Chronic Conductive Hearing Loss in Adults Effects on the Auditory Brainstem Response and Masking-Level Difference

ORIGINAL ARTICLE Chronic Conductive Hearing Loss in Adults Effects on the Auditory Brainstem Response and Masking-Level Difference

Michael O. Ferguson, MD; Raymond D. Cook, MD; Joseph W. Hall III, PhD; John H. Grose, PhD; Harold C. Pillsbury III, MD

Objective: To determine whether chronic conductive Results: When comparing the patients’ diseased ears hearing loss in adults results in changes in the auditory with their healthy ears, significant delays were seen for brainstem response (ABR) similar to those observed in wave V as well as for the I-V and III-V interwave inter- children with histories of otitis media with effusion. vals. For comparison with the control population, significant prolongations were again seen for wave V and Design: Test of effect of unilateral conductive hearing for the III-V interwave intervals. In addition, reduced loss on adult ABR using age-matched control group and masking-level differences and significant correlations subjects as their own controls. between the masking-level differences and the ABRs, independent of hearing threshold, were noted. Subjects: Twelve adults with a history of unilateral conductive ear disease. An age-matched control group of 21 Conclusions: The results suggest that chronic con- adults was also tested. ductive impairment in adults leads to changes in the ABR similar to those observed in children with histo- Methods: The ABR, an electrophysiologic test of audi- ries of otitis media with effusion. As such, these tory brainstem functioning, was used to evaluate pos- changes do not appear to be related to a critical period sible brainstem abnormalities in the impaired listeners. of development. In addition, the masking-level difference, a behavioral test of binaural auditory processing in the brainstem, was used. Arch Otolaryngol Head Neck Surg. 1998;124:678-685

EVERAL investigations1-7 have tent. Whereas Anteby et al1 found abnor- demonstrated that the audi- mally long wave III-V and wave I-V laten- tory brainstem response cies for children with a history of OME, (ABR) often shows abnor- Folsom et al3 noted significant increases malities in children having in the I-III and III-V interwave intervals, Sa history of otitis media with effusion with significant increases in the absolute (OME) and associated hearing loss. The latencies of waves III and V. Similarly, hypothesis underlying these investiga- Gunnarson and Finitzo5 found signifi- tions is that fluctuation of hearing levels cant delays in the absolute latencies of (HLs) during development may result in waves III and V as well as in the I-III and changes in auditory neural structure and I-V interwave intervals when comparing function, particularly if there is a critical controls with children with OME. In ad- period during maturation in which the dition, they noted an abnormality in the central neurophysiologic condition is rela- binaural interaction response in children tively labile.3 with OME. An investigation by Hall and A common finding in these ABR stud- Grose6 also found increases in the I-III and ies of the juvenile population is an in- I-V interwave intervals and significant decrease in the interwave intervals com- lays in the absolute latencies of waves III From the Division of pared with a control population, despite and V. Chambers2 noted prolongations in Otolaryngology–Head and resolution of effusion and the presence of the I-III interwave interval, but no in- Neck Surgery, University of normal audiometric thresholds at the time crease in either the III-V or I-V intervals. North Carolina School of Medicine, Chapel Hill. Dr Cook of testing. Although findings of altered A general synopsis of these studies is that is now with the Division of brainstem electrophysiologic features have early conductive impairment results in sig- Otolaryngology–Head and been universal among these studies, the nificant increases in the absolute laten- Neck Surgery, Duke University, specific nature of the interwave changes cies of wave III or V (or both) and 1 or Durham, NC. reported have been somewhat inconsis- more of the interwave intervals.

