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The boundary lubrication mechanism at the articulating surface of natural synovial joints has been the subject of much discussion in tribology. In this study, to elucidate the lubricating function of the superficial area of articular cartilage and synovial fluid (SF), cartilage specimens were processed with four different treatments: gentle and severe washing with detergent, incubation in NaCl solution, and trypsin digestion to selectively remove certain constituents from the cartilage surface. Subsequently, the frictional characteristics were examined in phosphate-buffered saline (PBS) and SF against glass. Angularly reciprocating sliding tests with a spherical glass probe and square articular cartilage specimens were performed at low contact loads in the mN range to extract the frictional behavior in the superficial area of the cartilage specimens. Meanwhile, the cartilage surface was observed to confirm the effects of treatments on the morphology of the cartilage surface using a fluorescence microscope and water-immersion methods. The coefficient of friction (COF) of the prepared cartilage specimens was varied from 0.05 to over 0.3 in PBS. However, a certain group of cartilage specimens exhibited a low COF of less than 0.1 with limited variation. For the low COF group of specimens, all four treatments increased the COF in PBS to different extents, and fluorescence microscopy revealed that the integrity of the cartilage surface was deteriorated by treatments. This means that the intact cartilage surface had lubricating constituents to maintain low friction, and the removal of such constituents resulted in the loss of the intrinsic boundary lubricity of the cartilage surface. The variation in the COF of the cartilage specimens was suppressed in SF because it had a clear boundary lubrication effect on the cartilage surface. The lubricating effect of SF could be confirmed even after degenerative treatment.


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Experimental study on boundary lubricity of superficial area of articular cartilage and synovial fluid

Show Author's information Wenxiao LI1( )Takehiro MORITA1,2Yoshinori SAWAE1,2,3
Departure of Mechanical Engineering, Kyushu University, Fukuoka 8190395, Japan
International Institute for Carton-Neutral Energy Research, Kyushu University, Fukuoka 8190395, Japan
Advanced Research Center for Biomechanics, Kyushu University, Fukuoka 8190395, Japan

Abstract

The boundary lubrication mechanism at the articulating surface of natural synovial joints has been the subject of much discussion in tribology. In this study, to elucidate the lubricating function of the superficial area of articular cartilage and synovial fluid (SF), cartilage specimens were processed with four different treatments: gentle and severe washing with detergent, incubation in NaCl solution, and trypsin digestion to selectively remove certain constituents from the cartilage surface. Subsequently, the frictional characteristics were examined in phosphate-buffered saline (PBS) and SF against glass. Angularly reciprocating sliding tests with a spherical glass probe and square articular cartilage specimens were performed at low contact loads in the mN range to extract the frictional behavior in the superficial area of the cartilage specimens. Meanwhile, the cartilage surface was observed to confirm the effects of treatments on the morphology of the cartilage surface using a fluorescence microscope and water-immersion methods. The coefficient of friction (COF) of the prepared cartilage specimens was varied from 0.05 to over 0.3 in PBS. However, a certain group of cartilage specimens exhibited a low COF of less than 0.1 with limited variation. For the low COF group of specimens, all four treatments increased the COF in PBS to different extents, and fluorescence microscopy revealed that the integrity of the cartilage surface was deteriorated by treatments. This means that the intact cartilage surface had lubricating constituents to maintain low friction, and the removal of such constituents resulted in the loss of the intrinsic boundary lubricity of the cartilage surface. The variation in the COF of the cartilage specimens was suppressed in SF because it had a clear boundary lubrication effect on the cartilage surface. The lubricating effect of SF could be confirmed even after degenerative treatment.

Keywords: boundary lubrication, articular cartilage, synovial fluid, the uppermost superficial layer

References(70)

