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Influence of spontaneous otoacoustic emissions on distortion product otoacoustic emission amplitudes
Hearing Research 127 (1999) 129^136
In£uence of spontaneous otoacoustic emissions on distortion product otoacoustic emission amplitudes Orhan Ozturan a; *, Cagatay Oysu a
b
Inonu University, Medical Faculty, Turgut Ozal Medical Center, Department of Otolaryngology, Malatya 44100, Turkey b Istanbul Medical Faculty, Department of Otolaryngology, Istanbul, Turkey Received 17 November 1997; received in revised form 19 September 1998; accepted 26 September 1998
Abstract Although the influence of the levels and ratios of the primary stimulus on the amplitude of distortion product otoacoustic emissions (DPOAEs) has been studied intensely, the influence of the presence of spontaneous otoacoustic emissions (SOAEs) has been investigated less thoroughly. The present investigation analysed whether the unilateral presence of 58 SOAEs in 43 normalhearing adults was related to larger DPOAEs in the ear with SOAEs compared to the contralateral ear having no SOAEs. The study was designed such that the only factor that could influence the amplitude of DPOAEs was the presence of SOAEs. Input/ output (I/O) functions were collected in response to primary tones that were presented in 5-dB steps from 70 to 40 dB SPL at the frequency of the unilaterally recorded SOAE of each subject. The primary outcome was the demonstration of statistically significant (P 6 0.05) larger DPOAEs in ears exhibiting SOAEs than in ears without measurable SOAEs, except at the highest stimulus level of 70 dB SPL. These results suggest that SOAEs play an additive role in the measurement of DPOAEs. The enhancing effect of the unilateral presence of SOAEs on DPOAEs was statistically significant for 65 dB SPL and lower levels of primary tones. The authors speculate that passive cochlear properties begin to participate in the generation of DPOAEs at primary-stimulus levels greater than 65 dB SPL. z 1999 Elsevier Science B.V. All rights reserved. Key words: Spontaneous otoacoustic emission; Distortion product otoacoustic emission; Normal-hearing human
1. Introduction Otoacoustic emissions (OAEs) are low-level sounds generated by the ear. Although their existence was predicted by Gold (1948), they were discovered 30 years later by Kemp (1978). He provided evidence that acoustic emissions can be detected in the external ear canal after stimulating the ear with clicks. These emissions are believed to originate from the active process of the cochlea (Pujol et al., 1991). Outer-hair cell motility, produced by electromotile-related proteins, generates mechanical energy within the cochlea that is propagated outward, by means of the middle ear system, to the ear canal. Vibration of the tympanic membrane then produces acoustic signals called OAEs that can be meas* Corresponding author. Tel.: +90 (422) 3410660; Fax: +90 (422) 3410728; E-mail: [email protected]
ured by a sensitive microphone inserted into the external ear canal (Martin et al., 1990). The accuracy and objectivity of OAEs in assessing cochlear function, combined with their non-invasive recording made emissions a good measure to use in clinical practice (Lonsbury-Martin et al., 1993 ; Norton, 1993). There are two general classes of OAE, spontaneous and evoked. Spontaneous otoacoustic emissions (SOAEs) are low-level signals measured in the external ear canal in the absence of any acoustic stimulation. They occur in 72% of healthy ears at frequencies that are individually ¢xed (Talmadge et al., 1993). In a recent study using more sophisticated recording and processing techniques the prevalence of SOAEs was reported as 83% for the females and 62% for the males (Penner and Zhang, 1997). The frequency £uctuations of SOAEs are small (1%) over long time periods, i.e., months or years (Strickland et al., 1984), but over short
0378-5955 / 99 / $ ^ see front matter ß 1999 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 8 - 5 9 5 5 ( 9 8 ) 0 0 1 8 4 - 1
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time periods their frequencies are extremely stable (Fritze and Koëhler, 1985). SOAEs are typically detected between 1000 and 5000 Hz (Bon¢ls, 1989). Right ears are 13% more likely to have SOAEs than are left ears, and the occurrence of multiple SOAEs is much more prevalent in females than males (Penner et al., 1993). The higher occurrence of SOAE peaks in females may be due to the smaller ear-canal volume, which enhances the amplitudes of low-level emissions, thus making them more easily detected. High-frequency SOAEs are generally of lower level than are low-frequency SOAEs (Penner et al., 1993). This may be attributed to the optimized transmission of sounds through the middle ear in the 1^3-kHz region (Kemp, 1980). The clinical utility of SOAEs is limited. While the absence of SOAEs is not clinically signi¢cant, their presence is a sign of normal cochlear processing, at least in the frequency regions surrounding the emission (Sininger, 1993). Evoked OAEs are obtained by acoustic stimulation in the external ear canal of all normal-hearing individuals. They are classi¢ed according to the characteristics of the stimulus used to elicit them or characteristics of the cochlear events that generate them. Distortion product otoacoustic emissions (DPOAEs) are produced when two pure-tone stimuli at f1 and f2 frequencies are presented to the ear simultaneously. The most robust DPOAE occurs at the frequency determined by the equation 2f1 3f2 (Norrix and Glattke, 1996). In general, human DPOAEs are optimally recorded when the ratio of the frequency of the primary tones (f2 /f1 ) is approximately 1.225, and the relative level of primary tones (L1 and L2 ) is between 0 and 15 dB (Gaskill and Brown, 1990). It has also been shown that the 2f1 3f2 DPOAE can be detected reliably in the frequency range of 500^8000 Hz (Lonsbury-Martin et al., 1993). There are two test methods for DPOAE measurement. The ¢rst is called the DPgram where the intensity levels of the primary tones are held constant and the DPOAE data are recorded for di¡erent frequency regions usually from lower to higher frequencies. The second method is referred to as the input/output (I/O) function whereby the frequencies of the primary stimuli are held constant and their intensity is varied systematically in an ascending or descending order in regular increments or decrements. DPOAE amplitudes can then be measured by means of a cursor function at each intensity level on the monitor screen as a function of primary-tone levels. DPOAEs are considered to be present when their amplitudes are 3 dB above the corresponding noise £oor (Lonsbury-Martin et al., 1993). Several authors reported that DPOAE amplitudes were higher when recorded at a frequency close to a SOAE frequency, i.e., within a 100-Hz span, but these studies had rather small sample sizes (Kemp, 1979; Burns et al., 1984; Furst et al., 1988; Wier et al.,
1988 ; Cianfrone et al., 1990). In the studies performed by Moulin et al. (1993) and Prieve et al. (1997), DPOAE levels from a group of ears with SOAEs were signi¢cantly higher than those from another group of ears without SOAEs in large populations of normally hearing individuals. In these large-scale studies, subjects were investigated by forming two groups, one group containing subjects who all had SOAEs clearly detectable above the noise £oor, the other group comprising subjects who did not show any SOAEs. Thereby many variables related to SOAE and DPOAE measurements could inevitably get involved in the results. The present study, however, was designed to examine DPOAE amplitudes in SOAE-positive and SOAE-negative ears within the same subject. This allowed a better control of the experiment and eliminated the in£uence of many variables on DPOAE amplitude. Despite the consistent results with the previous investigations, that is the major di¡erence of the present study. Hence, the purpose of the present investigation was to analyse whether the unilateral presence of SOAEs in a group of normalhearing adults was related to larger DPOAEs in that ear compared to the contralateral ear where SOAEs were not present. It should be emphasised that the results of the present investigation are in agreement with the previous experiments. Additionally, it corroborates the results of the prior studies by providing better design of within-subject measurements instead of betweengroup measurements. 2. Materials and methods Forty-three normal-hearing adults (10 males and 33 females) with unilateral SOAEs between the ages of 19 and 31 years (mean age 26 years) volunteered to participate in this study. Following an otoscopic examination, all subjects received a battery of tests, including the pure-tone threshold test, tympanometry, SOAE and DPOAE testing. All subjects had bilateral pure-tone thresholds of 15 dB or better in frequencies from 250 to 8000 Hz and had type A tympanograms. Volunteers with bilateral SOAEs, tinnitus, middle ear pathology or a history of noise exposure were not enrolled in the study. All subjects were seated in a double-walled quiet room and were instructed to remain silent during the testing period. The recording equipment used for the OAEs was the Madsen Celesta 503 Cochlear emission analyser that was operated by an IBM-compatible personal computer via the built-in RS232C connection. A calibration test was made once a week in the time period of the study to adjust the attenuators at the frequency-pair tested in order to obtain a speci¢ed value of sound pressure level in the sealed ear canal. The ¢t of the ear probe was always carefully checked before each test, which started automatically by pre-
