Abstract

Inferior synovial lubrication is a hallmark of osteoarthritis (OA), and synovial fluid (SF) lubrication and composition are variable among OA patients. Hyaluronic acid (HA) viscosupplementation is a widely used therapy for improving SF viscoelasticity and lubrication, but it is unclear how the effectiveness of HA viscosupplements varies with arthritic endotype. The objective of this study was to investigate the effects of the HA viscosupplement, Hymovis®, on the lubricating properties of diseased SF from patients with noninflammatory OA and inflammatory arthritis (IA). The composition (cytokine, HA, and lubricin concentrations) of the SF was measured as well as the mechanical properties (rheology, tribology) of the SF alone and in a 1:1 mixture with the HA viscosupplement. Using rotational rheometry, no difference in SF viscosity was detected between disease types, and the addition of HA significantly increased all fluids' viscosities. In noninflammatory OA SF, friction coefficients followed a typical Stribeck pattern, and their magnitude was decreased by the addition of HA. While some of the IA SF also showed typical Stribeck behavior, a subset showed more erratic behavior with highly variable and larger friction coefficients. Interestingly, this aberrant behavior was not eliminated by the addition of HA, and it was associated with low concentrations of lubricin. Aberrant SF exhibited significantly lower effective viscosities compared to noninflammatory OA and IA SF with typical tribological behavior. Collectively, these results suggest that different endotypes of arthritis exist with respect to lubrication, which may impact the effectiveness of HA viscosupplements in reducing friction.

References

1.
Jay
,
G. D.
,
Torres
,
J. R.
,
Rhee
,
D. K.
,
Helminen
,
H. J.
,
Hytinnen
,
M. M.
,
Cha
,
C.-J.
,
Elsaid
,
K.
,
Kim
,
K.-S.
,
Cui
,
Y.
, and
Warman
,
M. L.
,
2007
, “
Association Between Friction and Wear in Diarthrodial Joints Lacking Lubricin
,”
Arthritis Rheum.
,
56
(
11
), pp.
3662
3669
.10.1002/art.22974
2.
Elsaid
,
K. A.
,
Jay
,
G. D.
,
Warman
,
M. L.
,
Rhee
,
D. K.
, and
Chichester
,
C. O.
,
2005
, “
Association of Articular Cartilage Degradation and Loss of Boundary-Lubricating Ability of Synovial Fluid Following Injury and Inflammatory Arthritis
,”
Arthritis Rheum.
,
52
(
6
), pp.
1746
1755
.10.1002/art.21038
3.
Bonnevie
,
E. D.
,
Delco
,
M. L.
,
Bartell
,
L. R.
,
Jasty
,
N.
,
Cohen
,
I.
,
Fortier
,
L. A.
, and
Bonassar
,
L. J.
,
2018
, “
Microscale Frictional Strains Determine Chondrocyte Fate in Loaded Cartilage
,”
J. Biomech.
,
74
, pp.
72
78
.10.1016/j.jbiomech.2018.04.020
4.
Waller
,
K. A.
,
Zhang
,
L. X.
, and
Jay
,
G. D.
,
2017
, “
Friction-Induced Mitochondrial Dysregulation Contributes to Joint Deterioration in Prg4 Knockout Mice
,”
Int. J. Mol. Sci.
,
18
(
6
), p.
1252
.10.3390/ijms18061252
5.
Waller
,
K. A.
,
Zhang
,
L. X.
,
Fleming
,
B. C.
, and
Jay
,
G. D.
,
2012
, “
Preventing Friction-Induced Chondrocyte Apoptosis: Comparison of Human Synovial Fluid and Hylan G-F 20
,”
J. Rheumatol.
,
39
(
7
), pp.
1473
1480
.10.3899/jrheum.111427
6.
Waller
,
K. A.
,
Zhang
,
L. X.
,
Elsaid
,
K. A.
,
Fleming
,
B. C.
,
Warman
,
M. L.
, and
Jay
,
G. D.
,
2013
, “
Role of Lubricin and Boundary Lubrication in the Prevention of Chondrocyte Apoptosis
,”
Proc. Natl. Acad. Sci.
,
110
(
15
), pp.
5852
5857
.10.1073/pnas.1219289110
7.
Kosinska
,
M. K.
,
Ludwig
,
T. E.
,
Liebisch
,
G.
,
Zhang
,
R.
,
Siebert
,
H.-C.
,
Wilhelm
,
J.
,
Kaesser
,
U.
,
Dettmeyer
,
R. B.
,
Klein
,
H.
,
Ishaque
,
B.
,
Rickert
,
M.
,
Schmitz
,
G.
,
Schmidt
,
T. A.
, and
Steinmeyer
,
J.
,
2015
, “
Articular Joint Lubricants During Osteoarthritis and Rheumatoid Arthritis Display Altered Levels and Molecular Species
,”
PLoS One
,
10
(
5
), p.
e0125192
.10.1371/journal.pone.0125192
8.
Ludwig
,
T. E.
,
McAllister
,
J. R.
,
Lun
,
V.
,
Wiley
,
J. P.
, and
Schmidt
,
T. A.
,
2012
, “
Diminished Cartilage-Lubricating Ability of Human Osteoarthritic Synovial Fluid Deficient in Proteoglycan 4: Restoration Through Proteoglycan 4 Supplementation
,”
Arthritis Rheum.
