Dynamic High-Resolution Sonography Compared to Magnetic Resonance Imaging for Diagnosis of Temporomandibular Joint Disk Displacement

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1 ORIGINAL RESEARCH Dynamic High-Resolution Sonography Compared to Magnetic Resonance Imaging for Diagnosis of Temporomandibular Joint Disk Displacement Hadeel Habashi, MD, Ayelet Eran, MD, Israel Blumenfeld, MD, Diana Gaitini, MD Received January 10, 2014, from the Bruce and Ruth Rappaport School of Medicine, Technion, Haifa, Israel (H.H., D.G.); and Departments of Maxillofacial Reconstruction (A.E., D.G.) and Medical Imaging (I.B., D.G.), Rambam Health Care Campus, Haifa, Israel. Revision requested March 7, Revised manuscript accepted for publication April 8, Address correspondence to Diana Gaitini, MD, Department of Medical Imaging, Rambam Health Care Campus and Faculty of Medicine, Technion, Israel Institute of Technology, Ha alya Ha shnia 8, PO Box 9602, Haifa, Israel. Abbreviations CT, computed tomography; MRI, magnetic resonance imaging; NPV, negative predictive value; PPV, positive predictive value; TMJ, temporomandibular joint doi: /ultra Objectives The purpose of this study was to determine the value of dynamic highresolution sonography for evaluation of temporomandibular joint (TMJ) disk displacement compared to magnetic resonance imaging (MRI) with the mouth closed and during the maximal mandibular range of motion. Methods Dynamic high-resolution sonography with the mouth closed and during the maximal mandibular range of motion was performed on 39 consecutive patients (78 joints; 13 male and 26 female; age range, years; mean age ± SD, ± years) with TMJ disorders. A TMJ MRI study was performed 1 to 7 days after sonography. We searched for signs of disk displacement and findings compatible with degenerative joint disease. Both studies were performed and interpreted independently by blinded operators. Results Magnetic resonance imaging depicted 22 normal joints (28.2%), 21 (26.9%) with anterior disk displacement with reduction, 15 (19.2%) with anterior disk displacement without reduction, and 20 (25.6%) with degenerative disease. Sonography depicted 30 normal joints (38.5%), 22 (28.2%) with anterior disk displacement with reduction, 12 (15.4%) with anterior disk displacement without reduction, and 14 (17.9%) with degenerative disease. The overall sensitivity, specificity, and accuracy of sonography for diagnosis of disk displacement were 74.3%, 84.2%, and 77.7%, respectively. The sensitivity, specificity, and accuracy for diagnosis of disk displacement with reduction were 78.6%, 66.7%, and 73.0%, and the values for diagnosis of disk displacement without reduction were 66.7%, 78.6%, and 73.0%. Conclusions Dynamic high-resolution sonography is a potential imaging method for diagnosis of TMJ disk displacement and degenerative diseases. Further studies are needed to make dynamic high-resolution sonography the first-line test for diagnosis of TMJ disk displacement. Key Words disk displacement; dynamic imaging; magnetic resonance imaging; musculoskeletal ultrasound; sonography; temporomandibular joint The temporomandibular joint (TMJ) is a synovial joint between the condyle of the mandible and the glenoid fossa of the squamous temporal bone. It is divided into two compartments by a fibrocartilaginous disk, which allows movements in the lower and upper compartments. 1 Temporomandibular joint disorders constitute a number of functional and structural disorders 2015 by the American Institute of Ultrasound in Medicine J Ultrasound Med 2015; 34:

2 affecting not only the TMJ but also the masticator muscles and eventually all other parts of the stomatognatic system. 2 These disorders may present with a cluster of clinical signs, including TMJ pain, articular noises, and restricted jaw function. 3 The number of affected people is increasing, perhaps due to the influence of psychological tension in today s society. 2 The prevalence of at least 1 sign of temporomandibular disorders among adults in the United States is reported as high as 40% to 75%, and among those with at least 1 symptom, it is 33%. 4 The most frequent cause of TMJ dysfunction is disk displacement, which is an abnormal relationship between the disk and the condyle. 