Keywords magnetic resonance imaging - temporomandibular joint - temporomandibular joint disorders
- tinnitus
Introduction
The temporomandibular joint (TMJ), which is among the most complex joints in the human
body,[1 ] is routinely exposed to considerable loads, as indicated by animal, in vitro, and
mathematical models.[2 ] With time, such exposure, alone or associated with underlying disorders, is thought
to generate physiological and pathological changes,[3 ] which may lead to temporomandibular joint dysfunction (TMD) of varying complexity
and magnitude.[4 ]
[5 ]
[6 ]
[7 ] The most common symptoms reported by patients with TMD include pain, deviations
or restrictions in the range of motion, presence of clicking, crackling, or popping
sounds,[8 ] and otologic symptoms such as tinnitus,[9 ] defined as a phantom sound in the absence of an external source.[10 ]
The prevalence of tinnitus is higher in individuals with TMD than in the general population.[5 ] Neither TMD nor tinnitus are life-threatening, but both can cause great distress.[3 ]
[10 ]
[11 ] Although the pathogenesis of the relationship between TMD and tinnitus is poorly
understood, a common etiological mechanism has been suggested.[12 ] Therefore, the investigation of findings peculiar to TMD patients with tinnitus
may be useful to clarify the link between these two entities, and may shed light on
the mechanisms involved in the onset of TMD and tinnitus.
Magnetic resonance imaging (MRI) of the TMJ is the method of choice for investigation
of TMD.[13 ] It has been hypothesized that specific MRI findings might be observed in TMD with
comorbid tinnitus.[14 ] Thus, the aim of the present study was to comparatively describe MRI findings in
patients with TMD with and without tinnitus, identifying the most common TMJ alterations
and determining whether a correlation exists between the severity of TMD and tinnitus.
Methods
The project was approved by our local institutional review board. All procedures were
in accordance with the 1964 Helsinki declaration and its later amendments or comparable
ethical standards.
This cross-sectional comparative study analyzed chart data and imaging findings. All
investigators signed a data use agreement that ensured anonymity.
The inclusion criteria were age > 17 years and diagnosis of TMD,[15 ]
[16 ] based on clinical symptoms including pain, clicking or crackling sounds, and mandibular
opening with deviation. The exclusion criteria were objective tinnitus; tinnitus with
a diagnosed etiology; Ménière disease; noise-induced hearing loss, ear surgery, or
infections; and abuse of ototoxic medications or substances (furosemide, aspirin)
or stimulants. Individuals with certain systemic diseases (diabetes, hypothyroidism)
were also excluded.
Between 2009 and 2016, adult patients of both genders, with bilateral or unilateral
TMD, were selected for the study. Patients with tinnitus and a clinical history of
TMD were referred by their otologist to the investigator (a dentist specializing in
TMD and orofacial pain) after other otologic comorbidities had been ruled out. Patients
with TMD who did not have tinnitus were either referrals from otologists or other
specialists or were walk-ins to our service. All patients in both groups underwent
a clinical and dental assessment and MRI evaluation of the TMJ.
TMJ Evaluation
Temporomandibular joint evaluation was performed by the same examiner (DLB) in all
patients. Mandibular range of motion was measured as described by Emshoff et al.[15 ] Briefly, maximum opening (measured in mm from the central maxillary incisor to the
opposing mandibular incisor) and lateral excursions (relative to the maxillary midline,
with the teeth slightly separated) were evaluated. The TMJ was auscultated with a
stethoscope to detect unilateral or bilateral clicks during three openings and three
lateral and protrusive movements.
Disc displacement with reduction was identified in the presence of a click in the
TMJ during vertical mandibular motion and lateral or protrusive excursions and normal
closing with or without clicking, reproducible on two of three occasions. Disc displacement
without reduction was defined as a history of sudden reduction in mandibular opening,
maximum unassisted mandibular opening 35 mm, and mandibular opening with assistance
increased by 3 mm or less over maximum unassisted opening.
Otologic Evaluation
Patients reporting tinnitus underwent a full ear, nose and throat (ENT) investigation,
including pure tone audiometry, to identify the underlying etiology (ear or systemic
disorder). If a retrocochlear disorder was suspected, an evoked potential audiometry
was performed. If a systemic cause was suspected, a laboratory workup was performed
(metabolic, hormonal, renal function, and autoimmune panels).
