Aural symptoms in patients with temporomandibular joint disorders: multiple frequency tympanometry provides objective evidence of changes in middle ear impedance.

Abstract

The association of temporomandibular joint (TMJ) disorders with aural symptoms, such as tinnitus, otic fullness, and subjective decrease of hearing acuity, is a well-established clinical observation. Although several hypotheses have been made about the otic-conductive origin of these complaints, conventional 226-Hz tympanometry has failed to demonstrate any middle ear abnormalities. The aim of this study was to evaluate patients with TMJ disorders with multiple frequency tympanometry (MFT).
Prospective clinical study.
Outpatient clinic.
The population of this study consisted of 40 patients with unilateral TMJ disorders diagnosed for longer than 1 month.
After verifying that there were no abnormal otoscopic findings, 226-Hz tympanometry, conventional pure-tone audiometry, brainstem auditory evoked potentials, and MFT were performed.
Resonant frequency (RF) values.
With the exception of MFT, no abnormal audiologic findings were revealed. The ear ipsilateral to the lesion demonstrated significantly higher (p = 0.002) RF values in comparison to the contralateral ear. The difference in RF values was more obvious in patients aged 45 years or younger.
The results of this study imply an increase in the stiffness of the middle ear, which has not been detected by conventional tympanometry. This represents the first concrete documentation of minor alterations in the conductive properties of the middle ear and seems to support the various hypotheses on the middle-ear origin of aural complaints in patients with TMJ disorders. Further studies are needed before a clear insight on the presumably multifactorial pathophysiology of these complaints can finally be reached.

Full text

Page 1

Aural Symptoms in Patients With Temporomandibular
Joint Disorders: Multiple Frequency Tympanometry
Provides Objective Evidence of Changes
in Middle Ear Impedance
*Maria Riga, †John Xenellis, †Eleni Peraki, †Elisa Ferekidou, and †Stavros Korres
*ENT Department, University Hospital of Alexandroupolis, Demokritos University of Thrace, Alexandroupolis;
and ÞENT Department, Hippokration Hospital of Athens, National University of Athens, Athens, Greece
Objective: The association of temporomandibular joint (TMJ)
disorders with aural symptoms, such as tinnitus, otic fullness,
and subjective decrease of hearing acuity, is a well-established
clinical observation. Although several hypotheses have been
made about the otic-conductive origin of these complaints, con-
ventional 226-Hz tympanometry has failed to demonstrate any
middle ear abnormalities. The aim of this study was to evaluate
patients with TMJ disorders with multiple frequency tympano-
metry (MFT).
Study Design: Prospective clinical study.
Setting: Outpatient clinic.
Patients: The population of this study consisted of 40 patients
with unilateral TMJ disorders diagnosed for longer than 1 month.
Interventions: After verifying that there were no abnormal
otoscopic findings, 226-Hz tympanometry, conventional pure-
tone audiometry, brainstem auditory evoked potentials, and
MFT were performed.
Main Outcome Measure: Resonant frequency (RF) values.
Results: With the exception of MFT, no abnormal audiologic
findings were revealed. The ear ipsilateral to the lesion dem-
onstrated significantly higher (p = 0.002) RF values in com-
parison to the contralateral ear. The difference in RF values
was more obvious in patients aged 45 years or younger.
Conclusion: The results of this study imply an increase in the
stiffness of the middle ear, which has not been detected by
conventional tympanometry. This represents the first concrete
documentation of minor alterations in the conductive properties
of the middle ear and seems to support the various hypotheses
on the middle-ear origin of aural complaints in patients with
TMJ disorders. Further studies are needed before a clear in-
sight on the presumably multifactorial pathophysiology of
these complaints can finally be reached. Key Words: Multiple
frequency tympanometryVOtic fullnessVTemporomandibular
jointVTinnitus.
Otol Neurotol 31:1359Y1364, 2010.
Several epidemiologic studies have established the
observation that patients with temporomandibular joint
(TMJ) disorders complain for otologic symptoms in the
ear ipsilateral to the lesion, far more frequently than
controls (1Y3). In particular, the frequency of otalgia in
TMJ patients ranges from 20% to 100%, tinnitus from
31% to 59%, and hearing loss from 15% to 32% (4).