[1]
Murakami T, Nakashima K, Yarimitsu S, Sawae Y, Sakai N. Effectiveness of adsorbed film and gel layer in hydration lubrication as adaptive multimode lubrication mechanism for articular cartilage. Proc Inst Mech Eng Part J J Eng Tribol 225(12): 1174–1185 (2011)
[2]
Eyre D. Articular cartilage and changes in Arthritis: Collagen of articular cartilage. Arthritis Res Ther 4(1): 30 (2001)
[3]
Lane J M, Weiss C. Review of articular cartilage collagen research. Arthritis Rheum 18(6): 553–562 (1975)
[4]
Murakami T, Nakashima K, Sawae Y, Sakai N, Hosoda N. Roles of adsorbed film and gel layer in hydration lubrication for articular cartilage. Proc Inst Mech Eng Part J J Eng Tribol 223(3): 287–295 (2009)
[5]
Kumar P, Oka M, Toguchida J, Kobayashi M, Uchida E, Nakamura T, Tanaka K. Role of uppermost superficial surface layer of articular cartilage in the lubrication mechanism of joints. J Anat 199(3): 241–250 (2001)
[6]
Orford C R, Gardner D L. Ultrastructural histochemistry of the surface lamina of normal articular cartilage. Histochem J 17(2): 223–233 (1985)
[7]
Higaki H, Murakami T, Nakanishi Y, Miura H, Mawatari T, Iwamoto Y. The lubricating ability of biomembrane models with dipalmitoyl phosphatidylcholine and gamma-globulin. Proc Inst Mech Eng H 212(5): 337–346 (1998)
[8]
Cook S G, Guan Y, Pacifici N J, Brown C N, Czako E, Samak M S, Bonassar L J, Gourdon D. Dynamics of synovial fluid aggregation under shear. Langmuir 35(48): 15887–15896 (2019)
[9]
Schmidt T A, Gastelum N S, Nguyen Q T, Schumacher B L, Sah R L. Boundary lubrication of articular cartilage: Role of synovial fluid constituents. Arthritis Rheum 56(3): 882–891 (2007)
[10]
More S, Kotiya A, Kotia A, Ghosh S K, Spyrou L A, Sarris I E. Rheological properties of synovial fluid due to viscosupplements: A review for osteoarthritis remedy. Comput Methods Programs Biomed 196: 105644 (2020)
[11]
Jung S, Petelska A, Beldowski P, Augé W K, Casey T, Walczak D, Lemke K, Gadomski A. Hyaluronic acid and phospholipid interactions useful for repaired articular cartilage surfaces—A mini review toward tribological surgical adjuvants. Colloid Polym Sci 295(3): 403–412 (2017)
[12]
Ghosh S, Bowen J, Jiang K, Espino D M, Shepherd D E T. Investigation of techniques for the measurement of articular cartilage surface roughness. Micron 44: 179–184 (2013)
[13]
Charnley J. The lubrication of animal joints in relation to surgical reconstruction by arthroplasty. Ann Rheum Dis 19(1): 10–19 (1960)
[14]
Schmidt T A, Sah R L. Effect of synovial fluid on boundary lubrication of articular cartilage. Osteoarthritis Cartilage 15(1): 35–47 (2007)
[15]
Murakami T, Higaki H, Sawae Y, Ohtsuki N, Moriyama S, Nakanishi Y. Adaptive multimode lubrication in natural synovial joints and artificial joints. Proc Inst Mech Eng H 212(1): 23–35 (1998)
[16]
Tanner R I. An alternative mechanism for the lubrication of synovial joints. Phys Med Biol 11(1): 119–127 (1966)
[17]
Dowson D. Paper 12: Modes of lubrication in human joints. Proc Inst Mech Eng Conf Proc 181(10): 45–54 (1966)
[18]
Unsworth A. Tribology of human and artificial joints. Proc Inst Mech Eng H 205(3): 163–172 (1991)
[19]
McCutchen C W. Mechanism of animal joint: Sponge-hydrostatic and Weeping Bearings. Nature 184: 1284–1285 (1959)
[20]
Walker P S, Dowson D, Longfield M D, Wright V. “Boosted lubrication” in synovial joints by fluid entrapment and enrichment. Ann Rheum Dis 27(6): 512–520 (1968)
[21]
Ateshian G A. The role of interstitial fluid pressurization in articular cartilage lubrication. J Biomech 42(9): 1163–1176 (2009)
[22]
Ateshian G A, Wang H Q, Lai W M. The role of interstitial fluid pressurization and surface porosities on the boundary friction of articular cartilage. J Tribol 120(2): 241–248 (1998)
[23]
Mow M C, Ling F F. On weeping lubrication theory. Z Für Angew Math Und Phys ZAMP 20(2): 156–166 (1969)
[24]
Ateshian G A. A theoretical formulation for boundary friction in articular cartilage. J Biomech Eng 119(1): 81–86 (1997)
[25]
Linn F C, Radin E L. Lubrication of animal joints. iii. the effect of certain chemical alterations of the cartilage and lubricant. Arthritis Rheum 11(5): 674–682 (1968)
