Note: This copy is for your personal, non-commercial use only. To order presentation-ready copies for distribution to your colleagues or clients, contact us at www.rsna.org/rsnarights. ORIGINAL RESEARCH

Linda Z. Arvidsson, DDS Hans-Jørgen Smith, PhD, MD Berit Flatø, PhD, MD Tore A. Larheim, PhD, DDS

Purpose:

To assess the long-term temporomandibular joint (TMJ) manifestations of juvenile idiopathic arthritis (JIA), as depicted at computed tomography (CT) and magnetic resonance (MR) imaging, in 47 adult patients.

Materials and Methods:

The study was approved by a regional committee for medical research ethics, and informed consent was obtained from all patients. Forty-seven patients with JIA (32 women, 15 men; mean age, 35 years) were examined, on average, 30 years after the initial diagnosis. The findings of TMJ imaging, including CT and MR imaging, were evaluated by three observers. Bone and disk abnormalities, joint effusion, bone marrow abnormalities, and contrast enhancement were analyzed.

Results:

The TMJs were involved in 33 (70%) of the 47 patients with JIA, with bilateral involvement in 29 patients. Slight to moderate contrast enhancement was observed on the images obtained in 14 (42%) of the 33 patients with TMJ JIA abnormalities. All main joint components were abnormal in 28 of the 33 patients, mainly showing flat deformed condyles, wide flat fossae, and thin or perforated disks in the normal position, or absent disks. Condylar concavity or bifidity, and secondary osteoarthritis were found in approximately half of the abnormal joints.

Conclusion:

Long-term JIA manifestations in the TMJs, as demonstrated at CT and MR imaging, were frequent, usually bilateral, and characterized by mandibular condyle and temporal bone deformities, abnormal disk morphology, and, rather frequently, osteoarthritis and mild synovitis. q

RSNA, 2010

1

From the Department of Maxillofacial Radiology, Institute of Clinical Dentistry, University of Oslo, PO Box 1109, Blindern, 0317 Oslo, Norway (L.Z.A., T.A.L.); and Departments of Radiology (H.J.S.) and Rheumatology (B.F.), Rikshospitalet, Oslo University Hospital and University of Oslo, Oslo, Norway. Received September 29, 2009; revision requested November 3; revision received December 23; accepted January 6, 2010; final version accepted January 14. Supported by grants from the University of Oslo. L.Z.A. supported by a doctoral stipend from the University of Oslo. Address correspondence to L.Z.A. (e-mail: l.z.arvidsson@ odont.uio.no). q

RSNA, 2010

Radiology: Volume 256: Number 1—July 2010

n

radiology.rsna.org

191

n MUSCULOSKELETAL IMAGING

Temporomandibular Joint Findings in Adults with Long-standing Juvenile Idiopathic Arthritis: CT and MR Imaging Assessment1

MUSCULOSKELETAL IMAGING: CT and MR of Temporomandibular Joint Findings in Idiopathic Arthritis

J

uvenile idiopathic arthritis (JIA) is the most common autoimmune autoinflammatory musculoskeletal disease in childhood worldwide, affecting 1 in 1000 children younger than 16 years and manifesting in girls more frequently (1,2). This disease was formerly referred to as juvenile rheumatoid arthritis in the United States and as juvenile chronic arthritis in Europe. The International League of Associations for Rheumatology updated the classification system in 2001 to unite these two terms, taking into account the heterogeneity of the disease (2,3). JIA is subdivided into categories that are based on the number of joints affected and the presence or absence of specific serologic findings and systemic manifestations. In contrast to adultonset rheumatoid arthritis affecting small joints in the hands and feet, JIA predominantly involves the large joints— most frequently the knees, wrists, and ankles (1). Localized growth disturbances, bone fusion, atlantoaxial subluxation in the cervical spine, and mandibular underdevelopment (ie, micrognathia) are characteristic features (1). The temporomandibular joint (TMJ) has been dubbed “the forgotten joint” in pediatric rheumatology (4) because it is difficult to apply the clinical definition of arthritis (3) in this location (4,5). Relatively recent imaging studies have revealed that the TMJ is frequently affected in children with JIA (6–8); it has even been suggested that this is one of the most frequently involved joints in patients with this disease (5). However, little is known about the outcome of long-standing JIA in the TMJs. The few radiographic TMJ studies of adult JIA

Advances in Knowledge n Bilateral bone deformation is a frequent imaging feature of longstanding juvenile idiopathic arthritis (JIA) of the temporomandibular joint (TMJ). n Destroyed, fragmented, or evenly thinned disks are common in adults with JIA TMJ involvement. n Mild synovitis is relatively frequent in adults with JIA TMJ involvement. 192

have been either performed in small select patient series or limited to panoramic radiography (9–11). Because, to our knowledge, there has been no comprehensive study to follow up patients from childhood to adulthood to analyze the TMJ and mandibular growth abnormalities and this information is necessary for prognostic and therapeutic considerations, we sought to study such a population (5). The aim of this study was to assess the long-term TMJ manifestations of JIA, as demonstrated at computed tomography (CT) and magnetic resonance (MR) imaging, in 47 adult patients.

