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Experimental reconstruction of the mandibular joint
Int. J. Oral S,rg. 1974: 3:400-411 (Key words; cartilage; mandible, condyle; temporomandibular joint)
Experimental reconstruction of the mandibular joint DAVID POSWILLO
Royal College o] Surgeons o/ England, London, and Queen Victoria Hospital, East Grinstead, S,tssex, England
~U3STRACT-- It is proposed that the cartilage of the mandibular condyle is not the site of active growth but rather that of secondary adaptive and remodeling responses. Experiments were conducted in M. irtts monkeys replacing the surgically excised mandibular condyle with either a sliding ramus graft or a costochondral rib graft. After 2 years the characteristics of the grafts were examined. Both techniques produced acceptable functional condyles; when examined histologically, the condyle formed from the rib graft was shown to be closely comparable to the condyle on the unoperated side. The functional condyle formed by the sliding ramus graft lacked the histologic features of the normal condyle and showed less capacity for remodeling and adaptation. It is proposed that the histolog[c nature of the grafts used to restore the condyle could have a profound influence on subsequent growth and development. The costochondral graft is readily available, possesses the necessary mechanical properties, and has the capacity for remodeling into an adaptive mandibular condyle. These properties make it eminently suitable for use in reconstruction of the condyle in both the growth period and adult life; when placed correctly in the fossa, and facial height and symmetry are restored, the resultant condylar head adapts and responds to the demands of the functional matrix, thus permitting mandibular growth.
(Received Jor publication 23 Jzdy, accepted 26 Jzdy 1974)
F o r m a n y years it was believed that the m a n d i b l e could be regarded, for purposes of growth, as a long bone in disguise, albeit a " b e n t " Iong bone, and that the center of active growth was located in the condylar cartiIage~0. It is apparent now, from a recent review of the literature by DURKIN, HEALEY & IRVING~, that this classic concept can no longer be accepted without considerable
reservation. The response of the articular cartilages of both m a n d i b u l a r condyle and long bones to physiologic and pathologic changes has been shown to be similar, and quite distinct from the reaction in the u n i q u e epiphyseal growth plate cartilages. Study of the histology and the b i o c h e m ical behavior of the cartilage cells in both condylar and epiphyseal cartilages suggests
RECONSTRUCTION OF MANDIBULAR JOINT that these are the sites of adaptive and compensatory remodeling responses. They are not comparable with growth centers found in the growth plate cartilages. The histologic appearance of cartilage, in a specific location, appears to reflect the ultimate behavior of the site. For example in the growth plate, there are well-organized transverse cartilaginous bars, unmineralized, but penetrated by erosive capillaries. Calcification takes place only in the thick vertical compartments between the regular columns of cells. By contrast, in the mandibular condyle and articular epiphysis the cells are arranged in haphazard fashion, as distinct from vertical columns; calcification takes place in the pericellular space surrounding the cartilage cells. Thus one finds that in the growth plate, elongation takes place in a constant longitudinal fashion, parallel to the vertical columns. In the condyle and epiphysis growth is multidirectional, meeting the need to adapt the articular surfaces to constant changes in the intracapsular environment. As age progresses, and the need to adapt diminishes, so the capacity of the cartilage to remodel reduces accordingly. Although maturation of the cartilage in the condyle proceeds more slowly than in the epiphysis of a long bone, it follows a similar course. While slight histologie variations are observed, the process of maturation in the two sites is essentially the same. It involves the transformation of hypertrophic, or embryonic-type cartilage into a mature non-hypertrophic tissue in which the lower cartilage border is sealed off by subchondral bone. These distinctive histologic changes indicate that the mandibular condyle can no longer be thought of as a primary growth center, embodying normal endochondral bone formation, but rather as a modified epiphysis which, like that on the long bone, grows just enough to ensure proper modeling of the extremities 5. During early life both the mandibular and epiphy-
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seal cartilages are embryonic in character, having a capacity for rapid adaptive remodeling. The histologic appearance and behavior of the cartilage cells at that time further support the suggestion of embryonic or hypertrophic characteristics. In the formotive years of postnatal life the condylar cartilage must meet the demands of its changing environment; rapid dimensional changes occur in those temporal components of the joint comprising the glenoid fossa and articular eminence. These changes are met by the potential for flexibility and adaptation possessed by the mandibular cortdyle. As in the epiphysis, when the demand for adaptive remodeling ceases, the condylar cartilage reverts from the hypertrophic form to a resting, non-hypertrophic state. The function then becomes principally that of a protective articular veneer, with a capacity for replacement of lost or worn-out cells. This change from embryonal to mature form takes place slowly in the condyle by comparison with the epiphysis of a long bone. Growth of the craniofacjal complex is particularly active up to the age of 14 years. As age increases from 14 to 28 the changes in the eraniofacial region become less obvious, more subtle, and the demands on the compensatory mechanisms are reduced. During this period of diminishing need for adaptive remodeling the cartilage of the condyle is converted to adult articular form, the cartilage-bone interface consolidates and fnses, and adaptive changes cease. If, as appears likely, the mandibular condyle does not provide the dominant growth impetus to the mandible, what is it that enables the mandible to "lead the growth of the face"10? Moss~ has proposed that the relationship between muscles and the facial skeleton is such that a functional matrix is formed; the size, shape, position and maintenance of the mandible, therefore, are governed by the primary morphogenetic demands of specifically related mastieatory
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muscles and ligaments within the oro-faciaI capsule. If this hypothesis is valid, and there is c o n s i d e r a b l e evidence to support it, then it w o u l d appear I ogieal to approach the p r o b l e m of reconstruction of an absent or a n o m a l o u s condyle on the basis of this concept. T h a t being so, the priorities would a p p e a r to be early re-establishment of the m a n d i b u l a r ramal functional matrix with a c o n d y l a r cartilage capable of adaptive rem o d e l i n g responses rather than the provision of a graft embodying an "active growth center" e.g. a metatarsal. Attempts to maintain g r o w t h of the mandible by grafted femurs, f i b u l a r heads, and metatarsals have been m a r k e d by a conspicuous absence of growth; in many instances the growth plate was f o u n d to have disappeared, and only the articular surface of the transplant showed signs of cellular activity 2, 3,11,7, 12, 15, 16 Observations m a d e on the late effects of m a n d i b u l a r condylectomy support the contentiort that the m o r p h o l o g y and growth of the m a n d i b l e are governed by the functional matrix. Following condylectomy, in both m o n k e y a n d man, the mandible has been shown to "regenerate" a functional condylar head ta. Histologic examination of the regenerated condyle revealed an articular cap of cartilage, f e r m e d apparently by metaplasia of local fibroblasts, covering the articular s u r f a c e of the bone. The presence of an intact intra-articular meniscus promoted a smooth regular articular surface on the reconstituted condyle. This capacity of the m a n d i b l e for spontaneous regeneration of a functional condyle encouraged the speculation that satisfactory reconstruction of a d a m a g e d o r missing condyle could be achieved by the a d v a n c e m e n t of a strut of bone mobilized f r o m the posterior border of the r a m u s o f the mandible. Following the p l a c e m e n t o f such a sliding ramus graft in the a r t i c u l a r fossa it was anticipated that the a r t i c u l a r histology would rapidly grow to resemble that observed in the "regenerated"
