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Costochondral grafts in reconstruction of the temporomandibular joint after condylectomy: an experimental study in sheep
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British Journal of Oral and Maxillofacial Surgery (2001) 39, 189–195 © 2001 The British Association of Oral and Maxillofacial Surgeons doi: 10.1054/bjom.2001.0622, available online at http://www.idealibrary.com on
Journal of Oral and Maxillofacial Surgery
Costochondral grafts in reconstruction of the temporomandibular joint after condylectomy: an experimental study in sheep H. Matsuura,* H. Miyamoto,† J.-I. Ishimaru,‡ K. Kurita,§ A. N. Goss¶ *Visiting Research Fellow; †Former Visiting Research Fellow Oral and Maxillofacial Surgery Unit, Dental School, The University of Adelaide, Adelaide, South Australia and The First Department of Oral and Maxillofacial Surgery, School of Dentistry, Aichi-Gakuin University, Nagoya, Japan; ‡Chief, Department of Oral and Maxillofacial Surgery and Stomatology, Gifu Prefectural Gifu Hospital, Gifu, Japan; §Professor and Director, The First Department of Oral and Maxillofacial Surgery, School of Dentistry, Aichi-Gakuin University, Nagoya, Japan; ¶Professor and Director, Oral and Maxillofacial Surgery Unit, Dental School, The University of Adelaide, South Australia SUMMARY. The purpose of this study was to investigate the effect of costochondral grafts in the temporomandibular joint (TMJ) in sheep. Five pure-bred adult Merino sheep were used. The condyle alone was resected and replaced with a costochondral graft from the 13th rib. The sheep were killed 3 months after operation. The range of jaw movements before and after operation and at death were recorded. The joints were examined radiologically, macroscopically, and histologically. A new condylar head with normal configuration and function developed. Histologically, the chondrocytes were arranged in a fashion similar to that of a normal joint. All inferior joint spaces showed fibrous adhesions between the condylar head and disc. This study showed that, when such grafts are used to replace the condyle in an otherwise normal sheep TMJ, they fused to the ramus and reconstituted a nearly normal, fully functional joint. © 2001 The British Association of Oral and Maxillofacial Surgeons
laterally beyond the glenoid fossa.15 Most of the transplants were well attached to the ramus, but some were lost or incompletely joined to the mandible. Reconstruction of the sheep TMJ with a costochondral graft has not so far been reported to our knowledge. Anatomically, sheep have 13 pairs of ribs, the 13th of which is more or less rudimentary, being small and thin, often floating, or may be fused with the corresponding vertebra and have a cartilage about one inch long.17 The diaphragmatic line runs from the sternum to the cartilaginous part of the 8th and 9th ribs, and across to the costochondral junction of the 10th and 11th ribs, then dorsally behind the 13th to midway between the last thoracic and the first lumbar vertebrae,18 so the harvest of the 13th rib does not affect thoracic function and is safe. Sheep TMJ have the advantages of being similar in size, shape and structure to those of humans, and they are cheap and ethically acceptable.19–25 Sheep models of osteoarthritis,20 internal derangement,21 and ankylosis22–25 have been developed. The aim of this study was to investigate the shortterm effect of costochondral grafts for condylar replacement in an otherwise normal sheep TMJ.
INTRODUCTION Costochondral grafts are indicated in TMJ reconstruction for ankylosis, facial asymmetry, and the replacement of diseased mandibular condyles.1 Clinically, they have been extensively used for congenital dysplasias, ankylosis, osteoarthritis, trauma, and the replacement of the condyle after resection of a tumour. They resulted in restoration of jaw function and restore the growth potential of the mandible.2–5 Despite the favourable anatomical and adaptive characteristics of the graft, there are a number of well-known complications associated with costochondral grafting, including infection, fracture of the costochondral junction, pain, resorption, and mandibular overgrowth in children.6–11 We know of few experimental animal studies of costochondral grafts.12–16 Experimental studies of 17 young cynomolgus (Macaca irus) monkeys that were observed for 3 years showed that the costochondral junction changed little in the forward and vertical positions, and cartilaginous elements could still be identified on the surface of the transplant.12 Experimental studies in 20-day-old rats that were observed for 20 days showed that the grafts continued to grow posteriorly and 189
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MATERIALS AND METHODS Five pure-bred adult Merino sheep, aged about 2 years and weighing roughly 55 kg were used. All right joints were operated on and all left joints were served as control. Anaesthesia was induced with intravenous injection of thiopentone sodium 500–1000 mg into the external jugular vein. The sheep were intubated and anaesthesia maintained with a mixture of 3% halothane and oxygen, and nitrous oxide through an orotracheal tube. Their jaw movements were measured vertically and laterally. The right preauricular area and the right side of the chest were shaved and prepared with povidone iodine, and the field was isolated with sterile drapes. A 6-cm skin incision was made over the 13th rib on the right side. The costochondral bone with perichondrium A
was harvested from the 13th rib to a length of 70 mm (Fig. 1). This wound was closed primarily. A 4-cm vertical preauricular skin incision was made over the lateral capsule of the right TMJ. The inferior joint space was then opened by a horizontal incision through the joint capsule. The condylar head was excised at a measured 10 mm from the condylar articular surface with a fissure bur. The disc was preserved. To fit the graft, the postero-lateral margin of the mandibular ramus was reduced to half in thickness. The rib was trimmed until there was a 26-mm bony and 2-mm cartilaginous component. The periosteum of the costochondral bone was retained except for its contact surface with the mandibular ramus. The graft was placed in the joint space projecting 8 mm above the resection of the articular process and fixed in 2 places (superior and inferior to the mandibular ramus) with a 0.5-mm metal wire (Fig. 2). Debris was removed by irrigation and suction, and then the overlying tissues were repaired in layers. Just after the operation, the jaw movements were measured vertically and laterally. Benzyl penicillin 400 mg and streptomycin sulphate 500 mg were given intramuscularly twice daily for 2 days. The sheep were managed in a covered animal house for a week and then kept in a field. Their weight was monitored and recorded every week until they were killed three months after the operation with an overdose
B
Fig. 1 (A) The right 13th rib of a sheep (scale in mm). (B) Histological section of the 13th rib of sheep (haematoxylin and eosin stain, original magnification3.2). The cartilaginous tissue consists of hyaline cartilage, and the bone tissue consists of a thin cortical layer with cancellous marrow. (H:hyaline cartilage).
