Surg Radiol Anat (2005) 27: 51–55 DOI 10.1007/s00276-004-0289-0
O R I GI N A L A R T IC L E
G. Toure´ Æ C. Duboucher Æ C. Vacher
Anatomical modifications of the temporomandibular joint during ageing
Received: 8 July 2003 / Accepted: 21 May 2004 / Published online: 23 November 2004 Springer-Verlag 2004
Abstract It is essential to know the normal and pathological changes of ageing in the temporomandibular joint (TMJ) because of the frequency of pathology in this joint and the increased duration of life in current populations. A study was done on 70 TMJs harvested from 35 subjects older than 75 years. These joints were studied macroscopically, radiologically and histologically. Degenerative pathology of the TMJ affected more than 50% of the subjects studied and the disc was perforated in 7%. Ageing of the TMJ without any degenerative pathology is marked by radiographic signs which are not specific to the TMJ (cortical thinning, demineralisation). Histologically, amyloid degeneration was present in nearly 50% of TMJs studied. Keywords Temporomandibular joint Æ Ageing Æ Osteoarthritis Æ Anatomy
Introduction The temporomandibular joints (TMJs) link the mandible to the base of the skull, from which they are suspended. They are essential to occlusion and are a
G. Toure´ Æ C. Vacher (&) Faculte´ Bio-me´dicale des Saints-Pe`res, Institut d’Anatomie de Paris, 45 rue des Saints Pe`res, 75005 Paris, France E-mail:
[email protected] Tel.: +33-1-40875671 G. Toure´ Service de Chirurgie Maxillo-Faciale et Stomatologie, Centre Hospitalier Intercommunal de Villeneuve-Saint-Georges, Paris, France C. Duboucher Service d’Anatomie Pathologique, Centre Hospitalier de Saint Germain en Laye, Paris, France C. Vacher Service de Chirurgie Maxillo-Faciale et Stomatologie, AP-HP, Hoˆpital Beaujon, 100 boulevard Ge´ne´ral Leclerc, 92118 Clichy Cedex, France
part of the masticatory apparatus [11]. They are condylar joints with an articular disc separating the joint line into compartments: a superior temporodiscal compartment and an inferior condylodiscal compartment. Numerous studies have allowed definition of the anatomical characteristics of this joint and the manifestations of osteoarthritis [5]. According to Dijkgraaf et al., osteoarthritis shows itself early by cellular (increased chondrocyte activity) and biochemical (increased DNA synthesis) signs before the appearance of macroscopic signs (swelling then thinning and even necrosis of the cartilage) and clinical signs (pain then functional restriction) [5]. Most authors who have studied the TMJ in the elderly found macroscopic perforations of the articular disc, radiographic signs of progressive arthrosis (bony erosions, osteophytes, geodes) and, histologically, thinning of the cartilage and osteosclerosis in highly variable proportions of subjects [1, 2, 4, 12], but the modifications due to ageing of the different constituent elements of the joint are little known. We have, therefore, done a study of the macroscopic radiographic and histological anatomy in 35 subjects (70 joints) older than 75 years, the aim of which was to determine the frequency of anomalies of the TMJ related to ageing and the frequency of osteoarthrosis of the TMJ.
