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PHYSIOLOGIC AND BEHAVIORAL APPROACHES TO PEDIATRIC HEARING ASSESSMENT
HEARING LOSS IN CHILDREN
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PHYSIOLOGIC AND BEHAVIORAL APPROACHES TO PEDIATRIC HEARING ASSESSMENT Richard C. Folsom, PhD, and Allan 0. Diefendorf, PhD
The primary objective of detecting hearing loss in children as early as possible is that appropriate intervention(s) can be initiated in a timely fashion. Therefore, infants and young children referred from hearing screening programs must be followed up immediately and receive a comprehensive audiologic evaluation to confirm the presence of hearing loss and establish the magnitude, type, configuration, and symmetry of the hearing loss. Improved assessment procedures for infants and young children have meant greater precision in quantifying hearing losses at an early age, in turn facilitating achievement of this objective. Two approaches are available in diagnostic audiology to accurately and reliably assess hearing: (1) physiologic and (2) behavioral. For newborns and young infants ( 5 6 months), a physiologic measure is the approach of choice. Even normal, healthy babies do not provide reliable behavioral responses to sound before 6 months of age. Older infants and children, however, can be tested efficiently and effectively with both behavioral and physiologic measures. PHYSIOLOGIC APPROACH
The Joint Committee on Infant Hearing (JCIH)' recommends that all infants with hearing loss be identified before 3 months of age and receive intervention by 6 months of age. This recommendation necessitates the use of a physiologic measure because of problems in the reliability of behavioral measures within this age range of birth to 6 months. Behavioral observation audiometry (i.e., behavioral hearing assessment
From the Department of Speech and Hearing Sciences, Center on Human Development and Disability, University of Washington, Seattle, Washington (RCF); and Department of Otolaryngology, Head and Neck Surgery, Audiology and Speech Language Pathology, Indiana University School of Medicine, Indianapolis, Indiana (AOD)
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without reinforcement) is a poor predictor of auditory sensitivity. Therefore, behavioral observation audiometry is no longer recommended for assessing frequency-specific threshold sensitivity in newborns, infants, or young children. Only behavioral measurements in which infants are under stimulus-response control (e.g., visual reinforcement audiometry used after infants are 6 months of age developmentally, or conditioned play audiometry after the child is 2.5 years of age) can be used to accurately assess behavioral sensitivity. Yet despite age and developmental factors, some children are unable to reliably perform for behavioral hearing assessment. These children may present with immaturity, developmental delay, noncompliant behavior, or physical limitations that make behavioral hearing assessment unreliable. For example, fewer and fewer children are being identified with only hearing loss and no other complicating problems. These children often are unable to perform reliably enough for routine behavioral hearing tests during the first 12 months of life, and some may never be able to provide reliable behavioral audiometric data. Moreover, waiting for reliable behavioral data as a prerequisite to initiation of intervention services compromises the development of audition and reduces the window of opportunity in which development of auditory-oral language skills is optimal. Therefore, if intervention is to be provided by 6 months of age, a physiologic measure is recommended of the various approaches to pediatric assessment currently available, two physiologic measures, auditory brainstem response (ABR) and otoacoustic emissions (OAE), demonstrate the required operating characteristics for achieving this goal. These measures provide an estimate of auditory sensitivity as a function of frequency without relying on behavioral responses from the child. Over the past 25 years, developments in the recording of auditory evoked potentials (AEPs) (particularly the short-latency ABR) have made possible the accurate and reliable estimation of hearing levels in infants and young children. The use of short-latency AEPs has had a great impact on pediatric audiology. The application of scalp-recorded potentials, frequently in conjunction with existing behavioral information, has improved the ability to assess hearing in children early in life and has thus made a major contribution to early intervention and the management of hearing disorders. Any time electrodes are attached to the scalp, several AEPs emerge. This section focuses on short-latency potentials because they are the most widely used for the estimation of hearing levels in infants and children; however, other evoked potentials, primarily those from longer time epochs following the stimulus, have been applied to pediatric populations for hearing assessment. For example, the middle-latency response (10-50 ms) has been found to be useful in estimating hearing sensitivity for low-frequency although this response tends to be variable with level of sleep. Long-latency cortical-evoked potentials have a long history of clinical application in response to auditory signals, but for audiometric purposes, late cortical responses are sufficiently influenced by subject state, attention to the signal, and habituation to render them poorly suited for hearing assessment with infants and young children. In children for whom behavioral hearing assessment does not provide a complete picture of their hearing capability and for all infants fewer than 6 months of age, the ABR has become a very powerful tool. It has been shown to be particularly well-suited for the purpose of hearing loss estimation for the following reasons: (1) the ABR accurately approximates behavioral pure-tone (2) this response does not habituate thresholds in the mid to high freq~encies'~; and is stable over time and is therefore suitable for acquiring the multiple waveforms necessary for hearing level estimation; (3) it is unaltered by sleep or sedation40and is thus useful for the many infants and children who are unable
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to fully cooperate during a recording session. Furthermore, responses from 20, 34, 41 providing a broad infants and children have been extensively des~ribed,’~, literature base for the clinical application of this tool in pediatrics. The Auditory Brainstem Response
The ABR waveform is shown in Figure 1. Three prominent peaks, labeled I, 111, and V, are of primary interest for audiometric purposes. ABR wave V, the largest and most robust wave across stimulus intensities, is generally used to determine the ABR threshold or visual detection level (the point at which a replicated response can be visually differentiated from background noise), although in early infancy, wave I11 can be equally prominent.z3,46 The term ABR threshold should not be confused with hearing threshold as determined with puretone signals, because ABRs and the stimuli that generate them are substantially different from behavioral responses to sound.12,37, 50 Three aspects of the ABR are most often used in the assessment of the auditory system: (1) visual detection threshold, (2) amplitude, and (3) latency. As just described, the visual detection threshold is the level at which the ABR (usually wave V) can be differentiated from background noise and, by definition, is associated with the lowest stimulus intensity that just generates this response. Amplitude defines the magnitude voltage of the response (in volts) and is usually a peak-to-peak measurement. As shown in Figure 1, amplitude measures are most commonly made from the positive peak of the wave to the following negative deflection. Although amplitude is inextricably linked with the visual detection threshold of the ABR, it is not usually used in isolation for the differentiation of auditory disorders because it is highly variable and affected by nonauditory factors (e.g., electrode impedance or myogenic interference) and auditory
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Latency is the most widely used ABR measurement value. Two basic latency values can be obtained from the ABR waveform: (1) absolute latencies and (2) relative or intenvave latencies (Fig. 1). Absolute latencies are defined as the elapsed time from stimulus onset to the wave peak. Interwave latencies are defined as the difference between the absolute latencies of two wave peaks (i.e., waves I and V), and because this implies that it is the time required to travel from one generator site to the next, it is often referred to as centrul transmission time or neural conduction time. Absolute latencies of the ABR have an inverse relationship with stimulus level in that as intensity is decreased, latencies increase. This latency change is roughly equivalent for all waves of the response, suggesting that peripheral changes (e.g., stimulus level or peripheral hearing loss) first affect the latency of wave I; subsequent waves shift accordingly. In general, intenvave latencies are not substantially affected by peripheral hearing loss.yProlongation of the wave I to V interval suggests a disorder that involves the retrocochlear portion of the auditory pathway rather than the peripheral portion as with a conductive or sensorineural hearing loss (SNHL)? although the two portions of the pathway are linked. If all waves within the ABR are available for latency measurement, a disorder affecting the peripheral portion of the pathway can uSually be differentiated from a disorder involving the central portion. This is of great advantage in infant hearing screening, for example, when attempting to differentiate between those with significant hearing loss and those with neurologic disorder or immaturity.21Wave I is not always easily resolved in the ABR, particularly in individuals who have substantial high-frequency hearing loss. Stimulus Variables The ABR is sensitive to numerous stimulus and recording variables. Some of the most crucial are discussed later. Knowledge of how these variables influence the ABR is critical to its interpretation. For example, seemingly small differences in recording technique or stimulus presentation between clinical laboratories can create differences in response characteristics that would influence response interpretation (see Hall1*for a complete review of stimulus and subject variables). The clicks that are most commonly used for eliciting the ABR are abrupt in onset and broad in spectrum. This results in the simultaneous excitation of a large population of neurons whose synchronized firings make up the ABR. The neural synchronizing effect of the abrupt-onset click makes it the most effective stimulus for eliciting the ABR; however, this stimulus lacks frequency specificity because of the broad acoustic spectrum created with this onset. As intensity of the stimulus increases, wave V latency (and the latencies of all ABR components) decreases. Amplitude increases with elevation in intensity as well; however, these increases are not as systematic as observed with latency. The ABR can be elicited using short tone bursts that have sufficiently abrupt onsets to generate the response, yet carry some frequency specificity for definition of hearing loss configuration. Problems arise with this type of stimulus because the abrupt stimulus onset required to generate the ABR is contrary to the slow onset time that is required for a tone-pip to be frequency specific; however, when the appropriate recording and stimulus precautions are taken, data regarding various frequencies can be accurately obtained, and this is highly desirable in quantification of hearing loss.
