
,
M. N.
,
Portek
,
I.
,
Szomor
,
Z.
,
Ghosh
,
P.
,
Kirkham
,
B. W.
,
Murrell
,
G. A. C.
,
Wulf
,
S.
, and
Appleyard
,
R. C.
,
2004
, “
Biomechanical, Histologic and Macroscopic Assessment of Articular Cartilage in a Sheep Model of Osteoarthritis
,”
Osteoarthritis Cartilage
,
12
(
8
), pp.
667
679
.10.1016/j.joca.2004.05.006
30.
D'lima
,
D. D.
,
Hashimoto
,
S.
,
Chen
,
P. C.
,
Colwell
,
C. W.
, and
Lotz
,
M. K.
,
2001
, “
Human Chondrocyte Apoptosis in Response to Mechanical Injury
,”
Osteoarthritis Cartilage
,
9
(
8
), pp.
712
719
.10.1053/joca.2001.0468
31.
Lewis
,
J. L.
,
Deloria
,
L. B.
,
Oyen-Tiesma
,
M.
,
Thompson
,
R. C.
,
Ericson
,
M.
, and
Oegema
,
T. R.
,
2003
, “
Cell Death After Cartilage Impact Occurs Around Matrix Cracks
,”
J. Orthop. Res.
,
21
(
5
), pp.
881
887
.10.1016/S0736-0266(03)00039-1
32.
Waters
,
N. P.
,
Stoker
,
A. M.
,
Carson
,
W. L.
,
Pfeiffer
,
F. M.
, and
Cook
,
J. L.
,
2014
, “
Biomarkers Affected by Impact Velocity and Maximum Strain of Cartilage During Injury
,”
J. Biomech.
,
47
(
12
), pp.
3185
3195
.10.1016/j.jbiomech.2014.06.015
33.
Stolberg-Stolberg
,
J. A.
,
Furman
,
B. D.
,
Garrigues
,
N. W.
,
Lee
,
J.
,
Pisetsky
,
D. S.
,
Stearns
,
N. A.
,
DeFrate
,
L. E.
,
Guilak
,
F.
, and
Olson
,
S. A.
,
2013
, “
Effects of Cartilage Impact With and Without Fracture on Chondrocyte Viability and the Release of Inflammatory Markers
,”
J. Orthop. Res.
,
31
(
8
), pp.
1283
1292
.10.1002/jor.22348
34.
Natoli
,
R. M.
,
Scott
,
C. C.
, and
Athanasiou
,
K. A.
,
2008
, “
Temporal Effects of Impact on Articular Cartilage Cell Death, Gene Expression, Matrix Biochemistry, and Biomechanics
,”
Ann. Biomed. Eng.
,
36
(
5
), pp.
780
792
.10.1007/s10439-008-9472-5
35.
Bartell
,
L. R.
,
Xu
,
M. C.
,
Bonassar
,
L. J.
, and
Cohen
,
I.
,
2018
, “
Local and Global Measurements Show That Damage Initiation in Articular Cartilage is Inhibited by the Surface Layer and Has Significant Rate Dependence
,”
J. Biomech.
,
72
, pp.
63
70
.10.1016/j.jbiomech.2018.02.033
36.
Huser
,
C. A. M.
, and
Davies
,
M. E.
,
2007
, “
Calcium Signaling Leads to Mitochondrial Depolarization in Impact-Induced Chondrocyte Death in Equine Articular Cartilage Explants
,”
Arthritis Rheum.
,
56
(
7
), pp.
2322
2334
.10.1002/art.22717
37.
Delco
,
M. L.
,
Bonnevie
,
E. D.
,
Bonassar
,
L. J.
, and
Fortier
,
L. A.
,
2017
, “
Mitochondrial Dysfunction is an Acute Response of Articular Chondrocytes to Mechanical Injury
,”
J. Orthop. Res.
,
36
(
2
), pp.
739
750
.
38.
Haudenschild
,
D. R.
,
Carlson
,
A. K.
,
Zignego
,
D. L.
,
Yik
,
J. H. N.
,
Hilmer
,
J. K.
, and
June
,
R. K.
,
2019
, “
Inhibition of Early Response Genes Prevents Changes in Global Joint Metabolomic Profiles in Mouse Post-Traumatic Osteoarthritis
,”
Osteoarthr. Cartil
., 27(3), pp. 504–512. 10.1016/j.joca.2018.11.006
39.
Skala
,
M.
, and
Ramanujam
,
N.
,
2010
, “
Multiphoton Redox Ratio Imaging for Metabolic Monitoring In Vivo
,”
Methods Mol. Biol.
,
594
, pp.
155
162
.10.1007/978-1-60761-411-1
40.
Briscoe
,
B. J.
,
Sebastian
,
K. S.
, and
Adams
,
M. J.
,
1994
, “
The Effect of Indenter Geometry on the Elastic Response to Indentation
,”
J. Phys. D. Appl. Phys.
,
27
(
6
), pp.
1156
1162
.10.1088/0022-3727/27/6/013
41.
