Download Effects of tensor tympani muscle contraction on the middle ear and

The Laryngoscope
C 2012 The American Laryngological,
V
Rhinological and Otological Society, Inc.
TRIOLOGICAL SOCIETY
CANDIDATE THESIS
Effects of Tensor Tympani Muscle Contraction on the Middle Ear
and Markers of a Contracted Muscle
Manohar Bance, MB, MSc; Fawaz M. Makki, MD; Philip Garland, PhD; Wael A. Alian, MD, PhD;
Rene G. van Wijhe, MEng; Julian Savage, MBBS, FRCS
Objectives/Hypothesis: Many otologic disorders have been attributed to dysfunction of the tensor tympani muscle,
including tinnitus, otalgia, Meniere’s disease and sensorineural hearing loss. The objective of this study was to determine
adequate stimuli for tensor tympani contraction in humans and determine markers of the hypercontracted state that could
be used to detect this process in otologic disease.
Study Design: Multiple types of studies.
Methods: Studies included 1) measuring middle ear impedance changes in response to orbital puffs of air, facial stroking, and self-vocalization; 2) measuring changes in stapes and eardrum vibrations and middle ear acoustic impedance in
response to force loading of the tensor tympani in fresh human cadaveric temporal bones; 3) measuring changes in acoustic
impedance in two subjects who could voluntarily contract their tensor tympani, and performing an audiogram with the
muscle contracted in one of these subjects; and 4) developing a lumped parameter computer model of the middle ear while
simulating various levels of tensor tympani contraction.
Results: Orbital jets of air are the most effective stimuli for eliciting tensor tympani contraction. As markers for tensor
tympani contraction, all investigations indicate that tensor tympani hypercontraction should result in a low-frequency hearing
loss, predominantly conductive, with a decrease in middle ear compliance.
Conclusions: These markers should be searched for in otologic pathology states where the tensor tympani is suspected
of being hypercontracted.
Key Words: Tensor tympani, middle ear muscles, laser Doppler vibrometry, tensor tympani syndrome.
Laryngoscope, 123:1021–1027, 2013
INTRODUCTION
The middle ear muscles (MEM) have a long history
of being implicated in many inner ear otologic disorders
such as tinnitus, otalgia, Meniere’s disease, and sensorineural hearing loss (e.g., Weber1). More recently, spasm of
the tensor tympani (TT) has been implicated in a range of
conditions including tinnitus,2 otologic symptoms in myofascial pain-dysfunction syndrome,3 and Meniere’s
disease, for which sectioning of the TT has been a sugFrom the Division of Otolaryngology, Department of Surgery (M.B.,
School of Biomedical Engineering (P.G.), and Ear and Auditory
Sciences Laboratory (R.G.V.W.), Dalhousie University, Halifax, Nova Scotia,
Canada; Department of Otolaryngology and Head and Neck Surgery
(W.A.A.), Sahlgrenska University Hospital, Goteborg University, Goteborg,
Sweden; and Division of Otolaryngology (J.S.), Hôtel-Dieu, University de
Sherbrooke, Sherbrooke, Quebec, Canada.
Editor’s Note: This Manuscript was accepted for publication August 9, 2012.
This work was performed entirely at the Ear and Auditory
Research Laboratory, Division of Otolaryngology, Department of Surgery,
Dalhousie University, Halifax, NS, Canada.
Part of this work was funded by grants from Dalhousie University
Faculty of Medicine, Nova Scotia Health Research Foundation.
The authors have no other funding, financial relationships, or conflicts of interest to disclose.
Send correspondence to Manohar Bance, MB, Professor, Division
of Otolaryngology, Department of Surgery, Dalhousie University, 3184
Dickson Building, VGH Site, QEII HSC, 1278 Tower Road, Halifax, NS,
Canada B3H 2Y9. E-mail: [email protected]
F.M.M.),
DOI: 10.1002/lary.23711
Laryngoscope 123: April 2013
gested treatment.4 Klockhoff5 also described a tensor
tympani syndrome characterized by fluctuation in the
middle ear impedance and complaints of fullness, tinnitus, and dysacusis, and highly related to tension
headache and vertigo. It has also been speculated that the
TT medializes the stapes into the oval window, resulting
in changes in inner ear perilymphatic pressures,6 which
in turn may lead to various inner ear disorders.
