Einfluss der Synovialflüssigkeit auf die Schmiereigenschaften von Gelenkknorpel in vitro

Zusammenfassung

Der hyaline Gelenkknorpel besitzt einzigartige tribologische Eigenschaften, die für die Reduktion von Verschleiß und Abrieb essenziell erscheinen. Er ist in der Lage, trotz durchschnittlich 1 – 4 Mill. Belastungszyklen pro Jahr mit Spitzenbelastungen bis 18 MPa seine Funktion jahrzehntelang aufrechtzuerhalten. Maßgeblich scheinen hierfür verschiedene Schmiermechanismen und deren synergistisches Zusammenspiel verantwortlich zu sein. Insbesondere bei der Grenzflächenschmierung sind die physiologischen Schmiermoleküle („Biolubrikanzien“) der Synovialflüssigkeit von übergeordneter Wichtigkeit. Sie gewährleisten in Abhängigkeit vom vorherrschenden Schmiermechanismus eine nahezu friktionslose/kontaktlose Reibung der Gelenkoberflächen. Zur Testung dieser Eigenschaften und Abhängigkeiten wurden im Laufe der letzten Jahrzehnte verschiedene tribologische „In-vitro“-Prüfsysteme entwickelt. Hierdurch wurden Voraussetzungen für die Grundlagenforschung der Arthrose und Entwicklung von Substanzen zur Viskosupplementation geschaffen. Aufgrund der Komplexität und Vielfalt der Prüfsysteme und Prüfbedingungen ist es schwierig, in diesem Zusammenhang den Überblick zu behalten. Ziel dieses Beitrags ist es, einen kursorischen Überblick über den Einfluss der Synovialflüssigkeit und ihrer Bestandteile auf die Schmierung von Gelenkknorpel unter In-vitro-Prüfbedingungen vorzustellen und verständlich zu machen.

Abstract

Articular cartilage possesses unique tribological properties that are essential to reduce friction and wear. Especially under boundary lubrication conditions, synovial fluid as a whole, and its components (“biolubricants”), are important in assuring near frictionless/contactless lubrication of the joint surfaces. Therefore, several in vitro tribological models have been developed in recent years to investigate possible interdependencies. The aim of this article is to give a cursory overview of the influence of synovial fluid and its components on boundary lubrication of articular cartilage surfaces in vitro.

Schlüsselwörter

Synovialflüssigkeit - hyaliner Knorpel - Gelenkschmierung - Tribologie „in vitro“

Key words

synovial fluid - joint lubrication - articular cartilage - biolubricants

• Literatur

• 1 Pearle AD, Warren RF, Rodeo SA. Basic science of articular cartilage and osteoarthritis. Clin Sports Med 2005; 24: 1-12
• 2 Mow VC, Ratcliffe A, Poole AR. Cartilage and diarthrodial joints as paradigms for hierarchical materials and structures. Biomaterials 1992; 13: 67-97
• 3 Morlock M, Schneider E, Bluhm A. et al. Duration and frequency of every day activities in total hip patients. J Biomech 2001; 34: 873-881
• 4 Seedhom BB, Wallbridge NC. Walking activities and wear of prostheses. Ann Rheum Dis 1985; 44: 838-843
• 5 Wong M, Siegrist M, Goodwin K. Cyclic tensile strain and cyclic hydrostatic pressure differentially regulate expression of hypertrophic markers in primary chondrocytes. Bone 2003; 33: 685-693
• 6 McNary SM, Athanasiou KA, Reddi AH. Engineering lubrication in articular cartilage. Tissue Eng Part B Rev 2012; 18: 88-100
• 7 Walker PS, Dowson D, Longfield MD. et al. “Boosted lubrication” in synovial joints by fluid entrapment and enrichment. Ann Rheum Dis 1968; 27: 512-520
• 8 Charnley J. The lubrication of animal joints in relation to surgical reconstruction by arthroplasty. Ann Rheum Dis 1960; 19: 10-19