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senting bursts of 10 clicks in the ear canal. The response was measured and then shown on-screen. Probe ¢tting allowed the position of the probe to be optimised in the subject's ear canal for accurate and replicable measuring. The system contains a built-in noise rejection mechanism. When starting a measurement the ¢rst two input recordings were compared and, if the rejection criteria were exceeded, the ¢rst input was rejected. The old input 2 was then moved to input 1, and a new input 2 was collected and compared. This was repeated until two records meet the rejection criteria. If the actual noise level was greater than þ 3 standard deviation ( þ 3 S.D.) rejection level for any sample that signal acquisition was rejected from the average for SOAE and DPOAE measurements. The stop criterion was a factor of þ 3 S.D. The measurements were automatically stopped when the ratio of the DPOAE to noise has reached the factor speci¢ed. All subjects were examined bilaterally to identify the presence of unilateral SOAEs by inserting the probe into the external ear canal. The output from the microphone was ampli¢ed, and the response was subjected to spectral analysis. This was transformed into the frequency domain by Fast Fourier Transform analysis. Amplitude spectra of the ear canal sound-pressure levels were based on averages of at least 100 accepted sweeps for the purpose of noise reduction. The average was calculated, and the results were displayed. SOAEs were identi¢ed visually as narrow peaks in the frequency spectrum and via a cursor function. They were also characterised in terms of amplitude (dB SPL) and frequency (Hz). They were only considered valid if the amplitudes exceeded the noise £oor by at least 3 dB (Penner et al., 1993). Due to the in£uence of respiration noise and other subject-related disturbances, SOAEs below 500 Hz were disregarded. Measurements were made over the 0.5^10-kHz frequency range with 12.7-Hz frequency resolution. The subjects were allowed to participate in the study, following a preliminary SOAE testing which was performed in each subject to document the presence of the SOAEs unilaterally. After all the above-mentioned testings to identify eligible subjects, the ear probe was inserted to the SOAE-positive ear of the subject for SOAE measurement. Then DPOAEs were collected as I/O functions from the same ear of the subject without displacing the ear probe at the relevant frequency of the unilaterally recorded SOAE. The ear probe was moved to the SOAE-negative ear which was tested ¢rst for SOAEs and secondly for DPOAEs without displacing the ear probe in the same manner. The SOAEs detected in the preliminary testing must have repeated at the same frequency and amplitude level in the second testing for the subject to have been accepted into the study. The I/O functions were measured in response to equi-level f1 and f2 primary tones (f2 /f1 = 1.22) that were presented
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in 5-dB steps, from 70 to 40 dB SPL. The I/O functions in response to seven separate primary-tone levels were measured at the frequency of the unilaterally recorded SOAE for each ear of the subject. Primary-tone frequencies were chosen such that 2f1 3f2 almost equaled the SOAE frequencies. The quantity of the accepted sweeps was 20^100 for each primary-tone level for I/O function for the purpose of noise reduction. DPOAE I/O functions were also measured for each SOAE in subjects with multiple SOAEs. DPOAEs were considered as present when their amplitude was more than 3 dB above the noise £oor (Lonsbury-Martin et al., 1993). 2.1. Statistical method The mean DPOAE amplitudes recorded in response to 40 dB SPL primary-tone level from SOAE-positive and negative ears were compared statistically. Identical comparisons were also performed between the mean DPOAE amplitudes in response to 45, 50, 55, 60, 65, and 70 dB SPL primary-tone levels in SOAE-positive and negative ears. The Student's t-test (independent samples, two-tailed, P 6 0.05) was used to investigate the in£uence of the SOAE presence on DPOAE amplitudes (Daniel, 1987; Ryan and Joiner, 1994). The di¡erences were tested statistically between the means of DPOAE amplitudes for each primary-tone level in SOAE-positive and SOAE-negative ears. All statistical analyses were performed using the Minitab statistical package program, release 10 (Ryan and Joiner, 1994). 3. Results Among the 43 subjects with unilateral SOAEs, 31 subjects (72%) had only one SOAE, nine subjects (21%) had two SOAEs, and three subjects (7%) had three SOAEs. In 29 (67%) subjects only the right ear was emitting SOAEs and in 14 (33%) subjects only the left ear was emitting SOAEs. A scatter plot displaying the frequencies and amplitude levels of the 58 SOAEs and the average level of noise-£oor is shown in Fig. 1. SOAE amplitudes ranged from 31 dB to 17 dB SPL with a mean of 6.1 dB SPL, a median frequency of 1953 Hz, and a mean frequency of 2351 Hz. SOAE amplitude exceeded the noise £oor by a mean of 8.2 dB. Although measurements were made over the 0.5^10-kHz frequency range, detected SOAE peaks ranged from 1030 Hz to 5531 Hz. The most likely frequency region for SOAEs ranged between 1.2 and 3.6 kHz, covering 88% of the SOAEs detected. Line plot of mean I/O functions for ears with (¢lled circles) and without SOAEs (¢lled diamonds), including two related mean noise £oor levels for ears with (open
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Fig. 1. Scatter plot displaying the frequencies and amplitude levels of 58 SOAEs. 88% of the SOAEs were measured in the 1200^3600Hz frequency band. The solid line and shaded area represent the average noise £oor of the SOAE recordings.
circles) and without SOAEs (open diamonds) are shown in Fig. 2. The amplitude levels of DPOAEs were signi¢cantly higher in SOAE-positive ears than in SOAE-negative ears. DPOAE detection threshold can be measured as the lowest primary-stimuli level at which the DPOAE amplitude is 3 dB higher than the noise £oor (Lonsbury-Martin et al., 1993). DPOAE thresholds were not de¢ned in the present study, since in most of the measurements DPOAE levels were high above the noise-£oor level even at the lowest level of primarytone level, i.e., at 40 dB SPL. Statistical testing for evaluating the in£uence of the SOAE presence on DPOAE amplitudes for ears with and without SOAEs was performed for each of seven di¡erent primary-tone levels (Ryan and Joiner, 1994). The mean DPOAE amplitudes as a function of primary-tone levels in ears with and without SOAEs, their standard deviations, and P values are listed in Table 1. DPOAE amplitudes elicited by primaries from 40 to 65 dB SPL were signi¢cantly greater in ears with SOAEs than in ears without SOAEs (P 6 0.05). The greater
Fig. 2. Line plot displaying the mean I/O function for ears with (¢lled circles) and without SOAEs (¢lled diamonds) including related mean noise £oor levels (open circles and open diamonds, respectively).
amplitude of DPOAEs in ears with SOAEs ranged from about 6 to 7 dB for the lower level primary tones, and around 2 to 3 dB for more intense primaries. Although the mean DPOAE amplitude level was greater in ears with SOAEs compared to ears without SOAEs at 70 dB SPL primary-tone level, the relationship was not statistically signi¢cant (P s 0.05). Since only 23% of the present subjects were male, a search for a gender e¡ect was not attempted because of the unequal female and male subject ratio. 4. Discussion In recent years, DPOAE testing has been used increasingly in otolaryngology clinics. Among other factors, DPOAE amplitude depends on the proper ¢tting of the ear probe, the condition of the middle ear, the noise-£oor level, the sensitivity of the measuring device and the ratio, frequencies and intensities of f1 and f2 primary tones (Harris et al., 1989 ; Kemp et al., 1990; Musiek et al., 1994; Plinkert et al., 1994). Variation between acoustic probes used in the instrumentation for recording OAEs may also lead to relatively large
Table 1 The mean DPOAE amplitudes as a function of primary stimuli levels in ears with and without SOAEs, standard deviations and P values Primary stimuli level (dB SPL)
Amplitude levels of DPOAEs in ears with SOAEs (dB SPL)
Amplitude levels of DPOAEs in ears without SOAEs (dB SPL)
P value (P 6 0.05)
40 45 50 55 60 65 70
39.41 35.93 31.72 1.31 5.21 8.52 11.9
316.56 312 3 7.9 3 2.24 1.59 5.97 9.55
0.0002 0.0009 0.0001 0.018 0.0065 0.047 0.055*
( þ 8.37) ( þ 8.69) ( þ 6.42) ( þ 7.39) ( þ 6.58) ( þ 6.82) ( þ 6.44)
*Non-signi¢cant.