,
64
(
12
), pp.
3963
3971
.10.1002/art.34674
9.
Gupta
,
R. C.
,
Lall
,
R.
,
Srivastava
,
A.
, and
Sinha
,
A.
,
2019
, “
Hyaluronic Acid: Molecular Mechanisms and Therapeutic Trajectory
,”
Front. Vet. Sci.
,
6
, p.
192
.10.3389/fvets.2019.00192
10.
Altman
,
R. D.
,
Manjoo
,
A.
,
Fierlinger
,
A.
,
Niazi
,
F.
, and
Nicholls
,
M.
,
2015
, “
The Mechanism of Action for Hyaluronic Acid Treatment in the Osteoarthritic Knee: A Systematic Review
,”
BMC Musculoskelet. Disord.
,
16
(
321
), p.
321
.10.1186/s12891-015-0775-z
11.
Strauss
,
E. J.
,
Hart
,
J. A.
,
Miller
,
M. D.
,
Altman
,
R. D.
, and
Rosen
,
J. E.
,
2009
, “
Hyaluronic Acid Viscosupplementation and Osteoarthritis
,”
Am. J. Sports Med.
,
37
(
8
), pp.
1636
1644
.10.1177/0363546508326984
12.
Oliviero
,
F.
,
Scanu
,
A.
,
Ramonda
,
R.
,
Frallonardo
,
P.
,
Sfriso
,
P.
,
Dayer
,
J.-M.
, and
Punzi
,
L.
,
2015
, “
IL-1ß and IL-8 Are Scavenged by the Hexadecylamide Derivative of Hyaluronic Acid: A New Mechanism
,”
J. Biomed. Mater. Res. Part A
,
103
(
9
), pp.
2823
2829
.10.1002/jbm.a.35422
13.
Hochberg
,
M. C.
,
Altman
,
R. D.
,
April
,
K. T.
,
Benkhalti
,
M.
,
Guyatt
,
G.
,
McGowan
,
J.
,
Towheed
,
T.
,
Welch
,
V.
,
Wells
,
G.
, and
Tugwell
,
P.
,
2012
, “
American College of Rheumatology 2012 Recommendations for the Use of Nonpharmacologic and Pharmacologic Therapies in Osteoarthritis of the Hand, Hip, and Knee
,”
Arthritis Care Res. (Hoboken
),
64
(
4
), pp.
465
474
.10.1002/acr.21596
14.
Trojian
,
T. H.
,
Concoff
,
A. L.
,
Joy
,
S. M.
,
Hatzenbuehler
,
J. R.
,
Saulsberry
,
W. J.
, and
Coleman
,
C. I.
,
2016
, “
AMSSM Scientific Statement Concerning Viscosupplementation Injections for Knee Osteoarthritis
,”
Clin. J. Sport Med.
,
26
(
1
), pp.
1
11
.10.1097/JSM.0000000000000274
15.
McAlindon
,
T. E.
,
Bannuru
,
R. R.
,
Sullivan
,
M. C.
,
Arden
,
N. K.
,
Berenbaum
,
F.
,
Bierma-Zeinstra
,
S. M.
,
Hawker
,
G. A.
,
Henrotin
,
Y.
,
Hunter
,
D. J.
,
Kawaguchi
,
H.
,
Kwoh
,
K.
,
Lohmander
,
S.
,
Rannou
,
F.
,
Roos
,
E. M.
, and
Underwood
,
M.
,
2014
, “
OARSI Guidelines for the Non-Surgical Management of Knee Osteoarthritis
,”
Osteoarthr. Cartil.
,
22
(
3
), pp.
363
388
.10.1016/j.joca.2014.01.003
16.
Jevsevar
,
D. S.
,
2013
, “
Treatment of Osteoarthritis of the Knee: Evidence-Based Guideline
,”
J. Am. Acad. Orthop. Surg.
,
21
(
9
), pp.
571
576
.10.5435/JAAOS-21-09-571
17.
Wang
,
C.-T.
,
Lin
,
J.
,
Chang
,
C.-J.
,
Lin
,
Y.-T.
, and
Hou
,
S.-M.
,
2004
, “
Therapeutic Effects of Hyaluronic Acid on Osteoarthritis of the Knee
,”
J. Bone Jt. Surg.
,
86
(
3
), pp.
538
545
.10.2106/00004623-200403000-00012
18.
Eymard
,
F.
,
Chevalier
,
X.
, and
Conrozier
,
T.
,
2017
, “
Obesity and Radiological Severity Are Associated With Viscosupplementation Failure in Patients With Knee Osteoarthritis
,”
J. Orthop. Res.
,
35
(
10
), pp.
2269
2274
.10.1002/jor.23529
19.
Conrozier
,
T.
,
Eymard
,
F.
,
Chouk
,
M.
, and
Chevalier
,
X.
,
2019
, “
Impact of Obesity, Structural Severity and Their Combination on the Efficacy of Viscosupplementation in Patients With Knee Osteoarthritis
,”
BMC Musculoskeletal Disord
.,
20
(
376
), pp.
1
8
.10.1186/s12891-019-2748-0
20.
Conrozier
,
T.
,
Mathieu
,
P.
,
Schott
,
A.-M.
,
Laurent
,
I.
,
Hajri
,
T.
