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C H A P TE R 14

Auditory Brainstem
Response: Estimation of
Hearing Sensitivity
Linda J. Hood

frequency-specific stimuli in infants and young children.


INTRODUCTION These methods are the ABR and the auditory steady-state
Early identification of hearing loss is now well established response (ASSR). This chapter will focus on the ABR as it
in the evaluation and care of newborn infants. The positive can be applied to threshold prediction; the ASSR is thor-
impact of identification of hearing loss in infants on language oughly described in Chapter 15.
outcomes has been definitively demonstrated (e.g., Yoshinaga-
Itano et al., 1998). Timelines that include identification of
hearing loss before 1 month of age, thorough evaluation of
A HISTORICAL PERSPECTIVE
an infant by 3 months of age, and implementation of manage- AEPs from the cochlea to the cortex have been studied as
ment before 6 months of age are incorporated into widely rec- possible methods to assess hearing. Indeed, Hallowell Davis’
ognized recommendations (e.g., JCIH, 2007; see Chapter 23). pioneering work with cortical potentials first reported in
For early identification to be effective, test methods that can 1939 was, in part, directed toward the development of a
accurately quantify auditory threshold sensitivity in infants technique to assess auditory function without the need for
must be available to provide adequate follow-up of those who patient participation. Cortical responses and middle latency
do not pass newborn hearing screening. responses, studied in the 1950s and 1960s, proved useful in
Objective measures are key components in a test battery acquiring the necessary information about threshold sen-
for young children in whom, for reasons that might include sitivity (e.g., Davis, 1976). However, these responses gen-
developmental delays, the ability to obtain reliable responses erally require patients to be awake, cooperative, and alert
through behavioral testing is not possible. Auditory-evoked during testing to maintain response amplitude. Steady-state
potentials (AEPs), when used and interpreted properly, also responses, recorded with a slower rate of 40 Hz and primar-
provide a powerful method of obtaining reliable estimates of ily cortical in origin (Galambos et al., 1981; Kuwada et al.,
auditory sensitivity in individuals of all ages who either cannot 2002), are also an efficient method of obtaining estimates of
or will not provide reliable results on behavioral hearing tests. hearing sensitivity; however, this response again is affected
AEPs in general provide objective assessment of audi- by sleep and sedation which limit its application in infants
tory function with two broad areas of application: (1) Identi- and young children. Thus, whereas cortical responses have
fication of neurologic abnormalities of the VIII cranial nerve higher face validity in that they evaluate a greater propor-
and auditory pathways and (2) estimation of hearing thresh- tion of the auditory pathway, the applications in infants and
old sensitivity. Applications in both of these general areas young children are limited in the population most in need
exist across AEPs obtained from the cochlea to the cortex of an objective method of assessing hearing sensitivity.
and in patients of all ages. If the goal of hearing testing is to determine peripheral
The auditory brainstem response (ABR) is an evoked hearing sensitivity, then measurement of responses directly
potential used to both assess neural response integrity and from the cochlea would seem ideal. In fact, electrocochleog-
obtain estimates of hearing thresholds. Although the ABR raphy proved a very useful technique in the 1960s and 1970s.
is not a test of hearing per se, the information obtained can However, the somewhat invasive nature of transtympanic or
be useful in estimating or predicting hearing thresholds. To eardrum recording sites limited its widespread clinical appli-
accurately characterize threshold sensitivity, information cation, particularly in infants and young children. The relative
must be obtained for defined frequency regions, as is stan- ease of recording the ABR and its resistance to the effects of
dard practice in behavioral testing via puretone audiom- sleep and sedation have facilitated widespread use of this AEP
etry. Presently, there are two approaches that are considered in prediction of hearing thresholds in infants and children,
appropriate objective measures for obtaining responses to as well as adults.

249
250 SECTION II Ş 1IZTJPMPHJDBM1SJODJQMFTBOE.FBTVSFT

cially useful when one wishes to know the sensitivity of each


WHAT THE ABR TESTS ear separately, to compare responses by air and bone conduc-
Although AEPs have proven useful in estimating hearing tion with or without masking, and to estimate auditory func-
thresholds, it is important to remember that the ABR is tion in various frequency regions. Since AEPs are a test of the
NOT a test of hearing! The ABR and other evoked potentials neural system, insight into the integrity of the neural path-
assess neural synchrony, that is, the ability of the peripheral ways should also be considered. AEPs should not be used in
and central nervous system to respond to external stimu- lieu of a behavioral audiogram in patients who can provide
lation in a synchronous manner. A synchronous neural reliable behavioral responses. An ultimate goal in all patients,
response results from simultaneous firing of a group of where possible, should be to obtain behavioral responses
neurons. Since clinical recording of responses is completed and use this information in combination with physiologi-
in a far-field manner via electrodes placed on the scalp, away cal responses. In infants and young children, behavioral
from the source of the response, a sufficient number of responses may be obtained at a later time, but, in the mean-
neurons must fire together to yield a response of sufficient time, appropriate management can and should begin based
amplitude to be recorded at this distance. on AEP results. Comparisons of evoked potential and behav-
When the auditory nervous system pathways are func- ioral responses provide a valuable clinical cross-check and
tioning normally, we can use evoked potentials to record confirmation of results on each measure individually.
neural responses to stimuli presented at various intensity
levels. Thus, by presenting stimuli at a series of intensity
levels above and below threshold, one can infer sensitivity at
 8):"3&'3&26&/$:41&$*'*$
the periphery based on whether or not sound was able to 45*.6-*/&$&44"3:
pass through the ear and cause the sources of the neural Although broadband stimuli, such as clicks, are useful for
response to respond in a synchronous manner. For indi- evaluation of patients with suspected neurologic disease and
viduals who do display synchronous neural responses, we for establishing neural synchrony, clicks are not considered
can find the lowest stimulus intensity level that yields the appropriate for threshold testing. Because clicks are broad
neural response and relate that to a threshold for hearing. A band in nature and also stimulate more basal regions of the
limitation, in relation to patients with auditory neuropathy/ cochlea, it is not possible to know the exact frequency range
dys-synchrony, will be discussed later. being tested. This is particularly problematic in patients with
ABRs can be obtained at intensities very close to behav- sloping (either positively or negatively) hearing losses. Fur-
ioral thresholds if a sufficient number of responses are aver- thermore, behavioral puretone audiometry is completed at
aged to adequately reduce the background physiological noise multiple frequencies, not just one frequency. Figure 14.1 shows
(Elberling and Don, 1987). This requires a greater number two hearing losses where clicks or other broadband stimuli
of stimuli, on the order of 10,000 sweeps per test level and will underestimate or miss a hearing loss. In Figure 14.1A,
smaller intensity step sizes, and thus a longer time than is clicks will underestimate or miss this high-frequency hearing
clinically feasible. In routine clinical procedures where fewer loss. The latency may be longer since lower frequency regions
responses are averaged, responses can generally be obtained are stimulated. In Figure 14.1B, a click will underestimate or
near, but not at, behavioral thresholds in a quiet subject. more likely miss this low-frequency hearing loss. Responses
to clicks will be dominated by cochlear basal responses and
WHEN TO USE THE ABR TO will not reflect a hearing loss in more apical regions of the
cochlea.
&45*."5&"6%*503:'6/$5*0/
AEPs are best utilized when the clinician desires a noninva-
sive, objective approach to assessment of auditory function
5ZQFTPǨ'SFRVFODZ4QFDJǨJD4UJNVMJ
in infants, children, and adults who cannot participate in A 100-microsecond electrical pulse, impressed on an
voluntary behavioral audiometric procedures. AEPs are espe- earphone, generates a broadband signal whose primary

0.25 0.5 1 2 4 8 kHz 0.25 0.5 1 2 4 8 kHz


0 0

FIGURE 14.1 Example audiograms


depicting puretone thresholds for right 50 50
(dark gray) and left (light gray) ears that
are consistent with a downward sloping
hearing loss in (A) and an upward 100 100
sloping hearing loss in (B). A dB HL B dB HL
CHAPTER 14 Ş "VEJUPSZ#SBJOTUFN3FTQPOTF&TUJNBUJPOPǨ)FBSJOH4FOTJUJWJUZ 251