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©1998 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/25/2021 SUBJECTS AND METHODS hearing impairment was about 14 years (range, 2-25 years). None of the patients acquired the hearing loss prior to 12 years of age. SUBJECTS ABR STIMULI AND PROCEDURE Control Group Audiological testing took place in a single-walled sound The control group consisted of 21 adults (10 women and 11 suite. Otoscopic examination was performed by 1 of 2 in- men) ranging in age from 24 to 50 years (mean age, 31.4 years). vestigators (M.O.F. and R.D.C.). The ABR evaluation was Use of the adults as subjects was approved by the human sub- conducted in a quiet examination room after the proce- ject institutional review board. Adults older than 51 years were dures were fully explained and signed consents were ob- excluded from the study because of the possible changes in tained. Subjects were awake and encouraged to relax with the ABR secondary to the degenerative effects of age on the their eyes closed. They were tested in the prone position auditory system.23 Control subjects had no history of hear- in a comfortable reclining chair. The ABR evaluation was ing impairment, ear trauma, or ear surgery. Inclusion in the performed using a Nicolet Spirit evoked potential system control group required that an audiogram with normal results (Nicolet, Madison, Wis). Electroencephalographic activ- be obtained at the time of ABR data collection. ity was recorded for each ear by a midline forehead (non- inverting) electrode (Cz) and an ipsilateral ear canal (in- Experimental Group verting) electrode (A1 or A2), with a ground electrode placed 1 to 2 cm above the nasion. Nicolet gold foil TIPtrodes were This group was composed of 12 adults (10 women and 2 used in the ear canal since it was determined that they op- men) ranging in age from 19 to 49 years (mean age, 37.3 timized the recording of wave I amplitudes, otherwise sil- years). The subjects were drawn either from a list of pa- ver electroencephalographic electrodes were used.24 Inter- tients with conductive hearing impairment scheduled to electrode impedance was maintained at 5000 ⍀ or less. undergo corrective middle ear surgery or from conduc- Click stimuli were produced via 100-micosecond rect- tively impaired patients seen for a routine visit in the out- angular electrical pulses transduced through tube phones patient clinic. The cause of impairment was varied, includ- (ER-3A tube phones, Etymotic Research, Elk Grove Vil- ing otosclerosis, cholesteatoma, tympanic membrane lage, Ill). Insert earphones were deeply inserted to obtain perforation, and chronic infection. Inclusion in the experi- maximal interaural attenuation.25-27 Clicks had peak en- mental group required a unilateral chronic conductive hear- ergy at 3000 Hz. Each ear in the control group was stimu- ing loss between 25 and 55 dB HL at 2000 Hz and 4000 lated at click intensity levels of 60, 70, and 90 dB nHL. The Hz, confirmed by repeated audiograms at the time of the diseased ears in the patient group were additionally stimu- study. Individual patient audiograms (air conduction) are lated at 100 dB nHL, and the healthy ears in this group were shown in Table 1. Bone conduction thresholds were always 15 dB HL or better. Average length of time for Continued on next page

Animal research has provided additional support brainstem in children with recurrent OME.6,13-15 These for an association between attenuated auditory input studies have shown that the MLD is typically reduced and abnormalities in the auditory brainstem develop- when OME is present, remains significantly decreased ment. Experimentally induced conductive hearing even after the placement of tympanostomy tubes and the impairments during critical periods are known to pro- subsequent return of normal bilateral pure tone audio- duce neural alterations central to the cochlea. Specific metric thresholds in quiet (ie, no noise present),13 but studies have demonstrated abnormalities in the devel- often returns to normal 1 to 2 years following restora- opment of binaural neural elements in the auditory tion of normal hearing thresholds.16 Further study6 ex- brainstem, especially in cases of unilaterally induced amining both MLDs and ABRs in children having a his- conductive hearing loss.8-11 tory of OME with hearing loss showed both reduced MLDs In addition to the use of the ABR as a means of evalu- and abnormalities in the ABRs. In addition, the study ating auditory brainstem function, behavioral evidence showed a significant correlation between the decreased of abnormalities in the brainstem auditory processing can MLDs and the degree of ABR waveform asymmetry. Al- be obtained through the use of the masking-level differ- though the MLD is based on low-frequency stimulation ence (MLD).12 The MLD is a psychoacoustic test that mea- and the ABR is based primarily on high-frequency stimu- sures the sensitivity of the auditory system to interaural lation, both rely critically on brainstem function, and pre- differences of time and amplitude. In the basic configu- vious studies17,18 of listeners with presumed brainstem ration, the masking noise is presented in phase to the 2 pathologic features have shown a significant relation be- ears (No). The signal is presented either in phase to the tween ABR and MLD results. 2 ears (So) or ␲ radians out of phase at the 2 ears (S␲). Interestingly, studies19-22 of adults with acquired con- The MLD is the difference in the levels of the signal at ductive hearing impairment have also indicated re- masked threshold in these 2 configurations. It is as- duced MLDs. Research20,22 has shown that reduced MLDs sumed that the MLD is primarily dependent on audi- persist even after the postsurgical restoration of normal tory brainstem neurons receiving binaural input. Thus, audiometric thresholds, but often recover over a 1- to 2- the MLD too has been used as a tool for analyzing the year period. This pattern of results is similar to that found effects of early conductive hearing loss on the auditory by Hall et al16 for children with a history of OME. The