Materials and Methods This study was approved by the Regional Committee for Medical Research Ethics of Southern Norway, and informed consent was provided by all patients. A prospective longitudinal study involving 103 children was initiated in 1976. At that time, juvenile rheumatoid arthritis was the standard term used to refer to childhood arthritis in Norway (12). Such patients were hospitalized at Oslo Sanitetsforening Rheumatism Hospital (Oslo, Norway) and were selected consecutively, without regard to the TMJ condition, to be examined at the Faculty of Dentistry, University of Oslo. The baseline examinations were performed between 1976 and 1979 (13,14), and three follow-up examinations were performed in 2-year intervals. Disease variables such as age at onset, onset type, physical function (15), number of active joints (12), and disease activity were assessed, and radiologic and clinical data on the TMJs were collected (13). Disease activity was assigned a grade of 1–4, where 1 indicated remission and 4 indicated severe disease activity. Between 2002 and 2006, we attempted to contact the 103 patients to invite them to undergo a repeat exami-

Implication for Patient Care n CT and MR imaging in both symptomatic and asymptomatic TMJs in adult patients with JIA depict fairly overt changes.

Arvidsson et al

nation. We were able to contact 90 of them; eight were deceased, three could not be located, and two lived abroad. Twenty-eight of the 90 invited patients did not undergo the repeat examination: They either declined or did not reply. In addition, two patients were only partially examined and were therefore excluded. Thus, 60 patients (44 women, 16 men; mean age, 35.2 years) underwent complete repeat examinations a mean of 29.8 years after disease onset (16). The patients were clinically examined by rheumatologists, and their disease was recategorized according to the International League of Associations for Rheumatology classification of JIA (3) by one of the authors (B.F.), with old and new patient files available (16). In all patients, the TMJs and masticatory muscles were clinically examined (L.Z.A., more than 5 years experience in maxillofacial radiology). The patients were asked to report pain or tenderness at palpation, rest, or motion by pointing to the area of the TMJ or masticatory muscles. Mouth-opening capacity was measured between the incisal edges of the upper and lower first incisors. The lower limit for normal mouth-opening capacity was set at 38 mm for women and 42 mm for men (17). Imaging of the TMJs included CT and MR imaging. Because 13 patients declined to undergo MR examination, in this article we report the findings in the 47 patients (32 women, 15 men)

Published online 10.1148/radiol.10091810 Radiology 2010; 256:191–200 Abbreviations: JIA = juvenile idiopathic arthritis TMJ = temporomandibular joint Author contributions: Guarantors of integrity of entire study, L.Z.A., T.A.L.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, L.Z.A., B.F., T.A.L.; clinical studies, all authors; statistical analysis, L.Z.A.; and manuscript editing, L.Z.A., B.F., T.A.L. Authors stated no financial relationship to disclose.

radiology.rsna.org

n

Radiology: Volume 256: Number 1—July 2010

MUSCULOSKELETAL IMAGING: CT and MR of Temporomandibular Joint Findings in Idiopathic Arthritis

Table 1 Disease Variables and TMJ Involvement at Baseline and 2-year Follow-up Variable Female patients Age at disease onset (y)* Onset type Pauciarticular Polyarticular Systemic Age at baseline (y)* Disease duration (y)* Physical function class (1–4)*† No. of active joints* Disease activity grade (1–4)* TMJ involvement at baseline TMJ involvement at 2-y follow-up

Participants (n = 47)

Nonparticipants (n = 56)

32 (68) 5.5 6 2.9

39 (70) 5.4 6 3.6

28 (60) 12 (26) 7 (15) 8.8 6 2.6 3.3 6 2.7 1.6 6 0.7 6.4 6 4.6 2.5 6 0.7 18 (38) 24 (51)

36 (64) 13 (23) 7 (12) 9.2 6 3.2 3.8 6 3.1 1.8 6 0.7 8.2 6 6.0 2.7 6 0.9 24 (43) 28 (50)

Note.—Unless otherwise noted, data are numbers of patients, with percentages in parentheses. Differences between participating and nonparticipating patients were nonsignificant at all comparisons. * Mean values 6 standard deviations. †

Physical function according to Steinbrocker et al (15).

