LUBRICATION OF DIARTHRODIAL JOINTS: BASIC CONCEPTS M. Marcoux and P. Lamothe* IT WOULD APPEAR self-evident that the functional integrity of diarthrodial joints requires that they possess low frictional properties (1, 6, 7). Many different concepts of lubrication have been postulated to account for the low friction present in articulations. At first, joint surfaces were compared to mechanical bearings, most of which are lubricated hydrodynamically by oil. The relatively continuous motion of the surface produces a wedge of lubricant which keeps them apart (11). In joints, synovial fluid and its viscosity had always been considered very important in the lubrication of articular cartilage. More importance was attributed to synovia when it was demonstrated with synovial fluid and plastic materials that a fluid-film could be maintained between surfaces with loads two or three times as great as those encountered physiologically (22). It was then felt that the higher the viscosity, the better was the resistance of the joint to trauma. Charnley (3) later pointed out that hydrodynamic lubrication was impossible in animal joints because they oscillate slowly, stopping at each reversal of motion, thus precluding the maintenance of a fluidfilm. The fact that joint fluid does not effectively lubricate mechanical bearings supports this theory. In 1959, Lewis and McCutchen (8) suggested that weeping of cartilage could play an important role in lubrication. By weeping, they meant that mucopolysaccharides are extruded from the cartilage as pressure is applied to it. McCutchen (12) then proceeded to show that articular cartilage, even when wiped free of synovial fluid, retains much of its low frictional properties thus giving his theory experimental support. The same author later demonstrated that under loads, weeping elastic surfaces can achieve a coefficient of friction of the same order of magnitude as those of animal joints and that this coefficient of friction decreases as the load increases (13). Radin et al (17) recently showed the positive role played by weeping in joint lubrication. Using an experimental arthrotrypsometer designed by Linn (9), in which cartilage is rubbed against cartilage, they obtained data to show
that hydrostatic lubrication or weeping lubrication plays a significant function in joints. Radin and his associates stated that weeping of cartilage could well be the most important mechanism in protecting articular cartilage from damage in certain high load situations. Another means of articular lubrication had been suggested by Chamley (3) when he submitted the idea that mucin exerted its lubricating ability by actually binding to the cartilage surface, thus interposing a thin layer of molecules between joint surfaces. An experimental study performed seven years later gave boundary lubrication more emphasis. Using rubber against glass for the experiment, it was shown that films of adsorbed mucin molecules will, under certain mechanical pressures, resist being extruded between the rubber and the glass. Considerable reduction in the thickness of the film could be attained before the molecules were effectively extruded (14). This does not demonstrate that this sort of osmotic lubrication is the mechanism employed in joint lubrication but only that it could be under plausible statistical conditions. New concepts of diarthrodial lubrication have been established in the last decade. These started mainly when Dintinfass (4) showed that the hyaluronic acid of the synovial fluid could be depolymerized without loss of lubricating advantage to the cartilage. This meant that the lubricating action of the synovia on cartilage was not viscosity dependent. Linn and Radin (10) demonstrated this experimentally using the canine tarsal joint and bovine synovial mucin. Lowered viscosity due to treatment of the mucin with testicular hyaluronidase had no effect on the coefficient of friction. Testicular hyaluronidose has the ability to break down the hyaluronic acid molecule thus causing the viscosity to be lowered. By contrast, tryptic digestion destroyed the ability of the mucin to lubricate without reducing the viscosity. The effect of a proteolytic enzyme such as trypsin does not affect the hyaluronic acid molecule and thus, does not influence the viscosity of the fluid. These observations indicate that a protein is an important intrinsic component of the mucin molecule and that, together with the hyaluronate, it is responsible for the function of the mucin as a lubricant. Simon (23) did a similar experiment with human articular cartilage. Synovial fluid had
'Departement de Mcdecine, Faculte de Medc-
cine veterinaire de l'Universite de Montreal, C.P.
5000, Saint-Hyacinthe, Quebec J2S 7C6.