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The ABR latency is dependent on the repetition rate of the stimulus. Because multiple stimuli are presented for the signal averaging process required for the extraction of the ABR from background noise, the rate at which individual stimuli are presented relates to the overall time it takes to obtain one response. The fastest rate of presentation would seem to be the most efficient; however, there is a trade-off between response clarity and repetition rate. Simply stated, at high repetition rates, the latencies of all components are prolonged and the amplitudes of the early waves (I-IV) are diminished. A common clinically applied repetition rate is between 20 and 30 per second for hearing assessment. For neurologic applications, slower rates are used. To record electric potentials from the scalp of human patients, electrodes are attached to the scalp. The electric potentials recorded in this fashion are very small in amplitude and must be amplified before computer analysis. A differential amplifier is used for this type of work in that it creates an improvement in the response-to-noise level. To further improve the response-to-noise level, it is necessary to average responses to many stimulus presentations. This is done on a computer that has been designed to perform this activity, termed "signal averaging." Depending on stimulus level and the activity level of the patient, between 1000 and 4000 stimulus presentations are averaged to extract the response from background noise. Once the ABR has been sufficiently averaged, measurement of latency, amplitude, and detection threshold can be made. Subject Variables
In addition to stimulus variables that affect this response, the maturation of the auditory system early in life also affects the ABR. The maturational aspect of the ABR has implications for its use in infants with significant hearing loss. ABRs from infants differ substantially from responses of adults. In general, responses from infants show extended absolute and interwave latencies, diminished amplitudes, and greater within- and between-subject variability compared with adult responses.', '',ly, 34 Click-evoked ABRs can be recorded from infants although responses are poorly formed as young as 27 weeks of gestational and of long latency. By 33 to 35 weeks of gestation, responses are more stable and the visual detection level is comparable to that for older infants and adults.I4 Although the ABR is not a direct test of hearing sensitivity, it has gained considerable popularity as an assessment tool to evaluate the integrity of the auditory pathway from the external ear to the lower brain stem. The presence of clear, click-evoked ABRs at low stimulus intensities is a strong indicator of normal or near-normal hearing sensitivity in the mid- to high frequencies of infants.I4 The strength of the ABR lies in stability across subject state, ease of recording, and strong correlation between alterations of the ABR (threshold elevation or latency prolongation) and those with hearing impairment.'" Absence of the ABR, however, is not a positive indicator of deafness because of inherent limitations of the response. For example, the requirement for neural synchrony to generate the ABR limits the range of stimuli available to evoke the short-latency ABR. The necessity for a rapid-onset stimulus impacts the range of frequencies that are assessed* (e.g., depending on the earphone used, the click-evoked ABR, represents approximately 2 kHz to 8 kHz in normal hearing individuals). In some instances, better hearing in the low frequencies is not detected in the click-evoked ABR; thus, the overall amount of hearing loss can be overestimated. This drawback, however, is more a limitation in terms of assessment across the frequency range rather than in terms of its effectiveness as an initial screening tool.
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In addition, the presence of a neurologic disorder (including extreme prematurity) may affect the ability of auditory fiber populations to fire in synchrony, with consequent disruptions in the morphology or presence of the ABR.21These response abnormalities can be misinterpreted as indicating a hearing deficit when, in fact, auditory sensitivity may be unaffected. Applications
Screening infants for hearing loss provides only one small segment of the entire process of early detection. Screening outcomes place infants into one of two categories: (1) infants with normal hearing or (2) infants at serious risk for hearing loss. Initially, further testing of these infants is to rule out or confirm the presence of hearing loss. Subsequently, it is necessary to describe the hearing loss in terms of magnitude, configuration, and type to guide a program of intervention that is both individually,designed and thorough. Thus, two primary applications of physiologic measures exist in pediatrics: (1) screening for hearing loss during the neonatal period and (2) estimation of sensitivity in children who cannot otherwise provide reliable behavioral data. Neonatal Hearing Screening
A screening program that is designed to identify hearing loss at around the time of birth presents an obvious advantage-the identification of hearing loss at the earliest possible opportunity. To perform a reliable screen at this time in life, however, requires the use of a physiologic test of hearing and, as stated above, a physiologic measure is the most reliable and efficient tool for this purpose. Reliable estimates of peripheral sensitivity in newborn infants can be obtained with the ABR or, as described later, otoacoustic emissions (OAEs). In neonatal hearing screening programs, infants are screened just before discharge from the hospital. Testing at the time of discharge reduces the rate of false-positive findings because the infant is most likely to be stable and healthy at this point. Newborn hearing screening has evolved significantly with automated technology. Automated screening advances in AEP and OAE technology use automation and objective data analysis to simplify the task of infant hearing screening while rigorously maintaining accurate, consistent, and effective performance. Use of an automated screening device eliminates the requirement of the presence of a sophisticated examiner; objective data are collected under controlled conditions, with built-in criteria for a pass. The same statistical criterion is applied to every test, thus reducing examiner and interpretation error. The ability to use various personnel minimizes personnel cost, thereby increasing cost effectiveness. Estimation of Hearing Levels Using Auditory Brain Stem Response
Estimation of hearing sensitivity using a physiologic approach is most often necessary during early infancy when behavioral responses to sound are unreliable or with older children who are delayed or uncooperative and therefore not candidates for a behavioral approach in hearing assessment.