condyle. It was hoped that the correction of ramal and condylar deformity and mandibular height could be simply, but precisely corrected by this procedure utilizing the reconstitution of an intact functional matrix; it usurped all the advantages of spontaneous regeneration, without the disadvantages of imprecision and unpredictability which accompanied spontaneous reformation of a functional condyle. The concept of reconstitution of the functional matrix with an appropriate bone graft capped with cartilage demanded consideration also of the alternative method of reconstruction of an absent or anomalous condyle, grafting of an autogenous costochondral strut. This technique had been used successfully in a limited number of clinical studiest4, ~7. In preliminary studies, WARE & TAVLoI~t8 found that both fibular heads and costochondral grafts could be employed to reconstruct condyles in children affected by early ankylosis. T h e y reported that the overall results with eostochondra[ struts were superior to those from fibular heads; posttreatment growth was sustained, and the costochondral grafts were easier to obtain and quicker to adapt. When interpreting these findings in the light of recent knowledge concerning the behavior of the cellular component of articular and other forms of cartilage, it appeared that the cartilaginous element of the costochondral strut may have made a major contribution to the success of these grafts. Studies were designed, therefore, to compare radiologically and histologically the efficacy of mandibular ramus slides and costoehondral strut grafts in replacement of the resected mandibular condyle.
Experimental method Eight young adult Maraca irus monkeys, all of which had undergone unilateral or bilateral cnndylectomy 3 years previously, were divided
RECONSTRUCTION OF M A N D I B U L A R JOINT
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fossa and immobilized.
intra-articular disc, and placed with the long axis lying latero-medially. The costochondral graft consisted o f 0.5 cm of cartilage attached to 3 cm of rib bone. A strip of periosteum was left intact to cover the costochondral junction to reinforce the fragile junction zone. Ramus and rib grafts were both fastened in position by stainless steel wires. The wound was irrigated, dusted with antibiotic powder and closed in layers without drainage. N o intermaxillary fixation was used; had this been done, regulations relating to free-feeding of experimental animals would have been contravened. After recovery f r o m anesthesia, all animals were returned to normal cage life, with a soft diet for 2 weeks. Antibiotic therapy with intramuscular Triplopen| was maintained every second day for 1 week. The animals in Group 2 were treated similarly, with the distinction that a sliding ramus graft was carried out on one side (right or left) and the rib graft on the opposite side. In both groups, radiographs of both sides of the jaw were taken at 3-month intervals from the time of operation until sacrifice of all animals after 24 months. At the time of operation, in all animals in Group 1 (where a unilateral condylectomy had been carried out) the coronoid process was considerably enlarged on the
into two groups. Group I consisted of six animals with prior unilateral condylectomy; three were right sided cases and three were left sided. Group 2 comprised two animals in which condylectomy had been performed bilaterally. Under gas-oxygen-halothane anesthesia in all animals in Group 1 either a sliding ramns graft (Fig. 1) obtained from the posterior border of the mandible of the same side or an autogenous costochondral graft obtained from the seventh rib was carried out (Fig. 2). Immediately prior to the grafting procedure the condylar stump which had regenerated following the previous condylectomy, was removed by the submandibular approach. The d o n o r site on the ramns of the mandible was roughened by decortication prior to insertion of the rib graft. T h e sides were reversed so that right or left sliding grafts and rib grafts were reasonably distributed among the six animals. Where the sliding ramus graft was used it was shaped at the superior end to present a rounded articular head making contact with a carefully preserved
Fig. 2. Costochondral rib graft attached to posterior border of the ramus, with cartilage end in the fossa.
Fig. I. Sliding ramus graft placed in glenoid
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operated side, in comparison with the tmoperated side. In the animals in Group 2 both coronoid processes were hypertrophied. Throughout the postoperative period regular observations were made of the occlusion of the teeth and function of the jaws. At sacrifice the heads of the animals were perfused with buffered formol saline, and the decapitated heads were then skinned, sectioned in the sagittal plane, radiographed and stored for 1 month in fixative. They were then demineralized in 4N formic acid, the temporomandibu[ar apparatus was dissected out en bloc, and prepared for section in the frontal plane to avoid damage to the microtome by fixation wires in the specimens.
Results The regular radiographs showed reasonable progressive osseous reconstitution of a mandibular condyle in all animals in both groups. At the time of sacrifice there had been n o obvious change in morphology for 6 months. N o appreciable change was observed in the coronoid processes throughout the whole postoperative period. N o r m a l occlusion of the teeth was maintained in all animals in Group 1. For the first 6 m o n t h s there was a mild degree of deviation of the jaw to the operated side on m a x i m u m opening. Prior to operation both animals in Group 2 displayed a moderate anterior open bite which had followed the original condylectomy. Because intermaxillary fixation could not bc applied, tMs open bite was not corrected during the grafting procedure. Consequently the occlusal p a t t e r n of these animals exhibited open bite, b u t no other changes, after the joint replacement procedure; full mouth opening and n o r m a l function were maintained postoperatively in these animals until sacrifice. Radiographic examination at sacrifice revealed the presence of adequate functional condyles following both sliding ramus grafts and costochondral struts (Figs. 3 A C). O n every side where a sliding ramus graft h a d been used the anteroposterior width of the mandibular ramus remained
substantially smaller than the opposite side, whether unoperated or subjected to rib grafting without removal of the posterior border of the ramus (Fig. 3 B). Microscopic examination of the control and experimental mandibular heads revealed significant differences. In the unoperated mandibular condyle the typical diarthrodial joint was observed. The articular surface of the glenoid fossa consisted of thin compact bone. Superficiai cover was provided by thin fibrous connective tissue with some interposed cartilage cells. The intra-articular meniscus was composed of connective tissue, thicker on the medial and lateral sides, and thinned above the articular surface of the condyle. The condylar head was covered by a perichondrium comprising fibrous connective tissue in the deeper layers of which were found fibroblasts, chondroblasts and chondrocytes. Beneath the fibrous covet" were layers of cartilage cells, irregularly distributed, but increasing slightly in size from superficial to deep. There was little evidence of islands of irregular cartilage or chondroclast activity at the cartilage-bone interface. Beneath the cartilage cells were regular osseous trabeculae meeting in a linear fashion with the cartilage layer across the whole interface. There was scant evidence of active endochondral ossification. The articular apparatus was enclosed in an intact synovial membrane of thin connective tissue containing capillary vessels (Fig. 4 A, B). In the condylar heads derived from costochondral grafts there was a consistency of histologic appearance throughout the series, in both Group 1 and Group 2 animals. The condylar heads were smaller in all dimensions than the unoperated controls, but the temporomandibular apparatus which followed reconstruction with rib grafts was a typical diarthrodial joint enclosed in a normal synovial membrane. T h e temporal surface a n d intra-articular disc were closely comparable with the control specimens. The
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Fig,. 3. A, radiograph of mandibular condyle in experimental animal on the unoperated side. B, radiograph of functional condyle formed 2 years after sliding ranms graft. C, radiograph of functional condyle formed 2 years after costochondral graft.
