ORIGINAL ARTICLE

Evaluation of noise-induced hearing loss by auditory steady-state and auditory brainstem-evoked responses Karawani, H.,*† Attias, J.,*‡ Shemesh, R.* & Nageris, B.§¶ *Department of Communication Sciences & Disorders, University of Haifa, †Speech and Hearing center, Otolaryngology and Neck and Head Surgery Department, Rambam Health Care Campus, Haifa, ‡Institute for Audiology and Clinical Neurophysiology, Schneider Children’s Medical Center of Israel, §Department of Otolaryngology, Head and Neck Surgery, Rabin Medical Center, Petach Tikva, ¶ Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel Accepted for publication 21 April 2015 Clin. Otolaryngol. 2015, 40, 672–681

Objectives: Noise-induced hearing loss (NIHL) may result from occupational noise exposures and is considered as an ‘Occupational Disease’; therefore, it is compensable. To verify the existence and severity of the work-related hearing loss, there is a need of an objective, reliable auditory measure in cases of arbitration of financial disputes to resolve any medicolegal aspects. The objective of the study was to compare between the ABR and ASSR for predicting the behavioural threshold in subjects with normal hearing or NIHL. Design: The study included 82 subjects regularly exposed to high levels of occupational noise, with normal hearing and NIHL. ABR to clicks and to tone bursts were recorded followed by multiple-frequency ASSR. Physiological and behavioural thresholds were compared for specific frequencies (1000, 2000 Hz) and average of high-frequency range (2000 and 4000 Hz). In addition, Pearson correlations and the specificity and sensitivity of each measure were also

calculated using receiver operating characteristic (ROC) curves. Results: In the NIHL group, there was a significantly smaller difference between the behavioural threshold and click-ABR than the ASSR in high-frequency range. Pearson correlations were significantly higher for click-ABR. Analysis of specific frequencies yielded a smaller difference between behavioural and ASSR than tone-burst-ABR thresholds, with a slightly better correlation for ASSR than tone-burstABR. Higher sensitivity but lower specificity was suggested for ASSR than ABR. Conclusions: ASSR is associated with high-frequency specificity, shorter test sessions and good correlations with behavioural thresholds, making it a potentially better measure than ABR for predicting audiograms in subjects with NIHL. These findings have diagnostic implications, especially in cases of workers’ compensation when subjects may be uncooperative.

Noise-induced hearing loss (NIHL) is the most frequent occupational disease.1 The pattern of the hearing threshold is an essential part of its diagnosis. In the early stages of noise exposure, the most common audiologic indicator of a noiserelated hearing deficit is a ‘notch’ at 4000 Hz.2 With continued exposure, the damage spreads to the high frequencies and later, to the lower frequency range and the speech frequency spectrum (500–2000 Hz).3 At present, NIHL is detected and monitored primarily with behavioural audiometry. When subject unreliability or response inaccuracy is suspected, the test is repeated. This may be problematic in medico-legal cases in which full subject cooperation may not be obtained. Indeed, studies have shown that an

estimated 9–30% of noise-exposed workers exaggerate their hearing loss.4 This factor together with the growing awareness of the harmful effects of noise exposure by both the lay and medical communities have increased the need for an effective objective tool to shorten testing time and to hasten decisions on compensation, rehabilitation and treatment. The appropriate tool would need to fulfil the following criteria: (i) good sensitivity and specificity for high and low frequencies and for various degrees and types of impairment; (ii) objectivity in recording and interpretation of the results; and (iii) with good cost-effectiveness. There is number of electrophysiological measures that have been previously applied to the evaluation of NIHL. Such measures included the cortical auditory evoked potentials (CAEP)5 and the middle latency response (MLR).6 Prasher et al.5 examined the correlation between the N1 amplitude of the cortical auditory evoked potentials and behavioural hearing thresholds at 1000 and 4000 Hz in a

Correspondence: H. Karawani, Department of Communication Sciences & Disorders, University of Haifa, 199 Aba Khoushy Ave, Mount Carmel, Haifa 3498838, Israel. Tel.: +972 52 5617727; Fax: +972 4 8314026; e-mail: [email protected]

