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Background Leisure noise may have a significant impact on hearing thresholds and young adults are often exposed to loud music during leisure activities. This behavior puts them at risk of developing noise-induced hearing loss (NIHL). A frequent initial indication of NIHL is reduced hearing acuity at 4 kHz. The objective of the current study was to assess the role of the medial olivocochlear reflex (MOCR) in leisure noise-exposed individuals with and without a 4-kHz notch.
Materials and Methods Audiological evaluation, including pure-tone and immittance audiometry, was performed for 156 college-going, young adults between May 2019 to December 2019. All participants had averaged pure-tone audiometric thresholds within normal limits, bilaterally. Annual individual exposure to personal listening devices (PLDs) was calculated using the Noise Exposure Questionnaire. The participants were then categorized into exposed (with and without audiometric 4 kHz notch) and nonexposed groups. Transient-evoked otoacoustic emission amplitude and its contralateral suppression were measured using linear and nonlinear click stimuli to study the effect of leisure noise exposure on MOCR.
Results A significantly reduced overall contralateral suppression effect in participants exposed to PLD usage (P = 0.01) in both linear and nonlinear modes. On the contrary, significantly increased suppression was observed in linear mode for the 4 kHz frequency band in the PLD-exposed group without an audiometric notch (P = 0.009), possibly suggesting an early biomarker of NIHL.
Conclusion Measuring contralateral suppression of otoacoustic emissions may be an effective tool to detect early NIHL in leisure noise-exposed individuals.
Keywords: Medial olivocochlear reflex (MOCR), Noise Exposure Questionnaire (NEQ), noise-induced hearing loss (NIHL), transient-evoked otoacoustic emission (TEOAE)
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Hearing loss due to noise depends on the intensity level and duration of acoustic exposure, and on individual susceptibility for noise-induced hearing loss (NIHL), among many other factors.[1] Cochlear outer hair cells are known to be a key auditory transmission structure vulnerable to NIHL. Noise-induced damage reduces the hearing sensitivity of individuals and often results in a 4-kHz notch in behavioral audiograms.[2] The 4 kHz notch is defined as occurring when the threshold of hearing at 4 kHz is 10 dB greater than that at 2 and 8 kHz and has been considered as the characteristic notch in audiograms of individuals with NIHL.[3] This audiometric notch is considered as an early biomarker of exposure to noise.[4],[5],[6]
In the human ear, the efferent medial olivocochlear (eMOC) bundle may act to provide a protective mechanism for hearing by altering the mechanical properties of outer hair cells.[7],[8] Function of the eMOC system appears to include prevention or reduction of acoustic trauma, enhancement of speech perception in noise, and increasing efficiency of attention.[9]
The protective effect of eMOC in animals has been well studied. Kujawa and Liberman[10] observed a greater permanent threshold shift (PTS) in animals exposed to noise with completely lesioned olivocochlear bundle (OCB) than in partially lesioned or control groups. Zheng et al.[11] investigated the eMOC’s role in anatomically normal and de-efferented chinchillas. Greater temporary threshold shift and greater PTS and loss of outer hair cells were reported in de-efferented animals. Maison and Liberman[12] further investigated the protective function of eMOC in animals and found those with the weakest eMOC reflex exhibited greater damage to outer hair cells from exposure to noise.
However, the effect of the early NIHL biomarker, the audiometric 4 kHz notch, on medial OCB (MOCB) activity, is as yet unknown. Therefore, the current study assessed the effect of leisure noise exposure on MOCB function for leisure noise, through measurement of transient-evoked otoacoustic emission (TEOAE) contralateral suppression among individuals with and without an audiometric 4 kHz notch. It was hypothesized that individuals exposed to regular raised levels of sound from personal listening devices (PLDs) would exhibit auditory neural degeneration which in turn would lead to reduced afferent input[13],[14] to the MOCB bundle and, subsequently, reduce eMOC reflex activity levels.
