MRI of the TMJ: Morphometric comparison of asymptomatic volunteers and symptomatic patients

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MRI of the TMJ: Morphometric comparison of asymptomatic volunteers and symptomatic patients Publication Ingrid Peroz, Priv Doz 1 /Antje Seidel, DDS 2 /Mathias Griethe, DDS 3 / Arne-Jörn Lemke, Prof Dr Med 4 Objective: Morphologic and morphometric differences in the anatomy of the temporomandibular joint (TMJ) between asymptomatic volunteers and patients with temporomandibular disorders (TMDs) were evaluated using magnetic resonance imaging (MRI). Method and Materials: Forty volunteers were examined using a 1.5-T MRI and double surface coils. Both temporomandibular joints were imaged simultaneously; 78 joints could be evaluated. Each TMJ was examined in the intercuspal position in a parasagittal plane. Images were analyzed morphometrically and morphologically and compared to data retrospectively obtained from 91 age-matched patients. Results: Considering the position of the disc morphologically, 66.7% of the volunteers had a normal disc position while 28.6% of the patients did. Anterior disc displacement with reduction was diagnosed in 33.3% of volunteers and 31.0% of the patients. Anterior disc displacement without reduction was found only in patients (19.2%). Comparison of morphometric data between patients and volunteers revealed shortening of the disc and a thickening in the intermedial part and the posterior band in patients. In patients, the disc presented anteriorly and the condyle was positioned superiorly and posteriorly in the mandibular fossa when compared to the volunteers. Theree, the posterior and superior joint spaces were smaller in patients. Women showed disc displacement and combined morphometric changes in the TMJ structures significantly more often than men. Conclusion: A large variation of morphometric parameters in temporomandibular joints could be demonstrated. However, reduced disc length, thickening of the disc, narrowed interarticular superior and posterior distances, and a superior-posterior position of the condyle are more commonly associated with joint pathology. ( Int 2011;42:659 667) Key words: craniomandibular disorders, magnetic resonance imaging, temporomandibular joint About one-third of the population shows at least one symptom of temporomandibular disorders (TMDs), of which disc displacements are a part. 1 1 Associate Professor, Department Prosthodontics, Gerodontology and Craniomandibular Disorders, Charité University Medicine Berlin, Berlin, Germany. 2 Melbourne Dental School, The University of Melbourne, Melbourne, Australia. 3 Zahnärztliche Gemeinschaftspraxis im Axel-Springer-Haus, Berlin, Germany. 4 Professor, Gesundheit Nord Klinikverbund Bremen, Klinikum Bremun-Mitte, Zentrum für Radiologie und Nuklearmedizin, Bremen, Germany. Correspondence: Dr Ingrid Peroz, Charité, University Medicin Berlin Dental School, Department Prosthodontics, Gerodontology and Craniomandibular Disorders, Aßmannshauser Str 4 6, D 14197 Berlin, Germany. Email: ingrid.peroz@ charite.de Magnetic resonance imaging (MRI) is the gold standard showing structural changes, especially of soft tissues of the temporomandibular joint (TMJ). Based on MRI, numerous studies have obtained morphologic and morphometric data of TMJs with TMD and tried to correlate them to structural changes that could be responsible the functional disorders. 2 5 Different morphometric procedures have been introduced to evaluate MRIs. 2,6 11 Previous MRI-based examinations of volunteers have shown that even in joints without clinical signs and symptoms, structural changes can be seen. 12 Theree, it is currently unclear which structural changes are simply a variation of the norm and which are pathologic changes within the TMJ. VOLUME 42 NUMBER 8 SEPTEMBER 2011 659