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Little is required of patients in this type of assessment. For cooperative subjects, it is necessary to recline and be relatively relaxed so that muscle artifact, from head and shoulder movement, does not interfere with the recording of the small electric potentials that make up the ABR. For patients who cannot cooperate, a mild sedative is often required. As stated earlier, sedation (and accompanying sleep) does not influence the ABR. For the determination of hearing sensitivity, normative values are necessary to differentiate normal response patterns from those that are abnormal. Because the ABR is influenced by several different stimulus and recording parameters, each clinic establishes its own set of normative data against which clinical decisions can be made. For determination of hearing levels, each patient is administered a series of clicks at different intensities, just as might be presented to a patient undergoing a behavioral hearing test and asked to indicate the presence or absence of sound, except that in this instance the patient is not an active participant in the testing but rather is passive (e.g., quiet awake or sleeping). At each intensity, wave V is identified and measbred. As described earlier, wave V latency increases (shifts out in time) as intensity level is decreased. These measurements can be graphed in the form of a latency-intensity function. The amplitude of the response also decreases until it can no longer be differentiated from background noise. From these data, determination of the visual detection threshold and comparison of wave V latencies to the normal latency-intensity function can be made. Click-evoked ABRs cannot provide information in a frequency-specific manner. These responses are dominated by the frequencies 2 kHz to 8 kHz in the normal cochlea. Thus, it is necessary to modify signal and test paradigms in an effort to provide information describing response properties from specific cochlear regions. In contrast to detection thresholds for clicks, ABR thresholds to brief tonal stimuli presented in quiet or in noise-masking paradigms provide more frequency-specific results and enable the audiologist to obtain reasonably accurate estimates of the pure-tone behavioral audiogram from 0.5 kHz to 4.0 kHz; however, the successful recording of ABRs to brief tones requires careful consideration of the stimulus, masking, recording parameters, and response interpretation issues. How well do tone ABR thresholds predict the pure-tone behavioral audiogram? Stapells and c o l l e a g ~ e sdemonstrated ~~ high correlations (i.e., > 0.94) between ABR thresholds to 0.5 kHz, 2.0 kHz, and 4.0 kHz air conduction tones in noise masking and the pure-tone behavioral thresholds for infants and young children with normal hearing or SNHL. Their study found no effects of age at ABR on the results; the ABR was equally accurate in predicting young infants’ follow-up behavioral thresholds as it was in predicting those of older children. Moreover, tone-ABR thresholds accurately predicted the pure tone behavioral thresholds in infants and young children with normal hearing or SNHL: 98% were within 30 dB, 80% were within 15 dB, and 66% were within 10 dB. In addition, audiometric configuration (i.e., sloping high frequency, flat, or reverse slope) of the hearing loss did not appear to affect the accuracy of pure-tone behavioral threshold estimation^?^, 38 As with conventional behavioral audiometry, the addition of bone conduction tonal stimuli to ABR threshold protocols provides the clinician with a more complete picture of the type (e.g., conductive, mixed, or sensonneural) and degree of hearing loss. ABRs to 0.5 kHz and 2.0 kHz bone conducted tonal stimuli presented at low stimulus intensities show good frequency specificity in infants and ad~1ts.I~
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Otoacoustic Emissions
Otoacoustic emissions are sounds, generated in the inner ear, that can be recorded by sensitive microphones in the external ear canal.", 29 These sounds are most likely generated by the outer hair cells in the cochlea2*and are an indirect measure of the function of these hair cells. OAEs are not in and of themselves necessary for hearing nor are they a mechanism of hearing, but rather reflect the status of structures that are necessary for hearing (for complete review of OAEs, see Robinette and Glattke33). Although OAEs provide an excellent tool to identify the presence of hearing loss, and to confirm the status of outer hair cell function, their contribution to the quantification of hearing loss or to the definition of degree of hearing loss specifically remains uncertain. Yet the objectivity of OAE measurement makes it ideal for testing individuals who cannot be reliably evaluated with behavioral procedures. With the pediatric population, OAEs offer the clinician the opportunity to obtain ear specific data where other behavioral audiometric measures (i.e., sound field testing) may not be able to provide this information. The two basic categories of OAEs are distinguished by the signals that generate the emissions rather than differences in the underlying cochlear mechanism. Spontaneous Otoacoustic Emissions
Spontaneous OAEs are single- or multiple-frequency, narrow-band signals that are generated by the cochlea in the absence of auditory stimulation. Approximately 50% to 60% of normal ears produce spontaneous OAEs, a percentage that holds for neonates, infants, and adults.3, Spontaneous OAEs are thought to originate from the place in the cochlea that is tuned to that frequency. Evoked Otoacoustic Emissions
Evoked OAEs occur in response to an external auditory stimulus and are present in nearly all normal hearing adults and infants. Various signals can be used to evoke these emissions. Transient signals, such as the click used to evoke the ABR, are effective in generating transient evoked OAEs.%These emissions also can be recorded as acoustic distortion products, which originate in the cochlea as a result of interference (distortion) between two simultaneously presented frequencies (f, and f2) and which together create a combination tone (or distortion product) in the cochlea.*4 Emissions can be recorded relatively quickly, without active participation of the infant or child. As with the ABR, emissions are best recorded from quiet subjects (sleeping, in fact, provides the best recording circumstance). Emissions represent hearing for frequencies that are present in the stimulus; for example, high-frequency stimuli generate high-frequency emissions, and low-frequency stimuli generate low-frequency emissions." Clinical Application
The category of emissions that has the greatest potential for clinical application is evoked OAEs. Because all normally hearing individuals do not have spontaneous OAEs, their diagnostic potential is limited; however, both the transient evoked and the acoustic distortion product emissions show promise as
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tools that can be used to assess hearing in infants and children and to screen for hearing loss in newborns. Evoked emissions are robust, that is, they are found in all normally hearing infants and thus are easily recorded. Neonatal Hearing Screening Both transient evoked and distortion product emissions show promise as effective tools for screening hearing in newborn infants?,u( Potential advantages of OAEs over the ABR are that (1)emissions are a direct assessment of cochlear status and (2) OAEs may prove to be more time-efficient than the ABR for screening purposes. In the few studies that have been carried out comparing current infant hearing screening procedures with OAEs, emissions have been shown to be at least as good an indicator of hearing status as the tool to which it is being compared; however, more large-scale studies of both high-risk and normal newborn infants must be carried out before a clear picture of the sensitivity and specificity of the OAEs can be obtained. #
Estimation of Hearing Using Otoacoustic Emissions OAEs are present in virtually all adults and children in whom hearing is known to be 20 dB HL or better and absent in those in whom hearing levels are 35 dB to 45 dB HL or poorer. Therefore, OAEs have the clinical capability to indicate normal cochlear function when it exists. For pediatric audiology, this is particularly helpful when used in conjunction with other hearing assessment tools, such as the ABR and tests of middle ear function (tympanometry). For example, in children with neurologic involvement, an absent ABR can be the result of either severe cochlear impairment or lack of neural synchrony at the level of the brain stem. A finding of normal OAEs and normal middle ear function indicates normal peripheral (i.e., middle ear and cochlea) functioning, thus isolating the disorder to the brain stem auditory pathway. This finding illustrates an increasingly common audiologic challenge. Normal OAEs in combination with an abnormal ABR represent the hallmark signs in infants, children, and adults of some form of auditory nerve pathology, brain stem neuropathy, or brain stem conduction defect.37 BEHAVIORAL APPROACH
It is possible to approach the assessment of infants and young children behaviorally through operant conditioning paradigms, specifically through an operant discrimination procedure. In an operant discrimination procedure, a stimulus is used to cue the child that a response results in reinforcement. Reinforcement is used to strengthen an easily monitored single response and keep the child in an aroused or motivated state. Maintaining motivation and a high response probability through the use of age-appropriate reinforcement allows clinicians to investigate over time an infant’s or young child’s auditory response behavior. This, then, allows more precise estimation of ability and reduces the habituation found in behavioral assessment without reinforcement (i.e., behavioral observation audiometry). Visual Reinforcement Audiometry
Normally developing infants make head turns toward a sound source in the first few months of life. This localization response represents a behavioral
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“window” through which many aspects of auditory behavior can be evaluated. In visual reinforcement audiometry (VRA), a head-turn response after an auditory stimulus is rewarded with an interesting visual event, usually activation of an attractive three-dimensional animated toy. Without reinforcement, an infant’s responses to sound habituate rapidly and may not occur at low intensity levels. In addition, without reinforcement, the infant’s response depends on the nature of the stimulus. That is, the spectrum of the signal, its center frequency and bandwidth, its intensity level, and its meaningfulness to the child are all variables that can affect the child’s response when no reinforcement is used. As such, VRA has emerged as a successful procedure for infants and young children 6 months to 3 years of age! The success of VRA is certainly related to the fact that the response (head turn) and reinforcer (animated toy) are well suited to the developmental level of children between 6 months and 3 years of age, although there is less success with normally developing children between 2 and 3 years of age because they tend to quickly habituate to the reinforcers. Once the child is under stimulus control, he or she will continue to respond at low sensation levels long enough to provide an estimate of threshold. The clinical validity of results obtained with operant audiometry is well documented. Numerous studies have shown that infant responses differ only slightly from 32. 35, 45, 49 A variety of signals can be tested successfully in the those of sound field and under earphones.26, 49 The availability of insert receivers coupled to an appropriately sized ear tip also can be used with infants. These same transducers also are used during ABR testing, allowing comparisons between test results using the same transducers. Clinical reports shared among clinicians and reports in the literature reveal highly consistent findings from different settings.I6That is, for normally hearing infants, thresholds are consistently obtained within a conservative definition of normal hearing (< 20 dB HL). Moreover, the dispersion of normal responses is sufficiently small that even mild hearing impairments, such as those often accompanying otitis media, can be accurately defined. Comparisons of VRA audiograms in individual children with later audiograms determined with play audiometry show results from the two procedures that are essentially identical. It is generally agreed that, as long as the child is under stimulus control, the thresholds provide, with a high degree of confidence, valid information for making diagnostic and management decisions. Several studies17,44 have reported the use of VRA on children with Down syndrome and other developmental disabilities, suggesting that developmental age can be a determining factor in VRA success. Widen48evaluated VRA as a function of developmental age in high-risk infants. Clearly, the developmentally mature infants were more often tested successfully. Visual reinforcement audiometry was successful for most infants by 5 or 6 months corrected age. An infant’s ability to participate in the VRA task also was compared with their mental age score on the Bayley Scales of Infant Development. When test outcome in VRA was compared with developmental age in a subset of infants, success was achieved in approximately 90% of infants with a developmental age of 5.5 to 6.5 months. Therefore, application of VRA in clinical protocols must consider corrected age adjusted for prematurity rather than chronologic age or developmental age when disparities exist between corrected age and the child’s developmental status. Accurate VRA assessment depends in large part on the ability of one examiner to keep the child appropriately attentive while another assumes the responsibilities of audiometry and operant conditioning. The requirement for two examiners limits the efficiency of VRA; however, audiometric protocol can
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be programmed and peripheral hardware controlled by microcomputer so that a single examiner can accurately and efficiently test infants with VRA. In addition, a single examiner can use a simple, electronic "centering toy" for maintaining a child's attention at midline. This approach does remove the examiner from the test room and may increase test time but still allows the VRA procedure to be completed without compromising accuracy.