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series of consecutively referred medico-legal cases with alleged occupational NIHL. The thresholds of the cortical evoked potentials were within 10 dB for 84% of the cases of NIHL. However, cortical responses are severely affected by the state and the attention of the patient as the amplitude of N1 is said to vary directly with the level of confidence of detection of the stimulus5,7 and with excessive movements of any kind, particularly blinking or chewing. Regarding the MLRs, they may be recorded by frequency-specific brief stimuli such as tone bursts to assess hearing threshold evaluation of NIHL.6 In that study, it has been reported that the MLR and behavioural thresholds agreed within 10 dB in 91% of the cases of the NIHL group. However, narrowspectrum stimuli such as tone bursts and decrease in intensity levels reduce the degree of synchronous firing and weaken the reproducibility of the evoked response.8 This less synchronous firing, makes the MLR threshold difficult to be identified by the audiologist, and due to the low-band analog filter, more noises interfere with the MLR signal. Similar to the cortical evoked potentials, the MLR are severely affected by sedation.9 Another objective physiological measure is the otoacoustic emissions (OAE). Since their introduction,10 OAEs have gradually become a significant tool both in clinical audiology, particularly in hearing screening and in investigations of fine cochlear function. Clinical evidence indicated that the presence of OAE is associated with thresholds within normal limits. In addition, its recording in the external ear canal excludes middle ear and external ear conduction problems. As OAE cannot determine the severity of the impairment and only is used to filter normal frequency range, auditory brainstem response (ABR) is usually applied to be used as an objective tool to determine the severity of the impairment. Click-ABR is a well-recognised electrophysiological method for the assessment of hearing thresholds, particularly at high frequencies. The click-ABR threshold has been found to be within 6–20 dB of the behavioural threshold.11 However, click-ABR provides information primarily in the narrow range of 2000–4000 Hz12,13 and may underestimate or miss hearing loss restricted to other frequency regions,14 such as the low, notched and very high-frequency losses induced by noise exposure. In addition, technically, clickABR cannot be used to assess severe NIHL because stimulation at high intensities cannot be reached. Using ABR to tone bursts (tone-burst-ABR) makes the procedure more frequency specific and more easily correlated with behavioural thresholds at low frequencies. However, some studies have questioned the reliability of thresholds estimation in the low-frequency tone-burst range.15 ABR thresholds to tone-bursts were found to have a large difference from behavioural thresholds in subjects with sensorineural hearing loss (SNHL), measuring 27 dB at © 2015 John Wiley & Sons Ltd  Clinical Otolaryngology 40, 672–681

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500 Hz, 24 dB at 1000 Hz, 16 dB at 2000 Hz and 11 dB at 4000 Hz.16 Furthermore, applying both click- and toneburst-ABR requires subjective judgments of the waveforms, and a long test duration is necessary to perform the threshold evaluation at different frequencies and in both ears, as accepted for NIHL.17 Researchers have suggested that the auditory steady-state response (ASSR), first described by Galambos et al.,18 may serve as an alternative electrophysiological method to estimate behavioural thresholds. Responses are elicited by continuous tones modulated in amplitude and/or frequency rather than by transient stimuli,19 and multiple thresholds can be rapidly valuated at up to four frequencies for both ears simultaneously,20 thereby shortening test time.21 In addition, the ASSR is objective (responses are processed by statistical analysis) and frequency specific and is not affected by the state of the subject for modulation rates higher than 70 Hz.22 Attias et al.23 assessed the value of multifrequency ASSR in predicting behavioural warble-tone audiograms in a large sample of subjects with NIHL of varying severity. Pearson correlation coefficients ranged from 0.6 to 0.8 over the four frequencies tested (500, 1000, 2000, 4000 Hz), supporting earlier findings of Hsu et al.24 Differences between ASSR and behavioural thresholds ranged from 10 dB to 13 dB, and ASSR had a specificity and sensitivity of up to 92%. The main aims of this study were to evaluate hearing thresholds predicted by ASSR or by click- and tone-burstABR in subjects with normal hearing or NIHL. Specifically, we compared the average behavioural threshold for 2000 and 4000 Hz (avg-2,4-behavioural) to click-ABR and average ASSR for the same frequency range (avg-2,4-ASSR) and also the behavioural threshold for 1000 and 2000 Hz to toneburst-ABR and ASSR for the same specific frequencies. Pearson product correlations were calculated between each of them and the behavioural thresholds, and the sensitivity and specificity of ASSR and ABR in differentiating subjects with NIHL or normal hearing were determined. Subjects and methods Ethical considerations

Subjects provided written informed consent to participate in the study in accordance with the guidelines of the Institutional Review Board of the University of Haifa. Subjects

The study sample included 82 male subjects between the ages of 22–45 (164 ears) regularly exposed to high levels of occupational noise. The subjects were randomly selected