Although clonic (dynamic) contractions of the TT
might be detected easily, tonic (fixed) contractions are not,
because of the large normal ranges in the tests that could
detect contractions (e.g., middle ear compliance). Today,
the role of the TT in physiology and otologic disease is
largely speculative. Unlike the stapedius, the TT is not
normally activated by sound.7 After a flurry of scientific
activity in the late 19th and early 20th century, the TT
has been almost ignored in recent decades (see Wever and
Lawrence8 for an excellent review). Reflex contraction of
the TT muscle has been reported to be elicited by tactile
stimulation of facial areas,7 electrical stimulation of the
tongue,9 a puff of air against the orbit,10,11 swallowing,12
and during activation of some muscular groups of the
face, neck, and phonation.13 The TT is most commonly
reported to contract as part of the startle reaction.10
Reports implicating the MEM as the cause of otologic pathology tend to focus on the TT muscle, as does this work,
but it should be recognized that contraction of the TT
Bance et al.: Markers of Tensor Tympani Muscle Contraction
1021
Fig. 1. Modified mechanical lumped parameter model for human ear including the tensor tympani.
cannot be directly measured or reliably distinguished
from that of the stapedius with most tests, and they may
well co-contract in many pathologic situations. As such,
several lines of investigations were used in this report
because none can directly measure TT contraction.
MATERIALS AND METHODS
Experiments were approved by our institutional ethics
boards. This work is divided into several sections.
Stimuli Eliciting TT Contraction in
Live Subjects
Twenty subjects with self-reported normal hearing and tympanograms were tested. Middle ear compliance was tested with a
226-Hz tone using a GSI TympStar (Grason-Stadler, Eden Prairie, MN) middle ear analyzer. Impedance changes were measured
for the following stimuli: 1) stroking the face with a fine brush for
5 seconds, 2) mentally counting from 1 to 10 (true vocalization
would cause sound radiation into the ear), and 3) delivering four
puffs of air at random intervals from a rubber bulb to the closed
ipsilateral eye or to the contralateral eye. The conditions and left
and right ears were randomized in presentation.
Temporal Bone Data
Middle ear laser Doppler vibrometry measurements.
Five temporal bones were harvested from cadaveric donors
within 48 hours of death. Cortical mastoidectomy and posterior
tympanotomy were performed. This preparation has been
described for other experiments.14 Vibrations of the tympanic
membrane (TM) and stapes were measured using either a single-point laser Doppler vibrometer (LDV) (OFV-302 sensor
head, OFV-3000 vibrometer controller), or during later experiments a scanning laser Doppler vibrometer (PSV-I-400
scanhead, OFV-505 laser head, OFV-5000 vibrometer controller)
by Polytec PI (Tustin, CA). Three bones were tested with the
single point and two with the scanning laser.
To simulate TT contraction, a 5-0 nylon suture was looped
around the TT and directed posteriorly, and connected to a pulley system to provide force loading. In-line loading directly in
the axis of the TT would require drilling into the cochlea. Single-point LDV measurements were performed on the stapes
footplate center and on the umbo in three temporal bones corresponding to pulley masses of 0, 20, and 60 g. Measurements
with the scanning LDV were performed on the whole TM and
stapes footplate, with masses of 0, 26, 52, 76, and 100 g (and 13
g for the last bone). Not all measurements could be completed
on all bones because of various noise and preparation artifacts.
Therefore, one of the two bones used for scanning LDV only has
measurements on the umbo.
Two further bones were prepared similarly, and a tympanometer was used to measure the impedance change for a force
of 0.5 N (equivalent to 50-g mass) applied to the TT tendon.
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Live Subject Data
Several subjects were screened who could voluntarily
move their TMs, but most could not hold contractions for more
than few seconds. We hypothesized that eardrum movements
large enough to be macroscopically visible could only come from
TT contraction, although the stapedius may co-contract. Only
two participants, a male aged 45 years and a female aged 37
years, could hold contractions long enough for us to measure
tympanometry, and only one long enough to perform an audiogram. Acoustic impedance using a tympanometer was also
measured using a standard 226-Hz probe tone. Only the right
ear is reported, as results were symmetrical.
Computer Models
A lumped parameter computer model was created based
on the model by Feng and Gan.15 The nonlinear mechanical
properties of the TT described by Cheng and Gan16 were incorporated into this model. Details of this model can be found in
Garland et al.17 Essentially, the nonlinear effect of this muscle
is incorporated into the mathematical model by choosing a
given static load value (and corresponding displacement) on the
TT and taking the effective stiffness (KTT) as the slope of the
curve at this load point. The effect of TT contraction is implemented by including a linear spring attached to the malleus.