• 9 Jay GD, Tantravahi U, Britt DE. et al. Homology of lubricin and superficial zone protein (SZP): products of megakaryocyte stimulating factor (MSF) gene expression by human synovial fibroblasts and articular chondrocytes localized to chromosome 1q25. J Orthop Res 2001; 19: 677-687
• 10 Schmidt TA, Gastelum NS, Nguyen QT. et al. Boundary lubrication of articular cartilage: role of synovial fluid constituents. Arthritis Rheum 2007; 56: 882-891
• 11 Ateshian GA. The role of interstitial fluid pressurization in articular cartilage lubrication. J Biomech 2009; 42: 1163-1176
• 12 Forster H, Fisher J. The influence of loading time and lubricant on the friction of articular cartilage. Proc Inst Mech Eng H 1996; 210: 109-119
• 13 Krishnan R, Kopacz M, Ateshian GA. Experimental verification of the role of interstitial fluid pressurization in cartilage lubrication. J Orthop Res 2004; 22: 565-570
• 14 Katta J, Jin Z, Ingham E. et al. Biotribology of articular cartilage – a review of the recent advances. Med Eng Phys 2008; 30: 1349-1363
• 15 Murakami T, Higaki H, Sawae Y. et al. Adaptive multimode lubrication in natural synovial joints and artificial joints. Proc Inst Mech Eng H 1998; 212: 23-35
• 16 Jay GD, Torres JR, Rhee DK. et al. Association between friction and wear in diarthrodial joints lacking lubricin. Arthritis Rheum 2007; 56: 3662-3669
• 17 Marcelino J, Carpten JD, Suwairi WM. et al. CACP, encoding a secreted proteoglycan, is mutated in camptodactyly-arthropathy-coxa vara-pericarditis syndrome. Nat Genet 1999; 23: 319-322
• 18 Jay GD, Haberstroh K, Cha CJ. Comparison of the boundary-lubricating ability of bovine synovial fluid, lubricin, and Healon. J Biomed Mater Res 1998; 40: 414-418
• 19 Schwarz ML, Schneider-Wald B, Krase A. et al. [Tribological assessment of articular cartilage. A system for the analysis of the friction coefficient of cartilage, regenerates and tissue engineering constructs; initial results]. Orthopade 2012; 41: 827-836
• 20 Northwood E, Fisher J, Kowalski R. Investigation of the friction and surface degradation of innovative chondroplasty materials against articular cartilage. Proc Inst Mech Eng H 2007; 221: 263-279
• 21 Bell CJ, Ingham E, Fisher J. Influence of hyaluronic acid on the time-dependent friction response of articular cartilage under different conditions. Proc Inst Mech Eng H 2006; 220: 23-31
• 22 Swann DA, Silver FH, Slayter HS. et al. The molecular structure and lubricating activity of lubricin isolated from bovine and human synovial fluids. Biochem J 1985; 225: 195-201
• 23 Swann DA, Radin EL, Nazimiec M. et al. Role of hyaluronic acid in joint lubrication. Ann Rheum Dis 1974; 33: 318-326
• 24 Schmidt TA, Sah RL. Effect of synovial fluid on boundary lubrication of articular cartilage. Osteoarthritis Cartilage 2007; 15: 35-47
• 25 Forster H, Fisher J. The influence of continuous sliding and subsequent surface wear on the friction of articular cartilage. Proc Inst Mech Eng H 1999; 213: 329-345
• 26 Knobloch TJ, Madhavan S, Nam J. et al. Regulation of chondrocytic gene expression by biomechanical signals. Crit Rev Eukaryot Gene Expr 2008; 18: 139-150
• 27 Almarza AJ, Athanasiou KA. Design characteristics for the tissue engineering of cartilaginous tissues. Ann Biomed Eng 2004; 32: 2-17
• 28 Quinn TM, Hunziker EB, Hauselmann HJ. Variation of cell and matrix morphologies in articular cartilage among locations in the adult human knee. Osteoarthritis Cartilage 2005; 13: 672-678
• 29 Becerra J, Andrades JA, Guerado E. et al. Articular cartilage: structure and regeneration. Tissue Eng Part B Rev 2010; 16: 617-627