Materials and methods The two TMJs were harvested from 35 formalin-preserved cadavers aged between 76 and 106 years (average 91.8±4.69 years). The sex ratio was 23 women to 12 men. The dental formula was systematically noted for each subject as well as the wearing of a dental prosthesis and its type (mobile, fixed, maxillary, mandibular). The harvesting was done through a lateral approach through a pre-tragal incision extended at its superior extremity by a horizontal incision over the zygomatic arch. The mandibular fossa, the articular tubercle of the temporal bone, the condylar process of the mandible
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and the articular disc were harvested in a block using a saw and an osteotome. Macroscopic examination of the different specimens harvested was done to look for alterations in the different articular surfaces. All the specimens harvested had anteroposterior and lateral radiographs taken using Kodak intra-oral films (Extra Chrome Ultraspeed) with a Phillips Dens-O-Mat (voltage 65 kV; exposure 0.18 s at 7.5 mA). Any signs of bony ageing (demineralisation, narrowing of the bony cortices) and the signs of osteoarthrosis (geodes, erosions, flattening of the condylar process, osteophytes) were systematically noted. All the pieces were then fixed in 10% formalin, decalcified (Merck decalcifying mixture), embedded in paraffin using an automated embedder, sectioned in 5 lm semi-serial parasagittal cuts, and stained with haematoxylin-eosin-saffron. In order to demonstrate amyloidosis of the articular disc, Congo red staining with examination under polarised light was done. The histological lesions seen on the articular surface were classified according Dijkgraaf et al.’s description of osteoarthritis [5]. Stage Stage Stage Stage
0: 1: 2: 3:
normal joint swelling of the fibrocartilage thinning of the fibrocartilage necrosis of the cartilage and osteosclerosis corresponding to fibrosis of the bony marrow, thickening of the trabeculae and geode formation.
The histological lesions of the articular disc found were thinning, amyloid degeneration and discal perforation. We compared the distribution of the radiographic signs and the histological signs of osteoarthritis (stage 3) in the totally edentulous subjects and the subjects with more than 10 teeth using a corrected chi-square test [15] in order to determine whether there was a correlation between being edentulous and osteoarthritis of the TMJ.
Table 1 Macroscopic and radiological study of the 70 temporomandibular joints (TMJs) harvested
Discal perforation Radiological ageing Geode or ulceration Narrowing or osteophyte
No. of TMJs
Percentage
5 46 12 20
0.1% 66% 17% 29%
Macroscopic analysis The position of the disc was normal in all cases after harvesting of the joint. Macroscopic examination of the disc showed (Table 1): discal perforation in 3 subjects (bilateral in 2 cases) and discal erosion without perforation in 2 subjects (bilateral in 1 case). Perforations and erosions were all visible in the intermediate part of the disc at the level of its lateral region (Fig. 1). All cases of discal perforation were associated with irregularity of the articular surface of the condylar process and in one case the prominence of the articular tubercle had totally disappeared. Radiographic analysis The articular disc appeared abnormally calcified (Fig. 2) bilaterally in one case. The articular surfaces in 7 subjects were free of radiographic anomalies and in 12 subjects had signs of ageing such as demineralisation and thinning of the cortices. Amongst these 12 subjects, the signs of ageing were bilateral in 6. In 16 subjects, the articular surface had radiographic signs of osteoarthrosis, geodes, erosions, osteophytes (Fig. 3) or joint narrowing (Table 1). Amongst these 16 cases, the signs were bilateral in 6. Of the 70 TMJs studied, the temporal and mandibular articular surfaces were normal in 24 cases (34%),
Results Analysis of the dental formula Fourteen subjects were totally edentulous, of whom four had a total maxillary and mandibular prosthesis. The 16 other subjects were partially edentulous. The total number of teeth present varied from 4 to 29. Ten subjects had fewer than 10 teeth, three between 11 and 20 teeth and 3 more than 20 teeth. The frequency of the radiological and histological signs of osteoarthritis was compared in the totally edentulous subjects and subjects with more than 10 teeth. The corrected chi-square test for small numbers was 1.84 (nonsignificant) for the radiographic signs of osteoarthritis and 1.68 (nonsignificant) for the histological signs of osteoarthrosis (stage 3).
