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ISSN 1463-1741
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Noise & Health • Volume 15 • Issue 63 • March-April 2013 • Pages 81-152
A Bi-monthly Inter-disciplinary International Journal
www.noiseandhealth.org
March-April 2013 | Volume 15 | Issue 63
No cochlear dead regions detected in non‑pulsatile tinnitus
patients: An assessment with the threshold equalizing noise
(sound pressure level) test
Annick Gilles1,2,3, Dirk De Ridder4, Paul Van de Heyning1,2,3
Departments of Otorhinolaryngology and Head and Neck Surgery, Antwerp University Hospital, Edegem, 2Translational Neurosciences,
Faculty of Medicine, Campus Drie Eiken, Antwerp University, Wilrijk, 3Tinnitus Research Initiative Centre, BRAI2N, Antwerp University
Hospital, Edegem, Belgium, 4Surgical Sciences, Dunedin School of Medicine, University of Otago, New Zealand
1
Abstract
One of the hypotheses on the etiology of non‑pulsatile tinnitus in normal or hearing impaired patients is the existence
of sharp edged cochlear dead regions (DR) flanking normal functioning hair cells. The lack of inhibition of DR on
the neighboring neurons may lead to hyperactivity. Currently the Threshold Equalizing Noise test (TEN test) is the
reference test to clinically assess cochlear DR. To identify cochlear DR in patients with non‑pulsatile tinnitus with and
without hearing loss using the TEN (sound pressure level)‑test. Data were obtained from adult patients with non‑pulsatile
tinnitus visiting the Tinnitus Clinic of the University Hospital Antwerp. The TEN (SPL)‑test was performed to assess
the presence of cochlear DR for test frequencies ranging from 0.5 to 8 kHz. A total of 55 ears of 33 subjects (15 male;
18 female) with non‑pulsatile tinnitus were included in the study. Subjects were divided into subgroups based on the
audiometric configuration of hearing loss: Flat configuration (N = 23), high‑frequency gently sloping (N = 10) and
high‑frequency steeply sloping (N = 22). In forty‑eight ears there was no evidence of cochlear DR. In seven ears the
results were inconclusive. This occurred in patients with high‑frequency steeply sloping audiogram configurations.
The present study does not support the TEN (SPL) test as a reliable tool for the detection of cochlear DR in a tinnitus
population.
Keywords: Dead regions, inner hair cells, non‑pulsatile, threshold equalizing noise, tinnitus
Introduction
A dead region (DR) can be defined as a region in the cochlea
where the inner hair cells (IHCs) along the basilar membrane
and/or neurons are non‑functioning or missing, resulting in
the absence of basilar membrane vibration transduction to the
brain at those places.[1,2] This does not mean that a particular
tone is not audible. A tone producing peak vibration at a
particular place on the basilar membrane can be detected by
off‑place or off‑frequency listening provided that the stimulus
is sufficiently loud. The tone will not be detected at its usual
place on the basilar membrane but at an adjacent place where
the IHCs are functioning more effectively.[2,3] The extent of a
DR can be defined in 2 manners: Either by distance along the
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basilar membrane, described by the characteristic frequencies
related to this place (e.g., a DR extending from 4000 to 10
000 Hz), or by the characteristic frequency (CF) of IHCs or
neurons adjacent to the DR.[2] The presence of a DR can result
in several problems such as abnormal pitch perception,[4] rapid
loudness growth,[5] and distorted perception of pure tones.[6]
In order to diagnose cochlear DRs, the Threshold Equalizing
Noise (TEN) test was developed.[7] In this test a broadband
masking noise (the TEN) is used which is spectrally shaped
so that all auditory output filters contain an equal noise power.
