437

J. Anat. (1977), 123, 2, pp. 437-457 With 15 figures Printed in Great Britain

The collagen fibril organization in human articular cartilage R. J. MINNS* AND F. S. STEVENt

*Department of Engineering Science, University of Durham and tDepartment of Medical Biochemistry, University of Manchester

(Accepted 15 April 1976) INTRODUCTION

Articular cartilage consists of three major components: water, collagen and proteoglycans. The main function of the collagen fibrils is to bind proteoglycan into a structural gel which traps water. The collagen fibrils form a three-dimensional network adapted to load-bearing at the joint. Since Benninghoff's (1925) initial proposal that the collagen fibrils were arranged in arcades there have been many conflicting reports about the organization of fibrils in articular cartilage (Bullough & Goodfellow, 1968; Weiss, Rosenberg & Helfet, 1968; Clarke, 1971 b; Mital & Millington, 1971; Meachim, Denham, Emery & Wilkinson, 1974; Redler, 1974). Studies of collagen fibrillar structure within cartilage are difficult because of the presence of proteoglycans which bind strongly to collagen fibrils and mask them (Podrazky et al. 1971). Mulholland (1974) was able to remove part of the proteoglycan from the surface layers of cubes of human articular cartilage by short digestion with papain; the collagen fibrils were then examined in the scanning electron microscope, with excellent results. In the present study a new technique has been used which selectively depolymerises the proteoglycan (Steven & Thomas, 1973). Full-thickness samples of pure cartilage collagen can then be examined in the scanning electron microscope. A second enzymic technique has been developed to reveal the collagen network in the calcified zone. The non-calcified cartilage was removed by long digestion with papain and then a short decalcification with EDTA exposed collagen fibrils in the calcified cartilage. In this paper the framework of collagen fibrils in the deep, middle and superficial layers of human articular cartilage is described. MATERIALS AND METHODS

Cartilage was obtained post mortem from the medial femoral condyles of young male adults aged from 27 to 40 years. Brushing with India ink (Meachim, 1972) revealed no, or no more than minimal, fibrillation. To give an initial indication of collagen alignments, split lines were made by inserting a metal pin charged with India ink into the surface (Meachim et al. 1974) at approximately 5 mm intervals over the whole articular surface. Specimens of tissue were cut into strips approximately 3 x 3 x 1 mm, some parallel and some perpendicular to the split lines (Fig. 1). The strips cut perpendicular to the split lines were slightly tapered for identification after treatment. In addition cubes of tissue approximately 4 x 4 x 4 mm were cut which

438

R. J. MINNS AND F. S. STEVEN

Split line Knife Surface

A

Fractured face Cut surface

B

Artificial

4

Fig. 1. (A) Sketch showing method of exposing the area within the middle zone of the articular cartilage by removing the superficial layer with a sharp knife. (B) The specimen is then broken along a plane parallel to the split generated on the surface.

included the calcified layer and some subchondral bone. Unfixed tissue strips were washed to remove any residual India ink and then treated twice with 3 % H202 in 1 % NaCl in the dark at 20 °C for 18 hours, followed by digestion with trypsin and 1 % NaCl washing as described by Steven & Thomas (1973). Less than 1 % of the total tissue collagen was solubilized during this whole extraction procedure. Amino acid analysis of a small section removed from the strips before coating demonstrated the purity of the collagen fibrils, and the complete removal of the proteoglycans and cellular material, after the H202 and trypsin treatment. The structure observed by scanning electron microscopy consisted entirely of collagen. Unfixed cubes of cartilage were treated for 24 hours at 60 °C with 0- 1 % papain in 0 1 M-NaHCO3, the pH being adjusted to 8-5 with 10 mm cysteine. After washing, they were then suspended in 1 M ethylene diaminetetra-acetic acid (EDTA) at pH 7-0 for 30 minutes at 20 'C. The collagen fibrils at this stage were completely insoluble in either water or 0-2 M acetic acid. After washing in water the specimens were prepared for scanning electron microscopy. This entailed a very careful dehydration procedure using increasing strengths of acetone (50-100 % in steps of 10 %, 20 minutes at each step), followed by critical point drying using CO2 as the drying liquid (Polaron, Critical point drying apparatus type E3000).