MethodsA total of 156 students within the age range of 18 to 25 years recruited from Sri Ramachandra Institute of Higher Education and Research were the participants of this study. All participants volunteered for the study and signed an informed consent form. The study was approved by the institutional ethics committee of the university hospital. The study participants were classified into three groups.
Group I: Normal hearing adults less than 25 dBHL in air conduction (AC) threshold and less than 15 dBHL in bone conduction (BC) threshold in standard pure-tone audiometry for octave frequencies from 250 Hz to 8 kHz of AC and 250 Hz to 4 kHz of BC, in both ears. This group made no use of PLDs.
Group II: Normal hearing adults exposed to PLDs without 4 kHz AC notch in either ear.
Group III: Normal hearing adults exposed to PLDs with 4 kHz AC notch in both ears.
Noise Exposure Questionnaire
The Noise Exposure Questionnaire (NEQ) was developed to estimate the annual noise exposure for an individual, for either exposure to occupational or nonoccupational noise. The NEQ has been validated and utilized in several research studies to evaluate noise exposure in young adults.[14],[15] The NEQ includes demographic details of each respondent and six screening questions concerning high-risk noise exposure and 12 questions regarding episodic noisy activities. Participants were asked to report their usage of PLDs on a written English language questionnaire form. Then the annual exposure (dose %) of each subject with a history of PLD usage was calculated based on episodic frequency (EF) and episodic level (EL). EF calculations were based on the duration and frequency of PLD usage. The frequency of usage was estimated based on how often the individuals were using earphones and the duration of usage was estimated based on how many hours each listening period lasted. Then EF was estimated by multiplying the frequency and duration of PLD usage reported by each subject. Number of hours derived for EF was denoted as C.
The EL of PLDs was predetermined from the literature (i.e., arithmetic mean of low activity level and high activity level for PLDs), and was expressed in Leq (dBA). Annual exposure to PLDs was calculated as follows[15],[16]:
D = (C/T) × 100
where D is the annual exposure of PLD expressed as dose (%), C is the number of hours of exposure reported by each subject for usage of PLD, and T is the number of hours per year at which PLD usage was considered as hazardous. For example, 79 dBA is a commonly recommended exposure level for 8760 hours (i.e., multiplication of 365 days with 24 hours) with a 3-dB exchange rate.[17]
Based on the above calculations, individuals with more than a 1% annual dose were included in groups II and III (exposed to significant PLD usage). Participants with a less than 1% annual dose were included in group I (not exposed to significant PLD usage). The average annual doses for groups II and III were 1.5% and 3%, respectively.
Basic audiologic tests
The audiologic testing was carried out in a sound-treated room and the ambient noise level in that room was maintained within the permissible limits recommended by ANSI S3.1-1999 (R2013). A dual channel diagnostic audiometer (Inventis, Piano model Inventis S.R.L. a Socio Unico, Padova, Italy) was used to perform pure-tone audiometry. Hearing thresholds were determined for the octave frequencies from 250 to 8000 Hz for AC and 250 to 4000 Hz for BC through a modified Hughson–Westlake procedure.[18]
Immittance audiometry (Inventis, Clarinet model) was used to rule out middle ear pathology. Tympanometry was performed using a 226-Hz probe tone and acoustic reflex thresholds were measured for octave frequencies from 500 Hz to 4 kHz. Only participants who had hearing thresholds better than 25 dBHL at 500, 1, and 2 kHz, and “A”-type tympanogram (static compliance of 0.35–1.75 cc and peak pressure of −100 to +50 daPa)[19] with present acoustic reflexes across all frequencies in both ears were involved in the current study.