Fig. 1 Macroscopic aspect of a right temporomandibular joint (TMJ) open in the superior compartment under the mandibular fossa (F). The disc (D) is perforated (P) laterally allowing the articular surface of the condylar process to show through
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Fig. 4 Histological section (·5 magnification) of a TMJ showing the condylar process with irregularity (I) of its surface and a flap (F) of cartilage (C) ready to detach. The cartilage completely covers the trabecular bone (T). In the upper part of the figure, the articular disc can be seen (D) Fig. 2 Lateral radiograph of a harvested TMJ. The condylar process (CP) is in contact with the articular tubercle (T). The articular disc (D) is calcified opposite the mandibular fossa (F)
showed signs of ageing without osteoarthritis in 19 cases (27%) and showed osteoarthrosis in 27 cases (39%) on radiographic study. Histological analysis Articular surfaces In 8 subjects no histological anomaly was found, in 16 subjects minor anomalies of stage 1 or 2 of articular
Fig. 3 Lateral radiograph of a harvested TMJ. The condylar process (CP) lies in the mandibular fossa (F) and behind the articular tubercle (T). An osteophyte (O) is visible at the anterior extremity of the condylar process
surfaces were seen (Fig. 4) and in 11 subjects histological signs of osteosclerosis were seen (Fig. 5). These signs were present in both articular compartments (condylar process and articular tubercle of the temporal bone) in 5 cases. They involved only the condylar process in 5 cases and only the articular tubercle of the temporal bone in one case. Osteosclerosis was unilateral in 10 of 11 cases. The osteosclerosis was always associated with the appearance of osteoid tissue. Of the 70 TMJs studied, the temporal compartment: was normal (stage 0) in 43 cases (61%), showed thinning of the fibrocartilage (stage 2) in 22 cases (31%) and had signs of osteosclerosis (stage 3) in 5 cases (12%) (Table 2). The condylar process of the 70 TMJs was classified as stage 0 in 27 cases (39%), stage 1 in 4 cases (6%), stage 2 in 30 cases (43%) and stage 3 in 9 cases (13%) (Table 2).
Fig. 5 Histological section (·5 magnification) of a TMJ showing the condylar process with signs of osteoarthritis. The sub-chondral bone (B) is exposed and shows signs of osteofibrosis. The bony repair is seen as osteoid tissue (O). Necrotic debris (N) is detached within the joint space
54 Table 2 Histological study of the temporal and mandibular surfaces of the 70 temporomandibular joints (TMJs) harvested
Stage Stage Stage Stage
0 1 2 3
Temporal compartment
Mandibular condyle
43 (61%) 0 22 (31%) 5 (12%)
27 (39%) 4 (6%) 30 (43%) 9 (13%)
Table 3 Histological study of the articular disc of the 70 TMJs harvested
Thinning Amyloidosis Perforation
Number
Percentage
14 34 5
20% 49% 7%
Looking at both the temporal and mandibular compartments together of the 70 TMJs and taking the highest stage found in either compartment, the histological lesions were classified as follows: Stage Stage Stage Stage
0: 1: 2: 3:
22 cases (32%) 4 cases (6%) 32 cases (46%) 12 cases (17%).
Articular disc The articular disc was normal bilaterally in 13 subjects, had a unilateral perforation in 5 cases which had not been seen on macroscopic examination, and had minor anomalies and thinning of the cartilage in 14 joints in 11 subjects (Table 3). Amyloidosis of the disc was present in 34 joints in 20 subjects (Fig. 6).