Table 2 Disease Variables in 47 Patients with JIA Variable Age at disease onset (y) Age at baseline (y) Age at final examination (y) Disease duration at baseline (y) Disease duration at final examination (y) Follow-up time (y) Variables assessed after mean of 27 years† No. of active joints No. of joints with LROM Physicians’ global assessment score (0–100) HAQ physical function score (0–3) Patients’ global assessment score (0–100)

Range

Mean*

0.7–11.9 3.9–14.9 29.0–43.6 0.1–9.6 24.2–37.5 22.6–29.3

5.5 6 2.9 8.8 6 2.6 35.3 6 3.4 3.3 6 2.7 29.8 6 3.3 26.5 6 1.5

0–50 0–64 0–83 0.00–2.00 0–72

5.7 6 10.1 13.6 6 16.7 18.7 6 24.6 0.57 6 0.63 21.2 6 20.0

Note.—Disease variables are based on those of Fries et al (25) and Brewer and Giannini (26). * Mean values 6 standard deviations. †

HAQ = health assessment questionnaire, LROM = limited range of motion.

who were examined with both imaging modalities. The results of the conventional longitudinal TMJ examinations performed in the 60 patients, which consisted of panoramic, transcranial, and, occasionally, tomographic radiography at baseline and at 2-year, 4-year, and final follow-up, were recently reported (16). CT examinations of the TMJs were performed with a LightSpeed Ultra Radiology: Volume 256: Number 1—July 2010

n

scanner (GE Medical Systems, Milwaukee, Wis) by using thin (0.625– 1.25-mm) sections, a bone algorithm, and axial sections parallel to the hard palate. The CT examination results were viewed in the axial and reformatted oblique-coronal and oblique-sagittal planes. MR imaging was performed at 1.5 T with a Magnetom Sonata or Magnetom Avanto MR unit (Siemens, Erlangen,

radiology.rsna.org

Arvidsson et al

Germany) by using a wide flex coil (Magnetom Sonata) or 12-channel head coil (Magnetom Avanto). First, nonenhanced oblique-sagittal T1-weighted images (repetition time msec/echo time msec, 400/15 or 717/12) and intermediate- or T2-weighted fast spin-echo images (3090/14–85 or 2800/14–82) were obtained. Then, contrast material– enhanced oblique-sagittal and obliquecoronal T1-weighted fast spin-echo images were obtained with the patients’ mouths closed. Contrast-enhanced oblique-sagittal gradient-echo images (125/11 or 133/11, 30° flip angle) were obtained with the patients’ mouths open. All sequences were performed with a section thickness of 3 mm and an intersection gap of 0.3 mm, a matrix of 512 3 (305–512), and a field of view of 140–160 mm. Contrast enhancement was induced with intravenous injection of 0.1 mmol gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany) per kilogram of body weight. Contrast-enhanced MR imaging was commenced within half a minute after the contrast medium injection, meaning that the center of k-space for the two contrast-enhanced sequences (sagittal and coronal) occurred approximately 3–8 minutes after administration of the contrast medium. Dynamic contrast-enhanced MR imaging was not performed. All CT and MR images were studied separately by three radiologists (L.Z.A., H.J.S., T.A.L.), and any disagreements were discussed until a consensus was reached. One observer (L.Z.A.) had more than 5 years experience, and the other two (H.J.S., T.A.L.) had more than 20 years experience evaluating CT and MR imaging TMJ data. The radiologists were blinded to the clinical symptoms and prior TMJ disease history. We defined a normal TMJ as having an oval mandibular condyle in the axial plane and a convex, round, or flat condylar contour in the oblique-coronal plane (18). In the oblique-sagittal plane, the condyle should be round and the fossa-eminence should be S shaped, with the cortical outline intact, smooth, and even in thickness; however, there might be a slight condylar flattening (19). 193

MUSCULOSKELETAL IMAGING: CT and MR of Temporomandibular Joint Findings in Idiopathic Arthritis

Table 3

edema of the condyle, and an increased amount of joint fluid (24) were documented. A joint with an anteriorly displaced disk, normal bone tissue, and no contrast enhancement was considered to have internal derangement only. Statistical evaluations to compare baseline data between the 47 participants and 56 nonparticipants in the cohort of 103 patients were performed by using x2 testing for categorical variables. Continuous variables were compared by using a two-sided sample t test. The significance level was set at 5%, and the statistical analyses were performed by using SPSS, version 16.0, software (SPSS, Chicago, Ill). Owing to the small numbers of patients in the JIA subgroups, no testing for the significance of imaging findings was performed.

Distributions of Patients and TMJ Imaging Findings in Different JIA Categories ILAR Category Oligoarthritis Extended oligoarthritis Polyarthritis, RF negative Polyarthritis, RF positive Systemic arthritis Enthesitis-related arthritis

All Patients (n = 47)

Patients with TMJ Involvement (n = 33)

Patients with TMJ Contrast Enhancement (n = 14)

11 (23) 13 (28) 10 (21) 1 (2) 6 (13) 6 (13)

6 12 7 1 4 3

3 7 2 0 0 2

Arvidsson et al

Note.—Data are numbers of patients. Numbers in parentheses are percentages. ILAR = International League of Associations for Rheumatology, RF = rheumatoid factor.

Figure 1

Results

Figure 1: Normal TMJs in 34-year-old man with JIA. (a) Axial CT image of both TMJs. (b) Oblique-sagittal and (c) oblique-coronal CT images of right TMJ show normal bone structures. (d, e) Oblique-sagittal T1-weighted MR images of right TMJ before (d) and after (e) contrast medium administration show no contrast enhancement.