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from 1200 workers who attended the Audiological Clinical Center of the University of Haifa in 2009–2011 as part of their periodic evaluation for NIHL. All were enrolled in the annual periodic obligated hearing examinations for noiseexposed workers. The nature of the noise exposure was for most of the subjects a combination of industrial (continuous noise exposure) and military (impulsive noise exposure) types. Ten subjects were excluded because a documented ear infection, mixed or conductive hearing loss, or fluctuating, rapidly progressive or retrocochlear loss. Normal middle ear function was confirmed in all subjects by tympanometry and/or otoacoustic emissions on the day of testing. Subjects underwent behavioural pure-tone assessment and, on the basis of the results, were divided into two groups: bilateral normal hearing (control) or bilateral symmetrical (≤10 dB difference between ears for the same frequency) NIHL. Normal hearing was defined as a threshold of up to 20 dB HL for frequencies of 250–8000 Hz.25 NIHL was defined as a permanent hearing threshold of 25 dB HL or higher at multiple frequencies of 250–4000 Hz combined with the typical audiogram configuration of bilateral and symmetrical cochlear hearing loss with a possible notch at 3000–6000 Hz and with worse thresholds at high than at low frequencies. In a small portion of the noise-exposed subjects, audiograms showed deterioration in the mid–low frequencies in addition to that in the high frequencies, probably due to the repeated noise occupational exposures. All audiological tests were carried out by skilled audiologists. Behavioural warble-tone threshold

The behavioural tone thresholds were retested in doublewalled, sound-attenuated rooms with calibrated AC-40 audiometers (Interacoustic A/S, Assens, Denmark). The stimulus consisted of a warble tone that deviated 5% in frequency at a rate of 5 Hz. This stimulus was chosen as a more suitable match to the ASSR stimuli. As there were no significant differences between pure-tone and warble-tone thresholds, the warble-tone threshold was also used for comparisons with the click- and tone-burst-ABR. Airconduction thresholds were measured in each ear using insert earphones (EARTONEâ 5A; Auditory Systems, Indianapolis, IN, USA) at 250–8000 Hz; bone-conduction thresholds were measured using a B-71 Radioear vibrator at 250–4000 Hz. Threshold levels were determined by a 10 dB-down/5 dB-up approach.26 Clinical masking was used if necessary or warranted by the clinical audiologic data. The hearing results were included in the study only if the behavioural audiograms were considered reliable by the audiologists. An audiogram was addressed as reliable only if the pure-tone average met the speech reception threshold,

and the configuration of the audiogram fitted NIHL type or a deteriorated NIHL. Electrophysiological responses

All electrophysiological responses were assessed in a soundattenuated room with the subjects in the supine position. Subjects were told to relax, and most of them slept through the test. The Bio-logic MASTER Version 2.02 (Biologic System Corp., Mundelein, IL, USA), Bio-logic insert earphones (580-SINSER) and scalp electrodes were used in all cases. The impedance was 5 kO or less for each electrode, with a difference of 3 kO or less between electrodes. Auditory brainstem response (ABR)

Click-ABR. Monaural brainstem responses were elicited by acoustic clicks of 100 ls duration. Two blocks of click stimuli (2000 rarefaction sweeps each) were collected. Potentials were collected from Ag–AgCl electrodes located at Cz (active) and referenced to the right earlobe, with the left earlobe as ground. Clicks were presented at a rate of 13.3/s and recorded with a 10.66 ms recording window. Responses were filtered on line from 30 Hz to 3000 Hz. Sweeps with activity exceeding +25 lV were rejected from the average, and data collection continued until the target number of artefact-free responses was obtained. For threshold determination, stimuli were first presented at an intensity of 80 dB HL to determine the neurological waveform morphology (to exclude retrocochlear lesions) and the absolute latencies of all waves of interest were recorded. Wave V was identified and marked for each subject as a data point on the waveform before the negative slope that follows the wave. A normal click evoked response latency was defined as occurring within two standard deviations of the normal population.27 Recording continued until the lowest intensity at which wave V could be identified. Threshold of the ABR was obtained by a decrease of 10 dB increments. At threshold levels, recordings beyond 2000 sweeps were collected to verify conclusions regarding the presence or absence of a brain response and an increase of 5 dB increments were used to obtain threshold. The latencies of all waves of interest were identified by one clinician (H.K.) and confirmed by another (J.A.). The second clinician was blinded to the audiograms of the participants at the time the waveforms were examined. Only agreed results were included in the study. Tone-burst-ABR. Tone-burst-ABR thresholds were tested at 1000 and 2000 Hz and compared with ASSR thresholds at the same frequencies. Responses were collected in the same manner for both electrophysiological tests, during the same © 2015 John Wiley & Sons Ltd  Clinical Otolaryngology 40, 672–681