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( þ 11.1) ( þ 10.31) ( þ 9.72) ( þ 8.54) ( þ 7.45) ( þ 6.84) ( þ 6.57)
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discrepancies in the amplitude and frequency spectra of the OAE responses (Lutman et al., 1994). Following the preliminary SOAE testing and documentation of unilateral presence of SOAEs, the ear probe was carefully inserted into the SOAE-positive ear canal. Initial measurement of the SOAEs con¢rmed the eligibility of the particular subject for this investigation. The second recording of the SOAEs allowed the repeatability and stability of the initial testing to be determined. Peaks which were not repeatedly apparent were thought to re£ect random variations in the noise £oor or body sounds (Penner et al., 1993). Moreover, it also allowed DPOAE measurements to proceed without disturbing the seal of the ear probe in the external canal (Kemp et al., 1990). SOAE and DPOAE I/O function tests were performed consecutively within the same test session without displacing the ear probe. In this way, it was possible to eliminate artifactual factors related to the ear probe and its ¢tting. The interpretation and level of OAE results are very sensitive to factors that also in£uence the acoustic transfer function of the middle ear due to the double-pass of the stimulus and the subsequently elicited emission from the cochlea (Osterhammel et al., 1993). Hence, tympanometry was performed to eliminate ears with middle-ear insult that may mar OAE testing. It has been shown, in addition, that DPOAE detection thresholds increase and amplitudes decrease with increasing age (Lonsbury-Martin et al., 1991). Therefore, in the present study OAEs were measured in subjects who were close in age to eliminate an aging e¡ect. The in£uence of the presence of SOAEs on transiently-evoked otoacoustic emissions (TEOAEs) has also been studied. Osterhammel et al. (1996) analysed whether the presence of SOAEs related to larger TEOAEs in 24 normal-hearing adults. Their subjects were selected to form two groups of 12, one containing only subjects with SOAEs, the other group without SOAEs. They demonstrated signi¢cantly greater TEOAEs in subjects exhibiting SOAEs than in subjects without measurable SOAEs. Kok et al. (1993) compared the amplitude levels of TEOAEs between ears with and without SOAEs in healthy newborns, and they found statistically signi¢cant higher evoked OAE levels in ears with SOAEs. This ¢nding supports the hypothesis that the higher-evoked OAE levels measured in healthy newborns are partly due to the higher prevalence (78%) of SOAEs at this age. Additionally, Kulawiec and Orlando (1995) reported on 18 subjects with SOAEs present in only one ear (11 right and 7 left ear). These authors used a within-subjects experimental design in their study that was similar to the present one. Ten of the 11 subjects with SOAEs only in the right ear had greater TEOAE response levels in their right ear. Four of the seven subjects with SOAEs only in the left ear had greater TEOAE response levels in their left ear.
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So, 14 of 18 subjects had greater TEOAE response levels in the ear with SOAEs. They only found four subjects who had greater TEOAE response levels in the SOAE-negative ear, and each of these had one low-level SOAE ranging from 316.8 to 324.8 dB SPL. Their ¢ndings suggest that the presence of SOAEs in one ear generally results in a greater TEOAE response level in that ear. Together, these studies showed that the presence of SOAEs has a potentiating in£uence on the TEOAEs. In the present study, all subjects had greater DPOAE levels in the SOAE-positive ears. In other words, none of the subjects had greater DPOAE amplitude levels in the SOAE-negative ears. The aim of the present study was to clarify whether DPOAEs in normal-hearing adults with unilateral SOAEs have larger amplitudes in the ear with SOAEs compared to the contralateral ear without SOAEs. Therefore, two groups were formed in subjects with unilaterally detectable SOAEs: one group having one ear with SOAEs, and the other group having the other ear without SOAEs. Although the contributions of SOAEs to TEOAEs have been investigated by intersubject or within-subject design, the in£uence of the presence of the SOAEs on DPOAEs has only been investigated by an intersubject design. Wier et al. (1988) and Cianfrone et al. (1990) reported that DPOAE amplitudes were higher when recorded at a frequency close to the SOAE frequency, i.e., within a 100-Hz span, but both studies had rather small sample sizes. Wier et al. (1988) measured DPOAEs at frequencies close to the SOAEs before and after aspirin consumption. Not only were SOAEs abolished with aspirin consumption, but a uniform decrease in DPOAE amplitudes was also observed. DPOAEs were not reduced as severely as SOAEs. Thus, DPOAEs could not have been similarly a¡ected by aspirin. This SOAE and DPOAE behavioural dissociation from the drug consumption suggests that aspirin can abolish the amplifying role of the SOAE on the DPOAE, and thereby decrease DPOAE amplitude. The authors evaluated an I/O function and the in£uence of the SOAEs in only one subject, and found that the I/O function was also a¡ected similarly by aspirin consumption. In a recent study, Prieve et al. (1997) measured SOAEs and DPOAE I/O functions in only one ear of 196 infants, children and young adults to investigate the in£uence of the SOAEs on DPOAEs. They found that the group of individuals having SOAEs had higher mean DPOAE levels than those not having SOAEs. In addition, Moulin et al. (1993) investigated the in£uence of the SOAEs on DPOAEs. SOAEs were recorded in 262 ears of 134 subjects (63 males and 72 females). Of these subjects, 41% had SOAEs, i.e., 83 (31.7%) of 262 ears had at least one SOAE peak. The authors reported that the DPOAE amplitudes were signi¢cantly greater in ears with SOAEs than those
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without measurable SOAEs by applying the Student's t-test for statistical assessment. Several investigators have reported higher DPOAE amplitude when DPOAEs were recorded in the vicinity of a SOAE (Kemp, 1979; Furst et al., 1988) with a decrease of the e¡ect when DPOAEs recorded at more than 50 Hz from the SOAE (Wier et al., 1988). It has also been shown that SOAEs can in£uence DPOAE I/O patterns when their frequency is close to the DPOAE frequency (Cianfrone et al., 1990; Lonsbury-Martin et al., 1990). Moreover, Moulin et al. (1993) showed signi¢cantly higher DPOAE amplitudes in SOAE-positive ears, even when ears showing SOAE frequencies less than 300 Hz around distortion frequencies were excluded. Even so, the authors thought that the amplitude level would be measured at maximum level if primary-tone frequencies were adjusted such that 2f1 3f2 DPOAE almost equaled the SOAE frequencies in the present investigation. In the previous studies, statistically signi¢cant di¡erences between groups were found in spite of the intersubject di¡erences and factors a¡ecting OAE measurements, even though, because of large intersubject di¡erences in amplitude levels, selecting two groups of subjects representing the presence and absence of SOAEs is not the most optimal experimental design. Only subjects with SOAEs in one ear were allowed to participate in the present investigation in order to eliminate the factors causing intersubject di¡erences that may contaminate the results. Hence, this study was designed so that the only factor in£uencing the amplitude of the DPOAEs would be the presence of SOAEs. Since it was reported that having an SOAE in either ear signi¢cantly increased the likelihood of having one in the other ear (Penner et al., 1993), the investigators had to examine more than 200 individuals to discover eligible subjects for the present study. Although a¤rmative results were obtained by Moulin et al. (1993), there are system- and subject-related factors that deserve to be discussed. The most e¡ective f2 /f1 ratio for eliciting DPOAEs from 1 to 4 kHz was reported as 1.22 (Harris et al., 1989). While the f2 /f1 ratio used in the present study (1.22) was identical to the optimal ratio, the ratio used by Moulin et al. (1993) was 1.17. The estimates of the prevalence of SOAEs depend on the criterion for identifying a spectral peak as an SOAE, the number of spectra in which an emission must appear in order to be identi¢ed as an SOAE, the sensitivity of the microphone and the level of the noise £oor (Penner et al., 1993). SOAEs were considered valid if the amplitudes exceeded the noise £oor by at least 3 dB. Increasing the number of spectra averaged may potentially decrease the variability of the noise, thereby improving the chances that a low-level SOAE will be su¤ciently above the noise to be judged a peak.
