Effect of unilateral weight-bearing on pelvic limb development in broiler fowls: vascular studies

Research in Veterinary Science /988,44, /64-/74

Effect of unilateral weight-bearing on pelvic limb development in broiler fowls: vascular studies B. H. THORp·, S. R. I. DUFF, Institutefor Grassland and Animal Production, Poultry Division, Roslin, Midlothian EH259Pst Fifteen broiler fowls which habitually adopted a unilateral weight bearing stance were studied. In the majority of fowls the left pelvic limb was weight bearing and the right limb showed severe angular deformity. Dyschondroplasia occurred most frequently in the load-bearing limb. In the load-bearing limb the majority of lesions were in the femur and proximal tibiotarsus. In the non-load-bearing limb lesions most frequently occurred in the bone extremities of the distal tibiotarsus and proximal tarsometatarsus. Occluded epiphyseal vascular canals occurred in conjunction with physeal thickening at some dyschondroplastic sites. The majority of dyschondroplastic lesions contained elongated penetrating epiphyseal vessels and vessels derived from the perichondrial ring. These vessels were associated with chondrocyte hypertrophy and matrix calcification, which was considered to lead to the repair of the lesions. There was minimal calcification of cartilage at the base of the dyschondroplastic lesions and the underlying metaphyseal vessels were blunt ending. This suggested that a band of abnormal physeal cartilage was acting as a barrier to penetration by the metaphyseal vessels and so preventing subsequent endochondral ossification. INCREASED functional loading has been associated with a greater incidence and severity of dyschondroplasia in a number of mammalian species (Walker et al 1966, Paatsama et al 1972, Grondalen and Grondalen 1974, Duff 1986a). Similarly, in broiler fowls, Duff (1986d) recorded a higher incidence of dyschondroplasia in the weight-bearing limb of birds which adopted a unilateral weight-bearing stance. Riddell (1975), however, investigated the effect of overloading on dyschondroplasia in the fowl by sectioning gastrocnemius and flexor tendons, and changes were less severe in the overloaded limb. Dyschondroplastic lesions in the bone extremities of broiler fowls have been associated with changes in ·Present address: Veterinary Preclinical Centre, Cnr Flemington Road and Park Drive, Parkville, Victoria, Australia 3052 tFormerly part of the Agricultural and Food Research Council's Poultry Research Centre

vascular morphology (Thorp 1988). The purpose of this study was to investigate the vasculature associated with the development and repair of physeallesions in the limbs of unilateral weight-bearing fowls. Materials and methods A total of 15 broiler type fowls were studied. All habitually adopted a unilateral weight-bearing stance with the contralateral limb held free of the ground. Unilateral weight-bearing was of unknown duration. The broiler fowls were all skeletally immature, had been reared on deep litter and fed standard starter and grower diets. The broilers were examined and then injected intravenously with heparin. All birds were then killed by intravenous barbiturate overdose and perfused with a mixture of 17' 5 per cent barium sulphate powder, 3' 5 per cent sodium citrate and 2 per cent Berlin blue in a solution of 10 per cent buffered neutral formalin, The bone extremities from the pelvic limbs were processed and cleared in resin, using the technique described by Thorp et al (1986). The resin blocks containing the bone extremities were cut into 1 mm slabs and examined using a binocular microscope. Fifty slabs were re-embedded in resin and sections were cut with a microtome for subsequent histological examination (Thorp et al 1986). Results Abnormalities, which were all considered to be forms of dyschondroplasia, were observed in approximately 40 per cent of bone extremities examined. The distribution of such abnormalities varied between limbs (Fig I). In the weight-bearing limb lesions most frequently occurred in the femur and proximal tibiotarsus. In the non-weight-bearing limb the distal tibiotarsus and proximal tarsometatarsus most commonly showed abnormalities.

Proximal femur (weight-bearing) There were lesions in eight extremities. In four of the specimens there was thickening of the 164

Limb development in jowl

10

1m

Weight-bearing limb

o

Non-weight-bearing

8 en C

0

'iii

.!!!