The normal disk should be biconcave, with its posterior thick band located on top of the condyle when the mouth is closed (20). In normal joints, joint fluid, if present, should appear as only dots or lines of high signal intensity along the articular surfaces on T2-weighted MR images, and there should be no signal intensity abnormalities in the mandibular condyle indicating bone marrow edema or sclerosis (21,22) and either no or minimal contrast enhancement of 194

the intraarticular tissues after intravenous contrast medium injection (23). The following joint abnormalities were noted: abnormal shape or size, cortical bone defects, bone production, bone marrow abnormalities, anterior condyle position (with mouth closed), and abnormal disk or disk position. Intravenous contrast medium–induced enhancement greater than that seen on the images obtained in asymptomatic healthy volunteers (23), bone marrow

There were no significant differences in the disease variables recorded at baseline between the 47 participating and 56 nonparticipating patients in the present series (Table 1). Mean ages at baseline were 9.0 years (range, 2.5–16.4 years) for all 103 patients, 8.9 years (range, 2.5–16.2 years) for the female patients, and 9.3 years (range, 3.9–16.4 years) for the male patients. Specific disease variables for the 47 participating patients are given in Table 2. The distribution of patients and TMJ involvement in the different International League of Associations for Rheumatology categories of JIA are given in Table 3. Ten (21%) of the 47 patients—four women and six men—had no JIA TMJ involvement. Nine of these 10 patients had normal bone and disk tissue, and one had normal bone but bilaterally reducing disk displacement. No signs of joint effusion, marrow edema, or contrast enhancement were seen (Fig 1). Three of the 10 patients reported having pain in the TMJs and masticatory muscles. The mouth-opening capacity ranged from 39 to 63 mm (mean capacity, 53.1 mm 6 7.4 [standard deviation]); no one had a mouth-opening capacity below the normal limits. Four (9%) of the 47 participating patients, all women, had disk displacement

radiology.rsna.org

n

Radiology: Volume 256: Number 1—July 2010

MUSCULOSKELETAL IMAGING: CT and MR of Temporomandibular Joint Findings in Idiopathic Arthritis

Table 4

Arvidsson et al

Figure 2

TMJ Imaging Abnormalities in 33 Patients with JIA TMJ Involvement TMJ Abnormality

Value

Patient level* Bilateral abnormalities Contrast enhancement† Osteoarthritis Joint level, CT and MR imaging Abnormal condyle morphology Abnormal fossa-eminence morphology Abnormal disk Superior condylar concavity‡ Anterior condyle position Secondary osteoarthritis§ Joint level, CT Cortical defect without sclerotic margin Cortical defect with sclerotic margin Joint level, MR imaging Normal disk Disk displacement Abnormal disk other than displacement Destroyed-absent or only small fragment Ruptured or fragmented Evenly thinned Intact but adapted to condyle concavities Thickened, not biconcave Contrast enhancement† Fibrous defects|| Subchondral cysts# Other subchondral change Bone marrow edema with or without effusion

29 (88) 14 (42) 19 (58) 61 (98) 56 (90) 61 (98) 30 (48) 13 (21) 29 (47) 11 (18) 13 (21) 1 (2) 4 (6) 57 (92) 13 26 11 5 2 22 (35) 4 (6) 4 (6) 4 (6) 2 (3)

Note.—Unless otherwise noted, data are numbers of joints (n = 62), with percentages in parentheses. * Data are numbers of patients (n = 33), with percentages in parentheses. †

Contrast enhancement within cortical defects and/or lining the synovial spaces.

‡

Seven of the 30 joints had superior condylar concavity with complete bifidity.

§

Fourteen of the 29 joints had secondary osteoarthritis with osteophyte formation.

||

Cortical defect without increased T2 signal intensity or contrast enhancement.

#

High T2 signal intensity within cortical defect.

and minor bone abnormalities, sclerosis, osteophyte formation, cortical defects, effusion, or slight to moderate contrast enhancement that could be interpreted as manifestations of JIA or osteoarthritis (Fig 2). Thirty-three (70%) patients, 24 women and nine men, had JIA TMJ abnormalities. Bilateral involvement was dominant, and secondary osteoarthritis and slight to moderate contrast enhancement were relatively frequent (Table 4). Twenty-nine of the 33 patients had evidence of TMJ abnormalities before the age of 15 at conventional transcranial and panoramic radiography. Radiology: Volume 256: Number 1—July 2010

n

Twenty-two (67%) of the 33 patients reported having pain, mainly in the TMJs and masticatory muscles combined. Seven of these 22 patients had contrast enhancement. The mouthopening capacity ranged from 18 to 54 mm (mean capacity, 38.5 mm 6 9.5) in the 33 patients with JIA TMJ abnormalities and from 28 to 54 mm (mean capacity, 37.0 mm 6 8.5) in the 14 with contrast enhancement. Eighteen patients (55%) had a below-normal mouth-opening capacity, and 10 of them had contrast enhancement. Sixty-two TMJs in the 33 patients were abnormal and showed a wide

radiology.rsna.org

Figure 2: Disk displacement and osteoarthritis in 37-year-old woman with JIA. (a) Oblique-sagittal CT image shows osteophyte formation (arrow). (b) Oblique-sagittal intermediate-weighted MR image shows disk (arrow) in anterior position. (c) Obliquesagittal gradient-echo MR image at open mouth shows nonreducing disk (arrow).