Collagen fibrils in articular cartilage

439

In order to examine the middle layer of the cartilage a sharp knife was used to remove approximately 0-2 mm of the remaining articular surface of the dehydrated specimens (Fig. 1 a). The strip was then split by bending to expose a section parallel to the direction of the split line (Fig. 1 b). Some of the cube specimens after decalcification, and before drying, were also split by bending in order to reveal the internal structure. The specimens were mounted on marked aluminium stubs and coated with a layer of gold-palladium (60/40) 150-200 angstroms thick. The coated specimens were examined at tilt angles between 0 and 450 in a Cambridge Stereoscan S4-10 scanning electron microscope operated at an accelerating voltage of 20 kV. The results were recorded with an Exacta VX500 camera on Ilford FP4 135 roll film. RESULTS

The fibrillar architecture of the bony trabeculae and of the calcified cartilage shown in the Figures was revealed by papain digestion of the uncalcified cartilage followed by the partial decalcification of the remainder.

Fibrillar architecture of bony trabeculae Figure 2 shows a low magnification of the trabeculae just deep of the subchondral bone. The diameters of the intertrabecular spaces ranged between 300 and 500 ,tm. Figure 3 is a higher magnification of the surface of a single trabecula, showing the fibrillar organization. The details of the fibrils are presented at even higher magnification in Figure 4, in which the individual fine fibrils can be seen to be grouped in small bundles (referred to as trabecular fibre bundles in Table 1) 1-1 5 ,um in diameter. Some of these fine fibrils exhibit 70 nm surface periodicity.

Fibrillar architecture of the calcified cartilage zone Figure 5 shows a split through the calcified cartilage zone, revealing the underlying trabeculae (indicated by T). The trabecular fibres can be seen to be grouped into yet larger bundles of 10-15 ,um in this region (A of Fig. 5). It can also be seen from Figure 5 that the bundles marked A are grouped into even larger bundles (indicated by B in Figure 5) of 55 ,tm average diameter. These larger bundles are presented at higher magnification in Figure 6. In the side of one of these larger bundles (Fig. 6) can be seen two canaliculi labelled C1 and C2, each with a diameter of 8 ,tm. Cl is shown in higher magnification in Figure 7 and its wall appears to be constructed of a tight network of collagen fibrils approximately 0-08 to 010 l,m in diameter. An oblique view of the surface of the calcified cartilage zone after treatment with papain and EDTA shows an undulating surface made up of fibrils arranged as a fine random network (Fig. 8). A view normal to this undulating surface (Fig. 9) shows a group of tubules, one of which is marked Tu in Figure 9, with a diameter of approximately 20 ,um. Each tubule appears to be associated with its own set of radially oriented collagen fibrils, and each tubule is positioned between neighbouring tubules in a regular manner. The extent of each tubule domain (shown within the circle in Figure 9) is approximately 55 ,um and this corresponds to the fibre bundle

440

R. J. MINNS AND F. S. STEVEN

-. ... :t

,, . ;s;;;>

:r

s

¢,

>

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~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~T...

Fig. 2. Scanning electron micrograph of the trabeculae just deep to the subchondral bone after treatment with papain followed by EDTA. The removed cartilage was at the top, right. x 90.

diameter seen in the oblique view in Figure 5B. Trueta & Little (1960) observed similar tubules by transmission electron microscopy and considered them to be occupied by cells in the living tissue. The collagen fibres in the calcified zone are believed to continue through the uncalcified cartilage to the articular surface in the intact tissue (Lane & Weiss, 1975). In the preparations used to provide Figures 2-9 all the uncalcified collagen fibrils have been removed by papain digestion in order to expose the fibres of the calcified

Collagen fibrils in articular cartilage

441

Fig. 3. Higher magnification of the surface of a trabecula. x 855.