Otoacoustic emission assessment
The TEOAEs were recorded using the ILO V6 Echoport 292 (Otodynamics Ltd, Herts, United Kingdom) (II)-(S/N:0825) software/hardware system. Two recordings were performed in succession. In the first, TEOAE was elicited using 80 microseconds duration clicks with a repetition rate of 49 clicks/second. Probe fit was confirmed before initiating the test. Acoustic stimulation was delivered at 60 ± 3 dB peak Sound Pressure Level (SPL) using linear and nonlinear modes. This particular intensity level was chosen as optimal based on previous research.[20],[21],[22] The stability of the responses was observed through continuous monitoring of probe noise level. Responses were rejected if probe noise level exceeded 49 dB peak SPL. Totally, 300 averages were made in each test. The diagnostic criteria for the OAE to be considered present were (1) overall signal to noise ratio (SNR) ≥ 6 dB, and (2) response reproducibility and stimulus stability of the waveforms >80%.
Following the baseline linear and nonlinear OAE recordings, contralateral suppression of TEOAE was gauged by presenting continuous broadband noise (0.125–8 kHz) at 40 dB SL in the contralateral ear through ER 3A insert earphones while TEOAEs was recorded in the test ear.[23],[24] The subjects were instructed to remain quiet and keep their head straight during the measurement. The absolute (dB) suppression was calculated by finding the difference between the OAE amplitude obtained with a contralateral acoustic stimulus (CAS) from the CAS condition absent (the baseline TEOAE).
Statistical analysis
Statistical analyses were performed using SPSS 20 (IBM, Armonk, NY, USA). Descriptive statistics were used to analyze the results for the audiologic evaluations. An analysis of variance (ANOVA) followed by Tukey’s post hoc test was performed to analyze possible significant differences between the three groups (two groups exposed and one group not exposed to PLD listening). Chi-square analysis was performed as an additional test to compare the proportion of TEOAEs present across the three groups. A Mann–Whitney U test was conducted to determine whether there was a significant difference between linear and nonlinear suppression. In all cases, the significance criterion was P < 0.05.
ResultsBaseline TEOAE
[Table 1] represents the mean (M) and standard deviation (SD) of amplitude of TEOAE of the participants without CAS .The suppression was measured only for those who met the criteria of >6 dB SNR in TEOAE without CAS condition. Totally, 219 ears from linear TEOAE and 162 ears from nonlinear passed baseline TEOAE [Table 2]. As we can see in [Table 1], the mean of the global amplitude of group I was greater than groups II and III, and group II was greater than group III for the linear and nonlinear mode of both ears. The strongest amplitude was reported in group I and reduced amplitude was observed in group III in both linear and nonlinear TEAOEs.
Table 1 Mean (M) and standard deviation (SD) of the transient-evoked otoacoustic emission (TEOAE) amplitude without contralateral acoustic stimulus (60 dB peak SPL) for linear and nonlinear TEOAE
Table 2 Percentage and number of ears (n) meeting the diagnostic criteria in baseline transient-evoked otoacoustic emission (TEOAE; 60 dB peak SPL)[Table 2] summarizes the total number of ears in which baseline TEOAEs were present across the three groups. The global and half octave frequency bands suppression effects were obtained for these individuals. Totally, in linear mode 219/312 (70%) of ears and in nonlinear mode 162/312 (52%) of ears showed >6 dB SNR and were included in this study.
As can be observed, the number of ears meeting the TEOAE response criteria varied across the three groups. The difference in proportion of TEOAE presence across the three groups was statistically significant for linear (χ2(2, 219) = 76.87, P < 0.05) and nonlinear mode (χ2(2, 162) = 83.08, P < 0.05), with levels of TEOAE prevalence highest in group I and lowest in group III. Among the participants from group III, suppression was therefore not tested for 75% of participants for linear TEOAEs and 94% of participants for nonlinear TEOAEs due to an absence of an accepted baseline TEOAE recording. The sensitivity and specificity of TEOAE in identifying the exposed groups with and without audiometric notch is represented in [Table 3].
