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J Am Acad Audiol 3: 324-330 (1992)
Effects of Cochlear Hearing Loss on the ABR
Latencies to Clicks and 1000 Hz Tone Pips
Cynthia G. Fowler* t
Charlene M. Mikami*
Abstract
High-frequency hearing losses can substantially confound the interpretation of clickevoked auditory brainstem responses (ABRs) . One method proposed to circumvent
the problem is to use frequency-specific tone pips to stimulate equivalent areas on
the basilar membrane in normal and pathologic groups, or in both ears of asymmetrically impaired patients . This retrospective study investigated the ABRs to clicks and
1000-Hz tone pips from 90 asymmetrically impaired subjects with cochlear pathology.
The 4000 Hz threshold significantly affected the wave V latencies from both clicks and
tone pips for the most severely impaired subjects . The wave V latencies were
highly correlated between ears for both stimuli, but the correlation was higher with the
1000-Hz tone pips . It was concluded that the use of 1000-Hz tone pips can supplement
the interpretation of click-evoked ABRs, particularly in patients whose 2000- and/or
4000-Hz thresholds are worse than 75 dB HL .
Key Words: Auditory brainstem response (ABR), cochlear hearing loss, wave V
latency, asymmetrical hearing
ne difficulty in obtaining auditory brainstem responses (ABRs) from patients
0 with high-frequency hearing losses is
that the hearing loss shapes the effective spectrum of the click. The result is that different
areas on the basilar membrane are stimulated
depending on the configuration and degree of
the hearing loss (Aran et al, 1975 ; Elberling and
Salomon, 1976 ; Coats and Martin, 1977) . The
different areas of the basilar membrane, in
turn, produce different latencies, which leads to
a diagnostic dilemma when determining whether
a delayed latency is due to a cochlear or retrocochlear pathology, especially in cases in which
wave I is absent. Difficulties are encountered in
comparing ABR latencies of hearing-impaired
patients to norms collected on normal-hearing
subjects, as well as in comparing interaural
latencies of patients with unilateral or asymmetrical hearing losses .
Various methods have been suggested to
compensate for the delay caused by cochlear
*VA Medical Center, Long Beach, California
t University of California, Irvine, California
Reprint requests : Cynthia G . Fowler, Audiology-126,
VA Medical Center, 5901 East Seventh Street, Long Beach,
CA 90822
324
pathology, although none has achieved widespread use because of relatively poor predictive
results for individual cases (Fowler and Durrant,
in press) . These methods include adding a correction factor to the click-evoked latencies (Selters and Brackmann,1977 ; Jerger and Mauldin,
1978 ; Hyde and Blair, 1981) and using
electrocochleographic methods to elicit wave 1
(Durrant, 1986 ; Ferraro and Ferguson, 1989).
An alternative method suggested for circumventing the problems ofclick stimuli in hearingimpaired subjects is to use tone pips in an
attempt to stimulate equivalent areas of the
basilar membrane in normal and pathologic
ears (Fowler and Noflsinger, 1983 ; Telian and
Mleny, 1989).
The following is a retrospective study of
patients seen for routine ABRs in the Audiology
Section at the VA Medical Center, Long Beach,
California in 1983 and 1984 . The purpose of the
investigation was to evaluate the clinical utility
of 1000-Hz tone pips and clicks for eliciting the
ABR in patients with asymmetrical hearing
loss presumably of cochlear origin .
METHOD
S
ubjects were 90 patients referred for ABR
testing because of asymmetrical hearing
Cochlear Hearing Loss and ABR/Fowler and Mikami
loss or tinnitus . The subjects were male and
ranged in age from 21 to 82 years, with a mean
age of 56 years. The results of audiologic evaluations, consisting of air- and bone-conduction
thresholds at octave intervals from 250 to 8000
Hz, word recognition at PBm. and 90 dB HL,
tympanometry, and acoustic reflex thresholds
and adaptation, were consistent with cochlear
pathology. Subjects with confirmed retrocochlear pathology were not included in the
subject sample .