frequency emphasis is determined by the resonant fre- bursts with longer rise times will be more frequency specific,
quency of the transducer. With earphones typically used but will generate poorer neural synchrony which will affect
in clinical evaluation, the maximum energy peaks of these the quality of the ABR. As already emphasized, the goal of
clicks are focused in the frequency region between 1,000 using ABR for threshold prediction is to stimulate isolated
and 4,000 Hz (e.g., Don et al., 1979). The greatest agree- regions of the basilar membrane to analyze function in dis-
ment with puretone thresholds is in the 2,000- to 4,000-Hz tinct frequency regions. Thus, control of spread of acoustic
frequency range (Bauch and Olsen, 1986). energy to surrounding frequencies works in opposition to
Several types of stimuli and recording methods have the ability to activate a large number of neural units and
been proposed to obtain responses from narrower frequency obtain a clearly synchronous ABR. The more abrupt the
regions. Some alternative stimuli and methods include tone acoustic onset of the stimulus, the more synchronous the
bursts or tone pips, filtered clicks, tone bursts in notched neural discharge and the clearer the resulting ABR. How-
noise, and high-pass masking of clicks or tone bursts. Each ever, as noted previously, abrupt onset, broadband stimuli
type of stimulus appears to have advantages and limitations, have poor frequency specificity.
and stimulus selection is dependent on frequency specificity, Although the ideal stimulus for frequency-specific
the amount of time available for testing, and the equipment ABR would be a puretone, this is not possible because stim-
available. uli with long rise times (needed to maintain integrity of a
Techniques of masking test stimuli, in an effort to obtain puretone) will not yield sufficient neural synchrony to obtain
greater control and precision related to the frequency con- an ABR at the surface of the head. Thus, the stimulus used in
tent of the stimulus, have been the focus of several investiga- ABR testing has a shorter onset (rise time) than a puretone,
tions. In a method pioneered by Teas et al. (1962), the cutoff but longer than a click (which is essentially instantaneous).
frequency of a high-pass masker is progressively decreased This results in some spectral spread of the tone burst stimu-
and click ABRs at adjacent cutoff frequencies are subtracted lus, compared to a puretone. However, the spectrum of the
from the filtered ABR and/or from the preceding ABR. This tone burst is considerably narrower than a click and thus
method allows separation of frequency-specific wave com- stimulation along the basilar membrane is restricted and
ponents and has been shown to be useful in audiogram reasonably frequency specific. In interpreting results, it is
reconstruction (Don et al., 1979). A modification of this important to remember that the use of tone bursts results
method uses tone bursts presented in the presence of a high- in stimulation of the cochlea at frequency regions sur-
pass masker (Kileny, 1981). By presenting stimuli simulta- rounding the target frequency as well as at the desired
neous with a masker, the higher frequency response regions frequency.
of the cochlea are blocked and the resulting responses reflect
activity in frequency areas outside of the masker region. 'SFRVFODZ4QFDJǨJDJUZWFSTVT
Presentation of stimuli in notched noise narrows the
stimulation to limited regions of the basilar membrane
1MBDF4QFDJǨJDJUZ
through presentation of a noise masker with components There is a difference between frequency specificity and place
above and below the frequency range of interest (e.g., Picton specificity. Frequency specificity refers to the characteristics
et al., 1979). The presence of the notched noise masker of the stimulus whereas place specificity reflects a region of
restricts the cochlear region able to contribute to the ABR the cochlea. Although the frequency regions activated may
to those frequencies within the band of the notch. Although be relatively narrow at low intensities, there is consider-
the utility of this method has been clearly demonstrated, able spectral spread for moderate-to-high–intensity signals.
additional special equipment or software may be needed When presented at higher intensities, on the order of 60 to
to create and present the noise. Further, studies have dem- 80 dB HL or higher, even puretones can activate wider fre-
onstrated similar results with and without notched noise quency ranges on the basilar membrane surrounding the
masking for most cases of hearing loss, with exception being center frequency of the stimulus (Moore, 2004).
very steeply sloping losses (e.g., Johnson and Brown, 2005). Spread of excitation can be particularly problematic
Presently, tone bursts or tone pips, without high-pass in underestimating hearing loss in individuals with steeply
or notched noise masking, are the most widely accepted and sloping hearing losses. A tone burst presented to an ear with
preferred stimulus for frequency-specific ABR evaluation. a steeply sloping high-frequency hearing loss may yield a
This chapter focuses on the use of tone bursts centered at response, but that response may be generated from stimula-
various frequencies in recording frequency-specific ABRs. tion of a lower frequency responsive region where thresh-
olds are better. Although latencies may be longer because of
'SFRVFODZ4QFDJǨJDJUZWFSTVT more apical stimulation, it can remain difficult to determine
the source of the response and there is risk of underestimat-
/FVSBM4ZODISPOZ ing a hearing loss. Thus, caution must be exercised in inter-
When using frequency-specific stimuli there is a trade-off preting ABRs, particularly as in the case of infants where
between frequency specificity and neural synchrony. Tone behavioral thresholds are unknown.
252 SECTION II Ş 1IZTJPMPHJDBM1SJODJQMFTBOE.FBTVSFT

envelopes now used often have no plateau and are referred


 45*.6-64$0/4*%&3"5*0/4*/ to as 2-0-2 cycle envelopes.
ABR THRESHOLD TESTING The envelope of a stimulus is constructed using various
Characteristics of the ABR will change as a result of a num- types of windowing or gating functions, in other words the
ber of stimulus, recording, and patient factors. The effects of way in which stimuli are turned on and off. A linear enve-
these factors must be considered when designing test proto- lope involves an abrupt change from no signal to the rise (or
cols for various clinical populations, determining appropri- ramp) of the signal. A nonlinear windowing function, such as
ate stimulus parameters, setting recording parameters, and a Blackman window, has a curvilinear onset. Although differ-
interpreting ABRs. Stimulus, recording, and subject factors ences in spectra have been observed with linear versus non-
will be discussed in regard to applications in ABR threshold linear functions, studies have shown similar ABR results using
prediction in the following sections. We begin with stimulus either linear or Blackman windowing functions (e.g., Johnson
factors. and Brown, 2005; Oates and Stapells, 1997). Thus, although
Changes in the settings used in creating test stimuli some prefer to use a nonlinear, such as Blackman, function,
can affect the latency and the amplitude of the ABR. An either can be used. Most current clinical ABR equipment uses
understanding of the effects of parametric changes in the the Blackman or nonlinear functions as the default setting.
stimulus is necessary to correctly interpret test results. And, A caution is needed related to equipment settings for
importantly, understanding the results of adjusting various stimulus durations and windowing functions. The way in
stimulus settings can be used to the examiner’s advantage in which these are set varies across ABR systems. Some systems
obtaining the best possible responses. will differentially ask for duration settings in either cycles or
milliseconds depending on the type of envelope requested.
5POF#VSTU&OWFMPQF$IBSBDUFSJTUJDT Further, some systems require information about the total
duration of the stimulus whereas others set stimuli accord-
BOE(BUJOH'VODUJPOT ing to rise and fall times separately. The key here is to under-
Whereas puretones have long rise times, in the range of 20 to stand the desired and appropriate characteristics and know
200 ms, tone bursts must have shorter rise times to achieve how to calculate those according to the specific ABR sys-
needed synchronous neural responses. As noted earlier, tem requirements. Knowing this will avoid errors that could
shortening the onset time of a stimulus results in broadened result in stimuli with poor frequency specificity (rise time or
spectral characteristics. The optimal stimulus will maintain envelope too short) or poor neural responses (rise time or
as much frequency specificity as possible while allowing envelope too long).
activation of a sufficient number of neurons to record a far-
field response. Characteristics needed to achieve this goal
have been derived from studies that compare various stimu-
4UJNVMVT'SFRVFODZ
lus rise times and durations across frequency and intensity. Higher frequency stimuli elicit shorter ABR latencies than
Davis et al. (1985) recommended a tone burst with two lower frequency stimuli. These latency differences occur
cycles of rise time, a one-cycle plateau, and two cycles of decay, because high-frequency stimuli activate more basal portions
known as a “2-1-2 envelope.” Changes in envelope character- of the basilar membrane, resulting in earlier neural activa-
istics affect the spectrum of the stimulus, the intensity (and tion and shorter latencies compared to stimuli centered at
the loudness because of durational changes and temporal lower frequencies. Since lower frequency stimuli have to
integration), and the latency of the response because a longer travel further toward the apex of the cochlea, latencies for
rise time results in increased latency. By holding the number these stimuli will be longer. Because all components of the
of periods in the stimulus constant across different frequen- ABR are dependent on cochlear processing, all waves of the
cies, the power spectrum is held constant. ABR (e.g., Waves I, III, V) will display shorter latencies for
To create appropriate stimuli, one needs to recall the higher frequency tone bursts and longer latencies for lower
duration of a single cycle for various frequencies. For exam- frequency tone bursts. (For reference, a sample of a normal
ple, one cycle of a 500-Hz tone is 2 ms in duration. There- ABR, obtained with click stimuli, is shown in Figure 11.1
fore, to create a 2-1-2 envelope, the rise time would be 4 ms in Chapter 11.) ABRs obtained to tone bursts centered at
(two cycles at 2 ms per cycle), the plateau would be 2 ms 500, 1,000, 2,000, and 4,000 Hz are shown in Figure 14.2.
(one cycle), and the fall time would be 4 ms (two cycles). Here it can be seen that latencies for Wave V at comparable
This would add up to a total envelope duration of 10 ms. intensities are longer for low-frequency tone bursts than for
As another example, a 1,000-Hz tone burst would have a high-frequency tone bursts.
total envelope duration of 5 ms (2 ms rise, 1 ms plateau,
and 2 ms decay). These stimulus parameters have generally
held the test of time with some minor modifications. For
4UJNVMVT*OUFOTJUZ
example, since the ABR is an onset sensitive response, the As stimulus intensity decreases from 70 or 80 dB nHL to
plateau contributes little to the utility of the stimulus. Thus, the threshold of detectability, all waves of the ABR show a
CHAPTER 14 Ş "VEJUPSZ#SBJOTUFN3FTQPOTF&TUJNBUJPOPǨ)FBSJOH4FOTJUJWJUZ 253