'41 CAN. VET. JOUR., vol. 18, no. 9, September, 1977
CANADIAN VETERINARY JOURNAL
a distinct wear-protecting effect which could be eliminated by digestion of the mucin with trypsin but not with testicular hyaluronidase. In accordance with these experiments, a glycoprotein which possesses lubricating ability has been recently isolated from the synovial fluid; the removal of this fraction from the synovia deprives it of its lubricating advantages over buffer even though the hyaluronate remains (21). Elasticity of the articular cartilage is also very important in joint lubrication. The friction coefficient goes up when the cartilage is deprived of its weeping ability due to loss of elasticity (10) and from a purely mechanical standpoint, the presence of elastic rather than plastic behavior increases the efficiency of gliding surfaces by reducing the coefficient of friction. Elasticity reduces the velocity gradient at the articular surface through absorption and redistribution of forces. This ability to absorb significant forces may also protect subchondral bone from fracturing (2). Elasticity also enables the microscopic asperities of the cartilage to be pushed out of the way thus providing an elasto-hydrodynamic effect which should lower the friction considerably (5). In the early phases of loading, the depressions of the irregular cartilage surface tend to trap the fluid (26) and as a result of further deformation, the spaces between the opposing cartilage surfaces narrow down more at the margin than at the center thus resulting in more fluids trapped in the center of the contact area (5) where it helps to form a squeezefilm (fluid lubrication). Surface filtration of the cartilage then lets the fluids go but retains the hyaluronate molecules which are then trapped and hence provide a type of "boosted
which are the determinants of viscosity (16). Just recently, it has been shown that articular soft tissue lubrication depends mainly on the presence of hyaluronate in the lubricating fluid since viscous solutions containing no hyaluronate do not lubricate nearly as well as solutions of hyaluronate of equal or even lower viscosity (20). The difference is explainable by boundary lubrication. In this type of lubrication, the hyaluronate molecules stick to the surface of the synovial membrane. The importance of hyaluronate and boundary lubrication had also been mentioned by another author (18). Radin and Paul (19) summarized all these experiments on joint lubrication very well. They concluded that there are two lubricating systems present in a diarthrosis. One for the soft tissue which is of the boundary type and is hyaluronate dependent. The other, for the cartilage, is dependent on glyco-proteins at low loads and on a fluid squeeze-film at high loads, in which hyaluronic acid plays a role. SUMMARY
A review of the literature concerning the lubrication of diarthrodial joints is presented. From it, we can conclude it emerges that there are two lubricating systems in a diarthrosis. One, for soft tissue, is dependent on hyaluronic acid molecules and the other, for cartilage, relies on glycoproteins at low loads and on hyaluronic acid at high loads.
REsuME Cette revue de la litterature s'interesse aux modes de lubrification des articulations diarthrodiales. On peut en conclure qu'il existe deux systemes de lubrification intra-articulaire. L'un, pour les tissus mous, depend de la presence de molecules d'acide hyaluronique et l'autre, pour le cartilage, depend de la presence de glycoproteines lorsque la pression est faible, et de molecules d'acide hyaluronique lorsque la pression augmente.
lubrication" (25). Experimental work done in 1963 by Soko-
loff (24) yielded evidence that articular cartilage had this ability to concentrate synovial mucin on its surface. This was based on the fact that articular cartilage recovered its original form promptly after being under experimental load, suggesting that it selectively excluded the long chain polymers while allowing water and electrolytes to reenter the tissues. In regard to soft tissue lubrication, McCutchen (15) had demonstrated that the thixotropic nature of synovial fluid was directly related to its molecular size and mentioned that mucin played an important role as a diarthrodial soft tissue lubricant. The lubricating ability of synovial fluid has been mentioned to be dependent on the concentration and the molecular weight of the hyaluronic acid molecules,
REFERENCES 1. BARNETT, C. H. and A. F. COBBOLD. Lubrication within living joints. J. Bone Jt Surg. 44: 662-674. 1962. 2. CAMOSSO, M. E. and G. MAROTTI. The me-
chanical behavior of articular cartilage under compressive stress. J. Bone Jt Surg. 44: 699709. 1962.