,
Crozes
,
P.
,
Grand
,
P.
,
Laurent
,
H.
,
Marchand
,
F.
,
Meignan
,
F.
,
Noel
,
E.
,
Rozand
,
Y.
,
Savoye
,
J.-F.
, and
Vignon
,
E.
,
2003
, “
Factors Predicting Long-Term Efficacy of Hylan GF-20 Viscosupplementation in Knee Osteoarthritis
,”
Jt. Bone. Spine
,
70
(
2
), pp.
128
133
.10.1016/S1297-319X(03)00005-8
21.
Toh
,
E. M.
,
Prasad
,
P. S.
, and
Teanby
,
D.
,
2002
, “
Correlating the Efficacy of Knee Viscosupplementation With Osteoarthritic Changes on Roentgenological Examination
,”
Knee
,
9
(
4
), pp.
321
330
.10.1016/S0968-0160(02)00040-6
22.
Altman
,
R. D.
,
Farrokhyar
,
F.
,
Fierlinger
,
A.
,
Niazi
,
F.
, and
Rosen
,
J.
,
2016
, “
Analysis for Prognostic Factors From a Database for the Intra-Articular Hyaluronic Acid (Euflexxa) Treatment for Osteoarthritis of the Knee
,”
Cartilage
,
7
(
3
), pp.
229
237
.10.1177/1947603515620890
23.
Bonnevie
,
E. D.
,
Galesso
,
D.
,
Secchieri
,
C.
, and
Bonassar
,
L. J.
,
2019
, “
Frictional Characterization of Injectable Hyaluronic Acids is More Predictive of Clinical Outcomes Than Traditional Rheological or Viscoelastic Characterization
,”
PLoS One
,
14
(
5
), p.
e0216702
.10.1371/journal.pone.0216702
24.
Blagojevic
,
M.
,
Jinks
,
C.
,
Jeffery
,
A.
, and
Jordan
,
K. P.
,
2010
, “
Risk Factors for Onset of Osteoarthritis of the Knee in Older Adults: A Systematic Review and Meta-Analysis
,”
Osteoarthr. Cartil.
,
18
(
1
), pp.
24
33
.10.1016/j.joca.2009.08.010
25.
Felson
,
D. T.
,
Lawrence
,
R. C.
,
Dieppe
,
P. A.
,
Hirsch
,
R.
,
Helmick
,
C. G.
,
Jordan
,
J. M.
,
Kington
,
R. S.
,
Lane
,
N. E.
,
Nevitt
,
M. C.
,
Zhang
,
Y.
,
Sowers
,
M.
,
McAlindon
,
T.
,
Spector
,
T. D.
,
Poole
,
A. R.
,
Yanovski
,
S. Z.
,
Ateshian
,
G.
,
Sharma
,
L.
,
Buckwalter
,
J. A.
,
Brandt
,
K. D.
, and
Fries
,
J. F.
,
2000
, “
Osteoarthritis: New Insights—Part 1: The Disease and Its Risk Factors
,”
Ann. Intern. Med.
,
133
(
8
), pp.
635
646
.10.7326/0003-4819-133-8-200010170-00016
26.
Loeser
,
R. F.
,
Goldring
,
S. R.
,
Scanzello
,
C. R.
, and
Goldring
,
M. B.
,
2012
, “
Osteoarthritis: A Disease of the Joint as an Organ
,”
Arthritis Rheum.
,
64
(
6
), pp.
1697
1707
.10.1002/art.34453
27.
Bierma-Zeinstra
,
S. M.
, and
van Middelkoop
,
M.
,
2017
, “
Osteoarthritis: In Search of Phenotypes
,”
Nat. Rev. Rheumatol.
,
13
(
12
), pp.
705
706
.10.1038/nrrheum.2017.181
28.
Zhang
,
W.
,
Sun
,
G.
,
Likhodii
,
S.
,
Liu
,
M.
,
Aref-Eshghi
,
E.
,
Harper
,
P. E.
,
Martin
,
G.
,
Furey
,
A.
,
Green
,
R.
,
Randell
,
E.
,
Rahman
,
P.
, and
Zhai
,
G.
,
2016
, “
Metabolomic Analysis of Human Plasma Reveals That Arginine is Depleted in Knee Osteoarthritis Patients
,”
Osteoarthr. Cartil.
,
24
(
5
), pp.
827
834
.10.1016/j.joca.2015.12.004
29.
Clair
,
A. J.
, Anil, U. , Kingery, M. T. , Kenny, L. , and Strauss, E. J. ,
2019
, “
Synovial Fluid Biomarker Alternatives: Can Plasma and Urine Samples Shed Light on the Post-Traumatic Intra-Articular Environment
?,”
Transactions of the Orthopaedic Research Society 2019 Annual Meeting
,
Austin, TX
, Feb. 2–5,
Paper No. 427
.https://www.ors.org/Transactions/65/0427.pdf
30.
Loeser
,
R. F.
,
Pathmasiri
,
W.
,
Sumner
,
S. J.
,
McRitchie
,
S.
,
Beavers
,
D.
,
Saxena
,
P.
,
Nicklas
,
B. J.
,
Jordan
,
J.
,
Guermazi
,
A.