Stimuli were rarefaction clicks and 1000Hz tone pips . Clicks were produced from 100psec rectangular pulses through matched TDH39 earphones in MX-41/AR cushions . The clicks
were delivered to 30 subjects each at 75, 85, or
95 dB nSL (normalized sensation level*), which
were equivalent to 105, 115, and 125 dB peSPL
(peak equivalent sound pressure level) . The
clicks were presented at equal levels for both
ears at an overall level 2!15 dB above the audiometric threshold at 4000 Hz in the worse ear or
at 95 dB nSL if the 4000-Hz threshold was
>_80 dB HL . The choice of click level, therefore, ensured that the high-frequency audiometric thresholds would be higher for subjects
receiving the higher level stimuli. The three
subject groups are referred to by click level (i .e .,
the 75 group, 85 group, and 95 group) . Tone pips
at 1000 Hz (1-msec linear rise-fall times, 0msec plateau, fixed onset phase) were delivered
at 75 dB nSL (100 dB peSPL) to all subjects .
This level was ?15 dB above the 1000-Hz threshold in the poorer ear. The acoustic spectra for
the clicks and 1000-Hz tone pips are given in
Figure 1.
The ABR was recorded with gold cup electrodes attached to the skin at the vertex (noninverting input), ipsilateral earlobe (inverting
input), and at the forehead (ground) . Interelectrode impedance was !_5000 Q and equal
(±1000 S2). Physiologic activity was filtered
(Nicolet, Model 501-A) between 150 and 3000
Hz (3-dB down points, 12-dB/octave rejection
rates) . Responses were averaged (Nicolet, Model
812) over 3000 trials in a time window of 10 .48
msec . All responses were replicated to ensure
reliability . Latencies were measured from stimulus onset to the positive peak of the wave .
Averaged latencies from the two replications
were used in the data analysis .
*Sensation level, as defined by Sonn (1969), is "the pressure
level of the sound in decibels above its threshold of audibility
forthe individual subject or for a specified group of subjects ."
The prefix "n" denotes that a group of normal hearing
subjects is used as the referent .
0
-20
-40
m .60
v
w
0 -ao
F0
~
I
J
a
a -20
-40
-60
-a0
1
i
0
2500
5000
7500
10000
FREQUENCY (Hz)
Figure 1 The average acoustic spectra (N = 32) for the
clicks (upper panel) and 1000 Hz tone pips (lower panel) .
Spectra were obtained through TDH-39 earphones with
a spectrum analyzer (Brdel & Kjar, Type 2033).
RESULTS
he mean audiometric thresholds for ocT tave intervals from 500 to 4000 Hz for the
30 subjects in each group are shown in Figure 2.
Each group was characterized by a sloping highfrequency hearing loss, and as expected, this
slope was greater for the subject groups requirPOORER EAR
BETTER EAR
~I
I
75 GROUP
75 GROUP
85 GROUP
85 GROUP
95 GROUP
~
500 1000 2000 4000
95 GROUP
500
1000 2000 4000
FREQUENCY(Hz)
Figure 2 The means (squares) and ranges (bars) for the
auditory thresholds for the three groups ofsubjects . Open
symbols are thresholds from the better ear and filled
symbols are thresholds from the poorer ear.
