Histological Aspects of Articular Cartilage

S. Nürnberger; G. Brand; T. Jagersberger; V. Vécsei; S. Marlovits

doi:10.1055/s-2006-942284

Osteosynthesis and Trauma Care, Table of Contents

Osteosynthesis and Trauma Care 2006; 14(3): 158-167
DOI: 10.1055/s-2006-942284

Original Article

Histological Aspects of Articular Cartilage

S. Nürnberger¹ ^, ² , G. Brand³ , T. Jagersberger¹ , V. Vécsei¹ , S. Marlovits¹

¹Medical University of Vienna, Department of Traumatology, Center for Joints and Cartilage, Vienna, Austria
²Cell Imaging and Ultrastructure Research Unit, Vienna, Austria
³Medical University of Vienna, Department of Orthopedics, Vienna, Austria

Abstract

Articular cartilage, because of the particular function in the vertebrate skeletal system, has a highly specialized organization. The biomechanical properties of cartilage rely largely on the nature of the extracellular matrix (ECM) components, their three-dimensional arrangement, and the relative quantity of ECM in the tissue. Cells and ECM are closely functionally related, and their physiology and morphology are altered simultaneously with age, pathological influences, or alterations of mechanical stress. The cellular response to the environment and the variations of the ECM are morphologically discernible. The present article is intended to summarize the morphological features of articular cartilage from the histological point of view.

Key words

hyaline cartilage - ECM - collagen - proteoglycans - joint - morphology - histology