• 30 Darling EM, Athanasiou KA. Rapid phenotypic changes in passaged articular chondrocyte subpopulations. J Orthop Res 2005; 23: 425-432
• 31 Lin Z, Willers C, Xu J. et al. The chondrocyte: biology and clinical application. Tissue Eng 2006; 12: 1971-1984
• 32 Neu CP, Komvopoulos K, Reddi AH. The interface of functional biotribology and regenerative medicine in synovial joints. Tissue Eng Part B Rev 2008; 14: 235-247
• 33 Shi L, Sikavitsas VI, Striolo A. Experimental friction coefficients for bovine cartilage measured with a pin-on-disk tribometer: testing configuration and lubricant effects. Ann Biomed Eng 2011; 39: 132-146
• 34 Gleghorn JP, Bonassar LJ. Lubrication mode analysis of articular cartilage using Stribeck surfaces. J Biomech 2008; 41: 1910-1918
• 35 Fraser JR, Laurent TC, Laurent UB. Hyaluronan: its nature, distribution, functions and turnover. J Intern Med 1997; 242: 27-33
• 36 Hayes WC, Mockros LF. Viscoelastic properties of human articular cartilage. J Appl Physiol 1971; 31: 562-568
• 37 Peng G, McNary SM, Athanasiou KA. et al. Surface zone articular chondrocytes modulate the bulk and surface mechanical properties of the tissue-engineered cartilage. Tissue Eng Part A 2014; 20: 3332-3341
• 38 Radin EL, Swann DA, Weisser PA. Separation of a hyaluronate-free lubricating fraction from synovial fluid. Nature 1970; 228: 377-378
• 39 Swann DA, Slayter HS, Silver FH. The molecular structure of lubricating glycoprotein-I, the boundary lubricant for articular cartilage. J Biol Chem 1981; 256: 5921-5925
• 40 Dowson D, Wright V, Longfield MD. Human joint lubrication. Biomed Eng 1969; 4: 160-165
• 41 Daniel M. Boundary cartilage lubrication: review of current concepts. Wien Med Wochenschr 2014; 164: 88-94
• 42 Stribeck R. Die wesentlichen Eigenschaften der Gleit- und Rollenlager. Berlin: Julius Springer; 1903: 1-47
• 43 Soltz MA, Basalo IM, Ateshian GA. Hydrostatic pressurization and depletion of trapped lubricant pool during creep contact of a rippled indenter against a biphasic articular cartilage layer. J Biomech Eng 2003; 125: 585-593
• 44 Chan SM, Neu CP, Duraine G. et al. Atomic force microscope investigation of the boundary-lubricant layer in articular cartilage. Osteoarthritis Cartilage 2010; 18: 956-963
• 45 Wright V, Dowson D. Lubrication and cartilage. J Anat 1976; 121: 107-118
• 46 Gardner DL, Woodward D. Scanning electron microscopy and replica studies of articular surfaces of guinea-pig synovial joints. Ann Rheum Dis 1969; 28: 379-391
• 47 McCutchen CW. Sponge-hydrostatic and weeping bearings. Nature 1959; 184: 1284-1285
• 48 Ateshian GA, Lai WM, Zhu WB. et al. An asymptotic solution for the contact of two biphasic cartilage layers. J Biomech 1994; 27: 1347-1360
• 49 Jay GD, Waller KA. The biology of lubricin: near frictionless joint motion. Matrix Biol 2014; 39: 17-24
• 50 Hlavacek M. The role of synovial fluid filtration by cartilage in lubrication of synovial joints–II. Squeeze-film lubrication: homogeneous filtration. J Biomech 1993; 26: 1151-1160
• 51 Caligaris M, Ateshian GA. Effects of sustained interstitial fluid pressurization under migrating contact area, and boundary lubrication by synovial fluid, on cartilage friction. Osteoarthritis Cartilage 2008; 16: 1220-1227
• 52 Mazzucco D, Scott R, Spector M. Composition of joint fluid in patients undergoing total knee replacement and revision arthroplasty: correlation with flow properties. Biomaterials 2004; 25: 4433-4445