,
Hunter
,
D. J.
, and
Messier
,
S. P.
,
2016
, “
Association of Urinary Metabolites With Radiographic Progression of Knee Osteoarthritis in Overweight and Obese Adults: An Exploratory Study
,”
Osteoarthr. Cartil.
,
24
(
8
), pp.
1479
1486
.10.1016/j.joca.2016.03.011
31.
Carlson
,
A. K.
,
Rawle
,
R. A.
,
Adams
,
E.
,
Greenwood
,
M. C.
,
Bothner
,
B.
, and
June
,
R. K.
,
2018
, “
Application of Global Metabolomic Profiling of Synovial Fluid for Osteoarthritis Biomarkers
,”
Biochem. Biophys. Res. Commun.
,
499
(
2
), pp.
182
188
.10.1016/j.bbrc.2018.03.117
32.
Kosinska
,
M. K.
,
Liebisch
,
G.
,
Lochnit
,
G.
,
Wilhelm
,
J.
,
Klein
,
H.
,
Kaesser
,
U.
,
Lasczkowski
,
G.
,
Rickert
,
M.
,
Schmitz
,
G.
, and
Steinmeyer
,
J.
,
2013
, “
A Lipidomic Study of Phospholipid Classes and Species in Human Synovial Fluid
,”
Arthritis Rheum.
,
65
(
9
), pp.
2323
2333
.10.1002/art.38053
33.
Zheng
,
K.
,
Shen
,
N.
,
Chen
,
H.
,
Ni
,
S.
,
Zhang
,
T.
,
Hu
,
M.
,
Wang
,
J.
,
Sun
,
L.
, and
Yang
,
X.
,
2017
, “
Global and Targeted Metabolomics of Synovial Fluid Discovers Special Osteoarthritis Metabolites
,”
J. Orthop. Res.
,
35
(
9
), pp.
1973
1981
.10.1002/jor.23482
34.
Reesink
,
H. L.
,
Watts
,
A. E.
,
Mohammed
,
H. O.
,
Jay
,
G. D.
, and
Nixon
,
A. J.
,
2017
, “
Lubricin/Proteoglycan 4 Increases in Both Experimental and Naturally Occurring Equine Osteoarthritis
,”
Osteoarthr. Cartil.
,
25
(
1
), pp.
128
137
.10.1016/j.joca.2016.07.021
35.
Antonacci
,
J. M.
,
Schmidt
,
T. A.
,
Serventi
,
L. A.
,
Cai
,
M. Z.
,
Shu
,
Y. L.
,
Schumacher
,
B. L.
,
McIlwraith
,
C. W.
, and
Sah
,
R. L.
,
2012
, “
Effects of Equine Joint Injury on Boundary Lubrication of Articular Cartilage by Synovial Fluid: Role of Hyaluronan
,”
Arthritis Rheum.
,
64
(
9
), pp.
2917
2926
.10.1002/art.34520
36.
Ballard
,
B. L.
,
Antonacci
,
J. M.
,
Temple-Wong
,
M. M.
,
Hui
,
A. Y.
,
Schumacher
,
B. L.
,
Bugbee
,
W. D.
,
Schwartz
,
A. K.
,
Girard
,
P. J.
, and
Sah
,
R. L.
,
2012
, “
Effect of Tibial Plateau Fracture on Lubrication Function and Composition of Synovial Fluid
,”
J. Bone Jt. Surg. Am.
,
94
(
10
), p.
e64
.10.2106/JBJS.K.00046
37.
Jay
,
G. D.
,
Elsaid
,
K. A.
,
Zack
,
J.
,
Robinson
,
K.
,
Trespalacios
,
F.
,
Cha
,
C.-J.
, and
Chichester
,
C. O.
,
2004
, “
Lubricating Ability of Aspirated Synovial Fluid From Emergency Department Patients With Knee Joint Synovitis
,”
J. Rheumatol.
,
31
(
3
), pp.
557
564
.http://www.jrheum.org/content/31/3/557.tab-e-letters
38.
Elsaid
,
K. A. A.
,
Fleming
,
B. C. C.
,
Oksendahl
,
H. L. L.
,
Machan
,
J. T. T.
,
Fadale
,
P. D. D.
,
Hulstyn
,
M. J. J.
,
Shalvoy
,
R. M.
, and
Jay
,
G. D. D.
,
2008
, “
Decreased Lubricin Concentrations and Markers of Joint Inflammation in the Synovial Fluid of Patients With Anterior Cruciate Ligament Injury
,”
Arthritis Rheum.
,
58
(
6
), pp.
1707
1715
.10.1002/art.23495
39.
Asari
,
A.
,
Miyauchi
,
S.
,
Sekiguchi
,
T.
,
Machida
,
A.
,
Kuriyama
,
S.
,
Miyazaki
,
K.
, and
Namiki
,
O.
,
1994
, “
Hyaluronan, Cartilage Destruction and Hydrarthrosis in Traumatic Arthritis
,”
Osteoarthr. Cartil.
,
2
(
2
), pp.
79
89
.10.1016/S1063-4584(05)80058-5
40.
Belcher
,
C.
,
Yaqub
,
R.
,
Fawthrop
,
F.
,
Bayliss
,
M.
, and
Doherty
,
M.
,
1997
, “
Synovial Fluid Chondroitin and Keratan Sulphate Epitopes, Glycosaminoglycans, and Hyaluronan in Arthritic and Normal Knees
,”
Ann. Rheum. Dis.
