J. Anat. (1990), 171, pp. 1-15 1 Printed in Great Britain

Research Review Fibrocartilage

M. BENJAMIN AND E. J. EVANS Department of Anatomy, University of Wales College of Cardiff, PO Box 900, Cardif CF1 3 YF, Wales

Fibrocartilage has long been a neglected tissue that is too often viewed as a poor relation of hyaline . It failed to achieve the status of a tissue with the early histologists, but it is beginning to come of age, for modem techniques are revealing some exciting secrets about fibrocartilage in knee menisci and intervertebral discs in particular. Yet there has never been any general review on fibrocartilage, and workers concerned with the tissue in one organ rarely consider it in another. Consequently, we lack any global picture that would encourage the spread of interest in the tissue and the effective exchange of ideas. Our review deals largely with the white fibrocartilage of standard texts and for reasons of space excludes yellow . We have concentrated on fibrocartilage as a tissue rather than fibrocartilages as organs.

HISTORICAL CONSIDERATIONS The most important work on cartilage in the older literature is that of Schaffer (1930). His monograph is a thorough, comparative account of cartilage and related tissues throughout the animal kingdom. The reader interested in fibrocartilage must also study Schaffer's account of chondroid tissue, for some tissues that would now be regarded as fibrocartilage were viewed by Schaffer as hyaline-cell chondroid tissue. He had a narrow vision of 'true' cartilage and called tissues where the cells were not shrunken in lacunae, 'chondroid'.

GENERAL ASPECTS OF STRUCTURE Fibrocartilage is a transitional tissue that lacks a and has structural and functional properties intermediate between those of dense fibrous connective tissue and . Fibrocartilage merges with the hyaline cartilage of the radius in the triangular fibrocartilage complex of the wrist (Benjamin, Evans & Pemberton, 1990) and with dense fibrous connective tissue in and (Benjamin, Evans & Copp, 1986; Woo et al. 1988). In view of the gradual transition between fibrocartilage and dense fibrous connective tissue, it is worth noting that Masson's trichrome stains collagen under tension red and collagen under compression green (Flint, Lyons, Meaney & Williams, 1975). As fibrocartilage resists compression, it stains predominantly green. 2 M. BENJAMIN AND E. J. EVANS

Cells The cells of fibrocartilage may be irregularly arranged or lie in longitudinal rows. Except for the occasional cell that is more typical of loose connective tissues (e.g. mast cells), the majority ofcells look like or fibroblasts, but it is often difficult to know which to call them. Furthermore, Somer & Somer (1983) argue that parts of the knee joint menisci where chondroitin sulphate is absent from around the cells should be regarded as chondroid tissue. Edwards & Chrisman (1979) refer to both chondrocytes and fibroblasts in the fibrocartilage that appears in healing articular cartilage. Cooper & Misol (1970) distinguish typical chondrocytes from typical fibroblasts in attachments, but comment that "the cells gradually change structural characteristics" from one cell type to the other. Ghadially (1983) considers that most meniscal cells that look like fibroblasts are really flattened chondrocytes. At the electron microscope level, these cells have numerous short processes and are surrounded by a territorial matrix. The flattened meniscal cells are thus similar to those in the superficial zone of articular cartilage. As a general rule, the more chondrocytic cells are found in the centre of fibrocartilage, and the more fibroblastic at its periphery. Although Badi (1972) recognises only chondrocytes in the fibrocartilage at the attachment of the rat patellar ligament, he distinguishes two subclasses of tissue according to the size of the cells. Small-celled fibrocartilage can calcify without cell hypertrophy and remains throughout life. It is then the Type II chondroid of Beresford (1981). Large-celled fibrocartilage develops from the small and disappears at the end of skeletal growth. The ultrastructural features of fibrocartilaginous chondrocytes described by Cooper & Misol (1970), Merrilees & Flint (1980), Buckwalter (1982), Ghadially (1983) and by Okuda, Gorski & Amadio (1987) suggest that the fine structure of the cells is similar to that of the cells in hyaline cartilage. Eyre et al. (1988) distinguish between notochordal cells, fibroblasts and chondrocytes in . His descriptions of the chondrocytes are in broad agreement with those of Ghadially (1983) in menisci, but he makes no mention of chondrocytic features of the fibroblasts in the outer part of the annulus fibrosus. Fibres The collagen fibres can be irregularly arranged or form striking patterns. Circumferential hoops are conspicuous in knee joint menisci (Arnoczky et al. 1988) and collagen fibres running in the long axis ofa ligament or are typical ofmany attachment zones (Woo et al. 1988). However, in the fibrocartilaginous regions of tendons that pass around bony pulleys, the collagen fibres have a basket-weave appearance and some bundles run at right angles to the long axis of the tendon (Merrilees & Flint, 1980). The fibres in the inner, fibrocartilaginous part of the annulus fibrosus of intervertebral discs do not form such obvious lamellae as those in the outer, more fibrous parts (Buckwalter, 1982; Eyre et al. 1988). Seven different types ofcollagen have now been documented in the annulus fibrosus of the intervertebral disc (Eyre, 1988) and at least four in the menisci of the knee joint (Arnoczky et al. 1988). is the most abundant and accounts for about 90 % of the total meniscal collagen and 80% of the collagen of the annulus fibrosus. There is a reciprocal gradient in the distribution of Types I and II collagen in the intervertebral disc. Type II is absent from the most peripheral part of the disc, but accounts for 80% of collagen in the nucleus pulposus, where the proportion of Type Fibrocartilage 3 I collagen has fallen to low levels. Type II collagen accounts for 1-2 % of total meniscal collagens. Penile fibrocartilage of the rat is also predominantly Type I collagen, though Type II is present around the cells (Murakami, 1987). The abundant presence of Type I collagen (tensile in function) and the relative paucity of Type II collagen (characteristic of tissues subject to pressure) is often taken to be a key biochemical feature that distinguishes fibro- from hyaline cartilage (Arnoczky et al. 1988). Other collagens are present in fibrocartilage in small quantities. Types V and VI have been identified in both menisci and intervertebral discs, but Types IX and XI have only been found in discs (Eyre, 1988; Arnoczky et al. 1988). In addition, Type M collagen occurs in fibrocartilage that forms on the surface of osteophytes in degenerating femoral articular cartilage (Nemeth-Csoka & MeszaLros, 1983). The minor collagens may be important in anchoring chondrocytes to their matrix (Melrose & Ghosh, 1988) and in allowing collagen fibres to interact with one another and with proteoglycans (Eyre, 1988). Small numbers of elastic fibres and/or elastic system fibres are present in the fibrocartilage of intervertebral discs (Buckwalter, Cooper & Maynard, 1976; Cotta- Pereira, Del-Caro & Montes, 1984), menisci (Peters & Smillie, 1972; Ghadially, 1983; Arnoczky et al. 1988) and tendon or ligament attachment zones (Cooper & Misol, 1970). Amorphous matrix The major constituents of the amorphous matrix are proteoglycans. Our knowledge of them is based mainly on studies of knee joint menisci (Arnoczky et al. 1988) and intervertebral discs (Bogduk & Twomey, 1987; Eyre et al. 1988). It is only here that sufficient quantities ofthe tissue can be obtained for analysis. There is less proteoglycan in fibro- than in hyaline cartilage, but more than in pure fibrous tissue (Gillard, Reilly, Bell-Booth & Flint, 1979; Koob & Vogel, 1987). The mean amount of glycosamino- glycans in knee joint menisci is 10-12 % of that in hyaline articular cartilage (Arnoczky et al. 1988). The proteoglycans of fibrocartilage differ biochemically from those of hyaline cartilage (McNicol & Roughley, 1980; Roughley, McNicol, Santer & Buckwalter, 1981; Arnoczky et al. 1988; Eyre et al. 1988). They have been identified histochemically in fibrocartilaginous finger menisci where they are prominent in the territorial matrix of the chondrocytes (Fisher, Elliott, Cooke & Forrest, 1985). Little is known of the other non-collagenous proteins (NCP) in fibrocartilage. However, it is likely that the microenvironment of the cartilage cells is highly structured and that NCP (link proteins, calcium-binding proteins and matrix glycoproteins) are important for cell-matrix interrelationships (Melrose & Ghosh, 1988). The attachment of a to its matrix via specific cell membrane receptors and intercalated transmembrane glycoproteins may allow the cell to respond to any changes in its matrix and to co-ordinate growth and repair (Huang, 1977). It is thus interesting to note that degraded link proteins have been found in human intervertebral disc (Eyre et al. 1988).