242
BASIC CONCEPTS
3. CHARNLEY, J. The lubrication of animal joints. In Symposium on Biomechanics, Institute of Mechanical Engineers. London, England. 1959. 4. DINTINFAss, L. Lubrication in synovial joints. A theorical analysis. A rheological approach to the problems of joint movements and joint lubrication. J. Bone Jt Surg. 45: 1241-1256. 1963. 5. DoWSON, D. Models of lubrication in human joints. Proc. Inst. Mech. Engrs 181: 45-54. 1967. 6. FUKUOKA, Y. An experimental study of articular lubrication. Igaku Kenkyo 34: 100-110. 1964. 7. JONES, E. W. Joint lubrication. Lancet 1: 1043-1044. 1936. 8. LEWIS, P. R. and C. W. MCCUTCHEN. Mechanism of animal joints: experimental evidence for weeping lubrication in mammalian joints. Nature, Lond. 184: 1285. 1959. 9. LINN, F. C. Lubrication of animal joints. The arthrotripsometer. J. Bone Jt Surg. 49: 1079-1098. 1967. 10. LINN, F. C. and E. L. RADIN. Lubrication of animal joints. The effect of certain chemical alterations of the cartilage and lubricant. Arthritis Rheum. 11: 674-682. 1968. 11. MACCONAIL, M. A. The movements of bones and joints. The synovial fluid and its assistants. J. Bone Jt Surg. 32: 244-252. 1950. 12. MCCUTCHEN, C. W. Mechanism of animal joints. Sponge hydrostatic and weeping bearings. Nature, Lond. 184: 1284-1285. 1959. 13. MCCUTCHEN, C. W. The frictional properties of animal joints. Wear 5: 1-17. 1962. 14. MCCUTCHEN, C. W. Boundary lubrication by synovial fluid. Demonstration and possible osmotic explanation. Fedn Proc. 25: 10611068. 1966. 15. MCCUTCHEN, C. W. Why did nature make synovial fluid slimy? Proceedings of the Work-
shop on Cartilage Degradation and Repair. London, England. 1967. 16. OGSTON, A. G. and J. E. STANIER. Some effects of hyaluronidase on the hyaluronic acid of ox synovial fluid and their bearing on the investigation of pathological fluids. J. Physiol., Lond. 119: 253-258. 1953. 17. RADIN, E. L., I. L. PAUL and D. POLLOCK. Animal joint behavior under excessive loading. Nature, Lond. 226: 554-555. 1970. 18. RADIN, E. L., I. L. PAUL, D. A. SWANN and E. S. SCHOTTSTAEDT. Lubrication of synovial membrane. Ann. Rheum. Dis. 30: 322-325. 1971. 19. RADIN, E. L. and I. L. PAUL. A consolidated concept of joint lubrication. J. Bone Jt Surg. 54: 607-616. 1972. 20. RADIN, E. L., I. L. PAUL and P. A. WEISSER. Joint lubrication with artificial lubricants. Arthritis Rheum. 14: 126-129. 1971. 21. RADIN, E. L., D. A. SWANN and P. A. WEISSER. Separation of a hyaluronate-free lubricating fraction from synovial fluid. Nature, Lond. 228: 377-378. 1970. 22. ROPES, M. W., W. B. ROBERTSON, E. C. RossMEILS, R. B. PEABODY and W. BAUER. Synovial fluid mucin. Acta med. scand. 196:
700-744. 1947. 23. SIMON, W. H. Wear properties of articular cartilage in-vitro. J. Biochem. 4: 379-389. 1971. 24. SOKOLOFF, L. Elasticity of articular cartilage. Effects of ions and viscous solutions. Science 141: 1055-1057. 1963. 25. TANNER, R. I. On alternative mechanism for the lubrication of synovial joints. Phys. med. Biol. 11: 119-127. 1966. 26. WALKER, P. S., D. DowsON, M. D. LONGFIELD and V. WRIGHT. Booster lubrication in synovial joints by fluid entrapment and enrichment. Ann. Rheum. Dis. 27: 512-520. 1968.
RESEARCH GRANTS INVITED Applications are invited for grants in aid of research on animal disease in Canada. Preferred application dates are January 31 or July 31 each year. For further information contact: J. R. Kinney, Secretary Canadian Veterinary Research Trust Fund 360 Bronson Avenue Ottawa, Ontario KIR 6J3
243
that hydrostatic lubrication or weeping lubrication plays a significant function in joints. Radin and his associates stated that weeping of cartilage could well be the most important mechanism in protecting articular cartilage from damage in certain high load situations. Another means of articular lubrication had been suggested by Chamley (3) when he submitted the idea that mucin exerted its lubricating ability by actually binding to the cartilage surface, thus interposing a thin layer of molecules between joint surfaces. An experimental study performed seven years later gave boundary lubrication more emphasis. Using rubber against glass for the experiment, it was shown that films of adsorbed mucin molecules will, under certain mechanical pressures, resist being extruded between the rubber and the glass. Considerable reduction in the thickness of the film could be attained before the molecules were effectively extruded (14). This does not demonstrate that this sort of osmotic lubrication is the mechanism employed in joint lubrication but only that it could be under plausible statistical conditions. New concepts of diarthrodial lubrication have been established in the last decade. These started mainly when Dintinfass (4) showed that the hyaluronic acid of the synovial fluid could be depolymerized without loss of lubricating advantage to the cartilage. This meant that the lubricating action of the synovia on cartilage was not viscosity dependent. Linn and Radin (10) demonstrated this experimentally using the canine tarsal joint and bovine synovial mucin. Lowered viscosity due to treatment of the mucin with testicular hyaluronidase had no effect on the coefficient of friction. Testicular hyaluronidose has the ability to break down the hyaluronic acid molecule thus causing the viscosity to be lowered. By contrast, tryptic digestion destroyed the ability of the mucin to lubricate without reducing the viscosity. The effect of a proteolytic enzyme such as trypsin does not affect the hyaluronic acid molecule and thus, does not influence the viscosity of the fluid. These observations indicate that a protein is an important intrinsic component of the mucin molecule and that, together with the hyaluronate, it is responsible for the function of the mucin as a lubricant. Simon (23) did a similar experiment with human articular cartilage. Synovial fluid had
'Departement de Mcdecine, Faculte de Medc-
cine veterinaire de l'Universite de Montreal, C.P.