500 Hz TB 1,000 Hz TB 2,000 Hz TB 4,000 Hz TB


V
V V
V
75

V V V
55 V

V V V
V
35
V V V

25

15
dB nHL
20 ms 20 ms 20 ms 20 ms
FIGURE 14.2 ABRs to tone bursts centered at 500, 1,000, 2,000, and 4,000 Hz recorded from an indi-
vidual with normal hearing. The latencies of Wave V at 75 dB nHL are 8.53 ms for a 500-Hz tone burst,
7.70 ms for a 1,000-Hz tone burst, 7.03 ms for a 2,000-Hz tone burst, and 6.53 ms for a 4,000-Hz tone
burst, demonstrating the latency decrease as center frequency of the tone burst increases.

systematic increase in latency and decrease in amplitude 4UJNVMVT3BUF


(Picton et al., 1974; Starr and Achor, 1975). This is illus-
trated in Figure 14.2. Wave V is most visible at lower inten- The rate at which test stimuli are presented affects both the
sity levels whereas the earlier components tend to become latency and the amplitude of the various components of
indistinguishable at lower intensities. The intensity at which the ABR. In general, at stimulus rates above approximately
earlier waves become less apparent also depends on tone 30 stimuli per second, the latency of all components of the
burst frequency. Changes in Wave V latency with intensity ABR increases and the amplitude of the earlier components
are nonlinear with shifts on the order of approximately decreases (e.g., Don et al., 1977; Terkildsen et al., 1975).
0.2 to 0.3 ms per 10 dB through mid-intensity ranges and Latency does not increase by the same amount for all com-
more rapid changes in latency at lower intensities and near ponents. With increasing stimulus rate, the later compo-
response thresholds. nents (e.g., Wave V) show a greater latency increase than the
The amplitude of the ABR is rarely greater than earlier components, which results in a prolongation of the
1 microvolt and no consistent trend in amplitude growth Waves I–V interwave interval. Wave V also shows less of an
as a function of intensity has been reported (Hecox and amplitude decrease at high rates, which can facilitate the use
Galambos, 1974; Jewett and Williston, 1971). This is most of higher stimulus rates in evaluation.
likely related to the considerable variation in amplitude Stimulus rate is an important consideration in testing
within and among subjects, as amplitude is more highly infants and young children. Faster stimulus rates may help in
influenced by noise than latency. The amplitude of Wave decreasing test time since more stimuli can be presented in a
V is less affected by intensity decreases than earlier compo- shorter period of time. Faster stimulus rates may be useful,
nents (Pratt and Sohmer, 1976; Terkildsen et al., 1975). with some caveats discussed later, in threshold-seeking proce-
It is important to note that the actual intensity and fre- dures where only the presence or absence of Wave V is of inter-
quency information reaching the cochlea is dependent on est. However, faster stimulus rates may also reduce the clarity
the acoustic properties of the transducer, the volume of the and reproducibility of responses, particularly for the earlier
external ear canal, and middle-ear transmission character- components. As noted later, this can be problematic if response
istics. This can be particularly problematic in infants and amplitude is reduced and thus the signal-to-noise ratio is com-
young children whose ear canals are small. It is possible that promised. Here, results could suggest the presence of a hearing
technologic advances will facilitate use of a transducer con- loss when, in fact, hearing thresholds are normal.
taining a probe microphone to monitor the sound pressure
level in the ear canal and a method to account for intensity
differences as a function of ear canal volume. This should be
4UJNVMVT1PMBSJUZ
especially useful in neonatal screening and testing of infants Stimulus polarities for ABR testing can be selected as rar-
and young children. efaction, condensation, or alternating between rarefaction
254 SECTION II Ş 1IZTJPMPHJDBM1SJODJQMFTBOE.FBTVSFT

and condensation stimuli. Because latencies of the various frequency hearing loss show considerable latency changes
components in the resulting response are dependent on the within individuals as a function of polarity. Simulation of
polarity of the test stimuli, both consistent use of a particu- high-frequency hearing loss through high-pass masking
lar polarity when comparing results to normative data or indicates that the polarity effects are primarily because of
previous tests and knowledge of the effects of polarity are lower frequency contributions to the response that would be
critical. particularly apparent in person with high-frequency hearing
A rarefaction stimulus produces an initial outward move- loss (Schoonhoven, 1992). Large latency differences between
ment of the earphone diaphragm that generally leads to an polarities are observed in individual subjects whereas there
outward movement of the footplate of the stapes and an do not seem to be systematic trends when comparisons are
upward motion of the more basal structures of the organ of made on a group basis (Schoonhoven, 1992; Sininger and
Corti. Because the upward motion of the basilar membrane Masuda, 1990). Because phase reversals can degrade an
is the depolarizing motion for the hair cells, latency is slightly ABR sufficiently to interfere with accurate interpretation
shorter and amplitude is higher for the early components of and reversals appear to have a detrimental effect in some
the ABR for rarefaction pulses in comparison to condensa- individuals, use of single polarity stimuli is recommended
tion pulses in the majority of subjects (e.g., Stockard et al., in patients with high-frequency hearing loss and patients,
1979). Condensation stimuli produce an initial inward move- such as infants and young children, where hearing threshold
ment, followed by outward movement and depolarization of configuration is not known.
the hair cells. Thus the early components of the ABR may be There also is a group of patients in which ABRs appear
slightly longer in latency than those produced using rarefac- to be present when in fact the acquired waves represent the
tion pulses. Wave V amplitude tends to be larger in response to cochlear microphonic (CM; e.g., Berlin et al., 1998). In these
condensation stimuli for normal-hearing subjects. There is no patients, described as having auditory neuropathy/dys-
significant latency difference in Wave V latency to rarefaction synchrony, the peak latency does not increase as the inten-
or condensation stimuli (e.g., Stockard et al., 1979). sity of the stimulus is decreased; the first indication that this
At high intensities and for bone-conduction testing, use is not a neural response. When the polarity of the stimulus
of alternating polarity reduces stimulus artifact. Alternating is reversed, the waves also invert, consistent with the char-
polarity stimuli for air-conduction testing, particularly in acteristics of the CM. Present CMs are seen in infants with
the lower frequencies, can be a problem as responses in some no ABR but present otoacoustic emissions (OAEs). CM is
subjects to condensation versus rarefaction stimuli can be also seen in infants with present ABRs which is a normal
out of phase, as described below. Use of insert earphones, observation, providing evidence of intact cochlear and neu-
with an inherent delay of 0.9 ms that separates the stimu- ral function. Comparing separate averages of both rarefac-
lus generation from the time it reaches the ear, results in tion and condensation stimuli will aid in identification of
reduced interference of stimulus artifact with the response. patients with auditory neuropathy/dys-synchrony and, as
Therefore, the need for alternating polarity stimuli may be discussed later, this procedure is now a part of our standard
less of an issue for air-conduction testing. Alternating polar- ABR protocol.
ity stimuli are recommended when using a bone-conduction
transducer where large electrical artifacts from the bone
oscillator are problematic.
$IJSQT
As noted earlier, a click stimulus is theoretically broad in
bandwidth because of its rapid onset. Although clicks stimu-
POLARITY CONSIDERATIONS late broad regions of the cochlear partition, in cases of nor-
When the polarity of a stimulus is reversed, latency shifts in mal hearing or a flat hearing loss, the resulting ABRs are
the peak of the response may be observed. Typically, higher generally attributed to responses from more basal, or higher
frequency tone bursts (e.g., 2,000 or 3,000 Hz and above) frequency, regions of the cochlea. The tonotopic design of
tend to show little or no latency shift with polarity reversals. the cochlea results in temporal delays because basal portions
However, tone bursts centered at lower frequencies, such as are activated earlier in time than more apical regions. These
250 or 500 Hz, can show large latency shifts in some individ- cochlear delays can result in phase cancellations based on
uals that can degrade the waveform and even be out of phase the accumulation of responses from individual neural units
with the opposite polarity (Gorga et al., 1991; Orlando and that contribute to the total ABR (Don and Eggermont, 1978).
Folsom, 1995). Thus, whereas it may seem intuitively desir- Such phase cancellations can have a detrimental effect on the
able to alternate polarity to minimize stimulus artifact, in amplitude of the averaged response of the ABR.
fact the use of alternating tone bursts for lower frequencies Recently, stimuli that are called “chirps” have been
can be detrimental in some cases. applied to ABR testing (e.g., Fobel and Dau, 2004) and,
Consistent with the observation of greater latency dif- more recently, frequency band limited chirps have drawn
ferences between condensation and rarefaction polarity considerable interest as a stimulus for frequency-specific
stimuli for lower frequencies, studies of patients with high- ABR testing (Elberling and Don, 2010). Use of chirp stimuli
CHAPTER 14 Ş "VEJUPSZ#SBJOTUFN3FTQPOTF&TUJNBUJPOPǨ)FBSJOH4FOTJUJWJUZ 255