5 Anterior displacement with reduction is defined as disk displacement with the mouth closed that reduces (with a click) to the normal relationship at some time during opening. The mandible deviates to the affected side on opening until the click occurs and then returns to the midline. This situation may worsen from intermittent locking of the disk to anterior disk displacement without reduction (closed lock), the dislocated disk acting as a mechanical obstruction to opening and translation of the condyle, leading to a marked decrease in mandible opening on the affected side and a variable degree of pain. 2 The indications for imaging include failure of conservative treatment, worsening of symptoms or atypical symptoms, and preoperative assessment. 1,5 Magnetic resonance imaging (MRI) is accepted as the reference standard for imaging diagnosis of TMJ disorders, but the relatively low availability and high cost make the use of MRI as a screening method too inconvenient. 1,6,7 Conventional radiography such as panoramic radiography, which is generally available at every dental clinic, shows destructive changes in the TMJ only at a late stage. 1 Computed tomography (CT) is not able to visualize soft tissue structures such as the articular disk. 1 Furthermore, CT radiation exposure prevents its use as a screening method at a frequency of 1 to 2 times per year. Therefore, an inexpensive and quick imaging diagnostic method that is widely available would be an important improvement in the diagnosis of TMJ diseases. Furthermore, sonography allows dynamic evaluation of the TMJ soft structures, leading to an improvement in sensitivity, specificity, and accuracy compared to MRI. 7,8 The purpose of this study was to determine the value of dynamic high-resolution sonography with the mouth closed and during the maximal mandibular range of motion for evaluation of TMJ disk displacement compared to MRI. Our assumption was that dynamic high resolution sonography may be a reliable method for diagnosis of TMJ disk displacement. Materials and Methods Patient Population Between March and October 2011, 39 consecutive patients with symptoms and signs of TMJ disorders admitted to the craniofacial clinic in our institution were included in the study. The study was approved by the Institutional Review Board, and written informed consent was obtained. The clinical evaluation was performed by a dentist (I.B.) and included a comprehensive history and careful physical examination, including inspection and measurement of mandibular motion, palpation of the masticator and cervical muscles, palpation of the TMJ, and examination of the oral cavity, dentition, occlusion, salivary glands, and the anterior and posterior neck. Patients with a clinical diagnosis of disk displacement were asked to participate in the study. Inclusion criteria were adults aged 18 years and older and clinical signs suggestive of TMJ disk displacement. Exclusion criteria were patients without judgment who were unable to sign informed consent or undergo dynamic examinations, contraindications to MRI such as claustrophobia, metal prostheses, and pacemakers, and patients who were considered to have a muscular origin for their TMJ symptoms. Imaging Acquisition and Interpretation Dynamic High-Resolution Sonography Sonography was performed with a high-resolution (5 17-MHz) linear array transducer (iu22; Philips Healthcare, Bothell, WA). Patients were placed in a supine position. The transducer was placed over the TMJ, parallel and inferior to the zygomatic arch for an axial view and parallel to the mandible ramus for a coronal view. The transducer was tilted out until an optimal view of the joint was obtained according to the face anatomy for both axial and coronal planes. Static and dynamic examinations of the disk were performed. Static scans were obtained with the mouth closed and at maximal opening, and dynamic scans were obtained during mouth opening at different mandibular ranges of motion. On sonography, the condyle and glenoid fossa were depicted as hyperechoic lines, whereas the disk was depicted as a central hyperechoic line surrounded by a shallow hypoechoic rim. The disk position was categorized as follows: (1) a normal disk position was defined when the disk was placed over the condyle head with the mouth closed and at maximal mouth opening (Figure 1); (2) anterior disk displacement with reduction was defined when the disk was displaced anteriorly with the mouth closed and returned to its physiologic position during opening (Figure 2); and (3) anterior disk displacement 76 J Ultrasound Med 2015; 34:75 82

