Introduction
Pseudohypacusis has been defined as functional or non-organic hearing loss, the basis of which can be conscious (malingering) or unconscious (psychogenic).Reference Martin1, Reference Rintelmann, Schwann and Blakley2 For various medico-legal or financial reasons, some patients may clinically demonstrate an exaggerated hearing loss that varies in degree, nature and laterality, such as a unilateral profound hearing loss or bilateral mixed hearing loss.Reference Qiu, Yin, Stucker and Welsh3 On the other hand, some patients may feign better thresholds in the presence of genuine hearing impairment, in order to conceal a handicap. For example, feigning good hearing may occur during applications for such jobs as firefighter, police officer, teacher, physician and soldier.Reference Qiu, Yin, Stucker and Welsh3 Thus, pseudohypacusis is encountered fairly often in clinical practice, with a prevalence in adults of 9–45 per cent.Reference Gould and Hunsaker4–Reference Barrs, Althoff, Krueger and Olsson6
Standard audiological evaluation may include audiometry, tympanometry and acoustic reflex testing. Other diagnostic tests reported in the literature include the Bekesy test,Reference Chaiklin7 Lombard test and delayed auditory feedback.Reference Alberti and Beagley8 The Stenger test is widely used to evaluate unilateral or asymmetrical pseudohypacusis.Reference Rintelmann, Schwann and Blakley2 Although there are many ways to determine the presence of malingering, a rapid, objective and validated test to validate the audiogram has not been established. Electro-physiological responses are often used to fulfill this role.
Over the past two decades, auditory brainstem response (ABR) testing has been well documented as an objective means of evaluating hearing thresholds. Auditory brainstem responses elicited by click stimuli have less frequency specificity and usually only reflect average hearing in the 2000–4000 Hz region.Reference Brookhouser, Gorga and Kelly9, Reference Kileny and Magathan10 Such testing generates no low tone information, e.g. 500–1000 Hz. Auditory brainstem response testing elicited by tone burst stimuli can be estimated with reasonable accuracy in the mid-range to high frequencies. However, greater variability in the lower frequencies limits our ability to predict behavioural thresholds from ABR thresholds.Reference Stapells, Picton, Durieux-Smith, Edwards and Moran11 Clicks and tone bursts are typically restricted to presentation levels up to 90 dBHL; thus, both these ABR procedures are usually insufficient in assessing profound hearing loss.
Auditory steady-state responses are continuous, scalp-recorded potentials that arise in response to auditory stimuli which vary periodically over time, such as sinusoidal amplitude- and frequency-modulated tones.Reference Kuwada, Batra and Maher12, Reference Lins, Picton and Picton13 The response is generated when the stimulus tones are presented at a rate that is sufficient to cause an overlapping of transient potentials. This response represents the synchronous discharge of auditory neurons in the brainstem, phase-locked to the modulation frequency of the carrier stimulus. Continuous tones do not suffer the spectral distortion associated with brief tone bursts or clicks. Therefore, they are relatively frequency-specific. This specificity can be used to estimate the auditory threshold across the audiometric range.Reference Wu, Hsu and Chu14, Reference Rance, Rickards, Cohen, De Vidi and Clark15
Recently, auditory steady-state response testing has become available as an objective hearing test option for both hearing-impaired adults and young children.Reference Wu, Hsu and Chu14–Reference Lins, Picton, Boucher, Durieux-Smith, Champagne and Moran17 However, obtaining a complete audiogram with a single modulated frequency can be very time-consuming.Reference Wu, Hsu and Chu14 Traditionally, threshold-seeking procedures using auditory evoked responses are performed separately for each explored ear and each stimulus frequency (using 5-dB intensity steps). Unfortunately, the time required is not feasible in certain, time-critical clinical contexts, such as assessment of babies, small children and uncooperative adults.Reference Perez-Abalo, Savio and Torres18
The multi-channel auditory steady-state response is an optimised variant of the 75 to 110 Hz steady state response, which uses multiple simultaneous amplitude-modulated tones. It was first proposed by Lins and Picton.Reference Lins and Picton19 It relies on the fact that four different amplitude modulated tones, each with a particular carrier frequency and modulation frequency, can be combined into one complex acoustic stimulus which is capable of simultaneously activating different regions of the cochlea. Hence, by using a multiple frequency stimuli composed of 500, 1000, 2000 and 4000 Hz amplitude modulated frequencies, these four frequency-specific thresholds can be evaluated simultaneously. The technique can be further optimised by presenting two differently modulated multiple frequency stimuli to the left and right ears simultaneously.Reference Perez-Abalo, Savio and Torres18 In this way, auditory steady-state response thresholds for four frequencies can be recorded in both ears at the same time. This type of simultaneous stimulation has been proven to be a time-efficient method of determining auditory steady-state response thresholds.Reference Lins, Picton, Boucher, Durieux-Smith, Champagne and Moran17, Reference Perez-Abalo, Savio and Torres18
Most studies on hearing-impaired adults using auditory steady-state response testing have used mono-aural single channel testing. The use of multi-channel auditory steady-state response testing to estimate frequency-specific thresholds has not been clinically validated.