Stangl et al. (2013) compared physiological response


amplitudes and thresholds for stimuli currently used
in clinical settings (click, tone burst) to broadband and
frequency-specific chirp stimuli (CE-Chirp, octave-band
chirp). ABR Wave V amplitudes were significantly greater
for broadband chirp than click stimuli at 60, 40, and 20 dB
nHL, consistent with previous studies (Kristensen and
Elberling, 2012; Maloff and Hood, 2014). For frequency-
0 2 4 6 8 10
Time in ms specific stimuli, ABR Wave V amplitudes were generally
greater for octave-band chirps than for tone burst stimuli,
FIGURE 14.3 Example of a broadband chirp, plotted though the amplitude differences varied with stimulus
with time on the x-axis and amplitude on the y-axis. frequency and level. An example of an intensity series for
Note that lower frequencies (toward the left) precede a 2,000-Hz octave-band chirp is shown in Figure 14.4.
higher frequencies (toward the right) in time. In this way, Greater differences occurred at higher intensities and no
theoretically, more apical portions of the cochlea are significant differences were found for 500-Hz stimuli.
stimulated earlier than more basal regions, resulting in Higher amplitudes for frequency-specific stimuli have
increased synchronous neural firing. also been reported by Ferm et al. (2013) and Wegner and
Dau (2002).
results in ABRs that theoretically allow simultaneous con- Higher amplitude responses can result in improved
tribution of neural activity from all cochlear frequency signal-to-noise ratios. With similar noise levels and higher
regions. In creating a chirp stimulus, higher frequency com- amplitude responses for chirp stimuli, lower ABR thresh-
ponents contributing to the stimulus are delayed in time rel- olds and better agreement with behavioral thresholds
ative to the lower frequency components (Dau et al., 2000). would be predicted. With the desire to utilize the most
Through this stimulus generation, chirps are designed to efficient and sensitive paradigms in pediatric applications
offset cochlear delays and increase synchronous neural fir- where ABR is used to obtain estimates of hearing sensitiv-
ing, resulting in increased response amplitude (e.g., Fobel ity, frequency-specific chirp stimuli may offer advantages
and Dau, 2004). An example of a chirp stimulus is shown for accurately determining hearing sensitivity and hearing
in Figure 14.3. loss configuration.
Several studies have demonstrated higher ABR ampli-
tude with broadband chirps in comparison to clicks (e.g., RECORDING CONSIDERATIONS
Elberling and Don, 2008; Fobel and Dau, 2004; Maloff and
Hood, 2014). With the need for frequency-specific stimuli
IN ABR THRESHOLD TESTING
in using ABR to estimate hearing sensitivity in pediatric Infants differ from adults in many ways and this includes
populations, frequency-specific chirp stimuli have been characteristics affecting recording of ABRs. For example,
created. A type of frequency-specific chirps, known as differences in head size and shape should be considered in
octave-band chirps, may provide a more sensitive frequency- placing electrodes to obtain optimal responses. Infants have
specific metric through generation of higher amplitude longer ABR wave latencies than adults which translate to
responses and thus lower response thresholds (Elberling and lower frequency content of infant ABRs. Both longer laten-
Don, 2010). Reports are beginning to appear that systemati- cies and lower frequency characteristics require changes in
cally compare broadband and frequency-specific stimuli in the recording window and the filter settings, respectively, to
patients of various ages. be sure to encompass the response of interest.

Octave-band chirp Tone burst


V

60 60
V
V

40 40

V
V
FIGURE 14.4 Examples of ABRs to
octave-band chirps in the left panel
20 20 and tone bursts in the right panel
dB nHL dB nHL centered at 2,000 Hz recorded from
15 ms 15 ms an individual with normal hearing.
256 SECTION II Ş 1IZTJPMPHJDBM1SJODJQMFTBOE.FBTVSFT

&MFDUSPEF.POUBHFT infants, lowering the low-frequency filter setting from 100 to


30 Hz will often enhance the amplitude of infant ABRs
Placement of electrodes at the vertex (Cz) and ears (A1 and (Sininger, 1995; Spivak, 1993).
A2) and recording between vertex and ear (Cz–A1 for the left
side and Cz–A2 for the right side) are optimum for recording
the ABR in most conditions. Waves I–III are more promi- Time Window
nent in ipsilateral recordings whereas Waves IV and V are The recording time window, or analysis time, should be set
better separated in contralateral recordings. Earlobe sites to encompass all components of the response. The duration
tend to result in less muscle potential than mastoid record- of the time window will vary with the age of the patient and
ing sites and greater Wave I amplitude. Use of a noncephalic the intensity and type of stimulus used. For presentation
site (recording from the vertex to the nape of the neck, C7) of click stimuli in adult patients, a time window of 10 to
can enhance the amplitude of Wave V. 12 ms is usually sufficient to record the ABR since Wave V
In infants, the recommended electrode montages differ occurs in normal individuals within 5 to 6 ms of the stimu-
from adults. A contralateral montage (vertex or high fore- lus at high intensities and within 8 ms for intensities near
head to the ear contralateral to the stimulus ear) is not rec- threshold. Use of insert earphones will delay the response by
ommended in infants as the response is poor in newborns in slightly less than 1 ms which is still within this time frame.
this channel. In a comparison of two electrode montages in In infants, however, ABR waves are longer, on the order of
infants, thresholds were lower when recorded from the ver- 1 ms or more; therefore, a time window of at least 15 ms
tex to the nape of the neck (Sininger et al., 2000). Although is recommended when testing patients below 18 months of
amplitude was higher at this location, noise levels were also age or in patients older than 18 months where delays in neu-
higher than for a vertex to mastoid montage. This may be romaturation are suspected.
attributed to proximity of the nape electrode to the torso Whereas a 10- to 15-ms time window is usually suffi-
and additional physiological noise sources. Both electrode cient when presenting click stimuli, ABR testing with tone
montages appear to work well in threshold estimation bursts requires a time window of at least 20 ms. This is par-
application. ticularly true when using 250- or 500-Hz tone bursts where
the stimuli have a longer onset time and activate more apical
portions of the cochlear partition. In practice, when testing
'JMUFS4FUUJOHT low frequencies at low intensities in an immature system, a
When speaking of filtering and filter characteristics related window of 25 ms may be desired.
to the recording of the ABR, one is describing the filter band
through which the physiological response is recorded from
the electrodes. This is distinguished from any filtering of a
0OFWFSTVT5XP$IBOOFM
stimulus transduced through an earphone or bone oscilla- 3FDPSEJOHT
tor. Filtering of the physiological response is used to elimi- Recording two channels simultaneously allows acquisition
nate as much internal noise (e.g., unrelated muscle poten- of both ipsilateral and contralateral (or midline) recordings
tials, general physiological activity) and external electrical simultaneously. In infants, ipsilateral and midline channel
noise (e.g., 60 Hz, other equipment in the environment) as recordings are recommended. For diagnostic testing and
possible. The filters are set to pass the signal of interest, in threshold prediction there are several reasons to obtain two-
this case the ABR. channel recordings that include:
Changes in the frequency band through which the
physiological response is filtered affect waveform latency 1. To monitor the ear that was stimulated by the amplitude
and amplitude. Changing the filter so that there is more of the artifact in the response and the position of the
high-frequency information in the biologic signal generally trace containing Wave I.
decreases the latency of the response. Allowing more low- 2. To determine the presence and location of the CM and
frequency information into the average typically results in Wave I by comparison to a contralateral recording. The
more rounded peaks and longer latencies. Interference from CM and Wave I should not be present, or be diminished,
electrical sources and muscle activity increases as more low in the contralateral tracing.
frequencies are included. Wave V amplitude may increase 3. To obtain better definition of Waves IV and V since they
because it is dependent on the amount of low-frequency tend to be more separated in contralateral recordings.
energy included because of the low-frequency components
of Wave V. Use of very narrow filters and steep filter slopes is Number of Averages and Noise
discouraged because phase shifting may occur in frequency
regions near the cutoff frequencies.
2VBOUJǨJDBUJPO
As noted earlier, infant ABRs have longer latencies and The number of averages required varies according to the
contain more lower frequency energy. Therefore, when testing inherent amplitude of the evoked potential and the amount
CHAPTER 14 Ş "VEJUPSZ#SBJOTUFN3FTQPOTF&TUJNBUJPOPǨ)FBSJOH4FOTJUJWJUZ 257