3 without reduction was defined when the disk did not return to its physiologic position during mouth opening (Figure 3). In addition, we searched for findings compatible with degenerative joint disease, such as the presence of erosions in the condyle surface and irregular disk morphologic characteristics. The data were transferred to a picture archiving and communication system for diagnosis and archiving. The dynamic high-resolution sonographic examinations were performed and interpreted by a senior radiologist specializing in sonography (D.G.), who was blinded to the clinical examination and MRI results. Magnetic Resonance Imaging Magnetic resonance imaging examinations were performed 1 to 7 days after the sonographic examinations. A 3-T MRI machine (Discovery MR T; GE Healthcare, Milwaukee, WI) equipped with a high-resolution surface coil was used. The MRI protocol included T1- weighted (fast spin echo) and T2-weighted (proton density and fast spin echo) sequences in sagittal and coronal planes using a 2-mm slice width with the mouth closed and at maximal mouth opening. Patients were placed in a supine position. Sagittal scans were performed in a plane Figure 1. Sonograms of a normal TMJ. A, Closed mouth. The mandible condylar head (large arrow) and the temporal glenoid fossa (upper short arrow) are shown as hyperechoic curved lines. The disk (opposed short arrows) is shown between both over the mandible condyle. B, Open mouth. At maximal opening, the disk (arrows), shown as a hyperechoic line surrounded by a hypoechoic area, is seen over the mandible condylar head. C, Normal disk position (arrows) in a split image: closed mouth (left) and open mouth (right). A B C J Ultrasound Med 2015; 34:

4 parallel to the mandibular ramus. Coronal scans were performed on a plane perpendicular to the mandibular ramus through the condillar fossa. The MRI examinations were performed first with the mouth closed in sagittal and coronal planes on T1 and T2 sequences, followed by examinations with the mouth open by the same protocol. Patients Figure 2. Sonograms of anterior displacement of the disk with reduction. Left, With the mouth closed, the disk (arrow) is displaced anteriorly. Right, At maximal opening, the disk (arrow) returns to the normal position, over the head of the mandible condyle. Figure 3. Sonograms of anterior displacement of the disk without reduction. Left, With the mouth closed, the disk (arrow) is displaced anteriorly. Right, At maximal opening, the disk (arrow) remains in the abnormal position, anterior to the condyle. 78 J Ultrasound Med 2015; 34:75 82

5 received an intermaxillary device to obtain maximal mouth opening. Bilateral TMJ examinations were conducted. The data were collected in a matrix with a 12-mm field of view. Registration parameters were identical for all patients and were interindividually checked a number of times during the research to ensure standardization of examinations. The data were transferred to a picture archiving and communication system for diagnosis and archiving. Each TMJ was analyzed individually. Magnetic resonance images with the mouth closed were analyzed according to a protocol that included disk shape, signal intensity and position relative to the condyle, mandibular condyle shape, and position in the mandibular fossa. With the mouth open, the reading protocol included disk position relative to the condyle and movement of the condyle relative to the articular eminence. The articular disk was identified as a biconcave hypointense structure. The disk position was categorized as defined in the literature 2 as follows: (1) a normal disk position was defined when the posterior band of the disk was superior or at the 12-o clock position relative to the condyle with the mouth closed and at maximal mouth opening (Figure 4); (2) anterior disk displacement with reduction was defined when the posterior band of the disk was anterior to the condyle with the mouth closed and reduced to its normal physiologic position during mouth opening (Figure 5); and (3) anterior disk displacement without reduction was defined when the disk did not reduce during mouth opening (Figure 6). In addition, we searched for findings compatible with degenerative joint disease, such as the presence of erosions in the condyle surface and irregular disk morphologic characteristics. The MRI studies were interpreted by a senior neuroradiologist (A.E.), who was blinded to the clinical data and sonographic results. Statistical analysis Magnetic resonance imaging of the TMJ was the reference standard. The sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV), and accuracy of sonographic diagnoses were calculated. The statistical analyses were performed with the Pearson χ 2 test and SPSS version 14 software for Windows (IBM Corporation, Armonk, NY). Results Thirty-nine