This study investigated the relationship between pure tone thresholds and multi-channel auditory steady-state response thresholds in a group of adults with varying degrees of sensorineural hearing loss. The study also investigated whether multi-channel auditory steady-state response testing can be used to aid the assessment of hearing-impaired adults.
Patients and methods
Subjects
Subjects were chosen from adult patients visiting our ear, nose and throat department for hearing impairment issues, from January to June 2007.
Subjects requesting hearing handicap certification were excluded to avoid potential cases of pseudohypacusis. Conductive and mixed hearing loss subjects were also excluded.
A normal tympanometric result was a prerequisite for inclusion. Only subjects with sensorineural hearing loss were included in the study. Subjects were also selected on the basis of reliable pure tone thresholds and consent for further testing, with audiometric thresholds ranging from normal to profound.
There were 142 subjects (284 ears), 64 men and 78 women. Subjects' ages ranged from 20 to 84 years (mean, 44.6 years; median, 44.5 years).
All of the subjects underwent a battery of audiological tests, including otoscopy, tympanometry, pure tone audiometry and multi-channel auditory steady-state response measurement.
Procedures
Pure tone threshold measurement
Pure tone audiograms were obtained for each ear in all subjects, employing a standard threshold search procedure using a clinical audiometer (Unity PC Audiometer SD 100, Copenhagen, Denmark). Pure tone thresholds were typically obtained at 500, 1000, 2000 and 4000 Hz, via headphones. The maximum intensity for stimulation was 120 dBHL, using 5-dB intensity steps. Pure tone threshold levels were determined using a 10-dB down and 5-dB up search technique at each stimulation frequency. All pure tone threshold tests were conducted in a sound-proofed booth. The pure tone threshold for each individual ear was used as the control for the corresponding auditory steady-state response threshold.
Multi-channel auditory steady-state response threshold measurement
Auditory steady-state response measurements were performed within one week of pure tone threshold testing. All subjects were tested in a state of relaxation or natural sleep in a quiet, sound-proofed room. A binaural multi-channel auditory steady-state response audiometer (SmartEP auditory steady-state response system, Miami, Florida, USA) was used to estimate auditory steady-state response thresholds. Stimuli were presented to both ears via earphones with foam earplugs. The maximum stimulation level was 120 dBHL, approached in 10-dB intensity steps. Electroencephalogram (EEG) activity was recorded using silver–silver chloride disc electrode placed on the forehead (positive) and on both mastoid processes (negative). Intra-electrode impedance was less than 10 kΩ at 260 Hz. The three electrodes were all connected to the EEG amplifier and to the multi-channel auditory steady-state response frequency analyser.
