Dentomaxillofacial Radiology (2009) 38, 141147 2009 The British Institute of Radiology http://dmfr.birjournals.

org

RESEARCH

Evaluation of the severity of temporomandibular joint osteoarthritic changes related to age using cone beam computed tomography
KE Alexiou, HC Stamatakis and K Tsiklakis*
Department of Oral Diagnosis and Radiology, School of Dentistry, University of Athens, Greece

Objectives: The aim of this study is to evaluate and correlate with age the severity of temporomandibular joint (TMJ) osteoarthritic changes using cone beam CT (CBCT). Methods: The images of 71 patients with findings of degenerative arthritis were retrieved from the computer data base. All patients had been examined with CBCT (NewTom 9000 QR-DVT). Left and right TMJs were evaluated independently for each patient. TMJ evaluation included: (a) bony changes of the condyle (flattening, erosion, sclerosis, osteophytes, resorption); (b) joint space (normal, increased, reduced, bony contact between the condyle and the mandibular fossa); and (c) bony changes of mandibular fossa (normal, sclerosis, erosion, resorption). The radiographic findings were statistically analysed. Results: Significant differences in the mean age were found: (a) between absent and moderate erosion (P 5 0.019), as well as between absent and extensive erosion (P 5 0.048); (b) between absent and extensive formation of osteophyte (P 5 0.003), as well as between slight and extensive formation of osteophyte (P 5 0.025); (c) between normal joint space and bony contact (P 5 0.0002), as well as between reduced joint space and bony contact (P 5 0.001). Conclusions: Degenerative arthritis is an age-related disease. The progression and severity of osseous changes in the condylar head and mandibular fossa are increased with age. In older age groups, patients are expected to have more frequent and severe progressive degenerative bony changes due to the development of TMJ osteoarthritis than patients in younger age groups. Dentomaxillofacial Radiology (2009) 38, 141147. doi: 10.1259/dmfr/59263880 Keywords: temporomandibular joint, osteoarthritis, cone beam computed tomography

Introduction In many cases, radiographic examination of the temporomandibular joint (TMJ) is a decisive factor for the differential and final diagnoses of several pathological conditions of the TMJ.13 Degenerative arthritis or osteoarthritis is an age-related disorder and the most common pathological condition of the TMJ. Osteoarthritic bony changes include flattening, sclerosis, the formation of osteophytes, erosion, resorption of the condylar head, erosion of mandibular fossa and reduced joint space.411 Several techniques have been used for the examination of the TMJ, such as conventional tomography,
*Correspondence to: Prof. K Tsiklakis, Perikleous 12, 15451, Neo Psychico, Athens, Greece; E-mail: ktsiklak@dent.uoa.gr Received 12 January 2008; revised 19 April 2008; accepted 29 April 2008

MRI, arthrography and CT.12,13 Recently, cone beam CT (CBCT) has been considered as an alternative imaging technique for the diagnosis of degenerative changes of the TMJ,14,15 with its major advantage over CT being the lower radiation dose.1623 The aim of this study is to evaluate and correlate with age the severity of TMJ osteoarthritic changes using CBCT.

Materials and methods 114 cases of outpatients with clinical signs and symptoms such as pain, joint sounds and irregular or deviating jaw function who had undergone a CBCT

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examination between November 2001 and July 2005 were retrieved from the computer database. A total of 71 patients with imaging characteristics of degenerative arthritis were finally selected, after filtering out patients with history of TMJ injury, rheumatoid arthritis, psoriatic arthritis, chronic juvenile arthritis and other systemic diseases, as well as patients without any imaging characteristics of osteoarthritis. Right and left TMJs were examined separately, resulting in a total of 142 TMJs that were evaluated independently. All examinations were performed by the same operator using a NewTom QR-DVT 9000 (QR s.r.l., Verona, Italy) device. In order to evaluate the condylar position in the fossa and joint space, all examinations were performed in a central occlusal relationship according to the technique described in the literature.24 Right and left TMJs were evaluated from reconstructed lateral slices perpendicular to the long axis of the condyle, coronal slices parallel to the long axis and central lateral image of the joint. In order to avoid misinterpretation, hard tissue changes had to be found in at least two consecutive slices.7 The age of the patients ranged from 20 years to 75 years and the mean age was 48.17 years. 60 (84.5%) patients were females, with a mean age of 48.09 years and 11 (15.5%) were males, with a mean age of 48.18 years. Age and gender distribution are shown in Table 1. Two experienced oral radiologists were asked to evaluate all images independently and to record the findings on a specific evaluation sheet. All images were viewed on the same monitor under the same conditions. In cases of disagreement, a second evaluation was performed by the two observers simultaneously without knowledge of the preceding recorded findings. The two observers were asked to evaluate the following imaging characteristics: (a) Osseous changes of the condyles: (1) flattening, defined as a flat bony contour deviating from the convex form; (2) erosion, defined as an area of decreased density of the cortical bone and the adjacent subcortical bone; (3) osteophytes, defined as marginal bony outgrowths on the condyle; (4) sclerosis, defined as an area of increased density of cortical bone extending into the bone marrow; and (5) resorption, defined as partial loss of condylar head.8,11,25,26 Furthermore, a four-point rating scale (03)7,27,28 was used to define the severity of erosion in the condylar head as follows:

N N N N

0: 1: 2:

3:

absence of erosion slight erosion, when decreased density is observed only in the cortical bone moderate erosion, when decreased density is observed in the cortical bone and extends to the upper layers of the adjacent subcortical bone extensive erosion, when decreased density is observed in the cortical bone and extends below the upper layers of the adjacent subcortical bone.

A four-point rating scale was also used in order to define the severity of osteophyte formation in the condylar head as follows:

N N N N

0: absence 1: slight, when marginal bony outgrowth on the condyle was less than 1 mm 2: moderate, when marginal bony outgrowth on the condyle was 12 mm 3: extensive, when marginal bony outgrowth on the condyle was more than 2 mm.

(b) Osseous changes of the mandibular fossae: defined as (1) erosion, (2) sclerosis and (3) resorption. (c) Joint space: (1) increased, when the distance between the condylar head and mandibular fossa was more than 4 mm; (2) normal, when the distance between the condylar head and mandibular fossa was between 1.5 mm and 4 mm; (3) reduced, when the distance between the condylar head and mandibular fossa was less than 1.5 mm; and (4) bony contact between condyle and mandibular fossa.7,11,29 The measurements were performed on lateral slices at the subjectively closest distance between condyle and mandibular fossa11,30 using the measurement tool included in the NewTom CBCT software (QR s.r.l.). Statistics Differences between the left and right joints of the patients were analysed with the Pearson correlation test. The correlation between age and the observed radiographic findings was statistically analysed with ANOVA using the Statistica 6.0 for Windows software (StatSoft Inc., Tulsa, OK).

Results A correlation coefficient of 0.2 was calculated using the Pearson test, showing no statistically significant differences between left and right TMJs. Thus, data from both joints could be evaluated independently. Findings of osseous changes to the condylar head (Figures 13) and the respective mean ages are illustrated in Table 2. Flattening and resorption were observed in 56% and 43% of the cases, respectively, whereas sclerosis was observed in 25% of the joints. The mean age of patients with sclerosis was statistically

Table 1 Age (years) Females Males Total

Number of patients according to age and gender 2029 3039 4049 4 3 7 8 2 10 19 0 19 5059 20 4 24 60+ 9 2 11 Total 60 11 71 % 84.5 15.5 100

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Table 5 shows the differences in the severity of erosion and osteophytes with variable mean age and their resulting P-values. There is a significant difference in the mean age between absent and moderate erosion (P 5 0.019), as well as between absent and extensive erosion (P 5 0.048). A significant difference is also found in the mean age between absent and extensive formation of osteophyte (P 5 0.003), as well as between slight and extensive formation of osteophyte (P 5 0.025). Table 6 shows osseous findings of the mandibular fossa per mean age. Erosion was observed in 7%, sclerosis in 48% and resorption was observed in 1% of the cases. The mean ages of patients with presence of erosion and sclerosis were statistically significantly higher than the mean ages of patients without any findings. Table 7 shows joint space evaluation per mean age. Reduced joint space was observed in 50% of the joints with a mean age of 46.69 years. Bony contact between condylar head and mandibular fossa was observed in 25% of the joints with a mean age of 55.13 years. A strong correlation was recorded between joint space and mean age (P 5 0.0006). Table 8 shows analytically the P-values for the observed joint space with variable mean age. The statistical analysis revealed significant differences in the mean age between (a) normal and increased joint space (P 5 0.038), (b) normal joint space and bony contact (P 5 0.0002), and (c) reduced joint space and bony contact (P 5 0.017).
Figure 1 Female aged 74 years with radiographic findings of severe osteoarthritis in both temporomandibular joints (TMJs). (a) Right TMJ showing moderate osteophyte formation and flattening of condylar head, bony contact between condylar head and mandibular fossa and sclerosis of mandibular fossa. (b) Left TMJ showing resorption of the condylar head (white arrow), bony contact between condyle and mandibular fossa and sclerosis of mandibular fossa