325
Journal of the American Academy of Audiology/Volume 3, Number 5, September 1992
Table 1
Clicks
1000-Hz
Tone Pips
Latencies of Waves I and V and the
I-V Latency Differences
Group
Wave 1
Wave V
75
85
95
All
1 .87 (0 .17)
1 .81 (0 .21)
2 .15 (0 .53)
1 .92 (0 .35)
6 .00 (0 .32)
5 .98 (0 .22)
6 .12 (0 .36)
6 .03 (0 .33)
4 .10 (0 .29)
4 .17 (0 .26)
3 .89 (0 .43)
4 .06 (0 .35)
75
85
95
All
2 .87 (0 24)
3 .03 (0 .32)
3 .12 (0 .37)
3 .00 (0 .33)
6 .82
6 .99
7 .15
6 .99
3 .95 (0 .28)
3 .95 (0 .29)
4 .00 (0 .27)
3 .97 (0 .28)
(0 .31)
(0 .29)
(0 .36)
(0 .35)
1-V
Means and standard deviations (in parentheses) in
milliseconds .
ing higher stimulus levels . The group means do
not demonstrate the asymmetries because different audiometric frequencies were asymmetrical in each subject.
Wave V was present in all conditions for all
90 subjects, whereas wave I was absent in 25
subjects with the click stimuli and 31 subjects
with the 1000-Hz tone pips . The difference in
numbers of wave I present for the two stimulus
types, evaluated with a chi-square analysis
(Guilford, 1965), was not significant . The 4000Hz thresholds of the subjects missing wave I for
either stimulus ranged from 10 to 105 dB HL .
Only eight subjects, all in the 95 group, were
missing wave I for both stimulus conditions .
The mean 4000-Hz threshold for these eight
subjects was 86 dB HL, with a range of 65 to
105 dB HL.
The means and standard deviations for
wave I and V latencies and the I to V latency
differences for each subject group and for the
total group for both clicks and 1000-Hz tone
pips are given in Table 1 . Two-way analyses of
variance (ANOVAs) (Northwest Analytical,
1986) with one repeated measure (subject group
by stimulus type) indicated the same significant variables for both waves I and V. Significant group differences for the wave latencies
(Table 2) precluded pooling of data for the three
subject groups for most of the statistical analyses. As expected, the latencies elicited by clicks
and 1000-Hz tone pips were significantly different. The interaction between the latencies for
subject group and stimulus type was also statistically significant . For wave V, for example, the
latency difference between the 75 and 95 groups
was 0.12 msec for clicks and 0.33 msec for the
1000-Hz tone pips . The increase in latencies for
the 1000-Hz tone pips across subject groups,
which was not complicated by different stimu326
lus levels (as were the click latencies), demonstrates that an increasing latency delay was
imposed by an increasing hearing loss .
A linear regression analysis (Northwest
Analytical, 1986) indicated that the latency of
wave V varied significantly with the latency of
wave I. For all subjects having both waves I and
V, the wave I latency contributed less variability to the wave V latency for the clicks (r 2 = 0.20;
F [ 1, 158] = 38 .54; p < .01), than for the 1000-Hz
tone pips (r2 = 0.41 ; F [1, 147] =100 .52; p < .01) .
Bivariate plots of the relations between wave I
and V latencies for each subject group and both
stimuli are shown in Figure 3. The highest
correlations were in the 95 group, for which the
hearing loss was the greatest.
The wave V latencies from both the clicks
and 1000-Hz tone pips were subjected to a
linear regression analysis with respect to
behavioral thresholds between 500 and 4000 Hz
for all three subject groups . The linear regression lines deviated significantly from 0 (Table 3 )
only in the 95 group and only for the 4000 Hz
thresholds . These relations are shown in Figure
4, in which the wave V latencies increased with
increases in the auditory threshold at 4000 Hz
for waves V elicited by both clicks and 1000-Hz
tone pips . The 4000-Hz thresholds contributed
41 percent of the variability in the click-evoked
wave V latencies, but only 17 percent of the
variability in the 1000-Hz tone pip-evoked
latencies, indicating the greater effect of the
high-frequency hearing loss on the click-evoked
latencies.
