Evaluation of temporomandibular joint disk displacement and its correlation with pain and osseous abnormalities in symptomatic young patients with magnetic resonance imaging

Evaluation of temporomandibular joint disk displacement and its correlation with pain and osseous abnormalities

in symptomatic young patients with magnetic resonance imaging

Daniela Pita de Melo, BDS, MS, PhD,^aSaulo Leonardo Sousa Melo, BDS, MS, PhD,^b Luciana Soares de Andrade Freitas Oliveira, BDS, MS, PhD,^c

Flávia Maria de Moraes Ramos-Perez, BDS, MS, PhD,^dand Paulo Sérgio Flores Campos, BDS, MS, PhD^e

Objective. To evaluate the occurrence of temporomandibular joint disk displacement and its correlation with pain and osseous abnormalities using magnetic resonance imaging (MRI) in patients under 21 years of age.

Study Design. MRI images in open- and closed-mouth positions from 102 patients, under 21 years of age (mean age 17 years), were studied retrospectively. Patients were divided into six groups according to the diskecondyle relationship. Chi-square, Marascuilo procedure, and Cochran-Mantel-Haenszel tests were used to evaluate the relationships among pain,

abnormalities, and the groups.

Results. There was a statistically significant correlation between bilateral disk displacement without reduction and pain (P ¼ .011), and osseous changes (P < .0001). There was no proven link between pain and osseous abnormality (P ¼ .414).

Conclusion. Young patients are susceptible to all stages of disk displacement. There was a strong correlation only between each variable (osseous abnormalities and pain) and the most severe stage of disk displacement (bilateral disk displacement without reduction). (Oral Surg Oral Med Oral Pathol Oral Radiol 2015;119:107-112)

Temporomandibular disorders (TMDs) are defined as a subgroup of abnormal conditions involving masti- catory muscles, osseous and ligamentous components of the temporomandibular joints (TMJs), and associ- ated neurologic structures.^1-3 Common among adults, TMD does not appear to be a usualfinding in children but tends to increase in frequency with age during adolescence.⁴

Despite better knowledge of the structure and func- tion of the TMJ, the specific pathophysiology of TMDs is not completely understood.¹ It is well known that morphologic changes may be observed in the TMJ bone structures (mandibular condyle and articular eminence of the temporal bone) of patients with TMDs, including osteophytes, erosion, avascular necrosis, and sub- chondral cysts with intra-articular loose bodies and/or flattening.³Furthermore, the most common symptoms

are pain, muscle tenderness, a“clicking” or “popping”

sensation within the joint, headache, earache, and restricted mouth opening.⁵

Disk displacement (DD) is a common disorder of the TMJ, usually reported in young to middle-aged female adults (20 to 50 years of age).^1,6In adolescents, it has also been shown that females have a greater incidence of DD and associated pain compared with males.^2,4 Moreover, there appears to be a high incidence of DD in young preorthodontic patients (ages 6-15 years), with no gender predilection, and a tendency to more advanced stages of DD with increasing age.⁷

Magnetic resonance imaging (MRI) is considered the best method of evaluating DD, since it provides excellent soft tissue contrast without radiation or sur- gical invasion.^8,9 MRI scans taken with the patient in open- and closed-mouth positions are widely used to evaluate the position, configuration, and posterior attachment of the disk, as well as the mandibular marrow status, presence of joint effusion, and anatomic details of the TMJ.^1,2,8,9Its accuracy for assessment of the position and form of the disk has been reported to

aAssociate Professor, Division of Oral Radiology, Department of Oral Diagnosis, Paraíba Dental School, Paraíba State University, Campina Grande, Paraíba, Brazil.

bResident, Department of Oral Pathology, Radiology and Medicine, University of Iowa College of Dentistry, Iowa City, Iowa, USA.

cAssistant Professor, Division of Radiology, Department of Applied Sciences, School of Radiology, Federal Institute of Bahia, Salvador, Bahia, Brazil.

dAssociate Professor, Division of Oral Radiology, Department of Clinic and Preventive Dentistry, Federal University of Pernambuco, Recife, Pernambuco, Brazil.

eProfessor, Department of Radiology, School of Dentistry, Federal University of Bahia, Bahia, Brazil.