MRI
Bilateral parasagittal and coronal T1- and T2-weighted MRIs of the TMJ, as well as
cinematic images, were obtained using an HDXT GE 1,5 Tesla (GE Healthcare, Barueri,
SP, Brazil) with open and closed mouth. Magnetic resonance imaging findings of condylar
morphology, articular eminence morphology, and disc morphology, disc displacement
with or without reduction, condylar excursion, and intra-articular effusion were described
by an independent radiologist.
TMD Severity Score
The association between tinnitus and morphological aspects (changes in condylar morphology,
articular eminence morphology, and disc morphology), disc displacement (with or without
reduction), condylar translation, and intra-articular effusion was analyzed in MRIs
of the TMJ. The selection of these criteria was based on the work of Ahmad et al.[17 ]
A TMD severity score was created for comparison between the groups with or without
tinnitus. Each of the six criteria (changes in condylar morphology, articular eminence
morphology, and disc morphology, disc displacement, translation, and intra-articular
effusion) received a score of zero (absent), 1 (unilateral), or 2 (bilateral). The
sum of the scores (minimum zero, maximum 12) indicated the severity of TMD. The mean
TMD scores obtained for patients with tinnitus was then compared with the mean score
obtained for patients without tinnitus.
Statistical Analysis
The sample size was calculated as 44 patients (n = 22/group), considering α = 5% and a statistical power of 90% to detect a difference
of one standard deviation (SD) in TMD severity score between groups, with one SD assumed
to correspond to 2 score points.
Data were expressed as frequency of altered MRI findings. The TMD severity score was
expressed as mean and SD. The Student t -test for independent samples was used to compare group means. The Fisher exact test
was used to investigate association between categorical variables. Significance was
established at p < 0.05.
Results
Fifty-three patients were enrolled in the present study. Of these, 30 had tinnitus
(study group) and 23 did not have tinnitus (control group). The mean age was 46.12
years (standard deviation, 16.1 years). Thirty-three patients were women (63.5%).
[Table 1 ] shows a comparison of age and gender between groups; there were no statistically
significant differences.
Table 1
Distribution of age and gender in the overall sample and in the groups with and without
tinnitus
Variable
Overall
Tinnitus (n = 30)
No tinnitus (n = 23)
p
Age (years), mean ± SD
46.1 ± 16.1
48.9 ± 15.6
42.6 ± 16.4
0.172[a ]
Women, n (%)
33 (63.5)
16 (55.2)
17 (73.9)
0.247[b ]
a Student t -test.
b Fisher exact test.
As shown in [Table 2 ], disc displacement with reduction was the most common MRI finding in both groups.
A statistically significant difference was observed only for the frequency of disc
displacement with reduction, which was significantly higher in patients with tinnitus.
Table 2
Frequency of magnetic resonance imaging findings in patients with temporomandibular
joint disorder with and without tinnitus
Variable
Tinnitus (n = 30)
No tinnitus (n = 23)
p
[a ]
Condylar morphology
0.719
Unilateral
3 (10.0)
3 (13.0)
Bilateral
8 (26.7)
8 (34.8)
Articular eminence morphology
0.111
Unilateral
1 (3.3)
1 (4.3)
Bilateral
−
3 (13.0)
Disc morphology
0.325
Unilateral
1 (3.3)
2 (8.7)
Bilateral
14 (46.7)
14 (60.9)
Disc displacement with reduction
0.043
Unilateral
−
3 (13.0)
Bilateral
24 (80.0)
12 (52.2)
Intra-articular effusion
0.522
Unilateral
2 (6.7)
3 (13.0)
Bilateral
1 (3.3)
2 (8.7)
Condylar translation
0.095
Unilateral
9 (30.0)
14 (60.9)
Bilateral
10 (33.3)
4 (17.4)
All variables expressed as means and standard deviations.
Bold indicates statistical significance.
a Fisher exact test for comparison between total (unilateral + bilateral) values.
[Fig. 1 ] shows a representative MRI of disc displacement with reduction in a participant
from the tinnitus group.
Fig. 1 Parasagittal T1-weighted magnetic resonance imaging of the temporomandibular joint
(A, closed mouth; B, open mouth) showing anterior disc displacement (arrow) with reduction.