It was the aim of the present study to compare the data of a prospectively examined group of volunteers with a retrospectively examined group of patients whose data have already been published. 5 PATIENTS AND METHODS Volunteers All 40 subjects were dental students who were in their first three clinical semesters. They gave written consent to take part in the study, which was approved the ethics committee. The study group consisted of 16 men and 24 women, ranging in age from 21 to 33 years (mean, 25.0 3.0 years). The inclusion criteria were no history of TMJ disorders; no pain in the joints, ears, or muscles of mastication; and no functional limitation of mandibular movement. Due to motion artifacts, only 78 MRIs could be examined. Patients All patients of this study were treated at the TMD center of the dental school and had been referred to the department radiology due to a suspected disc displacement. To get an age-matched group of patients, only those up to 35 years of age were included in the study, resulting in 91 patients (25 men and 66 women, 182 joints) with a mean age of 25.7 ± 6.4 years (range, 17 to 35 years). Statistically, there was no significant difference in age between the patients and volunteers (Mann-Whitney, P =.098). However, there were significantly more women in the patient group (chi square test, P =.044). Due to motion artifacts, only 159 MRIs could be examined. Examination Patients and volunteers were physically examined bee MRI two of the authors. Clinical examination was conducted according to documented Research Diagnostic Criteria Temporomandibular Disorders (RDC/TMD). 13 MRI A 1.5-T tomograph (SP63, Siemens) was used to acquire the MRIs the patients and a 1.5-T Signa Twinspeed (GE Medical Systems) to examine the volunteers. For both groups, double coils were used with a diameter of 12 cm to acquire bilateral sagittal oblique images simultaneously in a closed and maximal open-mouth position. To adjust the sagittal MRI perpendicular to the long axis of the condyle, a transverse scout image of the TMJs was used. The intermediate-weight, fast low-angle shot sections were obtained with the following parameters: repetition time, 2,360 msec; echo time, 15 msec; echo train length, 6; means: 1; matrix, 320 224; 3-mm section thickness; aquisition time, 4:15 min. The image data were transferred to the Workstation internal network and evaluated the Radworks software (GE Medical Systems). The images of the volunteers were evaluated separate authors; both undertook a one-day training with a good interrater reliability (ICC 0.7). Morphologic image evaluation The disc-condyle-relation was classified morphologically according to Drace in a normal disc position (NDP), a disc displacement (ADD) with reduction (wr), and a disc displacement without reduction (ADDwoR) regarding the sagittal angulated slices in closed- and open-mouth position. 14 The condyle m was grouped morphologically, according to Müller-Leisse, into four groups: a round condyle, a degenerative flattened condyle, a condyle with osteophytes, and a condyle with a thickened cortex. 8 Morphometric image evaluation All morphometric measurements were carried out on the central section of the sagittal oblique images in closed mouth position. The morphometric measurement procedures used are described in detail elsewhere. 5 Briefly, the disc position was evaluated the disc angle (da) according to Rammelsberg (Fig 1). 7 The m of the disc was described its length and anterior, medial, and posterior thickness. The length is defined as the distance between the anterior and posterior band (dl), whereas the thickness of the disc is given the largest anterior (ath) and posterior (pth) dimension of the disc, perpendicular to the disc-length, and the smallest one in the intermediate zone (mth) (Fig 2). 15 Publication 660 VOLUME 42 NUMBER 8 SEPTEMBER 2011

Publication pfh pth dl da X C ath mth Fig 1 Measurement of the disc angle (da) in intercuspal position on sagittal oblique MRI of a volunteer (C, center of the condyle; pfh, parallel to Frankfurt horizontal plane). Fig 2 Measurement of the disc length and thickness in intercuspal position on a sagittal oblique MRI of a volunteer (dl, disc length; ath, anterior thickness; mth, medial thickness; pth, posterior thickness). sjs pfh ajs pjs ste X C Fig 3 Measurement of the condyle size and the position of the condyle within the fossa on a sagittal oblique MRI of a volunteer (ajs, anterior joint space; pjs, posterior joint space; sjs, superior joint space; C, center of the condyle). Fig 4 Measurement of the steepness of the eminence (ste) in intercuspal position on a sagittal oblique MRI of a volunteer (pfh, parallel to Frankfurt horizontal plane). The dimension of the condyle is defined the diameter of a circle, which embraces the condyle the best. The central point of this circle represents the center of the condyle (C) (Fig 3). The position of the condyle within the fossa is given the thickness of the joint spaces between the condyle and temporal bone. The shortest anterior (ajs) and posterior (pjs) distances are measured as well as the greatest superior distance (sjs) (Fig 3). 