Received for publication Apr 8, 2014; returned for revision Aug 20, 2014; accepted for publication Sep 20, 2014.

Ó 2015 Elsevier Inc. All rights reserved.

2212-4403/$ - see front matter

http://dx.doi.org/10.1016/j.oooo.2014.09.022

Statement of Clinical Relevance

This retrospective magnetic resonance imaging study of patients under 21 years of age found that these young patients are susceptible to all stages of disk displacement and that there is a strong corre- lation between osseous abnormalities or pain and the most severe stage of disk displacement.

107

be up to 95%.^10,11 On the other hand, it has demon- strated variable sensitivity (30%-82%) for the detection of osseous abnormalities, depending on the type and severity of such abnormality.^12,13However, this uneven sensitivity should not restrict the evaluation of bone abnormalities when a MRI scan has been acquired to investigate DD.

The majority of the literature to date has related gender, anatomic or clinical findings, and imaging features with TMJ characteristics. Only a few studies have specifically correlated disk displacement findings from young patients. For this reason, the aim of this study was to evaluate the occurrence of TMJ disk displacement and its possible correlation with pain and osseous abnormalities using MRI in patients under 21 years of age.

MATERIALS AND METHODS

This retrospective cross-sectional study protocol was approved by the last author’s Institutional Review Board and is in compliance with the Helsinki Decla- ration. All patients provided written informed consent.

MRI scans of 102 patients (22 males and 80 fe- males), aged between 10 and 20 years (mean age 17 years), were studied retrospectively. The patients had been referred to the same radiology practice for MRI to investigate possible TMD-related findings.

Before MRI, a professional with 15 years of experience in TMJ evaluation performed a clinical examination on all patients. To be included in the study, the subject had to present at least one of the following signs and symptoms: pain in joints and/or muscles, joint sounds, limitation of movement, history of headaches, and otologic complaints. Gender and the presence of joint pain, as reported by the subject, were registered for statistical purpose.

The MRI studies were conducted on a 1.5-T GE Signa scanner (General Electric, Milwaukee, WI). A bilateral TMJ dual-phased array coil (Signa; GE Med- ical System, Milwaukee, WI) was used, and the patients were placed in the supine position, with the sagittal plane perpendicular to the horizontal plane, and the Frankfort plane parallel to the scanner gantry. The protocol used a 256  256 matrix, 145-mm field of view, and a pixel size of 0.60 0.57 mm. Ten slices, 2-mm thick, were obtained for each TMJ in each sequence. Oblique parasagittal slices were obtained and corrected for the horizontal angulation of the condyle in all the following sequences: closed-mouth axial T1- weighted, coronal T1-weighted, and axial T2-weighted, as well as open-mouth axial T1-weighted. For the acquisition of images in the open-mouth position, a Burnett TMJ device (TMJ-200 s/n 0650; Medrad Inc., Pittsburgh, PA) was used to stabilize the maximal open- mouth position and to minimize motion artifacts.

Two experienced radiologists performed the MRI image evaluation, in a consensus approach, of all im- ages without any clinical information. The position of the disk in closed-mouth images was evaluated and classified according to Ahmad et al.¹¹ as “normal” or

“displaced.” The patients with disk displacement were subclassified according to the diskecondyle relation- ship in open-mouth images into (1) disk displacement with reduction (DDwR), when the normal relationship between the disk and condyle was restored on mouth opening; and (2) disk displacement without reduction (DDwoR), when the disk was still displaced on mouth opening. Exclusion criteria included cases in which the position of the disk was indeterminate or the disk itself was not visible.¹¹

Patients were then divided into six groups, on the basis of a previous study.¹⁴ These groups were determined by the results of TMJ MRI according to both TMJ disks status, in the following order: bilateral normal TMJs (Normal/Normal); unilateral DDwR and normal contralateral TMJ (DDwR/Normal);

bilateral DDwR (DDwR/DDwR); unilateral DDwoR and normal contralateral TMJ (DDwoR/Normal);

unilateral DDwR and DDwoR in the contralateral TMJ (DDwR/DDwoR); and bilateral DDwoR (DDwoR/DDwoR).