Time-domain waveforms were converted to frequency domain using fast Fourier transform. In the frequency domain, the response to each carrier frequency could be assessed by the amplitude and phase of the fast Fourier transform component corresponding to the frequency of modulation of the carrier. When combining responses, we used vector averaging, which maintained phase as well as amplitude information.Reference Lins and Picton19 The amplitude and the phase of the response at each stimulation frequency were measured automatically by a computer; no subjective judgment by an interpreter was needed, since no peaks needed to be identified.
For non-interaction between each response, each multiple channel stimuli consisted of a combination of four carrier frequencies (500, 1000, 2000 and 4000 Hz) modulated in amplitude at the following respective rates: 77, 85, 93 and 101 for the left ear frequencies, and 79, 87, 95 and 103 for the right ear frequencies. Stimuli calibration was done separately for each frequency. Binaural multiple frequencies were evaluated in both ears simultaneously. The threshold was defined as the minimum level at which the response could be automatically detected by the SmartEP auditory steady-state response system. After the whole procedure had been completed, an auditory steady-state response audiogram for each ear of each subject was constructed. The pure tone thresholds and auditory steady-state response thresholds of the 284 tested ears were compared and analysed. The duration of the multi-channel auditory steady-state response assessment was also recorded.
Statistical evaluation of data was performed using the Statistical Package for the Social Sciences software (SPSS Inc, Chicago, Illinois, USA). A p value of 0.05 was considered to be the limit of significance.
Results
Each ear was tested over four frequencies. A total of 1136 (284 × 4 = 1136) comparisons between pure tone thresholds and auditory steady-state response thresholds was made. Of these audiometric thresholds, eight exceeded 120 dBHL for pure tone thresholds, 23 exceeded 120 dBHL for auditory steady-state response thresholds, and two exceeded 120 dBHL for both pure tone thresholds and auditory steady-state response thresholds. These results were not included in the correlation analyses.
There were 1103 valid groups for data analysis. Of these, 284 were at 500 Hz, 279 at 1000 Hz, 273 at 2000 Hz and 267 at 4000 Hz. Out of all the comparisons between multi-channel auditory steady-state response thresholds and pure tone thresholds, a difference of less than 15 dB was found in 71 per cent (782/1103) and a difference of less than 20 dB in 83 per cent (912/1103). Both ears were tested simultaneously at four frequencies and eight groups of data were obtained; even so, we found that the objective results for multi-channel auditory steady-state response thresholds were close to the subjective results for pure tone thresholds.
The relationship between pure tone thresholds and auditory steady-state response thresholds for each ear at each of the test frequencies is shown as x–y scatter plots in Figure 1. The solid lines in the distributions represent linear regression lines. The Pearson correlation coefficient (r) was 0.89, 0.95, 0.96 and 0.97 for correlation of the two testing methods at 500, 1000, 2000 and 4000 Hz, respectively (Table I). According to the p < 0.05 test, there was no significant difference between auditory steady-state response thresholds and pure tone thresholds at any test frequency. The correlation coefficient increased with increasing test frequency.
Fig. 1 Distribution of comparisons between auditory steady-state response thresholds and pure tone thresholds for (a) 500 Hz, (b) 1000 Hz, (c) 2000 Hz and (d) 4000 Hz. Solid lines represent linear regression. Multiple data points falling at a particular coordinate are represented by larger circles. Note that more data points fall on the regression line at 4000 Hz and at higher auditory steady-state response thresholds.
Table I Correlation Between Multi-Channel Auditory Steady-State Response Threshold and Pure Tone Threshold At Each Test Frequency: Pearson Product-Moment Coefficient Values
The regression equations are shown in Table II. The results show that the multi-channel auditory steady-state response thresholds were typically close to the pure tone thresholds. Differences values were established for each of the auditory steady-state response–pure tone threshold comparisons. These values were obtained by subtracting the pure tone thresholds from the auditory steady-state response values. The mean differences and standard deviations are summarised in Table III. These values revealed that the mean difference between the auditory steady-state response threshold and the pure tone threshold had a tendency to decrease with increasing frequency.