Discussion CBCT has been recognized as a reliable method for the examination of the osseous components of the TMJ. This technique is easy to perform, is reproducible and delivers a relatively low dose to the patient. Its usefulness has been previously described in the literature.1416,20,23 Osteoarthritis of TMJ is an age-related degenerative disease and is more frequent in females than in males.3133 In our study 84.5% of the patients were females and 15.5% were males. According to the literature, approximately 40% of patients with TMJ osteoarthritis are over the age of 40 years. MartinezBlanco et al4 found the mean age of patients with TMJ osteoarthritis to be 46.6 years, which is in agreement with the results of our study that showed a mean age of 48.17 years. The most common radiographic findings of the condylar head in our study were erosion, flattening and osteophytes, which comes in agreement with results from previous studies of patients with TMJ degenerative arthritis.4,8 Although sclerosis was the less frequent radiographic finding (25%), there was a statistically significant difference in the mean age of patients with sclerosis of the condylar head (51.86 years) compared
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significantly higher than the mean age of patients without sclerosis. Table 3 shows the severity of erosion per mean age. Slight erosion was found in 25% of the joints with a mean age of 48.54 years. Moderate erosion was found in 19% of the joints with a mean age of 52.00 years. Extensive erosion was found in 15% of the joints with mean age of 51.36 years. No statistically significant difference was found between recorded erosion and mean age (P 5 0.074). Table 4 shows the severity of osteophyte formation per mean age. Slight osteophyte formation was observed in 26% with a mean age of 47.46 years. Moderate osteophyte formation was observed in 18% of the joints with a mean age of 50.64 years. Extensive osteophytes were observed in 12% of the joints with a mean age of 55.88 years. A statistically significant difference was found between recorded osteophyte formation and mean age (P 5 0.050).

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Table 2

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Presence of osseous changes of condylar head per mean age Present n 63 79 106 36 81 61 Percentage 44 56 75 25 57 43 Mean age (years) 50.11 46.62 46.92 51.86 47.07 49.62 SD 12.10 13.65 13.96 9.14 12.26 14.60 P-value 0.104 0.042* 0.674 No Yes No Yes No Yes

Flattening Sclerosis Resorption

*P , 0.05; SD, standard deviation

Table 3

Severity of erosion per mean age n Percentage 41 25 19 15 100 Mean age (years) SD 44.95 48.54 52.00 51.36 48.17 12.88 13.06 13.85 11.06 13.06 P-value 0.074

Table 4

Severity of osteophyte formation per mean age n Percentage 44 26 18 12 100 Mean age (years) SD 45.52 47.46 50.64 55.88 48.17 13.71 13.98 8.88 10.69 13.06 P-value 0.050*

None Slight Moderate Extensive Total

58 35 27 22 142

Absence Slight Moderate Extensive Total

63 37 25 17 142

SD, standard deviation

*P , 0.05; SD, standard deviation

Table 5

Resulting P-values of the least significant difference test for the severity of erosion and osteophytes with variable mean age None (44.95 years) 0.193 0.019* 0.048* None (45.52 years) 0.464 0.091 0.003* Slight (48.54 years) 0.193 0.295 0.421 Slight (47.46 years) 0.464 0.336 0.025* Moderate (52.00 years) 0.019* 0.295 0.863 Moderate (50.64 years) 0.091 0.336 0.192 Extensive (55.88 years) 0.003* 0.025* 0.192 Extensive (51.36 years) 0.048* 0.421 0.863

Erosion Severity None (44.95 years) Slight (48.54 years) Moderate (52.00 years) Extensive (51.36 years) Osteophytes Severity None (45.52 years) Slight (47.46 years) Moderate (50.64 years) Extensive (55.88 years) *P , 0.05

Table 6 Presence of osseous changes of the mandibular fossa per mean age Present No Yes No Sclerosis Yes No Resorption Yes Erosion n 132 10 74 68 140 2 Mean age Percentage (years) SD 93 7 52 48 99 1 47.52 56.80 44.93 51.69 47.89 67.50 13.07 9.83 14.08 10.89 12.92 9.19 P-value 0.030* 0.001*

Table 7

Joint space evaluation per mean age n Percentage 4 24 50 22 100 Mean age (years) 56.00 43.56 46.69 55.13 48.17 SD 15.31 11.98 12.93 11.25 13.06 P-value 0.0006*