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recording session, in the same room. Tone-burst-ABR was evoked with a 2 ms rise and fall time without plateau (2-0-2), using a Blackman filter. Stimuli were presented at a rate of 13.3/s and recorded with a 0–20 ms recording window. Responses were filtered on line from 30 Hz to 3000 Hz. Sweeps with activity exceeding +25 lV were rejected from the average, and data collection was continued until the target number of artefact-free responses was obtained. Two blocks of 2000 sweeps were recorded at each intensity level. Like for click-ABR, stimuli were first presented at an intensity of 80 dB HL, with a decrease of 10 dB and increase of 5 dB increments to obtain thresholds. Minimum intensity was 10 dB. The latencies of all waves of interest were identified by one clinician (H.K.) and confirmed by another (J.A.). The second clinician was blinded to the audiograms of the participants at the time the waveforms were examined and only agreed results were included in the study. Auditory steady-state response (ASSR)

Potentials were collected from scalp electrodes located at Cz (active) and referenced to the midline posterior neck (about 7 cm below the inion), with the right earlobe as ground. Carrier frequencies were matched to the audiometric frequencies: 500, 1000, 2000 and 4000 Hz. The corresponding modulation frequencies (AM/FM) were 82, 84, 87 and 89 Hz for the left ear, and 91, 94, 96 and 98 Hz for the right ear. These values were selected on the basis of earlier findings that high modulation rates are less affected by the state of subject arousal and that higher frequency modulators tend to show less of an interaction between carriers21 and exhibit lower growth function slopes.28 Each auditory stimulus consisted of a sinusoidal tone with a carrier frequency that was 25% frequency modulated and 100% amplitude modulated. A relative phase of 270° between the AM and FM components was chosen to elicit the largest combined response.29 All stimuli were routed through an Amplaid audiometer (Amplaid 319, Amplifon, Via Donizetti, Milan, Italy) and presented to both ears simultaneously through Bio-logic insert earphones (580SINSER) with foam earplugs. ASSR stimuli were calibrated at HL in the MASTER setup using the reference values reported by Wilber et al.30 who reviewed five studies of pure-tone hearing thresholds in normal-hearing subjects at a frequency range of 125–8000 Hz and calibration with a 2-cc coupler. To verify the stimulus intensities at 500, 1000, 2000 and 4000 Hz used in the ASSR, they were also measured with the Bruel & Kjaer (Naerum, Denmark) 2613 amplifier and a 2120 frequency processor coupled to a 4153 microphone. All measured intensities were well correlated (2 dB) to the normative dB SPL calibration data listed in the MASTER software. © 2015 John Wiley & Sons Ltd  Clinical Otolaryngology 40, 672–681

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In the dichotic multiple-frequency test, the initial stimulation level was 80 dB HL. If clear responses were recorded, the level was reduced in 10 dB increments until no responses were recorded, and then increased of 5 dB increments to determine the threshold at which a significant response was elicited. When there was no response to a level of 80 dB HL in the multicarrier condition, a single specific modulated tone of up to 132 dB SPL was presented. This minimised the possibility of undesired interactions between the carriers at levels above 80 dB HL. The audiologist who determined the electrophysiological threshold was blinded to the behavioural audiogram results. Responses were collected at a sampling rate of 1200 Hz at 16-bit resolution. The electroencephalography (EEG) responses were amplified using a gain of 10 000 at a filter band pass of 3–300 Hz (12 dB/octave). The data were recorded in epochs containing 1024 points; one response epoch lasted 0.853 s. Sixteen data epochs were collected and linked together to form one sweep with an overall duration of 13.653 s. Epochs that contained electrophysiological activity exceeding 25 lV were rejected and the next acceptable epoch was used to build the sweep. Once completed, each sweep was averaged in the time domain and subsequently analysed by fast Fourier transform (FFT) to yield an amplitude spectrum with a resolution of 0.0732 Hz. To determine whether the response at the modulation frequency was significantly different from the background EEG activity in neighbouring frequencies, we used the F ratio to compare the amplitude at the modulation frequency with the average amplitude of the noise in 120 adjacent frequency bins (60 bins above and 60 bins below the modulation frequency, i.e. 4.4 Hz). A response was accepted as present if the F ratio, calculated against the critical values for F at 2 d.f. and 240 d.f., was significant at P < 0.05.29,31 In multiple-frequency presentations, a response was considered present when three criteria were met: P < 0.05, noise level 0.9 for both electrophysiological methods for 2000 Hz (P < 0.01). There was no significant difference in the relationship of the behavioural threshold with either of the electrophysiological tests. Sensitivity and specificity – ROC analysis

ROC curves for predicting hearing thresholds by ASSR and ABR for 1000 and 2000 Hz are depicted in Figs 4 and 5,