disc was thinner in the central portion, and less cellular. The articular surface of the condyle was covered with a perichondrium identical to that on the unoperated sides. Beneath this was a typical cartilaginous cap rather thicker than normal, with tongues of cartilage penetrating the osseous trabeculae right across the interface. Islands of 9 cartilage ceils were seen in the center of the bony supports, and osteoblastic and osteoelastic activity were seen both in active (cel-
lular) progress and in multiple reversal lines across the cartilage-bone junction. With the exception of a mosaic of reversal lines the osseous trabeeulae were comparable with their unoperated counterparts (Fig. 5 A, B). There was less uniformity of histologic morphology in those cases in which joint reconstruction had been achieved by sliding ramus grafts. Generally, while the temporal surface was normal, the meniscus was irregular, with loose fibrous tissue adhesions
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Fig. 4. A, coronal section of the condylar head, meniscus, and fossa on unoperated side showing normal configuration of ioint components. B, higher power illustration of unopgrated condylar head showing cellular characteristics o~ the fibrocartilage of the condyle, and regular cartilage-bone interface.
observed between the articular surface of the condylar head a n d the disc. While the diarthrodiaI design existed, enclosed in a synovial apparatus, the boundaries were illdefined and the division into upper and lower j o i n t spaces was at times difficult to make in examination of serial sections. The form of the condylar heads was much less typical than in the rib graft series. The articular surfaces had frequent irregularities,
filled with fibrous tissue adherent to the meniscus. The head of the condyle consisted of a layer of compact bone, with many reversal lines, covered by dense parallel layers of fibrous tissue, rich in fibroblasts. In the deeper layers a few chondroblasts and chondrocytes were observed; there was no complete veneer of cartilage present as yet, and no evidence of endochondral ossification (Fig. 6 A,B).
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Fig. 5. A, coronal section of condylar head reconstituted from costochondral graft in animal shown in 4a. The head and disc are both smaller, but the appearance is consistent with a normal temporomandibular apparatus. B, higher power view of condylar head formed from rib graft, showing remodeling activity of cartilage and bone in the articular head.
Discussion Although considerable evidence is available to demonstrate the inherent growth forces of "growth plate" cartilage, the replacement of the mandibular condyle by a "growing" bone such as a metatarsal has met with little or no success. The architectural arrangement of the condylar cartilage is quite unlike that found in "growth plates", and its role in
overall growth of the mandible remains u n certain. Examination of excised condylar heads in cases of hyperplasla of the m a n dible reveals greatly thickened cartilage zones1; following condylar shave, the growth of the mandible reverts to normal. It appears possible therefore that when active growth, in contrast to adaptive remodeling, takes place in the condylar head, hyperplasia results. Thus, when the condylar head
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Fig. 6..4, coronal section of functional condyle formed from sliding ramus graft. B, higher power section of ramus-graft condyle showing fibrous adhesion between articular surface and meniscus, absence of obvious cartilaginous zone, and compact bone adjacent to the fibrous articular cover.
is replaced by a metatarsal in the expectation that growth will continue, several false assumptions may be made. Firstly, it could be assumed that the condylar head is normally a major growth center, and that a metatarsal graft would replace it. This is illogical, even if the mandibular condyle was a growth center, because the growth
plate of the metatarsal is not located in the epiphyseal articular cartilage. McKIBI3IN & I"IOLDSWORTH8,9 made this distinction when they pointed out that the articular and growth plate cartilages, on the basis of both embrylogic derivation and ultrastructure, are fundamentally different. Secondly, even if it were assumed that the condylar head was
RECONSTRUCTION OF MANDIBULAR JOINT not a site of major growth, but rather one of adaptive and compensatory modeling, its replacement by the non-hypertrophic articular cartilage of the metatarsal could not promote the necessary modifications in the condyle demanded by rapid compensatory changes in the environment. It is hardly surprising, therefore, that the result of metatarsal grafts was disappearance of the growth plate, with little to suggest the original character of the transplant. Only the character of the articular cartilage remained2, ts, a predictable result if one accepts that the true nature of the mandibular condyle was never that of a growth plate cartilage, and therefore not a primary growth center. All attempts to change it from a center of remodeling to a center of growth would thus be destined at the best to be a static situation, or at the worst to hyperplasia. This potential for hyperplasia was observed in one animal following metatarsal graft by WARE ~.~ TAYLOR 18, but the full significance of the observation was not appreciated. Where the (only) metatarsal graft was seen to grow actively at the growth plate, "it appeared both clinically and radiographically that the transplant grew more than the normal condyle". The success or failure of an approach to reconstruction of the mandibular joint may be more closely related to the adaptive capacity of the articular cartilage and the reconstitution of the functional periosteal matrix than the transplantation of a "growth center". The capacity os tke embryonic-type hypertrophic cartilage of the costochondral graft to adapt and remodel to a histologically perfect condyle within 2 years, in young adult monkeys, is a significant finding in this experiment. Growth studies were not performed, and in fact would have yielded no significant information in animals in which most craniofacial growth had ceased. Nonetheless, the reconstitution, following rib grafting, of a functional condyle capable of
