Department of Anatomy, Glasgow University

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1 THE UPTAKE OF LABELLED SULPHATE INJECTED INTO THE HOST ANIMAL BY CARTILAGE HOMOGRAFTS By G. M. WYBURN, D.Sc., F.R.F.P.S.G., and P. BACSICH, D.Sc., M.D. Department of Anatomy, Glasgow University INTRODUCTION THERE is now ample experimental and clinical evidence that fresh cartilage homografts survive in mammals for long periods, e.g. : man, three years (Peer, 1954); rabbit, eighteen months (Craigrnyle, 1955); and dog, eighteen months (Young, 1945). Histologically the chondrocytes remain alive in cartilage homografts, although there is a temporary change in their metabolism indicated by a decrease in lipid and glycogen content of the cells within fourteen days (Craigmyle, 1955). The ground substance retains its metachromasia which is regarded as a reliable quantitative test for the presence of ester sulphate of high molecular weight such as chondroitin sulphate, a characteristic constituent of healthy viable cartilage matrix. The metabolism of cartilage, which means the activity of the chondrocytes, is concerned with the " turnover " of ground substance including chondroitin sulphate. Direct evidence of this metabolic activity can be obtained by the uptake of labelled sulphate (35SO4) by living cartilage (Davies and Young, 1954 ; Bostrom, 1952 ; Pelc and Glucksmann, 1955) which is organically bound in its chondroitin sulphate. The purpose of this work is to show that cartilaginous homografts can assimilate '~5SO4 injected into the host animal and thus confirm the established histological criteria of their continued viability. MATERIAL AND METHODS A graft of xiphoid cartilage was inserted subcutaneously into each of four adult guinea-pigs and similarly a graft of costal cartilage into each of four additional animals. Three weeks after the insertion of the graft the host animal was given a subcutaneous injection of 5 mc. of 35SO~ at ph 5. The animals were killed and the grafts recovered twenty-four hours after this injection. The grafts, together with control specimens of the xiphoid and costal cartilage of the host animal, were fixed for one hour in a mixture (3 to I) of absolute alcohol and acetic acid and subsequently for twenty-four hours in formol saline. After paraffin embedding, 5/z sections of controls and cartilage were cut. A number of sections from each block were prepared for autoradiography by the stripping film technique (Pelc, 1947), with an exposure of about forty-two days. After development, fixation and drying the autoradiographs were photographed. Other sections were stained with hmmalum and eosin or with a o. 5 per cent. aqueous solution of toluidine blue. DESCRIPTION There was a mild cellular reaction round the grafts showing lymphocytes and fibroblasts, but no evidence of invasion of the substance of the graft. 3 A 177

2 178 BRITISH JOURNAL OF PLASTIC SURGERY Costal Cartilage.--The appearance of a section of costal cartilage varies. Adjoining the bony rib there is normally a central area of degenerating calcifying cartilage which is not present if the section is from the sternal end of the costal cartilage (Fig. I). All four grafts were histologically normal with no evidence of cell death, and showed the characteristic metachromasia of the ground substance (Fig. 2). With sections of 5/z it is possible to make a reasonably reliable visual comparison of autoradiographs of grafts and controls. The autoradiographs of the grafts resemble very closely those of the controls both in quantity and distribution of granules, indicating that the metabolic behaviour of the grafts is essentially similar to that of normal living cartilage. At twenty-four hours the intensity of the autoradiographs in both graft and control is around the cartilage cells, and this pericellular concentration of granules maps out the characteristic distribution of chondrocytes in costal cartilage. There is a much lower granular intensity in the matrix itself (Figs. 3 and 4). Xiphoid Carfilage.--In the adult guinea-pig the xiphoid is an actively growing cartilage with ossification extending into it from the sternal end. Sections, therefore, show cartilage cells in different phases of maturity. For example (Fig. 5), in a section of the xiphoid from the host animal, the central cells are large and surrounded by opaque cellular substance giving a honeycomb appearance to this part of the cartilage. They correspond to Phases 3 and 4 of Streeter's classification. The ground substance in this region is more intensely metachromatic than at the periphery where smaller cartilage cells occur singly. This difference in cell type in the central and peripheral zones is preserved and, indeed, is more marked in sections of the grafts of xiphoid cartilage as in Fig. 6, which is altogether a more active-looking cartilage than the control. Again, the autoradiographs of control and transplant are very similar, and indeed that of the graft is if anything more intense--not perhaps surprising in view of the more active-looking stained preparations of the graft. In both graft and control the labelled sulphate is present as a concentration of granules in the centre of the section. This is in agreement with Dziewiatkowski's (I95I) results, who records the greatest intensity of ass around cell Types 3 and 4 surrounding secondary centres of ossification. In the control xiphoid (Fig. 7) this granular concentration is periceuular and outlines the cell groups, but this arrangement is less apparent in the graft autoradiographs where there is a relatively greater intensity of granules in the intervening matrix (Fig. 8). Cartilage grafts may certainly show necrotic patches, but these are isolated areas of dead cartilage surrounded by more extensive territories of healthy tissue populated by viable chondrocytes. The nutrition of the cartilage depends on tissue diffusion, and these necrotic areas probably result from nutritional defects conditioned by the particular circumstances of the graft, such as thickness, site of implantation, etc., rather than from the effects of an immune response. Histologically the necrotic areas show cell death, eosinophilia of ground substance, and no uptake of 35S. Fig. 9 is a section of graft showing both living and necrotic cartilage. There are, however, isolated nests of living cells within the necrotic areas. In the corresponding autoradiograph (Fig. io) there is no labelled sulphate in the necrotic areas except scattered granule clusters outlining the odd nest of living cells.