This means that, for subjects with normal hearing thresholds,
the masked threshold for a pure tone is the same for all
frequencies over the range of 250‑10 000 Hz. More specifically,
the TEN level is specified as the level in a one‑Equivalent
Rectangular BandwidthN (ERBN) (132 Hz) wide band
centered at 1000 Hz, where ERBN stands for the average of
the auditory filter as determined for young normal‑hearing
subjects at moderate sound levels.[2] For example, if the TEN
noise is presented at a dial level of 70 (corresponding to 70
dB/ERB), then thresholds, for normal hearing subjects, across
a wide frequency range, measured in this noise should also be
70 dB SPL. Figure 1[2] illustrates the principle of the TEN test.
Looking at the top panel, the solid curve represents the basilar
Noise & Health, March-April 2013, Volume 15:63, 129-33
Gilles, et al.: Assessing dead regions in tinnitus patients
a
b
Figure 1: Illustration of the principle of the Threshold Equalizing Noise test (TEN [SPL]) test. The basilar membrane vibration of a 1.5
kHz tone is represented by the solid curve. (a) The shaded area reflects a dead zone starting at 1.07 kHz. 40 dB of basilar membrane
vibration is needed (long‑dashed line) in order to measure absolute thresholds below 1.07 kHz. The short‑dashed line represents the
absolute threshold value of a 1.5 kHz tone, which is 67 dB. A threshold is measurable due to intact IHC’s adjacent to the dead region.
(b) A TEN of 70 dB/ERBN is added to mask the 1.5 kHz tone at 67 dB. In case of a dead region, the intensity of the tone needs to be
raised substantially in order to achieve audibility again. This figure was derived from Moore et al. 2004[7]
membrane vibration pattern for a pure tone with a CF of.[1] 5
kHz, expressed by the maximum vibration at that frequency.
The shaded area reflects the presence of a high‑frequency
DR starting at approximately 1.07 kHz. To measure absolute
thresholds for frequencies below 1.07 kHz, 40 dB of basilar
membrane vibration is needed (long‑dashed line). As indicated
by the short‑dashed line, the absolute threshold value of a 1.5
kHz tone (which falls within the DR) is 67 dB. A threshold
is measurable because of the intact IHC’s adjacent to the DR
(= off‑frequency listening). In the bottom panel a TEN of 70
dB/ERBN is added masking the 1.5 kHz tone at 67 dB. To
make the tone audible again the level has to be increased so
that basilar vibration just below the 1.07 kHz DR slightly
exceeds 70 dB. A level of 97 dB is required in order to achieve
audibility of the tone again. A normal hearing subject with no
DR would have a masked threshold of approximately 70 dB.
This figure shows that for the person with a DR, the masked
threshold was 30 dB higher than the unmasked threshold
(97 dB vs. 67 dB) and that the masked threshold was 27 dB
higher than in the case where there was no DR (97 dB vs.
70 dB). This last remark demonstrates the two criteria that
need to be fulfilled to determine a DR: (1) at least 10 dB of
masking is required and (2) the masked threshold should be
at least 10 dB higher than normal.[2] There are currently two
commercially available TEN test versions: the TEN sound
pressure level test (TEN-SPL) and the TEN hearing loss level
test (TEN-HL).[2] They differ in 3 ways: Frequency range
tested, amplitude characteristics of the TEN noise and the
calibration. The TEN (SPL) test is calibrated in dB SPL and
covers a frequency range of 250‑10 000 Hz. The TEN (HL)
test is the modified version of the TEN (SPL), calibrated in
dB HL which is easier to interpret as the audiometer is also
calibrated in dB HL. The frequency range of the TEN (HL) is
narrowed to 250‑4000 Hz and the TEN noise contains a lower
Noise & Health, March-April 2013, Volume 15
crest factor. The present study aims to investigate whether
cochlear DRs are more prevalent in patients suffering from
tinnitus. Tinnitus, the perception of sound in the absence of an
external acoustic sound source, poses a clinical problem for
millions of people around the world.[8] The understanding of
the pathological mechanism of tinnitus generation remains in
the stage of hypothesis and conjecture. One of the hypotheses
on the etiology of non‑pulsatile tinnitus is the existence
of sharp edged cochlear DRs flanking normal functioning
hair cells. The lack of inhibition of DRs on the neighboring
neurons may lead to hyperactivity. Previous studies showed
that tinnitus in the absence of measurable hearing loss at
all frequencies or at the tinnitus frequency does not exclude
cochlear/neural damage.[9] Previously the detection of DRs
was reported in eight out of eleven subjects with normal
hearing and non‑pulsatile tinnitus,[10] providing evidence for
the theory that deafferentiation is also possible in tinnitus
subjects with audiometrically normal hearing thresholds.