,
56
(
5
), pp.
299
307
.10.1136/ard.56.5.299
41.
Temple-Wong
,
M. M.
,
Hansen
,
B. C. B.
,
Grissom
,
M. J.
,
Cai
,
M. Z.
,
Noori
,
N. B.
,
Roberts
,
J. M.
,
Love
,
R. E.
,
Oei
,
W. F.
,
Antonacci
,
J. M.
,
Schumacher
,
B. L.
,
Bugbee
,
W. D.
, and
Sah
,
R. L.
,
2010
, “
Effect of Knee Osteoarthritis on the Boundary Lubricating Molecules and Function of Human Synovial Fluid
,”
Transactions of the Orthopaedic Research Society 2010 Annual Meeting
,
New Orleans, LA
, Mar. 6–9,
Paper No. 340
.https://www.ors.org/Transactions/56/0340.pdf
42.
Plickert
,
H. D. D.
,
Bondzio
,
A.
,
Einspanier
,
R.
,
Tichy
,
A.
, and
Brunnberg
,
L.
,
2013
, “
Hyaluronic Acid Concentrations in Synovial Fluid of Dogs With Different Stages of Osteoarthritis
,”
Res. Vet. Sci.
,
94
(
3
), pp.
728
734
.10.1016/j.rvsc.2012.11.007
43.
Atarod
,
M.
,
Ludwig
,
T. E.
,
Frank
,
C. B.
,
Schmidt
,
T. A.
, and
Shrive
,
N. G.
,
2015
, “
Cartilage Boundary Lubrication of Ovine Synovial Fluid Following Anterior Cruciate Ligament Transection: A Longitudinal Study
,”
Osteoarthr. Cartil.
,
23
(
4
), pp.
640
647
.10.1016/j.joca.2014.12.017
44.
Feeney
,
E.
,
Peal
,
B. T.
,
Inglis
,
J. E.
,
Su
,
J.
,
Nixon
,
A. J.
,
Bonassar
,
L. J.
, and
Reesink
,
H. L.
,
2019
, “
Temporal Changes in Synovial Fluid Composition and Elastoviscous Lubrication in the Equine Carpal Fracture Model
,”
J. Orthop. Res.
,
37
(
5
), pp.
1071
1079
.10.1002/jor.24281
45.
Irwin
,
R. M.
,
Feeney
,
E.
,
Secchieri
,
C.
,
Galesso
,
D.
,
Cohen
,
I.
,
Oliviero
,
F.
,
Ramonda
,
R.
, and
Bonassar
,
L. J.
,
2020
, “
Distinct Tribological Endotypes of Pathological Human Synovial Fluid Reveal Characteristic Biomarkers and Variation in Efficacy of Viscosupplementation at Reducing Local Strains in Articular Cartilage
,”
Osteoarthr. Cartil.
,
28
(
4
), pp.
492
501
.10.1016/j.joca.2020.02.029
46.
Faryna
,
A.
, and
Goldenberg
,
K.
,
1990
, “
Joint Fluid,” Clinical Methods: The History
,”
Physical, and Laboratory Examinations
,
H.
Walker
,
W.
Hall
, and
J.
Hurst
, eds.,
Butterworths
,
Boston, MA
.
47.
MacWilliams
,
P. S.
, and
Friedrichs
,
K. R.
,
2003
, “
Laboratory Evaluation and Interpretation of Synovial Fluid
,”
Vet. Clin. North Am. Small Animal Pract.
,
33
(
1
), pp.
153
178
.10.1016/S0195-5616(02)00083-9
48.
Reginato
,
A. J.
,
Maldonado
,
I.
,
Reginato
,
A. M.
,
Falasca
,
G. F.
, and
O'Connor
,
C. R.
,
1992
, “
Supravital Staining of Synovial Fluid With Testsimplets
,”
Diagn. Cytopathol.
,
8
(
2
), pp.
147
152
.10.1002/dc.2840080211
49.
Robinson
,
D. B.
, and
El-Gabalawy
,
H. S.
,
2008
, “
Evaluation of the Patient
,”
Primer on the Rheumatic Diseases
,
J. H.
Klippel
,
J. H.
Stone
,
L .J.
Crofford
, and
P. H.
White
, eds.,
Springer
,
New York
, pp.
6
41.
50.
Taylor
,
W.
,
Gladman
,
D.
,
Helliwell
,
P.
,
Marchesoni
,
A.
,
Mease
,
P.
, and
Mielants
,
H.
, and
CASPAR Study Group,
2006
, “
Classification Criteria for Psoriatic Arthritis: Development of New Criteria From a Large International Study
,”
Arthritis Rheum.
,
54
(
8
), pp.
2665
2673
.10.1002/art.21972
51.
Rudwaleit
,
M.
, and
Taylor
,
W. J.
,
2010
, “
Classification Criteria for Psoriatic Arthritis and Ankylosing Spondylitis/Axial Spondyloarthritis
,”
Best Pract. Res. Clin. Rheumatol.
,
24
(
5
), pp.
589
604
.10.1016/j.berh.2010.05.007
52.
Zhang
,
W.
,
2006
, “
EULAR Evidence Based Recommendations for Gout. Part I: Diagnosis. Report of a Task Force of the Standing Committee for International Clinical Studies Including Therapeutics (ESCISIT
),”
Ann. Rheum. Dis.