However, despite the extensive research and the repeti-
tion of several hypotheses, this well-documented clinical
association has not been supported by audiometric doc-
umentation yet (5,6). As a result, the pathophysiology of
this clinical association remains unknown, controversial,
or even doubtful.
For the last few years, pure-tone audiometry, conven-
tional tympanometry, or even electromyographic studies
of the tensor palatini muscles have failed to demonstrate
an association between TMJ disorders and any middle
or inner ear lesion (4,7). Therefore, most theories have
focused on central nervous system networks. Conven-
tional 226-Hz tympanometry seems to be a far less sen-
sitive method than multiple frequency tympanometry
(MFT) to detect subtle mechanoacoustic changes of mass
and stiffness of the middle ear system (8Y12).
The aim of this study was to investigate the bio-
mechanics of the middle ear in patients with TMJ dis-
orders using MFT. The objective documentation of a
middle ear dysfunction in these patients may finally
provide some objective diagnostic proof for what has
been for many years only a clinical suspicion. Addition-
ally, it may contribute to the understanding of the
Address correspondence and reprint requests to Maria Riga, M.D.,
Ph.D., Demokritos University of Thrace, 35 Leoforos Makris, Nea Chili,
68100, Alexandroupolis, Greece; E-mail: mariariga@hotmail.com
Otology & Neurotology
31:1359Y1364 ? 2010, Otology & Neurotology, Inc.
1359
Copyright © 2010 Otology & Neurotology, Inc. Unauthorized reproduction of this article is prohibited.

Page 2

TABLE 1.
Multiple frequency tympanometry data and static compliance data from patients with unilateral temporomandibular joint disorders
Patient
Resonant frequency (Hz)
Static admittance (ml)
Peak pressure (daPa)
Tympanometric width (daPa)
Ipsilateral
Contralateral
Difference
Ipsilateral
Contralateral
Difference
Ipsilateral
Contralateral
Difference
Ipsilateral
Contralateral
Difference
1
1,200
1,000
200
0.5
0.4
+
10
10
=
111
122
j
2
950
750
200
1.2
1.1
+
5
j10
+
55.6
77.8
j
3
950
850
100
0.6
0.3
+
5
15
j
77.8
111
j
4
650
1,350
j700
0.9
0.4
+
j15
5
j
89
122
j
5
1,000
550
450
0.3
0.3
j
j5
j10
+
144
222
+
6
1,150
1,050
100
0.9
0.1
+
10
10
=
100
100
=
7
1,400
1,250
150
0.7
0.3
+
45
120
j
167
144
+
8
1,150
1,050
100
0.7
1
j
j35
5
j
44.4
77.8
j
9
1,500
1,350
150
0.7
1
j
5
5
=
55.6
67
j
10
1,300
950
350
1.2
1
+
5
j50
+
44.4
55.6
j
11
1,300
1,200
100
0.8
0.4
+
0
j10
+
89
111
j
12
1,300
1,000
300
0.5
0.5
=
5
5
=
77.8
89
j
13
1,250
950
300
1
2.2
j
10
10
=
55.6
33.3
+
14
1,050
900
150
1.8
1.9
j
5
10
+
133.3
100
+
15
950
900
50
1.6
2.3
j
5
5
=
67
67
=
16
1,000
950
50
1.7
1.5
+
5
5
=
67
56
+
17
1,150
950
200
0.4
0.4
=
25
15
+
122
111
+
18
1,200
1,000
200
1
1.3
j
j20
5
j
89
55.6
+
19
450
1,000
j550
0.3
0.8
j
10
10
=
267
44.4
+
20
1,100
1,300
j200
0.7
0.9
j
j25
5
j
89
67
+
21
1,300
1,100
200
1.5
1.8
j
0
5
j
99
67
+
22
1,150
1,000
150
0.4
1.1
j
10
5
+
144
33.3
+
23
600
950
j350
0.5
0.6
j
5
5
=
178
111
+
24
1,250
1,150
100
0.3
0.3
=
10
10
=
89
44.4
+
25
1,350
1,150
200
0.4
0.3
+
5
10
j
89
89
=
26
550
650
j100
0.6
0.7
j
10
10
=
122
111
+
27
900
950
j50
0.5
0.7
j
j5
5
j
100
33.3
+
28
950
900
50
0.9
0.6
+
20
35
j
55.6
55.6
=
29
800
650
150
0.3
0.3
=
5
10
j
111
122
j
30
1,500
1,000
500
0.4
0.5
j
j5
j5
=
55.6
76
j
31
1,400
1,100
300
0.4
0.8
j
20
15
+
44.4
55.6
j
32
1,300
900
400
1.1
0.7
+
10
10
=
128
131
j
33
1,200
900
300
0.9
0.6
+
j15
j45
+
77.8
89
j
34
1,100
850
250
1.2
1.1
+
10
j10
+
55.6
53.4
+
35
1,150
850
300
0.7
1.1
j
5
10
j
133.3
100
+
36
1,350
1,050
