Discectomy of the temporomandibular joint: an experimental study in monkeys

Journal of Cranio-Maxillofacial Surgery (1999) 27, 113 116 © 1999 European Association for Cranio-Maxillofacial Surgery

Discectomy of the temporomandibular joint: an experimental study in monkeys Tore Bjornland, Hans R. Haames

Department of Oral Surgery and Oral Medicine, Faculty of Dentistry, University of Oslo, Oslo, Norway SUMMARY. Postoperative changes have been observed in the temporomandibular joint (TMJ) after discectomies. Animal models have often shown that interventions in the TMJ may heal uneventfully. Discectomies were performed on 14 Macaeafascicularis and macroscopic and microscopic examination performed after sacrifice of the animals. Two of the animals did not show any apparent macroscopic or microscopic changes. The remaining 12 joints showed minor to major changes. The most serious changes were seen in three joints with fibrous ankylosis and five joints showed marked destruction of the articular cartilage.

INTRODUCTION

Laboratory in Stockholm were chosen for the study because of the close similarity to the human TMJ and the fact that these animals had been chosen for other investigations (Haanceset al., 1987). A great effort was made to make the study as stress-free as possible for the animals. The animals were closely observed postoperatively for any discomfort. The ethical committee approved the study. According to the classification of Bowen and Cock (1970) all monkeys were determined to be at least 48 months of age. The animals were in good condition, and had been kept in quarantine for several months prior to the experimental procedure. They were kept in cages, singly or in pairs and fed a standard diet of pellets and fresh fruit. The animals weighed from 1970-3100 g. In all animals, discectomy in the left TMJ was performed via the pre-auricular approach, as in humans. The procedures were performed under i.v. anaesthesia (Nembutal, Abbot). In all but one animal the disc was removed easily. In one of the animals the disc was difficult to remove because the condyle had a more bifid configuration, thus making the dissection of the disc more difficult. The animals were observed postoperatively for 3 h until full recovery. The animals were allowed to drink on the first postoperative day and thereafter put on a soft diet for the next 14 days, and after that on a regular chewing diet. The animals were sacrificed 6 months after the surgery with an overdose of barbiturate. After sacrifice, the heads were dissected and the condylar head and the articular fossa were inspected for macroscopic changes. The areas for histological examination were the same in all joints and included 5 mm thick sections of the articular fossa and the condyle. The right TMJ was also dissected after the sacrifice and served as a control. The control sides were also prepared in the same way for macroscopic and microscopic examination. All specimens were immediately fixed in 10% buffered formalin solution. The specimens were further embedded in paraffin wax and sectioned at 6 gm

Discectomy has been widely used as a treatment for internal derangement of the temporomandibular joint (TMJ). (Eriksson and Westesson, 1987, 1992; Goss, 1993a; Holmlund et al., 1993). Postoperative changes have often been observed in joints after discectomy (Gundlach, 1990; Eriksson and Westesson, 1992; Trumpy and Lyberg, 1995). However, improvement in mandibular function and decrease in symptoms from the masticatory system have been reported (Eriksson and Westesson, 1987, 1992; Holmlund et al., 1993; Bjornland and Larheim, 1995). Different techniques have been used to avoid postoperative changes in the TMJ such as discoplasty and replacement of the disc with various implants or autogenous grafts (Lindqvist et al., 1986; Meyer, 1988; Gundlach, 1990; Eriksson and Westesson, 1992; Goss, 1993a, 1993b; Trumpy and Lyberg, 1995). However, MRI studies have failed to show long-term reduction of the disc-repair (Westesson et al., 1991; Trumpy and Lyberg, 1995) and adverse reactions to implant materials have been described (Westesson et al., 1987; Trumpy and Lyberg, 1995; Trumpy et al., 1996). Animal models have been used to investigate the postoperative changes in the TMJ after different surgical procedures (Holmlund et al., 1986; Block et al., 1988; Block and Bouvier, 1990; Ishimaru and Goss, 1992; Bjornland et al., 1994; Feinberg and McDonnell, 1995; Ogi et al., 1997). But due to the highly variable reactions to surgical interventions among the different species, these results may not be directly applicable to man. The aim of this study was to evaluate the postoperative changes after discectomy of the TMJ in an animal study.