5000, Saint-Hyacinthe, Quebec J2S 7C6.
'41 CAN. VET. JOUR., vol. 18, no. 9, September, 1977
CANADIAN VETERINARY JOURNAL
a distinct wear-protecting effect which could be eliminated by digestion of the mucin with trypsin but not with testicular hyaluronidase. In accordance with these experiments, a glycoprotein which possesses lubricating ability has been recently isolated from the synovial fluid; the removal of this fraction from the synovia deprives it of its lubricating advantages over buffer even though the hyaluronate remains (21). Elasticity of the articular cartilage is also very important in joint lubrication. The friction coefficient goes up when the cartilage is deprived of its weeping ability due to loss of elasticity (10) and from a purely mechanical standpoint, the presence of elastic rather than plastic behavior increases the efficiency of gliding surfaces by reducing the coefficient of friction. Elasticity reduces the velocity gradient at the articular surface through absorption and redistribution of forces. This ability to absorb significant forces may also protect subchondral bone from fracturing (2). Elasticity also enables the microscopic asperities of the cartilage to be pushed out of the way thus providing an elasto-hydrodynamic effect which should lower the friction considerably (5). In the early phases of loading, the depressions of the irregular cartilage surface tend to trap the fluid (26) and as a result of further deformation, the spaces between the opposing cartilage surfaces narrow down more at the margin than at the center thus resulting in more fluids trapped in the center of the contact area (5) where it helps to form a squeezefilm (fluid lubrication). Surface filtration of the cartilage then lets the fluids go but retains the hyaluronate molecules which are then trapped and hence provide a type of "boosted
which are the determinants of viscosity (16). Just recently, it has been shown that articular soft tissue lubrication depends mainly on the presence of hyaluronate in the lubricating fluid since viscous solutions containing no hyaluronate do not lubricate nearly as well as solutions of hyaluronate of equal or even lower viscosity (20). The difference is explainable by boundary lubrication. In this type of lubrication, the hyaluronate molecules stick to the surface of the synovial membrane. The importance of hyaluronate and boundary lubrication had also been mentioned by another author (18). Radin and Paul (19) summarized all these experiments on joint lubrication very well. They concluded that there are two lubricating systems present in a diarthrosis. One for the soft tissue which is of the boundary type and is hyaluronate dependent. The other, for the cartilage, is dependent on glyco-proteins at low loads and on a fluid squeeze-film at high loads, in which hyaluronic acid plays a role. SUMMARY
A review of the literature concerning the lubrication of diarthrodial joints is presented. From it, we can conclude it emerges that there are two lubricating systems in a diarthrosis. One, for soft tissue, is dependent on hyaluronic acid molecules and the other, for cartilage, relies on glycoproteins at low loads and on hyaluronic acid at high loads.
REsuME Cette revue de la litterature s'interesse aux modes de lubrification des articulations diarthrodiales. On peut en conclure qu'il existe deux systemes de lubrification intra-articulaire. L'un, pour les tissus mous, depend de la presence de molecules d'acide hyaluronique et l'autre, pour le cartilage, depend de la presence de glycoproteines lorsque la pression est faible, et de molecules d'acide hyaluronique lorsque la pression augmente.
lubrication" (25). Experimental work done in 1963 by Soko-
loff (24) yielded evidence that articular cartilage had this ability to concentrate synovial mucin on its surface. This was based on the fact that articular cartilage recovered its original form promptly after being under experimental load, suggesting that it selectively excluded the long chain polymers while allowing water and electrolytes to reenter the tissues. In regard to soft tissue lubrication, McCutchen (15) had demonstrated that the thixotropic nature of synovial fluid was directly related to its molecular size and mentioned that mucin played an important role as a diarthrodial soft tissue lubricant. The lubricating ability of synovial fluid has been mentioned to be dependent on the concentration and the molecular weight of the hyaluronic acid molecules,
REFERENCES 1. BARNETT, C. H. and A. F. COBBOLD. Lubrication within living joints. J. Bone Jt Surg. 44: 662-674. 1962. 2. CAMOSSO, M. E. and G. MAROTTI. The me-
chanical behavior of articular cartilage under compressive stress. J. Bone Jt Surg. 44: 699709. 1962.