'0 Q;

6

.0

E :J

Z

4

2

o

PF

~i ~!:; ji:.!,':; I

DF

PT

Bone extremity

DT

PM

FIG 1: Histogram demonstrating the number of lesions occurring in each long bone extremity of birds with a unilateral weight-bearing stance. The weight and non-weight-bearing limbs are considered separately. DF Distal femur, DT Distal tibiotarsus, PF Proximal femur, PM Proximal tarsornetatarsus, PT Proximal tibiotarsus .

165

physis in the craniomedial femoral head, associated with uneven and irregular metaphyseal vessels (Mvs), and a local absence of epiphyseal vascular canals (EVCs) and penetrating epiphyseal vessels (PEvs) (Fig 2). Histological sections demonstrated occluded EVCs in the craniomedial femoral head (Fig 3). In three proximal femurs there were dyschondroplastic lesions of the mid-femoral head with thickening of the physeal cartilage due to an increase in the number of prehypertrophied chondrocytes, In these three lesions PEvs were present in the physeal cartilage, and in one the PEvs were elongated, extending into the cartilage mass. In one specimen there was extensive disruption of endochondrial ossification. The medial physis was thickened and the MEvs were uneven, irregular and blunt ending. Throughout the femoral head there was an absence of svcs and PEVs. Histological sections demonstrated occluded cartilage canals. The metaphysis contained a large mass of cartilage. Some eves, from the caudal perichondrial ring, formed elongated PEvs which crossed the physis into the mass of cartilage. One of these elongated PEvs divided extensively in the cartilage mass. The cartilage around the transphyseal PEVs was hypertrophied and the matrix calcified. There were clefts in the craniomedial physes of two femoral heads. Stained sections demonstrated that the clefts contained amorphous material and cellular debris (Fig 4). In a specimen, with severe dyschondro-

... . FIG 2: The femoral head from the weight bearing limb of a unilaterally weight-bearing fowl. EVCs and PEVs are not present in the craniomedial femoral head. A group (arrowed) of EVCs originating from vessels in the Teres ligament branch frequently at the periphery of the avascular cartilage. 1 mm slab x 10

166

B. H. Thorp, S. R. I. Duff

FIG 3: This section is prepared from the slab in Fig 2. There are occluded EVCs (arrowed) in the cartilaginous epiphysis. E Epiphyseal hyaline cartilage, P Physis. Masson Goldner trichrome x 14·5

piasia of the proximal femur, the PEVs in the centre of the physis were elongated and extended into the avascular cartilage where they branched (Fig 5).

Proximal femur tnon-weight-bearingy There were lesions in four extremities.

FIG4: A section from the femoral head of a five-week-old unilaterally weight-bearing fowl. A cleft (arrowed) in the physis contains amorphous material and cellular debris. E Epiphyseal hyaline cartilage, P Physis. Masson Goldner trichrome x 14·5

In three extremities there was thickening of the craniomedial physis. The craniomedial femoral head was poorly perfused by Eves and histological sections demonstrated the presence of occluded vessels, and an accumulation of prehypertrophied chondrocytes. At the periphery of the avascular cartilage there was extensive branching of Eves from the capital femoral

E

M'

\ FIG 5: The proximal femur from a five-week-old unilaterally weight-bearing fowl. The entire metaphysis is occupied by cartilage. Elongated PEVs (arrowed) extend into and divide in the cartilage. E Epiphyseal hyaline cartilage, P Physis, M Metaphysis. 1 mm slab x 12

Limb development in fowl

167

FIG 6: Distal femur from a four-week-old unilaterally weight-bearing fowl. EVCs and PEVs, which would be supplied by tCRVs, are absent in the medial condyle. 1 mm slab x 10

ligament. In the fourth extremity the lesion was in the centre of the femoral head where the physeal cartilage was thickened and PEVs elongated.

degenerating erythrocytes. The MVs adjacent to the thickened physis were widened and blunt ending. The metaphysis of one distal femur was occupied