In the present study we used the TEN (SPL) test in order to
assess cochlear DRs in an adult population with non‑pulsatile
tinnitus and various audiometric configurations.
Methods
Subjects
Thirty‑three patients presenting with non‑pulsatile tinnitus
in the University Hospital Antwerp (UZA) underwent the
standard otorhinolaryngologic (ORL) and audiometric
protocol for tinnitus. In addition, the TEN (SPL) test was
performed in tinnitus ears only. The group consisted of fifteen
male and eighteen female patients with a mean age of 51.7 ±
16.2‑years‑old (range 20‑73). Twenty‑two patients suffered
from bilateral tinnitus while eleven patients perceived a
unilateral tinnitus in either the right or left ear.
130
Gilles, et al.: Assessing dead regions in tinnitus patients
Pure‑tone audiometry
All patients received visual inspection of the eardrum by
an ORL‑specialist. In addition, tympanometry was normal
in all subjects so middle ear pathologies were excluded.
According to current clinical standards (ISO 8253‑1, 1989),
air conduction threshold were measured at 125, 250, 500,
1000, 2000, 3000, 4000, 6000 and 8000 Hz using a 2‑channel
Interacoustics AC‑40 audiometer in a soundproof booth.
Bone conduction thresholds were measured at 250, 500,
1000, 2000, 3000 and 4000 Hz. All the patients included in
this study had a normal hearing or a sensorineural hearing
loss (SNHL) as the air‑bone gap never exceeded 10 dB HL.
For all the analyses only those ears in which tinnitus was
perceived were included in this study. Tinnitus ears were
divided into 3 categories in accordance with Demeester et
al., (2009): A flat configuration, a high‑frequent gently
sloping (HFGS) configuration and a high‑frequent steeply
sloping (HFSS) configuration. To be categorized as a flat
configuration, the difference between the mean thresholds of
250/500 Hz, the mean of 1 kHz/2 kHz thresholds, and the
mean of 4 kHz/8 kHz should be less than or equal to 15 dB.
A HFGS configuration is defined as an audiogram where the
difference between the mean of 500 Hz/1 kHz thresholds and
the mean of 4 kHz/8 kHz thresholds is greater than 15 dB
but less than 29 dB. Finally, a HFSS configuration is present
when the difference between the mean of 500 Hz/1 kHz
thresholds and the mean of 4 kHz/8 kHz is 30 dB or more.[11]
Of all tinnitus ears, 24 were categorized with a flat, 10 with a
HFGS, and 21 with a HFSS configuration.
Tinnitus analysis
A Dutch validated version of the Tinnitus Questionnaire
(TQ),[12] was completed by the majority of patients (four
patients did not complete the questionnaire). The TQ was
originally published by Goebel and Hiller.[13] who described
the TQ as a global index of tinnitus‑related distress. Based on
the total score on the TQ, patients are assigned to a distress
category: Slight (0‑30 points: Grade 1), moderate (31‑46
points: Grade 2), severe (47‑59 points, grade 3) and very
severe (60‑84 points, grade 4).
played continuously and both volume unit (VU) meters were
adjusted to read 0 dB. Absolute thresholds were measured
using a final 2 dB‑step size to determine the threshold.
Subsequently, the TEN was presented with a level of 70 dB
and the masked thresholds were measured in a similar way.