As shown in [Table 3 ], no between-group difference in TMD severity score was observed.
Table 3
Temporomandibular severity score (mean ± SD) in patients with and without tinnitus
TMD severity score
p
[a ]
Tinnitus (n = 30)
No tinnitus (n = 23)
5.27 ± 2.05
5.78 ± 2.00
0.363
Abbreviations: SD, standard deviation; TMD, temporomandibular joint disorder.
a Student t -test for independent samples.
Discussion
The present study set out to analyze the existence of specific MRI findings in patients
with TMD and tinnitus that could differentiate them from patients with TMD without
tinnitus. A few studies so far have analyzed characteristic imaging features of tinnitus,[14 ]
[18 ] but none has focused specifically on the association of TMD and tinnitus.
Upon analysis of MRI findings in patients with tinnitus and those without, we observed
that disc displacement with reduction was significantly more frequent in patients
with tinnitus. Historical studies, such as that by Myrhaug,[19 ] suggest that tinnitus originates from a temporomandibular dysfunction of muscular
origin, which might cause secondary hypertonia of the tensor tympani and tensor veli
palatini, thus triggering aural symptoms. The sensory-motor theory, in turn, postulates
that tinnitus may be modulated by muscle contractions, such as those that occur on
palpation of myofascial trigger points. On the other hand, a classic study[20 ] reported the existence of a ligament (the discomalleolar ligament) that attaches
to the malleus, crosses the petrotympanic fissure, and then attaches to the posteromedial
aspect of the articular disc and capsule. Thus, excursion of the disc and condyle
during mandibular motion could impart mobility to the malleus and alter tension in
the tympanic membrane,[3 ] which could explain the otologic symptoms, among them tinnitus, experienced by patients
with disc displacement. Indeed, the landmark studies of Block,[21 ] Ren and Isberg,[22 ] and Paparo et al[23 ] correlated disc displacement with tinnitus, corroborating the findings of our investigation.
Costen,[24 ] Coleman,[25 ] and Komori et al[26 ] found no relationship between disc displacement without reduction and tinnitus,
but did find a correlation in disc displacement with reduction; these findings are
consistent with our results. It bears stressing that comparison of prior findings
to those of the present study is hindered by the fact that previous studies neither
performed objective MRI investigation nor used comparative designs. It should also
be noted that a causal relationship between tinnitus and TMD or MRI findings is still
hypothetical and has not yet been established in the literature.
The severity scale proposed in the present study can also contribute to further research
in the field (i.e., MRI-based investigation of the relationship between TMD and tinnitus).
The mean scores obtained in the groups with and without tinnitus were not significantly
different. However, this finding may simply reflect that MRI is unable to discriminate
between individuals with tinnitus and those without, which suggests that other imaging
criteria, or perhaps even another imaging modality, should be explored for study of
the relationship between TMD and tinnitus. Moreover, the fact that nearly all patients
with tinnitus and TMD exhibited bilateral disc displacement with reduction (80% versus
52% in patients without tinnitus) suggests that this specific abnormality warrants
further exploration in future studies with larger samples.
One positive aspect of this study was the homogeneity of gender and age distribution
between the groups with and without tinnitus. Another strength was the absence of
referral bias, as all patients had been referred to us by otologists after excluding
individuals with tinnitus of known etiology. Thus, inclusion in the present study
was restricted to patients with clinical symptoms of TMD in whom other comorbidities
had been ruled out.
Limitations of this study include the sample size, which, though adequate for the
proposed objective, did not allow statistical comparison of subgroups. This may have
prevented us from capturing the full dimension of the correlation between severity
and prevalence of TMD and tinnitus. Also, a causal relationship between tinnitus and
TMD was not established in the present study. However, the present results can serve
as a basis for larger prospective studies to shed further light on the relationship
between TMD and tinnitus. In addition, further studies are needed on the effect of
disc repair on tinnitus, an aspect which was not explored in the present study.
Conclusion
The present study shows that MRI may not be sufficiently sensitive to detect specific
aspects of the relationship between tinnitus and TMD. However, the identification
of differences in the prevalence of disc displacement with reduction between individuals
with and without tinnitus may provide an important contribution to treatment of these
patients, and suggests there is further room to explore the relationship between tinnitus
and TMD.