200
0.7
1.1
j
10
50
j
67
159
j
37
1,500
1,400
100
0.1
0.4
j
10
5
+
70
85
j
38
1,400
1,300
100
1
0.8
+
10
10
=
122
121
=
39
1,450
1,350
100
0.8
0.6
+
j75
5
j
89
55.6
+
40
1,350
1,100
250
0.9
1.1
j
20
40
j
237
64.4
+
Mean
1,138.8
1,015
121.2
0.8
0.8
0.6
7.3
99.6
86.1
Standard deviation
263.5
197.8
235.9
0.4
0.5
23.3
25.4
48.6
38.7
p
0.002
0.5
0.09
0.13
BIpsilateral[ and Bcontralateral[ refer to temporomandibular joint lesions. Difference = result after subtraction of the contralateral to the lesion tympanometric value from the respective ipsilateral to the
lesion value. A positive result (+) result means that the respective value is larger for the ear ipsilateral to the lesion.
1360 M. RIGA ET AL.
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Page 3

pathophysiology of otologic symptoms in patients with
TMJ disorders.
PATIENTS AND METHODS
The population of this study consisted of patients with uni-
lateral TMJ disorders diagnosed for longer than 1 month. The
diagnosis of TMJ disorders was made in the outpatient oral and
maxillofacial clinic upon a subjective symptom questionnaire,
a general medical history, a dental x-ray examination, and a
standardized clinical examination (7,13). The subjective inclu-
sion criteria were intrarticular pain and/or TMJ pain upon pal-
pation and especially upon mouth opening. Clunck sounds from
the TMJ, trismus, and restriction of the movement of the TMJ
were regarded as objective inclusion criteria. All patients were
subjected to panoramic x-ray imaging of the maxilla to exclude
dental pathology. Data on aural symptoms were gathered dur-
ing medical history taking from the patients_ positive or nega-
tive answers about the presence of otalgia, pain around the
ear, tinnitus, otic fullness, or subjective loss of hearing acuity.
Answers were recorded on a simple questionnaire, developed
in the clinic for the needs of this study. Patients with active or
recent history of otologic disease, ear surgery, inflammation of
the upper respiratory tract, major head trauma, meningoence-
phalitis, arthritis, exposure to noise, ototoxic medication, or
radiotherapy were excluded from the study. Family history for
hereditary hearing loss also was negative in all patients.
All patients were subjected to otoscopy and removal of any
cerumen from the external auditory canal. Provided that there
were no abnormal otoscopic findings, conventional tympano-
metry (226 Hz), conventional pure-tone audiometry, brainstem
auditory evoked potentials,and MFT were performed.Pure-tone
audiometry measurements were made using the clinical audi-
ometer amplaid 309. Brainstem auditory evoked potentials were
performed with Bera So 1 (Hornib & Zeisberg). Acoustic im-
mittance measurements were performed with GSI 33, version 2,
a middle ear analyzer of Grason Stadler (calibrated according to
the ANSI specifications for acoustic immittance instruments,
1987). Ear canal pressure for the conventional probe-tone fre-
quency of 226 Hz was swept in a positive-to-negative direction
from +20daPatoj400daPa ata pumpspeed of 50daPa/s.Three
immitance measures were used to compare the ears ipsilateral
to the lesion with the contralateral ones. Tympanometric peak
height or peak compensated static admittance in milliliters
(numerically equivalent to millimhos) and tympanometric peak
pressure in decapascals (daPa) were automatically printed on the
graphs, whereas the tympanometric width was calculated as
the pressure interval in daPa, where a horizontal line intersects
the tympanogram at 50% of its peak height (14,15).