Table 3 Sensitivity and specificity of linear and nonlinear transient-evoked otoacoustic emission (TEOAE) recordings in identifying personal listening device-exposed individuals with 95% confidence intervals (CIs)Comparison of contralateral suppression of TEOAE across groups
Comparison of global suppression of TEOAE
The mean and SD of TEOAE suppression amplitudes for the three groups are shown in [Table 4]. One-way ANOVA showed significant differences were observed among both linear and nonlinear groups (P < 0.05). Tukey posthoc test showed [Table 5] that significantly less suppression was observed in group III (0.3 dB) compared to group I (1.15 dB) and group II (1.26 dB). The suppression effect in group II was greater in magnitude than in group III for linear TEOAEs. A marginally higher TEOAE suppression effect was observed in group II compared to group I in linear mode, without reaching statistical significance. On the other hand, in nonlinear mode, significantly less suppression was observed in group III (0.58 dB) compared to group I (1.7 dB). No other group comparison showed significant differences, though the suppression effect in group II was observed to be marginally less than group I, and group III showed a lesser effect than group II.
Table 4 Mean and standard deviation (SD) of global and half-octave bands suppression for both linear and nonlinear modes across groups
Table 5 Posthoc Tukey (HSD) multiple comparison of suppression with respect to P-valueComparison of half-octave band suppression of TEOAE
The contralateral suppression effect was also examined for half-octave frequency bands at 1, 1.4, 2, 2.8, and 4 kHz. As summarized in [Table 5], in linear mode, significantly less suppression effect was obtained for group III compared to group I and group II for all half octave frequency bands. Only the 4 kHz frequency band of group II (1.22 dB) showed significantly greater suppression compared to group I (0.75 dB). No significant differences in suppression effect across half octave frequency bands in the other groups was seen.
DiscussionThe current study compared the strength of the MOCBin individuals who had significant PLD exposure with and without an early sign of NIHL (i.e., 4 kHz notch).
Baseline TEOAE (60 dB peSPL) as a function of stimulus type
The sensitivity and specificity of nonlinear TEOAE to detect the leisure noise-exposed group with 4 kHz notch were 94% and 92.3%, respectively. On the other hand, sensitivity and specificity were 75% and 100%, respectively, in linear mode. These findings indicate that the nonlinear TEOAE correlated well with audiometric notch findings and is more effective for detection of early NIHL, because so few valid recordings could be made with linear mode.
The effectiveness of nonlinear clicks to detect early NIHL does not seem to vary with stimulus intensity. The current study used a stimulus intensity of 60 dB peSPL. Moleti[25] used a stimulus intensity of 80 dB peSPL and found similar findings for nonlinear TEOAEs. Linear OAE has a probability of recording outer ear canal ringing artifacts that may confound the test results. Although the nonlinear mode was good for reducing stimulus artifact, it also cancels out the linear proportion of TOAE and thus reduces the SNR relative to the linear mode.[26] However, in the current study, 92% of the nonexposed participants (group I) passed (SNR < 6 dB) in nonlinear TEOAE and 100% in linear TEOAE [Table 2]. Though nonlinear TEOAE showed greater sensitivity in identifying individuals with 4 kHz notch (i.e., 6% have passed TEOAE in group III), it was not sensitive to detect individuals from the nonexposed group (i.e., 92% have passed TEOAE in group 1).
The sensitivity and specificity of nonlinear TEOAE of group II were 42% and 92%, respectively. For linear TEOAE, they were 14.4% and 100%, respectively. Both linear and nonlinear clicks yielded an unacceptable sensitivity. Hence, TEOAE at lower stimuli could not be an effective early risk detector of NIHL for participants without 4 kHz notch in the exposed population (group II).