The major limitation in increasing the number of samples is that the subject may not be able to sit quietly during the extended sampling period. It is possible to decrease the variability in the noise £oor by increasing the number of Fast Fourier Transforms average. Increasing the number of spectra averaged decreases the standard deviation of lower-level SOAEs (Penner et al., 1993). Another di¡erence between the Moulin et al. (1993) study and the present one is that, in the former study, only 10 sweep spectra were averaged for the measurement of SOAEs, whereas in the present study at least 100 sweep spectra were averaged for the detection of SOAEs. It has been reported that the prevalence of the SOAEs is greater in females (83%) than in males (62%) and the occurrence of multiple SOAEs is much more prevalent in females than males (Penner et al., 1993 ; Penner and Zhang, 1997). Moulin et al. (1993) also showed a gender e¡ect on DPOAE amplitude in the 1^2-kHz frequency region. These frequencies correspond to the prominent frequency range of SOAEs that the females had a higher incidence of SOAEs compared to the males. This gender e¡ect was strongly reduced when only SOAE-negative subjects were evaluated. In the present study, the SOAE-positive ears group and the SOAE-negative ears group included an equal number of males and females. Consequently, the within-subjects design eliminated any type of gender e¡ect on the DPOAEs. On the other hand, gender e¡ect had an in£uence on DPOAEs inevitably because of betweengroup measurements in the study performed by Moulin et al. (1993). In this study, the mean DPOAE amplitude measured in response to each primary-tone level in SOAE-positive ears was compared to the corresponding mean DPOAE amplitude level in SOAE-negative ears. That is the mean DPOAE amplitude obtained in response to 40 dB SPL primary-stimulus level in SOAE-positive ears was compared to the mean DPOAE amplitude measured in response to 40 dB SPL primary-tone level in SOAE-negative ears, etc. Thus, two means were derived from the two independent samples for each primarytone level. Identical comparisons were also made for the mean DPOAE amplitudes recorded in response to the other primary-tone levels, respectively. For levels from 40 to 65 dB SPL, DPOAE amplitudes of the ears with SOAEs were greater than those ears without SOAEs, and these results were determined to be statistically signi¢cant (P 6 0.05). At 70 dB SPL, mean DPOAE amplitude was greater in the ears with SOAEs compared to the ears without SOAEs, but not statistically signi¢cant (P s 0.05). Brown (1987) has pointed out that there is a distinction to be made between distortion generated by lowlevel stimuli and by stimuli at levels higher than 65^70 dB SPL in rodents. A distortion response to high-level
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stimuli was even detected in a `dead' ear and, thus, the high-level DPOAE may have been related to passive cochlear mechanics and/or hydrodynamics and has doubtful use as a monitor for cochlear function. The distortion generated by lower level stimuli, however, is physiologically vulnerable and should be directly linked to the activity of outer-hair cells in the cochlea. Norton and Rubel (1990) reported that the responses to highlevel stimuli are susceptible to stimulus artifacts and/or may represent the responses of passive cochlear elements in gerbils. Mills and Rubel (1994) observed also in gerbils the elimination of DPOAEs evoked by lowand moderate-stimulus levels following furosemide intoxication. On the other hand, the passive source of DPOAEs evoked by high stimulus levels was essentially unchanged at all frequencies. Whitehead et al. (1992) studied the source of DPOAEs in rabbits. The DPOAEs evoked by low-level ( 6 60^70 dB SPL) stimuli were abolished within 3^4 min of induction of anoxia, whereas DPOAEs evoked by high-level stimuli were unchanged in this period. Similarly, DPOAEs elicited by low-level stimuli were temporarily abolished by an acute administration of ethacrynic acid that had little e¡ect on high-level DPOAEs. These studies present evidence regarding the involvement of the passive cochlear elements, at least in animal subjects. These ¢ndings strongly suggest that low- and high-level 2f1 3f2 DPOAEs arise from discrete sources. Norrix and Glattke (1996) suggested that the micromechanics of the cochlea behave di¡erently at high- and low-stimulus levels. Active and passive elements are believed to contribute to basilar-membrane motion patterns at low- and high-stimulus levels, respectively. All these investigators suggested that DPOAEs evoked by low-level stimuli are an active, micromechanical process and vulnerable physiologically. This would agree with the knowledge suggesting the use of low levels of stimulation in clinical practice. The ¢ndings of the present study infers that primary-tone level higher than 65 dB SPL may evoke passive cochlear properties, also in humans. Even at 65 dB SPL primary-stimuli level, passive cochlear activities are assumed to take part in the response, to some extent, and that this may be the reason why the DPOAE amplitude di¡erences between SOAEpositive and SOAE-negative ears were not statistically signi¢cant at the highest test level. The present ¢ndings suggest that SOAEs add to the overall DPOAEs response level, except at the high-stimuli level of 70 dB SPL. Their potentiating e¡ect likely occurs from the synchronous capturing of SOAEs during DPOAE data collection. The evidence related to active and passive properties of the cochlea was obtained in the present study, in contrast to the previous investigations, possibly, due to the within-subject design. It may be useful to assess the number and level of SOAEs when considering the range of normality in
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DPOAE response levels in normal-hearing subjects. In other words, the DPOAE response level that is judged to indicate normal outer-hair-cell function will vary with the number and level of the SOAEs. This study may also imply that normal-hearing individuals with no or few SOAEs may have low levels of DPOAEs. Therefore, SOAEs play an important role in the DPOAE measurements. 5. Conclusion This investigation demonstrated signi¢cantly higher DPOAEs in the ears exhibiting SOAEs than in the ears without measurable SOAEs. The detectability of SOAEs should be assessed before the evaluation of DPOAE amplitudes is made among ears. SOAE presence causes an enhancement of DPOAE amplitudes. According to the present results, this enhancement clearly occurs for primary stimuli of 40^65 dB SPL, while passive cochlear properties begin to contribute to the DPOAE at primary-stimuli levels greater than 65 dB SPL. DPOAE recordings at low primary levels seem to be more directly linked to active cochlear mechanisms. Within-subject design of the present investigation may have a signi¢cant role to obtain results regarding the active and passive cochlear properties. This would argue in favour of the use of low levels of stimulation in clinical practice. Acknowledgments The authors would like to thank to Prof. Dr. Nermin Baserer and Prof. Dr. Mehmet Tinaz for the permission to use the OAE Laboratory.
References Bon¢ls, P., 1989. Spontaneous otoacoustic emissions: clinical interest. Laryngoscope 99, 752^765. Brown, A.M., 1987. Acoustic distortion from rodent ears: a comparison of responses from rats, guinea pigs and gerbils. Hear. Res. 31, 25^38. Burns, E.M., Strickland, E.A., Tubis, A., Jones, K., 1984. Interactions among spontaneous emissions. I. Distortion products and linked emissions. Hear. Res. 16, 271^278. Cianfrone, M., Mattia, M., Altissimi, G., Turchetta, R., 1990. Distortion product otoacoustic emissions and spontaneous otoacoustic emission suppression in humans. In: Grandori, G.F., Cianfrone, G., Kemp, D.T. (Eds.), Cochlear Mechanisms and Otoacoustic Emissions. Adv. Audiol. Basel, Karger, 7, pp. 126^ 138. Daniel, W.W., 1987. Biostatistics: A Foundation for Analysis in the Health Sciences. John Wiley, New York, NY, pp. 230. Fritze, W., Koëhler, W., 1985. Frequency composition of spontaneous cochlear emissions. Arch. Oto-Rhino-Laryngol. 242, 43^48. Furst, M., Rabinowits, W.M., Zurek, P.M., 1988. Ear canal acoustic
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distortion at 2f1 -f2 from human ears: relation to other emissions and perceived combination tones. J. Acoust. Soc. Am. 84, 215^ 221. Gaskill, S.A., Brown, A.M., 1990. The behavior of the acoustic distortion product, 2f1 -f2 , from the human ear and its relation to auditory sensitivity. J. Acoust. Soc. Am. 88, 821^839. Gold, T., 1948. Hearing, II: The physical basis of the action of the cochlea. Proc. R. Soc. London Ser. B 135, 492^498. Harris, F.P., Lonsburry-Martin, B.L., Stagner, B.B., Coats, A.C., Martin, G.K., 1989. Acoustic distortion products in humans: Systematic changes in amplitude as a function of f2/f1 ratio. J. Acoust. Soc. Am. 85, 220^229. Kemp, D.T., 1978. Stimulated acoustic emissions from within the human auditory system. J. Acoust. Soc. Am. 64, 1386^1391. Kemp, D.T., 1979. Evidence of mechanical nonlinearity and frequency selective wave ampli¢cation in the cochlea. Arch. Otorhinolaryngol. 224, 37^45. Kemp, D.T., 1980. Towards a model for the origin of cochlear echoes. Hear. Res. 2, 533^548. Kemp, D.T., Ryan, S., Bray, P., 1990. A guide to the e¡ective use of otoacoustic emissions. Ear Hear. 11, 93^105. Kok, M.R., van Zanten, G.A., Brocaar, M.P., 1993. Aspects of spontaneous otoacoustic emissions in healthy newborns. Hear. Res. 69, 115^123. Kulawiec, J.T., Orlando, M.S., 1995. The contribution of spontaneous otoacoustic emissions to the click evoked otoacoustic emissions. Ear Hear. 16, 515^520. Lonsbury-Martin, B.L., Harris, F.P., Stagner, B., Hawkins, M.D., Martin, G.K., 1990. Distortion product emissions in humans: II. Relations to acoustic immittance and stimulus frequency emissions in normally hearing subjects. Ann. Otol. Rhinol. Laryngol. 99 (Suppl. 147), 15^29. Lonsbury-Martin, B.L., Cutler, W.M., Martin, G.K., 1991. Evidence for the in£uence of aging on distortion-product otoacoustic emissions in humans. J. Acoust. Soc. Am. 89, 1749^1759. Lonsbury-Martin, B.L., McCoy, M.J., Whitehead, M.L., Martin, G.K., 1993. Clinical testing of distortion-product otoacoustic emissions. Ear Hear. 1, 11^22. Lutman, M.E., Jennings, K., Davis, A.C., Houston, H.G., Meredith, R., 1994. Coloration of click-evoked otoacoustic emissions by characteristics of the recording apparatus. In: Grandori, F. (Ed.), Advances in Otoacoustic Emissions. Fundamentals and Clinical Applications, Vol. 1, Stefanoni, Lecco, pp. 36^47. Martin, G.K., Probst, R., Lonsbury-Martin, B.L., 1990. Otoacoustic emissions in human ears: normative ¢ndings. Ear Hear. 11, 106^ 120. Mills, D.M., Rubel, E.W., 1994. Variation of distortion product otoacoustic emissions with furosemide injection. Hear. Res. 77, 183^ 199. Moulin, A., Collet, L., Veuillet, E., Morgon, A., 1993. Interrelations between transiently evoked otoacoustic emissions, spontaneous otoacoustic emissions and acoustic distortion products in normally hearing subjects. Hear. Res. 65, 216^233.