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adaptive responses is an important finding. If both facial height and the compensatory adjustment mechanism are shown to be restored by careful selection of transplantation tissues, then results should be equally acceptable in both the young growing patient and the mature adult. By comparison with the rib grafts, the ramal slkle grafts were poor substitutes. Functionally, these local grafts restored condylar form in an acceptable manner, but showed none of the capacity for adaptation and remodeling observed in the rib graft series. The additional disadvantage of the residual defect in the ramus (permanent reduction in overall size) would be more unacceptable if reconstruction was carried out in childhood or adolescence, before growth was complete. This failure of ramal form to redevelop could be doubly disadvantageous if the procedm'e was employed for reconstruction of an absent or anomalous mandibular condyle resulting from hemifacial microsomia or some other congenital defect. The facial abnormality which follows congenital deficiency, traumatic injury, o r ankylosis of a mandibular condyle in the growth period results from alterations in the pull of muscles and ligaments on the affected side, a change in the functional matrix, and not from damage to or deficiency in the condylar "growth center". E a r l y reconstruction of a growing mandible by a transplant selected for its cellular characteristics, and inserted with the long axis of the head transversely in such a way as to restore facial height and regain the lost dimensions of the functional matrix would appear, on the basis of these experiments, to be both desirable and practicable. As D t J ~ I y , HEALEY & IRVING4 have said "if normal anatomical integrity is to be maintained without periodic surgical h~tervention during the growth period, the adjustment mechanism must be restored". The costoehondral graft, by virtue of the adaptive potential of the
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cartilage, the mechanical properties of the strut, and the ready availability of various sizes and shapes cut to suit individual requirements, appears to be the graft of choice for reconstruction of the mandibular joint in both the growth period and later in adult life. T h e role of the sliding ramus graft is somewhat less certain. While functional anatomy can be restored simply in the original operative site, there are obvious deficiencies which p r e c l u d e the application of this technique for reconstruction of the condyle in the growing jaw. On the basis of histologic comparisons, the ramal strut lacks the capacity of. the r i b graft to adapt to the donor site o f the glenoid fossa, while it is probable that it is eventually c a p p e d by articular cartilage, this is non-hypertrophic in form ,and without the capacity for active remodeling. U n d e r such circumstances it could profitably be used for reconstruction of condylar deficiency in an adult in those cases where a simple functional condyle is considered advantageous, and the operative p r o c e d u r e to o b t a i n a rib graft is contraindicated. Previous experiments designed to study the growth o,f jaws following autogenous grafts were based on the concept that the cartilage of the m a n d i b u l a r condyle was an active g r o w t h center2, ~s. I t is believed that in the light o f more recent knowledge of the factors responsible for facial growth, and the observations m a d e in this experiment, fresh studies should be conducted in an att e m p t to regain n o r m a l growth following c o n d y l e c t o m y in the "growth period". I t is p r o p o s e d t h a t when the articulating surface of the chosen transplant is capped with h y p e r t r o p h i c cartilage, placed correctly in the fossa, a n d the facial height and symmetry are restored, the resultant condylar head will a d a p t a n d respond to the demands of the f u n c t i o n a l matrix, thus permitting adequate m a n d i b u l a r growth.
A c k n o w l e d g m e n t s - The assistance of Mr. PETER
BANKS and Dr. JOHN GEHRIO with operative procedures and Messrs. E. B. BRAIN and P. BROADEERY with photographic techniques is acknowledged with appreciation.
References 1. CARLSSON, G. E. & (~BERG, TA Remodeling of the temporomandibular joints, Oral Sci. Rev. 1974: 6: 53-86.
2. CHOUKAS,IN. u TOTe, P. D. & SHUKES,R. C.: Metatarsal transplantations following unilateral mandibular condylectomies in M a caca mulatta monkeys. J. Oral Surg. 1971: 29: 171-177. 3. DINOMAN, R. O. & GRABS, W. C.: Reconstruction of both mandibular condyles with metatarsal bone grafts. Plast. Reconstr. Surg. 1964: 34: 441-451. 4. DURKIN, J., HEELEY, J. &: IRVING, J. T.: The cartilage of the mandibular condyle. Oral Sci. Rev. 1973: 2: 29-99.
5. HAMILTON, W. J., BOYD, J. D. & MOSSMAN, H. W.: H u m a n embryology. 4th ed. Heifer, Cambridge 1972, p. 528-530. 6. KENDRICK, (~. W., CAMERON, J. A. & MATHEWS, ]'. L : Macaca rhesus monkey skull and surgicM intervention. Am. J. Orthod.
1962: 48: 34-44. 7. LANFRANCHI, lZ. P.: Surgical reconstruction oJ the mandible ]ollowing a condylectomy; in the rhesus monkey. Thesis, Northwestern
University, Chicago 1955. 8. McKmBIN, B. & HOLDSWORTH, F. W.: The nutrition of immature joint cartilage in the lamb. J. Bone Jt. Surg. 1966: 48B: 793-803. 9. McKmmN, B. & HOLDSWORTH, F. W.: The dual nature of epiphyseal cartilage. J. Bone Jr. Surg. 1967: 49B: 351-361. 10. MoFFETT, B.: The morphogenesis of the temporomandibutar joint. A m . J. Orthod. 1966: S2: 401--415. 11, Moss, M. L.: The primacy of functional matrices in orofacial growth. Dent. Pract. Dent. Rec. 1968: 19: 65-73. 12. PESKIN, S. 8r LASKIN, D. M.: Contribution of autogenous condylar grafts to mandibular growth. Oral Surg. 1965: 20: 517-534. 13. POSWILLO, D. E.: The late effects of mandibular condylectomy. Oral Surg. 1972: 33: 500-512. 14. POSWrLLO, D.: Surgery of the temporomandibular joint. Oral Sei. Rev. 1974: 6: 87-118.
RECONSTRUCTION OF MANDIBULAR JOINT 1.5. ROBINSON, E. R.: The gross anatomy of the temporomandibular joint of young Macaca rhesus monkeys following unilateral replacement of the mandibular condyles with atttogenous metatarsal bones. Thesis, Northwestern University, Chicago 1961. 16. STOTEVTLLE, O. H.: Surgical reconstruction of the mandible. Plast. Reconstr. Surg. 1957: 19: 229-234. Address: Royal College of Surgeons of England Research Establishment Downe, Orpington, Kent England
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17. WAGE,W. H.: Personal communication 1974-. 18. WARE, W. H. & TAYLOR, R. C.: Cartilaginous growth centres transplanted to replace mandibular condyles irt monkeys. J. Oral Sttrg. 1966: 24: 33-43. 19. Wg~qMANN, J. P. & SrClaER, H.: Bone and bones. 2nd ed., C. V. Mosby Co., St. Louis 1955.