The assessment of osseous abnormalities was adapted from Ahmad et al.¹¹and included osteophytes, flattening, erosion, sclerosis, edema, thickness of cortical eminence and/or condyle, focal or diffuse ne- crosis, bifid condyle, condylar hypoplasia or hyperpla- sia, and the presence of free bodies.

The prevalence of the morphologic changes of bone structures of the TMJ and the prevalence of the po- sition of the disk in the closed-mouth position were summarized as percentages. Chi-square test followed by the Marascuilo procedure for comparison of the K proportion was performed to evaluate the association of disk displacement with pain and with osseous ab- normalities. The correlation between both variables (pain and osseous abnormalities) was assessed by creating six contingency tables (each corresponding to a TMJ group). Cramer’s V, Chi-square test, and P values were calculated for each sub-table. These statistics were calculable only if the marginal sums were nonzero in each sub-table. Cramer’s V shows the strength of the links between the variables. It is close to zero when there is no link. The general cor- relation coefficient method of the Cochran-Mantel- Haenszel test was used to evaluate the relationship between pain and abnormalities, considering all disk displacement status. Data analysis was performed using XLStat (version 2014.2.1, Addinsoft Inc., Brooklyn, NY). The a priori level of significance was set at P< .05.

RESULTS

Two hundred and four TMJs were analyzed. Table I shows the distribution of patients among the TMJ disk displacement groups. Overall, young females repre- sented 78.43% of the sample (80 F/22 M). However, there was no statistically significant difference in the distribution of disk displacement according to gender (P> .05). For this reason, the following statistical tests were made considering the whole sample (both genders combined).

With respect to osseous abnormalities, 45.1% of the sample (46 patients) presented with at least one altered TMJ, that is, 31.86% (65 of 204) of all joints.Table II summarizes the distribution of the abnormalities

according to the number of TMJs involved. Some pa- tients presented with more than one entity.

The K proportions of pain and osseous abnormality among TMJ disk displacement groups are presented in Table III. Results indicated that there was a statistically significant correlation between DDwoR/DDwoR and pain. Of 16 patients presenting with bilateral disk displacement without reduction, pain was reported in 56.25% of the cases (P¼ .011). There was also a sta- tistically significant association between osseous changes and disk displacement without reduction (P < .0001). The DDwR/DDwoR and DDwoR/

DDwoR groups were more likely to present osseous abnormality compared with the other groups.

Table II. The distribution [n (%)] of the abnormalities according to the number of temporomandibular joints involved

Alteration Unilateral Bilateral

Total

Patients* TMJs

Condylar hypoplasia 13 (12.74) 11 (10.78) 24 (23.52) 35 (17.16)

Condylar erosion 15 (14.70) 2 (1.96) 17 (16.66) 19 (9.31)

Osteophyte 9 (8.82) 0 (0) 9 (8.82) 9 (4.41)

Bone necrosis 2 (1.96) 2 (1.96) 4 (3.92) 6 (2.94)

Flattened condyle 2 (1.96) 1 (0.98) 3 (2.94) 4 (1.96)

Articular eminence erosion 3 (2.94) 0 (0) 3 (2.94) 3 (1.47)

Effusion 1 (0.98) 1 (0.98) 2 (1.96) 3 (1.47)

Bone sclerosis 1 (0.98) 1 (0.98) 2 (1.96) 3 (1.47)

Thickening of condyle cortex 2 (1.96) 0 (0) 2 (1.96) 2 (0.98)

Thickening of temporal eminence 1 (0.98) 0 (0) 1 (0.98) 1 (0.49)

Bifid condyle 1 (0.98) 0 (0) 1 (0.98) 1 (0.49)

Condylar hyperplasia 1 (0.98) 0 (0) 1 (0.98) 1 (0.49)

*Some patients presented with more than one entity.