• 53 Schumacher BL, Block JA, Schmid TM. et al. A novel proteoglycan synthesized and secreted by chondrocytes of the superficial zone of articular cartilage. Arch Biochem Biophys 1994; 311: 144-152
• 54 Schumacher BL, Hughes CE, Kuettner KE. et al. Immunodetection and partial cDNA sequence of the proteoglycan, superficial zone protein, synthesized by cells lining synovial joints. J Orthop Res 1999; 17: 110-120
• 55 Schumacher BL, Schmidt TA, Voegtline MS. et al. Proteoglycan 4 (PRG4) synthesis and immunolocalization in bovine meniscus. J Orthop Res 2005; 23: 562-568
• 56 Katta J, Jin Z, Ingham E. et al. Effect of nominal stress on the long term friction, deformation and wear of native and glycosaminoglycan deficient articular cartilage. Osteoarthritis Cartilage 2009; 17: 662-668
• 57 Tanimoto K, Kamiya T, Tanne Y. et al. Superficial zone protein affects boundary lubrication on the surface of mandibular condylar cartilage. Cell Tissue Res 2011; 344: 333-340
• 58 Ogston AG, Stanier JE. The physiological function of hyaluronic acid in synovial fluid; viscous, elastic and lubricant properties. J Physiol 1953; 119: 244-252
• 59 DuRaine G, Neu CP, Chan SM. et al. Regulation of the friction coefficient of articular cartilage by TGF-beta1 and IL-1beta. J Orthop Res 2009; 27: 249-256
• 60 Jones AR, Flannery CR. Bioregulation of lubricin expression by growth factors and cytokines. Eur Cell Mater 2007; 13: 40-45
• 61 Lipshitz H, Etheredge 3rd R, Glimcher MJ. In vitro wear of articular cartilage. J Bone Joint Surg Am 1975; 57: 527-534
• 62 Pickard JE, Fisher J, Ingham E. et al. Investigation into the effects of proteins and lipids on the frictional properties of articular cartilage. Biomaterials 1998; 19: 1807-1812
• 63 Simon WH. Wear properties of articular cartilage in vitro. J Biomech 1971; 4: 379-389
• 64 Zhang Z, Christopher GF. The nonlinear viscoelasticity of hyaluronic acid and its role in joint lubrication. Soft Matter 2015; 11: 2596-2603
• 65 Ballard BL, Antonacci JM, Temple-Wong MM. et al. Effect of tibial plateau fracture on lubrication function and composition of synovial fluid. J Bone Joint Surg Am 2012; 94: e64
• 66 Caligaris M, Canal CE, Ahmad CS. et al. Investigation of the frictional response of osteoarthritic human tibiofemoral joints and the potential beneficial tribological effect of healthy synovial fluid. Osteoarthritis Cartilage 2009; 17: 1327-1332
• 67 Forsey RW, Fisher J, Thompson J. et al. The effect of hyaluronic acid and phospholipid based lubricants on friction within a human cartilage damage model. Biomaterials 2006; 27: 4581-4590
• 68 Katta J, Jin Z, Ingham E. et al. Chondroitin sulphate: an effective joint lubricant?. Osteoarthritis Cartilage 2009; 17: 1001-1008
• 69 Schiavinato A, Whiteside RA. Effective lubrication of articular cartilage by an amphiphilic hyaluronic acid derivative. Clin Biomech (Bristol, Avon) 2012; 27: 515-519
• 70 Sivan S, Schroeder A, Verberne G. et al. Liposomes act as effective biolubricants for friction reduction in human synovial joints. Langmuir 2010; 26: 1107-1116
• 71 Kwiecinski JJ, Dorosz SG, Ludwig TE. et al. The effect of molecular weight on hyaluronanʼs cartilage boundary lubricating ability – alone and in combination with proteoglycan 4. Osteoarthritis Cartilage 2011; 19: 1356-1362
• 72 Majd SE, Kuijer R, Kowitsch A. et al. 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 2014; 30: 14566-14572
• 73 Yu J, Banquy X, Greene GW. et al. The boundary lubrication of chemically grafted and cross-linked hyaluronic acid in phosphate buffered saline and lipid solutions measured by the surface forces apparatus. Langmuir 2012; 28: 2244-2250
