Cartilage and diarthrodial joints as paradigms for hierarchical materials and structures.

The anatomic forms of diarthrodial joints are important structural features which provide and limit the motions required for the joint. Typically, the length scale of topographic variation of anatomic forms ranges from 0.5 to 15 cm. Articular cartilage is the thin layer of hydrated soft tissue (0.5-5.0 mm thick) covering the articulating bony ends in diarthrodial joints. This tissue has a set of unique mechanical and physicochemical properties which are responsible for its load-carrying capabilities and near-frictionless qualities. The mechanical properties of articular cartilage are determined at the tissue-scale level and these properties depend on the composition of the tissue, mainly collagen and proteoglycan, and their molecular and ultrastructural organization (ultra-scale: 10(-8)-10(-6) m). Because proteoglycans possess a high density of fixed negative charges, articular cartilage exhibits a significant Donnan osmotic pressure effect. This physicochemically derived osmotic pressure is an important component of the total swelling pressure; the other component of the total swelling pressure stems from the charge-to-charge repulsive force exerted by the closely spaced (1-1.5 nm) negative charge groups along the proteoglycan molecules. Thus these interactions take place at a nano-scale level: 10(-10)-10(-9) m. Finally, cartilage biochemistry and organization are maintained by the chondrocytes which exist at a micro-scale level (10(-7)-10(-6) m). Significant mechanoelectrochemical transduction occurs within the extracellular matrix at the micro-scale level which affects and modulates cellular anabolic and catabolic activities. At present, the exact details of these transduction mechanisms are unknown. In this review, we present a summary of the hierarchical features for articular cartilage and diarthrodial joints and tables of known material properties for cartilage. Also we summarize how the multi-scale interactions in articular cartilage provide for its unique material properties and tribological characteristics.

[1]  M. Biot General Theory of Three‐Dimensional Consolidation , 1941 .

[2]  Duncan Dowson,et al.  The Frictional Behavior of Human Synovial Joints—Part I: Natural Joints , 1975 .

[3]  A F Mak,et al.  Nonlinear viscoelastic properties of articular cartilage in shear , 1989, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[4]  J. Heath,et al.  Transforming growth factor beta modulates the expression of collagenase and metalloproteinase inhibitor. , 1987, The EMBO journal.

[5]  C. A. Poole,et al.  Morphological and functional interrelationships of articular cartilage matrices. , 1984, Journal of anatomy.

[6]  J. Urban,et al.  The effects of hydrostatic pressure on matrix synthesis in articular cartilage , 1991, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[7]  D. Gardner The influence of microscopic technology on knowledge of cartilage surface structure. , 1972, Annals of the rheumatic diseases.

[8]  L. Pottenger,et al.  Influence of cartilage particle size and proteoglycan aggregation on immobilization of proteoglycans. , 1982, The Journal of biological chemistry.

[9]  A. Ratcliffe,et al.  Articular cartilage cultured with interleukin 1. Increased release of link protein, hyaluronate-binding region and other proteoglycan fragments. , 1986, The Biochemical journal.

[10]  A. Maroudas,et al.  Balance between swelling pressure and collagen tension in normal and degenerate cartilage , 1976, Nature.

[11]  V. Mow,et al.  The ultrastructure and biomechanical significance of the tidemark of articular cartilage. , 1975, Clinical orthopaedics and related research.

[12]  J. Clark,et al.  The organization of collagen in cryofractured rabbit articular cartilage: A scanning electron microscopic study , 1985, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[13]  P. Torzilli Influence of cartilage conformation on its equilibrium water partition , 1985, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[14]  M. Glimcher,et al.  In vitro studies of the wear of articular cartilage II. Characteristics of the wear of articular cartilage when worn against stainless steel plates having characterized surfaces , 1979 .

[15]  D. Mcgillivray,et al.  Living articular cartilage is not smooth. The structure of mammalian and avian joint surfaces demonstrated in vivo by immersion incident light microscopy. , 1971, Annals of the rheumatic diseases.

[16]  V C Mow,et al.  Effects of proteoglycan extraction on the tensile behavior of articular cartilage , 1990, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[17]  J CHARNLEY,et al.  The Lubrication of Animal Joints in Relation to Surgical Reconstruction by Arthroplasty * , 1960, Annals of the rheumatic diseases.

[18]  W C Hayes,et al.  Flow-independent viscoelastic properties of articular cartilage matrix. , 1978, Journal of biomechanics.

[19]  T. Hardingham,et al.  Proteoglycans: their structure, interactions and molecular organization in cartilage. , 1981, Biochemical Society transactions.