MATERIAL AND METHODS Fourteen Macaca fascicularis belonging to the vivarium of the Swedish National Bacteriological 113

114 Journalof Cranio-MaxillofacialSurgery

Fig. 1 Normal TMJ of Macacafascicularis operated on contralateral joint. (A) fossa; (B) disc; (C) condyle(H&E x 32).

Fig. 2 - Fossa (A), condyle(C) and joint space filledwith fibrous tissue (B) with small areas of bone-formation(arrows) in a TMJ 6 months after discectomy(H&E x 80).

Table 1 Microscopicfindings at autopsy after discectomiesin I4 Macacafascicularis (n=number &joints)

Fibrous ankylosis Discontinuity of cartilage Increased thickness of cartilage Synovialhyperplasia Fibrous tissue in fossa Fibrous tissue on the condyle Remodellingof bone Osteophytes

3 8 4 7 2 4 7 5

and stained with haematoxylin and eosin (H&E) and haematoxylin, apophloxin and saffron (HA&S).

Fig. 3 Condyle(bottom) with increasedthickness of the cartilage covering(arrowheads)and fossa (top) with fibrous covering(a), secondarycartilage (b) and bone (c) in a TMJ 6 months after discectomy(H&E x 80).

RESULTS

Clinical findings All the animals recovered well after the interventions without any apparent problems. They all seemed to chew their regular diet well and all but one gained weight during the postoperative period. On inspection all the incisions had healed well. Two of the animals seemed to have reduced mobility of the mandible with deviation towards the operated side.

Morphological Findings The unoperated joints showed no macroscopic or microscopic changes in any of the animals (Fig. 1). The macroscopic findings in 12 operated joints all showed slight variations from the normal joints. In seven joints the macroscopic changes were more evident. Three of the joints had a marked reduction in the joint space, indicating fibrous ankylosis. Two condyles were slightly flattened and two had slightly irregular surfaces. One joint had a rather evident disc remnant in one part of the joint. This last joint exhibited several

small osteophytes along the dorsal part of the condyle. In another four joints there was no evidence of remaining cartilage on the condyle or fossa. The microscopic findings are summarized in Table 1. Two of the joints did not show any apparent microscopic changes. In the remaining 12 joints varying microscopic changes were seen. The most serious changes were seen in three animals with development of fibrous ankylosis. Here the cartilage lining of the fossa and condyle were absent, with formation of fibrous tissue and small areas of newly formed bone (Fig. 2). In another five joints no cartilage was seen on the articulating bony surfaces. These changes were, in all but one, mostly prominent on the condyle. In another four animals the cartilage covering of the condyle showed increased thickness compared with the unoperated side (Fig. 3). The synovial lining was present in all joints but with hyperplastic areas in seven joints. Except for the synovial hyperplasia, no inflammatory cells were seen. At the condyle and fossa, cell-poor fibrous tissue was seen in six joints.

Discectomyof the temporomandibularjoint 115

Fig. 4 Bonemarrowinterspersedwith fat cells (arrowheads)in a condyle6 months after discectomy(H&E x 80).

The hard tissue changes consisted of remodelling of the condyle and fossa in seven cases. The bone marrow seemed to be more interspersed with fat cells than in the unoperated joints (Fig.4). In five joints, bony projections resembling osteophytes were found with three at the anterior border and two at the posterior part of the condyle.