Musiek, F.E., Smurzynski, J., Bornstein, S.P., 1994. Otoacoustic emissions testing in adults: An overview. Am. J. Otol. 15 (Suppl. 1), 21^28. Norrix, L.W., Glattke, T.J., 1996. Distortion product otoacoustic emissions created through the interaction of spontaneous otoacoustic emissions and externally generated tones. J. Acoust. Soc. Am. 100, 945^955. Norton, S.J., Rubel, E.W., 1990. Active and passive ADP components in mammalian and avian ears. In: Dallos, P., Geisler, C.D., Matthews, J.W., Ruggero, M.A., Steele, C.R. (Eds.), The Mechanics and Biophysics of Hearing. Springer-Verlag, New York, NY, pp. 217^227. Norton, S.J., 1993. Application of transient evoked otoacoustic emissions to pediatric populations. Ear Hear. 14, 64^73. Osterhammel, P.A., Nielsen, L.H., Rasmussen, A.N., 1993. Distortion product otoacoustic emissions. The in£uence of the middle ear transmission. Scand. Audiol. 22, 111^116. Osterhammel, P.A., Rasmussen, A.N., Olsen, S.Q., Nielsen, H.L., 1996. The in£uence of spontaneous otoacoustic emissions on the amplitude of transient-evoked emissions. Scand. Audiol. 25, 187^ 192. Penner, M.J., Glotzbach, L., Huang, T., 1993. Spontaneous otoacoustic emissions: Measurement and data. Hear. Res. 68, 229^237. Penner, M.J., Zhang, T., 1997. Prevalence of spontaneous otoacoustic emissions in adults revisited. Hear. Res. 103, 28^34. Plinkert, P.K., Bootz, F., Vobieck, T., 1994. In£uence of static middle ear pressure on transiently evoked otoacoustic emissions and distortion products. Eur. Arch. Otorhinolaryngol. 251, 95^99. Prieve, B.A., Kemp, D.T., Schulte, L.E., Fitzgerald, T.S., 1997. Basic characteristics of distortion product otoacoustic emissions in infants and children. J. Acoust. Soc. Am. 102, 2871^2879. Pujol, R., Zajic, G., Dulon, D., Raphael, Y., Altschuler, A.A., Schacht, J., 1991. First appearance and development of motile properties in outer hair cells isolated from guinea-pig cochlea. Hear. Res. 57, 129^141. Ryan, B.F., Joiner, B.L., 1994. Minitab Handbook, Wadsworth, Belmont, CA, pp. 227^253. Sininger, Y.S., 1993. Clinical application of otoacoustic emissions. Adv. Otolaryngol. Head Neck Surg. 7, 247^269. Strickland, A.E., Burns, E.M., Tubis, A., Jones, K., 1984. Long-term stability and familial aspects of spontaneous otoacoustic emissions. J. Acoust. Soc. Am. 75 (Suppl. 1), 82. Talmadge, C.L., Long, G.R., Murphy, W.J., Tubis, A., 1993. New o¡-line method for detecting spontaneous otoacoustic emissions in human subjects. Hear. Res. 71, 170^182. Whitehead, M.L., Lonsbury-Martin, B.L., Martin, G.K., 1992. Evidence for two discrete sources of 2f1-f2 distortion-product otoacoustic emission in rabbit. II: Di¡erential physiological vulnerability. J. Acoust. Soc. Am. 92, 2662^2682. Wier, C.C., Pasanen, E.G., McFadden, D., 1988. Partial dissociation of spontaneous otoacoustic emissions and distortion products during aspirin use in humans. J. Acoust. Soc. Am. 84, 230^237.
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In£uence of spontaneous otoacoustic emissions on distortion product otoacoustic emission amplitudes Orhan Ozturan a; *, Cagatay Oysu a
b
Inonu University, Medical Faculty, Turgut Ozal Medical Center, Department of Otolaryngology, Malatya 44100, Turkey b Istanbul Medical Faculty, Department of Otolaryngology, Istanbul, Turkey Received 17 November 1997; received in revised form 19 September 1998; accepted 26 September 1998
Abstract Although the influence of the levels and ratios of the primary stimulus on the amplitude of distortion product otoacoustic emissions (DPOAEs) has been studied intensely, the influence of the presence of spontaneous otoacoustic emissions (SOAEs) has been investigated less thoroughly. The present investigation analysed whether the unilateral presence of 58 SOAEs in 43 normalhearing adults was related to larger DPOAEs in the ear with SOAEs compared to the contralateral ear having no SOAEs. The study was designed such that the only factor that could influence the amplitude of DPOAEs was the presence of SOAEs. Input/ output (I/O) functions were collected in response to primary tones that were presented in 5-dB steps from 70 to 40 dB SPL at the frequency of the unilaterally recorded SOAE of each subject. The primary outcome was the demonstration of statistically significant (P 6 0.05) larger DPOAEs in ears exhibiting SOAEs than in ears without measurable SOAEs, except at the highest stimulus level of 70 dB SPL. These results suggest that SOAEs play an additive role in the measurement of DPOAEs. The enhancing effect of the unilateral presence of SOAEs on DPOAEs was statistically significant for 65 dB SPL and lower levels of primary tones. The authors speculate that passive cochlear properties begin to participate in the generation of DPOAEs at primary-stimulus levels greater than 65 dB SPL. z 1999 Elsevier Science B.V. All rights reserved. Key words: Spontaneous otoacoustic emission; Distortion product otoacoustic emission; Normal-hearing human
1. Introduction Otoacoustic emissions (OAEs) are low-level sounds generated by the ear. Although their existence was predicted by Gold (1948), they were discovered 30 years later by Kemp (1978). He provided evidence that acoustic emissions can be detected in the external ear canal after stimulating the ear with clicks. These emissions are believed to originate from the active process of the cochlea (Pujol et al., 1991). Outer-hair cell motility, produced by electromotile-related proteins, generates mechanical energy within the cochlea that is propagated outward, by means of the middle ear system, to the ear canal. Vibration of the tympanic membrane then produces acoustic signals called OAEs that can be meas* Corresponding author. Tel.: +90 (422) 3410660; Fax: +90 (422) 3410728; E-mail: [email protected]
ured by a sensitive microphone inserted into the external ear canal (Martin et al., 1990). The accuracy and objectivity of OAEs in assessing cochlear function, combined with their non-invasive recording made emissions a good measure to use in clinical practice (Lonsbury-Martin et al., 1993 ; Norton, 1993). There are two general classes of OAE, spontaneous and evoked. Spontaneous otoacoustic emissions (SOAEs) are low-level signals measured in the external ear canal in the absence of any acoustic stimulation. They occur in 72% of healthy ears at frequencies that are individually ¢xed (Talmadge et al., 1993). In a recent study using more sophisticated recording and processing techniques the prevalence of SOAEs was reported as 83% for the females and 62% for the males (Penner and Zhang, 1997). The frequency £uctuations of SOAEs are small (1%) over long time periods, i.e., months or years (Strickland et al., 1984), but over short
0378-5955 / 99 / $ ^ see front matter ß 1999 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 8 - 5 9 5 5 ( 9 8 ) 0 0 1 8 4 - 1
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time periods their frequencies are extremely stable (Fritze and Koëhler, 1985). SOAEs are typically detected between 1000 and 5000 Hz (Bon¢ls, 1989). Right ears are 13% more likely to have SOAEs than are left ears, and the occurrence of multiple SOAEs is much more prevalent in females than males (Penner et al., 1993). The higher occurrence of SOAE peaks in females may be due to the smaller ear-canal volume, which enhances the amplitudes of low-level emissions, thus making them more easily detected. High-frequency SOAEs are generally of lower level than are low-frequency SOAEs (Penner et al., 1993). This may be attributed to the optimized transmission of sounds through the middle ear in the 1^3-kHz region (Kemp, 1980). The clinical utility of SOAEs is limited. While the absence of SOAEs is not clinically signi¢cant, their presence is a sign of normal cochlear processing, at least in the frequency regions surrounding the emission (Sininger, 1993). Evoked OAEs are obtained by acoustic stimulation in the external ear canal of all normal-hearing individuals. They are classi¢ed according to the characteristics of the stimulus used to elicit them or characteristics of the cochlear events that generate them. Distortion product otoacoustic emissions (DPOAEs) are produced when two pure-tone stimuli at f1 and f2 frequencies are presented to the ear simultaneously. The most robust DPOAE occurs at the frequency determined by the equation 2f1 3f2 (Norrix and Glattke, 1996). In general, human DPOAEs are optimally recorded when the ratio of the frequency of the primary tones (f2 /f1 ) is approximately 1.225, and the relative level of primary tones (L1 and L2 ) is between 0 and 15 dB (Gaskill and Brown, 1990). It has also been shown that the 2f1 3f2 DPOAE can be detected reliably in the frequency range of 500^8000 Hz (Lonsbury-Martin et al., 1993). There are two test methods for DPOAE measurement. The ¢rst is called the DPgram where the intensity levels of the primary tones are held constant and the DPOAE data are recorded for di¡erent frequency regions usually from lower to higher frequencies. The second method is referred to as the input/output (I/O) function whereby the frequencies of the primary stimuli are held constant and their intensity is varied systematically in an ascending or descending order in regular increments or decrements. DPOAE amplitudes can then be measured by means of a cursor function at each intensity level on the monitor screen as a function of primary-tone levels. DPOAEs are considered to be present when their amplitudes are 3 dB above the corresponding noise £oor (Lonsbury-Martin et al., 1993). Several authors reported that DPOAE amplitudes were higher when recorded at a frequency close to a SOAE frequency, i.e., within a 100-Hz span, but these studies had rather small sample sizes (Kemp, 1979; Burns et al., 1984; Furst et al., 1988; Wier et al.,