[26]
Ishikawa Y, Hiratsuka K I, Sasada T. Role of water in the lubrication of hydrogel. Wear 261(5–6): 500–504 (2006)
[27]
Lin W F, Klein J. Hydration lubrication in biomedical applications: From cartilage to hydrogels. Acc Mater Res 3(2): 213–223 (2022)
[28]
Murakami T, Yarimitsu S, Nakashima K, Sawae Y, Sakai N. Influence of synovia constituents on tribological behaviors of articular cartilage. Friction 1(2): 150–162 (2013)
[29]
Bonnevie E D, Galesso D, Secchieri C, Cohen I, Bonassar L J. Elastoviscous transitions of articular cartilage reveal a mechanism of synergy between lubricin and hyaluronic acid. PLoS One 10(11): e0143415 (2015)
[30]
Seror J, Zhu L Y, Goldberg R, Day A J, Klein J. Supramolecular synergy in the boundary lubrication of synovial joints. Nat Commun 6: 6497 (2015)
[31]
Chang D P, Abu-Lail N I, Coles J M, Guilak F, Jay G D, Zauscher S. Friction force microscopy of lubricin and hyaluronic acid between hydrophobic and hydrophilic surfaces. Soft Matter 5(18): 3438–3445 (2009)
[32]
Jahn S, Seror J, Klein J. Lubrication of articular cartilage. Phys Today 71(4): 48–54 (2018)
[33]
Mendibil U, Ruiz-Hernandez R, Retegi-Carrion S, Garcia-Urquia N, Olalde-Graells B, Abarrategi A. Tissue-specific decellularization methods: Rationale and strategies to achieve regenerative compounds. Int J Mol Sci 21(15): 5447 (2020)
[34]
Gilbert T W, Sellaro T L, Badylak S F. Decellularization of tissues and organs. Biomaterials 27(19): 3675–3683 (2006)
[35]
Gleghorn J P, Jones A, Flannery C R, Bonassar L J. Boundary mode frictional properties of engineered cartilaginous tissues. Eur Cells Mater 14: 20–29 (2007)
[36]
Gleghorn J P, Jones A R C, Flannery C R, Bonassar L J. Boundary mode lubrication of articular cartilage by recombinant human lubricin. J Orthop Res 27(6): 771–777 (2009)
[37]
Jones A R C, Gleghorn J P, Hughes C E, Fitz L J, Zollner R, Wainwright S D, Caterson B, Morris E A, Bonassar L J, Flannery C R. Binding and localization of recombinant lubricin to articular cartilage surfaces. J Orthop Res 25(3): 283–292 (2007)
[38]
Pickard J E, Fisher J, Ingham E, Egan J. Investigation into the effects of proteins and lipids on the frictional properties of articular cartilage. Biomaterials 19(19): 1807–1812 (1998)
[39]
Poole A R, Pidoux I, Reiner A, Tang L H, Choi H, Rosenberg L. Localization of proteoglycan monomer and link protein in the matrix of bovine articular cartilage: An immunohistochemical study. J Histochem Cytochem 28(7): 621–635 (1980)
[40]
Seror J, Merkher Y, Kampf N, Collinson L, Day A J, Maroudas A, Klein J. Normal and shear interactions between hyaluronan–aggrecan complexes mimicking possible boundary lubricants in articular cartilage in synovial joints. Biomacromolecules 13(11): 3823–3832 (2012)
[41]
Stachowiak G, Batchelor A. Engineering tribology, 4th edn. Butterworth-Heinemann, 2013.
[42]
Gong J P. Friction and lubrication of hydrogels—Its richness and complexity. Soft Matter 2(7): 544–552 (2006)
[43]
Popov V L. Contact Mechanics and Friction: Physical Principles and Applications. Springer, 2010.
DOI
[44]
Persson B N J, Spencer N D. Sliding friction: Physical principles and applications. Phys Today 52(1): 66–68 (1999)
[45]
Bonnevie E D, Baro V J, Wang L, Burris D L. In situ studies of cartilage microtribology: Roles of speed and contact area. Tribol Lett 41(1): 83–95 (2011)
[46]
Delavoipière J, Tran Y, Verneuil E, Heurtefeu B, Hui C Y, Chateauminois A. Friction of poroelastic contacts with thin hydrogel films. Langmuir 34(33): 9617–9626 (2018)
[47]
Caligaris M, Ateshian G A. Effects of sustained interstitial fluid pressurization under migrating contact area, and boundary lubrication by synovial fluid, on cartilage friction. Osteoarthritis Cartilage 16(10): 1220–1227 (2008)
[48]
Majd S E, Rizqy A I, Kaper H J, Schmidt T A, Kuijer R, Sharma P K. An in vitro study of cartilage–meniscus tribology to understand the changes caused by a meniscus implant. Colloids Surf B Biointerfaces 155: 294–303 (2017)
[49]
Katta J, Pawaskar S S, Jin Z M, Ingham E, Fisher J. Effect of load variation on the friction properties of articular cartilage. Proc Inst Mech Eng Part J J Eng Tribol 221(3): 175–181 (2007)