Similarly, only in the 95 group, as the
interaural threshold differences increased for
both 2000 Hz and 4000 Hz, significant increases
occurred in the interaural wave V latency differences from both clicks and 1000-Hz tone pips
(see Table 3) . This relation is depicted in Figure
5, in which the interaural wave V latency differences are shown increasing with interaural
Table 2 Results of the ANOVAs for the
Latencies of Waves 1 and V for
Subject Group versus Stimulus
Wave I
Subject group
F Ratio
df
p
Stimulus
Interaction
1202 .92
7.04
20 .68
2,177
< ' 01
Wave V
Subject group
Stimulus
Interaction
8 .79
3726 .35
18 .40
2,177
1,177
2,177
< .01
< .01
< .01
1,137
1,137
< .01
< .01
Cochlear Hearing Loss and ABR/Fowler and Mikami
TONE PIPS
CLICKS
B
R 2=0 .14
R 2=0 .28
s
7
J}
C
75 GROUP
75 GROUP
R~=0 .27
Rx=0 .08
1
4000 Hz THRESHOLD (dB HL)
. .r
"
85 GROUP
85 GROUP
R~=0 .50
R x=0 .14
Figure 4 Bivariate plots of the wave V latency and
4000-Hz thresholds from the 95 group. The left panel
includes latencies from wave V elicited by clicks and the
right panel includes latencies from wave V elicited by
1000-Hz tone pips . The lines through the data are the best
fit regression lines.
51
"
2
95 GROUP
95 GROUP
3
4
1
2
3
4
WAVE ILATENCY (ms)
Figure 3 Bivariate plots of the wave I and wave V
latencies for the 75 group (upperpanels), 85 group (middle
panels), and 95 group (lower panels) for the click (left
panels) and 1000 Hz tone pip (right panels) stimuli . Lines
through the data are the best fit regression lines.
threshold differences for both 2000 Hz and 4000
Hz . The 2000-Hz and 4000-Hz threshold differences accounted for 23 percent and 52 percent,
respectively, of the variability in interaural
latency differences for click responses . In contrast, the 2000- and 4000-Hz threshold differences each accounted for 27 percent of the
variability in interaural latency differences for
1000-Hz tone pips . Thus, the wave V latencies
from clicks were more dependent on both absolute thresholds and interaural threshold differences than were the wave V latencies from
1000-Hz tone pips, and these dependencies were
only significant for the severe high-frequency
hearing losses . Of all the frequencies tested,
4000 Hz exerted the greatest effect on the wave
V latencies.
The wave V latencies between the left and
right ears were subjected to a linear regression
analysis . For the three subject groups combined, the left and right ears were significantly
correlated both for clicks (r2 = 0.67; F [1, 881 =
177.41 ; p < .O1) and for the 1000-Hz tone pips (r'
= 0.79; F [1, 881 = 343.93; p < .01) . The lesser
interaural correlation for click latencies than
for 1000-Hz tone pip latencies is undoubtably a
result of the greater dependence of the click
latency on the 4000-Hz auditory threshold, at
which most of these subjects had asymmetrical
hearinglosses . The interaural latency relations
for wave V for both clicks and 1000-Hz tone pips
are shown in Figure 6.
DISCUSSION
T
he use of tonal stimuli has been proposed
as a method for circumventing the latency
Table 3 Linear Regression Analyses for the 95 Group
Audiometric Thresholds and Wave V Latencies
r
r2
F
of
Absolute
Click V vs 2000 Hz
Click V vs 4000 Hz
1000 Hz V vs 2000 Hz
1000 Hz V vs 4000 Hz
0 .32
0 .64
0 .24
0 .41
0 .10
0 .41
0 .06
0 .17
6 .53
40 .05
1,58
1,58
p> .01
p < .01
12 .16
1,58
p< .01*
Relative
Click V vs 2000 Hz
Click V vs 4000 Hz
1000 Hz V vs 2000 Hz
1000 Hz V vs 4000 Hz
0 .48
0 .72
0 .52
0 .52
0 .23
0 .52
0 .27
0 .27
Comparison
3.52
1,58
p
p> .01
8.57
1,28
p< .01*
10 .34
1,28
p< .01*
30 .92
10 .44
1,28
1,28
p < .01 *
p< .01*
`Significant at p < .01
Absolute refers to the absolute wave V latencies compared to 2000- and 4000-Hz audiometric thresholds, and Relative
refers to the interaural wave V latency differences compared to the 2000- and 4000-Hz threshold differences .