range of changes in the condyle, fossa, and disks (Table 4). The mandibular condyle was abnormal in 61 joints, which were very small to very large. Typically, the condyle was flat, deviating from its normal cylindrical shape, with a wide anteroposterior dimension (Fig 3) and a large condylar angulation (Fig 4). Superior condylar concavities were seen in 30 joints (Table 4, Figs 4, 5). The temporal bone was abnormal in 56 joints, with a flat or widened glenoid fossa and/or a flat outline of the articular eminence (Figs 3, 5), deviating from the normal S shape. Eminence deformation with creation of a new and sclerotic articular surface was seen in seven joints (Fig 6). 195

MUSCULOSKELETAL IMAGING: CT and MR of Temporomandibular Joint Findings in Idiopathic Arthritis

Figure 3

Arvidsson et al

Figure 5

Figure 3: CT images of JIA in TMJ of 37-yearold woman. (a) Axial image at level of line in b shows round condyle; compare these findings with those in Figure 1. (b) Oblique-sagittal image shows wide flat fossa (arrow) and condyle, with sclerosis. (c) Oblique-coronal image shows small deformed condyle with sclerosis (arrow).

Figure 4

Figure 4: CT images of JIA in TMJ of 31year-old woman. (a) Axial image shows bifid left condyle (arrow). Note large condylar angulation bilaterally; compare these findings with those in Figure 1. (b) Oblique-coronal image shows bifid condyle (arrow).

In 13 joints, the condyle had an anterior position when the mouth was closed (Table 4, Fig 7). Secondary osteoarthritis with predominant sclerosis (Fig 3) was noted in 29 of the 62 joints; osteophyte formation (Figs 7, 8) 196

was seen in about half of these joints (Table 4). All but one disk examined were abnormal—that is, destroyed (Fig 6), ruptured, fragmented, evenly thinned (Fig 8), or adapted to the various condylar concavities but otherwise appearing intact (Fig 5). Two disks (in one patient) were thicker than normal and biconvex. Four joints (in four patients with bilateral JIA involvement) had disk displacement at MR imaging (Table 4). Slight to moderate contrast enhancement was seen in 22 of the 62 joints at MR imaging (Fig 9). This enhancement was seen mainly in the joints without cortical defects (11 joints) or in the joints with cortical defects without a sclerotic margin (seven joints), and it was seen less often in joints with defects with sclerotic margins (four joints) (Table 4). Thirteen of the joints with contrast enhancement had secondary osteoarthritis. Fibrous defects, subchondral cysts (Fig 7), other subchondral changes (Fig 10), and bone marrow edema with and without effusion were rare (Table 4). Three patients had undergone orthognathic surgery, one patient had chin augmentation, and three had received

Figure 5: JIA in TMJ of 34-year-old woman. (a) Coronal CT image shows condylar concavities in both TMJs (arrows). (b) Oblique-sagittal CT image shows condylar concavity and flat wide fossa (arrow). (c) Oblique-sagittal intermediate-weighted MR image shows thin but intact disk (arrow), adapted to condylar deformity.

corticosteroid injections in their TMJs as adults. No patient had undergone surgical intervention of the TMJs. One patient had signs of fibro-osseus ankylosis in one TMJ and was assigned to the enthesitis-related JIA subgroup. This patient had also experienced craniofacial trauma with a fractured zygoma on the same side as an adult.

Discussion Our study results demonstrate the long-term outcomes of JIA in the TMJs. In most joints, abnormalities had been present for at least 20 years, as documented at conventional radiography. There was a potential for bias in our study: Not all patients underwent a final repeat examination, and 13 patients were not willing to undergo the

radiology.rsna.org

n

Radiology: Volume 256: Number 1—July 2010

MUSCULOSKELETAL IMAGING: CT and MR of Temporomandibular Joint Findings in Idiopathic Arthritis

Figure 6

Figure 7

Figure 6: JIA in TMJ of 34-year-old woman. (a) Oblique-sagittal CT image shows hyperplastic fossa-eminence (arrow) with sclerosis and flat enlarged condyle. (b) Oblique-sagittal T1-weighted contrast-enhanced MR image shows destroyed disk; only disk fragment is visible.