Schneider
,
C. A.
,
Rasband
,
W. S.
, and
Eliceiri
,
K. W.
,
2012
, “
NIH Image to ImageJ: 25 Years of Image Analysis
,”
Nat. Methods
,
9
(
7
), pp.
671
675
.10.1038/nmeth.2089
42.
Aspden
,
R. M.
,
Jeffrey
,
J. E.
, and
Burgin
,
L. V.
,
2002
, “
Letter to the Editor
,”
Osteoarthritis Cartilage
,
10
(
7
), pp.
588
589
.10.1053/joca.2002.0803
43.
Tchetina
,
E. V.
, and
Markova
,
G. A.
,
2018
, “
Regulation of Energy Metabolism in the Growth Plate and Osteoarthritic Chondrocytes
,”
Rheumatol. Int.
, 38(11), pp.
1963
1974
. 10.1007/s00296-018-4103-4
44.
Zhang
,
R.-K.
,
Li
,
G.-W.
,
Zeng
,
C.
,
Lin
,
C.-X.
,
Huang
,
L.-S.
,
Huang
,
G.-X.
,
Zhao
,
C.
,
Feng
,
S.-Y.
, and
Fang
,
H.
,
2018
, “
Mechanical Stress Contributes to Osteoarthritis Development Through the Activation of Transforming Growth Factor Beta 1 (TGF-Β1)
,”
Bone Jt. Res.
,
7
(
11
), pp.
587
594
.10.1302/2046-3758.711.BJR-2018-0057.R1
45.
Gemmiti
,
C. V.
, and
Guldberg
,
R. E.
,
2009
, “
Shear Stress Magnitude and Duration Modulates Matrix Composition and Tensile Mechanical Properties in Engineered Cartilaginous Tissue
,”
Biotechnol. Bioeng.
,
104
(
4
), pp.
809
820
.10.1002/bit.22440
46.
Bartell
,
L. R.
,
Fortier
,
L. A.
,
Bonassar
,
L. J.
, and
Cohen
,
I.
,
2015
, “
Measuring Microscale Strain Fields in Articular Cartilage During Rapid Impact Reveals Thresholds for Chondrocyte Death and a Protective Role for the Superficial Layer
,”
J. Biomech.
,
48
(
12
), pp.
3440
3446
.10.1016/j.jbiomech.2015.05.035
47.
Harris
,
M. D.
,
Anderson
,
A. E.
,
Henak
,
C. R.
,
Ellis
,
B. J.
,
Peters
,
C. L.
, and
Weiss
,
J. A.
,
2012
, “
Finite Element Prediction of Cartilage Contact Stresses in Normal Human Hips
,”
J. Orthop. Res.
,
30
(
7
), pp.
1133
1139
.10.1002/jor.22040
48.
Wilson
,
W.
,
Van Rietbergen
,
B.
,
Van Donkelaar
,
C. C.
, and
Huiskes
,
R.
,
2003
, “
Pathways of Load-Induced Cartilage Damage Causing Cartilage Degeneration in the Knee After Meniscectomy
,”
J. Biomech.
,
36
(
6
), pp.
845
851
.10.1016/S0021-9290(03)00004-6
49.
Vincent
,
T. L.
,
McLean
,
C. J.
,
Full
,
L. E.
,
Peston
,
D.
, and
Saklatvala
,
J.
,
2007
, “
FGF-2 is Bound to Perlecan in the Pericellular Matrix of Articular Cartilage, Where It Acts as a Chondrocyte Mechanotransducer
,”
Osteoarthritis Cartilage
,
15
(
7
), pp.
752
763
.10.1016/j.joca.2007.01.021
50.
Millward-Sadler
,
S. J.
,
Wright
,
M. O.
,
Davies
,
L. W.
,
Nuki
,
G.
, and
Salter
,
D. M.
,
2000
, “
Mechanotransduction Via Integrins and interleukin-4 Results in Altered Aggrecan and Matrix Metalloproteinase 3 Gene Expression in Normal, but Not Osteoarthritic, Human Articular Chondrocytes
,”
Arthritis Rheum.
,
43
(
9
), pp.
2091
2099
.10.1002/1529-0131(200009)43:9<2091::AID-ANR21>3.0.CO;2-C
51.
Pfeiffer
,
T.
,
Schuster
,
S.
, and
Bonhoeffer
,
S.
,
2001
, “
Cooperation and Competition in the Evolution of ATP-Producing Pathways
,”
Science
,
292
(
5516
), pp.
504
507
.10.1126/science.1058079
52.
Zheng
,
J.
,
2012
, “
Energy Metabolism of Cancer: Glycolysis Versus Oxidative Phosphorylation (Review)
,”
Oncol. Lett.
,
4
(
6
), pp.
1151
1157
.10.3892/ol.2012.928
53.
Agathocleous
,
M.
, and
Harris
,
W. A.
,
2013
, “
Metabolism in Physiological Cell Proliferation and Differentiation
,”
Trends Cell Biol.
,
23
(
10
), pp.