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respectively, and the average of 2000 and 4000 Hz was also studied. For screening hearing thresholds at 1000 Hz, the AUC was 0.89 for ASSR and 0.82 for tone-burst-ABR. ROC curves (Fig. 4) suggested a cut-off of 37.5 for the ASSR to gain maximal sensitivity (85.7%) and specificity (76.9%) at 1000 Hz (P < 0.001). The same cut-off was suggested for the tone-burst-ABR test, although the maximal sensitivity (71.4%) and specificity (80.8%) gained were lower than for ASSR (significant difference in sensitivity, P < 0.01). For predicting hearing thresholds at 2000 Hz, the same AUC values were obtained for both ASSR and tone-burst-ABR, with better sensitivity and specificity, reaching almost 1 (AUC = 0.99, P < 0.001). There was no significant difference between the two electrophysiological methods, suggesting similar cut-off values to reach similar maximal sensitivity and specificity for tone-burst-ABR (35 dB, 95%, 83%, respectively) and ASSR (37 dB, 95%, 80%, respectively). For predicting the average hearing threshold at high frequencies; higher true-positive rates and lower falsepositive rates were achieved for avg-2,4-ASSR than for click-ABR. However, the AUC was slightly better for clickABR (0.89 versus 0.83). For the avg-2,4-ASSR threshold, the cut-off value to gain maximal sensitivity (93.2%) and specificity (70%) was 45.87 dB; for click-ABR, the value was 42.5 dB, which yielded 83% sensitivity and 80.8% specificity.

1000 Hz

Sensitivity

1.10

Reference line Tone burst-ABR ASSR

0.00 –0.1

Fig. 4. Receiver operating characteristic curve analysis of ability of ASSR (solid line) and tone-burst-ABR (dashed line) to detect normal and abnormal thresholds in all subjects for 1000 Hz.

The physiological findings were compared with behavioural audiometry, by Pearson correlations and calculated ROC curves. Average behavioural thresholds for frequencies of 2000 and 4000 Hz were compared with click-ABR and average ASSR thresholds in the same range, and behavioural thresholds for 1000 and 2000 Hz were compared with toneburst-ABR and ASSR for the same frequencies. The results showed that the click-ABR threshold was significantly closer to the avg-2,4-behavioural than the avg-2,4-ASSR threshold. Specificity was higher for click-ABR (80.8%) than for

Discussion

The present study is the first to compare the efficacy of ASSR and ABR in predicting behavioural thresholds in subjects with NIHL and normal hearing.

P < 0.01

P < 0.01

(b)

t

t

(a)

1.0

1 - Specificity

t

t

Fig. 3. Relationship between behavioural thresholds (vertical axis) and ASSR (triangle) and tone-burst (TB)-ABR (diamond) thresholds (horizontal axis). Linear regressions are shown for ASSR (solid line) and tone-burst-ABR (dashed line) for (a) 1000 Hz and (b) 2000 Hz. Correlation coefficients (r) appear on the upper right. © 2015 John Wiley & Sons Ltd  Clinical Otolaryngology 40, 672–681

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Fig. 5. Receiver operating characteristic curve analysis of ability of ASSR (solid line) and tone-burst ABR (dashed line) to detect normal and abnormal thresholds in all subjects for 2000 Hz.

avg-2,4-ASSR (70%), but sensitivity was better for avg-2,4ASSR (93% versus 83%). The smaller difference between the behavioural and click-ABR thresholds may indicate that average hearing in the region of 2000–4000 Hz can best be predicted by click-ABR, in agreement with previous reports in SNHL.13,33 The reason for this finding is unclear, but it may be attributable to the good synchronisation of the auditory system to clicks. This is not true for the pure-tone stimuli in the steady-state test, which need to be stronger and more intense to provoke a response, although once the response is achieved, the correlation between the severity of impairment and the ASSR results would be similar to that for the ABR. However, previous studies have shown that clickABR cannot differentiate between hearing losses in the severe and profound ranges,13,35 and in subjects with NIHL, clickABR or avg-2,4-ASSR alone may not be appropriate to predict the severity and configuration of the hearing loss because low tone and very high-frequency hearing losses may be missed.36 When measuring responses to specific frequencies, we noted a difference, albeit not significant, between the two electrophysiological measures. For predicting the behavioural threshold for a frequency of 1000 Hz, ASSR with a cutoff value of 37.5 dB had better sensitivity (86%) and specificity (77%) than tone-burst-ABR (81% and 71%, respectively). Moreover, the ASSR threshold was closer to the behavioural threshold at this frequency (difference of 12.9 dB) than the tone-burst-ABR threshold (difference of © 2015 John Wiley & Sons Ltd  Clinical Otolaryngology 40, 672–681