10,16 The steepness of the eminence (ste) was evaluated the angle between a parallel line to the Frankfurt horizontal plane (pfh) through the zenith of the fossa and a line through the zenith of the fossa and the trough of the eminence (Fig 4). VOLUME 42 NUMBER 8 SEPTEMBER 2011 661

RESULTS Publication eh ef Fig 5 Measurement of morphometrical parameters of the fossa mandibularis (fd, fossa deepness; fw, fossa width; eh, eminence height; pph, height of the processus postglenoidalis; ef, diagonal from the trough of the eminence and the zenith of the fossa; fpp, diagonal from the zenith of the fossa and the trough of the processus postglenoidalis. fd fw pfh fpp pph The width (fw) and deepness of the fossa (fd) were measured according to Pullinger et al. 9 The distance between the trough of the tuberculum articulare and postglenoidal processus was interpreted as the width of the fossa. A line perpendicular to the line between these two troughs through the zenith of the fossa was taken to represent the deepness of the fossa. Additionally, two connecting lines can be measured between the trough of the processus postglenoidalis and the zenith of the fossa (fpp) and between the trough of the eminence and the zenith of the fossa (ef). The height of the eminence (eh) and the processus postglenoidalis (pph) was measured using a parallel line to the pfh through the zenith of the fossa. Perpendicular to this parallel line, through the trough of the processus postglenoidalis and the eminence, respectively, the two heights are given (Fig 5). Statistics were permed using the PASW 18.0 (SPSS) using the Mann-Whitney U test metrical data comparing two groups, the Kruskal-Wallis test to compare more than two groups, and the chi squared test categoric data. Correlations were evaluated with the Pearson correlation coefficient. All P values less than.05 were considered statistically significant. Morphologic evaluations Considering the position of the disc morphologically, 66.7% of the volunteers and 28.6% of the patients had a normal disc position (NDP), 33.3% of the volunteers and 31.9% of the patients had ADDwR, and 19.2% of the patients had ADDwoR. In 20.3% of the patients, the disc position could not be classified clearly. Due to the morphologic disc position, patients differed significantly from volunteers (chi square test, P <.01; Table 1). The m of the condyles also differed significantly between the two groups (chi square test, P <.01; Table 2). Morphometric evaluation The disc angle was significantly greater in patients than in volunteers (Mann-Whitney test, P <.01; Table 3). In other words, the disc was significantly more anteriorly located in the patient group. The patients discs were significantly shorter and medially and posteriorly thicker than the discs of volunteers (Table 3). The size of the condyle was significantly greater in volunteers (Mann-Whitney, P <.01; Table 3) and correlated negatively with the disc angle (Pearson,.316; P <.01) and the morphologic disc positions (NDP, ADDwR, and ADDwoR). That is, the more anteriorly located the disc, the smaller the condyle. The anterior, superior, and posterior joint spaces were significantly smaller in patients (Mann-Whitney test, P <.01; Table 3). They correlated with the morphologic disc positions: NDP, ADDwR, and ADDwoR (Kruskal- Wallis, P =.02 in NDP, P <.01 in ADDwR and ADDwoR). The pairwise comparison of the morphologic disc positions showed a significantly larger anterior joint space in ADDwR in comparison to NDP. It also revealed significantly smaller superior and posterior joint spaces (Mann Whitney, P <.01; Table 4). When comparing ADDwoR to NDP, only the superior joint space was significantly reduced (Mann-Whitney, P <.01; Table 4). However, when comparing ADDwR with ADDwoR, the superior and posterior joint spaces were reduced significantly (Mann- 662 VOLUME 42 NUMBER 8 SEPTEMBER 2011