Fig. 2 Intra-operative appearance. The rib bone was placed and fixed in two places with an 0.5 mm metal wire. (R:rib bone, M:mandibular ramus, arrow:disc).
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Table 1 Criteria and score for radiological assessment23–25 Score Items
Criteria
Shape
Change of a joint form Concavity in the cortical plate of a joint surface with an indistinct outline Cortical thickening of a joint surface
Erosion
Sclerosis
Marrow Calcification
Change of underlying trabecular bone Development of calcification across the joint space
0 (No change)
1 (Mild change)
2 (Moderate change)
3 (Severe change)
May include reformed joint
Destruction
Multiple osteophytes
In a third of the surface of the joint
In two-thirds of the surface of the joint
Outgrowth (marginal proliferation) All over surface of the joint
Sclerosis in a third of the surface of the joint
Sclerosis in two-thirds of the surface of the joint
Sclerosis over all surface of the joint
Atrophy or absorption In a third of joint space
Sclerosing change in half of marrow In two-thirds of the joint space
Sclerosing change whole marrow Bony fusion across the joint space
This stage in all items includes normal joint and recent surgical intervention
No calcification
with pentothal. Just after death, the occlusal relation and the range of jaw movements were recorded. Immediately, the joints area were removed en bloc with a band-saw and fixed in 10% neutral buffered formalin. The TMJs were radiographed laterally and anteroposteriorly under standardized conditions, and the features assessed according to the criteria listed in Table 1.23–25 The morphological features of shape, erosion, and sclerosis were investigated for both the condylar and the temporal surfaces, and calcification was scored for the joint space in both radiographs. Changes in the marrow were scored on the temporal surface of the anteroposterior radiographs and in the condyles of both radiographs, with a range of 0 for normal to 3 for gross deviation. A maximum score of 51 could therefore be assigned to a joint. The specimens were decalcified with 9.5% hydrochloric acid, and 1% sodium acetate over saturated EDTA. The TMJs were then divided into three blocks (lateral, central, and medial segments), histologically prepared and stained with haematoxylin and eosin. The histological findings were assessed macroscopically and microscopically. Each slide was assessed at its anterior, central, and posterior aspects, so the joint was divided into nine zones. The histological degree of fibrous ankylosis in the joint spaces was scored in each zone (Table 2).22 The maximum thickness of the temporal bone surface, including the cartilaginous layer and the disc, were also measured in each zone. Scheffe’s F method of one-way analysis of variance (ANOVA) was used to compare the range of jaw movements over time. The Mann–Whitney U test was used to compare the differences in the radiological and histological scores, and the thickness of the temporal bone surface
Table 2 Stage and score for degree of fibrous ankylosis22 Stage 1 2 3 4 5 6
Score
Degree of ankylosis (%)*
0 1 2 3 4 5
0† 1–25‡ 26–50 51–75 76–99 100
* The degree of fibrous ankylosis shows the percentage of connective tissue in the joint space. This tissue may be fibrous tissue, cartilage, or bone. † Includes normal joint, the costal cartilage, and reaction to operation. ‡ May include an osteoarthrotic joint with adhesion.
including the cartilaginous layer and the disc between the experimental and control joints. Probabilities of 0.05 or less were accepted as significant. This experiment was approved by the Ethics Committee of the University of Adelaide.
RESULTS The changes in body weight are shown in Table 3. Each individual sheep marginally increased its body weight over the 3-month period. No malocclusions developed in any sheep. The ranges of jaw movements are shown in Table 4. There were some minor individual variations. The vertical movements increased in 3 of the 5 sheep and decreased in 2. The right lateral movements increased in 3 of the 5 sheep, one decreased and the other remained unchanged. The left lateral movements increased in
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British Journal of Oral and Maxillofacial Surgery Table 3 Body weight (kg) Sheep
Pre operatively
At the time of death
1 2 3 4 5 Mean
48.0 55.0 56.5 54.5 49.5 52.7
52.5 57.0 66.0 60.0 56.0 58.3
A
Table 4 Mean (SD) range of jaw movements in 5 sheep (mm)
Vertically Right Left
Preoperative
Immediately postoperatively
At the time of death
54.2 (5.3) 39.0 (1.4) 39.2 (1.3)
54.4 (5.3) 39.2 (1.3) 39.6 (0.5)
52.8 (8.0) 42.0 (4.6) 35.6 (6.1)
B
There was no significant difference between the groups.
1 of 5 sheep but decreased in the others. There were no significant differences between the groups at any time. Radiologically, radiolucent gaps were maintained between the temporal bone and the graft in all joints operated on (Fig. 3). The temporal articular surface was unchanged. In 4 of the 5 joints operated on, the graft looked like a normal condyle. In the remaining animal, there was moderate hyperosteosis. The mean (SD) radiological scores of the experimental joints was 8.8 (3.8) and of the control joints 1.4 (0.5). This difference was significant (P 0.01). Macroscopically, all grafts were well attached to the mandibular ramus. In all experimental joints, the inferior joint space showed fibrous adhesions between the graft and disc. However, partial clefts were present in all joints, so there was a partial inferior joint space. The superior joint space was maintained all joints. One of 5 TMJs had a perforation of the anterior part of the disc. No changes were found in the temporal articular bone in any specimen. In 2 of 5 lateral and central parasagittal planes, the graft had hyperosteosis beyond the glenoid fossa posteriorly. The medial and central parasagittal planes showed mild hyperplasia within the confines of the fossa. Histologically, all grafts were covered by fibrous connective tissue or fibrous cartilage, or both (Fig. 4). There was an irregular chondrocyte hyperplasia under the fibrous cover, and a proliferation of chondrocytes at the cartilage-bone junction. However, the graft had taken on the structure of the condylar head and no longer looked like a costochondral graft. The surface of the temporal bone was significantly thicker in the experimental than the control joints (Table 5) (P0.0001). In the parasagittal and coronal planes, all were thicker than those of controls (P0.05).