[20]  P. Prehm Synthesis of hyaluronate in differentiated teratocarcinoma cells. Mechanism of chain growth. , 1983, The Biochemical journal.

[21]  V. Mow,et al.  Biphasic creep and stress relaxation of articular cartilage in compression? Theory and experiments. , 1980, Journal of biomechanical engineering.

[22]  A. Katchalsky,et al.  Nonequilibrium Thermodynamics in Biophysics , 1965 .

[23]  E. Wachtel,et al.  Extrafibrillar proteoglycans osmotically regulate the molecular packing of collagen in cartilage. , 1986, Biochimica et biophysica acta.

[24]  H. Muir,et al.  Proteoglycans as organizers of the intercellular matrix. , 1983, Biochemical Society transactions.

[25]  J M Mansour,et al.  The permeability of articular cartilage under compressive strain and at high pressures. , 1976, The Journal of bone and joint surgery. American volume.

[26]  Van C. Mow,et al.  Recent Developments in Synovial Joint Biomechanics , 1980 .

[27]  F. C. Linn,et al.  MOVEMENT AND COMPOSITION OF INTERSTITIAL FLUID OF CARTILAGE. , 1965, Arthritis and rheumatism.

[28]  D. Eyre,et al.  Collagen type IX: Evidence for covalent linkages to type II collagen in cartilage , 1987, FEBS letters.

[29]  P. Bullough,et al.  The morphology of the calcification front in articular cartilage. Its significance in joint function. , 1983, The Journal of bone and joint surgery. British volume.

[30]  J. Kimura,et al.  [18] Biosynthesis of cartilage proteoglycan and link protein , 1987 .

[31]  V C Mow,et al.  Variations in the intrinsic mechanical properties of human articular cartilage with age, degeneration, and water content. , 1982, The Journal of bone and joint surgery. American volume.

[32]  R Huiskes,et al.  Analytical stereophotogrammetric determination of three-dimensional knee-joint geometry. , 1985, Journal of biomechanics.

[33]  M. Tombs,et al.  The osmotic pressure of biological macromolecules , 1974 .

[34]  G E Kempson,et al.  Mechanical properties of articular cartilage. , 1972, The Journal of physiology.

[35]  T. Hardingham,et al.  Assembly of newly synthesized proteoglycan and link protein into aggregates in cultures of chondrosarcoma chondrocytes. , 1980, The Journal of biological chemistry.

[36]  H J Mankin,et al.  Water content and binding in normal and osteoarthritic human cartilage. , 1975, The Journal of bone and joint surgery. American volume.

[37]  M. Sato [Mechanical properties of living tissues]. , 1986, Iyo denshi to seitai kogaku. Japanese journal of medical electronics and biological engineering.

[38]  O. Reynolds IV. On the theory of lubrication and its application to Mr. Beauchamp tower’s experiments, including an experimental determination of the viscosity of olive oil , 1886, Philosophical Transactions of the Royal Society of London.

[39]  V. Mow,et al.  The influence of link protein stabilization on the viscometric properties of proteoglycan aggregate solutions. , 1989, Biochimica et biophysica acta.

[40]  A. Grodzinsky,et al.  Biosynthetic response of cartilage explants to dynamic compression , 1989, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[41]  W. Comper,et al.  Water transport in extracellular matrices. , 1990, Connective tissue research.

[42]  W M Lai,et al.  Drag-induced compression of articular cartilage during a permeation experiment. , 1980, Biorheology.

[43]  M. E. van der Rest,et al.  Type IX collagen proteoglycan from cartilage is covalently cross-linked to type II collagen. , 1988, The Journal of biological chemistry.

[44]  D Dowson,et al.  "Boosted lubrication" in synovial joints by fluid entrapment and enrichment. , 1968, Annals of the rheumatic diseases.

[45]  J. Goodfellow,et al.  The significance of the fine structure of articular cartilage. , 1968, The Journal of bone and joint surgery. British volume.

[46]  J. Buckwalter,et al.  Interspecies comparisons of in situ intrinsic mechanical properties of distal femoral cartilage , 1991, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[47]  A. Ratcliffe,et al.  Immunochemical studies on the synthesis and secretion of link protein and aggregating proteoglycan by chondrocytes. , 1987, Collagen and related research.

[48]  V C Mow,et al.  Quantitation of articular surface topography and cartilage thickness in knee joints using stereophotogrammetry. , 1991, Journal of biomechanics.

[49]  F. Silver,et al.  The molecular structure and lubricating activity of lubricin isolated from bovine and human synovial fluids. , 1985, The Biochemical journal.