Experimental reconstruction of the mandibular joint DAVID POSWILLO
Royal College o] Surgeons o/ England, London, and Queen Victoria Hospital, East Grinstead, S,tssex, England
~U3STRACT-- It is proposed that the cartilage of the mandibular condyle is not the site of active growth but rather that of secondary adaptive and remodeling responses. Experiments were conducted in M. irtts monkeys replacing the surgically excised mandibular condyle with either a sliding ramus graft or a costochondral rib graft. After 2 years the characteristics of the grafts were examined. Both techniques produced acceptable functional condyles; when examined histologically, the condyle formed from the rib graft was shown to be closely comparable to the condyle on the unoperated side. The functional condyle formed by the sliding ramus graft lacked the histologic features of the normal condyle and showed less capacity for remodeling and adaptation. It is proposed that the histolog[c nature of the grafts used to restore the condyle could have a profound influence on subsequent growth and development. The costochondral graft is readily available, possesses the necessary mechanical properties, and has the capacity for remodeling into an adaptive mandibular condyle. These properties make it eminently suitable for use in reconstruction of the condyle in both the growth period and adult life; when placed correctly in the fossa, and facial height and symmetry are restored, the resultant condylar head adapts and responds to the demands of the functional matrix, thus permitting mandibular growth.
(Received Jor publication 23 Jzdy, accepted 26 Jzdy 1974)
F o r m a n y years it was believed that the m a n d i b l e could be regarded, for purposes of growth, as a long bone in disguise, albeit a " b e n t " Iong bone, and that the center of active growth was located in the condylar cartiIage~0. It is apparent now, from a recent review of the literature by DURKIN, HEALEY & IRVING~, that this classic concept can no longer be accepted without considerable
reservation. The response of the articular cartilages of both m a n d i b u l a r condyle and long bones to physiologic and pathologic changes has been shown to be similar, and quite distinct from the reaction in the u n i q u e epiphyseal growth plate cartilages. Study of the histology and the b i o c h e m ical behavior of the cartilage cells in both condylar and epiphyseal cartilages suggests
RECONSTRUCTION OF MANDIBULAR JOINT that these are the sites of adaptive and compensatory remodeling responses. They are not comparable with growth centers found in the growth plate cartilages. The histologic appearance of cartilage, in a specific location, appears to reflect the ultimate behavior of the site. For example in the growth plate, there are well-organized transverse cartilaginous bars, unmineralized, but penetrated by erosive capillaries. Calcification takes place only in the thick vertical compartments between the regular columns of cells. By contrast, in the mandibular condyle and articular epiphysis the cells are arranged in haphazard fashion, as distinct from vertical columns; calcification takes place in the pericellular space surrounding the cartilage cells. Thus one finds that in the growth plate, elongation takes place in a constant longitudinal fashion, parallel to the vertical columns. In the condyle and epiphysis growth is multidirectional, meeting the need to adapt the articular surfaces to constant changes in the intracapsular environment. As age progresses, and the need to adapt diminishes, so the capacity of the cartilage to remodel reduces accordingly. Although maturation of the cartilage in the condyle proceeds more slowly than in the epiphysis of a long bone, it follows a similar course. While slight histologie variations are observed, the process of maturation in the two sites is essentially the same. It involves the transformation of hypertrophic, or embryonic-type cartilage into a mature non-hypertrophic tissue in which the lower cartilage border is sealed off by subchondral bone. These distinctive histologic changes indicate that the mandibular condyle can no longer be thought of as a primary growth center, embodying normal endochondral bone formation, but rather as a modified epiphysis which, like that on the long bone, grows just enough to ensure proper modeling of the extremities 5. During early life both the mandibular and epiphy-
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seal cartilages are embryonic in character, having a capacity for rapid adaptive remodeling. The histologic appearance and behavior of the cartilage cells at that time further support the suggestion of embryonic or hypertrophic characteristics. In the formotive years of postnatal life the condylar cartilage must meet the demands of its changing environment; rapid dimensional changes occur in those temporal components of the joint comprising the glenoid fossa and articular eminence. These changes are met by the potential for flexibility and adaptation possessed by the mandibular cortdyle. As in the epiphysis, when the demand for adaptive remodeling ceases, the condylar cartilage reverts from the hypertrophic form to a resting, non-hypertrophic state. The function then becomes principally that of a protective articular veneer, with a capacity for replacement of lost or worn-out cells. This change from embryonal to mature form takes place slowly in the condyle by comparison with the epiphysis of a long bone. Growth of the craniofacjal complex is particularly active up to the age of 14 years. As age increases from 14 to 28 the changes in the eraniofacial region become less obvious, more subtle, and the demands on the compensatory mechanisms are reduced. During this period of diminishing need for adaptive remodeling the cartilage of the condyle is converted to adult articular form, the cartilage-bone interface consolidates and fnses, and adaptive changes cease. If, as appears likely, the mandibular condyle does not provide the dominant growth impetus to the mandible, what is it that enables the mandible to "lead the growth of the face"10? Moss~ has proposed that the relationship between muscles and the facial skeleton is such that a functional matrix is formed; the size, shape, position and maintenance of the mandible, therefore, are governed by the primary morphogenetic demands of specifically related mastieatory
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muscles and ligaments within the oro-faciaI capsule. If this hypothesis is valid, and there is c o n s i d e r a b l e evidence to support it, then it w o u l d appear I ogieal to approach the p r o b l e m of reconstruction of an absent or a n o m a l o u s condyle on the basis of this concept. T h a t being so, the priorities would a p p e a r to be early re-establishment of the m a n d i b u l a r ramal functional matrix with a c o n d y l a r cartilage capable of adaptive rem o d e l i n g responses rather than the provision of a graft embodying an "active growth center" e.g. a metatarsal. Attempts to maintain g r o w t h of the mandible by grafted femurs, f i b u l a r heads, and metatarsals have been m a r k e d by a conspicuous absence of growth; in many instances the growth plate was f o u n d to have disappeared, and only the articular surface of the transplant showed signs of cellular activity 2, 3,11,7, 12, 15, 16 Observations m a d e on the late effects of m a n d i b u l a r condylectomy support the contentiort that the m o r p h o l o g y and growth of the m a n d i b l e are governed by the functional matrix. Following condylectomy, in both m o n k e y a n d man, the mandible has been shown to "regenerate" a functional condylar head ta. Histologic examination of the regenerated condyle revealed an articular cap of cartilage, f e r m e d apparently by metaplasia of local fibroblasts, covering the articular s u r f a c e of the bone. The presence of an intact intra-articular meniscus promoted a smooth regular articular surface on the reconstituted condyle. This capacity of the m a n d i b l e for spontaneous regeneration of a functional condyle encouraged the speculation that satisfactory reconstruction of a d a m a g e d o r missing condyle could be achieved by the a d v a n c e m e n t of a strut of bone mobilized f r o m the posterior border of the r a m u s o f the mandible. Following the p l a c e m e n t o f such a sliding ramus graft in the a r t i c u l a r fossa it was anticipated that the a r t i c u l a r histology would rapidly grow to resemble that observed in the "regenerated"
condyle. It was hoped that the correction of ramal and condylar deformity and mandibular height could be simply, but precisely corrected by this procedure utilizing the reconstitution of an intact functional matrix; it usurped all the advantages of spontaneous regeneration, without the disadvantages of imprecision and unpredictability which accompanied spontaneous reformation of a functional condyle. The concept of reconstitution of the functional matrix with an appropriate bone graft capped with cartilage demanded consideration also of the alternative method of reconstruction of an absent or anomalous condyle, grafting of an autogenous costochondral strut. This technique had been used successfully in a limited number of clinical studiest4, ~7. In preliminary studies, WARE & TAVLoI~t8 found that both fibular heads and costochondral grafts could be employed to reconstruct condyles in children affected by early ankylosis. T h e y reported that the overall results with eostochondra[ struts were superior to those from fibular heads; posttreatment growth was sustained, and the costochondral grafts were easier to obtain and quicker to adapt. When interpreting these findings in the light of recent knowledge concerning the behavior of the cellular component of articular and other forms of cartilage, it appeared that the cartilaginous element of the costochondral strut may have made a major contribution to the success of these grafts. Studies were designed, therefore, to compare radiologically and histologically the efficacy of mandibular ramus slides and costoehondral strut grafts in replacement of the resected mandibular condyle.