Conditioned Play Audiometry
Conditioned play audiometry (CPA) is probably the most common procedure used in the hearing assessment of young children. Through conditioning, children learn to engage in some activity-putting rings on a peg, dropping or stacking blocks-each time they hear the test signal. These activities are assumed to be interesting to children and are used to identify a specific behavior that is used to denote a response tb signal. When teaching children to perform play audiometry, it is usually not difficult to select a response behavior that children are capable of performing. The challenge in play audiometry is teaching the child to wait, listen, and respond when the auditory signal is presented. Conditioned play audiometry follows a model of auditory stimulu-response+reinforcement, in which the play activity is the response and social praise is the reinforcement. Therefore, in addition to teaching the youngster under test the conditioned response in the CPA task, the examiner also must be skilled in delivering social reinforcement at the appropriate time and interval. Audiologic literature suggests that CPA is widely accepted among clinicians who interact with young childrena It is generally recognized that most 3-yearolds can be tested using play audiometry. Yet, how young can children be to achieve successful audiologic outcomes? Thompson and WebeF2 demonstrated the rate of success in obtaining detailed information with CPA is limited for children under the age of 30 months. Yet some 2-year-olds can be conditioned to play audiometry? Moreover, when 2-year-olds are proficient with CPA, they are more likely to provide more responses before habituation than they would if tested by VRA. Because overlap exists between VRA and CPA as suitable techniques with children in this age range, the successful evaluation of a child ultimately depends on the experience of a seasoned clinician. Experience with CPA indicates that reliable threshold responses can be obtained when auditory stimulus-response control has been established and response criterion are maintained. Results from a clinical study5 of 40 preschoolers, aged 30 to 48 months, revealed thresholds at an audiometric level of 10 dB HL or better. These findings were in close agreement with other 4-year old children."
SUMMARY
A behavioral approach is the first choice for hearing assessment in infants and children. It is the only true test of hearing. Physiologic measures are not tests of hearing, only indicators of auditory function. The use of physiologic measures in estimating hearing levels makes some presumptions regarding the concept of hearing. As such, these measures are used when a definitive statement about hearing cannot be made on the basis of behavioral audiometric results, or
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when other factors (eg., age or developmental delay) preclude obtaining reliable behavioral information.
References 1. American Speech-Language-Hearing Association: Joint Committee on Infant Hearing 1994 Position Statement. Aha 3638-41, 1994 2. Bergman BM, Gorga MP, Neely ST, et a1 Preliminary descriptions of transient-evoked and distortion-product otoacoustic emissions from graduates of an intensive care nursery. J Am Acad Audio1 6150-162, 1995 3. Burns EM, Arehart KH, Campbell SL Prevalence of spontaneous otoacoustic emissions in neonates. Abstracts of the Fourteenth Midwinter Research Meeting for the Association for Research in Otolaryngology, Clearwater Beach, FL, Feb., 1992, p 66 4. Cox LC: Infant assessment: developmental and age-related consideration. In Jacobson JT (ed): The Auditory Brainstem Response; Boston, College-Hill Press, 1985 5. Diefendorf AO: The effect of pre-play period on play audiometry. Presented at the Annual Convention of the Tennessee Speech-Language-Hearing Association, Memphis, April, 1981 6. Diefendorf AO, Gravel J S Behavioral observation and visual reinforcement audiometry. In Gerber SE (ed): The Handbook of Pediatric Audiology. Washington, DC,Gallaudet University Press, 1996, pp 53-83 7. Eggermont J, Don M, Brackmann D Electrocochleography and auditory brainstem electric responses in patients with pontine angle tumors. Ann Otol Rhino1 Laryngol 89(suppl):75,1980 8. Folsom RC: Auditory brainstem responses from human infants: Pure-tone masking profiles for clicks and filtered clicks. J Acoust Soc Am 78555562, 1985 9. Fowler CG, Noffsinger D: The Effects of stimulus repetition rate and frequency on the auditory brainstem response in normal, cochlear-impaired, and VIII nerve/brainstemimpaired subjects. J Speech Hear Res 26560-567,1983 10. Galambos R, Hicks G, Wilson MJ: The auditory brainstem response reliably predicts hearing loss in graduates of a tertiary intensive care nursery. Ear Hear 5:254-260, 1984 11. Gerwin KS, Glorig A (eds): Detection of Hearing Loss and Ear Disease in Children. Springfield, IL, Charles C. Thomas, 1974 12. Gorga MP, Beauchaine KA, Reiland JK, et al: Effects of stimulus duration on ABR thresholds and on behavioral thresholds. J Acoust SOCAm 7661W319, 1984 13. Gorga MP, Kaminski JP, Beauchaine KL, et al: A comparison of auditory brain stem response thresholds and latencies elicited by air- and bone-conducted stimuli. Ear Hear 1485-94, 1993 14. Gorga ME,' Reiland JK, Beauchaine KA, et al: Auditory brainstem responses from graduates of an intensive care nursery: Normal patterns of response. J Speech Hear Dis 30:311-318, 1987 15. Gorga MP, Worthington DW, Reiland JK, et al: Some comparisons between auditory brainstem response thresholds, latencies, and the pure-tone audiogram. Ear Hear 6105-112, 1985 16. Gravel JS, Traquina D N Experience with the audioIogicaI assessment of infants and toddlers. Jnt J Pediatr Otolaryngol 23:59-71, 1992 17. Greenberg DB, Wilson WR, Moore JM, et a1 Visual reinforcement audiometry (VRA) with young Down syndrome children. J Speech Hear Dis 43:448-458,1978 18. Hall JW(ed): Handbook of Auditory Evoked Responses. Boston, Allyn and Bacon, 1992 19. Hecox KE, Burkhard R Developmentaldependencies of the human brainstern auditory evoked response. Ann N Y Acad Sci 388:538-556, 1982 20. Hecox KE, Galambos RG: Brainstem auditory evoked responses in human infants and adults. Arch Otolaryngol 99:30-33, 1974 21. Hecox KE, Cone B, Blaw ME Brainstem auditory evoked response in the diagnosis of pediatric neurologic diseases. Neurology 31:832-839,1981 22. Kemp DT Stimulated acoustic emissions from the human auditory system. J Acoust Soc Am 61.13861391, 1978
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23. Klein AJ: Frequency and age-dependent auditory evoked potential thresholds in infants. Hear Res 16291-297,1984 24. Lonsbury-Martin BL, Harris FP, Stagner BB, et a1 Distortion product emissions in humans: I. Basic properties in normally hearing subjects. Ann Otorhinolaryngol 99(suppl):3-14, 1990 25. Mendel MI, Wolf K E Clinical applications of the middle latency response. Audiology: A Journal for Continuing Education 8:141-155, 1983 26. Moore JM, Wilson WR, Lillis KE, et al: Earphone auditory thresholds of infants utilizing visual reinforcement audiometry (VRA). Presented at the American Speech and Hearing Association Convention, Houston, November, 1976 27. Munnerley GM, Greville KA, Purdy SC, et al: Frequency-specific auditory brainstem responses relationship to behavioral thresholds in cochlear-impaired adults. Audiology 3025-32, 1991 28. Norton SJ: Application of transient evoked otoacoustic emissions to pediatric populations. Ear Hear 1464-73,1993 29. Norton SJ, Neely ST Tone-burst evoked otoacoustic emissions from normal-hearing subject. J Acoust Soc Am 81:1860-1872, 1987 30. Norton SJ, Widen JE: Evoked otoacoustic emissions in normal-hearing infants and children: Emerging data and issues. Ear Hear 11:121-127,1990 31. Nozza RJ, Wilson WR &asked and unmasked pure-tone thresholds of infants and adults: Development of auditory frequency selectivity and sensitivity. J Speech Hear Res 27613-622,1984 32. Olsho LW, Koch EG, Carter EA, et a1 Pure-tone sensitivity of human infants. J Acoust SOCAm 84:1316-1324, 1988 33. Robinette MS, Glattke TJ (eds): Otoacoustic Emissions: Clinical Applications. New York, Theime Medical Publishers, 1997 34, Salamy A, McKean C M Post-natal development of human brainstem potentials during the first year of life. Electroencephalogr Clin Neurophysiol 40:418-426, 1976 35. Sinnott JM, Pisoni DB, Aslin RN: A comparison of pure tone auditory thresholds in human infants and adults. Infant Behav Dev 65-17, 1983 36. Starr A, Amlie RN, Martin WH, et al: Development of auditory function in newborn infants revealed by auditory brainstem potentials. Pediatrics 60:831-839, 1977 37. Starr A, Picton TW, Sininger Y, et al: Auditory neuropathy. Brain 119:741-753, 1996 38. Stapells