[50]  A. Ratcliffe,et al.  Cartilage proteoglycan binding region and link protein. Radioimmunoassays and the detection of masked determinants in aggregates. , 1983, The Biochemical journal.

[51]  S. L. Lee,et al.  A Proposed Model of Boundary Lubrication by Synovial Fluid: Structuring of Boundary Water , 1979 .

[52]  Wright,et al.  Introduction to the Biomechanics of Joints and Joint Replacement , 1991 .

[53]  J. Buckwalter,et al.  Age‐related changes in articular cartilage proteoglycans: Electron microscopic studies , 1985, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[54]  V C Mow,et al.  The intrinsic tensile behavior of the matrix of bovine articular cartilage and its variation with age. , 1980, The Journal of bone and joint surgery. American volume.

[55]  P. Roughley,et al.  The properties of proteoglycan prepared from human articular cartilage by using associative caesium chloride gradients of high and low starting densities. , 1985, The Biochemical journal.

[56]  V C Mow,et al.  Tensile properties of human knee joint cartilage: I. Influence of ionic conditions, weight bearing, and fibrillation on the tensile modulus , 1986, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[57]  R. Schleyerbach,et al.  Articular Cartilage Biochemistry , 1986 .

[58]  M A Freeman,et al.  The composition of normal and osteoarthritic articular cartilage from human knee joints. With special reference to unicompartmental replacement and osteotomy of the knee. , 1984, The Journal of bone and joint surgery. American volume.

[59]  G. Selvik Roentgen stereophotogrammetry. A method for the study of the kinematics of the skeletal system. , 1989, Acta orthopaedica Scandinavica. Supplementum.

[60]  Van C. Mow,et al.  Rheological Equations for Synovial Fluids , 1978 .

[61]  P. Roughley,et al.  Degradation of proteoglycan aggregate by a cartilage metalloproteinase. Evidence for the involvement of stromelysin in the generation of link protein heterogeneity in situ. , 1989, The Biochemical journal.

[62]  H. Dorfman,et al.  Biochemical and metabolic abnormalities in articular cartilage from osteo-arthritic human hips. II. Correlation of morphology with biochemical and metabolic data. , 1971, The Journal of bone and joint surgery. American volume.

[63]  P. Stephens,et al.  Stromelysin is an activator of procollagenase. A study with natural and recombinant enzymes. , 1987, The Biochemical journal.

[64]  A R Poole,et al.  An immunoelectron microscope study of the organization of proteoglycan monomer, link protein, and collagen in the matrix of articular cartilage , 1982, The Journal of cell biology.

[65]  H. Muir,et al.  Proteoglycan aggregate formation by articular chondrocytes. Decrease in link-protein synthesis during culture. , 1983, The Biochemical journal.

[66]  A. Ratcliffe,et al.  Proteoglycan biosynthesis in chondrocytes: protein A-gold localization of proteoglycan protein core and chondroitin sulfate within Golgi subcompartments , 1985, The Journal of cell biology.

[67]  R. M. Bowen,et al.  Incompressible porous media models by use of the theory of mixtures , 1980 .

[68]  P. D. Rushfeldt,et al.  Improved techniques for measuring in vitro the geometry and pressure distribution in the human acetabulum--I. Ultrasonic measurement of acetabular surfaces, sphericity and cartilage thickness. , 1981, Journal of biomechanics.

[69]  G. Vaes,et al.  Further studies on the activation of procollagenase, the latent precursor of bone collagenase. Effects of lysosomal cathepsin B, plasmin and kallikrein, and spontaneous activation. , 1977, The Biochemical journal.

[70]  G. R. Dodge,et al.  Immunohistochemical detection and immunochemical analysis of type II collagen degradation in human normal, rheumatoid, and osteoarthritic articular cartilages and in explants of bovine articular cartilage cultured with interleukin 1. , 1989, The Journal of clinical investigation.

[71]  T. Koob,et al.  Quantitation of hydroxypyridinium crosslinks in collagen by high-performance liquid chromatography. , 1984, Analytical biochemistry.

[72]  D. Eyre,et al.  Sites of stromelysin cleavage in collagen types II, IX, X, and XI of cartilage. , 1991, The Journal of biological chemistry.

[73]  J. Sandy,et al.  Catabolism of aggrecan in cartilage explants. Identification of a major cleavage site within the interglobular domain. , 1991, The Journal of biological chemistry.

[74]  V. Mow,et al.  The density and strength of proteoglycan-proteoglycan interaction sites in concentrated solutions. , 1991, Journal of biomechanics.

[75]  F. P. Bowden,et al.  The Friction and Lubrication of Solids , 1964 .