Fig. 3 Radiographs of normal TMJ and one that has been operated on after three months (right). (A) Normal TMJ. The articular surfaces are smooth (T:temporal bone, C:condyle). (B) TMJ that has been operated on. The temporal articular surface was smooth and the head of the costochondral graft looked like a normal condyle. (T:temporal bone, CG:costochondral graft).
Central–lateral, central–central, and all anterior zones of the discs were thinner in the experimental, than in the control joints (Table 6), but not significantly so (P:0.7). The histological rating on the degree of ankylosis scale is shown in Table 7. The mean score of a zone in a joint was 2.2 (range 1–3) in experimental joints and 0.5 (range 0–1) in control joints (P0.001). The control joints were largely unaffected radiologically but one joint showed temporal and condylar flattening in the radiograph and histologically this joint had an increase in the cartilaginous layer. However, these changes were consistent with minor remodelling and were not pathological.
DISCUSSION This study shows that a costochondral graft after condylectomy with the preservation of the normal disc
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C
B
Fig. 4 Results for 4 of 5 joints. The histological section of the normal TMJ and one that has been operated on after three months (right). (A) Photomicrograph of a normal TMJ. (Haematoxylin and eosin stain, original magnification 2) (left/lateral parasagittal section). The articular surface is covered by cartilage. The joint space, which consists of superior and inferior joint spaces, is separated by the disc. (T:temporal bone, D:disc, C:condyle). (B) Photomicrograph of a TMJ that has been operated on. (Haematoxylin and eosin stain, original magnification1.4) (right/central parasagittal section). The graft took on the appearance of a condylar head. The inferior joint space shows partial fibrous adhesion between the condylar-like graft and the disc. The superior joint space is maintained. (T:temporal bone, D:disc, CG:costochondral graft) (C) Photomicrograph of TMJ postoperatively. (Haematoxylin and eosin stain, original magnification12.8) (right/central parasagittal section). At the cartilage-bone junction the parallel columns of chondrocytes are seen and the graft head is covered with the fibrous cartilage. (D:disc, H:hyaline cartilage, FC:fibrous cartilage).
allowed formation of a new condyle within 3 months. This is consistent with other experimental studies.12,13,16 An experimental study of young cynomolgus monkeys12 reported that the cartilage cells seemed disorderly, hyperplastic, and degenerate. In an experimental study using juvenile monkeys,14 the graft remained unchanged and did not respond to its new environment, so the graft was described as an inadequate replacement for the cartilage of the growing mandibular condyle. In a previous experimental study in sheep, in which condylectomy was done in young adult sheep, a similar condylar head almost completely reformed by remodelling. It was covered with fibrous tissue and the cartilage layer reformed similar to a normal condylar head. The inferior joint space had adhesions, in almost all joints operated on.26 However, in this experimental study, the graft took on the appearance of a condylar head and the cartilage layer
clearly showed hyperplastic activity. These reactions resembled a costochondral graft in the TMJ found in previous experimental studies.12,26 One sheep, which showed temporal and condylar flattening in the radiograph, showed an increase in the cartilage layer histologically on the control side. We suggest that this reaction is related to the bone proliferation beyond the glenoid fossa on the experimental side. This histological change was similar to the reaction to experimental disc perforation in sheep TMJ.21 It indicates a change in biomechanics with an abnormal graft resulting in adaptive changes on the opposite side. The temporal bone surface including the cartilage layer of the experimental joints was also thicker than that on the control side. Although the disc was thinner, it was not significantly so. The jaw movements were not affected despite the adhesions in the inferior joint space. The sheep could chew effectively as their body weight increased over the
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British Journal of Oral and Maxillofacial Surgery Table 5 Mean (SD) thickness of the temporal articular surface including the cartilage layer in 5 sheep (mm) Medial* Operate on *
Anterior Central* Posterior*
0.3 (0.2) 0.5 (0.5) 0.2 (0.1)
Central*
Control 0.2 (0.1) 0.1 (0.04) 0.2 (0.1)
Lateral*
Operated on
Control
Operated on
Control
0.3 (0.2) 0.3 (0.2) 0.3 (0.2)
0.1 (0.1) 0.2 (0.1) 0.1 (0.04)
0.2 (0.1) 0.3 (0.2) 0.3 (0.1)
0.2 (0.01) 0.1 (0.1) 0.1 (0.02)
Overall differences between the experimental and the control joints: P0.0001. Differences between the operated on and the control joints: *P0.05.
Table 6 Mean (SD) thickness of the disc in 5 sheep (mm) Medial
Central
Lateral
Operated on
Control
Operated on
Control
Operated on
Control
1.6 (0.3) 1.1 (0.4) 1.8 (0.5)
1.7 (0.3) 0.8 (0.3) 1.4 (0.2)
1.1 (0.5) 0.7 (0.4) 1.9 (0.6)
1.5 (0.2) 0.8 (0.1) 1.9 (0.2)
1.4 (0.7) 0.7 (0.4) 2.0 (0.3)
1.5 (0.2) 0.7 (0.4) 1.7 (0.2)
Anterior Central Posterior
There were no significant differences between the groups.
Table 7 Median (range) histological scores of the degree of fibrous ankylosis in 5 sheep Joint operated on*
Medial
1.6† (1–3) 1.8† (1–2) 1.6† (1–3)
Anterior 2.2‡ (1–4) 3.0† (1–4) 2.8† (2–4) Posterior
2.6‡ (2–3) 2.8‡ (2–3) 2.0‡ (1–3)
Joint not operated on*
Lateral
Medial
0.8† (0–1) 0.6† (0–1) 0.2† (0–1)
Anterior 0.4‡ (0–1) 0.8‡ (0–1) 0† (0) Posterior
0.4‡ (0–1) 0.8‡ (0–1) 0.2‡ (0–1)
Lateral
*P0.001; †P0.05; ‡P0.001.
3 months, so the graft had been stabilized both functionally and histologically within the sheep TMJ. This study could be criticized because of the relatively short duration of 3 months. There are many reasons for this. Sheep chew virtually continuously and with great force, so three months of jaw function in a sheep is equivalent to several years of jaw function in a human. For this reason, the Japan/Australia TMD study group settled on 3 months as our standard time duration for experiments.19–25 This study shows the behaviour of costochondral grafts in normal joints; future studies will look at their use in progressively more diseased joints including those with ankylosis.