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©1998 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/25/2021 stimulated at the intensity level necessary to compensate interaurally in phase (So) or 180° out of phase (S␲)tothe for the hearing loss in the impaired ear. The intensity level 2 ears. All stimuli were presented binaurally using ear- at which the healthy ear was stimulated was determined phones (MDR V6 earphones, Sony Electronics, Tokyo, Ja- by first calculating the interaural difference of the hearing pan) mounted in circumaural cushions. Stimulus timing thresholds of the healthy and diseased ears at 2000 Hz and and response collection were controlled by a microcom- 4000 Hz. This interaural difference was then subtracted from puter (Gateway microcomputer, Gateway 2000, North 100 dB nHL (the stimulus intensity for the diseased ear) Sioux, SD). The MLD was determined by subtracting the to determine the level of stimulation for the healthy ear. masked threshold level of the interaurally phase-shifted sig- This ensured that the stimulus level reaching the cochlea nal condition (NoS␲) from the masked threshold level of of each ear was matched for intensity. Clicks were pre- the interaurally in phase signal condition (NoSo). The sented at a rate of 15.1 per second. 300-Hz wide masker was presented continuously at a pres- The electroencephalographic response was amplified sure spectrum level of 60 dB. and bandpass filtered between 100 Hz and 3000 Hz, then sent to a signal averager set to scan a 10-millisecond ep- PROCEDURE FOR MLD och. The final averaged response, the result of 1500 stimulus presentations, was graphically displayed on the sys- Data were collected using a 3-alternative, forced choice, tem’s video monitor. 3-down, 1-up adaptive strategy that estimated the 79.4% For each subject, peak latencies of waves I, III, and V detection threshold.28 There were 3 observation intervals were measured and from these values interwave interval with the signal presented in only 1 interval, at random. values between waves I and III, waves III and V, and waves With 3 successive correct responses, the signal level was I and V were calculated. The ABR tracings were judged in- reduced; after 1 incorrect response, the signal level was dependently by the 2 investigators (M.O.F. and R.D.C.). increased. The threshold run was stopped after 12 rever- Differences in measurements between investigators were sals in the direction of signal attenuation, and the average reevaluated. For each group of subjects the average values of the last 8 reversals was taken as the threshold for the of peak latencies were computed, and measurements were run. An initial step size of 8 dB was reduced to 4 dB after compared both between groups and interaurally within each the first 2 reversals and reduced to 2 dB after the second 2 subject. reversals. The subject was provided with visual feedback after each response. At least 2 thresholds were obtained STIMULI FOR MLD and averaged for each signal condition, with a third condition added and included in the average if the range of The masking noise for the MLD test was a 300-Hz wide- the first 2 thresholds was greater than 3 dB. Ten of the 12 band arithmetically centered on 500 Hz and presented in patients underwent MLD testing. Normative data were phase to the 2 ears (No). The digitally generated 400- drawn from a previous study21 in our laboratory of 14 lis- millisecond 500-Hz pure tone signal had 50-millisecond teners with normal hearing who were tested under iden- cosinusoidal rise-fall times and was presented either tical conditions.