Blood supply Fibrocartilage is generally poorly vascularised. The lack of blood vessels is a striking feature of fibrocartilage in intervertebral discs (Humzah & Soames, 1988), knee joint menisci (Arnoczky et al. 1988), the articular portions of the menisci of the wrist (Thiru-Pathi, Ferlic, Clayton & McClure, 1986) and temporomandibular (McDevitt, 4 M. BENJAMIN AND E. J. EVANS 1989) , and in the attachment zones of tendons and ligaments (Benjamin et al. 1986; Woo et al. 1988). Where blood vessels are present, they are limited to the periphery of fibrocartilage. It is significant that chondrogenesis in the menisci of the knee joint largely follows the marked decline in vascularity that occurs after birth (Clark & Ogden, 1983). In adult vertebrae, relatively few blood vessels from the marrow spaces beneath the cartilage end plates perforate the calcified layer binding the end plate to the . In childhood and adolescence, the sites of the original blood vessels in the end plates are filled with fibrocartilage. These create weak points from which Schmorl's nodes develop (Taylor & Twomey, 1988). A similar obliteration of blood vessels occurs in the chick tibia when cartilage canals are replaced by fibrocartilage (Lutfi, 1970). In both cartilage end plates and tendon and ligament attachments, subchondral bone may be locally absent (Maroudas, Stockwell, Nachemson & Urban, 1975; Evans, Benjamin & Pemberton, 1990). Marrow spaces thus abut directly on fibrocartilage and this may be important for nutrition. The avascularity of fibrocartilage must be maintained by anti-angiogenesis factors and diffusion must be the principal mechanism for meeting the nutritional requirements of the cartilage cells. Fibrocartilage is usually subject to periodic compression and this motion may well favour an influx of nutrient-carrying water (Bogduk & Twomey, 1987). Inhibitors may also be responsible for the general resistance of fibrocartilage to tumour invasion. Nerve supply Nerve fibres and free nerve endings have been identified in many organs that contain fibrocartilage. The nerves are located mainly at the periphery of the intervertebral disc (Bogduk, 1988; Humzah & Soames, 1988). Mechanoreceptors have been recognised in menisci by the use of a gold chloride staining technique incorporating a prior treatment of the fibrocartilage with Triton X-100 (Zimny, Onge & Albright, 1987). Indeed Zimny (1988) argues that mechanoreceptors are invariably present in association with intra-articular discs, though McDevitt (1989) states, to the contrary, that the of the temporomandibular joint is devoid of all sensory receptors. Where mechanoreceptors are present, they are most conspicuous in areas related to the extremes of movement (e.g. meniscal horns). They could represent an important mechanism for sensing movement and providing proprioceptive information about joint position. Calcification and Matrix vesicles that are believed to act as the initial loci of calcification have been identified in fibrocartilage at tendon-bone junctions (Yamada, 1976). The calcified fibrocartilage is continuous with the adjacent, calcified, hyaline cartilage that is typical of the deeper reaches of the articular tissue lining synovial joints (Benjamin et al. 1986). Like this tissue, it has a permanence that one does not normally associate with calcified cartilage (Badi, 1972; Beresford, 1981). The 'tidemark' between calcified and uncalcified tissues stains basophilically with haematoxylin and eosin. It is here that hard and soft tissues separate during maceration (Benjamin et al. 1986). The fibrocartilage in the os penis of the rat calcifies with age under the influence of testosterone (Rasmussen, Vilmann & Juhl, 1986) and pathological deposits of calcium in meniscal fibrocartilage are characteristic of chondrocalcinosis (Sokoloff, 1983; Mandel, Mandel, Carroll & Halverson, 1984). When the crystals of calcium pyrophosphate dihydrate are released into the joint space they evoke an inflammatory reaction reminiscent of gout. Fibrocartilage 5 Calcified fibrocartilage that is considered to play a role in ossification has been described in epiphysial plates (Ogden, Hempton & Southwick, 1975), during fracture healing (Fawcett, 1986) and in normal and abnormal ligaments and tendons (Hirsch & Morgan, 1939; Knese & Biermann, 1958; Cooper & Misol, 1970; Badi, 1972). Modern imaging techniques Ultrasound can distinguish between hyaline and fibrocartilage. The acetabular labrum is echogenic as are fibrous structures elsewhere in the body (Yousefzadeh & Ramilo, 1987). Hyaline articular cartilage is hypoechoic. The echogeneity of fibrocartilage is probably associated with its lower water content. Computed tomography (CT) and magnetic resonance imaging (MRI) can also distinguish fibro- from hyaline cartilage. MRI has the advantage over CT that it can depict hyaline cartilage and fibrocartilage directly and with good tissue contrast (K6nig, Sauter, Deimling & Vogt, 1987). Tears and degenerative lesions of fibrocartilage cause an increase in spin density and thus signal enhancement. Arthroscopy, too, can be used to study fibrocartilaginous structures in joints (Altman & Gray, 1983). With ever- improving spatial resolution, these modern imaging techniques offer tremendous potential for investigating fibrocartilage. Mechanical properties Fibrocartilaginous structures such as menisci, and intervertebral discs that contain large amounts of Type I collagen, are anisotropic. Thus, their mechanical properties vary both with the position of the specimen and the direction of testing. Generally, the mechanical properties of fibrocartilage in menisci and intervertebral discs are intermediate between those of hyaline cartilage and tendon. The tensile strength of fibrocartilage (about 10 MPa) is less than that of tendon (about 55 MPa) but greater than that of hyaline cartilage (about 4 MPa) (Yamada, 1970). In view of these relationships, it is interesting that Smith (1962) has suggested that fibrous epiphysial plates (such as that at the upper end of the tibia) are subjected to tensile forces, while most epiphysial plates only withstand compression. The elongation of fibrocartilage at rupture (about 13 %) is less than that of hyaline cartilage (about 25 %), but greater then that of tendon (9-5 %) (Yamada, 1970). In compression, the strength of fibrocartilage is similar to that of hyaline cartilage, but it is less stiff. Both the aggregate and elastic moduli are about half those of articular cartilage (Arnoczky et al. 1988; Procter et al. 1989). Tendon cannot withstand compressive forces as it is too flexible. Fibrocartilage swells when exposed to buffers of low ionic concentration in a similar way to articular cartilage, while tendon does not. The swelling properties are correlated with the presence of glycosaminoglycans in fibrocartilage (Koob, 1989; Koob & Vogel, 1987).

DEVELOPMENT, GROWTH, DEGENERATION AND REPAIR Development and growth Fibrocartilage develops by metaplasia from precartilage, hyaline cartilage and particularly from fibrous tissue. Where it develops in mesenchyme, an increased fibrous content precedes the appearance of cartilage cells (Rasmussen et al. 1986; Murakami, 1987). Thus, chondrocytes are not responsible for the initial formation of collagen and the accumulation of amorphous cartilage matrix may need a fibrous environment. 6 M. BENJAMIN AND E. J. EVANS Metaplasia from precartilage occurs in intervertebral discs (Peacock, 1951) and metaplasia from hyaline cartilage occurs in the articular of the temporo- mandibular and acromioclavicular joints (Slootweg & Miller, 1986; Tiurina, 1985) and in ageing costal cartilage (Williams, Warwick, Dyson & Bannister, 1989). Metaplasia from hyaline cartilage is a feature of chondromalacia or achondroplasia in the tracheal rings of miniature dogs (Dallman, McClure & Brown, 1988) and is also found in hyaline articular cartilage damaged by freezing (Malinin, Wagner, Pita & Lo, 1985). Metaplasia from fibrous tissue is typical of the heart (Sandusky, Kerr & Capen, 1979) and is found in knee joint menisci (Clark & Ogden, 1983), a coracoclavicular joint (Lewis, 1959) and abnormal or aged ligaments and their attachments (Ferretti, Ippolito, Mariani & Puddu, 1983; Powers et al. 1986; Scapinelli, 1989; Yahia et al. 1989). Fibrocartilage also develops in the fibrous capsule surrounding cementless hip prostheses in areas subject to compression (Kozinn, Johanson & Bullough, 1986). Scapinelli & Little (1970) have suggested that it is a combination of compressive and rotatory forces that induces metaplasia of fibrous tissue into fibrocartilage. In the os penis of the rat, fibrocartilage develops from fibrous tissue under the influence of androgens (Murakami, 1986; Murakami & Mizuno, 1984; Rasmussen et al. 1986). Furthermore, Glucksmann & Cherry (1972) have shown that testosterone ad- ministered to female rats induces the development of an os clitoridis containing fibrocartilage. Fibrocartilage appears in the inner part of the annulus fibrosus of the intervertebral disc long before it is seen in the nucleus pulposus. It is formed from a specialised embryonic cartilage that surrounds the notochord (Peacock, 1951). This cartilage also contributes to the development of the nucleus pulposus. The cartilage has become fibrocartilaginous by birth, is invaded by notochordal cells and begins to liquefy. During childhood, the number of notochordal cells declines so that the nucleus of an adolescent or young adult is fibrocartilaginous like the inner annulus (Taylor & Twomey, 1988; Oda, Tanaka & Tsuzuki, 1988). The period when notochordal tissue is replaced by fibrocartilage coincides with a dramatic increase in the volume of the nucleus pulposus. The nutritional status of the notochordal cells becomes un- favourable and this may trigger the formation of fibrocartilage (Taylor & Twomey, 1988). It has been