MR examination. However, there were no significant differences in baseline data between the participants and nonparticipants, and no patient selections were made on the basis of TMJ symptoms or clinical findings. Regarding the initial patient recruitment, most children in Norway who had or were suspected of having JIA were referred to Oslo Sanitetsforening Rheumatism Hospital to have their diagnosis confirmed. The patient data described herein seem to be representative of those for similar patient groups in Scandinavia (16). The long-term JIA manifestations in the TMJ were frequent, usually bilateral, and characterized by mandibular condyle and temporal bone deformities, abnormal disks in the normal position, and, rather often, osteoarthritis and mild synovitis. More than 40% of our patients with TMJ abnormalities had mild synovitis. This is consistent with data in long-term follow-up studies of general disease activity, which show that approximately 50% (range, 37%–66%) of patients with JIA have active disease in adulthood (27–30). The synovitis, appearing as slight to moderate contrast Radiology: Volume 256: Number 1—July 2010

Arvidsson et al

n

Figure 7: Oblique-sagittal images of JIA in TMJ of 43-year-old woman. (a) CT image of right joint shows bone defect with sclerotic outline within deformed enlarged condyle (arrow). (b) CT image of left joint shows wide flat fossa-eminence and hypoplastic condyle in anterior position. (c, d) MR images of right joint show bone defect (arrow) with intermediate low signal intensity on contrast-enhanced T1-weighted image (c) and high signal intensity on T2-weighted image (d), indicating subchondral cyst.

Figure 8

Figure 8: JIA in TMJ of 36-year-old woman. Left-sided (a) oblique-sagittal CT, (b) oblique-coronal CT, and (c) oblique-sagittal intermediate-weighted MR images show deformed condyle and secondary osteoarthritis, osteophyte formation, and sclerosis (arrows). (d) Right-sided oblique-sagittal intermediate-weighted MR image shows wide fossa, flattened condyle, and evenly thinned disk (arrow) apparently in normal position.

radiology.rsna.org

197

MUSCULOSKELETAL IMAGING: CT and MR of Temporomandibular Joint Findings in Idiopathic Arthritis

Arvidsson et al

Figure 9

Figure 9: Oblique-sagittal images of JIA in TMJ of 36-year-old woman. (a) CT image shows bone defect (arrow) with sclerotic outline. (b, d) Nonenhanced and (c, e) contrast-enhanced T1-weighted MR images show contrast enhancement within bone defect (arrow in b and c) and synovial contrast enhancement (arrows in e) in lateral part of joint.

Figure 10

Figure 10: Oblique-sagittal (a) CT and (b) T1-weighted MR images of JIA in TMJ of 40-year-old woman show long-term subchondral change (arrows).

enhancement, was found in the joints with and without imaging findings of osteoarthritis. In joints without osteoarthritis, the contrast enhancement suggests continued synovial inflammation due to JIA. Enhancement in joints with superimposed osteoarthritis could also be due to synovitis caused by the osteoarthritis itself. Contrast enhancement in TMJ osteoarthritis secondary to permanently displaced disks has been observed 198

in patients without rheumatic disease (31,32). We feel confident that the osteoarthritis in the patients in our series was secondary to the JIA because the disks or disk remnants were mainly in a normal position. Relatively recent MR studies of the TMJs in children with JIA indicate an up to 75% prevalence of active disease, defined as joint effusion and/or increased contrast enhancement of the

synovium or bone, in this group (6–8). These children are treated with more aggressive therapies and more efficient medication compared with their treatment regimens in the 1970s and 1980s. The observations in our study should be useful references for evaluating TMJ disease activity and outcome in follow-up studies. TMJ involvement and contrast enhancement were most frequent in the extended oligoarthritis subgroup; however, not all subgroups were represented. Study results have demonstrated that TMJ involvement occurs in all JIA subgroups (5). We observed low concordance between the clinical findings—namely, pain and mouthopening capacity—and the TMJ imaging findings. Therefore, MR imaging may be necessary to confirm JIA involvement. TMJ involvement was characterized by heterogeneous joint deformities, which we believed were due to local growth disturbances, remodeling, or healed destructive processes. The mandibular condyle showed flattening and undergrowth, as described in previous

radiology.rsna.org

n

Radiology: Volume 256: Number 1—July 2010

MUSCULOSKELETAL IMAGING: CT and MR of Temporomandibular Joint Findings in Idiopathic Arthritis