,
65
(
10
), pp.
1301
1311
.10.1136/ard.2006.055251
53.
Finelli
,
I.
,
Chiessi
,
E.
,
Oddo
,
L.
,
Galesso
,
D.
,
Renier
,
D.
, and
Paradossi
,
G.
,
2014
, “
Collective Dynamics and Transient Behavior of Partially Hydrophobic Hyaluronic Acid Chains
,”
Macromol. Chem. Phys.
,
215
(
2
), pp.
140
147
.10.1002/macp.201300503
54.
Bonnevie
,
E. D.
,
Galesso
,
D.
,
Secchieri
,
C.
,
Cohen
,
I.
, and
Bonassar
,
L. J.
,
2015
, “
Elastoviscous Transitions of Articular Cartilage Reveal a Mechanism of Synergy Between Lubricin and Hyaluronic Acid
,”
PLoS One
,
10
(
11
), p.
e0143415
.10.1371/journal.pone.0143415
55.
Gleghorn
,
J. P.
, and
Bonassar
,
L. J.
,
2008
, “
Lubrication Mode Analysis of Articular Cartilage Using Stribeck Surfaces
,”
J. Biomech.
,
41
(
9
), pp.
1910
1918
.10.1016/j.jbiomech.2008.03.043
56.
de Vicente
,
J.
,
Stokes
,
J. R.
, and
Spikes
,
H. A.
,
2006
, “
Soft Lubrication of Model Hydrocolloids
,”
Food Hydrocoll.
,
20
(
4
), pp.
483
491
.10.1016/j.foodhyd.2005.04.005
57.
de Vicente
,
J.
,
Stokes
,
J. R.
, and
Spikes
,
H. A.
,
2005
, “
Lubrication Properties of Non-Adsorbing Polymer Solutions in Soft Elastohydrodynamic (EHD) Contacts
,”
Tribol. Int.
,
38
(
5
), pp.
515
526
.10.1016/j.triboint.2004.11.001
58.
Cassin
,
G.
,
Heinrich
,
E.
, and
Spikes
,
H. A.
,
2001
, “
The Influence of Surface Roughness on the Lubrication Properties of Adsorbing and Non-Adsorbing Biopolymers
,”
Tribol. Lett.
,
11
(
2
), pp.
95
102
.10.1023/A:1016702906095
59.
Shahrivar
,
K.
,
Ortigosa-Moya
,
E. M.
,
Hidalgo-Alvarez
,
R.
, and
de Vicente
,
J.
,
2019
, “
Isoviscous Elastohydrodynamic Lubrication of Inelastic Non-Newtonian Fluids
,”
Tribol. Int.
,
140
, p.
105707
.10.1016/j.triboint.2019.03.065
60.
Kuznetsova
,
A.
,
Brockhoff
,
P. B.
, and
Christensen
,
R. H. B.
,
2017
, “
LmerTest Package: Tests in Linear Mixed Effects Models
,”
J. Stat. Softw.
,
82
(
13
), pp. 1–26.10.18637/jss.v082.i13
61.
Lenth
,
R.
,
2019
, “
Emmeans: Estimated Marginal Means, Aka Least-Squares Means: R Package Version 1.4
”.https://cran.r-project.org/web/packages/emmeans/index.html
62.
Gleghorn
,
J. P.
,
Jones
,
A. R. C.
,
Flannery
,
C. R.
, and
Bonassar
,
L. J.
,
2009
, “
Boundary Mode Lubrication of Articular Cartilage by Recombinant Human Lubricin
,”
J. Orthop. Res.
,
27
(
6
), pp.
771
777
.10.1002/jor.20798
63.
Reimann
,
I.
,
1976
, “
Pathological Human Synovial Fluids. Viscosity and Boundary Lubricating Properties
,”
Clin. Orthop. Relat. Res.
, (
119
), pp.
237
241
.https://pubmed.ncbi.nlm.nih.gov/954317/
64.
Cooke
,
A. F.
,
Dowson
,
D.
, and
Wright
,
V.
,
1978
, “
The Rheology of Synovial Fluid and Some Potential Synthetic Lubricants for Degenerate Synovial Joints
,”
Eng. Med.
,
7
(
2
), pp.
66
72
.10.1243/EMED_JOUR_1978_007_021_02
65.
Schurz
,
J.
, and
Ribitsch
,
V.
,
1987
, “
Rheology of Synovial Fluid
,”
Biorheology
,
24
(
4
), pp.
385
399
.10.3233/BIR-1987-24404
66.
Fam
,
H.
,
Bryant
,
J. T.
, and
Kontopoulou
,
M.
,
2007
, “
Rheological Properties of Synovial Fluids
,”
Biorheology
,
44
(
2
), pp.
59
74
.https://content.iospress.com/articles/biorheology/bir452
67.
Zhang
,
Z.
,
Barman
,
S.
, and
Christopher
,
G. F.
,
2014
, “
The Role of Protein Content on the Steady and Oscillatory Shear Rheology of Model Synovial Fluids
,”
Soft Matter
,
10
(
32
), pp.
5965
5973
.10.1039/C4SM00716F
68.
Bonnevie
,
E. D.
,
Delco
,
M. L.
,
Galesso
,
D.
,
Secchieri
,
C.
