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Abstract
Recently, auditory steady-state responses (ASSRs) have been proposed as an alternative to the
auditory brainstem response (ABR) for threshold estimation . The goal of this study was to inves-
tigate the degree to which ASSR thresholds correlate with ABR thresholds for a group of sedated
children with a range of hearing losses . Thirty-two children from the University of Iowa Hospitals
and Clinics ranging in age from 2 months to 3 years and presenting with a range of ABR thresh-
olds participated . Strong correlations were found between the 2000-Hz ASSR thresholds and click
ABR thresholds (r = .96), the average of the 2000- and 4000-Hz ASSR thresholds and click ABR
thresholds (r = .97), and the 500-Hz ASSR and 500-Hz toneburst ABR thresholds (r = .86) .
Additionally, it was possible to measure ASSR thresholds for several children with hearing loss
that was great enough to result in no ABR at the limits of the equipment . The results of this study
indicate that the ASSR may provide a reasonable alternative to the ABR for estimating audiometric
thresholds in very young children .
Key Words : Auditory brainstem response, auditory evoked responses, auditory steady-state
responses
Surnario
Palabras Clave : Respuesta auditiva del tallo cerebral, respuestas auditivas evocadas, respuestas
auditivas de estado-estable
Abreviaturas : ABR = respuestas auditivas del tallo cerebral ; ASSR = respuestas auditivas de
estado-estable
*Department of Speech Pathology and Audiology, and 'Department of Otolaryngology-Head and Neck Surgery,
University of Iowa, Iowa City, Iowa
Reprint requests : Kathy R . Vander Werff. 311 WJSHC, Department of Speech Pathology and Audiology, University of
Iowa, Iowa City, IA 52242
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Journal of the American Academy of Audiology/Volume 13, Number 5, May 2002
ecently, both the National Institutes of ies, tone-ABR thresholds have been found to be
Health (National Institutes of Health, between 10 and 20 dB nHL in normal-hearing
R 1993) and the American Academy of individuals and are generally within 15 dB of
Pediatrics (American Academy of Pediatrics, behavioral threshold for hearing-impaired indi-
1999) issued statements calling for universal viduals (+5 to 15 dB for adults, ±10 dB for
hearing screening of all newborns . The impor- infants and young children) . However, some
tance of universal hearing screening is under- studies have questioned the frequency speci-
scored by the work of Yoshinaga-Itano and ficity and reliability of threshold estimation
colleagues (1998, 2000) and Moeller (2000), who with low-frequency tone-evoked ABR (Hayes
demonstrated that hearing-impaired children and Jerger, 1982 ; Gorga et al, 1988 ; Laukh et al,
who receive intervention during the first 6 to 12 1988). In addition, toneburst ABR waveforms,
months of life are able to develop better speech especially to low-frequency stimuli, tend to be
and language skills than children for whom inter- less distinct and more difficult to identify than
vention is delayed. However, the process of fit- the click ABR. Output limitations are also a
ting a hearing aid or determining if a specific child concern with toneburst stimuli, particularly for
is a cochlear implant candidate requires knowl- low-frequency tonebursts for which thresholds
edge of that child's residual hearing abilities . are elevated relative to behavioral threshold.
For many children, it may be possible to use These concerns may limit the implementation
age-appropriate behavioral techniques to esti- of toneburst ABR protocols in many clinics.
mate hearing thresholds for audiometric fre- The auditory steady-state response (ASSR)
quencies from 250 to 4000 Hz . For others, is an alternative evoked potential technique that
however, that is not the case. For those children, uses continuous rather than transient stimuli to
evoked potential estimates of audiometric thresh- elicit a response from the auditory system .