The GSI-33 plots the difference between susceptance (B)
and phase angle at an extreme ear canal pressure (+200 daPa)
and at the tympanometric peak as a function of frequency after
performing 2 consecutive sweeps of frequency from 250 to
2,000 Hz in 50 Hz steps. Then, by automated subtraction of
corresponding values for each frequency, the resonant fre-
quency (RF) is identified as the frequency where the change in
susceptance (DB) reaches 0 mmhos (16).
The immitance RF results obtained from the ear ipsilateral
to the TMJ disorder were compared with the contralateral ear,
which was used as control, through Wilcoxon_s signed rank test.
Nonparametric methods were chosen over parametric ones
because the distribution of the variables of interest was not
normal, and the sample of the study was limited. According
to their age, the patients were divided into 2 age groups, and
Mann-Whitney U test was used for the comparisons of the RF
measurements obtained from the 2 age groups. Fischer_s exact
test was used for comparing the frequencies of the reported aural
symptoms between the 2 age groups. The study was approved
by the local institutional review board.
RESULTS
Forty patients (36 women and 4 men ) aged 20 to
60 years (mean, 42.9 yr; standard deviation [SD] = 15)
were included in the study. The first age group consisted
of 19 patients aged 45 years or younger, and the second
group consisted of the remaining 21 patients aged older
than 45 years. Right unilateral TMJ disorder was diag-
nosed in 25 patients. In the remaining 15 patients, the
lesion was located in the left TMJ. Otalgia was reported
by 24 (60%) of the 40 patients in this study, pain around
the ear by 29 (72.5%), tinnitus by 28 (70%), otic fullness
by 12 (30%), and subjective loss of hearing acuity by 12
(30%). Fischer_s exact test revealed significant difference
in the reported aural symptoms between the 2 age groups
only for the subjective loss of hearing acuity (p = 0.002),
which was most frequently reported among patients aged
older than 45 years. Conventional pure-tone audiometry
attributed symmetrical audiograms in all patients. With
respect to each patient_s age, hearing acuity was within
normal limits for both ears and for all the patients
included in this study. Accordingly, auditory brainstem
evoked potentials did not demonstrate any abnormal
findings.
All patients exhibited type A 226-Hz tympanometric
curves,accordingtoJerger_s classification.Low-frequency
tympanometry failed to demonstrate any significant dif-
ferences between the ear ipsilateral to the lesion and that
contralateral to the lesion, although static admittance,
tympanometric peak pressure, and tympanometric width
were all recorded and compared (Table 1).
The RF values attributed by the subsequent MFT
examination were found higher in the ear ipsilateral to the
TABLE 2. Results of the present study in comparison to those of previous studies that have used
the same middle ear analyzer, GSI-33
Resonant
frequency (Hz) Hanks and Mortensen (21)Valvik et al. (17)
Ipsilateral to temporomandibular
joint disorder (present study)
Contralateral to temporomandibular
joint disorder (present study)
Mean
Standard deviation
Range
908
188
1,049
261
650Y1,500
1,138.75
263.48
450Y1,500
1,015
197.8
650Y1,400650Y1,300
Hanks and Mortensen (21) reported the results from 53 healthy subjects aged 18 to 25 years. Valvik et al. (17) reported the results from 100 subjects.