of background noise that includes muscle artifact, 60-Hz Amplitude of the ABR also changes with age. Peak
noise, and EEG activity. For the ABR, usually 1,000 to 2,000 amplitudes (typically measured from the peak to the fol-
sweeps are used to obtain clear responses in quiet patients lowing negative trough) increase over the first 1 to 2 years of
when using higher intensity stimuli. At lower intensities life (e.g., Salamy, 1984). In infants, the amplitude of Waves I
where the response is lower in amplitude and in cases where and/or III may be greater than Wave V, which is in contrast
patients are more active and noisier, more averages may be to higher Wave V amplitude in adults. This changes to more
necessary because of the reduced signal-to-noise ratio. adult-like patterns over the first few years of life.
Use of objective estimates of the signal-to-noise ratio,
such as Fsp, based on the F-ratio statistic, is very helpful in
determining when a sufficient number of responses have
Gender
been averaged (Don et al., 1984). Using methods such as Females tend to have shorter latency and higher amplitude
Fsp can allow, in an objective manner, for averaging of fewer ABRs than males. Wave V latency averages about 0.2 ms
responses at higher stimulus intensity levels where the shorter in females, and amplitude is higher in females, par-
response has high relative amplitude whereas more responses ticularly for Waves IV, V, VI, and VII. Females may also show
can be averaged to improve accuracy for low intensity stimuli shorter interwave latencies than males. It has been suggested
(i.e., close to response threshold) where the ABR amplitude that the source of the differences in latency and amplitude
is low. Point-optimized variance ratio (POVR) is another in the ABR between males and females may be related to
statistically based signal and noise estimation method, the observation that cochlear response times are shorter in
which is implemented in a newborn hearing screening sys- females than males (Don et al., 1994).
tem (Sininger, 1993). In addition to requiring fewer averages,
these methods reduce the need to replicate the response and PROTOCOLS AND PROCEDURES
provide objective estimate of response presence.
'031&%*"53*$1"5*&/54
A pediatric test protocol includes multiple measures to pro-
SUBJECT CONSIDERATIONS IN vide a cross-check among results and to maximize efficiency
ABR THRESHOLD TESTING (e.g., Gravel and Hood, 1999). The combination of middle-
ear measures that includes immittance and middle-ear
Age muscle reflexes, OAEs, and ABR provides a comprehensive
The ABR changes as a function of age, particularly dur- view of middle-ear, cochlear, and peripheral neural func-
ing the first 12 to 18 months of life, as the auditory neu- tion (Berlin and Hood, 2009). Once it is possible to obtain
ral system continues to mature. These changes have been reliable behavioral information, at around 6 months of age
attributed to continuing myelination of the auditory path- in typically developing children, a combination of physi-
way after birth. Characteristics of ABRs obtained in prema- ological and behavioral test results provides important test
ture and term infants vary from each other and from those cross-checks.
obtained in adults (e.g., Hecox and Galambos, 1974; Salamy, Our pediatric protocol utilizes a combination of mea-
1984). Reliable ABR components for 65-dB nHL clicks have sures, as described in Table 14.1. We measure either tran-
been reported in newborns of approximately 28 weeks ges- sient (TEOAE) or distortion product (DPOAE) otoacoustic
tational age (Starr et al., 1977). Waves I, III, and V are most emissions, tympanograms using a 1,000-Hz carrier tone,
visible in infant recordings and the normal Wave V abso- and a minimum of ipsilateral middle-ear muscle reflexes at
lute latency for click stimuli in a newborn approximates 1,000 and 2,000 Hz. We recommend completing these tests
7.0 ms at 60 dB nHL. Responses obtained from infants 12 to prior to the ABR, as pressure may change in the middle ear
18 months and older should resemble those acquired from over the course of a deep sleep or sedation period and this
adults (Hecox and Galambos, 1974). can affect accurate assessment and interpretation of OAEs
Wave I may be prolonged in infants, but generally not and middle-ear tests. All air-conduction testing is com-
as much as Wave V, generating longer interwave latencies on pleted in each ear individually.
the order of 5.0 ms compared to 4.0 ms in adults (Hecox
and Galambos, 1974; Starr et al., 1977). This may be related
to cochlear maturation, neuronal maturation, reduced effi-
"QQSPBDIFT
ciency in external and/or middle-ear sound transmission, For ABR testing, one can complete all ABR testing with tone
and occasionally collapsing ear canals. Neural maturation bursts or can use tone bursts in combination with a brief
of the auditory system is complex with conduction time neural integrity screening that uses a click stimulus. It must
adult-like by term birth, pathway lengthening continuing be emphasized that click stimuli in pediatric testing are not
to mature until about age 3 years, and different aspects of used for threshold prediction; clicks are only used to estab-
myelin development contributing to changes in ABRs in lish the presence of neural synchrony. Thus clicks are only
infants (Moore et al., 1996). briefly included and are presented at a moderate to high
258 SECTION II Ş 1IZTJPMPHJDBM1SJODJQMFTBOE.FBTVSFT

TA B LE 14 .1 /FVSBM*OUFHSJUZ
Suggested Tone Burst ABR Test Parameters To test neural integrity, we present clicks at a single high
intensity (e.g., 75 dB nHL or higher if there is no response
Parameter Comments at 75 dB nHL) using both condensation and rarefaction
Stimulus polarity, presented or collected separately, so that results can
Type Tone burst be compared to differentiate the CM from neural response
Polarity Condensation for AC, alternating components. The CM (which will reverse in phase as the
for BC stimulus does) is distinguished from Wave I of the ABR
Intensity Begin at 75 dB nHL, decrease in (which will not show a phase reversal with clicks). It is
20-dB steps, refine to 10-dB steps emphasized that testing with click stimuli is completed only
Rate 27.7/s; 39.1/s for 500 Hz at a single high intensity as a method of checking neural
Transducer Earphone, bone oscillator response integrity. When it is documented that an ABR is
Recording present, then testing proceeds immediately to tone bursts
Time window 20–30 ms to obtain estimations of frequency-specific thresholds.
Filter band High pass 30 or 100 Hz; Low pass Figure 14.5 shows examples of an infant with good neural
1,500 or 3,000 Hz synchrony and an infant with poor neural synchrony. The
Number of 1,500–2,000 at high intensities, infant with poor neural synchrony was found to have audi-
sweeps more sweeps nearer threshold tory neuropathy/dys-synchrony.
Electrode Noninverting at vertex or high
montage forehead; inverting at mastoid or "#3TUP"JS$POEVDUFE5POF
earlobe; second channel recom-
mended with inverting electrode
#VSTU4UJNVMJ
at nape A key in ABR testing for threshold estimation involves using
Subject well-defined frequency-specific stimuli. Typical stimulus
State Sleeping, resting quietly, sedated durations utilize a minimum of two cycles rise and fall times
for older infants (Davis et al., 1985; Gorga et al., 1988), which provide both
sufficient frequency specificity and neural synchrony. We
prefer condensation polarity tone bursts as these provide
intensity where responses to rarefaction and condensation higher Wave V amplitude in the majority of individuals. We
polarity stimuli are compared. If responses are present to do not recommend using alternating polarity signals (unless
clicks, then testing proceeds immediately to determine the each polarity is separately averaged), particularly in the
response thresholds for tone bursts. lower frequencies (Orlando and Folsom, 1995). Suggested
When the ABR protocol utilizes tone bursts for all tone burst ABR parameters are shown in Table 14.2.
aspects of testing, then testing begins with tone bursts. Click Four frequencies are tested in each ear: 500, 1,000,
stimuli may be used later in the test sequence if there is any 2,000, and 4,000 Hz. The test order is 2,000, 500, 1,000, and
question about the integrity of the tone burst responses that 4,000 Hz if OAEs are present at all frequencies. This order
might suggest a neural synchrony problem and possible was determined based on obtaining key information for
auditory neuropathy/dys-synchrony. management of and monitoring hearing loss along with the

GOOD neural synchrony, ABR POOR neural synchrony, only


preceded by cochlear microphonic cochlear microphonic present

FIGURE 14.5 A patient demonstrating good neural synchrony is


shown in the left panel where the recording contains a CM at the
beginning of the response and Waves I, III, and V of the ABR, with good
replication. The patient depicted in the right panel has poor neural
synchrony and the tracing only shows the reversing CM with no ABR
present. Two tracings with condensation clicks and one tracing with
rarefaction clicks are shown in each panel.
CHAPTER 14 Ş "VEJUPSZ#SBJOTUFN3FTQPOTF&TUJNBUJPOPǨ)FBSJOH4FOTJUJWJUZ 259