old may be the only information about the child's Steady-state responses were first reported in
hearing status that is available at the time these the literature decades ago (Galambos et al, 1981 ;
critical decisions need to be made . Stapells et al, 1984) . Kuwada et al (1986)
The auditory brainstem response (ABR) is published one of the first papers describing
a far-field evoked potential that is used almost steady-state responses evoked using amplitude-
universally to estimate auditory sensitivity in modulated sinusoidal stimuli. This study, and
children too young to be tested using standard many of the studies that followed, used rela-
behavioral methods. The ABR to click stimuli is tively low rates of amplitude modulation (approx-
probably the most commonly used clinically. imately 40 Hz) to evoke the response (Milford and
Although the abrupt onset of the click stimulus Birchall, 1989 ; Griffiths and Chambers, 1991 ;
is ideal for generating the ABR, the drawback Aoyagi et al, 1993) . Despite initial enthusiasm
is that the resulting frequency spectrum is broad. surrounding this research, it soon became clear
Additionally, behavioral thresholds have been that the ASSR, evoked using low-modulation
shown to increase as the duration of an acoustic frequencies, was adversely affected by sleep and
stimulus decreases (Gorga et al, 1984). There- sedation and was not able to be recorded reliably
fore, when short-duration stimuli such as clicks in very young children (Stapells et al, 1988 ;
are used, higher input voltages to the earphones Cohen et al, 1991 ; Aoyagi et al, 1993 ; Dobie and
are needed to produce threshold-level responses. Wilson, 1998). More recent research has shown
Transducer-dependent input voltage maximums that if modulation frequencies between approx-
effectively limit the maximum output levels, imately 70 and 100 Hz are used, the resulting
making it difficult to distinguish between severe response, although smaller in amplitude than the
and profound losses using the type of stimuli and response evoked using lower-modulation fre-
transducers typically used to record the ABR. quencies, can be recorded reliably in sedated
Studies have, in fact, shown that the click ABR infants (Aoyagi et al, 1994a; Rickards et al, 1994 ;
does a relatively poor job of differentiating hear- Rance et al, 1995 ; Lins et al, 1996).
ing losses in the severe range from those in the Several investigators have reported find-
profound range (Brookhouser et al, 1990 ; Rance ing significant correlations between high-rate
et al, 1998 ; Schoonhoven et al, 2000). ASSR thresholds and behavioral audiometric
ABR to brief tones can be used to obtain thresholds for individuals with a range of hear-
more frequency-specific threshold information ing losses (Aoyagi et al, 1994b ; Levi et al, 1995 ;
than is available from the click ABR. A recent Rance et al, 1995, Lins et al, 1996 ; Picton et al,
meta-analysis of the toneburst ABR literature 1998). Although these results appear promising,
by Stapells (2000) has shown that across stud- it is difficult to make definitive conclusions by
228
ASSR and ABR Thresholds/Vander Werff et al
230
ASSR and ABR ThresholdsNander Werff et al
RESULTS
231
Journal of the American Academy of Audiology/Volume 13, Number 5,
May 2002
Phase-locked Random
NV, left ear, 500 Hz, 50 dB HL NV, left ear, 500 Hz, 40 dB HL
120 0
A 0 0 .'- "00 3
100
-2 kHz 00 0
80 00
60 0 ~~O'
0 ,.
40
r= .96
20 °$ . . y=1 .18x+6 .7
0
Figure 4 Representative auditory steady-state response
0 10 20 30 40 60 60 70 80 90
results for one subject (NV) at two different levels . The Click ABR Threshold (dB nHL)
left panel shows a significant phase-locked response at
50 dB HL at 500 Hz . Note the clustering of the vectors
within one quadrant . The right panel shows a random,
120
non-phase-locked result from the same subject at 500 Hz 0
08 0
232
ASSR and ABR Thresholds/Vander Werff et al
ABR thresholds (r = .96) . A similar correlation thresholds (r = .863, n = 169) was higher than
is found between the average of the 2000- and that for ABR (r = .828, n = 93), although the dif-
4000-Hz ASSR thresholds and the click-evoked ference was not significant . The thresholds for
ABR threshold (r = .97), although there are the two types of evoked potential thresholds
fewer datum points (n = 18) in this figure owing were not directly compared .