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15.5 dB), with a slightly better Pearson correlation (0.7 versus 0.6). For predicting the behavioural threshold for 2000 Hz, both physiological measures had excellent sensitivity (95%) and good specificity (80%). We did not test tone-burst-ABR to 500 Hz because others have shown that this procedure is very difficult to perform and the prediction error is large, up to 40–50 dB.37 However, we were able to predict behavioural thresholds at 500 Hz using the ASSR. The difference between the measures was 13.9 dB (Table 1). The predictive ability of electrophysiological methods at low frequencies is important for assessing speech thresholds, which are used to determine the extent of compensation and the need for hearing rehabilitation. We also did not test the correlation of ASSR and tone-burst-ABR thresholds for 4000 Hz because tone-bursts at that frequency are rarely used in the clinical setting to evaluate adults with NIHL, and click-ABR provides a good estimate of the highfrequency region. Our findings are similar to earlier reports on SNHL38 (not noise-induced hearing loss) showing a similar correlation between behavioural thresholds and both ASSR and ABR thresholds.39 However, ABR may be a harder-to-use and less efficient tool than ASSR for predicting the full audiogram of subjects with NIHL. Multifrequency ASSR has several important advantages in this context. (i) It provides frequency-specific estimates of hearing thresholds22 with high reliability40 using either air- or bone-conduction signals.20 (ii) It uses continuous tones which are not subject to the spectral distortion associated with tone bursts or clicks.41 (iii) If each stimulus is modulated at different rates, thresholds can be evaluated for all frequencies for both ears simultaneously.20,42 This can significantly reduce the duration of the test without affecting its predictive efficacy, as reported in studies of subjects with SNHL.43 In the present study, the ABR method required double the testing time of multifrequency ASSR (500, 1000, 2000 and 4000 Hz) for individual subjects with NIHL. This factor has direct ramifications for clinical applications (human resources, equipment and analysis time). Increasing the stimulus rate of the ABR would have decreased the time of the test duration in the ABR. However, the time of the ASSR recording session would still be shorter, because in ASSR, simultaneously in one test recording one can get all the information needed (four frequencies for both ears) while in ABR, to obtain the results, sequential recording with breaks is needed (six recording sessions: click-ABR, tone-burstABR for 1000 Hz, 2000 Hz for the two ears). (iv) Responses are identified immediately and interpreted objectively with statistical measures, eliminating the need for subjective judgments by the audiologist during waveform analysis. By contrast, ABR requires clinician experience and specific skills to achieve repeatable identification of a response, especially

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when tone-bursts are used. Studies have shown that the variability in the subjective evaluation of ABR results can change the threshold by 10 dB or more.44 This is important in determinations of the degree of workers’ compensation in cases of NIHL. (v) The continuously modulated tones can be presented at higher levels, eliciting responses in subjects with hearing loss of up to 132 dB, and can be used to assess ears with only minimal amounts of residual hearing.35 In the ~20% of subjects in this study with severe NIHL, brainstem responses to clicks or tone bursts could not be recorded, whereas steady-state responses were reliably obtained. This is very important for identifying cochlear implant candidates with bilateral profound hearing loss.12 (vi) Overall, the sensitivity of ASSR, especially to high frequencies, is important for determining the frequencies at which thresholds are impaired in subjects with NIHL. With this regard, as NIHL is a compensable occupational disease and because of the growing awareness among noise-exposed workers, ASSR may provide a valuable objective tool for the evaluation of disability percentage associating NIHL. This is in line with previous reports12,23 showing similar sensitivity in subjects with SNHL and NIHL. (vii) ASSR can be applied for adjustment of hearing aids using free-field simulations.45 To date most of the auditory objective diagnosis is made by ABR to clicks and tone-bursts to either air conduction or bone conduction, and in that case the implication of the whole test procedure takes significant time. Both physiological measures had relatively low specificity but high sensitivity and are therefore less efficient for the detection of frequencies with normal thresholds, as noted previously in studies of ASSR23 and ABR.36,46 Therefore, we strongly recommend initial screening frequencies within normal thresholds with OAEs, which has been found to have very good sensitivity47 followed by ASSR testing of frequencies that failed the OAE. This combination could further enhance the application of efficient electrophysiological system for the clinical diagnosis of subjects with NIHL. Keypoints

• • • •

The ABR and ASSR for predicting the behavioral thresholds in subjects with NIHL were compared. ABR to clicks and to tone bursts followed by multifrequency ASSR were recorded in the current study. Specificity and sensitivity of the ABR and ASSR were calculated. Click-ABR yielded better correlation with the behavioral measure in high-frequency range. However, analysis of specific frequencies yielded a better correlation for the ASSR than the ABR.

•

ASSR is associated with better frequency specificity, shorter test sessions and good correlations with behavioral thresholds, making it a potentially better measure than ABR for predicting audiograms in subjects with NIHL.

