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. Author manuscript; available in PMC: 2022 Sep 1.
Published in final edited form as: Ear Hear. 2021 Mar 18;42(5):1328–1337. doi: 10.1097/AUD.0000000000001024

Age Effects of Bone Conduction Vibration Vestibular Evoked Myogenic Potentials (VEMPs) Using B81 and Impulse Hammer Stimuli

Jessie N Patterson 1, Amanda I Rodriguez 1,2, Katherine R Gordon 1, Julie A Honaker 3, Kristen L Janky 1
PMCID: PMC8387331  NIHMSID: NIHMS1664447  PMID: 33735908

Abstract

Objective:

Recently developed, the Radioear B81 bone oscillator allows for higher bone conduction vibration output; however, normative data is lacking regarding its use in vestibular evoked myogenic potential (VEMP) testing. The purpose of this study was to examine the effect of age on cervical and ocular VEMP (c- and oVEMP) responses using the B81 and to compare to air-conduction stimuli (ACS), and impulse hammer (IH) VEMP response characteristics.

Design:

c- and oVEMP were completed with ACS, B81, and IH stimuli in healthy participants (age range = 10-87 years, n = 85).

Results:

Regardless of stimulus type, c- and oVEMP amplitudes and response rates decreased with age. For cVEMP response rates, ACS performed better or equal to B81, which was superior to the IH. For cVEMP corrected amplitude, ACS had significantly higher amplitudes compared to B81 and IH. There was no difference in cVEMP corrected amplitude between B81 and IH. For oVEMP, response rates were comparable between stimuli with the largest disparity in response rates occurring in the oldest groups where IH outperformed both ACS and B81. For oVEMP amplitude, IH had significantly higher amplitudes compared to B81 and ACS. There was no difference in oVEMP amplitude between B81 and ACS.

Conclusions:

Age significantly affected c- and oVEMP amplitudes regardless of stimulus type (ACS, B81, IH). All stimuli are appropriate for eliciting c- and oVEMP in the young individuals. While ACS resulted in higher cVEMP corrected amplitudes, either ACS or B81 are appropriate for older individuals. However, for oVEMPs, higher response rates and larger amplitudes were noted for IH followed by B81 and ACS. Overall, the B81 performed well across the lifespan for c- and oVEMPs and may be a reasonable BCV option for patients with absent ACS VEMPs, but at this time is not recommended as a replacement to ACS.

Keywords: vestibular, vestibular evoked myogenic potentials, bone conduction, aging

1. Introduction

Vestibular evoked myogenic potentials (VEMPs) provide valuable information regarding the utricle and saccule, as well as the inferior and superior portions of the vestibular nerve. However, one limitation of using air-conduction stimuli (ACS) is the effect of age on the VEMP response. For both ACS cervical and ocular VEMPs (c– and oVEMPs), response rates and amplitudes decrease and frequency tuning shifts to higher frequencies with age (Welgampola et al., 2001; Piker et al., 2013; Piker et al., 2015). Specifically, absent cVEMP responses are six times more likely to occur in individuals in their 50’s and 60’s, 22 times greater in their 70’s and 54 times greater in their 80’s (Piker et al., 2015). Similar trends are observed for oVEMP, with absent responses six times greater for individuals in their 40’s, 50’s, and 60’s, and 13 times higher in their 70’s (Piker et al., 2015). Further, cVEMP thresholds are higher for individuals over the age of 50 (Janky & Shepard, 2009), and oVEMP thresholds are 5-10 dB higher than cVEMP thresholds (Park et al., 2010; Rosengren et al., 2011). While 500 Hz is the common stimulus used in the clinic, frequency tuning shifts to 1000 Hz for older adults around the 6th decade of life (Piker et al., 2013). Thus, it is challenging to distinguish whether an absent ACS VEMP response is due to age-related otolith loss or to ACS being an ineffective stimulus in older populations.

Furthermore, while sensorineural hearing loss (SNHL) does not affect VEMP responses, conductive hearing loss (CHL) will result in reduced or absent responses due to attenuation of ACS to the inner ear (Halmagyi et al., 1994; Bath et al., 1999). Air-bone gaps of 9 dB significantly reduce ACS VEMP responses (Bath et al., 1999), and air-bone gaps of 20 dB completely abolish ACS VEMP responses (Halmagyi et al., 1994). The presensce of air/bone gaps are especially problematic when testing children, who often have middle ear dysfunction and/or pressure equalization tubes. Air-bone gaps may also be present in ears following cochlear implantation, resulting in reduced ACS c- and oVEMP response rates (Merchant et al., in press). Thereby, the use of bone conduction vibration (BCV) is advantageous in pediatric and adult patient populations.