Distal femur (weight-bearing) There were lesions in seven extremities. In one specimen there was a large dyschondroplastic mass which occupied most of the metaphysis. In the other specimens the lesions were localised, usually peripheral, thickenings of physeal cartilage. Lesions which occurred in the medial aspect of the distal femur of four specimens were all similar (Fig 6). The medial metaphyses were flattened in profile and physes were thickened due to increased thickness of the prehypertrophic zone of chondrocytes. EVCs originating from the medial intracapsular retinacular vessels (ICRVs) were few or absent. MVs underlying the thickened physes were widened and blunt ending. There was an increase in the width of the metaphysis, caused by medial bulging where MVs appeared to be extending around the thickened physeal cartilage. Histological sections from the medial extremities contained scars of occluded PEVs and EVCs (Fig 7). In the cartilage matrix directly adjacent to the occluded vessels there was chondrocyte death. In two specimens there were lesions in the lateral periphery ofthe physis which were similar to those occurring medially. One distal femur had extensive clefts in the physeal cartilage parallel with and close to the cartilaginous epiphysis. The clefts contained

FIG 7: A section prepared from the slab in Fig 6. There is physeal thickening due to an increase in the number of prehypertrophied chondrocytes. Above the area of physeal thickening there are occluded EVCs (arrowed). In the physis there is an occluded PEV. E Epiphyseal hyaline cartilage, P Physis. Masson Goldner trichrome

x25

B. H. Thorp, S. R. I. Duff

168

I

1'1."(;2J;~ 't'· -{' Ifi··· .... ".~ .. , J~

,.

.

"
4'

M

•

i 'I;;

,;

.

~:! ':l.'~·

;~.~

'.~~~~

.'.'\..~;' ;

FIG 8: Distal femur from a four-week-old unilaterally weight-bearing fowl. A large mass of avascular cartilage occupies the metaphysis. PEVs are absent, normal or elongated. There are MV-like vessels (arrowed) derived from the perichondrial ring. E Epiphyseal hyaline cartilage, M Metaphysis, P Physis. 1 mm slab x 9·5

and an accumulation of prehyperytrophied chondrocytes . The bird with an extensive dyschondroplastic defect in the metaphysis of the distal femur of the weight-bearing limb had a similar lesion in the nonweight-bearing limb.

Proximal tibiotarsus (weight-bearing) by a large mass of cartilage which contained a few elongated PEVs. Mv-type vessels derived from the perichondrial ring penetrated the cartilaginous mass (Fig 8). Both the perichondrial derived MVs and the elongated PEVs were associated with localised chondrocyte hypertrophy and matrix calcification. There was a complete absence of chondrocyte hypertrophy and matrix calcification around the 'normal' sized PEVs of the condyles. The MVs adjacent to the thickened physeal cartilage were grossly enlarged, blunt ending and not associated with chondrocyte hypertrophy (Fig 9).

Distal femur (non-weight-bearing) There were lesions in five extremities. The lesions were similar to those noted above, but there were no physeal clefts in the femurs of nonweight-bearing limbs. In three specimens, thickening of the medial physis occurred in association with occluded EVCs and PEVs which originated from the medial ICRVs. In the lateral physis of one specimen there were few irregular MVs beneath a thickened physis, occluded EVCs and PEVs

There were lesions in nine extremities. In six specimens there was thickening of the lateral physis adjacent to the fibula. The MVs were enlarged, blunt ending and the metaphysis bulged laterally adjacent to the thickened physeal cartilage. In five of these specimens PEVs were present in the thickened physeal cartilage and were eitfier elongated or of normal length. The lateral physis and cartilaginous epiphysis of the sixth proximal tibiotarsus was poorly perfused and histological sections demonstrated vascular occlusion of PEVs and EVCs. In one proximal tibiotarsus, a lesion was noted in the physis below the epiphyseal ossification centre (EOC). The EVCs and PEVs below the EOC were occluded and the physis was slightly thickened. MV arrays below the physis were uneven and there was disruption of endochondral ossification in the adjacent periphery of the EOe. The physis below the EOC, contained small clefts which also traversed occluded PEVs. Adjacent EVCs branched extensively at the periphery of the avascular cartilage. In three proximal tibiotarsi the entire physis/ metaphysis was abnormal. There was a generalised increase in physeal thickness due to an accumulation