327
Journal of the American Academy of AudiologyNolume 3, Number 5, September
1992
0.6
0.4
0.2
0.0
-0 .2
-0 .4
-0 .6
-0 .8
0.4
0.2
0.0
-0 .2
-0 .4
-0 .6
-0 .8
-60
2000 Hz
4000 Hz
R2-0 .23
R2=0.52
R2 -0.27
-40
'
.20
0
R2
20
40
-60
.0.27
-40
'
.20
0
20
I
40
60
THRESHOLD DIFFERENCE (dB)
Figure 5 Bivariate plots of the interaural wave V latency difference and interaural threshold differences for
the 95 group. The latencies from clicks (upper panels) and
1000-Hz tone pips (lower panels) are shown with the
interaural threshold differences from 2000 Hz (leftpanels
and 4000 Hz (right panels). Best fit regression lines are
shown.
delays imposed by high-frequency hearing losses
on click-evoked ABRs . The present study indicates that this method has some advantages,
but does not completely alleviate the problem .
The use of the 1000-Hz stimuli was not necessary in the subjects with 2000-Hz and/or 4000Hz auditory thresholds below 80 dB HL . In
these subjects, the ABR stimulus was >_20 dB
relative to the auditory threshold at 4000 Hz
and the click-evoked wave V latencies were
within normal limits .
In the 95 group, some of the high-frequency
hearing losses were sufficiently severe to prolong the wave V latencies elicited by clicks and
by 1000-Hz tone pips . The effect of the 4000-Hz
thresholds is expected in the click-evoked ABR
because neurons that respond to the high-frequency components of the stimuli dominate the
latency of the click-evoked ABR (Don and
Eggermont, 1978 ; Fowler, in press) . Because
N
8
O
7
_E
a
U
Z
w
fa
J
CLICKS
TONE PIPS
6
55
6
7
8
5
6
LATENCY AS (ms)
7
8
9
Figure 6 Bivariate plots of the latency of wave Vin the
left ear (abscissa) and the right ear (ordinate) for the click
(left panel) and 1000-Hz tone pip (right panel) stimuli.
Regression lines are shown in both panels .
the spectral splatter of the 1000-Hz tone pips
excites fibers beyond the 1000-Hz area on the
basilar membrane in normal ears, a sufficiently
severe high-frequency hearing loss can also
prolong the wave V latencies to the 1000-Hz
tone pips . This finding was consistent with the
delay in wave V latencies to 1000-Hz tone pips
that was seen in subjects with such severe highfrequency hearing losses that wave V could not
be elicited with 4000-Hz tone pips (Fowler and
Leonards, 1985) . A persistent basal response
bias, therefore, may cause absolute latencies to
1000-Hz stimuli to be delayed in some patients
with severe-to-profound high-frequency cochlear
hearing losses . The tonal stimuli used in this
study had linear ramps . Other ramps, such as
the Blackman, may increase the frequency
specificity of the stimulus in normal hearing
subjects such that the latencies of more patients with high-frequency hearing losses will
fall within the norms .
Although the latencies of waves I and V
were positively correlated, wave I contributed
only 20 percent of the variability to the latency
of wave V for click stimuli and 41 percent for
1000-Hz stimuli. Among the subject groups, the
highest correlations were in the 95 group, in
which the high-frequency hearing losses were
the greatest . Further, I-V latency differences
were shortest for the 95 group with clicks, but
equal for all three subject groups with the 1000Hz tone pips . These results are consistent with
three previous indications that the click-evoked
wave I is derived from higher frequency responses than is wave V. First, Don and Eggermont
(1978) demonstrated the different frequency
responses of waves I and V by noting that wave
I disappeared sooner than wave V as the derived-band ABRs decreased in frequency. Second, Coats and Martin (1977) reported reduced
I-V latency differences in some subjects with
high-frequency cochlear hearing losses . In these
subjects, the click responses were derived from
lower frequencies than in normal-hearing subjects. Third, Fowler and Noffsinger (1983) found
shorter I-V latency differences in normal subjects for ABRs evoked by lower-frequency tone
pips as compared to higher-frequency tone pips .