to the fact that 4000-Hz thresholds were not The population for whom ASSR threshold
obtained in all subjects . estimation procedures may prove particularly
Panel C of Figure 5 shows the relationship beneficial is children with severe to profound
between 500-Hz toneburst ABR thresholds and hearing losses . In this study, we report data
the ASSR thresholds recorded using a 500-Hz from 31 ears for which no click ABR was recorded
carrier tone . Twenty-three ears with toneburst at the maximum stimulation levels . Fifty-eight
ABR responses are included in the regression, percent of these ears had measurable ASSR
whereas the 30 ears with no response to tone- thresholds at 2000 Hz . At 500 Hz, 33 percent of
burst ABR are not included but are shown in the the 30 ears that had no response at the limits
gray area of the graph . Although the correlation of the ABR equipment had measurable ASSR
between ASSR and ABR thresholds is not as thresholds . There were only 2 cases of ears for
strong as that observed between click ABR which an ABR response was judged to be present
thresholds and high-frequency ASSR thresh- (both within 5 dB of the maximum stimulation
olds, the correlation is still significant and level) with no response to ASSR in the high fre-
strong (r = .86) . quencies . Both of these cases had no response to
ASSR at 4000 Hz but did have a response at
DISCUSSION 2000 Hz at least 15 dB below the maximum
stimulation level. The 2000- to 4000-Hz average
T he purpose of this study was to compare click for these two subjects was calculated assuming
and 500-Hz ABR thresholds to ASSR thresh- an arbitrary threshold value of 125 dB HL at
olds at 500, 2000, and 4000 Hz in infants and 4000 Hz ; therefore, they are included in the
young children . The results of this study show that regression analysis in Figure 5. There were no
these two measures were found to have a strong cases at 500 Hz for whom a response was
positive relationship, with correlation coefficients obtained to the ABR stimulus but not to the
ranging between .97 for the click ABR and the ASSR .
2000- to 4000-Hz average ASSR thresholds to .86 These findings of a potential advantage of
for the 500-Hz ABR and ASSR . ASSR over ABR for severe to profound losses are
Limited data exist directly comparing ABR consistent with the results of previously reported
and ASSR thresholds in hearing-impaired sub- studies (Rance et al, 1995, 1998, 2001) . These
jects . Johnson and Brown (unpublished data studies have shown that the error in prediction
currently in review process) tested a small group of hearing loss decreases with increasing degree
of adults (N = 11) with a range of hearing losses of loss . Rance and colleagues (2001) found that
and compared toneburst ABR thresholds with the discrepancy between ASSR and behavioral
ASSR thresholds . A strong correlation (r = .91) thresholds was 5 dB or less for infants with
between ABR and ASSR thresholds was obtained severe to profound hearing loss . Rance and col-
when the results collected at 500, 1000, and leagues (1998) also found that no response to
2000 Hz were combined . The results of the pre- ASSR at maximum presentation levels strongly
sent study agree well with these results and indicated profound or total hearing loss in a
suggest that the ASSR may make a reasonable study of 108 infants and young children . Of the
alternative to the ABR for threshold estimation absent ASSR responses in the Rance and col-
in sedated infants . In studies that have compared leagues (1998) study, 99 .5 percent corresponded
the two types of physiologic thresholds to behav- to behavioral thresholds within 10 dB of the
ioral thresholds, the correlations between behav- maximum ASSR level . This evidence indicates
ioral thresholds and ASSR were similar to the that absent ASSR implies no usable hearing at
correlations to ABR (Aoyagi et al, 1994b, 1996, that frequency. This is not true ofABR, for which
1999) . In the study with the largest data set, evidence has shown that absent click ABR does
Aoyagi and colleagues (1999) compared behavioral not rule out useful residual hearing (Brook-
thresholds to 1000-Hz toneburst ABR thresholds houser et al, 1990 ; Rance et al, 1998 ;
and to 1000-Hz ASSR thresholds for a group of Schoonhoven et al, 2000) .
