Evaluation of Temporomandibular Joint Disk Displacement in Asymptomatic Volunteers Using Magnetic Resonance Imaging

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1 Int J Oral-Med Sci 14(1):21-27, Original Article Evaluation of Temporomandibular Joint Disk Displacement in Asymptomatic Volunteers Using Magnetic Resonance Imaging Takashi Uchida, 1,4 Osamu Komiyama, 2,4 Yasuhiro Okamoto, 1,4 Takashi Iida, 2,4 Masanobu Wakami, 3,4 and Takanori Ito, 1,4 Departments of 1 Oral Diagnosis, 2 Oral Function and Rehabilitation, and 3 Crown Bridge Prosthodontics, Nihon University, School of Dentistry at Matsudo, Chiba , Japan 4 Research Institute of Oral Science, Nihon University, School of Dentistry at Matsudo, Chiba , Japan Article History Received 30 April 2015 Accepted 26 June 2015 Keywords : temporomandibular joint, magnetic resonance imaging, asymptomatic volunteers, disk displacement Abstract Objective: The purpose of this study was to explore magnetic resonance imaging (MRI) findings of bilateral temporomandibular joints with no signs or symptoms of temporomandibular dysfunction to ascertain how disk displacement develops in both joints. Study design: Subjects comprised 54 asymptomatic volunteers (38 males, 16 females; average age 21.2±2.8 years). All 108 temporomandibular joints were analyzed by MRI. Results: Unilateral or bilateral disk displacement was present in 37% of subjects; 25 of 108 joints were classified as partial disk displacement (PDD) and 5 of 108 joints were classified as complete disk displacement (CDD). The numbers of subjects with unilateral and bilateral disk displacement were the same. In cases of bilateral disk displacement, the condition of displacement was likely to match on both sides. Conclusions: CDD may occur without temporomandibular dysfunction, and when disk displacement is bilateral, the condition of both disk displacements is often comparable. Introduction Disk displacement is often encountered in patients with temporomandibular disorders,(1,2) and diagnosing disk displacement is a major first step in diagnosing temporomandibular disorders. In recent years, the popularization of MRI has made possible further noninvasive diagnosis for the condition of temporomandibular joint disk. Such observations can identify disk displacement not just in individuals with temporomandibular disorders, but in those with no signs or symptoms of temporomandibular dysfunction,(1-10) suggesting that disk displacement may be a precursor of temporomandibular disorders. The jaw has a bilateral articular structure, and malfunctions on one side can affect the other side. In patients with temporomandibular disorders with unilateral symptoms, disk displacement without signs and symptoms is observed on the nonpain side, just as in asymptomatic patients.(11) Indeed, there is a Correspondence to : Takashi Uchida uchida.takashi@nihon-u.ac.jp possible bilateral temporomandibular joint (TMJ) disk displacement in asymptomatic volunteers deemed earlystage disk derangement of TMJ. Therefore, since bilateral TMJ examination with consideration of disk displacement without signs and symptoms is needed for making a diagnosis of jaw dysfunction, the MRI findings were evaluated to explore bilateral TMJ disk displacement at the early stage of disk derangement in asymptomatic volunteers. Materials and Methods Subjects The subjects were 54 students and faculty members at the Nihon University School of Dentistry at Matsudo (38 male, 16 female; age range 19 to 28 years; average age 21.2 ±2.8 years). All 108 TMJs were analyzed by MRI. Inclusion criteria were: no past history of orthodontic therapy; no past history of stomatognathic abnormalities, such as limited jaw opening, joint sounds, or TMJ pain; and no missing teeth, except for third molars, as confirmed by

2 22 Int J Oral-Med Sci 14(1):21-27, 2015 Fig. 1 Oblique sagittal MR images of the TMJ of complete disk displacement (CDD) with mouth closed position. The disk is anteriorly displacement in all images. Arrow indicates the posterior band of the disk A: Medial side E: Distal side Fig. 2 Oblique sagittal MR images of the TMJ of partial disk displacement (PDD) with mouth closed position. A and B show the normal superior position of the disk. But C, D and E show the anterior disk displacement and disk displacement was gradually increased with E from C. Arrow indicates the posterior band of the disk. A: Medial side E:Distal side oral examination. Both TMJs were analyzed in all subjects. Based on the The nature of the present study was explained explicitly system described by Larheim et al.,(2) the position of the to the subjects before obtaining their consent. The study articular disk was classified on proton-weighted images was approved