studies (11,33), but also overgrowth, which was seen primarily as enlargement in the horizontal direction. Concavity or varying degrees of bifidity of the mandibular condyle were frequent and have not been well established in the JIA literature. Such deformities are rare and have been related to developmental disturbances, trauma, and insufficient remodeling capacity (18,34). The flat smooth contour of the fossaeminence (11,33,35) has also been suggested as a consequence of TMJ involvement at a very early age, which prevents normal eminence development (36). In our study, we also observed a flat wide temporal eminence that was sclerotic and articulating with the mandibular condyle like a new fossa. The observation of an anteriorly located condyle when the mouth was closed is in agreement with previous study findings (11,33). A mandibular rotation around the molars occurs during growth in patients who have JIA with TMJ involvement (37). This could explain the forward tilting of the ramus and the anterior position of the condyle. The articular disk showed large variations in morphology. In the majority of cases, the disk or disk remnants were normally located. These findings are in accordance with findings in studies of adult-onset rheumatoid arthritis (38) and JIA in children and adolescents (35). The diagnostically problematic joints in our study were those few with disk displacement and minor bone abnormalities. Nonreducing disk displacement may also lead to a deformed condyle, particularly in children (39), and as already emphasized, joints with disk displacement and osteoarthritis may show contrast enhancement (31). Therefore, occasionally, it may be impossible to distinguish JIA involvement from disk displacement and osteoarthritis at imaging. The value of longitudinal examinations in such cases must be emphasized. In conclusion, 70% of the adult patients in this series had long-term JIA manifestations in the TMJs; these manifestations were dominated by a variety Radiology: Volume 256: Number 1—July 2010

n

Arvidsson et al

of bone structure and articular disk deformities. Secondary osteoarthritis and mild synovitis were observed relatively frequently.

9. Larheim TA, Haanaes HR, Ruud AF. Mandibular growth, temporomandibular joint changes and dental occlusion in juvenile rheumatoid arthritis: a 17-year follow-up study. Scand J Rheumatol 1981;10(3):225–233.

Acknowledgments: The authors thank Odd Vinje, MD, PhD, and Jørn Thoen, MD, PhD, senior consultants in the Department of Rheumatology, Rikshospitalet, Oslo University Hospital, for valuable advice and help with data collection; Håkon Størmer, photographer in the Faculty of Dentistry, University of Oslo, for helpful assistance with illustrations; and the staff members in the Departments of Rheumatology and Radiology, Rikshospitalet University Hospital, Oslo, and the Institute of Clinical Dentistry, Faculty of Dentistry, University of Oslo, for helpful assistance.

10. Bakke M, Zak M, Jensen BL, Pedersen FK, Kreiborg S. Orofacial pain, jaw function, and temporomandibular disorders in women with a history of juvenile chronic arthritis or persistent juvenile chronic arthritis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2001;92(4):406–414.

References

12. Brewer EJ Jr, Bass J, Baum J, et al. Current proposed revision of JRA criteria: JRA Criteria Subcommittee of the Diagnostic and Therapeutic Criteria Committee of the American Rheumatism Section of the Arthritis Foundation. Arthritis Rheum 1977;20(2 suppl):195–199.

radiology.rsna.org

1. Cassidy JT, Petty RE, Laxer RM, Lindsley CB. Textbook of pediatric rheumatology. 5th ed. Philadelphia, Pa: Elsevier Saunders, 2005;206–260. 2. Hayward K, Wallace CA. Recent developments in anti-rheumatic drugs in pediatrics: treatment of juvenile idiopathic arthritis. Arthritis Res Ther 2009;11(1):216. 3. Petty RE, Southwood TR, Manners P, et al. International League of Associations for Rheumatology classification of juvenile idiopathic arthritis: second revision, Edmonton, 2001. J Rheumatol 2004;31(2):390–392. 4. Arabshahi B, Cron RQ. Temporomandibular joint arthritis in juvenile idiopathic arthritis: the forgotten joint. Curr Opin Rheumatol 2006;18(5):490–495. 5. Ringold S, Cron RQ. The temporomandibular joint in juvenile idiopathic arthritis: frequently used and frequently arthritic. Pediatr Rheumatol Online J 2009;7:11. 6. Küseler A, Pedersen TK, Gelineck J, Herlin T. A 2 year followup study of enhanced magnetic resonance imaging and clinical examination of the temporomandibular joint in children with juvenile idiopathic arthritis. J Rheumatol 2005;32(1):162–169. 7. Weiss PF, Arabshahi B, Johnson A, et al. High prevalence of temporomandibular joint arthritis at disease onset in children with juvenile idiopathic arthritis, as detected by magnetic resonance imaging but not by ultrasound. Arthritis Rheum 2008;58(4): 1189–1196. 8. Müller 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 (Oxford) 2009;48(6):680–685.

11. Larheim TA, Haanaes HR, Dale K. Radiographic temporomandibular joint abnormality in adults with micrognathia and juvenile rheumatoid arthritis. Acta Radiol Diagn (Stockh) 1981;22(4):495–504.