Limb development in fowl

169

large mass of degenerating prehypertrophied chondrocytes which occupied the centre of the metaphysis (Fig 10). Elongated PEYs, some of which branched, extended into the cartilage mass. Around these extensive PEYs chondrocyte hypertrophy and matrix calcification occurred (Fig 11). Mv-type vessels, emanating from the perichondrial ring, radiated into the periphery of the thickened physeal cartilage. These MVs were also associated with chondrocyte hypertrophy and matrix calcification (Fig 12). Grossly enlarged, blunt ending MVs were observed at the base of the thickened physeal cartilage. The margin between these MYs and the cartilage assumed a scalloped appearance and there was no chondrocyte hypertrophy or matrix calcification.

Proximal tibiotarsus (non-weight-bearing) FIG 10: The proximal tibiotarsus from a four-week-old unilaterally weight-bearing fowl. A large mass of cartilage occupies the metaphysis. Elongated PEVs (arrowed) extend into the centre of the mass. At the periphery of the mass perichondrial ring derived vessels take on the appearance of MV. (*). 1 mm slab x 3·5

There were lesions in three extremities. The two birds with large dyschondroplastic masses

of prehypertrophied and hypertrophied chondrocytes. The MYs were widely spaced and of increased diameter. Two of these bone extremities contained a

to.,

- .Y ','('1 '~

, ~l

FIG 11: A section prepared from the slab in Fig 10. There is chondrocyte hypertrophy and matrix calcification adjacent to the elongated PEVs (arrowed). von Kossa x 17·5

.

'W

FIG 12: A section prepared from the slab in Fig 10. There is chondrocyte hypertrophy and matrix calcification adjacent to the perichondrial ring derived MV s, von Kossa x 22

170

B. H. Thorp, S. R. I. Duff

in the weight-bearing proximal tibiotarsi had similar gross lesions at the same site in the non-weightbearing limb. In one of these specimens, an enlarged PEV adjacent to the physeal defect anastomosed with the metaphyseal circulation. In the remaining bird there was thickening of the medial physis associated with accumulation of prehypertrophied chondrocytes and thickened irregular, blunt ending MVs. The PEVs appeared normal. Distal tibiotarsus (weight-bearing) There were lesions in four extremities. Three lesions occurred in the lateral physis and one medially. Two of the lateral lesions wesre small, due to an accumulation of prehypertrophied chondrocytes adjacent to blunt ending MVs. In the third there was an extensive mass of thickened physeal cartilage across the width of the physis, but the PEVs appeared normal. Mv-type vessels derived from the perichondrial ring extended into the periphery of the mass of prehypertrophied cartilage. These Mv-type vessels were distinct and separate from the MVs at the base of the lesion. The MVs at the base of the cartilage mass were enlarged, blunt ended and did not penetrate the cartilage mass. The medial lesion was a narrow physeal cleft, perpendicular to the direction of growth. The cleft contained haemorrhage and traversed the prehypertrophied chondrocytes.

FIG 14: A section prepared from the slab in Fig 13. The cleft contains blue dye, haemorrhage and cellular debris. Masson Goldner trichrome x 22

Distal tibiotarsus (non-weight-bearing) There were lesions in nine extremities. The lateral condyle of five specimens contained areas of physeal thickening in association with a lateral bulging in the external contour of the bone extremity. The MVs were reduced in number and irregular. PEVs were present in all physes and were frequently elongated. In two distal tibiotarsi with lateral physeal lesions there were large physeal clefts (Fig 13), which were perpendicular to the direction of growth and contained haemorrhage and cellular debris (Fig 14). Two specimens had medial lesiops, where there was a peripheral thickening of the physis and an absence of PEVs and Eves. One distal tibiotarsus had a large dyschondroplastic defect occupying the metaphysis. There were blunt ending MVs at the base of the lesion. Elongated PEVs with lateral branches extending into the cartilage mass were associated with chondrocyte hypertrophy and matrix calcification. The physis also contained many PEVs of normal length. There was no chondrocyte hypertrophy associated with 'normal' PEVs. MVs derived from the perichondrial ring were associated with chondrocyte hypertrophy and matrix calcification. Proximal tarsometatarsus (weight-bearing)