Acknowledgements

The study was supported by The National Insurance Institute, Jerusalem, Israel. A portion of this research was presented at 10th EFAS Congress, 22 June 2011 to 25 June 2011, Warsaw, Poland, and at ISAR 2011 Scientific Meeting, October 25th, Tel Aviv, Israel. Conflict of interest

The authors declare no conflict of interest. References 1 McBride D.I., Firth H.M. & Herbison G.P. (2003) Noise exposure and hearing loss in agriculture: a survey of farmers and farm workers in the Southland region of New Zealand. J. Occup. Environ. Med. 45, 1281–1288 2 Taylor W., Pearson J., Mair A. et al. (1965) Study of noise and hearing in jute weaving. J. Acoust. Soc. Am. 38, 113–120 3 Chen T., Chiang H. & Chen S. (1992) Effects of aircraft noise on hearing and auditory pathway function of airport employees. J. Occup. Med. 34, 613–619 4 Rickards F.W. & De Vidi S. (1995) Exaggerated hearing loss in noise induced hearing loss compensation claims in Victoria. Med. J. Aust. 163, 360 5 Prasher D., Mula M. & Luxon L. (1993) Cortical evoked potential criteria in the objective assessment of auditory threshold: a comparison of noise induced hearing loss with Meniere’s disease. J. Laryngol. Otol. 107, 780–786 6 Xu Z.M., De Vel E., Vinck B. et al. (1996) Middle-latency responses to assess objective thresholds in patients with noise-induced hearing losses and Meniere’s disease. Eur. Arch. Otorhinolaryngol. 253, 222–226 7 Squires K.C., Squires N.K. & Hillyard S.A. (1975) Decision related cortical potentials during an auditory signal detection task with cued observation intervals. J. Exp. Psychol. Hum. Percept. Perform. 1, 268–279 8 Wilson M. & Dobie R. (1987) Human short-latency auditory response obtained by cross-correlation. Clin. Neurophysiol. 66, 529–538 9 Goff W.R., Allison T., Lyons W. et al. (1977) Origins of short latency auditory evoked potentials in man. In Progress in Clinical Neurophysiology: Auditory Evoked Potentials in Man, Desmedt J.E. (ed.), pp. 30–44. Karger, Basel, Switzerland. 10 Kemp D.T. (1978) Stimulated acoustic emissions from within the human auditory system. J. Acoust. Soc. Am. 64, 1386–1391

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11 Pratt H. & Sohmer H. (1978) Comparison of hearing threshold determined by auditory pathway electric responses and by behavioural responses. Int. J. Audiol. 17, 285–292 12 Attias J., Buller N., Rubel Y. et al. (2006) Multiple auditory steadystate responses in children and adults with normal hearing, sensorineural hearing loss, or auditory neuropathy. Ann. Otol. Rhinol. Laryngol. 115, 268–276 13 Brookhouser P.E., Gorga M.P. & Kelly W.J. (1990) Auditory brainstem response results as predictors of behavioral auditory thresholds in severe and profound hearing impairment. Laryngoscope 100, 803–810 14 Picton T.W. (1978) The strategy of evoked potential audiometry. In Early Diagnosis of Hearing Loss, Gerber S.E. & Mencher G.T. (eds), pp 297–307. Grune & Stratton, New York 15 Laukli E., Fjermedal O. & Mair I. (1988) Low-frequency auditory brainstem response threshold. Scand. Audiol. 7, 171–178 16 Beattie R.C., Johnson A. & Garcia E. (1996) Frequency-specific auditory brainstem responses in adults with sensorineural hearing loss. Int. J. Audiol. 35, 194–203 17 Stapells D.R. (2002) The tone-evoked ABR: why it’s the measure of choice for young infants. Hear. J. 55, 14–18 18 Galambos R., Makeing S. & Talmachoff P. (1981) A 40 Hz auditory potential recorded from the human scalp. Proc. Natl Acad. Sci. USA 78, 2643–2647 19 Rickards F., Tan L., Cohen L. et al. (1994) Auditory steady-state evoked potential in newborns. Br. J. Audiol. 28, 327–337 20 Lins O.G., Picton T.W., Boucher B.L. et al. (1996) Frequencyspecific audiometry using steady-state responses. Ear Hear. 17, 81 21 Picton T.W., van Roon P. & John M.S. (2009) Multiple auditory steady state responses (80-101 Hz): effects of ear, gender, handedness, intensity and modulation rate. Ear Hear. 30, 100 22 Picton T.W., John M.S. & Dimitrijevic A. (2003) Human auditory steady-state responses. Int. J. Audiol. 42, 177–219 23 Attias J., Karawani H., Shemesh R. et al. (2014) Predicting hearing thresholds in occupational noise-induced hearing loss by auditory steady state responses. Ear Hear. 35, 330–338 24 Hsu R.F., Chen S.S., Lu S.N. et al. (2011) Dichotic multiplefrequency auditory steady-state responses in evaluating the hearing thresholds of occupational noise-exposed workers. Kaohsiung J. Med. Sci. 27, 330–335 25 ANSI. (1989) Specifications for audiometers (ANSI S3.6-1989). New York, American National Standards Institute. 26 Carhart R. & Jerger J.J. (1959) Preferred method for clinical determination of pure-tone thresholds. J. Speech Hear. Res. 24, 330–345 27 Hall J.W. (1992) Handbook of auditory evoked responses. Needham Heights, Mass, Allyn & Bacon. 28 Lins O.G., Picton P.E., Picton T.W. et al. (1995) Auditory steadystate responses to tones amplitude-modulated at 80–110 Hz. J. Acoust. Soc. Am. 97, 3051–3063 29 John M.S., Purcell D.W., Dimitrijevic A. et al. (2002) Advantages and caveats when recording steady-state responses to multiple simultaneous stimuli. J. Am. Acad. Audiol. 13, 246–259 30 Wilber L.A., Kruger B. & Killion M.C. (1988) Reference thresholds for the ER-3A insert earphone. J. Acoust. Soc. Am. 83, 669–676