active). However, if insertion of an earphone in the opposite


TA B LE 14 . 2
ear would result in awakening a sleeping baby, then testing is
Suggested Test Protocol for ABR completed in one ear before testing the opposite ear.
Threshold Testing Testing typically begins at a reasonably high intensity,
such as 75 dB nHL, or at a level where a response is likely to
1SPDFEVSF Comments be present based on history, observation, and so on. Inten-
Otoacoustic emissions sity is then increased or decreased by 20-dB steps with rep-
TEOAE or Assess aspects of cochlear lications at each level until no response is obtained. If there
DPOAE function, compare to ABR to is no response at 75 dB nHL, then the stimulus intensity
identify AN/AD is increased. Each of these responses is obtained twice to
For DPOAE, test at 2, 3, 4 kHz judge replicability and assist in determination of threshold.
with pass criteria of responses Once the threshold range has been bracketed, the step size
>0 dB SPL and at least 6 dB is decreased to 10-dB steps. Intensity is lowered until Wave
SNR for all three frequencies V disappears or a response is observed within the predicted
Middle-ear measures normal range. If the patient is quiet and we predict that suf-
Tympanogram For infants <7 months, use probe ficient time will be available to complete all parts of the test
tone >660 Hz battery, then the intensity level is increased 10 dB to deter-
Middle-ear Minimally screen at 1 and 2 kHz; mine the presence of a response at an intermediary level. For
muscle must be present at normal lev- example, if responses are obtained at 75, 55, and 35 dB nHL,
reflex els for both frequencies to pass but no response is observed at 15 dB nHL, then stimuli are
Checking neural Condensation and rarefaction presented at 25 dB nHL. At higher intensities where response
integrity clicks at 75 dB nHL amplitudes are higher and thus more easily seen over the
Conduct two runs with condensa- noise, fewer sweeps, such as 1,000 or 1,500, may be sufficient.
tion polarity and at least one Closer to threshold, averaging of more than 2,000 responses
run with rarefaction polarity. If may be necessary.
ABR obtained, proceed to tone Lower frequency tone bursts are typically more difficult
burst testing to discern as they generally do not have the familiar five- to
If no response, increase intensity seven-wave complex associated with ABRs to clicks or higher
If no response persists, clamp frequency stimuli. For 500-Hz tone burst ABRs, we adjust
earphone tube to distinguish the filters to 30 to 1,500 Hz to accommodate lower frequency
stimulus artifact physiological activity. Tone bursts with 4-ms (two cycles) rise
and fall times, Blackman envelopes, and either condensation
Threshold prediction
or rarefaction polarity are typically used. The time window
Tone burst Test order: 2,000, 500, 1,000,
is extended to 20 or 25 ms since these responses have longer
stimuli 4,000 Hz unless OAEs absent
latencies than responses to clicks. Tone bursts centered at 500
at 4,000 Hz; then test 4,000 Hz
Hz are presented at a rate near 40 per second (we use 39.1 per
before 1,000 Hz
Air conduction Increase or decrease intensity in
second) to each ear individually beginning at 75 dB nHL and
20-dB steps, then refining to
then decreasing in 20-dB steps until no response is obtained,
10-dB steps
with the 10-dB step filled in if time allows. If there is no
Bone conduc- Alternating polarity; care in response at 75 dB nHL, then the stimulus intensity is increased.
tion placement of bone oscillator When interpreting the responses obtained to 500-Hz
tone bursts, we look for a single replicable peak that repre-
sents Wave V of the ABR. We generally observe a single peak
additional consideration that testing at all frequencies may that may have a sinusoidal overlay at high intensities. The
not be possible if a patient wakes up prior to test comple- latencies obtained range from 8 to 10 ms for high-intensity
tion. If no OAE energy is present above 2,000 Hz, the order stimuli to 14 to 16 ms nearer threshold (Gorga et al., 1988).
of the tone burst center frequencies is 2,000, 500, 4,000, In infants, these latencies may be even longer. In our expe-
and 1,000 Hz to acquire higher frequency information at rience, ABR thresholds to 500-Hz tone bursts obtained
4,000 Hz that could be useful in monitoring possible high- from normal-hearing individuals using the test parameters
frequency progressive hearing loss. The ideal approach is to described here are generally between 25 and 35 dB nHL.
assess each frequency in each ear and alternate between ears
for each frequency (e.g., 2,000 Hz in the right then the left
ear). This approach allows the opportunity to obtain at least
"#3UP#POF$POEVDUFE4UJNVMJ
some information from each ear in the event that the entire When responses to air-conducted auditory stimuli are
test sequence cannot be completed (i.e., infant becomes too seen at predicted normal threshold levels, there is no need
260 SECTION II Ş 1IZTJPMPHJDBM1SJODJQMFTBOE.FBTVSFT

to obtain bone-conducted responses, as is true in behav- 3FMBUJPOPǨ"#35ISFTIPMETUP


ioral audiometry. However, when tone burst responses are
not present at predicted normal levels, then ABRs should
#FIBWJPSBM5ISFTIPMET
be completed using bone-conducted stimuli. Criteria for In the final step for predicting behavioral thresholds, the
obtaining bone-conduction thresholds are (1) if any of threshold of the ABR (i.e., the lowest level where a physiologi-
the air-conduction thresholds were not within the normal cal response is obtained) is adjusted to relate the physiologi-
range; (2) if OAEs, immittance, or reflexes are abnormal; or cal (ABR) thresholds to behavioral puretone thresholds. This
(3) for subsequent visits, if there is a reason to believe there information is helpful in planning management, fitting ampli-
has been a sensory change. fication, counseling, and reporting results. The term “estimated
The test parameters used are the same as those for air- hearing level” (eHL) is used (e.g., Bagatto et al., 2005). In the
conducted stimuli except that alternating polarity is used to case studies presented later in this chapter data are used from
reduce the electrical artifact emitted from the bone oscil- the Ontario Infant Hearing Program (OIHP) in Canada where
lator. Tone bursts are presented at progressively decreasing adjustments are 20 dB at 500 Hz, 15 dB at 1,000 Hz, 10 dB at
intensities via bone conduction to determine whether there 2,000 Hz, and 5 dB at 4,000 Hz.
is a discrepancy in intensity levels at which responses are The eHL values used in the OIHP as well as grossly
obtained between air- and bone-conduction stimuli. If such similar corrections that are used in other programs were
a discrepancy does exist, this suggests the presence of an air– derived from studies that directly compared ABR thresholds
bone gap and a conductive or mixed hearing loss. and behavioral thresholds in the same subjects. An excellent
Care must be taken in the placement of the bone oscilla- study by Stapells et al. (1995) recorded ABR thresholds to air-
tor in infants to assure appropriate response amplitude and conducted stimuli in infants and children with normal hear-
test accuracy. Oscillator placement in infants should be at the ing and various degrees of hearing losses. Relationships
mastoid since stimuli from the bone oscillator are conducted between ABR and behavioral thresholds were approximately
across the scalp less efficiently in infants than in adults. Stuart linear across a relatively wide range of intensities (20 to about
et al. (1994) demonstrated that bone oscillator placement in 90 dB nHL). Across the subject dataset, ABR thresholds aver-
infants has a significant effect on Wave V amplitude. Place- aged (with rounding to the nearest 5 dB) 15, 5, and 0 dB above
ment of the oscillator directly behind the ear canal is recom- behavioral thresholds at 500, 2,000 and 4,000 Hz, respec-
mended as placements higher on the mastoid result in lower tively. In another study, Stapells (2000) reviewed studies
amplitude. Coupling of the bone oscillator also takes special meeting test criteria and containing data for ABR and behav-
consideration. The procedure described by Yang and Stuart ioral thresholds. Although some differences existed among
(1990) provides an excellent method. They recommend cou- studies included in this meta-analysis, based on techniques
pling the bone oscillator using an elastic headband held in and calibrations, data were available for infants, children, and
place by a Velcro closure that can be adjusted. The tension of adults with normal hearing and with SNHL. Results of this
the headband can be adjusted to a recommended coupling analysis indicated overall approximate differences of 15, 10,
force of 400 to 450 g using a spring scale. 5, and 0 dB for 500, 1,000, 2,000, and 4,000 Hz, respectively,
The dynamic range for bone-conducted stimuli is though there was variation between children and adults and
different than that for air-conducted stimuli, as is true in between those with normal hearing and with SNHL.
audiometric applications. The dynamic range typically does
not exceed 50 to 60 dB and the relationship between the out-
put of the oscillator and the “dial reading” on the equipment
ADDITIONAL CONSIDERATIONS
may vary with different instruments. Stimuli are presented .BYJNJ[JOH"#35FTU"DDVSBDZ
beginning at the highest output level and then decreasing in
20-dB steps as in the other tests. Responses are first obtained
BOE&ǨǨJDJFODZ
without masking and then, if response thresholds are better There are modifications of ABR procedures that can be used
than those obtained by air conduction and/or there is an to improve test efficiency and decrease test time. This is partic-
asymmetry between ears, masking is used. ularly important since, when sedation is used, there is a finite
Because the output in bone conduction is limited, the time period during which a patient will be asleep and, thus, a
responses obtained by bone conduction will rarely show the limited amount of time to obtain all necessary information.
familiar five-wave complex seen at high intensities in stan- Picton (1978) recommended the use of faster stimulus
dard air conduction ABRs. Responses will resemble those presentation rates to reduce test time. He suggested the use
obtained with air-conducted clicks in the threshold-to-50 or of a slow rate at a relatively high intensity for accurate iden-
60 dB nHL range. The latency of waves may vary slightly from tification of the latencies of Waves I, III, and V. Then, when
those acquired by air conduction based on slight spectral dif- in the threshold-seeking mode of testing, stimuli can be pre-
ferences among bone-conduction transducers. However, sented at rates on the order of 50 to 70 clicks per second,
since the primary goal in bone-conduction testing in infants or faster. Although Wave V latency is prolonged, the ampli-
is determination of ABR threshold, this is rarely an issue. tude of Wave V in normal adults is not reduced as much as
CHAPTER 14 Ş "VEJUPSZ#SBJOTUFN3FTQPOTF&TUJNBUJPOPǨ)FBSJOH4FOTJUJWJUZ 261