In the latter two cases, a decrease in the effective stimulus frequency caused a greater prolongation of wave I than of wave V.
One disadvantage in using the tone pips is
the qualitative waveform degradation that can
sometimes result from the longer rise time in
the tone pips than in the clicks . This degradation is expected to affect elderly subjects and
328
rf~I
Cochlear Hearing Loss and ABR/Fowler and Mikami
those with hearing losses, because the waveforms in these subjects already have reduced
amplitudes relative to those of young normalhearing subjects . This degradation may compromise waveform identification and accuracy
in identifying peak latencies, and thus may
limit the usefulness of tonal stimuli in some
subjects .
A further, and perhaps more significant,
disadvantage of the use of tone pips is the
possibility that low-frequency tone pips may
reduce the sensitivity of the ABR to retrocochlear pathology compared to its sensitivity with
clicks or high-frequency tone pips . Clemis and
McGee (1979) reported a diagnostically significant difference in wave V latencies to tone pips
at various frequencies in only 1/17 patients with
acoustic neuromas . That case, however, was the
only one in which all interaural wave V latency
differences were under 1 .0 msec . Retrocochlear
pathology that exerts lesser effects on the wave
V latencies is more likely to be confused with
cochlear pathology, and therefore, is the targeted patient group for the use of tonal stimuli .
Fowler and Noffsinger (1983) reported that in
retrocochlearly impaired subjects, wave V was
more delayed with 4000-Hz stimuli than with
2000-Hz stimuli, and that this discrepancy was
exacerbated with faster stimulation rates .
This finding suggests that higher-frequency
tone pips or clicks may be more sensitive in
identifying retrocochlear disorders than are
lower-frequency tone pips .
Telian and Kileny (1989) found that 1000Hz tone pip ABRs were useful in confirming the
diagnosis of acoustic neuroma made by clickevoked ABR in 17 patients with high-frequency
sensorineural hearing losses . In many of these
patients, the abnormally long interaural wave
V latency differences with click stimuli were
considered to be at least partially caused by the
severity of the high-frequency hearing losses .
The abnormally long interaural differences from
1000-Hz tone pips, however, were attributed to
neural pathology because the 1000-Hz thresholds were better than the higher-frequency
thresholds, and thus, presumably were less
likely to produce a cochlear delay . Further
studies that compare the success rate in identifying retrocochlear lesions with clicks and tone
pips of various frequencies are warranted.
In summary, the use of 1000-Hz tone pips to
elicit the ABR is helpful in distinguishing between cochlear and retrocochlear pathology in
some cases of high-frequency, and particularly
asymmetrical, sensorineural hearing loss . Gen-
erally, the use of clicks is sufficient if the audiometric threshold at 4000 Hz is less than 80 dB
HL and the stimulus is delivered at least 20 dB
above the audiometric threshold at 4000 Hz .
For patients with more severe cochlear hearing
losses, the supplemental use of 1000-Hz tone
pips can reduce the number of equivocal ABRs
if only click stimuli are used . Still to be determined is the likelihood that cases of retrocochlear pathology will fall within normal limits with low-frequency tonal stimuli, but beyond normal limits with clicks or high-frequency
tonal stimuli . Further research is necessary to
determine the comparative diagnostic sensitivity of the ABR elicited by clicks and tone pips at
various frequencies.
Acknowledgment. This study was supported by a Merit
Review from the Medical Research Service, Department
of Veterans Affairs, Washington, DC .
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, '1`'