Full Text

References

1 Aigner T, Stove J. Collagens - major component of the physiological cartilage matrix, major target of cartilage degeneration, major tool in cartilage repair. Adv Drug Deliv Rev. 2003; 55 1569-1593
2 Asari A, Miyauchi S, Kuriyama S, Machida A, Kohno K, Uchiyama Y. Localization of hyaluronic acid in human articular cartilage. J Histochem Cytochem. 1994; 42 513-522
3 Aspden R M, Hukins D W. The lamina splendens of articular cartilage is an artefact of phase contrast microscopy. Proc R Soc Lond B Biol Sci. 1979; 206 (1162) 109-113
4 Bayliss M T. Metabolism of Animal and Human Osteoarthritic Cartilage. In: Kuettner KE, Schleyerbach R, Peyron JG, Hascall VC (eds). Articular Cartilage and Osteoarthritis. Raven Press, New York 1991; 487-499
5 Benninghoff A. Form und Bau der Gelenkknorpel in ihren Beziehungen und Funktionen. Zweiter Teil: Der Feinbau des Gelenkknorpels in seinen Beziehungen zur Funktion. Z Zellforsch. 1925; 2 783-862
6 Bobacz K, Erlacher L, Smolen J, Soleiman A, Graninger W B. Chondrocyte number and proteoglycan synthesis in the aging and osteoarthritic human articular cartilage. Ann Rheum Dis. 2004; 63 1618-1622
7 Broom N D, Poole C A. A functional-morphological study of the tidemark region of articular cartilage maintained in a non-viable physiological condition. J Anat. 1982; 135 (Pt 1) 65-82
8 Bruckner P, van der Rest M. Structure and function of cartilage collagens. Microsc Res Tech. 1994; 28 378-384
9 Buckwalter J A, Hunziker E B, Rosenberg L, Coutts R D, Adams M, Eyre D R. Articular Cartilage: Composition and Structure. In: Woo SS-Y, Buckwalter JA (eds). Injury and Repair of the Musculoskeletal Soft Tissues. American Academy of Orthopaedic Surgeons, Park Ridge, Illinois 1988; 405-425
10 Buckwalter J A, Mankin H J. Articular cartilage. Part I: Tissue design and chondrocyte-matrix interactions. J Bone Joint Surg [Am]. 1997; 79 600-611
11 Buckwalter J A, Rosenberg L, Coutts R D, Hunziker E B, Reddi A H, Van Mow C. Articular cartilage: Injury and Repair. In: Woo SS-Y, Buckwalter JA (eds). Injury and Repair of the Musculoskeletal Soft Tissues. American Academy of Orthopaedic Surgeons, Park Ridge, Illinois 1988; 465-482
12 Bullough P G, Jagannath A. The morphology of the calcification front in articular cartilage. Its significance in joint function. J Bone Joint Surg [Br]. 1983; 65 72-78
13 Buschmann M D, Maurer A M, Berger E, Perumbuli P, Hunziker E B. Ruthenium hexaammine trichloride chemography for aggrecan mapping in cartilage is a sensitive indicator of matrix degradation. J Histochem Cytochem. 2000; 48 81-88
14 Campbell C J. The healing of cartilage defects. Clin Orthop Relat Res. 1969; 64 45-63
15 Cheung H S, Cottrell W H, Stephenson K, Nimni M E. In vitro collagen biosynthesis in healing and normal rabbit articular cartilage. J Bone Joint Surg [Am]. 1978; 60 1076-1081
16 Clark J M. Variation of collagen fiber alignment in a joint surface: a scanning electron microscope study of the tibial plateau in dog, rabbit, and man. J Orthop Res. 1991; 9 246-257
17 Clark J M, Huber J D. The structure of the human subchondral plate. J Bone Joint Surg [Br]. 1990; 72 866-873
18 Collins D H. Histology and Physiology of Bone, Cartilage, Synovial Tissue and Joint Fluid. In: The Pathology of Articular and Spinal Diseases. Edward Arnold & Co, London 1949; 7-35
19 Comper W D. Physiochemical Aspects of Cartilage Extracellular Matrix. In: Hall B, Newman S (eds). Cartilage: Molecular aspects. CRC Press, Boca Raton 1991; 59-96
20 Deak F, Wagener R, Kiss I, Paulsson M. The matrilins: A novel family of oligomeric extracellular matrix proteins. Matrix Biol. 1999; 18 55-64
21 DiCesare P E, Morgelin M, Carlson C S, Pasumarti S, Paulsson M. Cartilage oligomeric matrix protein: isolation and characterization from human articular cartilage. J Orthop Res. 1995; 13 422-428
22 Duance V C. Surface of articular cartilage: immunohistological studies. Cell Biochem Funct. 1983; 1 143-144
23 Duncan H, Jundt J, Riddle J M, Pitchford W, Christopherson T. The tibial subchondral plate. A scanning electron microscopic study. J Bone Joint Surg [Am]. 1987; 69 1212-1220