Table II Linear Regression Equations for Distribution of Comparisons Between Auditory Steady-State Response Thresholds and Pure Tone Thresholds, At Each Test Frequency
Table III Differences Between Auditory Steady-State Response Thresholds and Pure Tone Thresholds, At Each Test Frequency
SD = standard deviation
The data for each frequency were divided into five categories based on pure tone threshold levels. Five groups were defined by degree of hearing loss, as follows: normal (≤20 dB), mild (25–40 dB), moderate (45–70 dB), severe (75–90 dB) and profound (95–120 dB). Table IV shows the mean difference between auditory steady-state response thresholds and pure tone thresholds on the basis of varying degrees of hearing loss, at each frequency. It was observed that the mean difference between auditory steady-state response thresholds and pure tone thresholds decreased with increasing degree of hearing loss, at all frequencies.
Table IV Mean Differences Between Auditory Steady-State Response Thresholds and Pure Tone Thresholds, At Each Test Frequency, For Varying Degrees of Hearing Loss
For each subject, an estimated behavioural hearing threshold was calculated from the recorded auditory steady-state response values, using the regression equations shown in Table II. In all groups, comparisons were made between predicted behavioural hearing thresholds and pure tone thresholds. The mean difference between predicted and actual pure tone thresholds, based on the varying degree of hearing loss at each frequency, is shown in Table V. It was evident that, despite differing frequencies and varying degrees of hearing loss, the mean estimated pure tone threshold was within 10 dB of the corresponding behavioural pure tone threshold, in all groups. The results revealed that the predicted behavioural hearing threshold, calculated from the auditory steady-state response value, was very close to the actual recorded pure tone threshold.
Table V Mean Difference Between Predicted and Actual Pure Tone Thresholds, For Varying Degrees of Hearing Loss
Moreover, the time required for multi-channel auditory steady-state response testing was considerably reduced (average recording time, 42 minutes), compared with the time required for single-channel auditory steady-state response testing.Reference Wu, Hsu and Chu14
Discussion
We found a strong relationship between the auditory steady-state response threshold and the pure tone threshold at all frequencies tested. The Pearson correlation coefficient indicated a significant correlation between auditory steady-state response threshold and pure tone threshold at all frequencies. The smallest threshold differences were recorded in subjects with severe and profound hearing loss, and the best correlation was obtained at 4000 Hz. The strength of the relationship increased with increasing frequency and increasing degree of hearing loss. The difference between predicted and actual pure tone thresholds which corresponded to the particular auditory steady-state response threshold was reasonably small (within 10 dB in all groups). Thus, we assume that the predicted pure tone threshold, calculated from the auditory steady-state response threshold by using regression lines, will be close to the actual threshold at all frequencies.
From the scatter plots presented in Figure 1, data indicate that auditory steady-state response thresholds more closely matched pure tone thresholds as the degree of hearing loss increased. This may be partly explained by the possible presence of recruitment, resulting in a more pronounced transition from below-threshold non-response to above-threshold response in ears with sensorineural losses.Reference Rance, Rickards, Cohen, De Vidi and Clark15
Our study showed the largest mean difference between auditory steady-state response threshold and pure tone threshold at 500 Hz. According to Lins et al.,Reference Lins, Picton, Boucher, Durieux-Smith, Champagne and Moran17 the problems encountered when estimating 500 Hz auditory steady-state response thresholds could result from the low frequency evoked response, which has a greater intrinsic jitter due to neural asynchrony and which could make threshold detection relatively difficult at low test frequencies compared with higher frequencies. Such problems could also be partly due to the enhanced masking effect of ambient noise at lower frequencies. This phenomenon requires further investigation.