cartilage and bony trabeculae. Less drastic enzymic techniques were used to expose the collagen fibrils within the middle zone of uncalcified cartilage. Fibrillar architecture of the middle zone The middle zone appeared to consist of bundles containing numerous collagen fibrils oriented radial to the articular surface. These bundles were defined by margins where bundles with slightly different orientation intersected (Fig. 10); a similar

442

R. J. MINNS AND F. S. STEVEN

Fig. 4. Individual collagen fibrils can be clearly seen in the trabecula, some showing characteristic 70 nm periodicity (arrowed). x 8550.

arrangement was observed by Clarke (1971 b). Although these bundles were of irregular shape and had been sectioned obliquely, the bundle thicknesses were fairly uniform, falling in the region of 50-60,um. Lacunae appeared occasionally within these bundles (Fig. 10) near their margins. The individual collagen fibrils within the bundles were of approximate uniform diameter, 0-06-0-08 ,am ((60-80 nm), allowance being made for the thickness of the metallic coating. A number of differences was observed in the collagen fibrils surrounding the lacunae (Fig. 11) as compared

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443

Table 1. Table of dimensions of the fibrillar structures observed in the full depth of human articular cartilage Trabecular space Trabecular fibrils Trabecular fibre bundles Calcified fibre bundles Calcified collagen fibrils Canaliculus diameter Calcified surface undulations (peak to peak) Calcified surface holes (diameter) Circular zones of calcified surface Bundles in mid-zone Fibrils in mid-zone Lacunae in mid-zone (vertical section) Lacunae on surface (transverse section) Surface fibrils

300-500 um across 0 08-0 10 jtm (80-100 nm) 1-1 5 tm 10-15 ,tm 0-08-0 10 ,tm (80-100 nm) 8 ,tm 55 ,m 15-20,m 50-60 /tm 55 ,tm 0-06-0 08 Atm (60-80 nm) 10 ,um x 15 ,tm 25 ,um x 12 ,tm 0 06-0-09 ,um (60-90 nm)

with the collagen fibrils situated farther away from lacunae. A random meshwork of collagen fibrils appeared to surround the lacuna and the fibrils appeared to be packed more densely than the fibrils within other collagen bundles in the middle zone, and they also appeared to be thinner (approximate diameter 0-04 ,am or 40 nm) than the middle zone fibrils. Fine collagen fibrils were observed to traverse some of the lacunae. The fine meshwork of collagen fibrils present in the depths of such a lacuna (Fig. 11) may have partitioned the cavity between two chondrocytes in the living cartilage.

Fibrillar architecture of the surface of uncalcified cartilage The most striking feature observed in the surface collagen fibrils was their random orientation (Fig. 12); the fibrils were of similar diameter to those in the middle zone. The surface remaining after the removal of proteoglycans and cellular material was not smooth. Lacunae were observed on the surface; some lacunae appeared to be quite superficial (Fig. 12) while others appeared to be emerging through the surface collagen fibrils. In Figure 12 a superficial lacuna is shown which probably contained two chondrocytes. The internal surface of this lacuna exhibits a fine network of collagen fibrils (Fig. 13), randomly oriented like they were in the middle layer lacunae (Fig. 11). The densely packed fine collagen fibrils within the base of the superficial lacuna are shown in Figure 13. Presumably these same densely packed fibrils give rise to the dense layer of fine collagen fibrils observed on the edge of the lacuna (Fig. 11). The surface lacunae appeared to be compressed in a direction normal to the surface, and were somewhat flatter than lacunae observed in the middle zone. The surface layer exhibited raised, intertwined collagen fibrils: MacConaill (1951) termed this layer a galea aponeurotica or 'fibrous web' (Fig. 14). 'Lamina splendens' In our preparations the acellular bright layer devoid of collagen fibres described by MacConaill (1951) as the 'lamina splendens' was not seen. However, such a non-collagenous layer would not have survived the enzyme treatments we employed.

444

R. J.

MINNS

AND F.

S.