ACKNOWLEDGEMENTS We thank Dr G. Kinoshita (Assistant Professor, Department of Orthopaedic Medicine, Hyogo College of Medicine, Japan) for his
advice on costochondral grafts in sheep, and the Australian Dental Research Foundation Inc. for financial support.
REFERENCES 1. Ware WH. Growth centre transplantation in temporomandibular joint surgery. In: Walker RV, ed. Transaction of Third International Conference on Oral Surgery. Edinburgh: Livingstone, 1970: 148–157. 2. Macintosh RB. Costochondral grafts. In: Bell WH, ed. Modern Practice in Orthognathic Surgery. Philadelphia: WB Saunders, 1992: 872–949. 3. Kaban LB, Perrott DH, Fisher K. A protocol for management of temporomandibular joint ankylosis. J Oral Maxillofac Surg 1990; 48: 1145–1151. 4. Lindqvist C, Pihakari A, Tasanen A, Hampf G. Autogenous costochondral grafts in temporo-mandibular joint arthroplasty. A survey of 66 arthroplasties in 60 patients. J Maxillofac Surg 1986; 14: 143–149. 5. Macintosh RB, Henny FA. A spectrum of application of autogenous costochondral grafts. J Maxillofac Surg 1977; 5: 257–267. 6. Merkx MA, Freihofer HP. Fracture of costochondral graft in temporomandibular joint reconstructive surgery: an unexpected complication. Int J Oral Maxillofac Surg 1995; 24: 142–144.
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Costochondral grafts in reconstruction of the TMJ after condylectomy 7. Tasanen A, Leikomaa H. Ankylosis of the temporomandibular joint of a child. Report of a case. Int J Oral Surg 1977; 6: 95–99. 8. Ware WH, Brown SL. Growth centre transplantation to replace mandibular condyles. J Maxillofac Surg 1981; 9: 50–58. 9. Obeid G, Guttenberg SA, Connole PW. Costochondral grafting in condylar replacement and mandibular reconstruction. J Oral Maxillofac Surg 1988; 48: 177–182. 10. Munro IR, Philips JH, Griffin G. Growth after construction of the temporomandibular joint in children with hemifacial microsomia. Cleft Palate 1989; 26: 303–311. 11. Peltomaki T, Isotupa K. The costochondral graft. A solution or a source of facial asymmetry in growing children. A case report. Proceedings of the Finnish Dental Society 1991; 87: 167–176. 12. Ware WH, Taylor RC. Cartilaginous growth centers transplanted to replace mandibular condyles in monkeys. J Oral Surg 1966; 24: 33–43. 13. Poswillo D. Experimental reconstruction of the mandibular joint. Int J Oral Surg 1974; 3: 400–411. 14. Daniels S, Ellis ED, Carlson DS. Histologic analysis of costochondral and sternoclavicular grafts in the TMJ of the juvenile monkey. J Oral Maxillofac Surg 1987; 45: 675–683. 15. Peltomaki T. Growth of a costochondral graft in the rat temporomandibular joint. J Oral Maxillofac Surg 1992; 50: 851–857. 16. Perrott DH, Vargervik K, Kaban LB. Costochondral reconstruction of mandibular condyles in nongrowing primates. J Craniofac Surg 1995; 6: 227–237. 17. Sisson S. The Anatomy of the Domestic Animals, 4th ed. Philadelphia: WB Saunders, 1953: 157. 18. May NDS. The Anatomy of the Sheep, 3rd edn. Queensland: University of Queensland Press, 1970: 43. 19. Bosanquet AG, Goss AN. The sheep as a model for temporomandibular joint surgery. Int J Oral Maxillofac Surg 1987; 16: 600–603. 20. Ishimaru J-I, Goss AN. A model for osteoarthritis of the temporomandibular joint. J Oral Maxillofac Surg 1992; 50: 1191–1195. 21. Bosanquet AG, Ishimaru J-I, Goss AN. Effect of experimental disc perforation in sheep temporomandibular joints. Int J Oral Maxillofac Surg 1991; 20: 177–181. 22. Miyamoto H, Kurita K, Ishimaru J-I, Goss AN. A sheep model for temporomandibular joint ankylosis. J Oral Maxillofac Surg 1999; 57: 812–817. 23. Miyamoto H, Kurita K, Ogi N, Ishimaru J-I, Goss AN. Experimental factors in the genesis of temporomandibular joint ankylosis. Int J Oral Maxillofac Surg 2000; 29: 290–295. 24. Miyamoto H, Kurita K, Ogi N, Ishimaru J-I, Goss AN. The role of the disk in sheep temporomandibular joint ankylosis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1999; 88: 151–158.
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25. Miyamoto H, Kurita K, Ogi N, Ishimaru J-I, Goss AN. Effect of limited jaw motion on ankylosis of the temporomandibular joint in sheep. Br J Oral Maxillofac Surg 2000; 38: 148–153. 26. Miyamoto K, Hirakawa T, Ishimaru J-I, Kurita K, Vickers R, Goss AN. The effect of unilateral condylectomy on the sheep temporomandibular joint. Br J Oral Maxillofac Surg 1999; 37: 401–404.