Using multiple simultaneous stimuli causes small changes in the responses, compared with responses evoked by a single stimulus. The clearest of these interactions is the attenuation of the responses to low-frequency stimuli in the presence of higher-frequency stimuli.Reference John, Purcell, Dimitrijevic and Picton20 However, at modulation rates between 75 and 110 Hz, there is little change in the amplitude of the responses when multiple stimuli are presented and the carrier frequencies differ by one octave.Reference Lins and Picton19
Few studies have investigated the multi-channel auditory steady-state response method's ability to estimate the hearing thresholds of subjects with hearing impairments. The reported detectability of such responses has varied across different studies. This variation may be due to such factors as the patient's age, the acoustic noise levels in the recording room and the duration of the recording.Reference Lins, Picton, Boucher, Durieux-Smith, Champagne and Moran17, Reference Luts and Wouters21 Regarding the effect of age, Lins et al. found that auditory steady-state response thresholds in the first few months of life were between one-third and one-half the size of adult thresholds.Reference Lins, Picton, Boucher, Durieux-Smith, Champagne and Moran17 Regarding the effect of recording duration, a longer recording will result in an increased signal to noise ratio, as the background electrical noise will decrease with averaging.Reference Luts and Wouters21
One of the advantages attributed to the binaural multi-channel technique is the possibility of minimising test time.Reference Lins, Picton, Boucher, Durieux-Smith, Champagne and Moran17, Reference Perez-Abalo, Savio and Torres18 Our study provides quantifiable evidence to support this claim. We found that an objective audiometric evaluation of both ears, using binaural multi-channel auditory steady-state responses elicited by simultaneous amplitude-modulated tones of 500, 1000, 2000 and 4000 Hz, could be completed in an average time of 42 minutes. This represents a considerable reduction in testing time, compared with single-channel auditory steady-state response testing (average testing time, 1.5–2 hours).Reference Wu, Hsu and Chu14
In our study, the multi-channel auditory steady-state response test had several distinct features which made it eminently suitable for objective evaluation of hearing thresholds.
First, the auditory steady-state response could be evoked by sinusoidal amplitude- and frequency-modulated tones, and thresholds at different frequencies could be assessed. Thus, we could evaluate precisely the subject's residual hearing.
Second, the continuously modulated tones used to elicit the auditory steady-state response could be presented at levels as high as 120 dBHL. Thus, auditory steady-state response measurement would be able to assess ears with only minimal amounts of residual hearing.Reference Rance, Dowell, Rickards, Beer and Clark16 This implies that auditory steady-state response measurement would be a reliable tool for assessment of profound or congenital hearing losses; frequency information is essential in such cases to enable proper treatment with hearing aids or cochlear implants.Reference John, Brown, Muir and Picton22
• Single-channel auditory steady-state response testing has recently become available as an objective hearing test option for both hearing-impaired adults and young children. However, it is time-consuming
• This study aimed to assess the usefulness of multi-channel auditory steady-state response testing in adults with sensorineural hearing loss
• The multi-channel auditory steady-state response testing procedure was more time-efficient than the corresponding single-channel procedure
• There appeared to be a very strong relationship between auditory steady-state response thresholds and pure tone thresholds. Regression lines calculated from auditory steady-state response thresholds could be used to predict pure tone thresholds
Third, the response was determined at the frequency of modulation by a computer using well established statistical procedures; no subjective judgment by an interpreter was necessary.Reference Lins, Picton and Picton13, Reference Rance, Dowell, Rickards, Beer and Clark16, Reference Perez-Abalo, Savio and Torres18
Fourth, although the amplitude of auditory steady-state responses may decrease during sedation or sleep,Reference Linden, Campbell, Hamel and Picton23 they can still be recorded at low sensation levels by using modulation rates in excess of 70 Hz.Reference Lins, Picton and Picton13, Reference Cohen, Rickards and Clark24 In other words, auditory steady-state response recording is not affected by sedation or sleep.Reference Rance, Rickards, Cohen, De Vidi and Clark15
Fifth, regression lines calculated from auditory steady-state response thresholds can be used to predict behavioural pure tone thresholds.
Sixth, the multi-channel auditory steady-state response procedure is more time-efficient than single-channel auditory steady-state response testing.
Conclusion
This study demonstrated that multi-channel auditory steady-state response threshold measurement is a reliable test enabling accurate prediction of auditory thresholds in adults with sensorineural hearing loss. This technology could represent a powerful, convenient and objective electro-physiological means of assessing pseudohypacusis.