484
492
.10.1016/j.tcb.2013.05.004
54.
Singh
,
P.
,
Marcu
,
K. B.
,
Goldring
,
M. B.
, and
Otero
,
M.
,
2019
, “
Phenotypic Instability of Chondrocytes in Osteoarthritis: On a Path to Hypertrophy
,”
Ann. N. Y. Acad. Sci.
, 1442(1), pp.
17
34
.10.1111/nyas.13930
55.
Goetz
,
J. E.
,
Coleman
,
M. C.
,
Fredericks
,
D. C.
,
Petersen
,
E.
,
Martin
,
J. A.
,
McKinley
,
T. O.
, and
Tochigi
,
Y.
,
2017
, “
Time-Dependent Loss of Mitochondrial Function Precedes Progressive Histologic Cartilage Degeneration in a Rabbit Meniscal Destabilization Model
,”
J. Orthop. Res.
,
35
(
3
), pp.
590
599
.10.1002/jor.23327
56.
Vanderploeg
,
E. J.
,
Wilson
,
C. G.
, and
Levenston
,
M. E.
,
2008
, “
Articular Chondrocytes Derived From Distinct Tissue Zones Differentially Respond to In Vitro Oscillatory Tensile Loading
,”
Osteoarthritis Cartilage
,
16
(
10
), pp.
1228
1236
.10.1016/j.joca.2008.02.016
57.
Klein
,
T. J.
,
Schumacher
,
B. L.
,
Blewis
,
M. E.
,
Schmidt
,
T. A.
,
Voegtline
,
M. S.
,
Thonar
,
E. J. M.
,
Masuda
,
K.
, and
Sah
,
R. L.
,
2006
, “
Tailoring Secretion of Proteoglycan 4 (PRG4) in Tissue-Engineered Cartilage
,”
Tissue Eng.
,
12
(
6
), pp.
1429
1439
.10.1089/ten.2006.12.1429
58.
Youn
,
I.
,
Choi
,
J. B.
,
Cao
,
L.
,
Setton
,
L. A.
, and
Guilak
,
F.
,
2006
, “
Zonal Variations in the 3D Morphology of the Chondron Measured In Situ Using Serial Confocal Sections
,”
Osteoarthritis Cartilage
,
14
(
9
), pp.
889
897
.10.1016/j.joca.2006.02.017
59.
Grogan
,
S. P.
,
Duffy
,
S. F.
,
Pauli
,
C.
,
Koziol
,
J. A.
,
Su
,
A. I.
,
D'Lima
,
D. D.
, and
Lotz
,
M. K.
,
2013
, “
Zone-Specific Gene Expression Patterns in Articular Cartilage
,”
Arthritis Rheum.
,
65
(
2
), pp.
418
428
.10.1002/art.37760
60.
Vernon
,
L. L.
,
Vance
,
D. D.
,
Wang
,
L.
,
Rampersaud
,
E.
,
Vance
,
J. M.
,
Pericak-Vance
,
M.
,
Huang
,
C. Y. C.
, and
Kaplan
,
L. D.
,
2016
, “
Regional Differential Genetic Response of Human Articular Cartilage to Impact Injury
,”
Cartilage
,
7
(
2
), pp.
163
173
.10.1177/1947603515618483
61.
Dumond
,
H.
,
Presle
,
N.
,
Pottie
,
P.
,
Pacquelet
,
S.
,
Terlain
,
B.
,
Netter
,
P.
,
Gepstein
,
A.
,
Livne
,
E.
, and
Jouzeau
,
J. Y.
,
2004
, “
Site Specific Changes in Gene Expression and Cartilage Metabolism During Early Experimental Osteoarthritis
,”
Osteoarthritis Cartilage
,
12
(
4
), pp.
284
295
.10.1016/j.joca.2003.11.008
62.
Novakofski
,
K. D.
,
Berg
,
L. C.
,
Bronzini
,
I.
,
Bonnevie
,
E. D.
,
Poland
,
S. G.
,
Bonassar
,
L. J.
, and
Fortier
,
L. A.
,
2015
, “
Joint-Dependent Response to Impact and Implications for Post-Traumatic Osteoarthritis
,”
Osteoarthritis Cartilage
,
23
(
7
), pp.
1130
1137
.10.1016/j.joca.2015.02.023
63.
Ateshian
,
G. A.
,
Ellis
,
B. J.
, and
Weiss
,
J. A.
,
2007
, “
Equivalence Between Short-Time Biphasic and Incompressible Elastic Material Responses
,”
ASME J. Biomech. Eng.
,
129
(
3
), pp.
405
412
.10.1115/1.2720918
64.
Chen
,
A. C.
,
Bae
,
W. C.
,
Schinagl
,
R. M.
, and
Sah
,
R. L.
,
2001
, “
Depth- and Strain-Dependent Mechanical and Electromechanical Properties of Full-Thickness Bovine Articular Cartilage in Confined Compression
,”
J. Biomech.
,
34
(
1
), pp.
1
12
.10.1016/S0021-9290(00)00170-6
You do not currently have access to this content.