1988 ; Cianfrone et al., 1990). In the studies performed by Moulin et al. (1993) and Prieve et al. (1997), DPOAE levels from a group of ears with SOAEs were signi¢cantly higher than those from another group of ears without SOAEs in large populations of normally hearing individuals. In these large-scale studies, subjects were investigated by forming two groups, one group containing subjects who all had SOAEs clearly detectable above the noise £oor, the other group comprising subjects who did not show any SOAEs. Thereby many variables related to SOAE and DPOAE measurements could inevitably get involved in the results. The present study, however, was designed to examine DPOAE amplitudes in SOAE-positive and SOAE-negative ears within the same subject. This allowed a better control of the experiment and eliminated the in£uence of many variables on DPOAE amplitude. Despite the consistent results with the previous investigations, that is the major di¡erence of the present study. Hence, the purpose of the present investigation was to analyse whether the unilateral presence of SOAEs in a group of normalhearing adults was related to larger DPOAEs in that ear compared to the contralateral ear where SOAEs were not present. It should be emphasised that the results of the present investigation are in agreement with the previous experiments. Additionally, it corroborates the results of the prior studies by providing better design of within-subject measurements instead of betweengroup measurements. 2. Materials and methods Forty-three normal-hearing adults (10 males and 33 females) with unilateral SOAEs between the ages of 19 and 31 years (mean age 26 years) volunteered to participate in this study. Following an otoscopic examination, all subjects received a battery of tests, including the pure-tone threshold test, tympanometry, SOAE and DPOAE testing. All subjects had bilateral pure-tone thresholds of 15 dB or better in frequencies from 250 to 8000 Hz and had type A tympanograms. Volunteers with bilateral SOAEs, tinnitus, middle ear pathology or a history of noise exposure were not enrolled in the study. All subjects were seated in a double-walled quiet room and were instructed to remain silent during the testing period. The recording equipment used for the OAEs was the Madsen Celesta 503 Cochlear emission analyser that was operated by an IBM-compatible personal computer via the built-in RS232C connection. A calibration test was made once a week in the time period of the study to adjust the attenuators at the frequency-pair tested in order to obtain a speci¢ed value of sound pressure level in the sealed ear canal. The ¢t of the ear probe was always carefully checked before each test, which started automatically by pre-
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senting bursts of 10 clicks in the ear canal. The response was measured and then shown on-screen. Probe ¢tting allowed the position of the probe to be optimised in the subject's ear canal for accurate and replicable measuring. The system contains a built-in noise rejection mechanism. When starting a measurement the ¢rst two input recordings were compared and, if the rejection criteria were exceeded, the ¢rst input was rejected. The old input 2 was then moved to input 1, and a new input 2 was collected and compared. This was repeated until two records meet the rejection criteria. If the actual noise level was greater than þ 3 standard deviation ( þ 3 S.D.) rejection level for any sample that signal acquisition was rejected from the average for SOAE and DPOAE measurements. The stop criterion was a factor of þ 3 S.D. The measurements were automatically stopped when the ratio of the DPOAE to noise has reached the factor speci¢ed. All subjects were examined bilaterally to identify the presence of unilateral SOAEs by inserting the probe into the external ear canal. The output from the microphone was ampli¢ed, and the response was subjected to spectral analysis. This was transformed into the frequency domain by Fast Fourier Transform analysis. Amplitude spectra of the ear canal sound-pressure levels were based on averages of at least 100 accepted sweeps for the purpose of noise reduction. The average was calculated, and the results were displayed. SOAEs were identi¢ed visually as narrow peaks in the frequency spectrum and via a cursor function. They were also characterised in terms of amplitude (dB SPL) and frequency (Hz). They were only considered valid if the amplitudes exceeded the noise £oor by at least 3 dB (Penner et al., 1993). Due to the in£uence of respiration noise and other subject-related disturbances, SOAEs below 500 Hz were disregarded. Measurements were made over the 0.5^10-kHz frequency range with 12.7-Hz frequency resolution. The subjects were allowed to participate in the study, following a preliminary SOAE testing which was performed in each subject to document the presence of the SOAEs unilaterally. After all the above-mentioned testings to identify eligible subjects, the ear probe was inserted to the SOAE-positive ear of the subject for SOAE measurement. Then DPOAEs were collected as I/O functions from the same ear of the subject without displacing the ear probe at the relevant frequency of the unilaterally recorded SOAE. The ear probe was moved to the SOAE-negative ear which was tested ¢rst for SOAEs and secondly for DPOAEs without displacing the ear probe in the same manner. The SOAEs detected in the preliminary testing must have repeated at the same frequency and amplitude level in the second testing for the subject to have been accepted into the study. The I/O functions were measured in response to equi-level f1 and f2 primary tones (f2 /f1 = 1.22) that were presented
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in 5-dB steps, from 70 to 40 dB SPL. The I/O functions in response to seven separate primary-tone levels were measured at the frequency of the unilaterally recorded SOAE for each ear of the subject. Primary-tone frequencies were chosen such that 2f1 3f2 almost equaled the SOAE frequencies. The quantity of the accepted sweeps was 20^100 for each primary-tone level for I/O function for the purpose of noise reduction. DPOAE I/O functions were also measured for each SOAE in subjects with multiple SOAEs. DPOAEs were considered as present when their amplitude was more than 3 dB above the noise £oor (Lonsbury-Martin et al., 1993). 2.1. Statistical method The mean DPOAE amplitudes recorded in response to 40 dB SPL primary-tone level from SOAE-positive and negative ears were compared statistically. Identical comparisons were also performed between the mean DPOAE amplitudes in response to 45, 50, 55, 60, 65, and 70 dB SPL primary-tone levels in SOAE-positive and negative ears. The Student's t-test (independent samples, two-tailed, P 6 0.05) was used to investigate the in£uence of the SOAE presence on DPOAE amplitudes (Daniel, 1987; Ryan and Joiner, 1994). The di¡erences were tested statistically between the means of DPOAE amplitudes for each primary-tone level in SOAE-positive and SOAE-negative ears. All statistical analyses were performed using the Minitab statistical package program, release 10 (Ryan and Joiner, 1994). 3. Results Among the 43 subjects with unilateral SOAEs, 31 subjects (72%) had only one SOAE, nine subjects (21%) had two SOAEs, and three subjects (7%) had three SOAEs. In 29 (67%) subjects only the right ear was emitting SOAEs and in 14 (33%) subjects only the left ear was emitting SOAEs. A scatter plot displaying the frequencies and amplitude levels of the 58 SOAEs and the average level of noise-£oor is shown in Fig. 1. SOAE amplitudes ranged from 31 dB to 17 dB SPL with a mean of 6.1 dB SPL, a median frequency of 1953 Hz, and a mean frequency of 2351 Hz. SOAE amplitude exceeded the noise £oor by a mean of 8.2 dB. Although measurements were made over the 0.5^10-kHz frequency range, detected SOAE peaks ranged from 1030 Hz to 5531 Hz. The most likely frequency region for SOAEs ranged between 1.2 and 3.6 kHz, covering 88% of the SOAEs detected. Line plot of mean I/O functions for ears with (¢lled circles) and without SOAEs (¢lled diamonds), including two related mean noise £oor levels for ears with (open
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Fig. 1. Scatter plot displaying the frequencies and amplitude levels of 58 SOAEs. 88% of the SOAEs were measured in the 1200^3600Hz frequency band. The solid line and shaded area represent the average noise £oor of the SOAE recordings.