In case the absolute thresholds of a patient were 60 dB SPL or
worse, the level of the TEN was raised. Therefore, the TEN
provided at least 10 dB of masking at all times. A DR was
considered present if the following criteria were both met.[7]
• The masked threshold is at least 10 dB worse than the
absolute threshold
• The masked threshold is at least 10 dB worse than the
masking noise (TEN)
The results were categorized as positive (DRs present),
negative (no DRs present) or inconclusive. Several
situations can cause inconclusive results. Firstly, it may be
impossible to produce 10 dB of masking in patients with
severe or profound SNHL because the maximum output of
the audiometer is reached. Therefore, the intensity of the
TEN will not cause sufficient masking. Secondly, when the
TEN level was considered as too loud by the patient, the
level was lowered and did not provide sufficient masking,
leading to inconclusive results. Finally, absolute and/or
masked thresholds could not be measured in some patients
with profound hearing loss at certain frequencies because of
output limitations of the audiometer.
Results
The audiometric results are represented graphically in Figure 2
where mean absolute hearing thresholds of patients with a flat
(N = 24), a HFGS (N = 10) and HGSS (N = 21) are shown. A
full tinnitus analysis was performed on 31 ears of 21 patients
(10 with bilaterally tinnitus, 11 with unilateral tinnitus).
Table 1 shows the results of the tinnitus analysis after pitch
matching as well as the tinnitus type (pure tone or noise‑like).
In addition, Table 2 shows the scores for VAS and TQ. The
Secondly, patients had to score their tinnitus loudness on
a Visual Analogue Scale (VAS) going from 0 (no tinnitus)
to 10 (tinnitus extremely loud). Finally, tinnitus pitch and
intensity were determined through tinnitus analysis using
pitch matching and loudness matching procedures.
Threshold equalizing noise (SPL) procedure
The TEN (SPL) test was performed in all fifty‑five tinnitus
ears using an original TEN (SPL) CD played by a CD player
(Sony CDP‑XE270) and presented through a TDH‑39
supra‑aural earphone. First, the audiometer was connected to
the CD player output plug. Input channel 1 on the audiometer
was selected on the left side, and channel 2 was selected on
the right side. The first track on the CD, a calibrating tone, was
131
Figure 2: Graphical illustration of the mean audiometric results
of the three subgroups (flat, high‑frequent gently sloping and
high‑frequent steeply sloping audiometric configurations) of the
tinnitus patients
Noise & Health, March-April 2013, Volume 15
Gilles, et al.: Assessing dead regions in tinnitus patients
majority of patients experienced a high‑pitched tinnitus and
mostly a noise‑like character. The tinnitus loudness was scored
on a VAS by nineteen of the thirty‑three patients (of which in
11 patients with bilateral tinnitus, the VAS was also scored
bilaterally). Tinnitus intensity was measured in 26 patients
and 29 patients completed the TQ of which eight patients were
categorized with a degree 1, 10 with a 2nd degree, 9 with a
3rd and 2 with a 4th degree. Because of time shortcomings in
the daily clinical practice, all (TQ, VAS and tinnitus analysis)
were not always done completely. Therefore, Tables 1 and
2 do not contain data of all ears of all patients on which the
TEN (SPL) was applied. In patients suffering from bilateral
tinnitus, the TEN (SPL) test was performed in both ears. In
patients with unilateral tinnitus, TEN (SPL) was performed
in the affected ear only. Figure 3 shows the mean masked
threshold per frequency in 70 dB SPL of TEN (or more in
subjects where the unmasked threshold exceeded 60 dB SPL).