24 Durr J, Lammi P, Goodman S L, Aigner T, von der Mark K. Identification and immunolocalization of laminin in cartilage. Exp Cell Res. 1996; 222 225-233
25 Eerola I, Salminen H, Lammi P, Lammi M, von der Mark K, Vuorio E, Saamanen A M. Type X collagen, a natural component of mouse articular cartilage: Association with growth, aging, and osteoarthritis. Arthritis Rheum. 1998; 41 1287-1295
26 Eggli P S, Hunziker E B, Schenk R K. Quantitation of structural features characterizing weight- and less-weight bearing regions in articular cartilage: A stereological analysis of medial femoral condyles in young adult rabbits. Anat Rec. 1988; 222 217-227
27 Eyre D R, Wu J J, Woods P. Cartilage-Specific Collagens: Structural Studies. In: Kuettner KE, Schleyerbach R, Peyron JG, Hascall VC (eds). Articular Cartilage and Osteoarthritis. Raven Press, New York 1991; 119-132
28 Gannon J M, Walker G, Fischer M, Carpenter R, Thompson R C, Oegema T R. Localization of type X collagen in canine growth plate and adult canine articular cartilage. J Orthop Res. 1991; 9 485-494
29 Ghadially F N. Articular cartilage. In: Ghadially FN (ed). Fine structure of synovial joints. A text and atlas of the ultrastructure of normal and pathological articular tissues. Butterworths, London 1983; 42-79
30 Ghadially F N. The articular surface. In: Ghadially FN (ed). Fine structure of synovial joints. A text and atlas of the ultrastructure of normal and pathological articular tissues. Butterworths, London 1983, 80-102
31 Glant T T, Hadhazy C, Mikecz K, Sipos A. Appearance and persistence of fibronectin in cartilage. Specific interaction of fibronectin with collagen type II. Histochemistry. 1985; 82 149-158
32 Hall M C. Cartilage changes after experimental relief of contact in the knee joint of the mature rat. Clin Orthop Relat Res. 1969; 64 64-76
33 Hardingham T. Immunochemical methods and their use in characterizing cartilage proteoglycans. In: Maroudas A, Kuettner K (eds). Methods in Cartilage Research. Adademic Press, London 1990; 156-163
34 Hardingham T E, Fosang A J, Dudhia J. Aggrecan, the chondroitin sulfate/keratan sulfate proteoglycan from cartilage. In: Kuettner KE, Schleyerbach R, Peyron JG, Hascall VC (eds). Articular Cartilage and Osteoarthritis. Raven Press, New York 1991; 5-20
35 Havelka S, Horn V, Spohrova D, Valouch P. The calcified-noncalcified cartilage interface: The tidemark. Acta Biol Hung. 1984; 35 271-279
36 Hills B A, Monds M K. Deficiency of lubricating surfactant lining the articular surfaces of replaced hips and knees. Braz J Med Biol Res. 1998; 37 143-147
37 Huch K. Knee and ankle: Human joints with different susceptibility to osteoarthritis reveal different cartilage cellularity and matrix synthesis in vitro. Arch Orthop Trauma Surg. 2001; 121 301-306
38 Hunziker E B. Articular Cartilage Structure in Humans and Experimental Animals. In: Kuettner KE, Schleyerbach R, Peyron JG, Hascall VC (eds). Articular Cartilage and Osteoarthritis. Raven Press, New York 1991; 183-200
39 Hunziker E B, Herrmann W. Ultrastructure of Cartilage. In: Bonucci E, Motta PM (eds). Ultrastructure of Skeletal Tissues - Bones and Cartilage in Health and Disease. Kluwer Academics Pub, Norwell 1990; 79-110
40 Hunziker E B, Herrmann W, Schenk R K. Improved cartilage fixation by ruthenium hexammine trichloride (RHT). A prerequisite for morphometry in growth cartilage. J Ultrastruct Res. 1982; 81 1-12
41 Hunziker E B, Herrmann W, Schenk R K. Ruthenium hexammine trichloride (RHT)-mediated interaction between plasmalemmal components and pericellular matrix proteoglycans is responsible for the preservation of chondrocytic plasma membranes in situ during cartilage fixation. J Histochem Cytochem. 1983; 31 717-727
42 Jadin K D, Wong B L, Bae W C, Li K W, Williamson A K, Schumacher B L, Price J H, Sah R L. Depth-varying density and organization of chondrocytes in immature and mature bovine articular cartilage assessed by 3-D imaging and analysis. J Histochem Cytochem. 2005; 53 1109-1119
43 Jeffery A K, Blunn G W, Archer C W, Bentley G. Three-dimensional collagen architecture in bovine articular cartilage. J Bone Joint Surg [Br]. 1991; 73 795-801