Experimental method Eight young adult Maraca irus monkeys, all of which had undergone unilateral or bilateral cnndylectomy 3 years previously, were divided
RECONSTRUCTION OF M A N D I B U L A R JOINT
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fossa and immobilized.
intra-articular disc, and placed with the long axis lying latero-medially. The costochondral graft consisted o f 0.5 cm of cartilage attached to 3 cm of rib bone. A strip of periosteum was left intact to cover the costochondral junction to reinforce the fragile junction zone. Ramus and rib grafts were both fastened in position by stainless steel wires. The wound was irrigated, dusted with antibiotic powder and closed in layers without drainage. N o intermaxillary fixation was used; had this been done, regulations relating to free-feeding of experimental animals would have been contravened. After recovery f r o m anesthesia, all animals were returned to normal cage life, with a soft diet for 2 weeks. Antibiotic therapy with intramuscular Triplopen| was maintained every second day for 1 week. The animals in Group 2 were treated similarly, with the distinction that a sliding ramus graft was carried out on one side (right or left) and the rib graft on the opposite side. In both groups, radiographs of both sides of the jaw were taken at 3-month intervals from the time of operation until sacrifice of all animals after 24 months. At the time of operation, in all animals in Group 1 (where a unilateral condylectomy had been carried out) the coronoid process was considerably enlarged on the
into two groups. Group I consisted of six animals with prior unilateral condylectomy; three were right sided cases and three were left sided. Group 2 comprised two animals in which condylectomy had been performed bilaterally. Under gas-oxygen-halothane anesthesia in all animals in Group 1 either a sliding ramns graft (Fig. 1) obtained from the posterior border of the mandible of the same side or an autogenous costochondral graft obtained from the seventh rib was carried out (Fig. 2). Immediately prior to the grafting procedure the condylar stump which had regenerated following the previous condylectomy, was removed by the submandibular approach. The d o n o r site on the ramns of the mandible was roughened by decortication prior to insertion of the rib graft. T h e sides were reversed so that right or left sliding grafts and rib grafts were reasonably distributed among the six animals. Where the sliding ramus graft was used it was shaped at the superior end to present a rounded articular head making contact with a carefully preserved
Fig. 2. Costochondral rib graft attached to posterior border of the ramus, with cartilage end in the fossa.
Fig. I. Sliding ramus graft placed in glenoid
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operated side, in comparison with the tmoperated side. In the animals in Group 2 both coronoid processes were hypertrophied. Throughout the postoperative period regular observations were made of the occlusion of the teeth and function of the jaws. At sacrifice the heads of the animals were perfused with buffered formol saline, and the decapitated heads were then skinned, sectioned in the sagittal plane, radiographed and stored for 1 month in fixative. They were then demineralized in 4N formic acid, the temporomandibu[ar apparatus was dissected out en bloc, and prepared for section in the frontal plane to avoid damage to the microtome by fixation wires in the specimens.
Results The regular radiographs showed reasonable progressive osseous reconstitution of a mandibular condyle in all animals in both groups. At the time of sacrifice there had been n o obvious change in morphology for 6 months. N o appreciable change was observed in the coronoid processes throughout the whole postoperative period. N o r m a l occlusion of the teeth was maintained in all animals in Group 1. For the first 6 m o n t h s there was a mild degree of deviation of the jaw to the operated side on m a x i m u m opening. Prior to operation both animals in Group 2 displayed a moderate anterior open bite which had followed the original condylectomy. Because intermaxillary fixation could not bc applied, tMs open bite was not corrected during the grafting procedure. Consequently the occlusal p a t t e r n of these animals exhibited open bite, b u t no other changes, after the joint replacement procedure; full mouth opening and n o r m a l function were maintained postoperatively in these animals until sacrifice. Radiographic examination at sacrifice revealed the presence of adequate functional condyles following both sliding ramus grafts and costochondral struts (Figs. 3 A C). O n every side where a sliding ramus graft h a d been used the anteroposterior width of the mandibular ramus remained
substantially smaller than the opposite side, whether unoperated or subjected to rib grafting without removal of the posterior border of the ramus (Fig. 3 B). Microscopic examination of the control and experimental mandibular heads revealed significant differences. In the unoperated mandibular condyle the typical diarthrodial joint was observed. The articular surface of the glenoid fossa consisted of thin compact bone. Superficiai cover was provided by thin fibrous connective tissue with some interposed cartilage cells. The intra-articular meniscus was composed of connective tissue, thicker on the medial and lateral sides, and thinned above the articular surface of the condyle. The condylar head was covered by a perichondrium comprising fibrous connective tissue in the deeper layers of which were found fibroblasts, chondroblasts and chondrocytes. Beneath the fibrous covet" were layers of cartilage cells, irregularly distributed, but increasing slightly in size from superficial to deep. There was little evidence of islands of irregular cartilage or chondroclast activity at the cartilage-bone interface. Beneath the cartilage cells were regular osseous trabeculae meeting in a linear fashion with the cartilage layer across the whole interface. There was scant evidence of active endochondral ossification. The articular apparatus was enclosed in an intact synovial membrane of thin connective tissue containing capillary vessels (Fig. 4 A, B). In the condylar heads derived from costochondral grafts there was a consistency of histologic appearance throughout the series, in both Group 1 and Group 2 animals. The condylar heads were smaller in all dimensions than the unoperated controls, but the temporomandibular apparatus which followed reconstruction with rib grafts was a typical diarthrodial joint enclosed in a normal synovial membrane. T h e temporal surface a n d intra-articular disc were closely comparable with the control specimens. The
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Fig,. 3. A, radiograph of mandibular condyle in experimental animal on the unoperated side. B, radiograph of functional condyle formed 2 years after sliding ranms graft. C, radiograph of functional condyle formed 2 years after costochondral graft.