BCV VEMPs using taps (reflex hammer) and lateral pulses (mini-shaker) may be less affected by age (Cheng et al., 2009; Rosengren et al., 2011). BCV also elicits lower VEMP thresholds compared to ACS (Welgampola et al., 2003; McNerney & Burkard, 2011). These findings may be attributed to BCV more effectively stimulating the otolith organs due to differences in deflection of the cilia (Curthoys et al., 2006). ACS causes pumping of the stapes to deflect the cilia relative to the stationary cell body, whereas BCV causes the cell body to move relative to the stationary cilia (Curthoys et al., 2006). While BCV may provide more efficient stimulation of the otolith organs, traditional bone oscillating devices (i.e., Radioear B71) which are more accessible for clinic use are less reliable in adults (Iwasaki et al.. 2007; Greenwalt et al., in press). Recently the Radioear B81 was developed to have higher output and less distortion (Freden Jansson et al., 2014), but normative data with VEMP testing is lacking. Therefore, the purpose of this study was to examine the effect of age on c- and oVEMP responses using the B81 and to compare to ACS and impulse hammer (IH) VEMP response characteristics. We hypothesized that BCV stimuli would be less susceptible to age as compared to ACS; thus, response rates and amplitudes for c- and oVEMPs would be higher for BCV (B81 and IH), specifically in older participants over the age of 40 years compared to ACS.

2. Methods

2.1. Participants

Eighty-five healthy participants between the ages of 10-87 (mean age 48.8 ± 21.9 years; 38 males) were divided into seven age groups based on decades of life (Table 1). Informed consent was obtained from all participants for testing approved by the Institutional Review Board at Boys Town National Research Hospital. All participants denied a history of known CHL, dizziness/balance symptoms, and diagnosis of neurologic disorders. Tympanic membrane motility was assessed with diagnostic tympanometry (MADSEN OTOflex 100, Schaumburg, IL, USA or GSI Tympstar, Grason-Stradler, Eden Prarie, MN, USA) using a 226 Hz probe tone. Tympanometry was considered normal if peak pressure was between −100 and 30 daPa and peak admittance ≥ 0.2 mmhos (British Society of Audiology, 2013). Participants with abnormal tympanometry were excluded from the study. All participants also received a hearing test that involved evaluating air conduction thresholds at 250 – 8000 Hz and bone conduction thresholds at 250 – 4000 Hz. The participants’ hearing was considered normal if thresholds were ≤ 20 dB. Participants were excluded if they had a CHL, defined as an air-bone gap larger than 10 dB in two consecutive frequencies or asymmetric hearing loss. Asymmetrical hearing loss was defined using guidelines recommended by ASHA (NICE, 2018) and our own clinical definition in multiple laboratories, as a 15 dB difference at two consecutive frequencies (NICE, 2018) or 20 dB at one frequency (authors clinical definition). Symmetrical SNHL in participants over the age of 65 was permissible.

Table 1.

Descriptive statistics for participant groups.

Group (age range) Sample Size Mean age (SD), range Males, Females
1 (10-19) 10 12.9 (3.3), 10-19 4, 6
2 (20-29) 11 26.4 (2.9), 21-29 4, 7
3 (30-39) 10 34.0 (3.3), 30-39 4, 6
4 (40-49) 10 44.0 (2.6), 40-48 5, 5
5 (50-59) 10 54.8 (2.6), 50-59 4, 6
6 (60-69) 12 64.0 (2.7), 60-69 7, 5
7 (70+) 15 77.0 (4.8), 70-87 6, 9
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2.2. VEMP Stimuli and Recording Parameters

ACS and B81 c- and oVEMP responses were obtained using the Interacoustics Eclipse EP15/25 System (Interacoustics, Middelfart, DK). ACS were delivered via ER-3A insert earphones at 120 dB SPL for ear canal volumes ≤ 0.8 ml and 125 dB SPL for ear canal volumes > 0.8 ml (Rodriguez et al., 2018). The B81 bone oscillator was placed on the mastoid bone using a standard bone conduction headband (5.4 N force) where it was felt to be most stable throughout testing. The bone oscillator was moved between the right and left mastoids to test each respective ear. Stimuli were delivered at a level of 70 dB nHL and increased to 75 dB nHL for 27 participants who had absent responses at 70 dB nHL. Of those 27 participants, 20 were over the age of 60 years. ACS and B81 stimuli were 4 msec, 500 Hz tone-bursts, at a repetition rate of 5.1/sec (Blackman gating window, 1 cycle rise/fall time, 0 sec plateau). A band-pass filter of 10 to 1000 Hz for c- and oVEMP was utilized. Rejection was disabled for both cVEMP (± 800 μV 66 dB) and oVEMP (± 400 μV 72 dB). One hundred sweeps were averaged for each c- and oVEMP test.