by the ethics review board of the Nihon during mouth closing into 1 of 11 categories of displacement University School of Dentistry at Matsudo (Approval direction: normal disk position (category of normal superi- number: EC09-020). or); complete disk displacement (CDD), defined as displacement seen on all sagittal MR images (categories of complete MR imaging anterior, complete anterolateral, and complete anterome- The left and right TMJs of each subject were examined dial)(fig. 1); and partial disk displacement (PDD), defined by MRI as the subjects opened and closed their mouths. MRI as displacement seen in some, but not all MR images was performed using a Signa Horizon 1.0T (General (categories of partial anterior in the lateral part, partial Electric Medical System Co, Milwaukee, Wisconsin / USA) anterior in the medial part, partial anterolateral, partial equipped with a 3.5-inch surface coil (General Electric) on anteromedial, lateral, medial, and posterior)(fig. 2). As the both sides. Imaging conditions were: fast spin echo; Field of subjects opened their mouths, whether the disk was reduced view = 12 cm; Repetition time = 1150 msec; Echo time = 17 was ascertained. In patients with disk displacement, the msec; matrix = 224 x 256; and slice thickness = 3 mm. signal intensity of the retrodiscal tissue was examined

3 Int J Oral-Med Sci 14(1):21-27, Table 1 Association between gender and disk displacement (n=54) Table 3 Distribution of disk displacement according to main categories (n=108) Table 4 Bi-or unilateral disk displacement (n=54) Table 2 Distribution of disk dilisplacement according to category (n=108) Table 5 Distribution of disk displacement of right and left side according to main categories (n=54) during mouth closing. Joint effusion during mouth closing, as observed on T2-weighted images, was also evaluated. The MR images were assessed by three dentists with a minimum of five years of clinical experience in temporomandibular joint therapy. Data Analysis SPSS (Version 17.0J)(SPSS Co, Shibuya, Tokyo / Japan) was used for the chi-squared test, with the level of significance set at p<0.05. Results The observations confirmed unilateral or bilateral disk displacement in 20 of the 54 subjects (37.0%). The incidence of displacement was 34.2% (13/38) in males and 43.8% (7/16) in females; the incidence of displacement was significantly higher in females (Table 1). Displacement was observed in 30 of the 108 joints (27.8%). The most common type of displacement was partial anterolateral displacement (9.3%, n = 10), followed by medial displacement (6.5%, n = 7). Displacement in the lateral direction or the medial direction was observed in 13 and 15 joints, respectively (Table 2). PDD was observed in 25 of the 108 joints (23.1%), and CDD was observed in 5 of the 108 joints (4.6%). The incidence of PDD was significantly higher than that of CDD (Table 3). The incidence of unilateral temporomandibular joint displacement was 18.5% (10/54). The incidence of bilateral temporomandibular joint displacement was identical (10/54; Table 4). Of the 10 subjects with bilateral displacement, PDD was observed on both sides in eight subjects and CDD was observed on both sides in one subject. The degree of displacement differed between the two sides in only one subject. The degree of displacement was the same in all other subjects with bilateral displacement (Table 5). Joint effusion was observed in 6 of the 108 joints; joint effusion was observed in unilateral cases only. Observed only in joints with displacement, joint effusion was detected in four PDD joints and two CDD joints (Table 6). During

4 24 Int J Oral-Med Sci 14(1):21-27, 2015 Table 6 Number of joints with joint effusion (n=108) mouth opening, the disk was reduced in all joints. The signal intensity of the retrodiscal tissue was low for all 30 joints with displacement. Discussion MRI was used in the present study to assess bilateral TMJs, identifying disk displacement in 37% of asymptomatic volunteers, with a significantly higher incidence of disk displacement in females than in males. Disk displacement was confirmed in approximately 28% of all joints: approximately 23% of cases involving PDD and approximately 5% of cases involving CDD. The number of subjects with unilateral displacement and the number of subjects with bilateral displacement were identical. In many subjects with bilateral displacement, the degree of displacement was the same on both sides. Additionally, while the cases were not always accompanied by symptoms, the incidence of joint effusion was high in CDD. In all cases with displacement, the signal intensity of the retrodiscal tissue was low. In asymptomatic volunteers, past studies have found an incidence of disk displacement ranging from 35% to 48% in females and from 24% to 32% in males. Disk displacement is more common in females.