125 children ranging in age from 3 to 15 years . The test time for the ASSR protocol used in
The correlation coefficient for ASSR to behavioral this study was generally longer than for the
233
Journal of the American Academy of Audiology/Volume 13, Number 5, May 2002
ABR. However, the fact that the ASSR was Aoyagi M, Yamazaki Y, Yokota M, et al . (1996) . Frequency
always completed last, when subjects tended to specificity of 80-Hz amplitude-modulation following
response . Acta Otolaryngol Suppl (Stockh) 522:6-10.
be noisier, may have contributed to the increased
test time . Also, the prototype device used for Aoyagi M, Suzuki Y, Yokota M, et al . (1999) . Reliability
ASSR did not have the capability for artifact of 80-Hz amplitude-modulation-following response
detected by phase coherence. Audiol Neurootol 4:28-37 .
rejection or the presentation of multiple-stimulus
frequencies either in the same ear or to both ears Brookhouser PE, Gorga MP, Kelly WJ . (1990) . Auditory
simultaneously. Future versions of the device brainstem response results as predictors of behavioral
auditory thresholds in severe and profound hearing
that allow for these features will most likely impairment . Laryngoscope 100:803-810 .
decrease test time significantly.
The behavioral thresholds of the subjects Cohen LT, Rickards FW, Clark GM . (1991) . A compari-
son of steady-state evoked potentials to modulated tones
in the current study were not known. Therefore, in awake and sleeping humans . J Acoust Soc Am 90 :
the relative accuracy of the threshold estima- 2647-2679.
tions based on the two evoked potentials can-
Dobie RA, Wilson MJ . (1998) . Low-level steady-state audi-
not be compared . However, the results of this tory evoked potentials : effects of rate and sedation on
study indicate that ASSR thresholds are highly detectability. JAcoust Soc Am 104:3482-3488 .
correlated with ABR results in sedated infants.
Galambos R, Makeig S, Talmachoff PJ . (1981) . A 40 Hz
These results are to be expected and are reas- auditory potential recorded from the human scalp. Proc
suring given that ABR and ASSR are likely Natl Acad Sci U S A 78 :2643-2647 .
generated from many of the same anatomic
Gorga MP, Beauchaine KA, Reiland JK, et al . (1984). The
structures . However, ASSR thresholds may effects of stimulus duration on ABR and behavioral thresh-
provide additional information for the charac- olds . JAcoust Soc Am 76 :616-619 .
terization of severe to profound hearing loss .
Gorga MP, Kaminski JR, Beauchaine KA, Jesteadt W.
These results support the use of ASSR as an (1988) . Auditory brainstem responses to tone bursts in
alternative to ABR for threshold assessment in normally hearing subjects . J Speech Hear Res 31 :87-97 .
infants.
Griffiths SK, Chambers RD . (1991) . The amplitude mod-
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Acknowledgment . This work was supported by research Hear 12 :235-241 .
grant DC00242 from the National Institutes of Health
(NIH)/National Institute on Deafness and Other Hayes D, Jerger J. (1982) . Auditory brainstem response
Communication Disorders; grant RR59, General Clinical (ABR) to tone-pips : results in normal and hearing-
Research Centers Program, NIH; and the National impaired subjects . Scand Audiol 11 :133-142 .
Organization of Hearing Research .
Johnson TA, Brown CJ . (In review). Within subject com-
The authors wish to thank Beth Macpherson,
parison of audiometric, steady state evoked potential and
Danielle Kelsay, Beth Wahl, Heather South, and Keely auditory brainstem response thresholds .
Seyle for their help with this project. Thanks are also
due to the three reviewers for their helpful comments on Kuwada S, Batra R, Maher VL . (1986) . Scalp potentials
the manuscript . of normal and hearing-impaired subjects in response to
Portions of this research were presented at the sinusoidally amplitude-modulated tones. Hear Res
XVIIth Biennial Symposium of the International Evoked 21 :179-192 .
Response Audiometry Study Group held at the University
Laukli E, Fjermedal O, Mair IWS . (1988) . Low-frequency
of British Columbia, Vancouver, BC, July 22-27, 2001 .
auditory brainstem response threshold . Scand Audiol
17 :171-178 .
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