DR, Gravel JS, Martin BA Thresholds for auditory brainstem responses to tones in notched noise from infants and young children with normal hearing or sensorineural hearing loss. Ear Hear 16361-371,1995 39. Stockard JE, Stockard JJ, Wesmorland BF, et a1 Brainstem auditory evoked responses: Normal variation as a function of stimulus and subject characteristics. Arch Neurol 36823-831, 1979 40. Strickland EA, Bums EM, Tubis A. Incidence of spontaneous otoacoustic emissions in children and infants. J Acoust SOCAm 78:931-935, 1985 41. Teas DC,Klein AJ, Kramer SK An analysis of auditory brainstem responses in infants. Hear Res 719-54, 1982 42. Thompson G, Weber BA: Responses of infants and young children to behavioral observation audiometry (BOA). J Speech Hear Dis 39:14&147,1974 43. Thompson MD, Thompson G, Vethivelu S A comparison of audiometric test thresholds for 2-year-old children. J Speech Hear Dis 54:174-179, 1989 44. Thompson G, Wilson WR, Moore JM: Application of visual reinforcement audiometry (VRA) to low-functioning children. J Speech Hear Dis &SO-90,1979 45. Trehub SE, Schneider BA, Endman M: Developmental changes in infants’ sensitivity to octave-band noises. J Exp Child Psycho1 29282-293, 1980 46. Weber BA Comparison and auditory brainstem response latency norms for premature infants. Ear Hear 3257-262,1982 47. Weber BA: Interpretation: problems and pitfalls. In Jacobson JT (ed): The Auditory Brainstem Response. Boston, CollegeHill Press, 1985 48. Widen JE: Behavioral screening of high-risk infants using visual reinforcement audiometry. Semin Hear 1132-356, 1990
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49. Wilson WR, Moore Jh4: Pure-tone earphone thresholds of infants utilizing visual reinforcement audiometry (VRA). Presented at the American Speech and Hearing Association Convention, San Francisco, 1978 50. Worthington DW, Peters J F Quantifiable hearing and no ABR Paradox or error? Ear Hear 1:281-285, 1980
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PHYSIOLOGIC AND BEHAVIORAL APPROACHES TO PEDIATRIC HEARING ASSESSMENT Richard C. Folsom, PhD, and Allan 0. Diefendorf, PhD
The primary objective of detecting hearing loss in children as early as possible is that appropriate intervention(s) can be initiated in a timely fashion. Therefore, infants and young children referred from hearing screening programs must be followed up immediately and receive a comprehensive audiologic evaluation to confirm the presence of hearing loss and establish the magnitude, type, configuration, and symmetry of the hearing loss. Improved assessment procedures for infants and young children have meant greater precision in quantifying hearing losses at an early age, in turn facilitating achievement of this objective. Two approaches are available in diagnostic audiology to accurately and reliably assess hearing: (1) physiologic and (2) behavioral. For newborns and young infants ( 5 6 months), a physiologic measure is the approach of choice. Even normal, healthy babies do not provide reliable behavioral responses to sound before 6 months of age. Older infants and children, however, can be tested efficiently and effectively with both behavioral and physiologic measures. PHYSIOLOGIC APPROACH
The Joint Committee on Infant Hearing (JCIH)' recommends that all infants with hearing loss be identified before 3 months of age and receive intervention by 6 months of age. This recommendation necessitates the use of a physiologic measure because of problems in the reliability of behavioral measures within this age range of birth to 6 months. Behavioral observation audiometry (i.e., behavioral hearing assessment
From the Department of Speech and Hearing Sciences, Center on Human Development and Disability, University of Washington, Seattle, Washington (RCF); and Department of Otolaryngology, Head and Neck Surgery, Audiology and Speech Language Pathology, Indiana University School of Medicine, Indianapolis, Indiana (AOD)
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without reinforcement) is a poor predictor of auditory sensitivity. Therefore, behavioral observation audiometry is no longer recommended for assessing frequency-specific threshold sensitivity in newborns, infants, or young children. Only behavioral measurements in which infants are under stimulus-response control (e.g., visual reinforcement audiometry used after infants are 6 months of age developmentally, or conditioned play audiometry after the child is 2.5 years of age) can be used to accurately assess behavioral sensitivity. Yet despite age and developmental factors, some children are unable to reliably perform for behavioral hearing assessment. These children may present with immaturity, developmental delay, noncompliant behavior, or physical limitations that make behavioral hearing assessment unreliable. For example, fewer and fewer children are being identified with only hearing loss and no other complicating problems. These children often are unable to perform reliably enough for routine behavioral hearing tests during the first 12 months of life, and some may never be able to provide reliable behavioral audiometric data. Moreover, waiting for reliable behavioral data as a prerequisite to initiation of intervention services compromises the development of audition and reduces the window of opportunity in which development of auditory-oral language skills is optimal. Therefore, if intervention is to be provided by 6 months of age, a physiologic measure is recommended of the various approaches to pediatric assessment currently available, two physiologic measures, auditory brainstem response (ABR) and otoacoustic emissions (OAE), demonstrate the required operating characteristics for achieving this goal. These measures provide an estimate of auditory sensitivity as a function of frequency without relying on behavioral responses from the child. Over the past 25 years, developments in the recording of auditory evoked potentials (AEPs) (particularly the short-latency ABR) have made possible the accurate and reliable estimation of hearing levels in infants and young children. The use of short-latency AEPs has had a great impact on pediatric audiology. The application of scalp-recorded potentials, frequently in conjunction with existing behavioral information, has improved the ability to assess hearing in children early in life and has thus made a major contribution to early intervention and the management of hearing disorders. Any time electrodes are attached to the scalp, several AEPs emerge. This section focuses on short-latency potentials because they are the most widely used for the estimation of hearing levels in infants and children; however, other evoked potentials, primarily those from longer time epochs following the stimulus, have been applied to pediatric populations for hearing assessment. For example, the middle-latency response (10-50 ms) has been found to be useful in estimating hearing sensitivity for low-frequency although this response tends to be variable with level of sleep. Long-latency cortical-evoked potentials have a long history of clinical application in response to auditory signals, but for audiometric purposes, late cortical responses are sufficiently influenced by subject state, attention to the signal, and habituation to render them poorly suited for hearing assessment with infants and young children. In children for whom behavioral hearing assessment does not provide a complete picture of their hearing capability and for all infants fewer than 6 months of age, the ABR has become a very powerful tool. It has been shown to be particularly well-suited for the purpose of hearing loss estimation for the following reasons: (1) the ABR accurately approximates behavioral pure-tone (2) this response does not habituate thresholds in the mid to high freq~encies'~; and is stable over time and is therefore suitable for acquiring the multiple waveforms necessary for hearing level estimation; (3) it is unaltered by sleep or sedation40and is thus useful for the many infants and children who are unable
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to fully cooperate during a recording session. Furthermore, responses from 20, 34, 41 providing a broad infants and children have been extensively des~ribed,’~, literature base for the clinical application of this tool in pediatrics. The Auditory Brainstem Response