consecutive patients with clinically diagnosed TMJ disorders participated in the study (78 joints; 13 male [33%] and 26 female [67%]; age range, years; mean age ± SD, ± years; median age, 32 years). Magnetic resonance imaging depicted 22 normal joints (28.2%), 21 (26.9%) with anterior disk displacement with reduction, 15 (19.2%) with anterior disk displacement without reduction, and 20 (25.6%) with degenerative changes. Dynamic high-resolution sonography depicted 30 normal joints (38.5%), 22 (28.2%) with anterior disk displacement with reduction, 12 (15.4%) with anterior disk displacement without reduction, and 14 (17.9%) with degenerative changes. Figure 4. Sagittal proton density MRI of a normal TMJ. A, With the mouth closed, the mandibular condyle is within the condylar fossa, with the biconcave disk (arrow) positioned above and anterior to the condyle. The posterior border of the disk is at the 12-o clock position relative to the condyle. B, During mouth opening, the condyle moves below the articular eminence, and the disk (arrow) follows the condyle and is positioned above it. J Ultrasound Med 2015; 34:

6 Compared to MRI, sonography had sensitivity of 74.3%, specificity of 84.2%, accuracy of 77.7%, a PPV of 89.7%, and an NPV of 64.0% for overall diagnosis of disk displacement. For diagnosis of disk displacement with reduction, sonography had sensitivity, specificity, and accuracy of 78.6%, 66.7%, and 73.0%, respectively. For diagnosis of disk displacement without reduction, the sensitivity, specificity, and accuracy were 66.7%, 78.6%, and 73.0%. For a closed mouth, the sensitivity, specificity, and accuracy of sonography for evaluation of disk displacement were 73.0%, 68.3%, and 70.5%. For an open mouth, the values were 61.1%, 88.3%, and 82.1%. Sonography had sensitivity, specificity, and accuracy of 83.1%, 36.8%, and 71.8% for diagnosis of normal condyle morphologic characteristics and 36.8%, 83.1%, and 71.8% for diagnosis of erosive condyle morphologic characteristics. The sensitivity, specificity, and accuracy of sonography were 78.1%, 43.5%, and 57.6% for diagnosis of normal disk morphologic characteristics and 43.5%, 78.1%, and 57.6% for diagnosis of abnormal disk morphologic characteristics. Figure 5. Sagittal proton density MRI of anterior disk dislocation with reduction. A, With the mouth closed, the disk (arrow) is irregular and positioned anterior to the condyle. B, On maximal mouth opening, the disk (arrow) resumes its normal position above the condyle. Figure 6.Sagittal proton density MRI of anterior disk dislocation without reduction. A, With the mouth closed, the disk (arrow) is irregular and positioned anterior to the condyle. B, On maximal mouth opening, the disk (arrow) remains in the abnormal position anterior to the condyle. 80 J Ultrasound Med 2015; 34:75 82

7 Discussion The history and physical evaluation are insufficient for diagnosis of TMJ disorders, raising the need for imaging studies The use of imaging techniques decreases overdiagnosis and overtreatment and, accordingly, decreases financial costs and patients psychological burdens. Panoramic radiography, CT, arthrography, and MRI have been used for depicting TMJ disorders Although MRI is considered the reference standard, its low availability, high cost, and limitations related to several patient conditions restrict its use as a routine imaging technique for investigation of TMJ disorders. Conventional imaging techniques such as panoramic radiography are not useful for depicting the first stages of TMJ disorders. Computed tomography is not able to visualize soft tissue structures such as the articular disk. Furthermore, the radiation exposure from CT does not allow its use as a screening method. Therefore, there is a need for an alternative imaging technique. 6,9 Sonography is a low-cost, noninvasive, quick, safe, and widely available dynamic technique for depicting soft joint tissues. 5 It is also routinely used for depicting dyarthrosis joints such as the shoulder joint. Some reports in the literature have discussed the use of sonography for diagnosis of TMD. The diagnostic accuracy of sonography for detecting disk displacement ranged from 62% to 100%, with sensitivity of 31% to 100%, specificity of 30% to 100%, PPVs of 41% to 100%, and NPVs of 51% to 100%. 