circles) and without SOAEs (open diamonds) are shown in Fig. 2. The amplitude levels of DPOAEs were signi¢cantly higher in SOAE-positive ears than in SOAE-negative ears. DPOAE detection threshold can be measured as the lowest primary-stimuli level at which the DPOAE amplitude is 3 dB higher than the noise £oor (Lonsbury-Martin et al., 1993). DPOAE thresholds were not de¢ned in the present study, since in most of the measurements DPOAE levels were high above the noise-£oor level even at the lowest level of primarytone level, i.e., at 40 dB SPL. Statistical testing for evaluating the in£uence of the SOAE presence on DPOAE amplitudes for ears with and without SOAEs was performed for each of seven di¡erent primary-tone levels (Ryan and Joiner, 1994). The mean DPOAE amplitudes as a function of primary-tone levels in ears with and without SOAEs, their standard deviations, and P values are listed in Table 1. DPOAE amplitudes elicited by primaries from 40 to 65 dB SPL were signi¢cantly greater in ears with SOAEs than in ears without SOAEs (P 6 0.05). The greater
Fig. 2. Line plot displaying the mean I/O function for ears with (¢lled circles) and without SOAEs (¢lled diamonds) including related mean noise £oor levels (open circles and open diamonds, respectively).
amplitude of DPOAEs in ears with SOAEs ranged from about 6 to 7 dB for the lower level primary tones, and around 2 to 3 dB for more intense primaries. Although the mean DPOAE amplitude level was greater in ears with SOAEs compared to ears without SOAEs at 70 dB SPL primary-tone level, the relationship was not statistically signi¢cant (P s 0.05). Since only 23% of the present subjects were male, a search for a gender e¡ect was not attempted because of the unequal female and male subject ratio. 4. Discussion In recent years, DPOAE testing has been used increasingly in otolaryngology clinics. Among other factors, DPOAE amplitude depends on the proper ¢tting of the ear probe, the condition of the middle ear, the noise-£oor level, the sensitivity of the measuring device and the ratio, frequencies and intensities of f1 and f2 primary tones (Harris et al., 1989 ; Kemp et al., 1990; Musiek et al., 1994; Plinkert et al., 1994). Variation between acoustic probes used in the instrumentation for recording OAEs may also lead to relatively large
Table 1 The mean DPOAE amplitudes as a function of primary stimuli levels in ears with and without SOAEs, standard deviations and P values Primary stimuli level (dB SPL)
Amplitude levels of DPOAEs in ears with SOAEs (dB SPL)
Amplitude levels of DPOAEs in ears without SOAEs (dB SPL)
P value (P 6 0.05)
40 45 50 55 60 65 70
39.41 35.93 31.72 1.31 5.21 8.52 11.9
316.56 312 3 7.9 3 2.24 1.59 5.97 9.55
0.0002 0.0009 0.0001 0.018 0.0065 0.047 0.055*
( þ 8.37) ( þ 8.69) ( þ 6.42) ( þ 7.39) ( þ 6.58) ( þ 6.82) ( þ 6.44)
*Non-signi¢cant.
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( þ 11.1) ( þ 10.31) ( þ 9.72) ( þ 8.54) ( þ 7.45) ( þ 6.84) ( þ 6.57)
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discrepancies in the amplitude and frequency spectra of the OAE responses (Lutman et al., 1994). Following the preliminary SOAE testing and documentation of unilateral presence of SOAEs, the ear probe was carefully inserted into the SOAE-positive ear canal. Initial measurement of the SOAEs con¢rmed the eligibility of the particular subject for this investigation. The second recording of the SOAEs allowed the repeatability and stability of the initial testing to be determined. Peaks which were not repeatedly apparent were thought to re£ect random variations in the noise £oor or body sounds (Penner et al., 1993). Moreover, it also allowed DPOAE measurements to proceed without disturbing the seal of the ear probe in the external canal (Kemp et al., 1990). SOAE and DPOAE I/O function tests were performed consecutively within the same test session without displacing the ear probe. In this way, it was possible to eliminate artifactual factors related to the ear probe and its ¢tting. The interpretation and level of OAE results are very sensitive to factors that also in£uence the acoustic transfer function of the middle ear due to the double-pass of the stimulus and the subsequently elicited emission from the cochlea (Osterhammel et al., 1993). Hence, tympanometry was performed to eliminate ears with middle-ear insult that may mar OAE testing. It has been shown, in addition, that DPOAE detection thresholds increase and amplitudes decrease with increasing age (Lonsbury-Martin et al., 1991). Therefore, in the present study OAEs were measured in subjects who were close in age to eliminate an aging e¡ect. The in£uence of the presence of SOAEs on transiently-evoked otoacoustic emissions (TEOAEs) has also been studied. Osterhammel et al. (1996) analysed whether the presence of SOAEs related to larger TEOAEs in 24 normal-hearing adults. Their subjects were selected to form two groups of 12, one containing only subjects with SOAEs, the other group without SOAEs. They demonstrated signi¢cantly greater TEOAEs in subjects exhibiting SOAEs than in subjects without measurable SOAEs. Kok et al. (1993) compared the amplitude levels of TEOAEs between ears with and without SOAEs in healthy newborns, and they found statistically signi¢cant higher evoked OAE levels in ears with SOAEs. This ¢nding supports the hypothesis that the higher-evoked OAE levels measured in healthy newborns are partly due to the higher prevalence (78%) of SOAEs at this age. Additionally, Kulawiec and Orlando (1995) reported on 18 subjects with SOAEs present in only one ear (11 right and 7 left ear). These authors used a within-subjects experimental design in their study that was similar to the present one. Ten of the 11 subjects with SOAEs only in the right ear had greater TEOAE response levels in their right ear. Four of the seven subjects with SOAEs only in the left ear had greater TEOAE response levels in their left ear.
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So, 14 of 18 subjects had greater TEOAE response levels in the ear with SOAEs. They only found four subjects who had greater TEOAE response levels in the SOAE-negative ear, and each of these had one low-level SOAE ranging from 316.8 to 324.8 dB SPL. Their ¢ndings suggest that the presence of SOAEs in one ear generally results in a greater TEOAE response level in that ear. Together, these studies showed that the presence of SOAEs has a potentiating in£uence on the TEOAEs. In the present study, all subjects had greater DPOAE levels in the SOAE-positive ears. In other words, none of the subjects had greater DPOAE amplitude levels in the SOAE-negative ears. The aim of the present study was to clarify whether DPOAEs in normal-hearing adults with unilateral SOAEs have larger amplitudes in the ear with SOAEs compared to the contralateral ear without SOAEs. Therefore, two groups were formed in subjects with unilaterally detectable SOAEs: one group having one ear with SOAEs, and the other group having the other ear without SOAEs. Although the contributions of SOAEs to TEOAEs have been investigated by intersubject or within-subject design, the in£uence of the presence of the SOAEs on DPOAEs has only been investigated by an intersubject design. Wier et al. (1988) and Cianfrone et al. (1990) reported that DPOAE amplitudes were higher when recorded at a frequency close to the SOAE frequency, i.e., within a 100-Hz span, but both studies had rather small sample sizes. Wier et al. (1988) measured DPOAEs at frequencies close to the SOAEs before and after aspirin consumption. Not only were SOAEs abolished with aspirin consumption, but a uniform decrease in DPOAE amplitudes was also observed. DPOAEs were not reduced as severely as SOAEs. Thus, DPOAEs could not have been similarly a¡ected by aspirin. This SOAE and DPOAE behavioural dissociation from the drug consumption suggests that aspirin can abolish the amplifying role of the SOAE on the DPOAE, and thereby decrease DPOAE amplitude. The authors evaluated an I/O function and the in£uence of the SOAEs in only one subject, and found that the I/O function was also a¡ected similarly by aspirin consumption. In a recent study, Prieve et al. (1997) measured SOAEs and DPOAE I/O functions in only one ear of 196 infants, children and young adults to investigate the in£uence of the SOAEs on DPOAEs. They found that the group of individuals having SOAEs had higher mean DPOAE levels than those not having SOAEs. In addition, Moulin et al. (1993) investigated the in£uence of the SOAEs on DPOAEs. SOAEs were recorded in 262 ears of 134 subjects (63 males and 72 females). Of these subjects, 41% had SOAEs, i.e., 83 (31.7%) of 262 ears had at least one SOAE peak. The authors reported that the DPOAE amplitudes were signi¢cantly greater in ears with SOAEs than those
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without measurable SOAEs by applying the Student's t-test for statistical assessment. Several investigators have reported higher DPOAE amplitude when DPOAEs were recorded in the vicinity of a SOAE (Kemp, 1979; Furst et al., 1988) with a decrease of the e¡ect when DPOAEs recorded at more than 50 Hz from the SOAE (Wier et al., 1988). It has also been shown that SOAEs can in£uence DPOAE I/O patterns when their frequency is close to the DPOAE frequency (Cianfrone et al., 1990; Lonsbury-Martin et al., 1990). Moreover, Moulin et al. (1993) showed signi¢cantly higher DPOAE amplitudes in SOAE-positive ears, even when ears showing SOAE frequencies less than 300 Hz around distortion frequencies were excluded. Even so, the authors thought that the amplitude level would be measured at maximum level if primary-tone frequencies were adjusted such that 2f1 3f2 DPOAE almost equaled the SOAE frequencies in the present investigation. In the previous studies, statistically signi¢cant di¡erences between groups were found in spite of the intersubject di¡erences and factors a¡ecting OAE measurements, even though, because of large intersubject di¡erences in amplitude levels, selecting two groups of subjects representing the presence and absence of SOAEs is not the most optimal experimental design. Only subjects with SOAEs in one ear were allowed to participate in the present investigation in order to eliminate the factors causing intersubject di¡erences that may contaminate the results. Hence, this study was designed so that the only factor in£uencing the amplitude of the DPOAEs would be the presence of SOAEs. Since it was reported that having an SOAE in either ear signi¢cantly increased the likelihood of having one in the other ear (Penner et al., 1993), the investigators had to examine more than 200 individuals to discover eligible subjects for the present study. Although a¤rmative results were obtained by Moulin et al. (1993), there are system- and subject-related factors that deserve to be discussed. The most e¡ective f2 /f1 ratio for eliciting DPOAEs from 1 to 4 kHz was reported as 1.22 (Harris et al., 1989). While the f2 /f1 ratio used in the present study (1.22) was identical to the optimal ratio, the ratio used by Moulin et al. (1993) was 1.17. The estimates of the prevalence of SOAEs depend on the criterion for identifying a spectral peak as an SOAE, the number of spectra in which an emission must appear in order to be identi¢ed as an SOAE, the sensitivity of the microphone and the level of the noise £oor (Penner et al., 1993). SOAEs were considered valid if the amplitudes exceeded the noise £oor by at least 3 dB. Increasing the number of spectra averaged may potentially decrease the variability of the noise, thereby improving the chances that a low-level SOAE will be su¤ciently above the noise to be judged a peak.