Figure 1 shows the slightly modified schematic representation
of the model presented by Feng and Gan15 used for this study.
The values of the masses were taken from previously published
works and some ad hoc assumptions.17
Wideband reflectance measurements were also made in several TT conditions, but the results were complex, and due to
article size limitations will be discussed in a separate publication.
RESULTS
Eliciting TT Contraction in Normal Subjects
A measurable impedance change associated with
stroking the side of the subject’s face or having the subject
mentally vocalize counting 1 to 10 was not found in any of
subjects tested. Results for orbital jets of air over the closed
eye are shown in Table I, as are the average compliance
changes. In general, positive changes (increase in impedance, decrease in compliance) were more than twice as
common as negative (decrease in impedance, increase in
compliance) changes. Only one subject had no change in
impedance to either ipsilateral or contralateral orbital jets.
Temporal bone LDV measurements. Figure 2A
and 2B show results of the single LDV measurements on
the vibrations of the umbo and stapes footplate, respectively, averaged over three temporal bones. With
increased traction on the TT, the vibration responses in
the lower frequencies are attenuated; at higher frequencies the responses remain relatively stable.
Bance et al.: Markers of Tensor Tympani Muscle Contraction
TABLE I.
Change in Impedance in the Middle Ear Associated With a Puff of
Air Directed Toward the Closed Ipsilateral and Contralateral Eyes
in 20 Subjects With Normal Hearing.
Stimulus
Response
Type
No. of
Subjects
Average
Amplitude (mL)
Standard
Deviation (mL)
Positive
12 (60%)
0.073
0.044
Negative
5 (25%)
0.030
0.046
None
3 (15%)
—
—
Ipsilateral
Contralateral
Positive
13 (65%)
0.062
0.046
Negative
None
6 (30%)
1 (5%)
0.033
—
0.011
—
the stapes footplate in one temporal bone. Scanning
LDV measurements average across the entire measured
surface over many points, and so are less affected by
spatial vibration modal nulls and peaks at a single
point. A clear reduction of responses in the lower frequencies can be seen in both figures. In Figure 3B, there
appears to be an improvement in footplate vibrations in
the higher frequencies with increasing force on the TT.
Tympanometry. In both bones tested, both the
tympanogram (Fig. 4A) and reflex decay (Fig. 4B)
showed a drop in static peak compliance with TT contraction. The position of peak pressure of the
tympanogram showed no major shift in either bone.
Results were very similar to those seen in the live
human data (Figs. 5 and 6).
A positive amplitude indicates an increase in impedance (decrease in
compliance), similar to a normal stapedial reflex compliance change, and a
negative amplitude indicates a decrease in impedance (increase in
compliance).
Live Subject Measurements
Figure 3A shows the average response of all measurement points on the TM as measured with the
scanning LDV in two temporal bones; Figure 3B shows
the averaged response of all the measurement points on
Subject 1 could hold his contraction long enough to
perform a contracted MEM audiogram, one frequency at
a time. Results in Figure 5A show a conductive hearing
loss with an air-bone gap of 30 and 20 dB at frequencies
of 250 and 500 Hz, respectively, on TT contraction.
Fig. 2. Vibration amplitudes measured using single-point laser
Doppler vibrometer. (A) Tympanic membrane (umbo), and (B) center of stapes footplate at baseline (blue) and with tensor tympani
traction of 20 g (green) and 60 g (red). Shown are averages for
three temporal bones. Y-axis is log10 velocity/pressure, and on
this log scale the change in the stapes velocity is larger than that
of the umbo velocity.
Fig. 3. Scanning laser Doppler vibration velocity measurements
on the tympanic membrane (TM), averaged for two bones (A) and
on the footplate for one bone (B).
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Fig. 4. (A) Temporal bones 1 (left)
and 2 (right). Tympanogram before
and after force applied to the tensor
tympani (TT). Tympanograms before
and after TT force applied. Black is
baseline, and red is after TT force
applied. Temporal bone 1 is on the
left, and temporal bone 2 is on the
right. Compliance changes from 0.6
to 0.3 mL in bone 1, and from 1 to
0.6 mL in bone 2. (B) Reflex decay
measurements before and after
force applied to TT. Reflex decay
recordings after force applied to the
TT (arrows). Temporal bones 1 (left)
and 2 (right). [Color figure can be
viewed in the online issue, which is
available at wileyonlinelibrary.com.]
