The effect of glycosaminoglycan depletion on the friction and deformation of articular cartilage

Abstract

Glycosaminoglycans (GAGs) have been shown to be responsible for the interstitial fluid pressurization of articular cartilage and hence its compressive stiffness and load-bearing properties. Contradictory evidence has been presented in the literature on the effect of depleting GAGs on the friction properties of articular cartilage. The aim of this study was to investigate the effect of depleting GAGs on the friction and deformation characteristics of articular cartilage under different tribological conditions.

A pin-on-plate machine was utilized to measure the coefficient of friction of native and chondroitinase ABC (CaseABC)-treated articular cartilage under two different models: static (4 mm/s start-up velocity) and dynamic (4 mm/s sliding velocity; 4 mm stroke length) under a load of 25 N (0.4 MPa contact stress) and with phosphate-buffered saline as the lubricant. Indentation tests were carried out at 1 N and 2 N loads (0.14 MPa and 0.28 MPa contact stress levels) to study the deformation characteristics of both native and GAG-depleted cartilage samples.

CaseABC treatment rendered the cartilage tissue soft owing to the loss of compressive stiff-ness and a sulphated-sugar assay confirmed the loss of GAGs from the cartilage samples. CaseABC treatment significantly increased (by more than 50 per cent) the friction levels in the dynamic model (p < 0.05) at higher loading times owing to the loss of biphasic lubrication. CaseABC treatment had no effect on friction in the static model in which the cartilage surfaces did not have an opportunity to recover fluid because of static loading unlike the cartilage tissue in the dynamic model, in which translation of the cartilage surfaces was involved, ensuring effective biphasic lubrication. Therefore the depletion of GAGs had a smaller effect on the coefficient of friction for the static model. Indentation tests showed that GAG-depleted cartilage samples had a lower elastic modulus and higher permeability than native tissue. These results corroborate the role of GAGs in the compressive and friction properties of articular cartilage and emphasize the need for developing strategies to control GAG loss from diseased articular cartilage tissue.

Keywords

cartilage glycosaminoglycans friction chondroitinase ABC deformation

Get full access to this article

View all access options for this article.

References

Ateshian

G. A.

Lai

W. M.

Zhu

W. B.

Mow

V. C.

An asymptotic solution for the contact of two biphasic cartilage layers. J. Biomechanics, 1994, 27(11), 1347–1360.

Forster

Fisher

The influence of loading time and lubricant on the friction of articular cartilage. Proc. Instn Mech. Engrs, Part H: J. Engineering in Medicine, 1996, 210(H2), 109–119.

Mow

V. C.

Kuei

S. C.

Lai

W. M.

Armstrong

C. G.

Biphasic creep and stress relaxation of articular cartilage in compression: Theory and experiments. J. Biomech. Engng, 1980, 102(1), 73–84.

Sasada

Abe

Morita

Mabuchi

Role of chondroitin sulfate in the low friction property of articular cartilages. In Proceedings of the Fifth Kobe International Forum on Biotribology, Kobe, Japan, 2005, pp. 64–67 (Japanese Society of Biotribologists, Japan).

Schiller

Arnhold

Benard

Reichl

Arnold

Cartilage degradation by hyaluronate lyase and chondroitin ABC lyase: A MALDI-TOF mass spectrometric study. Carbohydrate Res., 1999, 318(1-4), 116–122.

Pickard

Ingham

Egan

Fisher

Investigation into the effect of proteoglycan molecules on the tribological properties of cartilage joint tissues. Proc. Instn Mech. Engrs, Part H: J. Engineering in Medicine, 1998, 212(H3), 177–182.

Zhu

Mow

V. C.

Koob

T. J.

Eyre

D. R.

Viscoelastic shear properties of articular cartilage and the effects of glycosidase treatments. J. Orthop. Res., 1993, 11(6), 771–181.

Schmidt

M. B.

Mow

V. C.

Chun

L. E.

Eyre

D. R.

Effects of proteoglycan extraction on the tensile behavior of articular cartilage. J. Orthop. Res., 1990, 8(3), 353–163.

Basalo

I. M.

Mauck

R. L.

Kelly

T.-A. N.

Nicoll

S. B.

Chen

F. H.

Hung

C. T.

Ateshian

G. A.

Cartilage interstitial fluid load support in unconfined compression following enzymatic digestion. J. Biomech. Engng, 2004, 126(6), 779–786.

10.