The ABR waveform is shown in Figure 1. Three prominent peaks, labeled I, 111, and V, are of primary interest for audiometric purposes. ABR wave V, the largest and most robust wave across stimulus intensities, is generally used to determine the ABR threshold or visual detection level (the point at which a replicated response can be visually differentiated from background noise), although in early infancy, wave I11 can be equally prominent.z3,46 The term ABR threshold should not be confused with hearing threshold as determined with puretone signals, because ABRs and the stimuli that generate them are substantially different from behavioral responses to sound.12,37, 50 Three aspects of the ABR are most often used in the assessment of the auditory system: (1) visual detection threshold, (2) amplitude, and (3) latency. As just described, the visual detection threshold is the level at which the ABR (usually wave V) can be differentiated from background noise and, by definition, is associated with the lowest stimulus intensity that just generates this response. Amplitude defines the magnitude voltage of the response (in volts) and is usually a peak-to-peak measurement. As shown in Figure 1, amplitude measures are most commonly made from the positive peak of the wave to the following negative deflection. Although amplitude is inextricably linked with the visual detection threshold of the ABR, it is not usually used in isolation for the differentiation of auditory disorders because it is highly variable and affected by nonauditory factors (e.g., electrode impedance or myogenic interference) and auditory
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Latency is the most widely used ABR measurement value. Two basic latency values can be obtained from the ABR waveform: (1) absolute latencies and (2) relative or intenvave latencies (Fig. 1). Absolute latencies are defined as the elapsed time from stimulus onset to the wave peak. Interwave latencies are defined as the difference between the absolute latencies of two wave peaks (i.e., waves I and V), and because this implies that it is the time required to travel from one generator site to the next, it is often referred to as centrul transmission time or neural conduction time. Absolute latencies of the ABR have an inverse relationship with stimulus level in that as intensity is decreased, latencies increase. This latency change is roughly equivalent for all waves of the response, suggesting that peripheral changes (e.g., stimulus level or peripheral hearing loss) first affect the latency of wave I; subsequent waves shift accordingly. In general, intenvave latencies are not substantially affected by peripheral hearing loss.yProlongation of the wave I to V interval suggests a disorder that involves the retrocochlear portion of the auditory pathway rather than the peripheral portion as with a conductive or sensorineural hearing loss (SNHL)? although the two portions of the pathway are linked. If all waves within the ABR are available for latency measurement, a disorder affecting the peripheral portion of the pathway can uSually be differentiated from a disorder involving the central portion. This is of great advantage in infant hearing screening, for example, when attempting to differentiate between those with significant hearing loss and those with neurologic disorder or immaturity.21Wave I is not always easily resolved in the ABR, particularly in individuals who have substantial high-frequency hearing loss. Stimulus Variables The ABR is sensitive to numerous stimulus and recording variables. Some of the most crucial are discussed later. Knowledge of how these variables influence the ABR is critical to its interpretation. For example, seemingly small differences in recording technique or stimulus presentation between clinical laboratories can create differences in response characteristics that would influence response interpretation (see Hall1*for a complete review of stimulus and subject variables). The clicks that are most commonly used for eliciting the ABR are abrupt in onset and broad in spectrum. This results in the simultaneous excitation of a large population of neurons whose synchronized firings make up the ABR. The neural synchronizing effect of the abrupt-onset click makes it the most effective stimulus for eliciting the ABR; however, this stimulus lacks frequency specificity because of the broad acoustic spectrum created with this onset. As intensity of the stimulus increases, wave V latency (and the latencies of all ABR components) decreases. Amplitude increases with elevation in intensity as well; however, these increases are not as systematic as observed with latency. The ABR can be elicited using short tone bursts that have sufficiently abrupt onsets to generate the response, yet carry some frequency specificity for definition of hearing loss configuration. Problems arise with this type of stimulus because the abrupt stimulus onset required to generate the ABR is contrary to the slow onset time that is required for a tone-pip to be frequency specific; however, when the appropriate recording and stimulus precautions are taken, data regarding various frequencies can be accurately obtained, and this is highly desirable in quantification of hearing loss.
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The ABR latency is dependent on the repetition rate of the stimulus. Because multiple stimuli are presented for the signal averaging process required for the extraction of the ABR from background noise, the rate at which individual stimuli are presented relates to the overall time it takes to obtain one response. The fastest rate of presentation would seem to be the most efficient; however, there is a trade-off between response clarity and repetition rate. Simply stated, at high repetition rates, the latencies of all components are prolonged and the amplitudes of the early waves (I-IV) are diminished. A common clinically applied repetition rate is between 20 and 30 per second for hearing assessment. For neurologic applications, slower rates are used. To record electric potentials from the scalp of human patients, electrodes are attached to the scalp. The electric potentials recorded in this fashion are very small in amplitude and must be amplified before computer analysis. A differential amplifier is used for this type of work in that it creates an improvement in the response-to-noise level. To further improve the response-to-noise level, it is necessary to average responses to many stimulus presentations. This is done on a computer that has been designed to perform this activity, termed "signal averaging." Depending on stimulus level and the activity level of the patient, between 1000 and 4000 stimulus presentations are averaged to extract the response from background noise. Once the ABR has been sufficiently averaged, measurement of latency, amplitude, and detection threshold can be made. Subject Variables
In addition to stimulus variables that affect this response, the maturation of the auditory system early in life also affects the ABR. The maturational aspect of the ABR has implications for its use in infants with significant hearing loss. ABRs from infants differ substantially from responses of adults. In general, responses from infants show extended absolute and interwave latencies, diminished amplitudes, and greater within- and between-subject variability compared with adult responses.', '',ly, 34 Click-evoked ABRs can be recorded from infants although responses are poorly formed as young as 27 weeks of gestational and of long latency. By 33 to 35 weeks of gestation, responses are more stable and the visual detection level is comparable to that for older infants and adults.I4 Although the ABR is not a direct test of hearing sensitivity, it has gained considerable popularity as an assessment tool to evaluate the integrity of the auditory pathway from the external ear to the lower brain stem. The presence of clear, click-evoked ABRs at low stimulus intensities is a strong indicator of normal or near-normal hearing sensitivity in the mid- to high frequencies of infants.I4 The strength of the ABR lies in stability across subject state, ease of recording, and strong correlation between alterations of the ABR (threshold elevation or latency prolongation) and those with hearing impairment.'" Absence of the ABR, however, is not a positive indicator of deafness because of inherent limitations of the response. For example, the requirement for neural synchrony to generate the ABR limits the range of stimuli available to evoke the short-latency ABR. The necessity for a rapid-onset stimulus impacts the range of frequencies that are assessed* (e.g., depending on the earphone used, the click-evoked ABR, represents approximately 2 kHz to 8 kHz in normal hearing individuals). In some instances, better hearing in the low frequencies is not detected in the click-evoked ABR; thus, the overall amount of hearing loss can be overestimated. This drawback, however, is more a limitation in terms of assessment across the frequency range rather than in terms of its effectiveness as an initial screening tool.