The Authors H. Matsuura DDS Visiting Research Fellow Oral and Maxillofacial Surgery Unit Dental School, The University of Adelaide, Adelaide, South Australia; Instructor, The First Department of Oral and Maxillofacial Surgery School of Dentistry, Aichi-Gakuin University Nagoya, Japan H. Miyamoto DDS, PhD Staff, The First Department of Oral and Maxillofacial Surgery School of Dentistry, Aichi-Gakuin University Nagoya, Japan; Formerly Visiting Research Fellow Oral and Maxillofacial Surgery Unit Dental School, The University of Adelaide, Adelaide, South Australia J.-I. Ishimaru DDS, DMD Chief Department of Oral-Maxillofacial Surgery and Stomatology Gifu Prefectural Gifu, Hospital, Gifu, Japan K. Kurita DDS, PhD Professor and Director, The First Department of Oral and Maxillofacial Surgery School of Dentistry, Aichi-Gakuin University Nagoya, Japan A. N. Goss DDSc, FRACDS, OMS, FICD Professor and Director Oral and Maxillofacial Surgery Unit Dental School, The University of Adelaide Adelaide, South Australia Correspondence and requests for offprints to: Dr H. Matsuura, The First Department of Oral and Maxillofacial Surgery, School of Dentistry, Aichi-Gakuin University, 2-11 Suemori-dori, Chikusa-ku, Nagoya 464-8651, Japan. Tel: ;81 52 759 2157; Fax: ;81 52 759 2157; E-mail: [email protected] Accepted 23 January 2001
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British Journal of Oral and Maxillofacial Surgery (2001) 39, 189–195 © 2001 The British Association of Oral and Maxillofacial Surgeons doi: 10.1054/bjom.2001.0622, available online at http://www.idealibrary.com on
Journal of Oral and Maxillofacial Surgery
Costochondral grafts in reconstruction of the temporomandibular joint after condylectomy: an experimental study in sheep H. Matsuura,* H. Miyamoto,† J.-I. Ishimaru,‡ K. Kurita,§ A. N. Goss¶ *Visiting Research Fellow; †Former Visiting Research Fellow Oral and Maxillofacial Surgery Unit, Dental School, The University of Adelaide, Adelaide, South Australia and The First Department of Oral and Maxillofacial Surgery, School of Dentistry, Aichi-Gakuin University, Nagoya, Japan; ‡Chief, Department of Oral and Maxillofacial Surgery and Stomatology, Gifu Prefectural Gifu Hospital, Gifu, Japan; §Professor and Director, The First Department of Oral and Maxillofacial Surgery, School of Dentistry, Aichi-Gakuin University, Nagoya, Japan; ¶Professor and Director, Oral and Maxillofacial Surgery Unit, Dental School, The University of Adelaide, South Australia SUMMARY. The purpose of this study was to investigate the effect of costochondral grafts in the temporomandibular joint (TMJ) in sheep. Five pure-bred adult Merino sheep were used. The condyle alone was resected and replaced with a costochondral graft from the 13th rib. The sheep were killed 3 months after operation. The range of jaw movements before and after operation and at death were recorded. The joints were examined radiologically, macroscopically, and histologically. A new condylar head with normal configuration and function developed. Histologically, the chondrocytes were arranged in a fashion similar to that of a normal joint. All inferior joint spaces showed fibrous adhesions between the condylar head and disc. This study showed that, when such grafts are used to replace the condyle in an otherwise normal sheep TMJ, they fused to the ramus and reconstituted a nearly normal, fully functional joint. © 2001 The British Association of Oral and Maxillofacial Surgeons
laterally beyond the glenoid fossa.15 Most of the transplants were well attached to the ramus, but some were lost or incompletely joined to the mandible. Reconstruction of the sheep TMJ with a costochondral graft has not so far been reported to our knowledge. Anatomically, sheep have 13 pairs of ribs, the 13th of which is more or less rudimentary, being small and thin, often floating, or may be fused with the corresponding vertebra and have a cartilage about one inch long.17 The diaphragmatic line runs from the sternum to the cartilaginous part of the 8th and 9th ribs, and across to the costochondral junction of the 10th and 11th ribs, then dorsally behind the 13th to midway between the last thoracic and the first lumbar vertebrae,18 so the harvest of the 13th rib does not affect thoracic function and is safe. Sheep TMJ have the advantages of being similar in size, shape and structure to those of humans, and they are cheap and ethically acceptable.19–25 Sheep models of osteoarthritis,20 internal derangement,21 and ankylosis22–25 have been developed. The aim of this study was to investigate the shortterm effect of costochondral grafts for condylar replacement in an otherwise normal sheep TMJ.
INTRODUCTION Costochondral grafts are indicated in TMJ reconstruction for ankylosis, facial asymmetry, and the replacement of diseased mandibular condyles.1 Clinically, they have been extensively used for congenital dysplasias, ankylosis, osteoarthritis, trauma, and the replacement of the condyle after resection of a tumour. They resulted in restoration of jaw function and restore the growth potential of the mandible.2–5 Despite the favourable anatomical and adaptive characteristics of the graft, there are a number of well-known complications associated with costochondral grafting, including infection, fracture of the costochondral junction, pain, resorption, and mandibular overgrowth in children.6–11 We know of few experimental animal studies of costochondral grafts.12–16 Experimental studies of 17 young cynomolgus (Macaca irus) monkeys that were observed for 3 years showed that the costochondral junction changed little in the forward and vertical positions, and cartilaginous elements could still be identified on the surface of the transplant.12 Experimental studies in 20-day-old rats that were observed for 20 days showed that the grafts continued to grow posteriorly and 189
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British Journal of Oral and Maxillofacial Surgery
MATERIALS AND METHODS Five pure-bred adult Merino sheep, aged about 2 years and weighing roughly 55 kg were used. All right joints were operated on and all left joints were served as control. Anaesthesia was induced with intravenous injection of thiopentone sodium 500–1000 mg into the external jugular vein. The sheep were intubated and anaesthesia maintained with a mixture of 3% halothane and oxygen, and nitrous oxide through an orotracheal tube. Their jaw movements were measured vertically and laterally. The right preauricular area and the right side of the chest were shaved and prepared with povidone iodine, and the field was isolated with sterile drapes. A 6-cm skin incision was made over the 13th rib on the right side. The costochondral bone with perichondrium A
was harvested from the 13th rib to a length of 70 mm (Fig. 1). This wound was closed primarily. A 4-cm vertical preauricular skin incision was made over the lateral capsule of the right TMJ. The inferior joint space was then opened by a horizontal incision through the joint capsule. The condylar head was excised at a measured 10 mm from the condylar articular surface with a fissure bur. The disc was preserved. To fit the graft, the postero-lateral margin of the mandibular ramus was reduced to half in thickness. The rib was trimmed until there was a 26-mm bony and 2-mm cartilaginous component. The periosteum of the costochondral bone was retained except for its contact surface with the mandibular ramus. The graft was placed in the joint space projecting 8 mm above the resection of the articular process and fixed in 2 places (superior and inferior to the mandibular ramus) with a 0.5-mm metal wire (Fig. 2). Debris was removed by irrigation and suction, and then the overlying tissues were repaired in layers. Just after the operation, the jaw movements were measured vertically and laterally. Benzyl penicillin 400 mg and streptomycin sulphate 500 mg were given intramuscularly twice daily for 2 days. The sheep were managed in a covered animal house for a week and then kept in a field. Their weight was monitored and recorded every week until they were killed three months after the operation with an overdose
B
Fig. 1 (A) The right 13th rib of a sheep (scale in mm). (B) Histological section of the 13th rib of sheep (haematoxylin and eosin stain, original magnification3.2). The cartilaginous tissue consists of hyaline cartilage, and the bone tissue consists of a thin cortical layer with cancellous marrow. (H:hyaline cartilage).