disc was thinner in the central portion, and less cellular. The articular surface of the condyle was covered with a perichondrium identical to that on the unoperated sides. Beneath this was a typical cartilaginous cap rather thicker than normal, with tongues of cartilage penetrating the osseous trabeculae right across the interface. Islands of 9 cartilage ceils were seen in the center of the bony supports, and osteoblastic and osteoelastic activity were seen both in active (cel-
lular) progress and in multiple reversal lines across the cartilage-bone junction. With the exception of a mosaic of reversal lines the osseous trabeeulae were comparable with their unoperated counterparts (Fig. 5 A, B). There was less uniformity of histologic morphology in those cases in which joint reconstruction had been achieved by sliding ramus grafts. Generally, while the temporal surface was normal, the meniscus was irregular, with loose fibrous tissue adhesions
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Fig. 4. A, coronal section of the condylar head, meniscus, and fossa on unoperated side showing normal configuration of ioint components. B, higher power illustration of unopgrated condylar head showing cellular characteristics o~ the fibrocartilage of the condyle, and regular cartilage-bone interface.
observed between the articular surface of the condylar head a n d the disc. While the diarthrodiaI design existed, enclosed in a synovial apparatus, the boundaries were illdefined and the division into upper and lower j o i n t spaces was at times difficult to make in examination of serial sections. The form of the condylar heads was much less typical than in the rib graft series. The articular surfaces had frequent irregularities,
filled with fibrous tissue adherent to the meniscus. The head of the condyle consisted of a layer of compact bone, with many reversal lines, covered by dense parallel layers of fibrous tissue, rich in fibroblasts. In the deeper layers a few chondroblasts and chondrocytes were observed; there was no complete veneer of cartilage present as yet, and no evidence of endochondral ossification (Fig. 6 A,B).
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i: ~I i~ :!i~ilii~:~ ii;: r
Fig. 5. A, coronal section of condylar head reconstituted from costochondral graft in animal shown in 4a. The head and disc are both smaller, but the appearance is consistent with a normal temporomandibular apparatus. B, higher power view of condylar head formed from rib graft, showing remodeling activity of cartilage and bone in the articular head.
Discussion Although considerable evidence is available to demonstrate the inherent growth forces of "growth plate" cartilage, the replacement of the mandibular condyle by a "growing" bone such as a metatarsal has met with little or no success. The architectural arrangement of the condylar cartilage is quite unlike that found in "growth plates", and its role in
overall growth of the mandible remains u n certain. Examination of excised condylar heads in cases of hyperplasla of the m a n dible reveals greatly thickened cartilage zones1; following condylar shave, the growth of the mandible reverts to normal. It appears possible therefore that when active growth, in contrast to adaptive remodeling, takes place in the condylar head, hyperplasia results. Thus, when the condylar head
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Fig. 6..4, coronal section of functional condyle formed from sliding ramus graft. B, higher power section of ramus-graft condyle showing fibrous adhesion between articular surface and meniscus, absence of obvious cartilaginous zone, and compact bone adjacent to the fibrous articular cover.
is replaced by a metatarsal in the expectation that growth will continue, several false assumptions may be made. Firstly, it could be assumed that the condylar head is normally a major growth center, and that a metatarsal graft would replace it. This is illogical, even if the mandibular condyle was a growth center, because the growth
plate of the metatarsal is not located in the epiphyseal articular cartilage. McKIBI3IN & I"IOLDSWORTH8,9 made this distinction when they pointed out that the articular and growth plate cartilages, on the basis of both embrylogic derivation and ultrastructure, are fundamentally different. Secondly, even if it were assumed that the condylar head was
RECONSTRUCTION OF MANDIBULAR JOINT not a site of major growth, but rather one of adaptive and compensatory modeling, its replacement by the non-hypertrophic articular cartilage of the metatarsal could not promote the necessary modifications in the condyle demanded by rapid compensatory changes in the environment. It is hardly surprising, therefore, that the result of metatarsal grafts was disappearance of the growth plate, with little to suggest the original character of the transplant. Only the character of the articular cartilage remained2, ts, a predictable result if one accepts that the true nature of the mandibular condyle was never that of a growth plate cartilage, and therefore not a primary growth center. All attempts to change it from a center of remodeling to a center of growth would thus be destined at the best to be a static situation, or at the worst to hyperplasia. This potential for hyperplasia was observed in one animal following metatarsal graft by WARE ~.~ TAYLOR 18, but the full significance of the observation was not appreciated. Where the (only) metatarsal graft was seen to grow actively at the growth plate, "it appeared both clinically and radiographically that the transplant grew more than the normal condyle". The success or failure of an approach to reconstruction of the mandibular joint may be more closely related to the adaptive capacity of the articular cartilage and the reconstitution of the functional periosteal matrix than the transplantation of a "growth center". The capacity os tke embryonic-type hypertrophic cartilage of the costochondral graft to adapt and remodel to a histologically perfect condyle within 2 years, in young adult monkeys, is a significant finding in this experiment. Growth studies were not performed, and in fact would have yielded no significant information in animals in which most craniofacial growth had ceased. Nonetheless, the reconstitution, following rib grafting, of a functional condyle capable of