13. Larheim TA, Höyeraal HM, Stabrun AE, Haanaes HR. The temporomandibular joint in juvenile rheumatoid arthritis: radiographic changes related to clinical and laboratory parameters in 100 children. Scand J Rheumatol 1982;11(1):5–12. 14. Stabrun AE, Larheim TA, Höyeraal HM, Rösler M. Reduced mandibular dimensions and asymmetry in juvenile rheumatoid arthritis: pathogenetic factors. Arthritis Rheum 1988;31(5):602–611. 15. Steinbrocker O, Traeger CH, Batterman RC. Therapeutic criteria in rheumatoid arthritis. J Am Med Assoc 1949;140(8):659–662. 16. Arvidsson LZ, Flatø B, Larheim TA. Radiographic TMJ abnormalities in patients with juvenile idiopathic arthritis followed for 27 years. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2009;108(1):114–123. 17. Agerberg G. Maximal mandibular movements in young men and women. Sven Tandlak Tidskr 1974;67(2):81–100. 18. Yale SH, Allison BD, Hauptfuehrer JD. An epidemiological assessment of mandibular condyle morphology. Oral Surg Oral Med Oral Pathol 1966;21(2):169–177. 19. Brooks SL, Westesson PL, Eriksson L, Hansson LG, Barsotti JB. Prevalence of osseous changes in the temporomandibular joint of asymptomatic persons without internal derangement. Oral Surg Oral Med Oral Pathol 1992;73(1):118–122. 20. Drace JE, Enzmann DR. Defining the normal temporomandibular joint: closed-, partially open-, and open-mouth MR imaging

199

MUSCULOSKELETAL IMAGING: CT and MR of Temporomandibular Joint Findings in Idiopathic Arthritis

of asymptomatic subjects. Radiology 1990; 177(1):67–71.

Group studies. I. Design. J Rheumatol 1982;9(1):109–113.

21. Westesson PL, Brooks SL. Temporomandibular joint: relationship between MR evidence of effusion and the presence of pain and disk displacement. AJR Am J Roentgenol 1992;159(3):559–563.

27. Zak M, Pedersen FK. Juvenile chronic arthritis into adulthood: a long-term follow-up study. Rheumatology (Oxford) 2000;39(2): 198–204.

22. 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 2001;30(2): 113–117. 23. Smith HJ, Larheim TA, Aspestrand F. Rheumatic and nonrheumatic disease in the temporomandibular joint: gadoliniumenhanced MR imaging. Radiology 1992; 185(1):229–234. 24. Larheim TA, Westesson PL, Sano T. MR grading of temporomandibular joint fluid: association with disk displacement categories, condyle marrow abnormalities and pain. Int J Oral Maxillofac Surg 2001;30(2): 104–112. 25. Fries JF, Spitz P, Kraines RG, Holman HR. Measurement of patient outcome in arthritis. Arthritis Rheum 1980;23(2):137–145. 26. Brewer EJ Jr, Giannini EH. Standard methodology for Segment I, II, and III Pediatric Rheumatology Collaborative Study

200

28. Minden K, Niewerth M, Listing J, et al. Long-term outcome in patients with juvenile idiopathic arthritis. Arthritis Rheum 2002;46(9):2392–2401. 29. Packham JC, Hall MA. Long-term follow-up of 246 adults with juvenile idiopathic arthritis: functional outcome. Rheumatology (Oxford) 2002;41(12):1428–1435. 30. Flatø B, Lien G, Smerdel A, et al. Prognostic factors in juvenile rheumatoid arthritis: a case-control study revealing early predictors and outcome after 14.9 years. J Rheumatol 2003;30(2):386–393. 31. Suenaga S, Hamamoto S, Kawano K, Higashida Y, Noikura T. Dynamic MR imaging of the temporomandibular joint in patients with arthrosis: relationship between contrast enhancement of the posterior disk attachment and joint pain. AJR Am J Roentgenol 1996;166(6):1475–1481. 32. Farina D, Bodin C, Gandolfi S, De Gasperi W, Borghesi A, Maroldi R. TMJ disorders and pain: assessment by contrastenhanced MRI. Eur J Radiol 2009;70(1): 25–30.

Arvidsson et al

33 . Bache C . Mandibular growth and dental occlusion in juvenile rheumatoid arthritis. Acta Rheumatol Scand 1964 ; 10: 142 –153 . 34. Antoniades K, Hadjipetrou L, Antoniades V, Paraskevopoulos K. Bilateral bifid mandibular condyle. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2004;97(4):535–538. 35. Taylor DB, Babyn P, Blaser S, et al. MR evaluation of the temporomandibular joint in juvenile rheumatoid arthritis. J Comput Assist Tomogr 1993;17(3):449–454. 36. Larheim TA. Radiographic appearance of the normal temporomandibular joint in newborns and small children. Acta Radiol Diagn (Stockh) 1981;22(5):593–599. 37. Björk A, Skieller V. Normal and abnormal growth of the mandible: a synthesis of longitudinal cephalometric implant studies over a period of 25 years. Eur J Orthod 1983; 5(1):1–46. 38. Larheim TA, Smith HJ, Aspestrand F. Rheumatic disease of the temporomandibular joint: MR imaging and tomographic manifestations. Radiology 1990;175(2):527–531. 39. Katzberg RW, Tallents RH, Hayakawa K, Miller TL, Goske MJ, Wood BP. Internal derangements of the temporomandibular joint: findings in the pediatric age group. Radiology 1985;154(1):125–127.

radiology.rsna.org

n

Radiology: Volume 256: Number 1—July 2010