Basalo

I. M.

Raj

Krishnan

Chen

F. H.

Hung

C. T.

Ateshian

G. A.

Effects of enzymatic degradation on the frictional response of articular cartilage in stress relaxation. J. Biomechanics, 2005, 38(6), 1343–1349.

11.

Rieppo

Toyras

Nieminen

M. T.

Kovanen

Hyttinen

M. M.

Korhonen

R. K.

Jurvelin

J. S.

Helminen

H. J.

Structure—function relationships in enzymatically modified articular cartilage. Cells Tissues Organs, 2003, 175(3), 121–132.

12.

Chen

A. C.

Nguyen

T. T.

Sah

R. L.

Streaming potentials during the confined compression creep test of normal and proteoglycan-depleted cartilage. Ann. Biomed. Engng, 1997, 25(2), 269–277.

13.

Basalo

I. M.

Chen

F. H.

Hung

C. T.

Ateshian

G. A.

Frictional response of bovine articular cartilage under creep loading following proteoglycan digestion with chondroitinase ABC. J. Biomech. Engng, 2006, 128(1), 131–134.

14.

Katta

Pawaskar

Jin

Ingham

Fisher

Effect of load variation on the friction properties of articular cartilage. Proc. IMechE, Part J: J. Engineering Tribology, 2007, 221(3), 175–181.

15.

Bell

C. J.

Carrick

L. M.

Katta

Jin

Ingham

Aggeli

Boden

Waigh

T. A.

Fisher

Self-assembling peptides as injectable lubricants for osteoarthritis. J. Biomed. Mater. Res. A, 2006, 78(2), 236–246.

16.

Mow

V. C.

Ateshian

G. A.

Friction, lubrication and wear of diarthrodial joints. In Basic orthopaedic biomechanics (Eds Mow

V. C.

Hayes

W. C.

), second edition, 1997 (Raven Press, New York).

17.

Graindorge

Ferrandez

Ingham

Jin

Twigg

Fisher

The role of the surface amorphous layer of articular cartilage in joint lubrication. Proc. IMechE, Part H: J. Engineering in Medicine, 2006, 220(H5), 597–607.

18.

Crockett

Roos

Rossbach

Dora

Born

Troxler

Imaging of the surface of human and bovine articular cartilage with ESEM and AFM. Tribology Lett., 2005, 19(4), 311–317.

19.

Crockett

Grubelnik

Roos

Dora

Born

Troxler

Biochemical composition of the superficial layer of articular cartilage. J. Biomed. Mater. Res. A, 2007, 82(4), 958–964.

20.

Mak

A. F.

Lai

W. M.

Mow

V. C.

Biphasic indentation of articular cartilage — I. Theoretical analysis. J. Biomechanics, 1987, 20(7), 703–714.

21.

Mow

V. C.

Gibbs

M. C.

Lai

W. M.

Zhu

W. B.

Athanasiou

K. A.

Biphasic indentation of articular cartilage — II. A numerical algorithm and an experimental study. J. Biomechanics, 1989, 22(8-9), 853–861.

22.

Bonassar

L. J.

Frank

E. H.

Murray

J. C.

Paguio

C. G.

Moore

V. L.

Lark

M. W.

Sandy

J. D.

J.-J.

Eyre

D. R.

Grodzinsky

A. J.

Changes in cartilage composition and physical properties due to stromelysin degradation. Arthritis Rheum., 1995, 38(2), 173–183.

23.

Caligaris

Ateshian

G. A.

Migrating articular contact areas promote sustainable low friction coefficients. In Proceedings of the 52nd Annual Meeting of the Orthopaedic Research Society, Chicago, Illinois, USA, 2006, p. 83 (Orthopaedic Research Society, Rosemont, Illinois).

24.

Naka

M. H.

Morita

Ikeuchi

Influence of proteoglycan contents and of tissue hydration on the frictional characteristics of articular cartilage. Proc. IMechE, Part H: J. Engineering in Medicine, 2005, 219(H3), 175–182.

25.

Kumar

Oka

Toguchida

Kobayashi

Uchida

Nakamura

Tanaka

Role of uppermost superficial surface layer of articular cartilage in the lubrication mechanism of joints. J. Anatomy, 2001, 199(3), 241–250.

26.

Bell

C. J.

Ingham

Fisher

Influence of hyaluronic acid on the time-dependent friction response of articular cartilage under different conditions. Proc. IMechE, Part H: J. Engineering in Medicine, 2006, 220(H1), 23–31.