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adaptive responses is an important finding. If both facial height and the compensatory adjustment mechanism are shown to be restored by careful selection of transplantation tissues, then results should be equally acceptable in both the young growing patient and the mature adult. By comparison with the rib grafts, the ramal slkle grafts were poor substitutes. Functionally, these local grafts restored condylar form in an acceptable manner, but showed none of the capacity for adaptation and remodeling observed in the rib graft series. The additional disadvantage of the residual defect in the ramus (permanent reduction in overall size) would be more unacceptable if reconstruction was carried out in childhood or adolescence, before growth was complete. This failure of ramal form to redevelop could be doubly disadvantageous if the procedm'e was employed for reconstruction of an absent or anomalous mandibular condyle resulting from hemifacial microsomia or some other congenital defect. The facial abnormality which follows congenital deficiency, traumatic injury, o r ankylosis of a mandibular condyle in the growth period results from alterations in the pull of muscles and ligaments on the affected side, a change in the functional matrix, and not from damage to or deficiency in the condylar "growth center". E a r l y reconstruction of a growing mandible by a transplant selected for its cellular characteristics, and inserted with the long axis of the head transversely in such a way as to restore facial height and regain the lost dimensions of the functional matrix would appear, on the basis of these experiments, to be both desirable and practicable. As D t J ~ I y , HEALEY & IRVING4 have said "if normal anatomical integrity is to be maintained without periodic surgical h~tervention during the growth period, the adjustment mechanism must be restored". The costoehondral graft, by virtue of the adaptive potential of the
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cartilage, the mechanical properties of the strut, and the ready availability of various sizes and shapes cut to suit individual requirements, appears to be the graft of choice for reconstruction of the mandibular joint in both the growth period and later in adult life. T h e role of the sliding ramus graft is somewhat less certain. While functional anatomy can be restored simply in the original operative site, there are obvious deficiencies which p r e c l u d e the application of this technique for reconstruction of the condyle in the growing jaw. On the basis of histologic comparisons, the ramal strut lacks the capacity of. the r i b graft to adapt to the donor site o f the glenoid fossa, while it is probable that it is eventually c a p p e d by articular cartilage, this is non-hypertrophic in form ,and without the capacity for active remodeling. U n d e r such circumstances it could profitably be used for reconstruction of condylar deficiency in an adult in those cases where a simple functional condyle is considered advantageous, and the operative p r o c e d u r e to o b t a i n a rib graft is contraindicated. Previous experiments designed to study the growth o,f jaws following autogenous grafts were based on the concept that the cartilage of the m a n d i b u l a r condyle was an active g r o w t h center2, ~s. I t is believed that in the light o f more recent knowledge of the factors responsible for facial growth, and the observations m a d e in this experiment, fresh studies should be conducted in an att e m p t to regain n o r m a l growth following c o n d y l e c t o m y in the "growth period". I t is p r o p o s e d t h a t when the articulating surface of the chosen transplant is capped with h y p e r t r o p h i c cartilage, placed correctly in the fossa, a n d the facial height and symmetry are restored, the resultant condylar head will a d a p t a n d respond to the demands of the f u n c t i o n a l matrix, thus permitting adequate m a n d i b u l a r growth.
A c k n o w l e d g m e n t s - The assistance of Mr. PETER
BANKS and Dr. JOHN GEHRIO with operative procedures and Messrs. E. B. BRAIN and P. BROADEERY with photographic techniques is acknowledged with appreciation.
References 1. CARLSSON, G. E. & (~BERG, TA Remodeling of the temporomandibular joints, Oral Sci. Rev. 1974: 6: 53-86.
2. CHOUKAS,IN. u TOTe, P. D. & SHUKES,R. C.: Metatarsal transplantations following unilateral mandibular condylectomies in M a caca mulatta monkeys. J. Oral Surg. 1971: 29: 171-177. 3. DINOMAN, R. O. & GRABS, W. C.: Reconstruction of both mandibular condyles with metatarsal bone grafts. Plast. Reconstr. Surg. 1964: 34: 441-451. 4. DURKIN, J., HEELEY, J. &: IRVING, J. T.: The cartilage of the mandibular condyle. Oral Sci. Rev. 1973: 2: 29-99.
5. HAMILTON, W. J., BOYD, J. D. & MOSSMAN, H. W.: H u m a n embryology. 4th ed. Heifer, Cambridge 1972, p. 528-530. 6. KENDRICK, (~. W., CAMERON, J. A. & MATHEWS, ]'. L : Macaca rhesus monkey skull and surgicM intervention. Am. J. Orthod.
1962: 48: 34-44. 7. LANFRANCHI, lZ. P.: Surgical reconstruction oJ the mandible ]ollowing a condylectomy; in the rhesus monkey. Thesis, Northwestern
University, Chicago 1955. 8. McKmBIN, B. & HOLDSWORTH, F. W.: The nutrition of immature joint cartilage in the lamb. J. Bone Jt. Surg. 1966: 48B: 793-803. 9. McKmmN, B. & HOLDSWORTH, F. W.: The dual nature of epiphyseal cartilage. J. Bone Jr. Surg. 1967: 49B: 351-361. 10. MoFFETT, B.: The morphogenesis of the temporomandibutar joint. A m . J. Orthod. 1966: S2: 401--415. 11, Moss, M. L.: The primacy of functional matrices in orofacial growth. Dent. Pract. Dent. Rec. 1968: 19: 65-73. 12. PESKIN, S. 8r LASKIN, D. M.: Contribution of autogenous condylar grafts to mandibular growth. Oral Surg. 1965: 20: 517-534. 13. POSWILLO, D. E.: The late effects of mandibular condylectomy. Oral Surg. 1972: 33: 500-512. 14. POSWrLLO, D.: Surgery of the temporomandibular joint. Oral Sei. Rev. 1974: 6: 87-118.
RECONSTRUCTION OF MANDIBULAR JOINT 1.5. ROBINSON, E. R.: The gross anatomy of the temporomandibular joint of young Macaca rhesus monkeys following unilateral replacement of the mandibular condyles with atttogenous metatarsal bones. Thesis, Northwestern University, Chicago 1961. 16. STOTEVTLLE, O. H.: Surgical reconstruction of the mandible. Plast. Reconstr. Surg. 1957: 19: 229-234. Address: Royal College of Surgeons of England Research Establishment Downe, Orpington, Kent England
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17. WAGE,W. H.: Personal communication 1974-. 18. WARE, W. H. & TAYLOR, R. C.: Cartilaginous growth centres transplanted to replace mandibular condyles irt monkeys. J. Oral Sttrg. 1966: 24: 33-43. 19. Wg~qMANN, J. P. & SrClaER, H.: Bone and bones. 2nd ed., C. V. Mosby Co., St. Louis 1955.