suggested that viable notochordal cells can destroy the fibrocartilaginous inner annulus (Butler, 1988). Where notochordal cells are absent or greatly reduced in number later in life (as in the human disc), the nucleus pulposus is a fibrocartilage formed by proliferation of the inner annulus (Butler, 1988). Although the essence of the highly complex architecture of the annulus fibrosus is established long before movement or stress occurs in the vertebral column (Peacock, 1951), the postnatal growth of the intervertebral disc is influenced by mechanical phenomena associated with normal posture (Taylor, 1975). Furthermore, the development of matrix, loss of blood vessels and the orientation of fibres in knee joint menisci, are thought to be influenced by joint movement (Arnoczky et al. 1988). Merrilees & Flint (1980) attach great importance to the influence of pressure on the development of fibrocartilage in tendons that pass round bony pulleys and Beckhan, Dimond & Greenlee (1977) have shown that fibrocartilage fails to develop in the tendons of paralysed chick embryos. Fibrocartilage can appear and disappear in tendons that are re-routed to confront or avoid bony pulleys (Gillard et al. 1979; Beresford, 1981). Fibrocartilaginous nodules develop by metaplasia in the ligamentum nuchae of man in regions of great mobility, where the ligament is pressed against Fibrocartilage 7 vertebral spines during neck flexion (Scapinelli, 1963). They become calcified and are replaced by bone. Abnormal biomechanical forces can lead to fibrocartilaginous proliferation at the attachment sites of ligaments and tendons. Jumper's knee is a tendonitis that affects the bone-tendon junction of the patellar or quadriceps tendons (Ferretti et al. 1983). The changes include a marked thickening of the zone of fibrocartilage and its eventual conversion to bone. In supra- and interspinous ligaments of young adults with disc disease, there is a metaplasia to fibrocartilage which is associated with other signs of wear and tear (Yahia et al. 1989). A proliferation of fibrocartilage is also characteristic of the ligamentum flavum in horses with cervical static stenosis (Powers et al. 1986). Murakami (1987) has presented some interesting data on the time sequence with which chondrocytes and collagen types appear in the developing fibrocartilage of the os penis in the rat. His studies show that the dominant collagen in the fibrocartilage (Type I) precedes the first appearance of mature cartilage cells and that the differentiation of the chondrocytes corresponds with the first immunocytochemical detection of Type II collagen. Degeneration Fibrocartilage can degenerate with age (Mikic, 1978; Oda et al. 1988; Arnoczky et al. 1988; Eyre et al. 1988) or in response to external influences (Jasin, 1983). Degeneration is particularly common in avascular regions. Thus, avascularity is often required for fibrocartilage to develop, but may lead to its degeneration. Cellular degeneration occurs in the early stages of remodelling of the mandibular attachment of masseter during bite raising (Yamada, Hanada, Morita & Ozawa, 1988). Where bacterial products induce fibrocartilage degeneration, there is evidence that they do so by stimulating chondrocytes directly (Jasin, 1983). An unusual complication that may arise from the degeneration of fibrocartilage is the formation of emboli from the intervertebral disc that may enter the anterior spinal artery and cause a fatal spinal cord infarction (Khang-Loon, Gorell & Hayden, 1980). Degenerative changes are prominent in the triangular fibrocartilage disc of the wrist joint in elderly people (Mikic, 1978). The degeneration is more frequent and advanced on the ulnar side of the disc - perhaps because the biomechanical forces are more intense on that side. The degeneration affects the avascular portion of the disc but not the vascularised edges. Avascularity and degeneration of knee joint menisci become more obvious in the elderly and are particularly characteristic of the central regions of a meniscus (Ghosh & Taylor, 1987). This may be related to the horizontal tears that affect this region. Although collagen degenerates with age, there is a surprising, age-related increase in extractable proteoglycans. These changes are in sharp contrast to those in articular cartilage (Arnoczky et al. 1988). Proteoglycan synthesis in menisci from osteoarthritic and rheumatoid knee joints is also enhanced (Ghosh, Ingman & Taylor, 1975). However, the enzymatic mechanisms involved in the turnover of collagen and proteoglycans are largely unkndwn. The available data have been reviewed by Ghosh & Taylor (1987). Degeneration is common in the intervertebral discs of the cat (Butler, 1988). As a disc degenerates, fibrocartilage initially proliferates in the inner annulus and bulges into an area vacated by the notochordal cells of the nucleus pulposus. These are extruded into the synovial sheath of the intercapital