,
Fortier
,
L. A.
, and
Bonassar
,
L. J.
,
2017
, “
Sub-Critical Impact Inhibits the Lubricating Mechanisms of Articular Cartilage
,”
J. Biomech.
,
53
, pp.
64
70
.10.1016/j.jbiomech.2016.12.034
69.
Bonnevie
,
E. D.
,
Galesso
,
D.
,
Secchieri
,
C.
, and
Bonassar
,
L. J.
,
2018
, “
Degradation Alters the Lubrication of Articular Cartilage by High Viscosity, Hyaluronic Acid-Based Lubricants
,”
J. Orthop. Res.
,
36
(
5
), pp.
1456
1464
.10.1002/jor.23782
70.
Shi
,
L.
,
Sikavitsas
,
V. I.
, and
Striolo
,
A.
,
2011
, “
Experimental Friction Coefficients for Bovine Cartilage Measured With a Pin-on-Disk Tribometer: Testing Configuration and Lubricant Effects
,”
Ann. Biomed. Eng.
,
39
(
1
), pp.
132
146
.10.1007/s10439-010-0167-3
71.
Lane
,
N. E.
,
Brandt
,
K.
,
Hawker
,
G.
,
Peeva
,
E.
,
Schreyer
,
E.
,
Tsuji
,
W.
, and
Hochberg
,
M. C.
,
2011
, “
OARSI-FDA Initiative: Defining the Disease State of Osteoarthritis
,”
Osteoarthr. Cartil.
,
19
(
5
), pp.
478
482
.10.1016/j.joca.2010.09.013
72.
Greene
,
G. W.
,
Banquy
,
X.
,
Lee
,
D. W.
,
Lowrey
,
D. D.
,
Yu
,
J.
, and
Israelachvili
,
J. N.
,
2011
, “
Adaptive Mechanically Controlled Lubrication Mechanism Found in Articular Joints
,”
Proc. Natl. Acad. Sci.
,
108
(
13
), pp.
5255
5259
.10.1073/pnas.1101002108
73.
Das
,
S.
,
Banquy
,
X.
,
Zappone
,
B.
,
Greene
,
G. W.
,
Jay
,
G. D.
, and
Israelachvili
,
J. N.
,
2013
, “
Synergistic Interactions Between Grafted Hyaluronic Acid and Lubricin Provide Enhanced Wear Protection and Lubrication
,”
Biomacromolecules
,
14
(
5
), pp.
1669
1677
.10.1021/bm400327a
74.
Elsaid
,
K. A.
,
Machan
,
J. T.
,
Waller
,
K.
,
Fleming
,
B. C.
, and
Jay
,
G. D.
,
2009
, “
The Impact of Anterior Cruciate Ligament Injury on Lubricin Metabolism and the Effect of Inhibiting Tumor Necrosis Factor Alpha on Chondroprotection in an Animal Model
,”
Arthritis Rheum.
,
60
(
10
), pp.
2997
3006
.10.1002/art.24800
75.
Flannery
,
C. R.
,
Zollner
,
R.
,
Corcoran
,
C.
,
Jones
,
A. R.
,
Root
,
A.
,
Rivera-Bermúdez
,
M. A.
,
Blanchet
,
T.
,
Gleghorn
,
J. P.
,
Bonassar
,
L. J.
,
Bendele
,
A. M.
,
Morris
,
E. A.
, and
Glasson
,
S. S.
,
2009
, “
Prevention of Cartilage Degeneration in a Rat Model of Osteoarthritis by Intraarticular Treatment With Recombinant Lubricin
,”
Arthritis Rheum.
,
60
(
3
), pp.
840
847
.10.1002/art.24304
76.
Teeple
,
E.
,
Elsaid
,
K. A.
,
Fleming
,
B. C.
,
Jay
,
G. D.
,
Aslani
,
K.
,
Crisco
,
J. J.
, and
Mechrefe
,
A. P.
,
2008
, “
Coefficients of Friction, Lubricin, and Cartilage Damage in the Anterior Cruciate Ligament-Deficient Guinea Pig Knee
,”
J. Orthop. Res.
,
26
(
2
), pp.
231
237
.10.1002/jor.20492
77.
Jay
,
G. D.
,
Elsaid
,
K. A.
,
Kelly
,
K. A.
,
Anderson
,
S. C.
,
Zhang
,
L.
,
Teeple
,
E.
,
Waller
,
K.
, and
Fleming
,
B. C.
,
2012
, “
Prevention of Cartilage Degeneration and Gait Asymmetry by Lubricin Tribosupplementation in the Rat Following Anterior Cruciate Ligament Transection
,”
Arthritis Rheum.
,
64
(
4
), pp.
1162
1171
.10.1002/art.33461
78.
Cui
,
Z.
,
Xu
,
C.
,
Li
,
X.
,
Song
,
J.
, and
Yu
,
B.
,
2015
, “
Treatment With Recombinant Lubricin Attenuates Osteoarthritis by Positive Feedback Loop Between Articular Cartilage and Subchondral Bone in Ovariectomized Rats
,”
Bone
,
74
, pp.
37
47
.10.1016/j.bone.2014.12.065
79.
Jay
,
G. D.
,
Fleming
,
B. C.
,
Watkins
,
B. A.
,
McHugh
,
K. A.
,
Anderson
,
S. C.
,
Zhang
,
L. X.
,
Teeple
,
E.