Fig. 6 Histological section (·25 magnification) of the articular disc (D) of a TMJ with amyloidosis (A) shown by staining with Congo red and seen under polarised light
Discussion In this study of ageing of the temporomandibular joint in 35 subjects, we have shown that over the age of 75 years, articular degeneration of the TMJ occurs in nearly half the population. In 17 of the 35 subjects we found at least one radiographic or histological sign in one or both TMJs. Only one subject had TMJs without signs of ageing or articular degeneration. We defined normal ageing as the absence of macroscopic alteration and a radiological appearance of diffuse mineralisation and bony cortical thinning. Histologically, ageing was characterised by thinning of the cartilage and amyloidosis of the articular disc. Pathological ageing, called osteoarthrosis, is marked by macroscopic anomalies such as discal perforation associated with alterations in the opposing articular surfaces, radiological anomalies such as geodes, osteophytes and narrowing of the articular surface, and histological anomalies of increasing severity up to cartilaginous necrosis and osteosclerosis of the bony surfaces. A cadaveric study such as we have done is always incomplete because it lacks clinical information. It does not allow one to know whether the subjects studied suffered from symptoms in their TMJs. However, we noted systematically the dental formula and the presence of a dental prosthesis. Our study did not demonstrate a statistical correlation between the subject being edentulous and the presence of osteoarthrosis of the TMJ. It thus confirmed the clinical and imaging studies of Holmlund and Axelsson [9] and that of Widmalm et al. on an anatomical series [18] and seems to contradict the study of Hansson et al. [8] who demonstrated in a population suffering from problems of the TMJ a strong correlation between posterior edentulation and the presence of radiographic signs of osteoarthrosis. Our macroscopic studies demonstrated 10 perforated discs out of 70 joints studied (14%), if one adds the perforations seen during macroscopic examination and those found during histological examination. This figure is clearly lower than in most other studies, since Nannmark et al. noted 14 perforations in 37 TMJs studied (41%) [12], Stratmann et al. found 27% [16] and Flygare et al. found 40% discal perforations or exposed bone on the articular surfaces [7]. However, Brussel did not find any discal perforations out of 60 discs studied [3]. We noted, as did Weisengreen, that discal perforation started in the lateral part of the articular disc [17], in contrast to Akerman et al. who noted that the perforations were preferentially in the retro-discal zone in a study of 42 TMJs [1]. Oberg et al. had previously shown that osteoarthrosis starts preferentially in the lateral part of the joint [14]. Our radiographic study demonstrated bony erosions or geodes in 12 of 70 TMJs (17%), compared with 13 of 40 TMJs (32.5%) in the study by Flygare [6]. This confirmed, however, the marked frequency of radiographic images of osteoarthrosis over 70 years of age
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(39% of TMJs studied). The histological study was done at low magnification which did not allow study of cellular changes in the cartilage but only morphological appearances. It showed that osteosclerosis was much more frequent on the condylar process. Indeed, it was nearly always affected in cases of osteosclerosis (10 of 11 cases) and most often unilaterally. These results confirmed the observations of Akerman et al. [2] and of Castelli et al. [4]. Osteosclerosis was considered as an early sign of osteoarthrosis by Norman and Bramley [13]. The presence of osteoid tissue is a marker of a process of bony repair. The most frequent histological anomaly found in the articular disc was amyloid degeneration (49%), which was demonstrated by specific stains which have not been used in other published studies on ageing of the TMJ. Our study did not show a good correlation between the radiographic and histological signs of osteoarthrosis. Histological examination concerned primarily the articular disc and the most superficial zones of the articular surfaces. It did not allow demonstration of anomalies of the whole condylar process such as was provided by the radiographs. While the histological analysis showed perfectly the cartilaginous signs of osteoarthrosis, as was well shown by Dijkgraaf et al. [5], osteoarthrosis of the TMJ may start by remodelling of the sub-articular bony tissue [7]. It therefore appears important to study the alterations in the TMJ by different methods, as has been done in this study, because the macroscopic radiological and histological definitions of osteoarthrosis are not completely superimposable even before one discusses the clinical aspects, which have not been approached in this study. The radiological/histological correlation would without doubt be better if the bony specimens had been examined by computed tomographic scanning but the overall study of the specimen by simple radiography is similar to the usual conditions of diagnosis osteoarthrosis in the elderly subject, which is most often done by a simple panoramic radiograph. Conclusion More than half of our subjects older than 75 years showed radiological manifestations of osteoarthrosis of the TMJ. Even though the temporomandibular joint is not a weight-bearing joint, the forces acting on it are considerable. In addition, it is known that osteoarthrosis affects not only the weight-bearing joints such as the hip or the knee but also the smaller joints of the hand [13], and that this involvement is linked to age [10]. Localised osteoarthritis in the TMJ affects half of people older than 75 years although it is most often unilateral and, if one believes certain clinical studies, asymptomatic [10,13]. The definition of TMJ osteoarthrosis, however,
as our study has shown, is difficult to understand and depends on the method utilised, be it clinical, macroscopic examination, radiological or histological.
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