(2,5,7) The present study had similar findings. Either unilateral or bilateral disk displacement was observed in roughly one of every two females and one of every three males. With respect to sex differences, Katzberg et al.(3) reported that there is a clear association between disk displacement and TMJ pain and dysfunction, and a high ratio of females to males in patients presenting with TMJ pain and dysfunction, but only a slight preponderance of females versus males for disk displacement in a nonpatient population. Systemic joint laxity is more pronounced in males than females, resulting in a higher incidence of disk displacement.(7) With respect to the direction of disk displacement in asymptomatic volunteers, Tominaga et al.(12) stated that the change of the disk position would be likely to start from the lateral position of the disk, while Katzberg et al.(3) found that anterior and anterolateral displacements were the most common. Larheim et al.(2) reported that displacement in the lateral direction is common. However, Foucart et al(15) reported that most of the sideways displacement occurred in a medial direction, and Scmitter et al.(10) reported that, in most cases, the disk was located medially relative to the condyle, and a medial position of the disk in the coronal plane seems to be physiologic. Meanwhile, Haiter-Nio et al.(8) reported that the number of displacements in the lateral direction is equal to the number of displacements in the medial direction. In short, the reports are conflicting. Crowley et al.(13) found that interpretation of disk position over the lateral pole is difficult, because this is the area where the joint space is narrowest and the disk is often thinned. Katzberg et al.(3) found the attachment of the superior belly of the lateral pterygoid muscle onto the medial aspect of the joint capsule, and they believed that muscle spasm of the superior belly of the lateral pterygoid muscle is a cause of disk displacement; this has led to the speculation that most disk displacements are in the medial direction. Chewing exerts considerable stress to the lateral regions of the joint,(14) tending to stretch the attachment of the lateral regions of the joint; the lateral capsular attachment is weak and easily stretched. In contrast, the medial capsular attachment is stronger and reinforced by the insertions of lateral pterygoid.(15) According to Foucart et al.(16), lateral partial anterior disk displacement is the first phase of disk displacement pathology. No conclusion has been reached on displacement in the mesiolateral direction. The observations from the present study suggest that partial anterolateral displacement is the most common, but since the number of displacements in the lateral direction and the number of displacements in the medial direction were almost the same, it is difficult to identify a specific direction in which disk displacement is more likely to occur at an early stage. With respect to unilateral versus bilateral displacement, Larheim et al.(2) reported 15 unilateral displacements and 8 bilateral displacements, concluding that unilateral displacement is more common. Tallents et al.(4) reported 14 unilateral and 13 bilateral cases; Ribeiro et al.(7) reported 10 unilateral and 9 bilateral cases. In these studies, the numbers of unilateral and bilateral cases were comparable. The present study identified 10 unilateral and 10 bilateral cases. Of the 10 bilateral cases, the condition of displacement was the same for nine. In most bilateral cases, the comparable bilateral displacements may be due to the morphology of the two joints. Galante et al.(17) reported no significant

5 Int J Oral-Med Sci 14(1):21-27, differences in angular and linear measurements in the articular fossa with temporomandibular joint dysfunction, but Sülün et al.(18) reported that not only a steeper slope but also the ratio of the angulations at different depths of the fossa may have some relationshipto disk displacement. Pullinger et al.(19) applied multifactorial analysis to examine the relationshipbetween the mandibular head and eminence. Reviewing past studies of the bilateral temporomandibular joints of temporomandibular disorder patients with unilateral symptoms, Kozeniauskase et al.(20) performed arthrography and found temporomandibular internal derangements on the asymptomatic TMJs as well. Rudish et al.(11) performed MRI of 41 temporomandibular disorder patients with unilateral pain and confirmed disk displacement on the nonpain side in 19 patients. Emshoff et al.