• 74 Balazs EA, Watson D, Duff IF. et al. Hyaluronic acid in synovial fluid. I. Molecular parameters of hyaluronic acid in normal and arthritis human fluids. Arthritis Rheum 1967; 10: 357-376
• 75 Ghosh P, Guidolin D. Potential mechanism of action of intra-articular hyaluronan therapy in osteoarthritis: are the effects molecular weight dependent?. Semin Arthritis Rheum 2002; 32: 10-37
• 76 Knudson CB, Knudson W. Hyaluronan and CD44: modulators of chondrocyte metabolism. Clin Orthop Relat Res 2004; S152-162
• 77 Scott JE. Supramolecular organization of extracellular matrix glycosaminoglycans, in vitro and in the tissues. FASEB J 1992; 6: 2639-2645
• 78 Antonacci JM, Schmidt TA, Serventi LA. et al. Effects of equine joint injury on boundary lubrication of articular cartilage by synovial fluid: role of hyaluronan. Arthritis Rheum 2012; 64: 2917-2926
• 79 Barton KI, Ludwig TE, Achari Y. et al. Characterization of proteoglycan 4 and hyaluronan composition and lubrication function of ovine synovial fluid following knee surgery. J Orthop Res 2013; 31: 1549-1554
• 80 Waddell DD, Marino AA. Chronic knee effusions in patients with advanced osteoarthritis: implications for functional outcome of viscosupplementation. J Knee Surg 2007; 20: 181-184
• 81 Higaki H, Murakami T, Nakanishi Y. et al. The lubricating ability of biomembrane models with dipalmitoyl phosphatidylcholine and gamma-globulin. Proc Inst Mech Eng H 1998; 212: 337-346
• 82 Mabuchi K, Obara T, Ikegami K. et al. Molecular weight independence of the effect of additive hyaluronic acid on the lubricating characteristics in synovial joints with experimental deterioration. Clin Biomech (Bristol, Avon) 1999; 14: 352-356
• 83 Das S, Banquy X, Zappone B. et al. Synergistic interactions between grafted hyaluronic acid and lubricin provide enhanced wear protection and lubrication. Biomacromolecules 2013; 14: 1669-1677
• 84 Lee DW, Banquy X, Das S. et al. Effects of molecular weight of grafted hyaluronic acid on wear initiation. Acta Biomater 2014; 10: 1817-1823
• 85 Tadmor R, Janik J, Klein J. et al. Sliding friction with polymer brushes. Phys Rev Lett 2003; 91: 115503
• 86 Jay GD, Lane BP, Sokoloff L. Characterization of a bovine synovial fluid lubricating factor. III. The interaction with hyaluronic acid. Connect Tissue Res 1992; 28: 245-255
• 87 Kohlhof H, Gravius S, Kohl S. et al. Single molecule microscopy reveals an increased hyaluronan diffusion rate in synovial fluid from knees affected by osteoarthritis. Sci Rep 2016; 6: 21616
• 88 Flannery CR, Hughes CE, Schumacher BL. et al. Articular cartilage superficial zone protein (SZP) is homologous to megakaryocyte stimulating factor precursor and Is a multifunctional proteoglycan with potential growth-promoting, cytoprotective, and lubricating properties in cartilage metabolism. Biochem Biophys Res Commun 1999; 254: 535-541
• 89 Klein TJ, Schumacher BL, Schmidt TA. et al. Tissue engineering of stratified articular cartilage from chondrocyte subpopulations. Osteoarthritis Cartilage 2003; 11: 595-602
• 90 Sarma AV, Powell GL, LaBerge M. Phospholipid composition of articular cartilage boundary lubricant. J Orthop Res 2001; 19: 671-676
• 91 Zea-Aragon Z, Terada N, Ohno N. et al. Replica immunoelectron microscopic study of the upper surface layer in rat mandibular condylar cartilage by a quick-freezing method. Histochem Cell Biol 2004; 121: 255-259