[50]
Furmann D, Nečas D, Rebenda D, Čípek P, Vrbka M, Křupka I, Hartl M. The effect of synovial fluid composition, speed and load on frictional behaviour of articular cartilage. Materials 13(6): 1334 (2020)
[51]
Jurvelin J S, Müller D J, Wong M, Studer D, Engel A, Hunziker E B. Surface and subsurface morphology of bovine humeral articular cartilage as assessed by atomic force and transmission electron microscopy. J Struct Biol 117(1): 45–54 (1996)
[52]
Murakami T, Sawae Y, Ihara M. Protective mechanism of articular cartilage to severe loading: Roles of lubricants, cartilage surface layer, extracellular matrix and chondrocyte. JSME Int J, Ser C 46(2): 594–603 (2003)
[53]
Saito T. The superficial zone of articular cartilage. Inflamm Regen 42(1): 14 (2022)
[54]
Thielen N G M, van der Kraan P M, van Caam A P M. TGFβ/BMP signaling pathway in cartilage homeostasis. Cells 8(9): 969 (2019)
[55]
Bhosale A M, Richardson J B. Articular cartilage: Structure, injuries and review of management. Br Med Bull 87: 77–95 (2008)
[56]
Fujioka R, Aoyama T, Takakuwa T. The layered structure of the articular surface. Osteoarthritis Cartilage 21(8): 1092–1098 (2013)
[57]
Sawae Y, Murakami T, Matsumoto K, Horimoto M. Study on morphology and lubrication of articular cartilage surface with atomic force microscopy. Jpn J Tribol 45(1): 51–62 (2000)
[58]
Jahn S, Klein J. Hydration lubrication: The macromolecular domain. Macromolecules 48(15): 5059–5075 (2015)
[59]
Gaisinskaya-Kipnis A, Klein J. Normal and frictional interactions between liposome-bearing biomacromolecular bilayers. Biomacromolecules 17(8): 2591–2602 (2016)
[60]
Jahn S, Seror J, Klein J. Lubrication of articular cartilage. Annu Rev Biomed Eng 18: 235–258 (2016)
[61]
Johnson K L, Kendall K, Roberts A D. Surface energy and contact of elastic solids. Proc R Soc A 324(1558): 301–313 (1971)
[62]
He B, Chen W, Wang Q J. Surface texture effect on friction of a microtextured poly(dimethylsiloxane) (PDMS). Tribol Lett 31(3): 187–197 (2008)
[63]
Singh S, Afara I O, Tehrani A H, Oloyede A. Effect of decellularization on the load-bearing characteristics of articular cartilage matrix. Tissue Eng Regen Med 12(5): 294–305 (2015)
[64]
Chan S M T, Neu C P, Duraine G, Komvopoulos K, Reddi A H. Atomic force microscope investigation of the boundary-lubricant layer in articular cartilage. Osteoarthritis Cartilage 18(7): 956–963 (2010)
[65]
Wahlquist J A, DelRio F W, Randolph M A, Aziz A H, Heveran C M, Bryant S J, Neu C P, Ferguson V L. Indentation mapping revealed poroelastic, but not viscoelastic, properties spanning native zonal articular cartilage. Acta Biomater 64: 41–49 (2017)
[66]
Rojas F P, Batista M A, Lindburg C A, Dean D, Grodzinsky A J, Ortiz C, Han L. Molecular adhesion between cartilage extracellular matrix macromolecules. Biomacromolecules 15(3): 772–780 (2014)
[67]
Lawrence A, Xu X, Bible M D, Calve S, Neu C P, Panitch A. Synthesis and characterization of a lubricin mimic (mLub) to reduce friction and adhesion on the articular cartilage surface. Biomaterials 73: 42–50 (2015)
[68]
Soltz M A, Ateshian G A. A conewise linear elasticity mixture model for the analysis of tension-compression nonlinearity in articular cartilage. J Biomech Eng 122(6): 576–586 (2000)
[69]
Shoaib T, Yuh C, Wimmer M A, Schmid T M, Espinosa-Marzal R M. Nanoscale insight into the degradation mechanisms of the cartilage articulating surface preceding OA. Biomater Sci 8(14): 3944–3955 (2020)
[70]
Bahrami M, Le Houérou V, Rühe J. Lubrication of surfaces covered by surface-attached hydrogel layers. Tribol Int 149: 105637 (2020)
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Received: 08 March 2023
Revised: 09 August 2023
Accepted: 30 August 2023
Published: 02 February 2024
Issue date: May 2024

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© The author(s) 2023.

Acknowledgements

Financial support was given by the Grant-in Aid for Scientific Research (A) of Japan Society for the Promotion of Science (21H04535).

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