earlier components, making acquisition of responses near /FVSBM"COPSNBMJUJFT


threshold possible. Slower rates at all levels are indicated if
the response disappears when stimulus rate is increased. Measuring AEPs requires an intact neural system. Thus,
Other methods use very high stimulus rates (on the abnormalities that can affect the neural system must be con-
order of 500 to 1,000 stimuli per second) with random- sidered in interpreting test results. For example, in the presence
ized presentation sequences, known as maximum length of hydrocephalus, the ABR can be obliterated despite normal
sequences (MLS; e.g., Picton et al., 1992) and continu- hearing (Kraus et al., 1984). Patients with auditory neuropathy/
ous loop averaging deconvolution (CLAD; Delgado and auditory dys-synchrony (AN/AD) are characterized by absent
Özdamar, 2004). Presentation of different sequences to each or highly abnormal ABRs and present OAEs (Starr et al.,
ear allows testing of both ears simultaneously which, when 1996). Thus, it is particularly important to obtain OAEs in
coupled with fast presentation rates, could decrease overall patients who fail to show an ABR at any intensity. Presence of
test time. Limitations in testing immature or compromised an ABR at high intensities but not to lower intensity stimuli is
systems at very high rates and noise levels need to be consid- consistent with a peripheral hearing loss. Absence of an ABR
ered. Caution should be exercised when testing in infants as to high and low intensities may mean either a more severe
responses to faster rates may result in decreased amplitude. peripheral hearing loss or a neural disorder. OAEs are useful
In cases where no or poor responses are obtained at high in distinguishing these two groups and therefore we always
rates, testing with slower rates should follow. obtain OAEs in patients who fail to show an ABR response.

5FTU1SPUPDPMǨPS0MEFS$IJMESFO 4VCKFDU/PJTF
BOE"EVMUT Improper subject preparation can result in noisy or difficult-
to-interpret recordings. Poor electrode impedance or dis-
The test protocol used for older children, over approxi-
similar impedances among electrodes may yield poorly
mately 8 to 10 years of age who are not sedated, and adults
defined, difficult-to-interpret responses. Subjects who are
may vary from that used for infants and young children.
fussy or tense or placed in an uncomfortable position may
Frequency-specific stimuli remain necessary to adequately
produce excessive muscle artifact.
complete threshold estimation; however, there are addi-
tional paradigms in which tone bursts can be presented.
For example, 40-Hz ASSR techniques may be added to tone $PMMBQTJOH&BS$BOBMT
burst ABR and other ASSR methods (see Chapters 15 and Ear canal collapse or earphone slippage can reduce sig-
17). Although the 40-Hz response has not been found useful nal intensity at the ear without the examiner’s knowledge.
in young patients, it is quite useful in older patients for esti- We always use insert earphones to avoid the possibility of
mating auditory function using frequency-specific stimuli collapsing ear canals, a common problem in infants when
(Stapells et al., 1984). using supra-aural earphones. Insert earphones are also
more comfortable which may enhance the patient’s state of
6TFPǨ.BTLJOH relaxation or sleep.
When using tone bursts or tone pips, as with other stim-
uli, masking should be used when sensitivity differences .JEEMF&BS'VODUJPO
between ears could create crossover of sound to the nontest Part of our test battery always includes middle-ear immit-
ear. With insert earphones the intensities where crossover tance and middle-ear muscle reflexes as well as OAEs. If
occurs during air-conduction testing is higher than with a patient requires sedation (as in the case of infants over
supra-aural earphones. The bandwidth of the masking about 4 to 5 months of age and young children) or sleeps
stimulus should be sufficiently wide to encompass the tone deeply, then it is important to obtain these measures before
burst stimulus being used. The masking stimulus can be doing the ABR. During sedated or natural deep sleep, posi-
generated via sources other than the ABR equipment, such tive pressure may build up in the middle ears that will com-
as an audiometer, as long as effective masking levels for the promise the results of middle-ear measures and OAEs if
tone burst stimuli are established. completed at the end of testing.

CAUTIONS AND 5IF"#3*T/PUB)FBSJOH5FTU


CONSIDERATIONS Finally, it is always important to remember that the ABR
There are a number of factors to keep in mind to assure and other AEPs are not hearing tests. In those patients who
accurate recording of ABRs and correct interpretation of do not have good neural synchrony, other means of estimat-
results. Some of the many factors that we consider when ing auditory function must be sought. In addition, pass-
using ABR to predict threshold sensitivity are the following. ing an ABR as an infant does not preclude the possibility
262 SECTION II Ş 1IZTJPMPHJDBM1SJODJQMFTBOE.FBTVSFT

of acquired or later onset hereditary hearing loss. Thus, in cochlear hair cell and peripheral neural function. On behav-
reporting test results, we always inform parents and referral ioral measures, patients with AN/AD show puretone thresh-
sources of the importance of monitoring a child’s speech olds ranging from normal sensitivity to the severe or profound
and language development and observing a child’s responses hearing loss range (e.g., Berlin et al., 1993; Starr et al., 1996).
to his/her auditory environment. If a child fails to develop Speech recognition is variable across individual patients in
speech and language, parents are advised to seek appropri- quiet and generally poorer than expected with ipsilateral com-
ate evaluation and management. peting stimuli (e.g., babble, noise) in all patients with AN/AD.
In infants and young children, ABR is used as the
 "6%*503:/&6301"5): definitive measure in determining AN/AD. ABRs are typi-
cally absent in patients with AN/AD, although some patients
"6%*503:%:44:/$)30/: demonstrate small responses for high-level stimuli. In the
The term auditory neuropathy/auditory dys-synchrony (AN/ germinal paper defining auditory neuropathy, Starr et al.
AD), also referred to as auditory neuropathy spectrum dis- (1996) reported absent ABRs in 9 of 10 patients (aged 4 to
order (ANSD), describes patients who demonstrate intact 49 years) and the 10th patient had an abnormal ABR char-
outer hair cell function/active cochlear processes shown by acterized by Wave V responses only to high-intensity stimuli.
OAEs and/or CMs and poor VIII nerve/brainstem responses The Berlin et al. (2010) review of ABR data for 186 patients
as a consequence of disturbed input from the inner hair cells, with AN/AD ranging in age from infants through adults
abnormal synaptic function, or peripheral neural pathol- indicated that 138 (74%) patients had absent ABRs whereas
ogy (Berlin et al., 1993; Starr et al., 1991, 1996). Further 48 (26%) showed abnormal responses characterized by pres-
evidence of effects on neural function are demonstrated by ence of low-amplitude Wave V only at high stimulus levels
generally absent or sometimes elevated middle-ear muscle of 75 to 90 dB nHL. This distribution of responses is very
reflexes (Berlin et al., 2005) and abnormal medial olivoco- similar to that reported by Starr et al. (2000) for 52 patients
chlear reflexes, measured via efferent stimulation effects on where 73% had no ABR and 27% had abnormal responses.
OAEs (Hood et al., 2003). Most AN/AD patients show bilat- The absence or abnormality of all components of the
eral symptoms, though function may be asymmetric between ABR including Wave I suggests that the most distal portions
ears, and cases of unilateral AN/AD have been documented. of the VIII nerve are affected, either directly or indirectly,
Despite fairly similar findings from current physiologi- in AN/AD. This characteristic distinguishes AN/AD from
cal measures, there is considerable variation in characteris- space-occupying lesions affecting the VIII nerve, where
tics and functional communication abilities across patients Wave I of the ABR may be seen in recordings obtained with
(e.g., Berlin et al., 2010; Starr et al., 2000). Clinical presenta- surface electrodes. Results of radiologic (MRI and CT) eval-
tion typically, but not always, includes difficulty listening in uation are characteristically normal in AN/AD patients.
noise, may include fluctuation in hearing ability, and, in the Several distinct differences exist between cochlear
case of infants and children, most often involves delayed or responses, such as the CM, and neural responses, such as
impaired development of speech and language. AN/AD may the ABR. These responses can be distinguished by using
or may not be accompanied by neural problems in other appropriate recording methods. The most direct method
systems. Patients with AN/AD typically demonstrate timing of separating the CM and ABR is to compare responses
problems (Zeng et al., 1999), which suggest a disturbance obtained with rarefaction polarity stimuli to those obtained
in neural synchrony. This variation impacts both evaluation with condensation stimuli. CM follows the characteristics of
and management of AN/AD. the external stimulus; thus, the direction of the CM reverses
Estimates of the incidence of AN/AD suggest that it with a change in polarity of the stimulus. For higher fre-
occurs at a rate of about 10% in those individuals who have quency stimuli and clicks, neural responses such as the ABR
a dys-synchronous ABR (see Figure 14.5 for an example of in normal individuals may show slight latency shifts with
poor synchrony) or an ABR result consistent with a severe or polarity changes but do not invert. Therefore, cochlear and
profound estimate of hearing sensitivity. This rate is based neural components can be distinguished based on whether
on evidence from studies of school-aged children with or not the peaks invert with reversing stimulus polarity.
severe–profound hearing losses (e.g., Berlin et al., 2000) and Refer to Figure 14.5 that shows ABRs obtained to both con-
infant populations (e.g., Rance et al., 1999; Sininger, 2002). densation and rarefaction polarity stimuli. In the left panel,
Some studies and populations report higher incidence the CM inverts at the beginning of the tracing whereas the
of AN/AD. For example, in the NICU, Berg et al. (2005) ABR (neural response) does not invert. In AN/AD, the entire
observed that about 24% of 477 infants failed their ABR in response inverts with polarity changes confirming that it is
one or both ears, while passing OAEs bilaterally. To detect completely CM and not ABR activity.
AN/AD in newborns, hearing screening must include ABR. An important consideration in evaluating ABRs in new-
If only OAEs are tested, then AN/AD will be overlooked. borns and infants is neuromaturation of the ABR after birth
Clinical findings in patients with an AN/AD are most that continues through 12 to 18 months of age. Although
accurately described with physiological measures that assess the ABR is typically present at birth, it is possible that factors
CHAPTER 14 Ş "VEJUPSZ#SBJOTUFN3FTQPOTF&TUJNBUJPOPǨ)FBSJOH4FOTJUJWJUZ 263

