Surface structure of articular cartilage. Historical review.

In the previous paper it has been shown that the surfaces of articular cartilage in living mammals and birds are not smooth but are covered by a series of secondary irregularities and of 20 to 30 [km. tertiary undulations, both superimposed on the broad primary anatomical contours (Gardner and McGillivray, 1971). The experiments from which this evidence has been derived have drawn attention to a historical paradox: the conspicuous smoothness of articular cartilage, emphasized by William Hunter (1742-43), is evident grossly. Yet the scanning electron microscope quickly revealed that articular cartilage surfaces are irregular and that the surface irregularities are sufficiently large to be easily seen with a primitive compound microscope. Cartilage surfaces have been viewed with hand lenses since 1742 and with compound microscopes since 1820 or earlier. How is it that observers failed to note the small irregularities which exist upon all varieties of articular cartilage? To examine this question and the historical development of knowledge of articular surfaces is the object of this short historical review which should be read in conjunction with the earlier report (Gardner and McGillivray, 1971). Considerable effort was directed towards understanding the structure of articular cartilage by William Hunter (1742-43); the 19th century literature attests to a continued interest in this problem. The literature demonstrates clearly that early workers in cartilage histology were biased in their approach and that they were preoccupied with the questions: Is cartilage cellular? Is cartilage vascular or avascular? and Is the articular surface covered by a synovial membrane? A substantial number of 19th century workers, armed with compound microscopes fitted with the new achromatic objective lenses introduced in the 1820s, made detailed studies of sections of mammalian articular cartilage cut freehand with a razor or with the early Rutherford microtome. Until 1845 or thereabouts, these investigators were mainly concerned to establish whether articular cartilage was vascular, whether, as William Hunter (1742-43) and Benjamin Brodie (1813) believed, the cartilage surface was covered by synovial 'membrane', and whether cartilage possessed cells, a question which arose naturally from the promulgation of the cell theory (Schleiden, 1838; Schwann, 1847). Several of the early students of cartilage histology drew careful illustrations showing the detailed microscopic structure of hyaline cartilage. In a number of these illustrations, the cartilage surface, with its small tertiary undulations, was clearly depicted. The small prominences were shown to overlie zones in which flattened chondrocytes were situated immediately beneath the surface. Why then did these observers make no mention of surface structure, or question the superficial smoothness of the surface first seen en face in the fresh preparation, or even draw attention to the undulations shown in their own drawings'? The explanation, surely, is twofold. First, 18th and early 19th century students of cartilage structure were preoccupied with the debates on 'Cartilage Vascularity', on the 'Role of Chondrocytes', and, later, with 'Mechanisms of Cartilage Injury' (Axhausen, 1923; Pommer, 1927). Second, the surface of articular cartilage appeared and felt so smooth, and served its articulating function so efficiently, that to question this smoothness would have seemed the height of foolish scepticism. Hence the persistence of the view, restated as recently as 1969 (Davies, 1969), that the surface of articular cartilage is 'strikingly smooth'. Only one early author (Hammar, 1894) may be said to have offered explicit opinions which conform with those described in the previous report (Gardner and McGillivray, 1970). Hammar wrote 'Die Gelenkflache ist niemals glatt, erbietet aber uibrigens ein sehr wechselendes Aussehen. Selten ist es ein und dasselbe auf der ganzen Flache desselben Knorpels'. He went on to say: 'It (the joint surface) is frequently covered with shallow depressions'. And '... . the free edge of the cartilage is rarely smooth on vertical section'. In the older literature it is not always easy