results from adult listeners may suggest a relatively slow same listeners may shed light on the question of whether adjustment of the mature auditory system to the changes peripheral ear disease in adults may result in brainstem in binaural cues associated with hearing loss and subse- abnormalities. If so, then these data may provide fur- quent restoration of normal hearing. ther evidence that an element of plasticity or lability un- The similarity of the MLD effects found in children related to a critical period of development might exist in with a history of OME and in adults with a history of ac- the mature auditory system. quired conductive hearing loss suggests that it may not be necessary to appeal to the concept of a critical period RESULTS or developmentally related plasticity to account for the MLD effects found in children with a history of OME. AUDITORY BRAINSTEM RESPONSE Given this possibility, it may likewise be unnecessary to appeal to developmentally related plasticity to account Control Group for the abnormalities in the ABR results found in children with a history of OME. To examine this question Preliminary analyses of the ABR tracings, including the further, it is of interest to ascertain the effect of acquired absolute wave latencies of waves I, III, and V as well as conductive hearing loss on the ABRs of adult listeners. interwave intervals I-V, I-III, and III-V, showed no sig- Our study addresses this question by investigating the nificant interaural differences between the left and right ABR and the MLD in a group of adults with known uni- ear for the control group. Therefore, data from both ears lateral chronic conductive loss and a control group of age- of an individual control listener were averaged. The mean matched adults with no known history of ear disease. The ABR absolute wave and interwave latencies at the stimu- main goal was to determine whether chronic conduc- lus levels of 60, 70, and 90 dB nHL are shown in Table 2. tive hearing loss in adults results in ABR abnormalities As the click stimulus increased in intensity, the mean la- that are similar to those seen in the juvenile population. tencies for waves I, III, and V decreased, demonstrating Examination of both the ABR, an electrophysiologic test the expected effect of stimulus intensity on ABR wave la- of auditory brainstem functioning, and the MLD, a be- tency. The I-III interwave interval increased proportion- havioral test of auditory brainstem functioning, in the ally to stimulus intensity, while the III-V and the I-V

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©1998 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/25/2021 interwave intervals were inversely related to intensity. The wave latencies for healthy ears were calculated from ABR variation in the I-V interwave interval across stimulus level recordings at stimulus levels that were adjusted to com- is shown in Figure 1. The graph shows a monotonic pensate for hearing loss in the impaired ear on an indi- relationship between interwave interval and stimulus in- vidual basis. Thus, the stimuli reaching the cochlea of tensity, demonstrating a need to compensate for HL dis- both diseased and healthy ears were matched with re- crepancies when comparing healthy ears with conduc- spect to intensity levels. tively impaired ears. Comparison of Diseased Ears Patient Group With Healthy Ears in Patients