• 92 Rhee DK, Marcelino J, Baker M. et al. The secreted glycoprotein lubricin protects cartilage surfaces and inhibits synovial cell overgrowth. J Clin Invest 2005; 115: 622-631
• 93 Waller KA, Zhang LX, Elsaid KA. et al. Role of lubricin and boundary lubrication in the prevention of chondrocyte apoptosis. Proc Natl Acad Sci U S A 2013; 110: 5852-5857
• 94 Chang DP, Abu-Lail NI, Guilak F. et al. Conformational mechanics, adsorption, and normal force interactions of lubricin and hyaluronic acid on model surfaces. Langmuir 2008; 24: 1183-1193
• 95 Jay GD, Britt DE, Cha CJ. Lubricin is a product of megakaryocyte stimulating factor gene expression by human synovial fibroblasts. J Rheumatol 2000; 27: 594-600
• 96 Zappone B, Greene GW, Oroudjev E. et al. Molecular aspects of boundary lubrication by human lubricin: effect of disulfide bonds and enzymatic digestion. Langmuir 2008; 24: 1495-1508
• 97 Elsaid KA, Fleming BC, Oksendahl HL. et al. Decreased lubricin concentrations and markers of joint inflammation in the synovial fluid of patients with anterior cruciate ligament injury. Arthritis Rheum 2008; 58: 1707-1715
• 98 Elsaid KA, Zhang L, Waller K. et al. The impact of forced joint exercise on lubricin biosynthesis from articular cartilage following ACL transection and intra-articular lubricinʼs effect in exercised joints following ACL transection. Osteoarthritis Cartilage 2012; 20: 940-948
• 99 Flannery CR, Zollner R, Corcoran C. et al. Prevention of cartilage degeneration in a rat model of osteoarthritis by intraarticular treatment with recombinant lubricin. Arthritis Rheum 2009; 60: 840-847
• 100 Jay GD, Fleming BC, Watkins BA. et al. Prevention of cartilage degeneration and restoration of chondroprotection by lubricin tribosupplementation in the rat following anterior cruciate ligament transection. Arthritis Rheum 2010; 62: 2382-2391
• 101 Wei L, Fleming BC, Sun X. et al. Comparison of differential biomarkers of osteoarthritis with and without posttraumatic injury in the Hartley guinea pig model. J Orthop Res 2010; 28: 900-906
• 102 Young AA, McLennan S, Smith MM. et al. Proteoglycan 4 downregulation in a sheep meniscectomy model of early osteoarthritis. Arthritis Res Ther 2006; 8: R41
• 103 Neu CP, Khalafi A, Komvopoulos K. et al. Mechanotransduction of bovine articular cartilage superficial zone protein by transforming growth factor beta signaling. Arthritis Rheum 2007; 56: 3706-3714
• 104 Nugent GE, Aneloski NM, Schmidt TA. et al. Dynamic shear stimulation of bovine cartilage biosynthesis of proteoglycan 4. Arthritis Rheum 2006; 54: 1888-1896
• 105 Coles JM, Zhang L, Blum JJ. et al. Loss of cartilage structure, stiffness, and frictional properties in mice lacking PRG4. Arthritis Rheum 2010; 62: 1666-1674
• 106 Neu CP, Reddi AH, Komvopoulos K. et al. Increased friction coefficient and superficial zone protein expression in patients with advanced osteoarthritis. Arthritis Rheum 2010; 62: 2680-2687
• 107 Hills BA, Butler BD. Surfactants identified in synovial fluid and their ability to act as boundary lubricants. Ann Rheum Dis 1984; 43: 641-648
• 108 Hills BA, Crawford RW. Normal and prosthetic synovial joints are lubricated by surface-active phospholipid: a hypothesis. J Arthroplasty 2003; 18: 499-505
• 109 Hills BA, Monds MK. Deficiency of lubricating surfactant lining the articular surfaces of replaced hips and knees. Br J Rheumatol 1998; 37: 143-147
• 110 Purbach B, Hills BA, Wroblewski BM. Surface-active phospholipid in total hip arthroplasty. Clin Orthop Relat Res 2002; 115-118
• 111 Bell CJ, Carrick LM, Katta J. et al. Self-assembling peptides as injectable lubricants for osteoarthritis. J Biomed Mater Res A 2006; 78: 236-246