44 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. 2001; 199 (Pt 3) 241-250
45 Kummer B. Articular cartilage as a Biomechanical System. In: Gastpar H (ed). Biology of the articular cartilage in health and disease. Schattauer, Stuttgart 1980; 3-15
46 Lammi P E, Lammi M J, Hyttinen M M, Panula H, Kiviranta I, Helminen H J. Site-specific immunostaining for type X collagen in noncalcified articular cartilage of canine stifle knee joint. Bone. 2002; 31 690-696
47 Lane L B, Bullough P G. Age-related changes in the thickness of the calcified zone and the number of tidemarks in adult human articular cartilage. J Bone Joint Surg [Br]. 1980; 62 372-375
48 Lane L B, Villacin A, Bullough P G. The vascularity and remodelling of subchondrial bone and calcified cartilage in adult human femoral and humeral heads. An age- and stress-related phenomenon. J Bone Joint Surg [Br]. 1977; 59 272-278
49 Llauger J, Palmer J, Roson N, Bague S, Camins A, Cremades R. Nonseptic monoarthritis: Imaging features with clinical and histopathologic correlation. Radiographics. 2000; 20 Spec No S263-S278
50 Lyons T J, Stoddart R W, McClure S F, McClure J. The tidemark of the chondro-osseous junction of the normal human knee joint. J Mol Histol. 2005; 36 207-215
51 MacConaill M A. The movements of bones and joints; the mechanical structure of articulating cartilage. J Bone Joint Surg [Br]. 1951; 33 251-257
52 Malinin G I, Malinin T I. Detection of cartilage PG's. In: Malinin GI, Malinin TI (eds). Microscopic and Histochemical Manifestations of Hyaline Cartilage Dynamics. Urban & Fischer, Jena 1999; 197-204
53 Marlovits S, Hombauer M, Tamandl D, Vécsei V, Schlegel W. Quantitative analysis of gene expression in human articular chondrocytes in monolayer culture. Int J Mol Med. 2004; 13 281-287
54 Marlovits S, Hombauer M, Truppe M, Vécsei V, Schlegel W. Changes in the ratio of type-I and type-II collagen expression during monolayer culture of human chondrocytes. J Bone Joint Surg [Br]. 2004; 86 286-295
55 Marlovits S, Vécsei V. Möglichkeiten zur Therapie von Knorpeldefekten - Teil 1: Grundlagen der Knorpelbiologie und der Heilung von Knorpeldefekten. Acta Chir Austriaca. 2000; 320 124-129
56 Meachim G. Age changes in articular cartilage. Clin Orthop Relat Res. 1969; 64 33-44
57 Mendler M, Eich-Bender S G, Vaughan L, Winterhalter K H, Bruckner P. Cartilage contains mixed fibrils of collagen types II, IX, and XI. J Cell Biol. 1989; 108 191-197
58 Newman A P. Articular cartilage repair. Am J Sports Med. 1998; 26 309-324
59 O'Connor K M. Unweighting accelerates tidemark advancement in articular cartilage at the knee joint of rats. J Bone Miner Res. 1997; 12 580-589
60 Oettmeier R, Abendroth K, Oettmeier S. Analyses of the tidemark on human femoral heads. I. Histochemical, ultrastructural and microanalytic characterization of the normal structure of the intercartilaginous junction. Acta Morphol Hung. 1989; 37 155-168
61 Oettmeier R, Abendroth K, Oettmeier S. Analyses of the tidemark on human femoral heads. II. Tidemark changes in osteoarthrosis - a histological and histomorphometric study in non-decalcified preparations. Acta Morphol Hung. 1989; 37 169-180
62 Poole A R, Kojima T, Yasuda T, Mwale F, Kobayashi M, Laverty S. Composition and structure of articular cartilage: a template for tissue repair. Clin Orthop Relat Res. 2001; (391 Suppl) S26-S33
63 Poole C A. The Structure and Function of Articular Cartilage Matrices. In: Woessner JF, Howell DS (eds). Joint Cartilage Degradation. Basic and Clinical Aspects. Marcel Dekker, Inc., New York 1993; 1-33
64 Poole C A. Articular cartilage chondrons: Form, function and failure. J Anat. 1997; 191 (Pt 1) 1-13
65 Poole C A, Ayad S, Gilbert R T. Chondrons from articular cartilage. V. Immunohistochemical evaluation of type VI collagen organisation in isolated chondrons by light, confocal and electron microscopy. J Cell Sci. 1992; 103 (Pt 4) 1101-1110
66 Poole C A, Flint M H, Beaumont B W. Chondrons in cartilage: Ultrastructural analysis of the pericellular microenvironment in adult human articular cartilages. J Orthop Res. 1987; 5 509-522