Association between exposure to PLDs and strength of MOCB
The major finding of the current study was that suppression reduces in the noise-exposed adults with audiometric 4 kHz notch, irrespective of the type of recording mode (linear and nonlinear) in TEOAE (P < 0.05). A similar conclusion was reached by Kotylo[27] who reported that elevated thresholds at high frequencies associated with reduced suppression were observed in individuals who were exposed to varying levels of noise exposure within a metal manufacturing factory. An audiometric sign of early NIHL could well match with abnormal TEOAE suppression. In line with this finding, Nada et al.[28] observed weaker suppression in individuals who were exposed to a high level of noise in a textile factory and also found elevated high-frequency thresholds of 3 to 6 kHz, with the most affected frequency being 4 kHz. The current study also indicates that the suppression was weaker or reduced in individuals exposed to leisure noise compared to nonexposed populations.
The inhibitory effect in the presence of contralateral stimulation relies upon the strength of crossed MOCB and normal function of outer hair cells, which are the fundamental effector cells in the system. This inhibitory effect could be compromised for at least two potential reasons. Firstly, there could be cochlear nerve synaptic loss or, secondly, the acetyl-cholinergic receptor (neurotransmitter) on the cochlear outer hair cells could blocked.[29]
On the other hand, although the findings are not statistically significant, a marginally stronger suppression was observed in group II with linear TEOAE (P > 0.05). When we compare the half-octave band suppression responses of group II with other groups, significantly greater suppression was observed at 4 kHz frequency band (P < 0.05) of linear TEOAE. This suggested that an enhanced MOC function was observed in group II. Similar findings were reported by Bhatt,[19] who compared the MOC function across noise exposure background (NEB; i.e., adults routinely exposed or not routinely exposed to leisure noise) and found stronger global suppression in subjects with higher NEB than lower NEB using linear mode TEOAE recordings. However, Bhatt[19] did not investigate the contralateral suppression effect in half-octave frequency bands. Though the current study failed to reach significance at the global level, stronger suppression was observed at a 4-kHz frequency band in group II for linear recordings. This could be due to a MOCB conditioning mechanism. It is also possible that prolonged music exposure can result in an increased discharge rate of MOCB neurons.[30] Hence, it is hypothesized that enhanced strength in a 4-kHz frequency band of exposed without audiometric notch individuals might be a temporary “top–down” adjustment to protect the cochlear structures from NIHL.[10]
It is possible that the MOC efferent system might return to normal functioning if the usage of PLDs is reduced or totally eliminated, because there is evidence of temporary excitotoxicity in the auditory brainstem after the injury to the cochlea in a mouse model.[31] This temporary brainstem excitotoxicity is probably mediated by the MOC efferent system.
The current study found two stages of suppression in NIHL. With continuous exposure to PLDs initially, there is an increased suppression only at 4 kHz, noted in linear mode TEAOE suppression responses. Then, with longer durations of exposure, suppression was observed to be reduced both in linear and nonlinear TEOAE modes, in combination with a 4-kHz audiometric notch.
Hence, in addition to pure tone audiometry and OAE, contralateral suppression may be able to aid detection of early NIHL. This may alert clinicians, trigger hearing conservation actions, and help to prevent further permanent hearing damage.
ConclusionThere was a significant reduction of suppression in both linear and nonlinear TEOAEs among leisure noise-exposed individuals who had an audiometric 4 kHz notch. Those who had leisure noise exposure without 4 kHz notch did not have reduction of suppression response. There was increased suppression only at 4 kHz frequency band in linear TEOAEs. The above findings could be an early biomarker for identification of leisure NIHL. Hence, suppression of TEOAEs can be used as an additional tool for monitoring and prevention of PLD-induced NIHL through appropriate counseling and feedback. Further research is needed to compare the strength of MOC using DPOAE for a better understanding of the use of frequency-specific information of MOC efferent system in the assessment of leisure noise-exposed individuals.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
References
Correspondence Address:
Heramba Ganapathy Selvarajan
Department of Speech Language and Hearing Sciences, Faculty of Allied Health Sciences, Sri Ramachandra Institute of Higher Education and Research (DU), Porur, Chennai 600116, Tamil Nadu
India
Source of Support: None, Conflict of Interest: None
CheckDOI: 10.4103/nah.nah_17_21
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