Figure 2 shows an example of ABRs recorded in the A 2-factor repeated measures analysis of variance was per- healthy and diseased ears of a subject from the patient formed on the absolute wave latencies (I, III, and V) of group. The subject’s tracings were selected to reflect typi- the healthy and diseased ears to determine if any signifi- cal waveforms and latencies for the patient group. The cant differences existed. This analysis showed no effect mean ABR wave latencies and interwave latencies for both of ear (F[1,11] = 1.56; P = .24) and the expected main ef- the diseased ears and the healthy ears are shown in Table fect of wave latency (F[2,22] = 8948.44; P = .001). The 2. Diseased ear mean wave latencies were derived from interaction between ear and wave latency was also sig- ABR recordings at a stimulus level of 100 dB nHL. Mean nificant (F[2,22] = 11.75; P = .001) and therefore, simple main effects were assessed.29 The results revealed no significant differences between the 2 ears for wave I la- Table 1. Summary of Patient Audiogram Data tency or wave III latency, but the wave V latency for the diseased ear was prolonged in comparison with the healthy Frequency, Hz ear (F[1,11] = 37.65; P = .001). Mean absolute wave la- Patient No. Ear 250 500 1000 2000 4000 8000 tencies (I, III, and V) of the diseased ears relative to the mean latencies of the healthy ears are shown in the first 1 Diseased 40 25 25 30 25 35 Figure 3 Healthy −10 15 10 0 10 20 half of . 2 Diseased −5 35 20 20 30 25 These results suggest that differences in the de- Healthy −10 −10 0 −5 5 5 rived interwave latencies should also emerge between 3 Diseased 65 50 40 45 50 60 ears. A 2-factor repeated measures analysis of variance Healthy 10 10 10 −5 10 5 applied to the interwave latencies (I-V, I-III, and III-V) 4 Diseased 55 50 40 45 40 35 for the 2 ears showed a significant difference between Healthy 15 10 10 5 15 15 5 Diseased 25 25 30 30 30 45 the ears (F[1,11] = 27.39; P = .001), demonstrating an Healthy 30 35 15 10 5 20 increase in the overall interwave latencies in the dis- 6 Diseased 35 30 25 25 40 75 eased ears. As expected, there was also a significant Healthy 15 5 10 10 15 25 main effect of interwave latencies (F[2,22] = 3337.96; 7 Diseased 20 20 30 25 45 65 P =.001). However, the interaction between ear and Healthy 10 10 10 5 20 20 interwave latency was not significant (F[2,22] = 2.83; 8 Diseased 35 30 30 45 40 55 P = .08). Preplanned analyses of the individual inter- Healthy 5 10 5 5 5 20 9 Diseased 20 25 35 40 40 70 wave latencies were performed using independent t 29 Healthy −10 −10 0 10 −5 10 tests. Ear differences were significant for both the I-V 10 Diseased 45 30 25 20 35 50 and the III-V interwave intervals (T11 = −5.29, PϽ.05; Healthy 15 5 10 5 0 15 T11 = −0.50, PϽ.05, respectively), but not significant 11 Diseased 65 50 45 40 25 35 for the wave I-III interval (T11 = −1.27; P = .23). Inter- Healthy 30 30 25 10 10 20 wave intervals (I-V, I-III, and III-V) relative to the mean 12 Diseased 65 50 50 35 40 60 Healthy 20 20 10 5 10 25 latency of the patients’ healthy ears are shown in the second half of Figure 3.

Table 2. Auditory Brainstem Response Absolute Wave and Interwave Latencies for Patient and Control Groups*

Absolute Wave and Interwave Latencies

I III V I-V I-III III-V Patients Diseased ear 1.84 (0.22) 3.99 (0.21) 5.95 (0.28) 4.12 (0.16) 2.15 (0.13) 1.97 (0.11) Normal ear 1.86 (0.11) 3.95 (0.12) 5.78 (0.16) 3.92 (0.13) 2.09 (0.09) 1.83 (0.14) Controls At 60 dB nHL 1.98 (0.19) 4.11 (0.22) 6.04 (0.22) 4.06 (0.22) 2.11 (0.17) 1.95 (0.15) At 70 dB nHL 1.75 (0.14) 3.89 (0.16) 5.74 (0.22) 3.99 (0.18) 2.14 (0.11) 1.86 (0.15) At 90 dB nHL 1.55 (0.18) 3.76 (0.11) 5.49 (0.21) 3.94 (0.19) 2.22 (0.17) 1.72 (0.17)

*All values are mean (SD) milliseconds. Results for the diseased ear were obtained at a stimulus level of 100 dB normal hearing level (nHL). Normal ear measurements were intensity matched to compensate for interaural hearing disparity.

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0.0 3.95 I-V Interwave Interval, ms 3.90 –0.2

3.85 –0.4 60 7080 90 ms Latency With Regard to Patient Healthy Ear, I III VI-V I-III III-V Click Intensity Level, dB nHL ABR Absolute Waves and Interwave Intervals

Figure 1. Mean latencies of the I-V interwave intervals of the control group Figure 3. Mean auditory brainstem response (ABR) latencies for patients’ at intensity levels of 60, 70, and 90 dB normal hearing level (nHL). Vertical diseased ears relative to mean latencies of patients’ healthy ears. Stippled bars represent±1SD. region indicates±1SDofhealthy ear results; vertical bars,±1SDof diseased ear latencies; and asterisks, significant differences between ears ( PϽ.05). I-V

0.6 I-III III-V ∗

0.4 ∗

0.2 Healthy Ear 0.0

I III V –O.2

I-V Latency With Regard to Control, ms

Wave Amplitude Wave –0.4 I III VI-V I-III III-V I-III III-V ABR Absolute Waves and Interwave Intervals