1,6,13 The variability of the results is partially explained by the different resolutions of ultrasound equipment. High-resolution ( 12-MHz) transducers allow better visualization of the TMJ than low-resolution devices that were used in older studies. Another factor affecting the results of sonography is the operator s skill and experience, as sonography is an operator-dependent method. In this study, we prospectively investigated the value of dynamic high-resolution sonography for evaluation of TMJ displacement. Patients included in the study had signs such as articular noises, tenderness at the TMJ region, malocclusion, and deviation of the mandible. Patients who were thought to have a muscular origin for the symptoms were excluded. Most of the patients were young women, in correspondence with the well-known fact that TMJ disorders are sex related. 3 Although patients were strictly selected, there were high ratios of normal TMJs and minor degenerative changes. This fact implies the need for an imaging technique in diagnosing and evaluating TMJ disk displacement: the correct diagnosis of TMJ disorders cannot be based on a clinical examination alone 5 ; this consideration also supports the fact that articular noises (clicks) can sometimes be a normal physiologic condition. 3 The sonographic studies were performed by a senior radiologist specializing in sonography with 20 years of experience. State-of-the art high-resolution ultrasound equipment was used, and a strict protocol was followed. The TMJ was examined on axial and coronal scans with the mouth closed and during maximal mouth opening and in real time during mouth opening. Scans were repeated several times for each joint. The sonographic studies were compared with MRI studies performed within 1 week of the sonographic examinations. In our study, the sensitivity of sonography for diagnosis of disk displacement was 74.3%, and specificity was 84.2%. In the literature, the specificity has been, in general, higher than the sensitivity for depicting the disk position, with a wide range of reported sensitivity and specificity values, and the predictive values were even more variable among different studies. 1 We also found that the sensitivity of sonography with the mouth closed was higher than that during mouth opening. Another observation was that it was hard to distinguish between displacement of the disk with reduction and displacement of the disk without reduction, as has also been described in the literature. We suggest that this difficulty is due to suboptimal depiction of the articulation components (condyle, disk, and glenoid fossa) in the open-mouth position, when the position of the disk in this small joint is close to large bone structures. In a previous study, the accuracy rates for diagnosis of internal derangement, disk displacement with reduction, and disk displacement without reduction based on prospective interpretation of high-resolution sonograms were 95%, 92%, and 90%, respectively. 8 It was concluded that when real-time images are interpreted by expert radiologists, dynamic sonography performed during the maximal mandibular range of motion may provide valuable information about TMJ disk displacement. Another study evaluated the accuracy and reliability of sonography for diagnosis of TMJ disk position abnormalities compared to MRI in 41 patients with signs and symptoms of TMJ disorders. 13 Sonography had good accuracy for detecting a normal disk position, showing sensitivity of 65.8% and specificity of 80.4%, resulting in a positive likelihood ratio of 3.35, a negative likelihood ratio of 0.42, and a diagnostic odds ratio of The PPV and NPV were 77.1% and 70.2%, and the overall agreement between the two radiologic techniques was 73.1%. Sonography was less useful for the distinction between disk displacement with and without reduction, in accordance with the results of our study. In another prospective study, the value of J Ultrasound Med 2015; 34:

8 dynamic high-resolution sonography versus clinical diagnosis for evaluation of TMJ derangements was assessed. 14 The study included symptomatic and asymptomatic patients (50 cases each) from an outpatient clinic. The results obtained showed sensitivity of 64%, specificity of 88%, a PPV of 84%, and an NPV of 71%, with accuracy of 76%. This study showed that dynamic high-resolution sonography can provide valuable information about internal derangement of the TMJ in closed- and open-mouth positions. In our study, we found that the accuracy of sonography for diagnosis of a normally shaped disk and normal condyle morphologic characteristics was higher than for the diagnosis of an abnormal disk and condyle morphologic characteristics. A prospective study of 100 patients with signs and symptoms of TMJ disorders by Jank et al 15 aimed to evaluate degenerative