ligament. The now central fibrocartilage disintegrates and the adjacent vertebrae move closer together. Melrose 8 M. BENJAMIN AND E. J. EVANS & Ghosh (1988) have suggested that proteins similar to those that inhibit mineralisation of bone matrix are present in normal intervertebral discs. It is thus worth noting that degeneration of the fibrocartilaginous nucleus pulposus of the adult disc follows mineralisation and bony invasion of the cartilage end plate (Oda et al. 1988). Repair Fibrocartilage can repair itself and is also involved in the healing of articular cartilage and bone. Basic scientific studies on fibrocartilage repair have become more important now that meniscectomy is known to increase the risk of degenerative joint disease. There is evidence to suggest that repair is better in young animals than old (Moon, Kim & Ok, 1984). It seems that meniscal fibrocartilage cells are normally incapable of healing the tissue and that repair depends on fibrous tissue generated by mesenchymal cells derived from the synovium or the peripheral vasculature (Kim & Moon, 1979; Ghadially, Wedge & Lalonde, 1986; Ghosh & Taylor, 1987). Only later is there a metaplasia of fibrous tissue to fibrocartilage (Arnoczky et al. 1988). However, Whipple, Caspari & Meyers (1984) have suggested that repair is mediated by a proliferation of chondrocytes. If defects in the avascular region of the meniscus are filled with an exogenous fibrin clot, the wound is healed and fibrous tissue appears which undergoes metaplasia to fibrocartilage (Arnoczky et al. 1988). In addition, Webber, Harris & Hough (1985) have demonstrated that cultured, meniscal cartilage cells divide and synthesise in response to platelet-derived growth factors. It may be that the clot resulting from an injury involving the peripheral blood vessels of a meniscus provides an appropriate chemotactic and mitogenic stimulus for the reparative cells (Arnoczky et al. 1988). Injury to the annulus fibrosus of the intervertebral disc is followed by an ingrowth of scar tissue with little repair (Eyre et al. 1988). However, Lipson (1988) has shown that the protruding tissue removed at operation for prolapsed intervertebral disc contains less mature collagen than in situ annulus fibrosus, and shows proliferative fronts of fibrocartilage cells near the surface. He therefore makes the unusual suggestion that herniated discs are proliferating, metaplastic fibrocartilage that is probably derived from the annulus fibrosus rather than the nucleus pulposus. Injection of chemopapain into the nucleus pulposus of dogs causes reduction of disc thickness with a loss of proteoglycan (Humzah & Soames, 1988). Provided the dose is not too high, the nucleus eventually regenerates and the height ofthe disc is restored. However, surgical excision of the nucleus is not followed by regeneration. The extent to which fibrocartilage at the attachment zones of ligaments is reconstituted in autografts and allografts is largely unknown, although the work of Jones et al. (1987) suggests that the tissue does re-establish itself during the surgical reconstruction of the long flexor tendons of the fingers. It would be of interest to investigate the influence of fibrin clots in stimulating the regeneration of fibrocartilage at attachment sites. The role of fibrocartilage in the repair of articular hyaline cartilage has been extensively investigated. The response of articular cartilage to injury varies according to the depth of the wound and whether or not it encroaches on the bony vasculature. Full thickness lesions, such as those produced by drill holes, are initially filled by a clot, which is replaced by fibrous tissue, fibrocartilage and then hyaline cartilage (Albright & Misra, 1983). The fibrocartilage arises from cancellous bone or synovial pannus, but is not derived from articular cartilage at the edges of the defect (Meachim & Roberts, 1971; Edwards & Chrisman, 1979). If chondrocytes are damaged by Fibrocartilage 9 freezing prior to transplantation of articular hyaline cartilage, the dead tissue is initially replaced by fibrocartilage, but may form hyaline cartilage after long periods of time (Salenius, Holmstrom, Koskinen & Alho, 1982; Malinin et al. 1985). Materials such as collagen sponge, or glutaraldehyde-treated meniscus placed in defects of articular cartilage encourage repair (Speer, Chuapil, Volz & Holmes, 1979; Rubak, 1982; Heatley & Revell, 1985). Collagen sponge stimulates more fibrocartilage than hyaline cartilage, but periosteal grafts enhance the formation of hyaline cartilage (Speer et al. 1979; Rubak, 1982). Passive motion of the involved joints speeds fibrocartilaginous healing. Indeed, according to Radin (1987), motion is essential for fibrocartilage formation from an initial fibrous repair and Sevitt (1981) comments that large amounts of fibrocartilage are associated with excessive motion and non-union of the bony fragments during fracture healing.