Figure 4. Mean auditory brainstem response (ABR) latencies for patients’ diseased ears relative to mean latencies of control group. Stippled region indicates±1SDofcontrol results; vertical bars,±1SDofdiseased ear Diseased latencies; and asterisks, significant differences between groups ( PϽ.05). Ear

2 groups indicated a significant main effect of group (F[1,31] = 4.69; P = .04) and, as expected, a significant main effect of absolute wave (F[2,62] = 11.140; P = .001). 1.0 3.05.0 7.0 No significant main effect was found for the interaction Latency, ms between group and wave (F[2,62] = 2.94; P = .06). Pre- Figure 2. Representative waveforms for the healthy and diseased ears of a planned independent t tests were again performed to de- subject in the patient group. Patient chosen had absolute wave and interwave termine group differences at each independent wave. As latencies close to the means for the patient group. with the results of the patients’ diseased vs healthy ears, the latency of the absolute wave V in the patient group Comparison of Diseased Ears With Control Group was significantly prolonged compared with the control population (T31 = −2.46; P = .02). Again, consistent with As with the interaural analyses above, comparing the ABR the previous analysis comparing the healthy vs the dis- data of the diseased ears of the patient group with the eased ear of the experimental group, no significant ABR data from the control group requires that the 2 groups differences were found for wave I or III (T31 = −1.61, be matched by intensity to compensate for the conduc- P = .12; T31 = −1.63, P = .11). Absolute wave latencies relative hearing impairment in the patient group. The aver- tive to the mean latencies of the control group are shown age pure tone threshold at 2000 and 4000 Hz in the im- in the first half of Figure 4. paired ear of the patient group was approximately 35 dB The analysis of variance on the interwave latencies HL. The average pure tone threshold for the control group showed no significant main effect of group (F[1,31] = 3.78; was approximately 5 dB HL. Thus, using the mean con- P = .06), an expected significant main effect of inter- trol data at 70-dB click stimulus to compare with the mean wave latencies (F[1,31] = 3663.02; P = .001), and a non- patient data at 100 dB will on average adjust for the dis- significant interaction between group and interwave la- parity in hearing sensitivity between groups. tencies (F[2,62] = 2.78; P = .07). Preplanned independent A 2-factor analysis of variance (one within, one be- t tests indicated results that are fairly consistent with that tween) performed on the absolute wave latencies of the seen in the interaural analyses. No group difference was