(21) reported displacement in 57.1% of pain-free joints among temporomandibular disorder patients. Thus, disk displacement in one TMJ is related to disk displacement on the contralateral side,(3) so that even when symptoms are unilateral, disk displacement is often bilateral; and in bilateral disk displacement, the condition of displacement is likely to match on both sides. Since disk displacement could represent a congenital normal anatomic variant,(22) joint morphologies, which tend to result in displacement, arise symmetrically. Larheim et al.(2) classified disk displacements as PDD or CDD, finding that PDD was more common in asymptomatic volunteers, but CDD was more common in temporomandibular disorder patients. Although disk displacement is not always associated with pain and dysfunction,(21) the onset of temporomandibular disorders is higher in CDD than in PDD. In the present study, the incidence of PDD was significantly higher. However, some subjects had bilateral CDD, suggesting that the progression from PDD to CDD does not always result in symptoms. Even when symptoms are absent in certain joint morphologies, displacement may advance to CDD on both sides. The degree of displacement failed to match between the two sides in one subject, and the number of subjects with unilateral displacement was comparable to the number of subjects with bilateral displacement. While this indicates that joint anatomical morphology may be a factor inducing disk displacement, disk displacement is believed to be caused not just by anatomical morphologic characteristics, but also by other accompanying factors. Joint effusion is often observed in painful TMJs, and a strong association was seen between MR evidence of joint effusion and pain.(23) Examining asymptomatic volunteers, Larheim et al.(24) reported incidences of joint effusion in patients with and without displacement of 27.6% and 4.2%, respectively, pointing to a significant association between joint effusion and disk displacement. In the present study, joint effusion was seen only in joints with displacement, not in joints without displacement. Particularly in CDD, joint effusion was seen in two of the five joints, suggesting that joint effusion is more closely related to disk displacement than to pain. However, joint effusion was only seen with unilateral cases, not bilateral cases. With regard to the retrodiscal tissue, signal intensity was high in painful temporomandibular joints.(25) Low signal intensity has been shown to be related to retrodiscal tissue fibrosis, and longstanding disk displacement contributes to retrodiscal tissue fibrosis.(26) Sakuma et al.(27) asserted that the decreased T 1 signal intensity clinically observed in the retrodiscal tissue of TMJs may not suggest an increased density of collagen fibers. The relationshipbetween temporomandibular pain and low signal intensity in the retrodiscal tissue remains unclear.(27) In the present study, the signal intensity of the retrodiscal tissue was low in all 40 joints with disk displacement. While it is difficult to ascertain whether low signal intensity is attributable to retrodiscal tissue fibrosis, the results indicate that if pain is absent, the signal intensity of the retrodiscal tissue is likely to be low. Conclusions In the present study, MRI was performed to examine the left and right temporomandibular joints of asymptomatic volunteers. The results indicate that CDD may occur without temporomandibular dysfunction, and that when displacement is bilateral, the conditions of the left and right displacements are often comparable. Furthermore, the incidence of joint effusion is high in asymptomatic CDD patients, and the signal intensity of retrodiscal tissue is low in the presence of disk displacement. Diagnostic imaging of the TMJ may identify disk displacement or internal derangement in asymptomatic joints, pointing to a need to assess the conditions of the left and right TMJs. In short, diagnosing temporomandibular disorders, planning treatments, predicting prognoses, or assessing therapeutic effects based solely on unilateral clinical symptoms is likely to be inadequate; instead, we should assess the left and right TMJs using diagnostic imaging.