1361 IMMITANCE CHANGES IN TMJ DISORDERS
Otology & Neurotology, Vol. 31, No. 9, 2010
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Page 4

TMJ disorder in 34 (85%) of 40 patients compared with
the ear contralateral to the lesion of the same patient
(Table 1). RF values in the ear ipsilateral to the TMJ dis-
order were found lower in comparison to the contralateral
ear of the same patient in a significantly smaller percen-
tage, in 6 (15%) of 40 patients. The RF values recorded
from the ear ipsilateral to the TMJ disorder ranged from
450 to 1,500 Hz (mean, 1,138.75; SD, 263.48). The RF
values recorded from the ear contralateral to the TMJ
lesion ranged from 650 to 1,400 Hz (mean, 1,015; SD,
197.8) (Table 2). The ear ipsilateral to the lesion demon-
strated significantly higher RF values (mean difference,
121.7 Hz; Wilcoxon signed ranks test, p = 0.002). The
difference in RF values between the 2 ears was more
obvious in patients aged 45 years or younger (Mann-
Whitney U test, p = 0.031).
DISCUSSION
MFT is the measurement of acoustic immitance of the
middle ear as a function of ear canal air pressure. RF
corresponds to the frequency at which mass and stiffness
contribute equally to the middle ear admittance. This
means that near RF total susceptance is nearly zero, so
conductance is the only component contributing to the
admittance of the system at this frequency. RF is directly
proportional to the square root of stiffness of the middle
ear system and indirectly proportional to the square root
of mass. Therefore, mass loading pathologies (such as
ossicular discontinuity) are known to be associated with a
lowering of RF, whereas pathologies that increase middle
ear stiffness (e.g., otosclerosis, tympanosclerosis, or
Me ´nie `re_s disease) have been shown to shift resonance to
a higher frequency (17Y19). The diagnostic sensitivity of
MFT has been repeatedly proven higher than that of
standard tympanometry because the latter often has failed
to distinguish normal middle ears from ears with lesions
that specifically affect the ossicular chain, such as oto-
sclerosis (10Y12) or otitis media with effusion (8,9,20).
To date, the acoustic immitance of the middle ear of
patients with TMJ disorders has only been examined by
the use of conventional 226-Hz tympanometry (4).
According to the results of this study, TMJ disorders
seem to be another example, where subtle alterations in
the biomechanics of the middle ear nondetectable with
standard tympanometry are revealed with MFT (Table 1).
In particular, TMJ disorders seem to be associated with an
increase in the stiffness of the middle ear system, which
is demonstrated as an increase in the middle ear RF.
BecauseofthewiderangeofnormalRFvalues,thehealthy
earofeachpatientwasusedascontrol.Theresultsobtained
for the ears contralateral to the TMJ lesion were in accor-
dancewiththereferencerangeformeasurementsinhealthy
ears performed with the GSI middle ear analyzer and
reported by Hanks and Mortensen (21) (908 T 188 Hz),
Valvik et al. (17) (1049 T 261 Hz), and Ogut et al. (19)
(934.6 T 142.7 Hz) (Table 2).
The increase of RF reported in this study provides the
first documentation of minor middle ear pathology in
patients with TMJ disorders using immitance measure-
ments. Indeed, human adult and fetus dissection has
confirmed a direct anatomic link between the malleus and
the TMJ through the discomalleolar and anterior mal-
leolar ligaments (22Y25). The sphenomandibular liga-
ment is inferiorly fixed to the mandible and superiorly
fixed to the sphenoid spine. Alkofide et al. (26) found that
in 68% of their specimens, the sphenomandibular liga-
ment of the mandible passed through the petrotympanic
fissure, into the middle ear and on the anterior malleolar
ligament, whereas in 8% of their specimens, it attached
directly to the malleus. The force that is transmitted from
these ligaments to the malleus may result in an altered
stapes_ position. Nakajima et al. (27) demonstrated that a
total or partial fixation of the anterior malleolar ligament
may reduce hearing sensitivity in a pattern simulating an
otosclerosis condition. Functional or inflammatory joint
disorders, such as disc luxation or secondary edema,
might thus affect middle ear ossicular equilibrium pro-
vided that the fibrous connections on the walls of the
petrotympanic fissure are loose (28Y30).
The increase in the stiffness of the middle ear system
may be attributed to additional pathogenetic mechanisms.