Increased 5 Normal 34 Reduced 71 Bony contact 32 Total 142

*P , 0.05; SD, standard deviation

*P , 0.05; SD, standard deviation

Table 8

Resulting P-values of the least significant difference test for the observed joint space with variable mean age Increased (56.00 years) Normal (43.55 years) 0.0383* 0.2289 0.0002* Reduced (46.69 years) 0.1076 0.2289 0.0017* Bony contact (55.12 years) 0.8837 0.0002* 0.0017*

Joint space (mean age)

Increased (56.00 years) Normal (43.55 years) 0.0383* Reduced (46.69 years) 0.1076 Bony contact (55.12 years) 0.8837 *P , 0.05
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Figure 2 Right and left temporomandibular joint (TMJ) of a female aged 52 years. (a) Right TMJ showing flattening of condylar head and reduced joint space. (b) Left TMJ showing slight osteophyte formation and erosion (white arrow) of the condylar head, normal joint space and sclerosis of mandibular fossa

with the mean age of patients without sclerosis (46.92 years). As was suggested by Gynther et al,7 this could be explained by the fact that sclerosis develops secondarily in more progressive forms of the disease. The mean age (50.27 years) of patients with osteophytes on the condylar head was statistically higher compared with the mean age (45.52 years) of patients without osteophytes (P 5 0.05). As for the severity of osteophyte formation with variable age, statistically significant differences were found between the mean age of patients with absence of osteophytes (45.52 years) and the mean age of either slight (47.46 years) or extensive (55.88 years) osteophyte formation. This result indicates a statistically significant correlation between the age and the presence as well as the severity of osteophytes, which is in accordance with previous reports.34,35 No statistically significant difference was detected between the mean age of patients with and without signs of erosion. This observation indicates lack of strong correlation between mean age and erosion and is in agreement with results presented by Sato et al.36 Nevertheless, the P-value (P 5 0.074) was close to the level of significance 0.05, revealing a tendency for an increased frequency of observed erosion in older

Figure 3 Male aged 49 years with radiographic findings of osteoarthritis in both right and left temporomandibular joints (TMJs). (a) Right TMJ showing sclerosis, extensive osteophyte formation and erosion (white arrow) of the condylar head, sclerosis of mandibular fossa and bony contact between condylar head and mandibular fossa. (b) Left TMJ showing reduced joint space and moderate osteophyte formation

patients, as found in other studies.34,35 When we compared the severity of erosion with variable age, statistically significant differences were found between the mean age of patients without erosion (44.95 years) and mean ages of either moderate (52.00 years) or extensive (51.36 years) erosion. This indicates a statistically significant correlation between the severity of erosion and age. Previous studies reported that osseous changes of the mandibular fossa are common in patients with osteoarthritis as a result of progressive joint remodelling.3638 In our study, sclerosis of the mandibular fossa was found in 68 joints (48%) and was the most frequent radiographic finding of the fossa with a mean age of 51.69 years. No conclusions are drawn regarding possible correlation between age and fossa resorption due to the limited number of cases with this finding. One of the most common findings in patients with degenerative arthritis is reduced joint space.11 In our study, joint space was found to be reduced in 50% of the joints, and bony contact between the condylar head
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and mandibular fossa was found in 22% of the joints. Moreover, the mean age of patients with bony contact was 55.12 years, which was statistically higher when compared with normal (43.55 years) and reduced (46.69 years) joint space. This strongly indicates that in patients with osteoarthritis, bony contact is expected to be seen in older age groups.
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In conclusion, degenerative arthritis is an age-related disease. The progression and severity of osseous changes in condylar head and mandibular fossa are increased with age. In older age groups, patients are expected to have more frequent and severe progressive degenerative bony changes due to the development of TMJ osteoarthritis, than patients in younger age groups.

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37. Honda K, Larheim TA, Sano T, Hashimoto K, Shinoda K, Westesson PL. Thickening of the glenoid fossa in osteoarthritis of the temporomandibular joint. An autopsy study. Dentomaxillofac Radiol 2001; 30: 1013. 38. Sulun T, Cemgil T, Duc JM, Rammelsberg P, Jager L, Gernet W. Morphology of the mandibular fossa and inclination of the articular eminence in patients with internal derangement and in symptom-free volunteers. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2001; 92: 98107. 39. Yamada K, Tsuruta A, Hanada K, Hayashi T. Morphology of the articular eminence in temporomandibular joints and condylar bone change. J Oral Rehabil 2004; 31: 438444.

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