FIG 13: The distal tibiotarsus from a four-week-old unilaterally weight-bearing fowl. There is a cleft containing blue dye (arrowed) in the physeal cartilage. 1 mm slab x 18

There were lesions in four bone extremities. In two specimens the lateral physis was thickened and contained elongated PEVs. In one bone extremity

Limb development in fowl

171

cytes. Although the majority of PEVs were of normal length, some were elongated and descended into the cartilage mass. Elongated PEVs were associated with focal chondrocyte hypertrophy and matrix calcification. MVs derived from the perichondrial ring and metaphysis penetrated the periphery of the cartilage mass. In one specimen there was a large dyschondroplastic mass of cartilage in the lateral metaphysis. In the cartilaginous epiphyses of one specimen there was an accessory ossification centre deep to the point of attachment of the medial collateral ligament (Fig 16). The accessory EOC was not associated with or a continuation of the 'normal' EOC in the centre of the cartilaginous epiphysis. The periphery of the accessory EOC was undergoing endochondral ossification. ICRVs were a source of vessels to the accessory EOC. There were clefts in the cartilaginous epiphysis adjacent to and contiguous with the accessory EOC. The clefts contained haemorrhage and cellular debris. Discussion FIG 15: The proximal tarsometatarsus from a six-week-old unilaterally weight-bearing fowl. The metaphyses of the lind and IVth metatarsi are occupied by avascular cartilage. The majority of PEVs are normal in length, although some are elongated. MV type vessels larrowedl are extending into the cartilage mass from the perichondrial ring. 1 mm slab x 6

In the majority of fowls in the present study, the left limb was weight-bearing with the contralateral limb showing severe angular deformity. This report complements earlier reports on unilateral weightbearing fowls (Duff 1986d) and gives credence to the

there were symmetrical dyschondroplastic defects in the medial and lateral metaphyses (Fig 15). The majority of PEVs were of normal length although at the periphery some PEVs were elongated. Distally, MVs which penetrated the cartilage mass were grossly enlarged.

Proximal tarsometatarsus (non-weight-bearing) There were lesions in seven bone extremities. Lateral displacement of the gastrocnemius tendon had occurred in four birds, and in three of these the medial cartilaginous epiphysis and articular surface was grossly misshapen. The periphery of the medial physis was thickened and contained elongated PEVs. In two of the birds, without lateral displacement of the gastrocnemius tendon, similar physeal lesions were noted medially. Medial displacement of the gastrocnemius tendon had occurred in one intertarsal joint. Haemarthrosis of the joint was noted and resin slabs revealed a cleft containing haemorrhage which extended through the physeal cartilage perpendicular to the direction of growth. The three metaphyses of one proximal tarsometatarsus contained masses of degenerating chondro-

FIG 16: The proximal tarsometatarsus from a six-weak-old fowl. There is an accessory ossification centre (ADC) in the cartilaginous epiphysis (E), deep to the point of attachment of the medial collateral ligament. Clefts (arrowed) are present adjacent to the ADC. P Physis. Masson Goldner trichrome x 9