Another widely accepted explanation seems to derive
from an auditory innervation pattern involving the tri-
geminal nerve (2,31). The tensor tympani (TT, malleus
muscle) and the tensor veli palatini (TVP, Eustachian
tube muscle) are middle ear muscles functionally modu-
lated by trigeminal motor nucleus motoneurons, which
also modulate mastication muscles. The TVP and the TT
muscles intermingle their fibers in the middle ear and act
synergistically, raising temporarily intratympanic pres-
sure when they contract together (31,32). Hypertonia of
the internal pterygoid muscle caused by neuromuscular
dysfunction in TMJ patients can produce a reflex hyper-
tonia of the TT muscle (33,34). The association of aural
symptoms in patients with TMJ disorders with hypertonia
of the mastication muscles seems to be further supported
by the observation that 75% to 80% of patients were able
to vary tinnitus intensity by isometric orofacial and cra-
niocervical manipulations (35Y37). This association was
questioned (38Y40), mainly on the basis that deaf people
demonstrated the same high prevalence of somatically
induced tinnitus and tinnitus changes (38). Because
deafness might, through neural plasticity, have its own
unpredictable and unknown effect on the central nervous
system pathways, the possible causal effect of neural
interactions between the trigeminal somatosensory inputs
from the jaw muscles and the dorsal cochlear nucleus
projections seems to remain a strong pathogenetic alter-
native. Moreover, the trigeminal nerve plays an important
role in regulating and balancing cochlear vascular tone
and inner ear blood flow. These patterns along with
individual anatomic differences may account for the
decreased RF values found in a limited number of ears
ipsilateral to the TMJ disorder (Patients 4,19, and 23) (2)
(Table 1).
Following previous reports on otitis media with effu-
sion, persistence of middle ear fluid seems to be the
1362M. RIGA ET AL.
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Page 5

simplest but less probable suggestion (7,8,19). Marasa
and Ham (41) suggested that edema produced by TMJ
inflammatory disorders can spread through the petro-
tympanic fissure to the middle ear and produce serous
otitis media. Furthermore, fdema produced in the TMJ
can spread collected fluid through the petrotympanic
fissure to the middle ear (42).
In everyday clinical practice, the interpretation of MTF
recordings often may be difficult because of the wide
reference range and the considerable overlapping of the
distributions of RF values in normal and abnormal ears
(Table 1). However, in a population of patients with TMJ
disorders, the significant elevation of RF values in the
ears ipsilateral to the lesion provides the first concise evi-
dence of an increase in the stiffness of the middle ear
system and offers new insight in the pathophysiology of
aural symptomsof patientswith TMJ disorders.The causal
association of these subtle alterations in the middle ear
stiffness with aural symptoms, such as tinnitus, otic full-
ness, and loss of hearing acuity, may be supported by the
fact that the results of this study are comparable with those
of Ogut et al. (19), where similar changes in the middle ear
stiffness have been demonstrated to differentiate healthy
from surgically confirmed otosclerotic ears.
CONCLUSION
TMJ disorders seem to be associated with an increased
stiffness of the middle ear system ipsilateral to the lesion
compared with the contralateral ear. This difference may
account for the aural complaints that are frequently pres-
ent in these patients. The documentation of this small
change in the middle ear biomechanics through MFT
is not surprising, whereas conventional tympanometry
studies have failed to diagnose any middle ear pathol-
ogy. Several previous studies have concluded that MFT
is much more sensitive than 226-Hz tympanometry in
diagnosing small changes caused by a variety of middle
ear pathologies, particularly otitis media with effusion
and otosclerosis. This MFT study provides the first con-
crete audiologic evidence for an association between
TMJ and middle ear conduction disorders and thus sup-
ports the respective hypotheses that have previously
been suggested by several researchers. Further studies
are needed before the presumably multifactorial patho-
physiology (conductive, vascular, and somatosensory)
of this common clinical observation finally becomes
comprehendible.
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considerationson the dis-
1363 IMMITANCE CHANGES IN TMJ DISORDERS
Otology & Neurotology, Vol. 31, No. 9, 2010
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