DISTRIBUTION Fibrocartilage is widely distributed throughout the animal kingdom. It is well known in mammals and is also present in teleosts (Benjamin, 1989), reptiles (Haines, 1942), and birds (Schaffer, 1930; Bock, 1974). Schaffer (1930) also draws our attention to fibrocartilage in the endosternite or endocranial cartilage of the cephalopod Limulus. According to Person & Philpott (1969), similar tissues are found in scorpions, spiders and mites. Many points relating to fibrocartilage at specific sites have already been discussed. This section mentions certain additional features of interest, but space precludes a comprehensive survey of the distribution of fibrocartilage. Ligaments and tendons Fibrocartilage is constantly present at the attachment sites of epiphysial limb tendons, but is largely absent from metaphysial and diaphysial tendons (Schneider, 1956; Benjamin et al. 1986). The work of Cooper & Misol (1970) did much to correct the traditional view that all ligaments are attached to bone by Sharpey's fibres. They recognised four zones at certain attachment sites - fibrous tissue, fibrocartilage, mineralised fibrocartilage and bone. However, the widespread implication in the recent literature that most ligaments and tendons attach to bone via a zone of fibrocartilage is incorrect. Furthermore, the amount of fibrocartilage varies between different ligaments or tendons, between the two ends of the same ligament or tendon and in the superficial and deep parts of the same attachment zone (Evans et al. 1990). Schneider (1956) suggested that fibrocartilage is present in epiphysial tendons or ligaments because epiphyses remain cartilaginous for longer than diaphyses. However, Benjamin et al. (1986) postulated that fibrocartilage is characteristic of epiphysial tendons because of the change in angle that occurs between tendon and bone during joint movements. Other authors too have also suggested a mechanical function for fibrocartilage at attachment sites (Schneider, 1956; Knese & Biermann, 1958; Cooper & Misol, 1970; Noyes, DeLucas & Torvik, 1974; Woo et al. 1988). A cartilage matrix that binds collagen fibres together should diffuse forces over the attachment site and minimise local concentrations of stress. The zonal arrangement of tissues may reflect a gradual change in mechanical properties from ligament to bone. The decrease in stress concentration would reduce the chance of failure of a ligament under force. Pathological increases in the amount of uncalcified fibrocartilage at attachment sites might diminish mechanical efficiency by altering the proportions of the tissues (Ippolito & Postacchini, 1981; Ferretti et al. 1983). This would increase the risk of ligament or tendon failure. In contrast, when meniscal fibrocartilage is used to repair 10 M. BENJAMIN AND E. J. EVANS anterior cruciate ligaments, the tissue undergoes a metaplasia to pure fibrous tissue (Braun, Rohe, Buchmann & Ewerbeck, 1987). This presumably increases mechanical efficiency in the central region of the ligament, which is subject only to tension. The fibrocartilage could also contribute to the growth of the ligament, tendon or bone (Knese & Biermann, 1958; Cooper & Misol, 1970; Hurov, 1986), be involved in the remodelling of fibrous tissue (Yamada et al. 1988) and inhibit bone resorption or the spread of mineralisation into fibrous tissue (Cooper & Misol, 1970; Laros, Tipton & Cooper, 1971). Frost (1986) has long argued that cartilage of any kind that lies directly on bone completely prevents bone resorption. The development of fibrocartilage in tendons in contact with bony pulleys has already been discussed. The pulleys themselves may also be covered with fibrocartilage, for the tissue is found on the tibia and fibula where bone is in contact with tendons that pass behind the ankle joint (Stilwell & Gray, 1954). Where tendons or ligaments lie in grooves, the marginal crests of the grooves are fibrocartilaginous and serve for the attachment of ligaments, retinacula or tendon sheaths. Synovial joints Mention has already been made of fibrocartilaginous articular surfaces in the occasional coracoclavicular joint of man. The temporomandibular and acromio- clavicular joints, which at first are lined by hyaline articular cartilage, develop fibrocartilaginous articular surfaces at approximately 17-20 years (Tiurina, 1985; Slootweg & Miller, 1986). Indeed, cartilage matrix and cells may be so sparse in the temporomandibular joint that the articular surface must often be regarded as pure fibrous tissue (McDevitt, 1989). Fibrocartilaginous articular surfaces are generally considered an adaptation to resisting large shearing forces. The temporomandibular joint is subject to great wear and tear and a consequent demand for adaptive remodelling (McDevitt, 1989). However, the generality of equating a fibrocartilaginous articular surface with shearing forces has been questioned by Bock & Morioka (1971). They describe a unique that is lined by fibrocartilage in birds of the family Meliphagidae. These birds have an extraordinary ectethmoid-mandibular joint that lies on the ramus of the half way