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In addition, the presence of a neurologic disorder (including extreme prematurity) may affect the ability of auditory fiber populations to fire in synchrony, with consequent disruptions in the morphology or presence of the ABR.21These response abnormalities can be misinterpreted as indicating a hearing deficit when, in fact, auditory sensitivity may be unaffected. Applications
Screening infants for hearing loss provides only one small segment of the entire process of early detection. Screening outcomes place infants into one of two categories: (1) infants with normal hearing or (2) infants at serious risk for hearing loss. Initially, further testing of these infants is to rule out or confirm the presence of hearing loss. Subsequently, it is necessary to describe the hearing loss in terms of magnitude, configuration, and type to guide a program of intervention that is both individually,designed and thorough. Thus, two primary applications of physiologic measures exist in pediatrics: (1) screening for hearing loss during the neonatal period and (2) estimation of sensitivity in children who cannot otherwise provide reliable behavioral data. Neonatal Hearing Screening
A screening program that is designed to identify hearing loss at around the time of birth presents an obvious advantage-the identification of hearing loss at the earliest possible opportunity. To perform a reliable screen at this time in life, however, requires the use of a physiologic test of hearing and, as stated above, a physiologic measure is the most reliable and efficient tool for this purpose. Reliable estimates of peripheral sensitivity in newborn infants can be obtained with the ABR or, as described later, otoacoustic emissions (OAEs). In neonatal hearing screening programs, infants are screened just before discharge from the hospital. Testing at the time of discharge reduces the rate of false-positive findings because the infant is most likely to be stable and healthy at this point. Newborn hearing screening has evolved significantly with automated technology. Automated screening advances in AEP and OAE technology use automation and objective data analysis to simplify the task of infant hearing screening while rigorously maintaining accurate, consistent, and effective performance. Use of an automated screening device eliminates the requirement of the presence of a sophisticated examiner; objective data are collected under controlled conditions, with built-in criteria for a pass. The same statistical criterion is applied to every test, thus reducing examiner and interpretation error. The ability to use various personnel minimizes personnel cost, thereby increasing cost effectiveness. Estimation of Hearing Levels Using Auditory Brain Stem Response
Estimation of hearing sensitivity using a physiologic approach is most often necessary during early infancy when behavioral responses to sound are unreliable or with older children who are delayed or uncooperative and therefore not candidates for a behavioral approach in hearing assessment.
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Little is required of patients in this type of assessment. For cooperative subjects, it is necessary to recline and be relatively relaxed so that muscle artifact, from head and shoulder movement, does not interfere with the recording of the small electric potentials that make up the ABR. For patients who cannot cooperate, a mild sedative is often required. As stated earlier, sedation (and accompanying sleep) does not influence the ABR. For the determination of hearing sensitivity, normative values are necessary to differentiate normal response patterns from those that are abnormal. Because the ABR is influenced by several different stimulus and recording parameters, each clinic establishes its own set of normative data against which clinical decisions can be made. For determination of hearing levels, each patient is administered a series of clicks at different intensities, just as might be presented to a patient undergoing a behavioral hearing test and asked to indicate the presence or absence of sound, except that in this instance the patient is not an active participant in the testing but rather is passive (e.g., quiet awake or sleeping). At each intensity, wave V is identified and measbred. As described earlier, wave V latency increases (shifts out in time) as intensity level is decreased. These measurements can be graphed in the form of a latency-intensity function. The amplitude of the response also decreases until it can no longer be differentiated from background noise. From these data, determination of the visual detection threshold and comparison of wave V latencies to the normal latency-intensity function can be made. Click-evoked ABRs cannot provide information in a frequency-specific manner. These responses are dominated by the frequencies 2 kHz to 8 kHz in the normal cochlea. Thus, it is necessary to modify signal and test paradigms in an effort to provide information describing response properties from specific cochlear regions. In contrast to detection thresholds for clicks, ABR thresholds to brief tonal stimuli presented in quiet or in noise-masking paradigms provide more frequency-specific results and enable the audiologist to obtain reasonably accurate estimates of the pure-tone behavioral audiogram from 0.5 kHz to 4.0 kHz; however, the successful recording of ABRs to brief tones requires careful consideration of the stimulus, masking, recording parameters, and response interpretation issues. How well do tone ABR thresholds predict the pure-tone behavioral audiogram? Stapells and c o l l e a g ~ e sdemonstrated ~~ high correlations (i.e., > 0.94) between ABR thresholds to 0.5 kHz, 2.0 kHz, and 4.0 kHz air conduction tones in noise masking and the pure-tone behavioral thresholds for infants and young children with normal hearing or SNHL. Their study found no effects of age at ABR on the results; the ABR was equally accurate in predicting young infants’ follow-up behavioral thresholds as it was in predicting those of older children. Moreover, tone-ABR thresholds accurately predicted the pure tone behavioral thresholds in infants and young children with normal hearing or SNHL: 98% were within 30 dB, 80% were within 15 dB, and 66% were within 10 dB. In addition, audiometric configuration (i.e., sloping high frequency, flat, or reverse slope) of the hearing loss did not appear to affect the accuracy of pure-tone behavioral threshold estimation^?^, 38 As with conventional behavioral audiometry, the addition of bone conduction tonal stimuli to ABR threshold protocols provides the clinician with a more complete picture of the type (e.g., conductive, mixed, or sensonneural) and degree of hearing loss. ABRs to 0.5 kHz and 2.0 kHz bone conducted tonal stimuli presented at low stimulus intensities show good frequency specificity in infants and ad~1ts.I~
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Otoacoustic Emissions
Otoacoustic emissions are sounds, generated in the inner ear, that can be recorded by sensitive microphones in the external ear canal.", 29 These sounds are most likely generated by the outer hair cells in the cochlea2*and are an indirect measure of the function of these hair cells. OAEs are not in and of themselves necessary for hearing nor are they a mechanism of hearing, but rather reflect the status of structures that are necessary for hearing (for complete review of OAEs, see Robinette and Glattke33). Although OAEs provide an excellent tool to identify the presence of hearing loss, and to confirm the status of outer hair cell function, their contribution to the quantification of hearing loss or to the definition of degree of hearing loss specifically remains uncertain. Yet the objectivity of OAE measurement makes it ideal for testing individuals who cannot be reliably evaluated with behavioral procedures. With the pediatric population, OAEs offer the clinician the opportunity to obtain ear specific data where other behavioral audiometric measures (i.e., sound field testing) may not be able to provide this information. The two basic categories of OAEs are distinguished by the signals that generate the emissions rather than differences in the underlying cochlear mechanism. Spontaneous Otoacoustic Emissions
Spontaneous OAEs are single- or multiple-frequency, narrow-band signals that are generated by the cochlea in the absence of auditory stimulation. Approximately 50% to 60% of normal ears produce spontaneous OAEs, a percentage that holds for neonates, infants, and adults.3, Spontaneous OAEs are thought to originate from the place in the cochlea that is tuned to that frequency. Evoked Otoacoustic Emissions
Evoked OAEs occur in response to an external auditory stimulus and are present in nearly all normal hearing adults and infants. Various signals can be used to evoke these emissions. Transient signals, such as the click used to evoke the ABR, are effective in generating transient evoked OAEs.%These emissions also can be recorded as acoustic distortion products, which originate in the cochlea as a result of interference (distortion) between two simultaneously presented frequencies (f, and f2) and which together create a combination tone (or distortion product) in the cochlea.*4 Emissions can be recorded relatively quickly, without active participation of the infant or child. As with the ABR, emissions are best recorded from quiet subjects (sleeping, in fact, provides the best recording circumstance). Emissions represent hearing for frequencies that are present in the stimulus; for example, high-frequency stimuli generate high-frequency emissions, and low-frequency stimuli generate low-frequency emissions." Clinical Application
The category of emissions that has the greatest potential for clinical application is evoked OAEs. Because all normally hearing individuals do not have spontaneous OAEs, their diagnostic potential is limited; however, both the transient evoked and the acoustic distortion product emissions show promise as