172

B. H. Thorp, S. R. I. Duff

concept that limb dominance may occur in the fowl (Duff and Thorp 1985a,b). Pressure applied to rabbit physes caused thickening due to an accumulation of prehypertrophied chondrocytes (Trueta and Trias 1961). The pressure was considered to cause interference to the metaphyseal blood supply. When a plastic insert was placed in the physeal/metaphyseal junction of the growing fowl, there was failure of MV penetration and physeal thickening occurred due to an accumulation of 'dyschondroplastic' type cartilage. This suggested that dyschondroplasia was due to failure of MV penetration of physeal cartilage (Riddell 1975). Fowls with a unilateral weight-bearing stance have a greater frequency of lesions in the load-bearing limb (Duff 1986d). In studies of fowls with asymmetrical loadbearing, caused by angular limb deformities, dyschondroplasia occurs most frequently in the overloaded limb (Duff 1984a, Duff and Thorp 1985b). In the pig, rapid growth in conjunction with overloading leads to extensive 'osteochondritis' -like changes (Paatsama et al 1975). The growing broiler is susceptible to dyschondroplasia and a unilateral weightbearing stance would be expected to result in more extensive lesions than in slower growing fowls. Indeed overloading had apparently increased the extent and incidence of dyschondroplasia in these susceptible fowls. Disturbance of normal growth in one physis may lead to abnormal stress in another, resulting in more deformity (Reiland et al 1978). In the present study the majority of lesions in the non-load-bearing limb were in bone extremities of the intertarsal joint. Dyschondroplasia in one of these bone extremities may have contributed through abnormal joint loading, to dyschondroplasia in the other. The development of dyschondroplasia in the proximal tarsometatarsus and distal tibiotarsus may have been responsible for the development of abnormal bone angulation and torsion, initially causing abnormal joint loading and culminating in displacement of the gastrocnemius tendon. This would have resulted in greater joint deformity and would also explain the high incidence of dyschondroplastic lesions in these two bone extremities. The present study augments earlier reports of physeal clefts in the fowl (Riddell et a11983, Duff and Randall 1986) which are considered to be a consequence of repeated minor trauma. Clefts have also been reported in physeal cartilage of fowls with windswept deformities (Duff 1986b). These clefts are probably the result of abnormal stresses induced in physeal cartilage by abnormal limb angulation and altered functional torque. The histological appearance of physeal clefts in the present study was similar to the earlier reports in the fowl. The clefts were site specific in each bone extremity suggesting a localised

susceptibility. In the present study the predilection site for physeal clefts was in the femur and proximal tibiotarsus of the overloaded limb. These clefts were probably the result of increased functional load bearing. In the contralateral limb there were clefts in the physes of distal tibiotarsi and proximal tarsometatarsi. These clefts probably developed in response to altered stresses induced by abnormal intertarsal angulation of that limb. One proximal tibiotarsus contained a lesion which bore a similarity to Osgood Schlatter's disease in man (Osgood 1903, La Zerte and Rudd 1958). There was vascular disruption and a physeal cleft which was associated with local disruption of endochondrial ossification. In man, Osgood Schlatter's disease is considered to be due to excessive functional stress at the site of attachment of the patellar ligament (Ehrenborg and Engfeldt 1961, Ehrenborg et aI1961). No references have been found in the literature to an accessory ossification centre in the lateral aspect of the cartilaginous epiphysis of the proximal tarsometatarsus in fowls. The accessory EOC is deep to the site of attachment of the lateral collateral ligament and as such would be subject to traction forces. Duff (I 986c) described radiodense foci in distal tibiotarsi of fowls, at the point of attachment of the lateral collateral ligament. The foci contained woven bone and a traumatic aetiology was suggested. In man endochondrial ossification has been found to occur in response to trauma at the tendinous insertions of muscles (Hirsch and Morgan 1939). In the present study a traumatic aetiology is suspected causing modification to the local environment and inducing osteogenesis. This suggestion is supported by the presence of traumatic clefts. In the present study occlusion of EVCs in the craniomedial femoral head was frequently seen. There appeared to be revascularisation of the avascular regions in the femoral head by ·'iVCs dividing and branching as they descended from the capital femoral ligament. The EVCs then formed PEVs which reestablished cell hypertrophy and some of them extended into the thickened physeal cartilage occupying the metaphysis. Similarly in a report by Duff (l984a) there was thickening of the physeal cartilage in some examples of PEV!EVC occlusion. EVCs from the capital femoral ligament have been reported as forming an EOC in the fowl as part of the repair process in dyschondroplasia of the femoral head (Duff 1984b). In the present study other examples have been described where there appeared to be revascularisation of avascular cartilage. Lowther et al (1974) suggested that the avascularity of dyschondroplastic lesions resulted in impairment of the degradation and biosynthesis of cartilage proteoglycans, which are thought to play an important role in the mineralisation of cartilage