3 LABELLED SULPHATE INJECTED INTO HOST ANIMAL BY CARTILAGE HOMOGRAFTS I ~ section of control costal cartilage. FIG. I T h i s section is from the sternal end and shows no central degeneration, x I33. FIG. 2 5 ~ section of graft costal cartilage. T h i s section is f r o m the costal end of cartilage and s h o w s characteristic " degeneration "' in the centre, x i33.

4 180 BRITISH JOURNAL OF PLASTIC SURGERY FIG. 3 Autoradiograph o f 5 v section control costal cartilage. N o t e periceuular concentration o f granules. F o r description see text. x 920. FIG. 4 Autoradiograph of 5 ~ section o f graft costal cartilage. Note pericellular concentration o f granules. Compare with Fig

5 LABELLED SULPHATE INJECTED INTO HOST ANIMAL BY CARTILAGE HOMOGRAFTS IS It FIG. 5 5 v section of control xiphoid cartilage. Note difference in cell types. T h e large m a t u r e cartilage cells in the centre, smaller cells at periphery FIG. 6 5 ~ section of graft xiphoid cartilage. Note difference in cell type as in Fig

6 I82 BRITISH JOURNAL OF PLASTIC SURGERY FIG. 7 Autoradiograph of 5 ~ section control xiphoid cartilage. Note pericellular concentration of granules round central chondrocytes, x 315. FI~. 8 Autoradiograph of 5 ~ section graft xiphoid cartilage. Compare with Fig. 7. x 315.

7 I8 3 LABELLED SULPHATE INJECTED INTO HOST ANIMAL BY CARTILAGE HOMOGRAFTS FIG. 9 5 ~ section of graft xiphoid cartilage showing necrotic area. x 315.,+ I t/ FIG. i o Autoradiograph of 5 u section of graft xiphoid s h o w n in Fig. 9area Note absence of z:'s in necrotic

8 I8 4 BRITISH JOURNAL OF PLASTIC SURGERY DISCUSSION These results provide direct evidence that cartilage can survive as a homograft and confirm that the histological criteria of viability denote an actively metabolising tissue. Pelc and Glucksmann (1955), in a time-interval study of labelled sulphate, find that the 3sS is concentrated in the cartilage cells within two hours after injection. They conclude that the 35S is stored in the cartilage cells and used there in the formation of chondroitin sulphate for the renewal of matrix in static adult cartilage. Little is known of the details of the stages of intracellular formation of cartilage mucopolysaccharides. The similarity in the appearance of the control and graft autoradiographs justifies the conclusion that the graft has established normal nutritional relations with the host tissue and a " turnover " of ground substance parallel to that of the host cartilage. It is now generally recognised that chondroitin sulphate is the functionally significant and biologically specific constituent of cartilage (Sylvan, 1947 ; Bacsich and Wyburn, I947), and its continued formation is an important factor in the survival properties of this tissue as a homograft. Nothing is known concerning the life span of normal chondrocytes, whether they are renewed from time to time or last throughout the life of the cartilage, but it seems improbable that the graft chondrocytes could continue to synthesise a chondroitin sulphate antigenic to the host tissue. Thus in this respect it might be argued there is " replacement," but this is not by host tissue but by material elaborated by the native cells of the graft. The uptake of labelled sulphate is suppressed by cyanide poisoning or by heat (Laytor, et al., I95O). It is therefore an active cellular process and so, despite its avascularity, the relative intensity of cartilage autoradiographs indicates an active metabolism concerned with the breakdown and continuous new formation of chondroitin sulphate. This cycle presumably involves a depolymerisation of high-grade molecules and the possible diffusion of the degraded molecules into the host tissue. The mild non-invasive lymphocytosis--the characteristic host reaction of cartilage homografts--suggests, however, that these products of the cartilage metabolism do not act as antigens. It has been stated that it is the immunologically inert ground substance which confers survival value on cartilage homografts and that deprived of this protection the cartilage cells die. We have found, however (Bacsich and Wyburn, 1955), that growing cartilage with a high cell content and little ground substance not only survives but shows active cell proliferation and deposition of ground substance. This is interpreted to imply that it is the active production of the mucopolysaccharides by the cells which gives protection against or prevents host reaction rather than the quantitative characteristics of the tissue, although little is known concerning the chemical mechanism of this intracellular process. We are indebted to G. Popjak and S. R. Pelc of the Experimental Radiopathological Research Unit at Hammersmith Hospital for help and advice in the preparation of the autoradiographs. We have to acknowledge a contribution from the Misses Cruden Fund towards the expenses of the work, and a grant from the Medical Research Council for the purchase of radioactive sulphur.

9 LABELLED SULPHATE INJECTED INTO HOST ANIMAL BY CARTILAGE HOMOGRAFTS I8~ REFERENCES BACSICH, P., and WYBURN~ G. M. (1947). Proc. roy. Soc. Edinb., 62, 32I. -- (1955). Transpl. Bull., 2, 4. BOSTROM, H. (I952). J. Biol. Chem., x96, 477. CRAIGMYLE, M. L. (1955). Brit. J. plast. Surg., 8, 93. DAVIES, D. V., and YOUNG, L. (1954). J. Anat., 88, 174. DZIXWlATKOWSKI, D. D. (I95I). 7. exp. Med., 93, 5, 451- LAYTON, L. L., FRANKEL, D. R., and SCAPA, S. (I95O). Cancer, 3, 725. PEER, L. A. (1954). Transpl. Bull., I, 87. PELC, S. R. (1947)- Nature, Lond., x6o, 749. PELC, S. R., and GLUCXSMANN, A. (1955). (In press.) SYLVAN, B. (1947). J. Bone Jr. Surg., 29, 3. YOUNG (1945). Surgery, XT, 616.

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