STEVEN

Fig. 5. A split in the fibrillar structure of the calcified zone showing fibre bundles oriented toward the surface. Calcified fibre bundles (arrow A) appear to be aggregated to form larger bundles (arrow B) shown sectioned at the exposed surface. The underlying trabecula (T) are also exposed at the base of the split. x 330. DISCUSSION

Previous studies on human articular cartilage have led to a number of opposing concepts of fibril organization. Most of these studies have employed intact cartilage containing collagen fibrils and associated proteoglycans. However, the proteoglycans obscure the surface of collagen fibrils (see Clarke, 1971 a and b), so that no

Collagen fibrils in articular cartilage

445

Fig. 6. Higher magnification of the bundles exposed in the split seen in Fig. 5. Cl and C2 are canaliculi sectioned obliquely by the split, passing from the underlying trabeculae. x 82 5.

characteristic collagen periodicity is visible with the scanning electron microscope. A short digestion with papain removes proteoglycans and facilitates study of collagen fibrils and their organization (Mulholland, 1974). In the present study we removed the proteoglycans from the middle and superficial zones, and decalcified the deep zones, in human articular cartilage, thus enabling the organization of collagen fibrils in three zones of cartilage to be visualized by scanning electron microscopy.

446

R. J. MINNS AND F. S. STEVEN

k6l A-1"A'W_§.&. in*V7'v

8,

_

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-

_

_

,

.

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Fig. 7. View of an obliquely split canaliculus observed passing through the calcified zone from a trabecula. x 8250.

The buffer which replaced the enzymically removed non-collagenous components in its turn was very carefully replaced by acetone and then by liquid carbon dioxide, the latter disappearing during the critical point drying procedure. It is recognized that artifacts may be introduced at any stage in the preparation of unfixed material for scanning electron microscopy. The enzymic digestion of the space-filling proteoglycan molecules could conceivably have destabilized the collagen

Collagen fibrils in articular cartilage

447

Fig. 8. Oblique view of the calcified zone of articular cartilage showing the exposed surface. x 1020.

meshwork, allowing distortion of the fibrils during the drying process. However, in this study, deformation of the fibrils was not evident; they exhibited normal periodicity, were of uniform thickness along their length, and were not kinked except at the specimen faces. Clarke (1971 b) employed fixed tissue and reported collagen arrangements similar to those we found, supporting the conclusion that the techniques used in the present study caused minimal structural alterations. Clarke also noted surface distortion effects produced during the preparation of thin sections for scanning

448

R. J. MINNS AND F. S. STEVEN

to

M.

m

"I

I

_

r

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..*,

-

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at

Fig. 9. Collagen fibrillar arrangement of the calcified cartilage surface exposed after removal of the non-calcified cartilage. The circle has a diameter equivalent to that of an average fibre bundle (55 ,Itm). It is centred on the tubule (TU). x 1650.

electron microscopy: we cut our tissue into as large cubes as possible to minimize surface distortion during dehydration. Experience in our laboratory is that critical point drying after acetone dehydration of unfixed tissues is much more satisfactory than direct removal of the acetone from the specimen, in that it greatly reduces the distortion effects associated with acetone dehydration. The specimens were coated and held under vacuum until they were introduced into the scanning electron

Collagen fibrils in articular cartilage

449

i3iM. __.ff !s9-si _ M Fig. 10. View of the cloven surface of the middle zone, sectioned by the method shown in Fig. 1 (b), showing the demarcation between three large bundles of collagen fibrils, and an obliquely sectioned lacuna (L). x 1725.

w

microscope in order to prevent the specimens adsorbing atmospheric moisture. Each specimen was examined in detail before it was removed from the microscope, and then it was destroyed to prevent possible re-examination of a rehydrated specimen. We believe that, by the precautions we have taken, we have reduced artifacts to a minimum. Collagen fibrils were observed throughout the calcified and uncalcified zones of 29

ANA I23

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R. J. MINNS AND F. S. STEVEN

Fig. 11. A view of a lacuna showing an intricate system of collagen fibrils linking the lacunar walls, and which probably partitioned two chondrocytes. x 9000.