Table I. The gender distribution [n (%)] of patients with pain and osseous abnormality among temporomandibular joint disk displacement groups

Group Gender Total

Pain* Osseous abnormality*

Yes No Yes No

Normal/Normal Male 1 (0.98) 1 (0.98) 0 (0) 0 (0) 1 (0.98)

Female 22 (21.57) 8 (7.84) 14 (13.73) 3 (2.94) 19 (18.63)

Total 23 (22.55) 9 (8.82) 14 (13.73) 3 (2.94) 20 (19.61)

DDwR/Normal Male 6 (5.88) 0 (0) 6 (5.88) 1 (0.98) 5 (4.90)

Female 11 (10.78) 4 (3.92) 7 (6.86) 2 (1.96) 9 (8.82)

Total 17 (16.66) 4 (3.92) 13 (12.74) 3 (2.94) 14 (13.72)

DDwR/DDwR Male 8 (7.84) 1 (0.98) 7 (6.86) 0 (0) 8 (7.84)

Female 14 (13.73) 5 (4.90) 9 (8.83) 7 (6.86) 7 (6.86)

Total 22 (21.57) 6 (5.88) 16 (15.69) 7 (6.86) 15 (14.7)

DDwoR/Normal Male 1 (0.98) 1 (0.98) 0 (0) 1 (0.98) 0 (0)

Female 4 (3.92) 4 (3.92) 0 (0) 2 (1.96) 2 (1.96)

Total 5 (4.9) 5 (4.9) 0 (0) 3 (2.94) 2 (1.96)

DDwR/DDwoR Male 2 (1.96) 1 (0.98) 1 (0.98) 2 (1.96) 0 (0)

Female 17 (16.67) 10 (9.81) 7 (6.86) 14 (13.73) 3 (2.94)

Total 19 (18.63) 11 (10.79) 8 (7.84) 16 (15.69) 3 (2.94)

DDwoR/DDwoR Male 4 (3.92) 2 (1.96) 2 (1.96) 2 (1.96) 2 (1.96)

Female 12 (11.76) 7 (6.86) 5 (4.90) 12 (11.76) 0 (0)

Total 16 (15.68) 9 (8.82) 7 (6.86) 14 (13.73) 2 (1.96)

Overall 102 (100) 44 (43.14) 58 (56.86) 46 (45.1) 56 (54.9)

*The distribution of pain and osseous abnormalities were made independently.

Table IVpresents the contingency sub-tables of the correlation between pain and osseous abnormality.

Cramer’s V was close to zero in all groups, demon- strating no links between the variables. When taking the tables all together for a Cochran-Mantel-Haenszel test, there was a common odds ratio of 0.737 with a 95% confidence interval that included the value 1 (0.187-2.555). Generally, there was no proven link between pain and the presence of osseous abnormalities (P¼ .414).

DISCUSSION

Although the prevalence of TMD is higher in older adults, its presence among young patients should not be neglected. In fact, an early diagnosis must be pursued.

It has been suggested that disk displacements occur frequently in preorthodontic adolescents and, indepen- dent of the age group, females are highly predis- posed.^3,15-18 According to a longitudinal study that

included female adolescents, a history of clicking or grating sounds in the joint was related to a subsequent development of symptoms.¹⁶

There appear to be few studies in the English liter- ature on the assessment of MRI findings of TMJs of adolescents with suspicion of TMD, other than one study of normal MRI findings of juvenile TMJs in children without rheumatism (range 3-13 years)¹⁹ and several cases of juvenile idiopathic arthritis.^9,20-22 In part, the use of MRI for the evaluation of the TMJ in patients is limited by its high cost.¹⁴ Also, as already mentioned, there is a lack of early diagnoses of TMD in the young population, which makes this present study unique. The 102 patients recruited for this study were under 21 years of age (range 10-20 years; mean age 17 years) and had been referred for MRI examinations for assessment of TMDs. In other words, the referring dentists identified a sign and/or symptom that justified an investigation of the joints.

In order to correctly diagnose and treat TMDs, an accurate diagnostic method is necessary. Undoubtedly, MRI is the gold standard for diagnosis of internal derangement of the TMJ.1,10,11,14,23On the other hand, the diagnosis of osseous changes is still questionable.