Interestingly, there was a small but repeatable drop in
the bone curve at 250 Hz as well.
The tympanogram (Fig. 5B for subject 1 and Fig.
6A for subject 2) and reflex decay (Fig. 5C for subject 1
and Fig. 6B for subject 2) showed a drop in compliance
with MEM contraction (increase in impedance). The
tympanometric peak pressure did not change with TT
contraction (i.e., there does not seem to be any associated change in middle ear pressure). This would also be
evidence against these changes being due to pumping of
the middle ear by the eustachian tube.
Computer Modeling
Computer simulations predicted results qualitatively similar to temporal bones and live subject results.
The simulated admittance (i.e., reciprocal of impedance)
results for the TM and stapes footplate during various
Fig. 5. Subject 1. Tests before and
after tensor tympani (TT) contraction.
(A) Effect on audiogram of TT contraction in subject 1. Each frequency
was separately tested before and after contraction. (B) Tympanogram
before and after voluntary middle
ear muscle (MEM) contraction. Compliance changes from 1 mL before
MEM contraction to 0.5 mL after
MEM contraction. (C) Reflex decay
during voluntary contractions of
MEM (arrows). [Color figure can be
viewed in the online issue, which is
available at wileyonlinelibrary.com.]
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1024
Bance et al.: Markers of Tensor Tympani Muscle Contraction
Fig. 6. Subject 2. (A) Tympanogram before and after voluntary
tensor tympani (TT) contraction. (B) Reflect decay during TT contractions. [Color figure can be viewed in the online issue, which is
available at wileyonlinelibrary.com.]
levels of TT contraction can be seen in Fig. 7A and 7B,
respectively. The amount of TT contraction is given as a
fraction of the maximum change of length of the TT. The
frequency at which the peak admittance occurs increases
with larger TT contractions. Somewhat surprising is the
drastic decrease in peak admittance magnitude experienced by the stapes footplate with TT contraction
compared to the slight increase in peak admittance magnitude of the TM.
do not have any change in eardrum stiffness and usually, in clinical practice, show no static compliance
changes from normal.
On the eliciting factors for TT contraction, overall,
95% of the subjects had an impedance change in
response to the orbital jets of air (65% an increase, 30%
a decrease). These results are similar to other published
studies with orbital air jets. Mulder et al.18 found 97% of
the control subjects had an impedance change in
response to the startle reaction, 57% had an increase in
impedance, 23% had a decrease in impedance (so-called
reversed response), and in 17% the response was not
clearly an increase or decrease in impedance. It is
unclear why this startle reaction causes an increase in
impedance in some subjects and a decrease in impedance
in others. Mulder et al.18 postulate that the decrease in
the impedance is caused by the TT, and the increase in
impedance is dominated by contraction the stapedius.
Our results in temporal bones do not support this theory
(Fig. 4), as TT contraction causes an increase in impedance. In the past, other authors have also postulated
that a reversed ipsilateral reflex (i.e., decrease in impedance) in response to acoustic stimulation is caused by
the TT (e.g., Ochi et al.19), but this is unlikely because
such a reversed reflex has been observed by us and
others,20 even in cadaveric temporal bones where no TT
muscle contraction is possible. Our results from Figure 3
would indicate that in contraction of the stapedius and
TT muscles, both increase the tympanometric impedance
of the middle ear. The two human subjects who could
DISCUSSION
Overall, the investigations in this work tend to reinforce and support each other in several aspects. First, all
seem to point to contraction of the TT causing attenuation
of low-frequency acoustic energy transmission through
the middle ear. This can be inferred from the decreased
low-frequency stapes and umbo vibrations in temporal
bone LDV, the computer model results, and finally the
audiogram in one subject who could voluntarily contract
his MEM for long enough to obtain this measure. Hence,
certainly we would expect a low-frequency conductive
component with TT contraction, but whether there is a
partial sensorineural component is not easy to infer from
our results. The small drop in the bone curve in subject 1
could also have been from masking from the tinnitus he
experienced with TT contraction.
Second, all the results seem to point to a decrease
in tympanometric static compliance with TT contraction
(measured with a standard 226 Hz probe tone). This distinguishes TT contraction from other entities such as
otosclerosis or ossicular fixation or erosion, which often
Laryngoscope 123: April 2013
Fig. 7. Model simulations of the effects on admittance of tensor
tympani (TT) contraction on admittance for (A) the tympanic membrane and (B) the stapes footplate. V ¼ velocity, F ¼ Force.