The mean masked thresholds were 10 dB SPL or more better
than the ‘normal’ masked threshold (which would be 70 dB
SPL in 70 dB TEN) for all frequencies meaning that the tone
was audible even at a level much lower than the TEN level. As
one of the criteria for a DR states that the masked threshold
should be at least 10 dB worse than the unmasked threshold,
no DRs were found in these patients. Therefore, the outcome
of most TEN (SPL) tests were negative. Nevertheless, four
patients showed inconclusive results at certain frequencies. In
one patient with a symmetric HFSS audiogram configuration
and bilateral non‑pulsatile tinnitus, the unmasked threshold
could not be measured bilaterally upwards from 2 kHz
because of audiometer output limitation as the unmasked
threshold exceeded 120 dB HL. In three other patients with
a HFSS configuration (two patients with bilateral tinnitus and
one with unilateral tinnitus), the unmasked threshold were
measured but the TEN noise could not be set loud enough
to provide sufficient masking. Therefore the results in these
patients remained inconclusive for a DR located in the high
frequencies. An oversight of inconclusive results along with
the reason of inconclusiveness is given in Table 3.
Discussion
It has been suggested that tinnitus is often accompanied by
severe (IHCs damage in certain cochlear regions, even in the
absence of measurable hearing loss.[9,10] Severe IHC damage
causes deafferentiation and therefore DRs in the cochlea. In
the present study tinnitus patients with different audiometric
configurations and hearing thresholds (going from normal
hearing to profound hearing loss) were tested for DRs by use of
the TEN (SPL) test. In the study of Weisz et al., (2006) a normal
hearing student population suffering from tinnitus was tested of
which eight out of eleven subjects were identified with a DR.[10]
In another study, in which the TEN (HL) test was applied, 15%
of tinnitus patients with normal hearing sensitivity had positive
TEN results, indicative for a DR.[14] In our normal hearing
subjects with tinnitus (N = 16 ears), no DRs were identified. It
has been reported earlier that it is more likely that IHC damage/
loss is involved in subjects where the hearing loss exceeds 55
to 60 dB.[15] Furthermore, it has been found that a DR is more
prevalent in subjects with a hearing loss exceeding 55 to 60 dB
SPL.[3,14] In addition, severe high‑frequency hearing loss or high
frequency steeply sloping audiograms are more associated with
DRs and positive TEN findings. Several studies found a greater
prevalence of DRs in subjects with a steep slope.[3,16] The present
study was not able to confirm these findings as also those ears
with a HFSS audiogram configuration (N = 22) showed negative
TEN results. However, as mentioned earlier and elucidated in
Table 3, in four patients with a HFSS configuration, unmasked
or masked thresholds could not be obtained in seven tinnitus
ears because of audiometer output limitations. Here the TEN
Table 1: tinnitus characteristics of 31 measured tinnitus ears:
pitch and tinnitus type
0.125 0.75
Ears
1
2
1
1
Pitch (kHz)
1.5
2
4
2
1
9
6
5
8
9
9
1
Tinnitus Type
PT
N
11
20
PT= pure tone; N= noise
Table 2: Mean scores for the VAS, tinnitus intensity (in dB SL)
and TQ, including standard deviations for N (=amount) out of
the 33 patients
VAS
Mean
5.74
SD
2.25
N=19
dB SL
Mean
SD
7.73
8.53
N= 26
TQ
Mean
SD
37.55
16.47
N= 29
Table 3: Oversight of inconclusive results at a particular
frequency with reasoning for the categorizing as ‘inconclusive'
Figure 3: Mean difference between the masked thresholds and
the Threshold Equalizing Noise test noise given for all TEN (SPL)
test frequencies of all ears with measurable thresholds (48 ears
of 29 patients)
Noise & Health, March-April 2013, Volume 15
Patient
#8
#8
#24
#24
#25
#26
#26
Ear
Right
Left
Right
Left
Left
Right
Left
Frequency
8 kHz
8 kHz
4 kHz to 8 kHz
2 kHz to 8 kHz
6 kHz to 8 kHz
4kHz to 8 kHz
8 kHz
Reason
Unmasked threshold not measurable
Unmasked threshold not measurable
Insufficient TEN noise
Insufficient TEN noise
Insufficient TEN noise
Insufficient TEN noise
Insufficient TEN noise
132