DISCUSSION The present study clearly showed that marked postoperative changes may occur after discectomy in the Macaque fascicularis TMJ. These findings are in agreement with other studies with intervention on the TMJ in animals (Helmy et al., 1988; Ishimura and Goss, 1992; Bjornland et al., 1994; Mills et al., 1994). The findings of degenerative changes in the TMJ contrast, however, with the conclusions of other studies (Kurita et al., 1990a, 1990b; Lekkas, 1994) where no histopathological changes were seen after surgical opening of the TMJ capsule. The use of animals for the purpose of investigations has always to be thoroughly considered, for ethical reasons. In animal studies using rabbits and rats, the healing capacity of these animals may give uneventful healing but conclusions of most favourable results are not directly applicable to man (Holmlund et al., 1986; Kurita et al., 1990a; Lekkas, 1994; Feinbergand McDonnell, 1995). The presence of fibrous ankylosis in three joints after discectomy is a rather uncommon finding in human material. This may be caused by the lack of mandibular exercise advocated after TMJ surgery in humans. The discontinuity of cartilage in the fossa and condyle, may be due to instrumentally caused defects or a sign of osteoarthritis or osteoarthrosis as seen in man (Blackwood, 1963) and some animals (Helmy et al., 1988; Block and Bouvier, 1990; Ellis and Hinton, 1991; Macher et al., 1992;). Another explanation for the loss of cartilage may be the texture of the

diet, as suggested by Block et al. (1988) and Block and Bouvier (1990). The animals in this study had no dietary restrictions after the first 14 days postoperativeIy. Fibrous tissue formation in the fossa and condyle may be an attempt at repair of defects on the articular surfaces or a sign of osteoarthrosis as described by Bjornland and Refsum (1994). In four of the joints increased thickness of the articulating cartilage was seen. This corresponds well with the observations of Hansson et al. (1992) on the TMJ after discectomy, where the space between the condyle and glenoid fossa was interpreted on magnetic resonance imaging as thickened articular cartilage. The synovial hyperplasia found in seven of the joints may originate from blood clots formed in the joint after the surgery as a similar reaction to hyperplastic tissue formation seen in disc-displacement (Isberg et al., 1986) and reported in a study of discdisplacement in monkeys (Helmy et al., 1988). The microscopic findings of remodelling of bone and osteophytes in seven and five joints respectively may be described as the classical findings of osteoarthrosis (Doherty et al., 1993) or a remodelling process because of altered biomechanical properties of the joint after discectomy (Eriksson and Westesson, 1985). Remodelling of the bone has also been reported in other animal studies (Helmy et al., 1988; Ellis and Hinton, 1991). The lack of inflammatory cells is not surprising, because osteoarthrosis is mainly a degenerative disease, and that only biochemical examination may indicate an inflammatory response (Axelsson et al., 1992; Doherty et al., 1993; Shafer et al., 1994; Flygare et al., 1997; Sandler et al., 1998). Such examinations were not performed in our study. This study has shown that experimental discectomies may cause osteoarthritis and osteoarthrosis after 6 months in the Macaca TMJ. The extent of the microscopic changes in the TMJ was variable, with apparently minor changes in seven and more extensive changes in another seven of the TMJs. The reason for the variations is not clear but these findings are in agreement with the findings of postoperative changes after discectomies in man (Eriksson and Westesson, 1985, 1987; Holmlund et al., 1993). The relatively immediate function of the TMJ in our study may have had an adverse effect, but intermaxillary fixation in monkeys may also produce histopathological changes as described in a previous study (Ellis and Hinton, 1991). The results of this study indicate that discectomy may have a detrimental effect on the TMJ. Surgical intervention by discectomy, therefore, has to be thoroughly followed up postoperatively and the possible adverse reactions such as fibrous ankylosis or osteoarthrosis have to be taken into consideration before the decision to perform discectomy is taken.

116 Journal of Cranio-Maxillofacial Surgery

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Associate Professor Tore Bjornland Department of Oral Surgery and Oral Medicine Faculty of Dentistry UnNersity of Oslo Geitmyrsveien 71 N-0455 Oslo Norway Tel: +47 22852229 Fax: +47 22852341 Paper received 21 October 1998 Accepted 9 February 1999