the cartilage. In the trabeculae aggregates of collagen fibrils were arranged in small bundles which were observed to coalesce into larger bundles just beneath the ' tidemark' (the interface between the calcified and uncalcified zones). The bundles ran radially towards the articular surface. Canaliculi within the subchondral bone, which may be channels connecting the vascular system (Trueta & Little, 1960), were observed within the trabeculae and also passing through the tidemark. The papain-exposed surface of the calcified zone, viewed from the articular surface

Collagen fibrils in articular cartilage

451

Fig. 12. The surface viewed normally, showing a lacuna. This lacuna was approximately 20 Am long, 10 Am wide and 5 ,um deep. x 1650.

towards the subchondral bone, exhibited tubules which were much more frequent than the canaliculi observed within the calcified zone. These tubules may be associated with the canalicular system, but they could also be derived from the spaces remaining after the enzymic removal of chondrocytes. The large bundles of collagen fibrils observed just deep to the tidemark were of similar diameter to the circular zones observed around each tubule on the papain exposed calcified surface (Figs. 8 and 9). Trueta & Little (1960), using the 29-2

452

R. J. MINNS AND F. S. STEVEN

__tv~~~~~~W 4ftj%.

N'". d.-

_-.

Fig. 13. Collagen fibrils observed within the base of the lacuna shown in Fig. 12. The fibrous division (P) across the middle suggests that two chondrocytes formerly occupied this lacuna. x 8250.

transmission electron microscope, described columns of orientated collagen fibres in calcified cartilage as well as columns of cells occupying lacunae alongside the collagen fibres. The diameters of the columns of cells observed in fixed tissue by these authors are comparable with the diameters of the tubules described in this study. The bundles of collagen fibrils observed in the uncalcified cartilage zone had similar dimensions to the fibre bundles at the tidemark, and also to the tubule circular zones, which suggests that the collagen bundles pass through the tidemark, through the surface

a,

Collagen fibrils in articular cartilage

453

Fig. 14. Surface collagen fibrils viewed normal to the articular surface, showing random orientation. The direction of the split line which was generated close to this specimen was left to right. x 8250.

of the calcified zone, and then upwards through the uncalcified cartilage, in agreement with Benninghoff's (1925) arcade concept. Weiss, Rosenberg & Helfet (1968) reported that the middle zone of cartilage contained randomly oriented collagen fibrils with little tendency to form bundles, but we found that the collagen fibrils of this zone had a radial orientation and did appear to be in bundles. We would agree with these authors that the surface fibrils run parallel to the articular surface, and that the

454

R. J. MINNS AND F. S. STEVEN

'Tide mark'

Fig. 15. Schematic view of the collagen fibrillar organisation in human articular cartilage in a full thickness block, from the surface to the deep subchondral bone, approximately fifty times full size.

lacunar walls consist of a denser organization of collagen fibrils than is found in the regions between lacunae. This has recently been confirmed by Lane & Weiss (1975). We did not observe any organization of collagen fibrils on the surface which might give rise to the ridge patterns observed by Mow, Lai & Redler (1974) and Redler (1974). The surface depressions reported by Mital & Millington (1971) may be identical to the depressions caused by surface lacunae observed in this study. Our overall observations on the fibrillar organization of articular cartilage (Fig. 15) are in general agreement with those proposed by Bullough & Goodfellow (1968). The observation that the superficial zone contains collagen fibrils which are predominantly aligned along one main axis and parallel to the surface, supports the explanations of Meachim et al. (1974) and of Bullough & Goodfellow (1968) regarding the mechanism by which 'split' lines are formed through the full thickness of cartilage. Ghadially, Ailsby & Oryschak (1974) reported the presence of a sheet of fine textured material covering the articular surface. MacConaill (1951) noted a thin acellular layer on the articular surface, which he termed the 'lamina splendens'. In the present study we would not have expected to see such a layer because it would have been removed by enzymic digestion. Fibrillation, as revealed by India ink staining, exhibits two forms (Meachim, 1972).