© 2015 John Wiley & Sons Ltd  Clinical Otolaryngology 40, 672–681

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31 Picton T.W., Durieux-Smith A. & Champagne S.C. (1998) Objective evaluation of aided thresholds using auditory steady-state responses. J. Am. Acad. Audiol. 9, 315–331 32 Zweig M.H. & Campbell G. (1993) Receiver-operating characteristic (ROC) plots: a fundamental evaluation tool in clinical medicine. Clin. Chem. 39, 561–577 33 Lin Y.-H., Ho H.-C. & Wu H.-P. (2009) Comparison of auditory steady-state responses and auditory brainstem responses in audiometric assessment of adults with sensorineural hearing loss. Auris Nasus Larynx 36, 140–145 34 Vander Werff K.R., Brown C.J., Gienapp B.A. et al. (2002) Comparison of auditory steady-state response and auditory brainstem response thresholds in children. J. Am. Acad. Audiol. 13, 227–235 35 Rance G., Dowell R.C., Rickards F.W. et al. (1998) Steady-state evoked potential and behavioral hearing thresholds in a group of children with absent click-evoked auditory brain stem response. Ear Hear. J. 19, 48–61 36 Stapells D.R., Picton T.W., Durieux-Smith A. et al. (1990) Thresholds for short-latency auditory-evoked potentials to tones in notched noise in normal-hearing and hearing-impaired subjects. Int. J. Audiol. 29, 262–274 37 Stapells D.R. (2000) Frequency-specific evoked potential audiometry in infants. 38 Johnson T.A. & Brown C.J. (2005) Threshold prediction using the auditory steady-state response and the tone burst auditory brain stem response: a within-subject comparison. Ear Hear. J. 26, 559–576 39 Aoyagi M., Yamazaki Y., Yokota M. et al. (1995) Frequency specificity of 80-Hz amplitude-modulation following response. Acta Otolaryngol. Suppl. 522, 6–10 40 Hsu W.C., Wu H.P. & Liu T.C. (2003) Objective assessment of auditory thresholds in noise-induced hearing loss using steady-state evoked potentials. Clin. Otolaryngol. 28, 195–198 41 Rance G. & Rickards F. (2002) Prediction of hearing threshold in infants using auditory steady-state evoked potentials. J. Am. Acad. Audiol. 13, 236–245 42 Lins O.G. & Picton T.W. (1995) Auditory steady-state responses to multiple simultaneous stimuli. Electroencephalogr. Clin. Neurophysiol. 96, 420–432 43 Picton T.W., Dimitrijevic A., Perez Abalo M.C. et al. (2005) Estimating audiometric thresholds using auditory steady-state responses. J. Am. Acad. Audiol. 16, 140–156 44 Vidler M. & Parker D. (2004) Auditory brainstem response threshold estimation: subjective threshold estimation by experienced clinicians in a computer simulation of the clinical test. Int. J. Audiol. 43, 417–429 45 Shemesh R., Attias J., Hassan M. et al. (2012) Prediction of aided and unaided audiograms using free-field auditory steady-state evoked responses. Int. J. Audiol. 51, 746–753 46 Picton T.W., Ouellette J., Hamel G. et al. (1979) Brainstem evoked potentials to tone pips in notched noise. J. Otolaryngol. 8, 289–314 47 Prieve B.A., Gorga M.P., Schmidt A. et al. (1993) Analysis of transient-evoked otoacoustic emissions in normal-hearing and hearing-impaired ears. J. Acoust. Soc. Am. 93, 3308–3319