Some authors^11,12 have stated that MRI has fair reli- ability and marginal sensitivity in diagnosing osseous changes compared with computed tomography (CT) and cone-beam CT (CBCT). Therefore, MRI would not be an ideal imaging technique for detecting osseous changes, and CT or CBCT would remain the imaging modality of choice for that task.^11,12 However, in a comparison of the detection of erosion by T1-weighted, 1.5-T MRI and microCT sections of the meta- carpophalangeal joints of patients with rheumatoid arthritis, a recent investigation¹³ found that MRI demonstrated high sensitivity and specificity (0.79 and 1.00, respectively) in detecting bone erosions, and only very small lesions escaped detection. In fact, the few bone erosions that could not be depicted by MRI were very small lesions with volume of less than 10 mm.^3,13 TMJs are unique paired joints that attach a single bone (the mandible) to the base of the skull. Although some authors consider them separate entities, the pre- sent study considered them a single functional unit. For this reason, our sample was divided into six groups according to the status of both articular disks when in function: Normal/Normal, DDwR/Normal, DDwR/

DDwR, DDwoR/Normal, DDwR/DDwoR, and DDwoR/

DDwoR. The disk was considered displaced when its posterior band was not positioned on top of the mandibular condyle (in the 11 to 12 o’clock position) in the closed-mouth position.

The establishment of a relationship among preva- lence, disk displacement type, and disk function could be difficult, since TMDs can be progressive. Some Table III. K proportion of pain and osseous abnor-

mality among temporomandibular joint disk displace- ment groups*

Group Pain Osseous abnormality

Normal/Normal 0.235^A 0.13^x

DDwR/Normal 0.273^A 0.176^x

DDwR/DDwR 0.391^A 0.318^x

DDwoR/Normal 0.563^A 0.6^x,Z

DDwR/DDwoR 0.579^A 0.842^Z

DDwoR/DDwoR 1^B 0.875^Z

*Proportions in the same column with different letter mean differ- ences statistically significant (A/B, P ¼ .011; X/Z, P < .0001). Chi- square, Marascuilo procedure.

Table IV. Distribution of patients according to the presence/absence of pain in the presence or absence of osseous abnormality among temporomandibular joint disk displacement groups

Group Pain

Osseous

abnormality Cramer’s

V Chi-square P value Yes No

Normal/Normal Yes 2 7 0.219 1.098 .538

No 1 13

DDwR/Normal Yes 0 4 0.257 1.121 .541

No 3 10

DDwR/DDwR Yes 2 4 0.020 0.009 1.000

No 5 11

DDwoR/Normal Yes 3 2 d d d

No 0 0

DDwR/DDwoR Yes 9 2 0.077 0.112 1.000

No 7 1

DDwoR/DDwoR Yes 7 2 0.333 1.778 .475

No 7 0

Cochran-Mantel-Haenszel test: Odds ratio ¼ .737; confidence interval¼ .187  2.555); P ¼ .414.

authors have stated that DDwR is expected to be an initial phase of the disk displacement process, which evolves to DDwoR in a later phase.¹⁷Even though our sample consisted of young patients, which could sug- gest that those individuals would present an early stage of TMD, 39.21% already presented with DDwoR in at least one joint. This could suggest that in some patients, TMD progression seems to be faster than in others, independent of age.

A displaced disk may lead to TMJ clicking, pain, and restricted jaw movements.¹⁴According to a study from 1981, temporomandibular arthropathy (better known nowadays as TMD) may progress from an initial stage of clicking and locking to a terminal stage of crepitation and constriction.²⁴ However, the major reason for patients with TMDs seeking treatment seems to be persistent pain. In the present study, there was a statistically significant correlation only between the presence of bilateral DDwoR and pain (P¼ .011;

see Table III). In a study conducted in a “stress free”

population, there was no observed association between disk position and pain.¹⁷ On the other hand, a study conducted in 72 patients reported a statistically signifi- cant difference in the occurrence of disk displacement between symptomatic and asymptomatic joints (54% vs 22%; P< .001).⁶When a sample of 144 patients with known TMJ dysfunction was selected, the group without reduction presented with significant increases in the risk of experiencing symptoms (P¼ .002).²⁵