455 Collagen fibrils in articular cartilage The parallel linear patterns described by Meachim (1972), run in the same direction as the long axes of artificial splits, and seem to result from India ink remaining in the clefts between parallel bundles of collagen fibrils of the kind we observed just beneath the surface fibrils in the present study. It is probable that, with increasing age, the surface collagen fibrils become damaged and are removed, exposing the underlying bundles of collagen and giving the typical appearance of fibrillation. On the other hand the vertical clefts observed in fibrillated cartilage (Byers, 1974) may be caused by lateral separation of the collagen fibre bundles in the mid-zone, the result of shear fatigue severing the inter-connecting fibrils. Both explanations of fibrillation are compatible with the present observation that the bulk of the collagen in both the calcified and uncalcified zones is present in the form of oriented bundles rather than as randomly oriented fibrils. A third form of cartilage damage has been reported (Meachim, 1976) in which horizontal clefts have been observed in the deep zone at the calcified-uncalcified interface. When vertical clefts and horizontal clefts intersect, groups of bundles may become separated and then completely detach from the cartilage, as observed in grossly ulcerated cartilage (Byers, 1974). Redler et al. (1975) proposed that the tidemark helps to prevent shear damage to the collagen fibrils. The transition from calcified to uncalcified fibres within this zone, together with lateral movement of the collagen fibres during load bearing, (McCutchen, 1965) would almost certainly make the fibres more susceptible to shear fatigue at the interface: cleavage here would produce the horizontal clefts observed by Meachim (1976). The thickness of the tidemark may in fact be directly related to the resistance of the collagen fibres to shear fatigue fracture (Minns, 1976). SUMMARY

In this scanning electron microscopic study blocks of collagen fibrils were prepared from human articular cartilage, using two techniques which selectively removed either the proteoglycans alone, or both the proteoglycans and the collagen fibrils, of the non-calcified cartilage layer. Amino acid analysis of the fibrils confirmed the purity of the collagen after proteoglycan extraction. The cartilage was scanned in four different ways: (1) normal to the articular surface, (2) in superficial sections, (3) on surfaces of blocks which had been broken in planes parallel to artificial splits made by the insertion of a pin, and (4) on fracture surfaces which traversed the calcified cartilage and the subchondral bone. Five features of the organization of the collagen fibrils were specially noted: (1) Individual fibrils within the trabeculae joined to form small fibre bundles which became grouped into larger bundles at the calcified/uncalcified interface. (2) Fibrils in the deep and middle zones which, exhibiting the characteristic surface periodicity of collagen, were generally oriented toward the articular surface in large bundles approximately 55 ,tm across. (3) In the superficial zone, fibrils ran parallel to the surface. (4) The surface fibrils had random orientation, even at the bases of empty lacunae vacated by chondrocytes during specimen preparation. (5) The collagen fibrils of the lacunar walls appeared to be thinner and more closely packed than those between the lacunae. The fine collagen fibrils associated with the lacunar walls