• 112 Rabinowitz JL, Gregg JR, Nixon JE. Lipid composition of the tissues of human knee joints. II. Synovial fluid in trauma. Clin Orthop Relat Res 1984; 292-298
• 113 Chen Y, Crawford RW, Oloyede A. Unsaturated phosphatidylcholines lining on the surface of cartilage and its possible physiological roles. J Orthop Surg Res 2007; 2: 14
• 114 Graindorge S, Ferrandez W, Ingham E. et al. The role of the surface amorphous layer of articular cartilage in joint lubrication. Proc Inst Mech Eng H 2006; 220: 597-607
• 115 Kawano T, Miura H, Mawatari T. et al. Mechanical effects of the intraarticular administration of high molecular weight hyaluronic acid plus phospholipid on synovial joint lubrication and prevention of articular cartilage degeneration in experimental osteoarthritis. Arthritis Rheum 2003; 48: 1923-1929
• 116 Schwarz IM, Hills BA. Surface-active phospholipid as the lubricating component of lubricin. Br J Rheumatol 1998; 37: 21-26
• 117 Ozturk HE, Stoffel KK, Jones CF. et al. The effect of surface-active phospholipids on the lubrication of osteoarthritic sheep knee joints: friction. Tribol Lett 2004; 16: 283-289
• 118 Oloyede A, Gudimetla P, Crawford R. et al. Consolidation responses of delipidized articular cartilage. Clin Biomech (Bristol, Avon) 2004; 19: 534-542
• 119 Vecchio P, Thomas R, Hills BA. Surfactant treatment for osteoarthritis. Rheumatology (Oxford) 1999; 38: 1020-1021
• 120 Basalo IM, Chen FH, Hung CT. et al. Frictional response of bovine articular cartilage under creep loading following proteoglycan digestion with chondroitinase ABC. J Biomech Eng 2006; 128: 131-134
• 121 Thompson jr. RC, Oegema jr. TR. Metabolic activity of articular cartilage in osteoarthritis. An in vitro study. J Bone Joint Surg Am 1979; 61: 407-416
• 122 Basalo IM, Raj D, Krishnan R. et al. Effects of enzymatic degradation on the frictional response of articular cartilage in stress relaxation. J Biomech 2005; 38: 1343-1349
• 123 Kumar P, Oka M, Toguchida J. et al. Role of uppermost superficial surface layer of articular cartilage in the lubrication mechanism of joints. J Anat 2001; 199: 241-250
• 124 Basalo IM, Chahine NO, Kaplun M. et al. Chondroitin sulfate reduces the friction coefficient of articular cartilage. J Biomech 2007; 40: 1847-1854
• 125 Bian L, Kaplun M, Williams DY. et al. Influence of chondroitin sulfate on the biochemical, mechanical and frictional properties of cartilage explants in long-term culture. J Biomech 2009; 42: 286-290
• 126 Dettmer N. [The therapeutic effect of glycosaminoglycan polysulfate (Arteparon) in arthroses depending on the mode of administration (intraarticular or intramuscular)]. Z Rheumatol 1979; 38: 163-181
• 127 Hess H, Rothhaar J, Thiel W. [Clinical studies of intra-articular injections of Arteparon. Retrospective study following the treatment of 754 patients]. Fortschr Med 1982; 100: 1624-1627
• 128 Olijhoek G, Drukker J, van der Linden TJ. et al. Drug effects on arthrosis. Comparison in rabbits of 3 modes of action. Acta Orthop Scand 1988; 59: 186-190
• 129 Skrivankova B, Podrazky V, Trnavsky K. et al. Effect of selected antirheumatic drugs on the metabolism of cartilage and synovial tissue in experimental arthropathy. Methods Find Exp Clin Pharmacol 1991; 13: 523-528
• 130 Bassleer CT, Combal JP, Bougaret S. et al. Effects of chondroitin sulfate and interleukin-1 beta on human articular chondrocytes cultivated in clusters. Osteoarthritis Cartilage 1998; 6: 196-204