Fig. 2 Intra-operative appearance. The rib bone was placed and fixed in two places with an 0.5 mm metal wire. (R:rib bone, M:mandibular ramus, arrow:disc).
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Table 1 Criteria and score for radiological assessment23–25 Score Items
Criteria
Shape
Change of a joint form Concavity in the cortical plate of a joint surface with an indistinct outline Cortical thickening of a joint surface
Erosion
Sclerosis
Marrow Calcification
Change of underlying trabecular bone Development of calcification across the joint space
0 (No change)
1 (Mild change)
2 (Moderate change)
3 (Severe change)
May include reformed joint
Destruction
Multiple osteophytes
In a third of the surface of the joint
In two-thirds of the surface of the joint
Outgrowth (marginal proliferation) All over surface of the joint
Sclerosis in a third of the surface of the joint
Sclerosis in two-thirds of the surface of the joint
Sclerosis over all surface of the joint
Atrophy or absorption In a third of joint space
Sclerosing change in half of marrow In two-thirds of the joint space
Sclerosing change whole marrow Bony fusion across the joint space
This stage in all items includes normal joint and recent surgical intervention
No calcification
with pentothal. Just after death, the occlusal relation and the range of jaw movements were recorded. Immediately, the joints area were removed en bloc with a band-saw and fixed in 10% neutral buffered formalin. The TMJs were radiographed laterally and anteroposteriorly under standardized conditions, and the features assessed according to the criteria listed in Table 1.23–25 The morphological features of shape, erosion, and sclerosis were investigated for both the condylar and the temporal surfaces, and calcification was scored for the joint space in both radiographs. Changes in the marrow were scored on the temporal surface of the anteroposterior radiographs and in the condyles of both radiographs, with a range of 0 for normal to 3 for gross deviation. A maximum score of 51 could therefore be assigned to a joint. The specimens were decalcified with 9.5% hydrochloric acid, and 1% sodium acetate over saturated EDTA. The TMJs were then divided into three blocks (lateral, central, and medial segments), histologically prepared and stained with haematoxylin and eosin. The histological findings were assessed macroscopically and microscopically. Each slide was assessed at its anterior, central, and posterior aspects, so the joint was divided into nine zones. The histological degree of fibrous ankylosis in the joint spaces was scored in each zone (Table 2).22 The maximum thickness of the temporal bone surface, including the cartilaginous layer and the disc, were also measured in each zone. Scheffe’s F method of one-way analysis of variance (ANOVA) was used to compare the range of jaw movements over time. The Mann–Whitney U test was used to compare the differences in the radiological and histological scores, and the thickness of the temporal bone surface
Table 2 Stage and score for degree of fibrous ankylosis22 Stage 1 2 3 4 5 6
Score
Degree of ankylosis (%)*
0 1 2 3 4 5
0† 1–25‡ 26–50 51–75 76–99 100
* The degree of fibrous ankylosis shows the percentage of connective tissue in the joint space. This tissue may be fibrous tissue, cartilage, or bone. † Includes normal joint, the costal cartilage, and reaction to operation. ‡ May include an osteoarthrotic joint with adhesion.
including the cartilaginous layer and the disc between the experimental and control joints. Probabilities of 0.05 or less were accepted as significant. This experiment was approved by the Ethics Committee of the University of Adelaide.
RESULTS The changes in body weight are shown in Table 3. Each individual sheep marginally increased its body weight over the 3-month period. No malocclusions developed in any sheep. The ranges of jaw movements are shown in Table 4. There were some minor individual variations. The vertical movements increased in 3 of the 5 sheep and decreased in 2. The right lateral movements increased in 3 of the 5 sheep, one decreased and the other remained unchanged. The left lateral movements increased in
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British Journal of Oral and Maxillofacial Surgery Table 3 Body weight (kg) Sheep
Pre operatively
At the time of death
1 2 3 4 5 Mean
48.0 55.0 56.5 54.5 49.5 52.7
52.5 57.0 66.0 60.0 56.0 58.3
A
Table 4 Mean (SD) range of jaw movements in 5 sheep (mm)
Vertically Right Left
Preoperative
Immediately postoperatively
At the time of death
54.2 (5.3) 39.0 (1.4) 39.2 (1.3)
54.4 (5.3) 39.2 (1.3) 39.6 (0.5)
52.8 (8.0) 42.0 (4.6) 35.6 (6.1)
B
There was no significant difference between the groups.
1 of 5 sheep but decreased in the others. There were no significant differences between the groups at any time. Radiologically, radiolucent gaps were maintained between the temporal bone and the graft in all joints operated on (Fig. 3). The temporal articular surface was unchanged. In 4 of the 5 joints operated on, the graft looked like a normal condyle. In the remaining animal, there was moderate hyperosteosis. The mean (SD) radiological scores of the experimental joints was 8.8 (3.8) and of the control joints 1.4 (0.5). This difference was significant (P 0.01). Macroscopically, all grafts were well attached to the mandibular ramus. In all experimental joints, the inferior joint space showed fibrous adhesions between the graft and disc. However, partial clefts were present in all joints, so there was a partial inferior joint space. The superior joint space was maintained all joints. One of 5 TMJs had a perforation of the anterior part of the disc. No changes were found in the temporal articular bone in any specimen. In 2 of 5 lateral and central parasagittal planes, the graft had hyperosteosis beyond the glenoid fossa posteriorly. The medial and central parasagittal planes showed mild hyperplasia within the confines of the fossa. Histologically, all grafts were covered by fibrous connective tissue or fibrous cartilage, or both (Fig. 4). There was an irregular chondrocyte hyperplasia under the fibrous cover, and a proliferation of chondrocytes at the cartilage-bone junction. However, the graft had taken on the structure of the condylar head and no longer looked like a costochondral graft. The surface of the temporal bone was significantly thicker in the experimental than the control joints (Table 5) (P0.0001). In the parasagittal and coronal planes, all were thicker than those of controls (P0.05).