242
BASIC CONCEPTS
3. CHARNLEY, J. The lubrication of animal joints. In Symposium on Biomechanics, Institute of Mechanical Engineers. London, England. 1959. 4. DINTINFAss, L. Lubrication in synovial joints. A theorical analysis. A rheological approach to the problems of joint movements and joint lubrication. J. Bone Jt Surg. 45: 1241-1256. 1963. 5. DoWSON, D. Models of lubrication in human joints. Proc. Inst. Mech. Engrs 181: 45-54. 1967. 6. FUKUOKA, Y. An experimental study of articular lubrication. Igaku Kenkyo 34: 100-110. 1964. 7. JONES, E. W. Joint lubrication. Lancet 1: 1043-1044. 1936. 8. LEWIS, P. R. and C. W. MCCUTCHEN. Mechanism of animal joints: experimental evidence for weeping lubrication in mammalian joints. Nature, Lond. 184: 1285. 1959. 9. LINN, F. C. Lubrication of animal joints. The arthrotripsometer. J. Bone Jt Surg. 49: 1079-1098. 1967. 10. LINN, F. C. and E. L. RADIN. Lubrication of animal joints. The effect of certain chemical alterations of the cartilage and lubricant. Arthritis Rheum. 11: 674-682. 1968. 11. MACCONAIL, M. A. The movements of bones and joints. The synovial fluid and its assistants. J. Bone Jt Surg. 32: 244-252. 1950. 12. MCCUTCHEN, C. W. Mechanism of animal joints. Sponge hydrostatic and weeping bearings. Nature, Lond. 184: 1284-1285. 1959. 13. MCCUTCHEN, C. W. The frictional properties of animal joints. Wear 5: 1-17. 1962. 14. MCCUTCHEN, C. W. Boundary lubrication by synovial fluid. Demonstration and possible osmotic explanation. Fedn Proc. 25: 10611068. 1966. 15. MCCUTCHEN, C. W. Why did nature make synovial fluid slimy? Proceedings of the Work-
shop on Cartilage Degradation and Repair. London, England. 1967. 16. OGSTON, A. G. and J. E. STANIER. Some effects of hyaluronidase on the hyaluronic acid of ox synovial fluid and their bearing on the investigation of pathological fluids. J. Physiol., Lond. 119: 253-258. 1953. 17. RADIN, E. L., I. L. PAUL and D. POLLOCK. Animal joint behavior under excessive loading. Nature, Lond. 226: 554-555. 1970. 18. RADIN, E. L., I. L. PAUL, D. A. SWANN and E. S. SCHOTTSTAEDT. Lubrication of synovial membrane. Ann. Rheum. Dis. 30: 322-325. 1971. 19. RADIN, E. L. and I. L. PAUL. A consolidated concept of joint lubrication. J. Bone Jt Surg. 54: 607-616. 1972. 20. RADIN, E. L., I. L. PAUL and P. A. WEISSER. Joint lubrication with artificial lubricants. Arthritis Rheum. 14: 126-129. 1971. 21. RADIN, E. L., D. A. SWANN and P. A. WEISSER. Separation of a hyaluronate-free lubricating fraction from synovial fluid. Nature, Lond. 228: 377-378. 1970. 22. ROPES, M. W., W. B. ROBERTSON, E. C. RossMEILS, R. B. PEABODY and W. BAUER. Synovial fluid mucin. Acta med. scand. 196:
700-744. 1947. 23. SIMON, W. H. Wear properties of articular cartilage in-vitro. J. Biochem. 4: 379-389. 1971. 24. SOKOLOFF, L. Elasticity of articular cartilage. Effects of ions and viscous solutions. Science 141: 1055-1057. 1963. 25. TANNER, R. I. On alternative mechanism for the lubrication of synovial joints. Phys. med. Biol. 11: 119-127. 1966. 26. WALKER, P. S., D. DowsON, M. D. LONGFIELD and V. WRIGHT. Booster lubrication in synovial joints by fluid entrapment and enrichment. Ann. Rheum. Dis. 27: 512-520. 1968.
RESEARCH GRANTS INVITED Applications are invited for grants in aid of research on animal disease in Canada. Preferred application dates are January 31 or July 31 each year. For further information contact: J. R. Kinney, Secretary Canadian Veterinary Research Trust Fund 360 Bronson Avenue Ottawa, Ontario KIR 6J3
243
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