[76]  W M Lai,et al.  Fluid transport and mechanical properties of articular cartilage: a review. , 1984, Journal of biomechanics.

[77]  W M Lai,et al.  Boundary conditions at the cartilage-synovial fluid interface for joint lubrication and theoretical verifications. , 1989, Journal of biomechanical engineering.

[78]  Y. Yamada,et al.  Rat and human cartilage proteoglycan (aggrecan) gene structure. , 1990, Biochemical Society transactions.

[79]  M. Holmes,et al.  Squeeze Film Lubrication for Articular Cartilage with Synovial Fluid , 1990 .

[80]  F. C. Linn,et al.  Lubrication of animal joints. II. The mechanism. , 1968, Journal of biomechanics.

[81]  R. Aspden,et al.  Collagen organization in articular cartilage, determined by X-ray diffraction, and its relationship to tissue function , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[82]  A. Poole Proteoglycans in health and disease: structures and functions. , 1986, The Biochemical journal.

[83]  J. C. Copray,et al.  Effects of compressive forces on proliferation and matrix synthesis in mandibular condylar cartilage of the rat in vitro. , 1985, Archives of oral biology.

[84]  A. Maroudas,et al.  Chemical composition and swelling of normal and osteoarthrotic femoral head cartilage. II. Swelling. , 1977, Annals of the rheumatic diseases.

[85]  F. C. Linn,et al.  Lubrication of animal joints. I. The arthrotripsometer. , 1967, The Journal of bone and joint surgery. American volume.

[86]  V. Mow,et al.  Triphasic Theory for Swelling Properties of Hydrated Charged Soft Biological Tissues , 1990 .

[87]  D. Dowson,et al.  Micro-elastohydrodynamic lubrication of synovial joints. , 1986, Engineering in medicine.

[88]  V. Mow,et al.  Curvature characteristics and congruence of the thumb carpometacarpal joint: differences between female and male joints. , 1992, Journal of biomechanics.

[89]  V C Mow,et al.  The nonlinear characteristics of soft gels and hydrated connective tissues in ultrafiltration. , 1990, Journal of biomechanics.

[90]  B. Caterson,et al.  Changes in the metabolism of the proteoglycans from sheep articular cartilage in response to mechanical stress , 1978 .

[91]  R. Palmiter,et al.  Rabbit procollagenase synthesized and secreted by a high-yield mammalian expression vector requires stromelysin (matrix metalloproteinase-3) for maximal activation. , 1990, The Journal of biological chemistry.

[92]  A. Ratcliffe,et al.  Modulation of native chondroitin sulphate structure in tissue development and in disease. , 1990, Journal of cell science.

[93]  W M Lai,et al.  A continuum theory and an experiment for the ion-induced swelling behavior of articular cartilage. , 1984, Journal of biomechanical engineering.

[94]  F. G. Donnan,et al.  The Theory of Membrane Equilibria. , 1924 .

[95]  S. Pasternack,et al.  Solvent-dependent changes in proteoglycan subunit conformation in aqueous guanidine hydrochloride solutions. , 1974, The Journal of biological chemistry.

[96]  H. Muir,et al.  Biochemical changes in the cartilage of the knee in experimental and natural osteoarthritis in the dog. , 1976, The Journal of bone and joint surgery. British volume.

[97]  D. Yates ROUND-TABLE DISCUSSIONS , 1969 .

[98]  Savio Lau-Yuen Woo,et al.  Biomechanics of diarthrodial joints , 1990 .

[99]  C. McCutchen,et al.  Mechanism of Animal Joints: Experimental Evidence for Weeping Lubrication in Mammalian Joints , 1959, Nature.

[100]  A. J. Bollet,et al.  Biochemical Findings in Normal and Osteoarthritic Articular Cartilage. II. Chondroitin Sulfate Concentration and Chain Length, Water, and Ash Content. , 1966, The Journal of clinical investigation.

[101]  K. Doege,et al.  Complete coding sequence and deduced primary structure of the human cartilage large aggregating proteoglycan, aggrecan. Human-specific repeats, and additional alternatively spliced forms. , 1991, The Journal of biological chemistry.

[102]  Y C Fung,et al.  Residual strains in porcine and canine trachea. , 1991, Journal of biomechanics.

[103]  C. McCutchen,et al.  Mechanism of Animal Joints: Sponge-hydrostatic and Weeping Bearings , 1959, Nature.

[104]  G E Kempson,et al.  The effects of proteolytic enzymes on the mechanical properties of adult human articular cartilage. , 1976, Biochimica et biophysica acta.