The major limitation in increasing the number of samples is that the subject may not be able to sit quietly during the extended sampling period. It is possible to decrease the variability in the noise £oor by increasing the number of Fast Fourier Transforms average. Increasing the number of spectra averaged decreases the standard deviation of lower-level SOAEs (Penner et al., 1993). Another di¡erence between the Moulin et al. (1993) study and the present one is that, in the former study, only 10 sweep spectra were averaged for the measurement of SOAEs, whereas in the present study at least 100 sweep spectra were averaged for the detection of SOAEs. It has been reported that the prevalence of the SOAEs is greater in females (83%) than in males (62%) and the occurrence of multiple SOAEs is much more prevalent in females than males (Penner et al., 1993 ; Penner and Zhang, 1997). Moulin et al. (1993) also showed a gender e¡ect on DPOAE amplitude in the 1^2-kHz frequency region. These frequencies correspond to the prominent frequency range of SOAEs that the females had a higher incidence of SOAEs compared to the males. This gender e¡ect was strongly reduced when only SOAE-negative subjects were evaluated. In the present study, the SOAE-positive ears group and the SOAE-negative ears group included an equal number of males and females. Consequently, the within-subjects design eliminated any type of gender e¡ect on the DPOAEs. On the other hand, gender e¡ect had an in£uence on DPOAEs inevitably because of betweengroup measurements in the study performed by Moulin et al. (1993). In this study, the mean DPOAE amplitude measured in response to each primary-tone level in SOAE-positive ears was compared to the corresponding mean DPOAE amplitude level in SOAE-negative ears. That is the mean DPOAE amplitude obtained in response to 40 dB SPL primary-stimulus level in SOAE-positive ears was compared to the mean DPOAE amplitude measured in response to 40 dB SPL primary-tone level in SOAE-negative ears, etc. Thus, two means were derived from the two independent samples for each primarytone level. Identical comparisons were also made for the mean DPOAE amplitudes recorded in response to the other primary-tone levels, respectively. For levels from 40 to 65 dB SPL, DPOAE amplitudes of the ears with SOAEs were greater than those ears without SOAEs, and these results were determined to be statistically signi¢cant (P 6 0.05). At 70 dB SPL, mean DPOAE amplitude was greater in the ears with SOAEs compared to the ears without SOAEs, but not statistically signi¢cant (P s 0.05). Brown (1987) has pointed out that there is a distinction to be made between distortion generated by lowlevel stimuli and by stimuli at levels higher than 65^70 dB SPL in rodents. A distortion response to high-level
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stimuli was even detected in a `dead' ear and, thus, the high-level DPOAE may have been related to passive cochlear mechanics and/or hydrodynamics and has doubtful use as a monitor for cochlear function. The distortion generated by lower level stimuli, however, is physiologically vulnerable and should be directly linked to the activity of outer-hair cells in the cochlea. Norton and Rubel (1990) reported that the responses to highlevel stimuli are susceptible to stimulus artifacts and/or may represent the responses of passive cochlear elements in gerbils. Mills and Rubel (1994) observed also in gerbils the elimination of DPOAEs evoked by lowand moderate-stimulus levels following furosemide intoxication. On the other hand, the passive source of DPOAEs evoked by high stimulus levels was essentially unchanged at all frequencies. Whitehead et al. (1992) studied the source of DPOAEs in rabbits. The DPOAEs evoked by low-level ( 6 60^70 dB SPL) stimuli were abolished within 3^4 min of induction of anoxia, whereas DPOAEs evoked by high-level stimuli were unchanged in this period. Similarly, DPOAEs elicited by low-level stimuli were temporarily abolished by an acute administration of ethacrynic acid that had little e¡ect on high-level DPOAEs. These studies present evidence regarding the involvement of the passive cochlear elements, at least in animal subjects. These ¢ndings strongly suggest that low- and high-level 2f1 3f2 DPOAEs arise from discrete sources. Norrix and Glattke (1996) suggested that the micromechanics of the cochlea behave di¡erently at high- and low-stimulus levels. Active and passive elements are believed to contribute to basilar-membrane motion patterns at low- and high-stimulus levels, respectively. All these investigators suggested that DPOAEs evoked by low-level stimuli are an active, micromechanical process and vulnerable physiologically. This would agree with the knowledge suggesting the use of low levels of stimulation in clinical practice. The ¢ndings of the present study infers that primary-tone level higher than 65 dB SPL may evoke passive cochlear properties, also in humans. Even at 65 dB SPL primary-stimuli level, passive cochlear activities are assumed to take part in the response, to some extent, and that this may be the reason why the DPOAE amplitude di¡erences between SOAEpositive and SOAE-negative ears were not statistically signi¢cant at the highest test level. The present ¢ndings suggest that SOAEs add to the overall DPOAEs response level, except at the high-stimuli level of 70 dB SPL. Their potentiating e¡ect likely occurs from the synchronous capturing of SOAEs during DPOAE data collection. The evidence related to active and passive properties of the cochlea was obtained in the present study, in contrast to the previous investigations, possibly, due to the within-subject design. It may be useful to assess the number and level of SOAEs when considering the range of normality in
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DPOAE response levels in normal-hearing subjects. In other words, the DPOAE response level that is judged to indicate normal outer-hair-cell function will vary with the number and level of the SOAEs. This study may also imply that normal-hearing individuals with no or few SOAEs may have low levels of DPOAEs. Therefore, SOAEs play an important role in the DPOAE measurements. 5. Conclusion This investigation demonstrated signi¢cantly higher DPOAEs in the ears exhibiting SOAEs than in the ears without measurable SOAEs. The detectability of SOAEs should be assessed before the evaluation of DPOAE amplitudes is made among ears. SOAE presence causes an enhancement of DPOAE amplitudes. According to the present results, this enhancement clearly occurs for primary stimuli of 40^65 dB SPL, while passive cochlear properties begin to contribute to the DPOAE at primary-stimuli levels greater than 65 dB SPL. DPOAE recordings at low primary levels seem to be more directly linked to active cochlear mechanisms. Within-subject design of the present investigation may have a signi¢cant role to obtain results regarding the active and passive cochlear properties. This would argue in favour of the use of low levels of stimulation in clinical practice. Acknowledgments The authors would like to thank to Prof. Dr. Nermin Baserer and Prof. Dr. Mehmet Tinaz for the permission to use the OAE Laboratory.
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