such as premature birth, risk factors, or other trauma sur-


Left ear Right ear
rounding birth may delay development of synchronous V
I III V 4kHz
neural responses. More information is needed to adequately
understand the reasons for poor synchrony and the fac- 50 V
V
tors that may contribute to later development of the ABR 20
in some infants who initially present with the signs of AN/
2kHz I III V
AD. At present, estimates of the number of newborn infants I III V
who present with dys-synchronous ABRs and later develop 60 V
V
a normal ABR are unclear. In the meantime, it is important 40 V
to closely monitor infants over the first year of life both with 30
ABR and with other indices of auditory development, con-
tinually modifying management plans as needed. 0.5 kHz I
V III V
I III
CASE STUDIES 60
I III
V V
Two case studies are shown here to exemplify the use of tone 40
bursts in ABR testing. Responses to tone bursts centered
30
at frequencies ranging from 500 to 4,000 Hz, as described
in this chapter, provide the information needed to make
predictions about the degree and configuration of hear- FIGURE 14.6 ABRs obtained for tone bursts centered
ing thresholds. When predicted thresholds are not normal, at 500, 2,000, and 4,000 Hz for the pediatric patient
sufficient information is obtained to proceed directly with described in case study 1. The time window for all
responses is 20 ms.
appropriate management.
nHL in each ear for tone bursts centered at 2,000 Hz, and
$BTF4UVEZ/PSNBM)FBSJOH 20 dB nHL in each ear for tone bursts centered at 4,000 Hz.
Case study 1 is an 18-month-old female who was referred Correction factors, based on the Ontario program guide-
for testing based on delayed speech and language develop- lines, were used to obtain estimated hearing levels. Predicted
ment. Development was otherwise normal. There was his- thresholds for all frequencies were within normal limits for
tory of hyperbilirubinemia and the possibility of AN/AD both ears. Therefore, test results ruled out AN/AD and also
was considered, prompting the recommendation of an ABR. suggested that peripheral hearing loss was not a factor in
Middle-ear tests and OAEs were within the normal this child’s speech and language delay. This child and her
range for each ear. Following a check for neural synchrony, family were referred for speech/language intervention.
as described above, in each ear, tone burst ABRs were com-
pleted. Testing began with tone bursts centered at 2,000 Hz, $BTF4UVEZ.PEFSBUF
followed by 500 Hz and 4,000 Hz. Testing of tone bursts
centered at 1,000 Hz was not completed because of patient
Hearing Loss
restlessness. However, with information in both ears at three Case study 2 is a 2-year-old male who was referred for test-
frequencies, sufficient information was available to make ing based on a history of middle-ear problems and a family
threshold predictions. history of hearing loss. Parents were concerned with speech
Replicated responses were obtained at several intensity and language development and lack of responses to sound
levels for each tone burst stimulus. Not all responses are in some situations. Development was otherwise normal.
shown; rather those used to determine response threshold Middle-ear tests were within the normal range for each
are displayed. As shown in Figure 14.6 and in Table 14.3, ear at the time of ABR testing. OAEs were absent in both
ABR threshold was 40 and 30 dB nHL for the left and right ears. Following a check for neural synchrony, as described
ears, respectively, for tone bursts centered at 500 Hz, 30 dB above, in each ear, tone burst ABRs were completed. Testing

TABL E 14.3

Case Study 1: Normal Hearing


- - - 3 3 3
dB nHL 40 30 20 30 30 20
Correction 20 10 5 20 10 5
dB eHL 20 20 15 10 20 15
264 SECTION II Ş 1IZTJPMPHJDBM1SJODJQMFTBOE.FBTVSFT

Left ear Right ear  46.."3:


4 kHz I III V
I III V A number of considerations to increase accuracy and effi-
60
ciency of the ABR in pediatric threshold prediction have
50
been presented through discussion of normal characteris-
40
tics, considerations in improving test sensitivity and accu-
2 kHz V III V racy, and in the context of a clinical test protocol. Use of
I III V
70 a test battery and cross-check principles is important in
60 all assessments. History, physiological, and behavioral test
50 results need to make sense (agree). Efficiency is needed in
minimizing time and prioritizing information. It is impor-
1 kHz
V 60 tant to use strict criteria and technically correct methods in
V both physiological and behavioral testing. Finally, whereas
50
the ABR is not a hearing test per se, the information related
40 to auditory function and hearing threshold sensitivity
V 0.5 kHz V obtained from physiological measures can and should be
50 used in implementing management programs.
40 There is no dispute that the ABR is an objective, indirect
method of estimating hearing sensitivity based on the presence
FIGURE 14.7 ABRs obtained for tone bursts centered of responses at various intensity levels. This is particularly valu-
at 500, 1,000, 2,000, and 4,000 Hz for the pediatric able in infants and young children. Ear-specific and frequency-
patient described in case study 2. The time window for specific information can be obtained and directly applied to
all responses is 20 ms. management of identified hearing losses. Using ABR in esti-
mating hearing sensitivity can be challenging in assuring accu-
began with tone bursts centered at 2,000 Hz, followed by racy of responses while also obtaining the needed information
500, 1,000, and 4,000 Hz. in a timely manner, a necessity in pediatric patients. Key goals
Replicated responses were obtained at several intensity include maximizing the signal, in this case the amplitude of
levels for each tone burst stimulus. As with the previous case the ABR, while controlling and minimizing noise as much as
presented, not all responses are shown; rather those used to possible. Although the ABR is well established as a method of
determine response threshold are displayed. As shown in predicting hearing thresholds, areas remain for investigation
Figure 14.7 and in Table 14.4, ABR threshold was 50 dB nHL and refinement. Such areas include refinement of stimuli and
in each ear for tone bursts centered at 500 Hz, 50 dB nHL in stimulus paradigms, accurate calibration of signals in infants
each ear for tone bursts centered at 1,000 Hz, 60 dB nHL for (e.g., Lightfoot et al., 2007), methods of accurately assessing
each ear for tone bursts centered at 2,000 Hz, and 50 dB nHL and controlling noise levels, and removing subjectivity from
in each ear for tone bursts centered at 4,000 Hz. Correction determination of response presence.
factors, based on the Ontario program guidelines, were used
to obtain estimated hearing levels. Predicted air-conduction
thresholds were consistent with a mild-to-moderate hear-
'00%'035)06()5
ing loss bilaterally. Because air-conduction thresholds were 1. What do you think is the “most ideal” stimulus or stimu-
not normal, bone-conduction ABRs were completed using lus set for predicting hearing thresholds in infants and
alternating polarity tone bursts. Bone-conduction ABR young children? Consider the current state of the art,
thresholds were similar to air-conduction thresholds, con- what you want to know when testing an infant, the char-
sistent with a sensory/neural hearing loss. Based on the air- acteristics of an auditory system that is still maturing,
and bone-conduction test results, this child and his family and what might yield the most accurate information.
were referred for speech/language intervention and man- 2. Noise is an issue in evoked potential testing, as electrodes
agement with amplification. cannot select the response from the noise. Several methods

TA BL E 14 . 4

Case Study 2: Moderate SN Hearing Loss


- - - - 3 3 3 3
dB nHL 50 50 60 50 50 50 60 50
Correction 20 15 10 5 20 15 10 5
dB eHL 30 35 50 45 30 35 50 45
CHAPTER 14 Ş "VEJUPSZ#SBJOTUFN3FTQPOTF&TUJNBUJPOPǨ)FBSJOH4FOTJUJWJUZ 265

hold promise for providing specific information about Delgado RE, Özdamar Ö. (2004) Deconvolution of evoked
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