Limb development in jowl matrix (Bernard et aI1977). Impaired matrix synthesis by prehypertrophic chondrocytes has been associated with tibial dyschondroplasia in the fowl (Hargest et al 1985). Any defect in the cartilage proteoglycans may prevent mineralisation of the matrix. It seems reasonable to postulate that the formation of a narrow band of matrix which is not readily calcified would provide an effective barrier to MY penetration. More rapid growth rates would result in a thicker barrier of abnormal cartilage. In the present study the dyschondroplastic lesions were all similar demonstrating an accumulation of prehypertrophied chondrocytes and a failure of matrix calcification. Vessels failed to penetrate the abnormal mass of cartilage, and the PEYs were blunt ending and tortuous. The retained cartilage underwent regressive changes. A band of abnormal cartilage by preventing MY penetration would block the calcification of normal matrix produced subsequently. This would result in a mass of thickened physeal cartilage at the base of which there was failure of MY penetration. The repair of dyschondroplastic lesions appeared to involve two processes. These were: the re-establishment of endochondral ossification and the removal of abnormal physeal cartilage. The abnormal physeal cartilage that occupied the metaphyses was removed in association with enlarged MYs from the base of the lesion. A similar MY morphology was described in hypocalcaemic rickets, where there was a failure of MYs to penetrate thickened physeal cartilage (Lacey and Huffer 1982). Ultrastructural studies in the chick embryo provide evidence for a suggested mechanism of resorption in the cartilage models of long bones by My-type vessels (Silvestrini et al 1979). There was no calcification of matrix before MY invasion. The cartilage proteoglycans were digested by enzymes, which were produced by cells in the MVs. These cells subsequently matured into macrophages to remove the rest of the matrix (Silvestrini et al 1979). In the present study the large mushrooming MYs which slowly eroded the base of the retained cartilage bore a lot of similarities to the description of cartilage resorption in the chick embryo. The impression in the present study was that the layer of cartilage at the base of dyschondroplastic lesions was innately resistant to MY invasion. There was minimal calcification of the matrix and little or no hypertrophy of chondrocytes. In the majority of dyschondroplastic physes attempts were being made to re-establish endochondral ossification in the retained cartilage above this barrier. Three vascular sources penetrated the physeal cartilage to re-establish chondrocyte hypertrophy and matrix calcification: elongated PEYs; MY type vessels derived from the perichondrial ring; and MYs that had circumvented the periphery of the retained cartilage. The ability of some vessels to

173

penetrate this cartilage re-establishing its maturation testifies to its normality. It was also apparent that in a disease state transphyseal PEYs are associated with the calcification of cartilage. In the pig PEYs have been described as functioning in the repair of physeal osteochondrosis, and they can re-establish centres of ossification in abnormally thickened physeal cartilage (Kincaid and Lidvall 1982). The connective tissue of the PEYs is considered to be a source of osteogenic cells (Lutfi 1970, Hunt et a11979). A similar function could be ascribed to MY and perichondrial ring derived vessels in the present study. The introduction of osteogenic cells into cartilage at sites of chondrocyte hypertrophy and matrix calcification would enable the physis to return to normal function above the dyschondroplastic lesion. Acknowledgements The Animal and Grassland Research Institute is financed through the Agricultural and Food Research Council. This work is part of a commission from the Ministry of Agriculture, Fisheries and Food. B.H.T. is in receipt of an AFRC studentship. References BERNARD. B.. STAGNI. N.. COLOUTTI. 1.. YITTUR. F. & BONUCCI. E. (1977) Clinical Orthopaedics and Related Research 126, 285-291

DUFF, S. R. 1. (l984a) Research in Veterinary Science 37. 293-302 DUFF, S. R. 1. (1984b) Research in Veterinary Science 37,303-309 DUFF, S. R. 1. (1986a) Journal of Comparative Pathology 96, 3-13

DUFF. S. R.