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were frequently observed to pass through a large lacunar space, resulting in the formation of two or more compartments, each of which was presumably filled with a chondrocyte in the living cartilage. We wish to acknowledge the assistance of Mr I. H. Emery, Department of Orthopaedic Surgery, University of Liverpool; Dr G. Williams and Mr D. Page, Department of Pathology, University of Manchester, and Miss P. Edge and Mrs J. Watkins, Department of Medical Biochemistry, University of Manchester. We would also like to thank Professor M. A. MacConaill, University of Cork, and Dr G. E. Kempson, University of Southampton, for helpful comments in the preparation of the manuscript. REFERENCES BENNINGHOFF, A. (1925). Form und Bau der Gelenkknorpel in ihren Beziehungen zur Funktion. II. Der Aufbau des Gelenkknorpels in seinen Beziehungen zur Funktion. Zeitschrift fur Zellforschung und mikroskopische Anatomie 2, 783-862. BULLOUGH, P. & GOODFELLOW, J. W. (1968). The significance of the fine structure of articular cartilage. Journal of Bone and Joint Surgery 50B, 852-857. BYERS, P. D. (1974). What is osteoarthritic carilage? In Proceedings of the Symposium, Normal and Osteoarthritic Articular Cartilage (ed. S. Y. Ali, M. W. Elves and D. H. Leaback), pp. 131-139. London: Institute of Orthopaedics. CLARKE, I. C. (1971 a). Surface characteristics of human articular cartilage - a scanning electron microscope study. Journal of Anatomy 108, 23-30. CLARKE, I. C. (1971 b). Articular cartilage: a review and scanning electron microscope study. 1. The interterritorial fibrillar architecture. Journal of Bone and Joint Surgery 53B, 732-750. GHADIALLY, F. N., AILSBY, R. L. & ORYSCHAK, A. F. (1974). Scanning electron microscopy of superficial defects in articular cartilage. Annals of the Rheumatic Diseases 33, 327-332. LANE, J. M. & WEIss, C. (1975). Review of articular cartilage collagen research. Arthritis and Rheu,natism 18, 553-562. MACCONAILL, M. A. (1951). The movement of bones and joints. IV. The mechanical structure of articular cartilage. Journal of Bone and Joint Surgery 33B, 251-257. MCCUTCHEN, C. W. (1965). A note upon the tensile stresses in the collagen fibres of articular cartilage. Medical and Biological Engineering 3, 447-448. MEACHIM, G. (1972). Light microscopy of Indian ink preparations of fibrillated cartilage. Annals of the Rheumatic Diseases 31, 457-464. MEACHIM, G. (1976). Cartilage thinning in osteoarthrosis. British Orthopaedic Research Society, Meeting at Harlow Wood, 5 March. MEACHIM, G., DENHAM, D., EMERY, I. H. & WILKINSON, P. H. (1974). Collagen alignments and artificial splits at the surface of human articular cartilage. Journal of Anatomy 118, 101-118. MINNS, R. J. (1976). Cartilage ulceration and shear fatigue failure. Lancet 1, 907-908. MITAL, M. A. & MILLINGTON, P. F. (1971). Surface characteristics of articular cartilage. Micron 2, 236-249. Mow, V. C., LAI, W. M. & REDLER, I. (1974). Some surface characteristics of articular cartilage. I. A scanning electron microscopy study and a theoretical model for the dynamic interaction of synovial fluid and articular cartilage. Journal of Biomechanics 7, 449-456. MULHOLLAND, R. (1974). Lateral hydraulic permeability and morphology of articular cartilage. In Proceedings of the Symppsium, Normal and Osteoarthritic Articular Cartilage (ed. S. Y. Ali, M. W. Elves and D. H. Leaback), pp. 85-100. London: Institute of Orthopaedics. PODRAZKY, V., STEVEN, F. S., JACKSON, D. S., WEISS, J. B. & LEIBOVICH, S. J. (1971). Interaction of tropocollagen with protein-polysaccharide complexes. An analysis of the ionic groups responsible for interaction. Biochimica et biophysica acta 229, 690-697. REDLER, 1. (1974). A scanning electron microscopic study of human normal and osteoarthritic articular cartilage. Clinical Orthopaedics and Related Research 103, 262-268. REDLER, I., MOW, V. C., ZIMNY, M. L. & MANSELL, J. (1975). The ultrastructure and biomechanical significance of the tidemark of articular cartilage. Clinical Orthopaedics and Related Research 112, 357362.

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STEVEN, F. S. & THOMAS, H. (1973). Preparation of insoluble collagen from human cartilage. Biochemical Journal 135, 245-247. TRUETA, J. & LITTLE, K. (1960). The vascular contribution of osteogenesis. II. Studies with the electron microscope. Journal ofBone and Joint Surgery 42B, 367-376. WEISS, C., ROSENBERG, L. & HELFET, A. J. (1968). An ultra-structural study of normal young adult human articular cartilage. Journal ofBone and Joint Surgery 50A, 663-674.

The collagen fibril organization in human articular cartilage.

437 J. Anat. (1977), 123, 2, pp. 437-457 With 15 figures Printed in Great Britain The collagen fibril organization in human articular cartilage R. J...
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