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©1998 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/25/2021 noted for the I-III interwave latency (T31 = −0.078; P = .86), while group differences were significant for the Table 3. Summary of Threshold and III-V interwave latency (T31 = −2.32; P = .03), again re- Masking-Level Difference (MLD) Data* flecting the longer intervals of the patient group. The only statistical result that differed from the previous analysis NoSo NoS␲ MLD comparing the healthy vs the diseased ear of the experi- Healthy group, mean (SD) 77.9 (1.3) 63.1 (1.6) 14.8 (1.4) mental group was that for the I-V interwave latency. The Patient group, mean (SD) 77.4 (1.4) 68.8 (2.4) 09.6 (2.9) Individual patients, mean present analysis found the group difference of this in- 1 77.6 65.1 12.5 terwave latency marginally insignificant (T31 = −1.93; 2 75.1 69.1† 06.0† P = .06). The interwave intervals relative to the control 3 75.8† 71.6† 04.2† group are shown in the second half of Figure 4. 4 77.3 69.8† 07.5† 5 79.8 69.3† 10.5† MASKING-LEVEL DIFFERENCE 6 76.8 64.6 12.2 7 77.1 68.6† 08.5† 8 79.1 68.3† 10.8† As previously mentioned, the MLD is derived by sub- 9 77.8 69.3† 08.5† tracting the NoS␲ threshold from the NoSo threshold. 10 77.6 72.3† 05.2† Although the NoS␲ and the NoSo thresholds are included in the results, attention is focused primarily on *Normative data from previous study evaluating adult masking-level 21 the MLD as the main measure of binaural processing. Bin- difference. Thresholds are reported in decibel sound pressure level. See the introductory section for explanation of NoSo and NoS␲. aural cues influence the NoS␲ detection thresholds, and †Data outside 95th percentile of normal listener. thus binaural hearing is measured by this threshold, but this threshold is also influenced by the general processing efficiency of the listener.30 This general efficiency fac- regard to interwave intervals, the I-V and the I-III inter- tor is theoretically canceled out by the subtraction of the wave intervals correlated significantly (PϽ.05) with the NoS␲ threshold from the NoSo threshold, since both MLD (r = −0.63 and r = −0.78, respectively), while the III-V thresholds are affected by processing efficiency. The interwave interval was not significantly correlated (r = thresholds for NoSo, NoS␲, and the derived MLDs for −0.11). individual impaired listeners are shown in Table 3. Also shown are control data from a group of adults with healthy COMMENT hearing obtained from a previous study21 using identical stimulus parameters. The most notable distinction be- This study was undertaken to determine whether chronic tween the patient results and the control data is that both conductive hearing loss in adults results in similar ABR the patient NoS␲ thresholds and the MLDs were consis- measurement abnormalities as seen in the juvenile popu- tently poorer than those of the control group, while the lation. If so, it could provide some evidence that a de- NoSo thresholds were similar to the control results. Eight gree of lability or neuronal adjustment unrelated to any of 10 impaired listeners were outside of the 95th per- critical developmental period might exist in the mature centiles (estimated using ± 2 SDs) of the listeners with auditory system. As described earlier, several studies in- healthy hearing for the MLD and NoS␲ threshold. For vestigating children with histories of OME found abnor- the NoSo threshold, 9 of 10 patients were within the 95% malities in their ABRs that were not seen in control popu- confidence interval. Thus, the abnormality in the MLD lations. Despite some individual variation among studies, measure was caused primarily by an abnormally high it was generally noted that wave III or V (or both) were NoS␲ threshold. delayed, and several interwave intervals were prolonged. Our results obtained in adult listeners are in gen- RELATION BETWEEN MLD AND ABR eral agreement with most published reports on children with histories of OME. When comparing the patients’ dis- Because both the MLD and the ABR are related to audi- eased ears with their healthy ears, significant delays were tory brainstem processing, the next step in the analysis seen for wave V as well as for the I-V and III-V inter- was to examine possible relations between the reduced wave intervals. For comparison with the control popu- MLDs and the abnormality in the ABR latencies of the lation, significant delays were again seen for wave V and patient group. The most obvious correlation to investi- for the III-V interwave interval, whereas the difference gate was that between the MLDs and the absolute wave for the I-V interwave interval did not attain signifi- latencies and interwave latencies of the impaired listen- cance. Overall, our results are most consistent with the ers. Because of the influence of HL on both the MLD and study of Anteby et al,1 who found significantly pro- the ABR, it is possible that any relationship between the longed interwave latencies between waves III and V and MLD and the ABR would be attributable simply to the between waves I and V. Our results support an interpre- association of each of those variables to HL. Therefore, tation that conductive hearing loss in adults leads to ab- MLD and ABR correlations were determined using a par- normalities in their ABRs beyond those attributable to tial correlation analysis, with the effects of HL being con- simply loss of hearing sensitivity. trolled statistically (pure-tone average Ͼ500, 1000, 2000, A unique feature of this study is that the diseased and 4000 Hz). No significant correlations were noted be- ears in the patient group could be compared, in essence, tween the MLD and the absolute wave latencies (wave I, with 2 different “control” groups. The similar findings r = 0.35; wave III, r = −0.03; and wave V, r = −0.08). With between the 2 control comparisons suggest a relatively