Publication Table 1 Morphologic evaluation of the disc position in patients and volunteers according to Drace 14 NDP ADDwR ADDwoR determinable Volunteers 52 (66.7) 26 (33.3) 0 (0) 0 (0) Patients 52 (28.6) 58 (31.9) 35 (19.2) 37 (20.3%) P value <.01 Table 2 Morphologic ms of the condyle of volunteers and patients Form of condyle Round Flattened Osteophytes Thickened corticalis Volunteers 62 (79.5) 3 (3.8) 1 (1.3) 12 (15.4) Patients 67 (42.1) 60 (37.7) 19 (11.9) 13 (8.2) P value <.01 Table 3 Comparison of mean morphometric data between volunteers and patients Structure Volunteers Patients P value Disc angle (degrees) 0.1 56.3 <.01 Disc length (mm) 12.8 9.5 <.01 Anterior disc thickness (mm) 2.6 2.7.331 Medial disc thickness (mm) 1.2 2.1 <.01 Posterior disc thickness (mm) 2.6 3.0.015 Condyle diameter (mm) 7.4 6.6 <.01 Anterior joint space (mm) 2.5 2.1 <.01 Superior joint space (mm) 3.5 2.7 <.01 Posterior joint space (mm) 2.1 1.6 <.01 Steepness of the eminence (degrees) 44.0 39.0 <.01 Fossa width (mm) 17.4 18.2 <.01 Fossa deepness (mm) 6.0 6.7 <.01 Eminence height (mm) 8.8 8.4.1460 Height of processus postglenoidalis (mm) 4.4 5.3 <.01 Diagonal ts fs (mm) 10.3 9.5 <.01 Diagonal ps fs (mm) 9.7 8.6 <.01 Table 4 Joint spaces in relation to the disc position (mean) Group Joint spaces NDP (mm) ADDwR (mm) ADDwoR (mm) A Anterior joint space 2.0 (AB) 2.4 (ABC) 2.3 (AB) B Superior joint space 3.3 2.9 (BAC) 1.4 (BA) C Posterior joint space 2.0 1.6 (CAB) 1.8 The letter behind the numbers indicate the significance between the different groups. VOLUME 42 NUMBER 8 SEPTEMBER 2011 663

Table 5 Sex differences in morphometric data (mean) Structure Men Women P value Disc length (mm) 12 9.9 <.01 120 100 Disc position NDP ADDwR ADDwoR Publication Anterior disc thickness (mm) 2.9 2.6.034 Condyle diameter (mm) 7.3 6.7 <.01 80 Disc angle (degrees) 22.3 44.6.018 Superior joint space (mm) 3.3 2.8 <.01 No. 60 40 20 0 Males Females Fig 6 Distribution of male and female patients and volunteers within the groups according to disc position (NDP, normal disc position; ADDwR, disc displacement with reduction; ADDwoR, disc displacement without reduction). Whitney, P =.023). Theree, ADDwR was combined with a retrocranial position of the condyle, whereas ADDwoR with a cranial position only. The steepness of the eminence was higher in volunteers than in patients (Mann- Whitney, P <.01; Table 3). When comparing patients and volunteers with NDP, ADDwR, or ADDwoR, no statistically significant difference was observed with respect to the steepness of the articular eminence. The height of the articular eminence correlates significantly with its steepness (Pearson, P <.01). The deepness and width of the fossa were significantly greater in patients than in volunteers (Mann-Whitney, P <.01; Table 3). The correlation of the width of the fossa and the joint spaces showed that the condyle was more anteriorly and superiorly positioned the greater the posterior-anterior width of the fossa (Pearson, P =.012 anterior joint space and P <.01 superior joint space). The width of the fossa correlated also with the height of the eminence and the processus postglenoidalis (Pearson, P <.01). The greater the width of the fossa, the higher the tuberculum as well as the processus. Sex differences Men had a significantly longer and an anteriorly thicker disc than women. The disc is more anteriorly positioned in the fossa, which results in a greater superior joint space. Disc displacements appeared significantly more often in women than in men (Mann Whitney; Table 5, Fig 6). DISCUSSION Morphologic evaluation Analogue to the results of comparable studies, the structures of the TMJ of volunteers showed a great variability and a high amount of ADD (33.3%). 17 20 Due to the high incidence of ADD in asymptomatic volunteers, it was discussed whether ADD is a normal variation of the disc position and therapeutic consequences should not be derived from imaging presentations of a TMJ but from the clinical situation. 4,21 Due to the correlation between ADD and osseous demations of the condyle, such as flattening of the condyle, thickening of the cortex, or osteophytes, they should be 664 VOLUME 42 NUMBER 8 SEPTEMBER 2011