changes, effusion, and TMJ disk displacement on high-resolution sonography versus MRI. For determination of degenerative changes, high-resolution sonography had sensitivity of 94%, specificity of 100%, and accuracy of 94%. For detection of effusion, high-resolution sonography yielded sensitivity of 81%, specificity of 100%, and accuracy of 95%. For determination of disk displacement in the closed-mouth position, high-resolution sonography had sensitivity, specificity, and accuracy of 92% each. In the maximal open-mouth position, high-resolution sonography reached sensitivity of 86%, specificity of 91%, and accuracy of 90%. The study concluded that sonography is a useful alternative method but still not able to replace MRI. Our study had some limitations. The patient population was rather small, and each imaging examination was conducted by a single examiner, precluding analysis of reproducibility and interobserver differences. In conclusion, because of its greatly improved nearfield tissue differentiation, current state-of-the art highresolution sonography is a potential imaging method for diagnosis of TMJ disk displacement and for depicting further TMJ disorders, although MRI is still needed in select cases. Better standardization of the sonographic technique and normal parameters need to be determined. References 1. Manfredini D, Guarda-Nardini L. Ultrasonography of the temporomandibular joint: a literature review. Int J Oral Maxillofac Surg 2009; 38: Tomas X, Pomes J, Berenguer J, et al. MR imaging of temporomandibular joint dysfunction: a pictorial review. Radiographics2006; 26: Scrivani SJ, Keith DA, Kaban LB. Temporomandibular disorders. N Engl J Med 2008; 359: Badel T, Marotti M, Keros J, Kern J, Krolo I. Magnetic resonance imaging study on temporomandibular joint morphology. Coll Antropol 2009; 33: Petr T. Methods of imaging in the diagnosis of temporomandibular joint disorders. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 2007; 151: Cakir-Ozkan N, Sarikaya B, Erkorkmaz U, Aktürk Y. Ultrasonographic evaluation of disc displacement of the temporomandibular joint compared with magnetic resonance imaging. J Oral Maxillofac Surg 2010; 68: Siegfried J, Stephan H. Sonographic Investigation of the temporomandibular joint in patients with juvenile idiopathic arthritis: a pilot study. Arthritis Rheum 2007; 57: EmshoffR, Jank S, Bertram S, Rudisch A, Bodner G. Disk displacement of the temporomandibular joint: sonography versus MR imaging. AJR Am J Roentgenol 2002; 178: Takafumi H, Jusuke I, Jun-ichi K, Kazuhiro Y. The accuracy of sonography for evaluation of internal derangement of the temporomandibular joint in asymptomatic elementary school children: comparison with MR and CT. AJNR Am J Neuroradiol 2001; 22: Koh KJ, List T, Petersson A, Rohlin M. Relationship between clinical and magnetic resonance imaging diagnoses and findings in degenerative and inflammatory temporomandibular joint diseases: a systematic literature review. J Orofac Pain 2009; 23: Landes CA, Sader R. Sonographic evaluation of the ranges of condylar translation and of temproromandicular joint space as well as first comparison with symptomatic joints. J Craniomaxillofac Surg 2007; 35: Vilanova JC, Barceló J, Puig J, Remollo S, Nicolau C, Bru C. Diagnostic imaging: magnetic resonance imaging, computed tomography and ultrasound. Semin Ultrasound CT MR 2007; 28: Tognini F, Manfredini D, Bosco D, Melchiorre M. Comparison of ultrasonography and magnetic resonance imaging in the evaluation of temporomandibular joint disc displacement. J Oral Rehabil2005; 32: Byahatti SM, Ramamurthy BR, Mubeen M, Agnihothri PG. Assessment of diagnostic accuracy of high-resolution ultrasonography in determination of temporomandibular joint internal derangement. Indian J Dent Res 2010; 21: Jank S, Emshoff R, Norer B, et al. Diagnostic quality of dynamic highresolution ultrasonography of the TMJ: a pilot study. Int J Oral Maxillofac Surg 2005; 34: Styles C, Whyte A. MRI in the assessment of internal derangement and pain within the temporomandibular joint: a pictorial essay. Br J Oral Maxillofac Surg 2002; 40: Muller L, Kellenberger CJ, Cannizzaro E, et al. Early diagnosis of temporomandibular joint involvement in juvenile idiopathic arthritis: a pilot study comparing clinical examination and ultrasound to magnetic resonance imaging. Rheumatology 2009; 48: Bas B, Yılmaz N, Gökce E, Akan H. Diagnostic value of ultrasonography in temporomandibular disorders. J Oral Maxillofac Surg2011; 69: J Ultrasound Med 2015; 34:75 82

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