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©1998 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/25/2021 robust effect. Perhaps the more powerful, or informa- tion between these possibilities, it suggests that abnor- tive, of the 2 controls is the interaural comparison within malities in the ABRs in the presence of long-term each patient. With this interear evaluation, it was pos- conductive hearing loss should not be summarily attrib- sible to match the intensity level reaching the cochlea of uted to a critical period of development in the immature the diseased ear precisely with the intensity level of its system. control. Although the comparison with the control group As with the ABR data, the MLD results are in gen- of subjects with normal hearing was also intensity eral agreement with prior studies19-22 demonstrating a re- matched, it was done so on a group average basis, and duced MLD in listeners with a conductive hearing loss. thus exact intensity matching for each patient was not The reduced MLDs demonstrated in our patients are likely obtained. The interaural comparison represents a tighter to be due to not only poor use of binaural cues but also control because any effect caused by a variable other than to the elevated hearing thresholds and threshold asym- hearing impairment is essentially canceled out. This fea- metry.21 Hall et al21 demonstrated that MLDs will often ture may explain why the results of the 2 control com- improve considerably when tested under conditions of parisons were not identical. In addition, individualized equal sensation level, indicating that the smaller MLDs intensity matching of the interear comparison more closely measured with equal sound pressure level presentation reflects the equal hearing threshold between controls and are attributable to primarily the elevated thresholds in patients that was present in the juvenile investigations. quiet rather than to diminished binaural processing. How- This may account for the fact that the interaural results ever, the same study found that even under conditions agree more closely with the findings of the childhood OME of equal sensation level testing, the resulting MLDs were studies. often still reduced. In addition, a study by Hall and Grose20 In speculating on the cause of the abnormalities in demonstrated a persistence of reduced MLDs for up to the ABRs seen in the conductively impaired ears, it is im- 2 years following surgical correction that resulted in nor- portant to consider all possible sites along the auditory mal audiometric thresholds. Thus, the present MLD re- pathway. One obvious candidate is simply the acoustic sults are of greatest interest when hearing threshold is attenuation resulting from the middle ear disease.3 statistically controlled, as was done in the partial corre- Whereas individual ABR wave latencies generally in- lation between the MLD and ABR. The significant cor- crease in cases of conductive hearing loss, it is believed relations obtained imply an association that is indepen- that this effect is simply related to the decreased level of dent of hearing threshold. While the positive correlation stimulation reaching the cochlea.31 Furthermore, it is be- of the MLDs to the I-V interwave intervals fits well with lieved that interwave intervals are not influenced by con- the significant differences seen interaurally for that par- ductive hearing loss when the sensation level of the stimu- ticular metric, the positive correlation between the MLDs lus is controlled.32 As mentioned previously, the and the I-III interwave intervals is not as compatible with conductive hearing loss in this study was controlled by the current ABR results. adjusting the level of stimulation to each ear. The acous- Overall, this study suggests that chronic conductive tic attenuation resulting from conductive hearing loss hearing impairment in adults leads to changes in the ABR would therefore not appear to be a strong candidate to unrelated to a critical period but similar to those ob- account for the abnormalities in ABR results found in the served in children with histories of OME. This similarity hearing-impaired listeners. warrants the continued investigation of adult patients to Possible effects of middle ear disease on cochlear determine whether the ABR and MLD patterns again change function have also been suggested as a source of the ob- subsequent to the return of normal audiometric thresh- served increases in absolute wave latencies and inter- olds following corrective middle ear surgery. wave intervals.3 However, the literature is unclear re- garding the effect of cochlear hearing loss on I-V interwave Accepted for publication February 2, 1998. intervals. Although some reports suggest that cochlear Reprints: Michael O. Ferguson, MD, Division of Oto- loss is associated with an increase in the I-V interval,33 laryngology–Head and Neck Surgery, CB No. 7070, Burnett- other reports suggest either no effect34 or even a de- Womack, University of North Carolina at Chapel Hill, crease in the I-V interwave interval.35 However, the au- Chapel Hill, NC 27599-7070 (e-mail: fergusom@med diometric data obtained in our study suggest little evi- .unc.edu). dence of cochlear hearing loss. Therefore, cochlear dysfunction is not considered to be a likely contributor to the results obtained in this study. REFERENCES In keeping with the above discussion, the finding of wave V abnormalities in the presence of normal wave 1. Anteby I, Hafner H, Pratt H, et al. Auditory brainstem evoked potentials in evalu- I characteristics suggests that the basis of the abnormal- ating the central effects of middle ear effusion. 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