,
Waller
,
K. A.
, and
Elsaid
,
K. A.
,
2010
, “
Prevention of Cartilage Degeneration and Restoration of Chondroprotection by Lubricin Tribosupplementation in the Rat Following Anterior Cruciate Ligament Transection
,”
Arthritis Rheum.
,
62
(
8
), pp.
2382
2391
.10.1002/art.27550
80.
Teeple
,
E.
,
Elsaid
,
K. A.
,
Jay
,
G. D.
,
Zhang
,
L.
,
Badger
,
G. J.
,
Akelman
,
M.
,
Bliss
,
T. F.
, and
Fleming
,
B. C.
,
2011
, “
Effects of Supplemental Intra-Articular Lubricin and Hyaluronic Acid on the Progression of Posttraumatic Arthritis in the Anterior Cruciate Ligament–Deficient Rat Knee
,”
Am. J. Sports Med.
,
39
(
1
), pp.
164
172
.10.1177/0363546510378088
81.
Elsaid
,
K. A.
,
Zhang
,
L.
,
Waller
,
K.
,
Tofte
,
J.
,
Teeple
,
E.
,
Fleming
,
B. C.
, and
Jay
,
G. D.
,
2012
, “
The Impact of Forced Joint Exercise on Lubricin Biosynthesis From Articular Cartilage Following ACL Transection and Intra-Articular Lubricin's Effect in Exercised Joints Following ACL Transection
,”
Osteoarthr. Cartil.
,
20
(
8
), pp.
940
948
.10.1016/j.joca.2012.04.021
82.
Waller
,
K. A.
,
Chin
,
K. E.
,
Jay
,
G. D.
,
Zhang
,
L. X.
,
Teeple
,
E.
,
McAllister
,
S.
,
Badger
,
G. J.
,
Schmidt
,
T. A.
, and
Fleming
,
B. C.
,
2017
, “
Intra-Articular Recombinant Human Proteoglycan 4 Mitigates Cartilage Damage After Destabilization of the Medial Meniscus in the Yucatan Minipig
,”
Am. J. Sports Med.
,
45
(
7
), pp.
1512
1521
.10.1177/0363546516686965
83.
Nemirov
,
D.
,
Nakagawa
,
Y.
,
Sun
,
Z.
,
Lebaschi
,
A.
,
Wada
,
S.
,
Carballo
,
C.
,
Deng
,
X.-H.
,
Putnam
,
D.
,
Bonassar
,
L. J.
, and
Rodeo
,
S. A.
,
2020
, “
Effect of Lubricin Mimetics on the Inhibition of Osteoarthritis in a Rat Anterior Cruciate Ligament Transection Model
,”
Am. J. Sports Med.
,
48
(
3
), pp.
624
634
.10.1177/0363546519898691
84.
Koch
,
A. E.
,
2005
, “
Chemokines and Their Receptors in Rheumatoid Arthritis: Future Targets?
,”
Arthritis Rheum.
,
52
(
3
), pp.
710
721
.10.1002/art.20932
85.
Lotz
,
M.
,
Terkeltaub
,
R.
, and
Villiger
,
P. M.
,
1992
, “
Cartilage and Joint Inflammation. Regulation of IL-8 Expression by Human Articular Chondrocytes
,”
J. Immunol.
,
148
(
2
), pp.
466
473
.https://www.jimmunol.org/content/148/2/466.long
86.
Jones
,
A.
,
Hughes
,
C.
,
Wainright
,
S.
,
Flannery
,
C.
,
Little
,
C.
,
Caterson
,
B.
,
Sd
,
W.
,
Cr
,
F.
,
Cb
,
L.
, and
Caterson
,
B.
,
2003
, “
Degradation of PRG4/SZP by Matrix Proteases [Abstract]
,”
49th Annual Meeting on Orthopedics Research Society
, Vol.
28
,
New Orleans, LA
, Feb. 2–5,
Paper No. #0133
.https://www.ors.org/Transactions/49/0133.pdf
87.
Elsaid
,
K. A.
,
Chichester
,
C. O.
, and
Jay
,
G. D.
,
2005
, “
Cathepsin B and Neutrophil Elastase Degrade Lubricin and Increase Friction in Excised Murine Joints [Abstract]
,” Trans. Orthop. Res. Soc.,
30
(
924
),
Paper No. 924
.https://www.ors.org/Transactions/51/0924.pdf
88.
Cook
,
S. G.
, and
Bonassar
,
L. J.
,
2020
, “
Interaction With Cartilage Increases the Viscosity of Hyaluronic Acid Solutions
,”
ACS Biomater. Sci. Eng.
,
6
(
5
), pp.
2787
2795
.10.1021/acsbiomaterials.0c00100
89.
Majd
,
S. E.
,
Kuijer
,
R.
,
Köwitsch
,
A.
,
Groth
,
T.
,
Schmidt
,
T. A.
, and
Sharma
,
P. K.
,
2014
, “
Both Hyaluronan and Collagen Type II Keep Proteoglycan 4 (Lubricin) at the Cartilage Surface in a Condition That Provides Low Friction During Boundary Lubrication
,”
Langmuir
,
30
(
48
), pp.
14566
14572
.10.1021/la504345c
You do not currently have access to this content.