Bance et al.: Markers of Tensor Tympani Muscle Contraction
1025
move their TM would also point to TT contraction causing an increase in acoustic impedance (Figs. 5 and 6),
both in static compliance measurements with tympanometry and on dynamic changes using the reflex decay
settings.
In neither of these patients, nor in the temporal
bones, could we see a reliable change in the orientation
of the malleus handle, or shape of the eardrum with TT
contraction. Eardrum movements that could be seen
were quite subtle. The underlying shape of the eardrum
or malleus is not a clue to static contraction. In this, we
agree with Pau et al.,21 who conducted similar experiments to ours in five temporal bones. Pau et al. found a
decrease in compliance, similar to our findings, and an
increase in middle ear resonant frequency with force
applied to the TT.
The results of the temporal bone LDV experiments
shown in Figures 2 and 3 would suggest that there is
decreased transmission of low frequencies through the
middle ear when the TT is contracted. Figure 2 shows
single point recordings, and Figure 3 shows scanning
laser recordings averaged over many points. In terms of
amplitude, clearly, there is a graded reduction in low-frequency vibrations in both the umbo and the stapes
footplate when increasing force is applied to the TT.
Using single-point LDV, there appears to be little change
at higher frequencies. The scanning LDV results show a
similar low-frequency reduction in both the TM and stapes footplate. At the TM, the effects are a nicely graded
reduction in low-frequency transmission with little effect
on the higher frequencies. Also, there is little change in
the first broad resonance peak frequency. For the footplate, a scanning laser is possibly more accurate, as the
whole structure may rock, and single-point laser results
may be somewhat misleading, as it does not show the
net change in deflection of the structure, whereas the
scanning laser will average over all recorded points.
This may explain why the single-point measurements do
not show an increase in high-frequency transmission
with TT tension, whereas the scanning laser in Figure 5
clearly does for all weights except the 13-g weight. The
scanning laser also shows a clear increase in the first
broad resonance frequency of the stapes with TT
tension.
The computer model seems to qualitatively predict
some similar findings to our empirical data, but not in
all aspects. It does predict mostly a low-frequency drop
in admittance at the stapes. It also predicts that TT contraction would cause a much greater effect on the stapes
vibrations and resonant frequency than on the TM. Figure 3 shows that the stapes drop is bigger than the TM
drop, but not hugely so. In both the TM and the stapes,
there is a reduction in low-frequency vibrations,
although with the TM, the peak amplitude changes very
little with TT tension. The empirical data for the single
laser point umbo recordings could be interpreted as
showing this effect (Fig. 2A). The model also clearly
shows an increase in high-frequency transmission for
the stapes footplate, again similar to the effect seen in
Figure 3B. Overall, the model is qualitatively similar,
but not exactly the same, to what is seen empirically.
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Geometric and material property data differences
between the actual bones tested and the values used in
the simulation are most likely responsible for the lack of
quantitative agreement.
CONCLUSION
Of the stimuli tested, the most effective stimulus
for eliciting TT contraction is the startle reaction
induced from a jet of air on the closed eye. It is very difficult to detect changes in the TM position alone due to
TT contraction, so tonic contractions of the TT would be
difficult to detect by visual inspection alone. The main
effect of TT contraction seems to be an increase in middle ear stiffness, and this primarily affects the passage
of low-frequency acoustic energy to the inner ear, resulting in a predominately low-frequency conductive hearing
loss. Any change in inner ear hearing is slight, at least
acutely. Pure sensorineural hearing loss (SNHL) is difficult to explain from TT dysfunction alone. The expected
markers for TT contraction are: 1) a decrease in peak
static compliance measured with acoustic tympanometry; and 2) a low-frequency conductive hearing loss, with
a possible smaller low-frequency SNHL component.
These markers should be sought in disorders thought to
be associated with TT spasm (such as Meniere’s disease),
or in subjects with tinnitus, otalgia, low-frequency
SNHL, or other symptoms/signs where tonic TT spasm
is thought to be involved. Future work would look for
these markers in various otologic disorders, particularly
Meniere’s disease.
Acknowledgments
Jean MacLachlan was a summer medical student
who collected some of the data on the electing stimuli for
TT contraction.
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