between the quadrate articulation and the anterior tip of the mandible. It forms a brace for the jaw and is an adaptation for the bird's feeding habits. There is virtually no movement between the articular surfaces the are simply pressed together when the mouth is closed and move directly away from each other when it is opened. Whether menisci and articular discs are fibrocartilaginous has long been a matter for debate. Certainly to use the term fibrocartilage as a synonym for menisci and discs is inaccurate. Sickle & Kincaid (1978) point out that many menisci and discs are devoid of any form of cartilage cell and the status of menisci in the temporomandibular and knee joints, in particular, is debated by Murakami & Hoshino (1985) and by Somer & Somer (1983). Discs are common in the oro-mandibular region of teleosts, but there is tremendous variation in their structure. Some resemble fibrocartilage (Benjamin, 1989). The triangular fibrocartilage complex of the wrist contains a fibrocartilaginous articular disc, but has other parts that are purely fibrous (Benjamin et al. 1990). Numerous fibrocartilaginous menisci have been described in the interphalangeal and metacarpophalangeal joints of the hand (Fisher et al. 1985). They probably serve similar functions to those in the knee and may be involved in the disease pattern and deformity of rheumatoid arthritis. The finger menisci are associated with fibrocartilaginous volar plates (Norregaard, Jakobsen & Nielsen, 1987). Fibrocartilage 11 Symphyses Fibrocartilage is the most abundant tissue of the intervertebral disc (Bogduk & Twomey, 1987). The inner portions of the annulus fibrosus are more fibrocartilaginous than the outer (Butler, 1988; Hukins, 1988). However, fibrocartilage is present at the attachment of the outer annulus to the vertebral end plates (Peacock, 1951; Butler, 1988). Indeed, the end plates themselves are largely fibrocartilaginous in older, lumbar vertebrae (Bogduk & Twomey, 1987). The presence of fibrocartilage in the nucleus pulposus varies with age and species, but the tissue is normally found in adult man. There is an extraordinary mandibular in whalebone whales (Pivorunas, 1977). An enormous Y-shaped fibrocartilage extends from the symphysis into the muscular ventral pouch. The stem of the Y is attached to the symphysis and the arms are parallel to the mandibular rami. Both produce visible surface ridges. Pivorunas (1977) suggests that the fibrocartilage helps to open the mouth - a problem for these whales! The of the female guinea-pig undergoes a spectacular relaxation that is associated with the large size of the young. An intracartilaginous fissure forms by the degeneration of hyaline cartilage before birth (Ruth, 1936). Either side of the fissure, the hyaline cartilage transforms into fibrocartilage, which is continuous with strands of fibrous tissue that cross the fissure. However, according to Crelin & Koch (1965) the fibrocartilage in the pubic symphysis of the mouse does not arise from hyaline cartilage, but from a metaplasia of fibrous tissue. Other sites Fibrocartilage is associated with the penis of many animals. The distal segment of the os penis in the rat is a fibrocartilage that is gradually replaced by bone after 10 weeks of age (Murakami, 1987). In small domestic ruminants, the urethra extends beyond the tip of the penis as a filiform appendage or urethral process that has a fibrocartilaginous (Ghoshal & Bal, 1976). The fibrocartilage supports the erectile tissue and enables it to expand without bending during copulation. In the ram, fibrocartilage is also present in large amounts in the glans penis and, in the bull, the tunica albuginea is fibrocartilaginous. The fibrocartilage in the bull's penis is responsible for its firmness and rigidity (Fitzgerald, 1963). Fibrocartilage is found in the centre of the ligamentum arteriosum and in the central fibrous body of the heart (Balogh, 1971; Sandusky et al. 1979; Dohr, Ebner & Gallasch, 1986). It also develops as a small nodule within the leaflets of the aortic and pulmonary valves (Seemayer, Thelmo & Morin, 1973). According to the early histologists, fibrous connective tissue in the aortic wall can transform into fibrocartilage and indeed, in the dog, fibrocartilage is commonly present at the root of the aorta (Sandusky et al. 1979). Perhaps avascularity and mechanical factors associated with the pulse wave may be responsible for the presence of fibrocartilage in this vessel. It is intriguing to note that metaplasia to cartilage occurs in the tunica media of vessels that are prevented from normal expansion during the passage of pulse waves (Rodbard, 1958). According to most standard teaching texts, labra are fibrocartilaginous, although Johnson (1987) states that the glenoidal labrum is mainly pure fibrous tissue. The spheno-petrosal and petro-occipital synchrondroses are normally fibrocartilaginous fissures that never ossify, although the fibrocartilage can be replaced by bone in patients suffering from Crouzon syndrome (Kreiborg & Bjork, 1982). 12 M. BENJAMIN AND E. J. EVANS

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