1. (l986b) Journal of Comparative Pathology 96.

DUFF. S. R.

I. (l986c, Journal of Comparative Pathology 96,

142-148

159-169

DUFF, S. R. 1. (1986d) Research in Veterinary Science 40.393-405 DUFF. S. R. 1. & RANDALL. C. J. (1986) Research in Veterinary Science 40, 333-338

DUFF, S. R. 1. & THORP. B. H. (l985a) Research in Veterinary Science 39,307-312

DUFF. S. R. 1. & THORP. B. H. (1985b) Research in Veterinary Science 39.313-319 I. F. & LANCASTER,

DUTHIE.

76.263-273

M.

L. (1964) Veterinary Record

EHRENDORG, G. & ENGFELDT. B. (1961) Acta Chirurgia Scandinavica 121,491-499

EHRENBORG. G.. ENGFELDT, B.& OLSSON, S. E. (1961) Acta Chirurgia Scandinavica 122, 445-457

GRONDALEN. T. & GRONDALEN. J. Scandinavica 15, 53-60

(1974) Acta Veterinaria

HARGEST. T. E.. GRAY. C. Y. & LEACH. R.M.(1985) American Journal of Pathology 119, 119-209

HIRSCH. E. F. & MORGAN. R. H. (1939) Archives uf Surgery 39, 824-837 C. 0 .•

HUNT,

OLLERICH, D. A. & NIELSON, F. H.

Anatomical Record 194,143-158

(1979)

KINCAID, S. A. & L1DYALL, E. R. (1982) American Journal of Veterinary Research 43. 938-944

LACEY, D. L.

&

HUFFER.

Pathology 109. 288-301

W.

LA ZERTE, G. O. & RUDD,

1.

E. (1982) American Journal of H. (1958) American Journal of

174

B. H. Thorp, S. R. I. Duff

Pathology 34,803-81 5 LUTFI, A. M. (1970) Journal of Anatomy 109, 135-145 LOWTHE R, D. A., ROBINSON, H. c.. DOLMAN, J. W. & THOMAS , K. W. (1974) Journal of Nutrition 104,922-9 29 NACHLO V, I. W. & OLPP, S. L. (1945) Surgical Gynaecology and Obstetrics 81,206-2 12 OSGOOD , R. B. (1903) Boston Medical and Surgical Journal ex LVIII, 114-117 PAATSA MA, S., JUSSILA , J. & ALITALO , I. (1972) Proceedings 2nd International Pig Veterinary Society Congress, Hanover. p 123 PAATSAM A, S., ROKKANEN, P. & JUSSILA. J. (1975) Acta Orthopaedica Scandinavica 46, 906-918 REILAND , S., OLSSON, S. K., POULOS , P. W. & ELWING ER, K. (1978) Acta Radiologica Supplement 358, 277-298 RIDDELL , C. (1975) A vian Diseases 19, 483-489

RIDDELL , c.. KING, M. W. & GUNASE KERA, K. R. (1983) A vian Diseases 27, 980-991 SILVESTRINI, G., RICORD! , M. E. & BONUCCI, E. (1979) Cell and Tissue Research 196,221-2 35 THORP, B. H., LYNCH, M. & DUFF, S. R. I. (1986) Research in Veterinary Science 40, 236-240 THORP, B. H. (1988) Research in Veterinary Science 44, 112-124 TRUETA , J. & TRIAS, A. (1961) Journal of Bone and Joint Surgery 438, 800-814 WALKER, T., FELL, B. F., JONES, A. S., BOYNE, R. & ELLIOT, M. (1966) Veterinary Record 79,472-47 9

Received December 23, 1986 Accepte d March 30, 1987