67 Poole C A, Flint M H, Beaumont B W. Chondrons extracted from canine tibial cartilage: Preliminary report on their isolation and structure. J Orthop Res. 1988; 6 408-419
68 Poole C A, Gilbert R T, Herbage D, Hartmann D J. Immunolocalization of type IX collagen in normal and spontaneously osteoarthritic canine tibial cartilage and isolated chondrons. Osteoarthritis Cartilage. 1997; 5 191-204
69 Poole C A, Matsuoka A, Schofield J R. Chondrons from articular cartilage. III. Morphologic changes in the cellular microenvironment of chondrons isolated from osteoarthritic cartilage. Arthritis Rheum. 1991; 34 22-35
70 Radin E L, Swann D A, Weisser P A. Separation of a hyaluronate-free lubricating fraction from synovial fluid. Nature. 1970; 228 (5269) 377-378
71 Rhee D K, Marcelino J, Al Mayouf S, Schelling D K, Bartels C F, Cui Y, Laxer R, Goldbach-Mansky R, Warman M L. Consequences of disease-causing mutations on lubricin protein synthesis, secretion, and post-translational processing. J Biol Chem. 2005; 280 31325-31332
72 Roughley P J, Lee E R. Cartilage proteoglycans: Structure and potential functions. Microsc Res Tech. 1994; 28 385-397
73 Sandell L J, Aigner T. Articular cartilage and changes in arthritis. An introduction: Cell biology of osteoarthritis. Arthritis Res. 2001; 3 107-113
74 Schwarz I M, Hills B A. Surface-active phospholipid as the lubricating component of lubricin. Braz J Med Biol Res. 1998; 37 21-26
75 Simionescu N, Simionescu M. Galloylglucoses of low molecular weight as mordant in electron microscopy. I. Procedure, and evidence for mordanting effect. J Cell Biol. 1976; 70 608-621
76 Sokoloff (ed) L. The biology of degenerative joint disease. University of Chicago Press, Chicago 1969; 1-162
77 Stockwell R A. The cell density of human articular and costal cartilage. J Anat. 1967; 101 753-763
78 Stockwell R A. Chondrocytes. J Clin Pathol Suppl (R Coll Pathol). 1978; 12 7-13
79 Stockwell (ed) R A. Biology of cartilage cells. Cambridge University Press, Cambridge 1979; 1-329
80 Stoltz J F, Dumas D, Wang X, Payan E, Mainard D, Paulus F, Maurice G, Netter P, Muller S. Influence of mechanical forces on cells and tissues. Biorheology. 2000; 37 3-14
81 Swann D A, Slayter H S, Silver F H. The molecular structure of lubricating glycoprotein-I, the boundary lubricant for articular cartilage. J Biol Chem. 1981; 256 5921-5925
82 Szirmai J A. Structure of Cartilage. In: Engel A, Larsson T (eds). Aging of Connective and Skeletal Tissue. Nordiska Bokhandelns Förlag, Stockholm 1969: 163-184
83 Takada N, Wada I, Sugimura I, Sakuma E, Maruyama H, Matsui N. A possible barrier function of the articular surface. Kaibogaku Zasshi. 1999; 74 631-637
84 Todd A R, Robertson C M, Harwood F L, Sasho T, Williams S K, Pomerleau A C, Amiel D. Characterization of mature vs aged rabbit articular cartilage: analysis of cell density, apoptosis-related gene expression and mechanisms controlling chondrocyte apoptosis. Osteoarthritis Cartilage. 2004; 12 917-923
85 Van Mow C, Fithian D C, Kelly M A. Fundamentals of Articular Cartilage and Meniscus Biomechanics. In: Ewing JW (ed). Articular Cartilage and Knee Joint Function: Basic Science and Arthroscopy. Raven Press, New York 1990; 1-18
86 Van Mow C, Rosenwasser M. Articular Cartilage: Biomechanics. In: Woo SS-Y, Buckwalter JA (eds). Injury and Repair of the Musculoskeletal Soft Tissues. American Academy of Orthpaedic Surgeons, Park Ridge, Illinois 1988; 427-463
87 Van Sickle D C, Kincaid S A. Comparative Arthroscopy. In: Sokoloff L (eds). The Joints and Synovial Fluid. Academic Press, New York 1978; 1-47
88 von der Mark K, Kirsch T, Nerlich A, Kuss A, Weseloh G, Gluckert K, Stoss H. Type X collagen synthesis in human osteoarthritic cartilage. Indication of chondrocyte hypertrophy. Arthritis Rheum. 1992; 35 806-811
89 Wilkins R J, Browning J A, Urban J P. Chondrocyte regulation by mechanical load. Biorheology. 2000; 37 67-74
90 Wilsman N J, Farnum C E, Reed-Aksamit D K. Caveolar system of the articular chondrocyte. J Ultrastruct Res. 1981; 74 1-10

Mag. S. Nürnberger

Medical University of Vienna · Department of Traumatology

Waehringer Guertel 18-20

1090 Vienna

Austria

Phone: +43/1/4 04 00 59 44

Email: sylvia.nuernberger@meduniwien.ac.at