Fig. 3 Radiographs of normal TMJ and one that has been operated on after three months (right). (A) Normal TMJ. The articular surfaces are smooth (T:temporal bone, C:condyle). (B) TMJ that has been operated on. The temporal articular surface was smooth and the head of the costochondral graft looked like a normal condyle. (T:temporal bone, CG:costochondral graft).
Central–lateral, central–central, and all anterior zones of the discs were thinner in the experimental, than in the control joints (Table 6), but not significantly so (P:0.7). The histological rating on the degree of ankylosis scale is shown in Table 7. The mean score of a zone in a joint was 2.2 (range 1–3) in experimental joints and 0.5 (range 0–1) in control joints (P0.001). The control joints were largely unaffected radiologically but one joint showed temporal and condylar flattening in the radiograph and histologically this joint had an increase in the cartilaginous layer. However, these changes were consistent with minor remodelling and were not pathological.
DISCUSSION This study shows that a costochondral graft after condylectomy with the preservation of the normal disc
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C
B
Fig. 4 Results for 4 of 5 joints. The histological section of the normal TMJ and one that has been operated on after three months (right). (A) Photomicrograph of a normal TMJ. (Haematoxylin and eosin stain, original magnification 2) (left/lateral parasagittal section). The articular surface is covered by cartilage. The joint space, which consists of superior and inferior joint spaces, is separated by the disc. (T:temporal bone, D:disc, C:condyle). (B) Photomicrograph of a TMJ that has been operated on. (Haematoxylin and eosin stain, original magnification1.4) (right/central parasagittal section). The graft took on the appearance of a condylar head. The inferior joint space shows partial fibrous adhesion between the condylar-like graft and the disc. The superior joint space is maintained. (T:temporal bone, D:disc, CG:costochondral graft) (C) Photomicrograph of TMJ postoperatively. (Haematoxylin and eosin stain, original magnification12.8) (right/central parasagittal section). At the cartilage-bone junction the parallel columns of chondrocytes are seen and the graft head is covered with the fibrous cartilage. (D:disc, H:hyaline cartilage, FC:fibrous cartilage).
allowed formation of a new condyle within 3 months. This is consistent with other experimental studies.12,13,16 An experimental study of young cynomolgus monkeys12 reported that the cartilage cells seemed disorderly, hyperplastic, and degenerate. In an experimental study using juvenile monkeys,14 the graft remained unchanged and did not respond to its new environment, so the graft was described as an inadequate replacement for the cartilage of the growing mandibular condyle. In a previous experimental study in sheep, in which condylectomy was done in young adult sheep, a similar condylar head almost completely reformed by remodelling. It was covered with fibrous tissue and the cartilage layer reformed similar to a normal condylar head. The inferior joint space had adhesions, in almost all joints operated on.26 However, in this experimental study, the graft took on the appearance of a condylar head and the cartilage layer
clearly showed hyperplastic activity. These reactions resembled a costochondral graft in the TMJ found in previous experimental studies.12,26 One sheep, which showed temporal and condylar flattening in the radiograph, showed an increase in the cartilage layer histologically on the control side. We suggest that this reaction is related to the bone proliferation beyond the glenoid fossa on the experimental side. This histological change was similar to the reaction to experimental disc perforation in sheep TMJ.21 It indicates a change in biomechanics with an abnormal graft resulting in adaptive changes on the opposite side. The temporal bone surface including the cartilage layer of the experimental joints was also thicker than that on the control side. Although the disc was thinner, it was not significantly so. The jaw movements were not affected despite the adhesions in the inferior joint space. The sheep could chew effectively as their body weight increased over the
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British Journal of Oral and Maxillofacial Surgery Table 5 Mean (SD) thickness of the temporal articular surface including the cartilage layer in 5 sheep (mm) Medial* Operate on *
Anterior Central* Posterior*
0.3 (0.2) 0.5 (0.5) 0.2 (0.1)
Central*
Control 0.2 (0.1) 0.1 (0.04) 0.2 (0.1)
Lateral*
Operated on
Control
Operated on
Control
0.3 (0.2) 0.3 (0.2) 0.3 (0.2)
0.1 (0.1) 0.2 (0.1) 0.1 (0.04)
0.2 (0.1) 0.3 (0.2) 0.3 (0.1)
0.2 (0.01) 0.1 (0.1) 0.1 (0.02)
Overall differences between the experimental and the control joints: P0.0001. Differences between the operated on and the control joints: *P0.05.
Table 6 Mean (SD) thickness of the disc in 5 sheep (mm) Medial
Central
Lateral
Operated on
Control
Operated on
Control
Operated on
Control
1.6 (0.3) 1.1 (0.4) 1.8 (0.5)
1.7 (0.3) 0.8 (0.3) 1.4 (0.2)
1.1 (0.5) 0.7 (0.4) 1.9 (0.6)
1.5 (0.2) 0.8 (0.1) 1.9 (0.2)
1.4 (0.7) 0.7 (0.4) 2.0 (0.3)
1.5 (0.2) 0.7 (0.4) 1.7 (0.2)
Anterior Central Posterior
There were no significant differences between the groups.
Table 7 Median (range) histological scores of the degree of fibrous ankylosis in 5 sheep Joint operated on*
Medial
1.6† (1–3) 1.8† (1–2) 1.6† (1–3)
Anterior 2.2‡ (1–4) 3.0† (1–4) 2.8† (2–4) Posterior
2.6‡ (2–3) 2.8‡ (2–3) 2.0‡ (1–3)
Joint not operated on*
Lateral
Medial
0.8† (0–1) 0.6† (0–1) 0.2† (0–1)
Anterior 0.4‡ (0–1) 0.8‡ (0–1) 0† (0) Posterior
0.4‡ (0–1) 0.8‡ (0–1) 0.2‡ (0–1)
Lateral
*P0.001; †P0.05; ‡P0.001.