6 26 Int J Oral-Med Sci 14(1):21-27, 2015 References 1. Tasaki MM, Westesson PL, Isberg AM, Ren YF, Tallents RH: Classification and prevalence of temporomandibular joint disk displacement in patients and symptom-free volunteers. Am J Orthod Dentofacial Orthop, 109: , Larheim TA, Westesson P, Sano T: Temporomandibular joint disk displacement: comparison in asymptomatic volunteers and patients. Radiology, 218: , Katzberg RW, Westesson PL, Tallents RH, Drake CM: Anatomic disorders of the temporomandibular joint disc in asymptomatic subjects. J Oral Maxillofac Surg, 54: , Tallents RH, Katzberg RW, Murphy W, Proskin H: Magnetic resonance imaging findings in asymptomatic volunteers and symptomatic patients with temporomandibular disorders. J Prosthet Dent, 75: , Morrow D, Tallents RH, Katzberg RW, Murphy WC, Hart TC: Relationship of other joint problems and anterior disc position in symptomatic TMD patients and in asymptomatic volunteers. J Orofac Pain, 10: 15-20, 1996 Winter. 6. Rammelsberg P, Pospiech PR, Jäger L, Pho Duc JM, Böhm AO, Gernet W: Variability of disk position in asymptomatic volunteers and patients with internal derangements of the TMJ. Oral Surg Oral Med Oral Pathol Oral Radiol Endod, 83: , Ribeiro RF, Tallents RH, Katzberg RW, Murphy WC, Moss ME, Magalhaes AC, Tavano O: The prevalence of disc displacement in symptomatic and asymptomatic volunteers aged 6 to 25 years. J Orofac Pain, 11: 37-47, Haiter-Neto F, Hollender L, Barclay P, Maravilla KR: Disk position and the bilaminar zone of the temporomandibular joint in asymptomatic young individuals by magnetic resonance imaging. Oral Surg Oral Med Oral Pathol Oral Radiol Endod, 94: , Katzberg RW, Tallents RH: Normal and abnormal temporomandibular joint disc and posterior attachment as depicted by magnetic resonance imaging in symptomatic and asymptomatic subjects. J Oral Maxillofac Surg, 63: , Schmitter M, Kress B, Ludwig C, Koob A, Gabbert O, Rammelsberg P: Temporomandibular joint disk position assessed at coronal MR imaging in asymptomatic volunteers. Radiology, 236: , Rudisch A, Innerhofer K, Bertram S, Emshoff R: Magnetic resonance imaging findings of internal derangement and effusion in patients with unilateral temporomandibular joint pain. Oral Surg Oral Med Oral Pathol Oral Radiol Endod, 92: , Tominaga K, Konoo T, Morimoto Y, Tanaka T, Habu M, Fukuda J: Changes in temporomandibular disc position during growth in young Japanese. J Dentomaxillofac Radiol, 36: , Crowley C, Wilkinson T, Piehslingher E, Wilson D, Czerny C: Correlations between anatomic and MRI sections of human cadaver temporomandibular joints in the coronal and sagittal planes. J Orofac Pain, 10: , Tanne K, Tanaka E, Sakuda M: The elastic modulus of the temporomandibular joint disc from adult dogs. J Dent Res, 70: , Whyte AM, McNamara D, Rosenberg I, Whyte AW: Magnetic resonance imaging in the evaluation of temporomandibular joint disc displacement--a review of 144 cases. Int J Oral Maxillofac Surg, 35: , Foucart JM, Carpentier P, Pajoni D, Marguelles-Bonnet R, Pharaboz C: MR of 732 TMJs: anterior, rotational, partial and sideways disc displacements. Eur J Radiol, 28: 86-94, Galante G, Paesani D, Tallents RH, Hatala MA, Katzberg RW, Murphy W: Angle of the articular eminence in patients with temporomandibular joint dysfunction and asymptomatic volunteers. Oral Surg Oral Med Oral Pathol Oral Radiol Endod, 80: , Sülün T, Cemgil T, Duc JM, Rammelsberg P, Jäger 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, 92: , Pullinger AG, Seligman DA: Multifactorial analysis of differences in temporomandibular joint hard tissue anatomic relationships between disk displacement with and without reduction in females. J Prosthet Dent, 86: , Kozeniauskas JJ, Ralph WJ: Bilateral arthrographic evaluation of unilateral temporomandibular joint pain and dysfunction. J Prosthet Dent, 60: , Emshoff R, Innerhofer K, Rudisch A, Bertram S: Relationship between temporomandibular joint pain and magnetic resonance imaging findings of internal derangement. Int J Oral Maxillofac Surg, 30: , Paesani D, Salas E, Martinez A, Isberg A: Prevalence of temporomandibular joint disc displacement in infants and young children. Oral Surg Oral Med Oral Pathol Oral Radiol Endod, 87: 15-19, Westesson PL, Brooks SL: Temporomandibular joint: relationshipbetween MR evidence of effusion and the presence of pain and disk displacement. Am J Roentgenol, 159: , Larheim TA, Katzberg RW, Westesson PL, Tallents RH, Moss ME: MR evidence of temporomandibular joint fluid and condyle marrow alterations: occurrence in asymptomatic volunteers and symptomatic patients. Int J Oral Maxillofac Surg, 30: , Suenaga S, Hamamoto S, Kawano K, Higashida Y, Noikura T: Dynamic MR imaging of the temporomandibular joint in

7 Int J Oral-Med Sci 14(1):21-27, patients with arthrosis: relationship between contrast enhancement of the posterior disk attachment and joint pain. Am J Roentgenol, 166: , Westesson PL, Paesani D: MR imaging of the TMJ. Decreased signal from the retrodiscal tissue. Oral Surg Oral Med Oral Pathol, 76: , Sakuma K, Sano T, Yamamoto M, Tachikawa T, Okano T: Does decreased T1 signal intensity in the retrodiscal tissue of the temporomandibular joint reflect increased density of collagen fibres? Dentomaxillofac Radiol, 32: , 2003.

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