Gilles, et al.: Assessing dead regions in tinnitus patients
findings remained inconclusive. The problem of the amount of
inconclusive results of the TEN (SPL) test has been previously
reported by Hornsby and Dundas (2009) where in 80% of the
ears inconclusive results were found for at least one frequency
and 30% at three frequencies or more.[3] Vinay and Moore
(2007) also noted that it is more likely to have inconclusive
results when the audiometric thresholds exceed 85 dB HL.[14]
The TEN (HL) test can be presented at higher levels without
distortion and might therefore reduce the amount of inconclusive
results.[2] Nevertheless, in the present study, the TEN (SPL) was
deliberately chosen over the TEN (HL) because of the wider
frequency range. Furthermore, as tinnitus analysis showed
that most patients included in this study, perceived a high
pitched tinnitus, we were especially interested in the cochlear
preservation at those frequencies. Thirty‑two ears of the patients
included in the present study, were characterized as a HFGS (N
= 10) or a HFSS (N = 22) configuration. As mentioned before,
patients with high‑frequency steeply sloping audiometric
configurations are more likely to have a DR in that area. Such
results were not found by the current study. As the present
study aimed to assess the TEN (SPL) as a clinical tool for the
explanation of tinnitus, the question arises whether cochlear
DRs are necessary for a tinnitus percept. It has been shown
that immediately after acute (impulse) noise trauma in military
personnel, 88% of the soldiers perceived a noise‑induced
tinnitus.[16] The presence of cochlear DRs was determined by the
use of psychophysical tuning curves (PTCs), which is considered
as a more reliable tool by some authors.[17] It has been shown
that immediately after acute impulse noise trauma in military
personnel 70% of the soldiers had DRs, 50% of which recovered
partially or completely (narrowing or disappearing of the DR
zone) after some time. The high prevalence of DRs after noise
trauma may be involved in noise‑induced tinnitus. However,
the fact that some patients with tinnitus had no DRs and some
patients with DRs had no tinnitus supports the hypothesis that
the presence of a DR is neither necessary nor sufficient to induce
tinnitus.[16] These findings fit the suggestion that OHCs might be
of more importance than IHCs in the generation of tinnitus as in
a previous study in a group of normal hearing tinnitus patients
85% demonstrated abnormal transient otoacoustic emissions, of
which only 15% abnormal TEN (HL) findings.[18] In conclusion,
tinnitus is a common phenomenon in modern society. While the
etiology of tinnitus remains elusive in many cases, research is
needed in order to identify a possible causative factor. One of the
hypotheses on non‑pulsatile tinnitus is the presence of cochlear
DR leading to central hyperactivity. If DR can be identified
by use of the TEN test, the present study does not support the
concept that DR are necessary for tinnitus. Therefore, the use of
the TEN test as a diagnostic tool in a tinnitus population might
be of limited value. The authors would like to point out that the
present study does not designate the TEN test to be unreliable
as a whole but as a result of the present findings the TEN test
does not provide a useful tool in the diagnostics of tinnitus
patients. Further research with the TEN test in tinnitus patients
is necessary in order to confirm these findings.
133
Acknowledgments
This research was supported by the Stavros Niarchos Foundation
and a TOP‑BOF project of the University Antwerp.
Address for correspondence:
Mrs. Annick Gilles,
University Hospital Antwerp, Wilrijkstraat 10, 2650
Edegem, Belgium.
E‑mail: annick.gilles@UZA.be
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How to cite this article: Gilles A, De Ridder D, Van de Heyning P. No
cochlear dead regions detected in non-pulsatile tinnitus patients: An
assessment with the threshold equalizing noise (sound pressure level)
test. Noise Health 2013;15:129-33.
Source of Support: Nil, Conflict of Interest: None declared.
Noise & Health, March-April 2013, Volume 15