3 months, so the graft had been stabilized both functionally and histologically within the sheep TMJ. This study could be criticized because of the relatively short duration of 3 months. There are many reasons for this. Sheep chew virtually continuously and with great force, so three months of jaw function in a sheep is equivalent to several years of jaw function in a human. For this reason, the Japan/Australia TMD study group settled on 3 months as our standard time duration for experiments.19–25 This study shows the behaviour of costochondral grafts in normal joints; future studies will look at their use in progressively more diseased joints including those with ankylosis.
ACKNOWLEDGEMENTS We thank Dr G. Kinoshita (Assistant Professor, Department of Orthopaedic Medicine, Hyogo College of Medicine, Japan) for his
advice on costochondral grafts in sheep, and the Australian Dental Research Foundation Inc. for financial support.
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Costochondral grafts in reconstruction of the TMJ after condylectomy 7. Tasanen A, Leikomaa H. Ankylosis of the temporomandibular joint of a child. Report of a case. Int J Oral Surg 1977; 6: 95–99. 8. Ware WH, Brown SL. Growth centre transplantation to replace mandibular condyles. J Maxillofac Surg 1981; 9: 50–58. 9. Obeid G, Guttenberg SA, Connole PW. Costochondral grafting in condylar replacement and mandibular reconstruction. J Oral Maxillofac Surg 1988; 48: 177–182. 10. Munro IR, Philips JH, Griffin G. Growth after construction of the temporomandibular joint in children with hemifacial microsomia. Cleft Palate 1989; 26: 303–311. 11. Peltomaki T, Isotupa K. The costochondral graft. A solution or a source of facial asymmetry in growing children. A case report. Proceedings of the Finnish Dental Society 1991; 87: 167–176. 12. Ware WH, Taylor RC. Cartilaginous growth centers transplanted to replace mandibular condyles in monkeys. J Oral Surg 1966; 24: 33–43. 13. Poswillo D. Experimental reconstruction of the mandibular joint. Int J Oral Surg 1974; 3: 400–411. 14. Daniels S, Ellis ED, Carlson DS. Histologic analysis of costochondral and sternoclavicular grafts in the TMJ of the juvenile monkey. J Oral Maxillofac Surg 1987; 45: 675–683. 15. Peltomaki T. Growth of a costochondral graft in the rat temporomandibular joint. J Oral Maxillofac Surg 1992; 50: 851–857. 16. Perrott DH, Vargervik K, Kaban LB. Costochondral reconstruction of mandibular condyles in nongrowing primates. J Craniofac Surg 1995; 6: 227–237. 17. Sisson S. The Anatomy of the Domestic Animals, 4th ed. Philadelphia: WB Saunders, 1953: 157. 18. May NDS. The Anatomy of the Sheep, 3rd edn. Queensland: University of Queensland Press, 1970: 43. 19. Bosanquet AG, Goss AN. The sheep as a model for temporomandibular joint surgery. Int J Oral Maxillofac Surg 1987; 16: 600–603. 20. Ishimaru J-I, Goss AN. A model for osteoarthritis of the temporomandibular joint. J Oral Maxillofac Surg 1992; 50: 1191–1195. 21. Bosanquet AG, Ishimaru J-I, Goss AN. Effect of experimental disc perforation in sheep temporomandibular joints. Int J Oral Maxillofac Surg 1991; 20: 177–181. 22. Miyamoto H, Kurita K, Ishimaru J-I, Goss AN. A sheep model for temporomandibular joint ankylosis. J Oral Maxillofac Surg 1999; 57: 812–817. 23. Miyamoto H, Kurita K, Ogi N, Ishimaru J-I, Goss AN. Experimental factors in the genesis of temporomandibular joint ankylosis. Int J Oral Maxillofac Surg 2000; 29: 290–295. 24. Miyamoto H, Kurita K, Ogi N, Ishimaru J-I, Goss AN. The role of the disk in sheep temporomandibular joint ankylosis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1999; 88: 151–158.
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25. Miyamoto H, Kurita K, Ogi N, Ishimaru J-I, Goss AN. Effect of limited jaw motion on ankylosis of the temporomandibular joint in sheep. Br J Oral Maxillofac Surg 2000; 38: 148–153. 26. Miyamoto K, Hirakawa T, Ishimaru J-I, Kurita K, Vickers R, Goss AN. The effect of unilateral condylectomy on the sheep temporomandibular joint. Br J Oral Maxillofac Surg 1999; 37: 401–404.
The Authors H. Matsuura DDS Visiting Research Fellow Oral and Maxillofacial Surgery Unit Dental School, The University of Adelaide, Adelaide, South Australia; Instructor, The First Department of Oral and Maxillofacial Surgery School of Dentistry, Aichi-Gakuin University Nagoya, Japan H. Miyamoto DDS, PhD Staff, The First Department of Oral and Maxillofacial Surgery School of Dentistry, Aichi-Gakuin University Nagoya, Japan; Formerly Visiting Research Fellow Oral and Maxillofacial Surgery Unit Dental School, The University of Adelaide, Adelaide, South Australia J.-I. Ishimaru DDS, DMD Chief Department of Oral-Maxillofacial Surgery and Stomatology Gifu Prefectural Gifu, Hospital, Gifu, Japan K. Kurita DDS, PhD Professor and Director, The First Department of Oral and Maxillofacial Surgery School of Dentistry, Aichi-Gakuin University Nagoya, Japan A. N. Goss DDSc, FRACDS, OMS, FICD Professor and Director Oral and Maxillofacial Surgery Unit Dental School, The University of Adelaide Adelaide, South Australia Correspondence and requests for offprints to: Dr H. Matsuura, The First Department of Oral and Maxillofacial Surgery, School of Dentistry, Aichi-Gakuin University, 2-11 Suemori-dori, Chikusa-ku, Nagoya 464-8651, Japan. Tel: ;81 52 759 2157; Fax: ;81 52 759 2157; E-mail: [email protected] Accepted 23 January 2001