interpreted as reactive changes that are a consequence of ADD. Macroscopic anatomical studies show demations, sclerosis and the mation of osteophytes in relation to ADD. 5,22 These results are in concordance with other studies. 8,16,23 Lemke et al could show that structural demations increase and the size of the condyle decrease in correlation with the degree of ADD. 5 Theree, it could be concluded that these changes are secondary structural reactions and not primary predisposing ones. Although the actual data of the age-matched controls presented a significantly greater size of the condyle, there is no final answer to the question whether the decreasing size of the condyles was a risk factor, a consequence, or an adverse effect in the pathogenesis of ADD. Several previous studies could show that anterior disc position results in decreased superior joint space. 23 28 As longitudinal studies are lacking, it is not clear whether this is a predisposing factor ADD. Nevertheless, it could be a consequence of disc displacement. The pairwise comparison of joints with NDP and ADDwR revealed an increased anterior joint space and decreased superior and posterior ones. The condyle was displaced retrocranially due to ADD. An increasing anterior joint space could be explained a reaction to a compensatory resorption of the condylar and articular eminence-loading surface due to ADD. Indeed, a decreased steepness of the eminence and a flattening of the condyle were correlated to ADD. Furthermore, in an ADD, the thicker posterior band is interposed between the anterior part of the condyle and the eminence, which could also increase the anterior joint space. Additionally, the data could show that the posterior thickness of the disc was increased in patients with ADD. In ADDwoR, only the superior joint space was significantly reduced compared to NDP or ADDwR. These results show a contrast to other studies. 3,29 Nevertheless, they are confirmed Rammelsberg et al. 10 Theree, osseous changes within the TMJ are possibly a result of remodeling reactions of the disc. The steepness of the eminence as a predisposing factor ADD is controversially discussed. Some studies revealed a steep eminence as a risk factor ADD. 5,30 Other studies found no differences of the eminence steepness between patients and volunteers. 16,24,31 Isberg and Westesson reported a correlation between a posterior disc position and an increasing steepness of the eminence. 32 In contrast, Ren et al found a steeper eminence in asymptomatic volunteers and disagreed with the hypothesis that a steep eminence is an etiologic factor ADD. They assume that a flattening of the eminence is a result of remodeling or degenerative changes of the bone as a reaction to internal derangement. 33 The results of the present study underline these conclusions as the volunteers revealed a significantly steeper eminence than the patients. The increasing width of the fossa is a result of the flattening of the eminence. The deeper fossa correlates with a higher processus postglenoidalis. According to Major et al, a significantly longer disc was found in men, which could be a result of larger TMJ structures in general in men. 34 The more anteriorly positioned disc in men can be interpreted as a protective factor and might be an explanation the lesser presence of men in TMD clinics. The limitations of our study are the difference of sex distribution between patients and volunteers and the different data acquisition of both groups. Whereas the volunteers were examined clinically and MRI prospectively two examiners, the data of the patients were collected over 8 years. The clinical examination was done two examiners, but the MRIs were permed different examiners at the department of radiology. The MRIs were evaluated two different examiners, who trained each other in using the same evaluation methods and reached a good reliability with an ICC of at least 0.7 all parameters. In conclusion, the changes in the m of the disc and condyle seem to be a result of ADD. The more superior condyle position seems to be more a secondary change due to ADD. A flattening of the eminence is assumed to be a consequence rather than a primary predisposing factor of ADD. Publication VOLUME 42 NUMBER 8 SEPTEMBER 2011 665

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