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tools that can be used to assess hearing in infants and children and to screen for hearing loss in newborns. Evoked emissions are robust, that is, they are found in all normally hearing infants and thus are easily recorded. Neonatal Hearing Screening Both transient evoked and distortion product emissions show promise as effective tools for screening hearing in newborn infants?,u( Potential advantages of OAEs over the ABR are that (1)emissions are a direct assessment of cochlear status and (2) OAEs may prove to be more time-efficient than the ABR for screening purposes. In the few studies that have been carried out comparing current infant hearing screening procedures with OAEs, emissions have been shown to be at least as good an indicator of hearing status as the tool to which it is being compared; however, more large-scale studies of both high-risk and normal newborn infants must be carried out before a clear picture of the sensitivity and specificity of the OAEs can be obtained. #
Estimation of Hearing Using Otoacoustic Emissions OAEs are present in virtually all adults and children in whom hearing is known to be 20 dB HL or better and absent in those in whom hearing levels are 35 dB to 45 dB HL or poorer. Therefore, OAEs have the clinical capability to indicate normal cochlear function when it exists. For pediatric audiology, this is particularly helpful when used in conjunction with other hearing assessment tools, such as the ABR and tests of middle ear function (tympanometry). For example, in children with neurologic involvement, an absent ABR can be the result of either severe cochlear impairment or lack of neural synchrony at the level of the brain stem. A finding of normal OAEs and normal middle ear function indicates normal peripheral (i.e., middle ear and cochlea) functioning, thus isolating the disorder to the brain stem auditory pathway. This finding illustrates an increasingly common audiologic challenge. Normal OAEs in combination with an abnormal ABR represent the hallmark signs in infants, children, and adults of some form of auditory nerve pathology, brain stem neuropathy, or brain stem conduction defect.37 BEHAVIORAL APPROACH
It is possible to approach the assessment of infants and young children behaviorally through operant conditioning paradigms, specifically through an operant discrimination procedure. In an operant discrimination procedure, a stimulus is used to cue the child that a response results in reinforcement. Reinforcement is used to strengthen an easily monitored single response and keep the child in an aroused or motivated state. Maintaining motivation and a high response probability through the use of age-appropriate reinforcement allows clinicians to investigate over time an infant’s or young child’s auditory response behavior. This, then, allows more precise estimation of ability and reduces the habituation found in behavioral assessment without reinforcement (i.e., behavioral observation audiometry). Visual Reinforcement Audiometry
Normally developing infants make head turns toward a sound source in the first few months of life. This localization response represents a behavioral
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“window” through which many aspects of auditory behavior can be evaluated. In visual reinforcement audiometry (VRA), a head-turn response after an auditory stimulus is rewarded with an interesting visual event, usually activation of an attractive three-dimensional animated toy. Without reinforcement, an infant’s responses to sound habituate rapidly and may not occur at low intensity levels. In addition, without reinforcement, the infant’s response depends on the nature of the stimulus. That is, the spectrum of the signal, its center frequency and bandwidth, its intensity level, and its meaningfulness to the child are all variables that can affect the child’s response when no reinforcement is used. As such, VRA has emerged as a successful procedure for infants and young children 6 months to 3 years of age! The success of VRA is certainly related to the fact that the response (head turn) and reinforcer (animated toy) are well suited to the developmental level of children between 6 months and 3 years of age, although there is less success with normally developing children between 2 and 3 years of age because they tend to quickly habituate to the reinforcers. Once the child is under stimulus control, he or she will continue to respond at low sensation levels long enough to provide an estimate of threshold. The clinical validity of results obtained with operant audiometry is well documented. Numerous studies have shown that infant responses differ only slightly from 32. 35, 45, 49 A variety of signals can be tested successfully in the those of sound field and under earphones.26, 49 The availability of insert receivers coupled to an appropriately sized ear tip also can be used with infants. These same transducers also are used during ABR testing, allowing comparisons between test results using the same transducers. Clinical reports shared among clinicians and reports in the literature reveal highly consistent findings from different settings.I6That is, for normally hearing infants, thresholds are consistently obtained within a conservative definition of normal hearing (< 20 dB HL). Moreover, the dispersion of normal responses is sufficiently small that even mild hearing impairments, such as those often accompanying otitis media, can be accurately defined. Comparisons of VRA audiograms in individual children with later audiograms determined with play audiometry show results from the two procedures that are essentially identical. It is generally agreed that, as long as the child is under stimulus control, the thresholds provide, with a high degree of confidence, valid information for making diagnostic and management decisions. Several studies17,44 have reported the use of VRA on children with Down syndrome and other developmental disabilities, suggesting that developmental age can be a determining factor in VRA success. Widen48evaluated VRA as a function of developmental age in high-risk infants. Clearly, the developmentally mature infants were more often tested successfully. Visual reinforcement audiometry was successful for most infants by 5 or 6 months corrected age. An infant’s ability to participate in the VRA task also was compared with their mental age score on the Bayley Scales of Infant Development. When test outcome in VRA was compared with developmental age in a subset of infants, success was achieved in approximately 90% of infants with a developmental age of 5.5 to 6.5 months. Therefore, application of VRA in clinical protocols must consider corrected age adjusted for prematurity rather than chronologic age or developmental age when disparities exist between corrected age and the child’s developmental status. Accurate VRA assessment depends in large part on the ability of one examiner to keep the child appropriately attentive while another assumes the responsibilities of audiometry and operant conditioning. The requirement for two examiners limits the efficiency of VRA; however, audiometric protocol can
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be programmed and peripheral hardware controlled by microcomputer so that a single examiner can accurately and efficiently test infants with VRA. In addition, a single examiner can use a simple, electronic "centering toy" for maintaining a child's attention at midline. This approach does remove the examiner from the test room and may increase test time but still allows the VRA procedure to be completed without compromising accuracy.
Conditioned Play Audiometry
Conditioned play audiometry (CPA) is probably the most common procedure used in the hearing assessment of young children. Through conditioning, children learn to engage in some activity-putting rings on a peg, dropping or stacking blocks-each time they hear the test signal. These activities are assumed to be interesting to children and are used to identify a specific behavior that is used to denote a response tb signal. When teaching children to perform play audiometry, it is usually not difficult to select a response behavior that children are capable of performing. The challenge in play audiometry is teaching the child to wait, listen, and respond when the auditory signal is presented. Conditioned play audiometry follows a model of auditory stimulu-response+reinforcement, in which the play activity is the response and social praise is the reinforcement. Therefore, in addition to teaching the youngster under test the conditioned response in the CPA task, the examiner also must be skilled in delivering social reinforcement at the appropriate time and interval. Audiologic literature suggests that CPA is widely accepted among clinicians who interact with young childrena It is generally recognized that most 3-yearolds can be tested using play audiometry. Yet, how young can children be to achieve successful audiologic outcomes? Thompson and WebeF2 demonstrated the rate of success in obtaining detailed information with CPA is limited for children under the age of 30 months. Yet some 2-year-olds can be conditioned to play audiometry? Moreover, when 2-year-olds are proficient with CPA, they are more likely to provide more responses before habituation than they would if tested by VRA. Because overlap exists between VRA and CPA as suitable techniques with children in this age range, the successful evaluation of a child ultimately depends on the experience of a seasoned clinician. Experience with CPA indicates that reliable threshold responses can be obtained when auditory stimulus-response control has been established and response criterion are maintained. Results from a clinical study5 of 40 preschoolers, aged 30 to 48 months, revealed thresholds at an audiometric level of 10 dB HL or better. These findings were in close agreement with other 4-year old children."
SUMMARY
A behavioral approach is the first choice for hearing assessment in infants and children. It is the only true test of hearing. Physiologic measures are not tests of hearing, only indicators of auditory function. The use of physiologic measures in estimating hearing levels makes some presumptions regarding the concept of hearing. As such, these measures are used when a definitive statement about hearing cannot be made on the basis of behavioral audiometric results, or
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when other factors (eg., age or developmental delay) preclude obtaining reliable behavioral information.
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49. Wilson WR, Moore Jh4: Pure-tone earphone thresholds of infants utilizing visual reinforcement audiometry (VRA). Presented at the American Speech and Hearing Association Convention, San Francisco, 1978 50. Worthington DW, Peters J F Quantifiable hearing and no ABR Paradox or error? Ear Hear 1:281-285, 1980
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