Overall, when bone changes were considered, 50%

of the cases were not associated with pain. The cor- relation between pain and each bone abnormality separately was not possible due to the small sample size for each one, making the statistical tests less sensitive. Only a larger sample size for each abnor- mality could generate statistical evidence valid for the population sample. As shown in Table IV, the pres- ence of bone abnormalities was not related to referred pain, even when the “disks in function” subgroups were considered independently (odds ratio ¼ .737;

confidence interval, 0.187-2.555; P ¼ .414). A pre- vious study with 131 symptomatic patients found a significant relationship between pain and the MRI diagnosis of osteoarthritis.²⁶ However, this study considered a large age range (14-79 years), which could be related to more severe presentations of bone changes.

Despite the known limitations of MRI, a statistically significant association was demonstrated between osseous changes and disk displacement without reduc- tion (P< .0001). A previous study that investigated 74 symptomatic patients who underwent MRI found that erosion of the articular eminence and the combination of erosion of the condyle and osteophytes were more common in DDwoR.²⁷ An association between

DDwoR and degenerative bone changes was also seen in a study of 180 patients (mean age 33.4 years) referred for MRI and CT.³Moreover, it has been sug- gested that the risk of degenerative changes and joint effusions increases with the severity of disk displace- ment.^26-28 For this reason, patients with TMD with confirmed DDwoR or disk deformity on MRI should undergo examination with CBCT.²⁹

The occurrence of osseous abnormalities in a study based on CBCT images of 55 patients (mean age 41 years) ranged from 5% to 25%.¹² Our results demonstrated a distribution from 0.49% to 17% (see Table II). In some types of abnormalities, the difference between both results was up to 12 times higher. These results showed that MRI was better at detecting changes in the size of the TMJ, such as deformities, than in detecting changes in shape, for example, flattening, osteophyte formation, or erosion. According to those authors, this could be primarily due to the limited spatial resolution of MRI; the slice thickness of MRI (3 mm in their study) may be too thick to detect subtle osseous changes.¹² Our results do not corroborate those previousfindings. The most common alterations observed in the present investigation were condylar hypoplasia (23.52% of patients e 17.16% of TMJs), condylar erosion (16.66% of patients e 9.31% of TMJs), and the presence of osteophytes (8.82% of pa- tients e 4.41% of TMJs) (see Table II). This contra- diction could be due to the difference in the mean age of the patients and/or to the protocol used (i.e., the present research acquired 10 slices, 2 mm thick, per sequence, and the previous authors had used 7 slices, 3 mm thick).

It is important to remember that TMD is a multi- factorial disease. Psychosocial factors, such increased levels of stress, somatic complaints, and emotional problems, may play a more prominent role than anatomic factors in adolescents with TMD.³⁰ This could justify the presence of severe TMD in some of the young patients included in our study. However, those psychosocial factors were not taken into consideration in the present study. A future study would be necessary to investigate this possible association. Other inter- esting future studies would be (1) a longitudinal follow- up study to determine the MRIfindings of the evolution of disk displacement from adolescence to adulthood, and (2) a transversal comparison of the most common findings in each age group (e.g., children, adults, and older adults) to try to establish a direct relationship between age and TMJ alterations.

CONCLUSIONS

On the basis of the data presented for a specific popu- lation of patients under 21 years of age, it is possible to conclude that (1) young patients are susceptible to all stages of disk displacement, and (2) there was a lack of

a statistically significant association between osseous abnormalities, pain, and disk displacement, except for the most severe stage of disk displacement (bilateral disk displacement without reduction), which was strongly correlated with both variables.

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Reprint requests:

Saulo Leonardo Sousa Melo, BDS, MS, PhD 801 Newton rd

S367 Dental Science Bld Iowa City

IA, 52246

sauloleonardo-sousamelo@uiowa.edu