IH taps were obtained using a Piezotronics IH with integrated force sensor (Model 086C01) and recorded using an Intelligent Hearing Systems 1.30 Opti-Amp differential amplifier (Intelligent Hearing Systems, Miami, FL, USA). IH were manually delivered at the center of the forehead near the hairline (approximately Fz), at a rate of approximately two taps per second, for 30 taps per trial. Taps were administered at a bandage used as a target to reduce variability. The data collection program provided simultaneous feedback on appropriate rate and to ensure that only taps between 10 – 30 Newtons were accepted for analysis (Rodriguez et al., 2020). The epoch began when the hammer force exceeded a 2.0 Newton threshold. There is a ~1 ms delay (Rodriguez et al., 2020); thus all IH latencies were adjusted accordingly in the present study.

Peak force level (pFL) was measured as described in Greenwalt et al., (in press), using the following equation: dB pFL= 20 log(pV/Vcal) +SPLcal + dB conversion. For the B81, 70 dB nHL = 136 dB pFL and 75 dB nHL = 138 dB pFL. For the IH, taps limited between 10-30 Newtons equated to a range of ~140-150 dB pFL (average = 144.8 dB pFL).

2.3. VEMP Testing

The electrode montage for both ACS and BCV cVEMP included placement of the active electrode on the belly of the sternocleidomastoid (SCM) muscle, the ground electrode on the right inner canthus and the reference electrode on the sternum. Electromyography (EMG) was monitored through the active electrode. Impedances were kept below 5k Ω for all electrodes. For cVEMPs, participants lay supine and were instructed to lift their head in the midline position for bilateral SCM contraction. For ACS and B81 cVEMPs, EMG was monitored throughout collection (100-300 μV). Participants received verbal feedback from the examiner to indicate if EMG levels were too low or high. For cVEMPs, the root-mean-square (RMS) EMG was calculated using a pre-stimulus window, which was rectified and averaged to create an estimated pre-stimulus tonic EMG level (Rodriguez et al., 2020). EMG was limited between 100 and 400 μV for 55 of the total 85 participants. The maximum for EMG limiting software was increased to 450 or 500μV to accommodate naturally high EMG levels in 30 participants. Two tracings of each recording were completed to ensure reproducibility. Outcome measures for cVEMP testing included the p13 and n23 latencies, as well as the p13-n23 corrected amplitude (raw peak-to-peak amplitude/raw EMG).

The electrode montage for both ACS and BCV oVEMP included placement of the active electrodes medio-laterally under the contralateral eye, the ground electrode on the sternum and the reference electrode on the right inner canthus. Participants were in a seated position and gazed upwards ~ 30 degrees at a video on an iPod attached to the wall. Two tracings of each recording were completed to ensure reproducibility. Outcome measures for oVEMP testing included the n10 and p16 latencies, as well as the n10-p16 amplitude.

2.4. Statistical Analysis

Descriptive statistics, including means, standard deviations, and responses rates were calculated for the dichotomized age groups. We conducted linear mixed effects models in an R environment using the lme4 package to determine the relationship between VEMP amplitude and age (continuous), gender, and stimulus. Mixed effects models were selected as they allowed us to determine the relationship between the outcome (VEMP amplitude) and predictor variables (age, gender, stimulus) while controlling for variability between participants (Gordon, 2019). Only present responses were included in the models. For all models, the maximal model included age (continuous), stimulus (ACS, B81, IH), and gender as well as all interactions as fixed effects. The maximal model, in all cases, also included random intercepts for ear (left, right) nested within participants.

3. Results

3.1. cVEMP

Representative c- and oVEMP tracings for all stimuli in a 67-year old subject are shown in Figure 1. Descriptive statistics for cVEMP characteristics including p13 and n23 latencies, EMG level, and corrected peak-to-peak amplitudes can be found in Table 2. There was no significant difference in EMG level between groups for any stimuli except for groups 2 and 7 for ACS, where group 2 had significantly lower EMG compared to group 7 (p = .02). As shown in Table 3, overall cVEMP response rates were equal between ACS (92%) and the B81 (92%), both of which were superior to the IH (79%). Between groups, response rates decreased with age regardless of stimulus type. Between ACS and B81 stimuli, ACS response rates were better or equal to the response rates of B81 for 5/7 groups. For two groups (50-59 years and 60-69 years), B81 had superior response rates compared to ACS. Between B81 and IH stimuli, B81 had higher response rates for all groups, except group 1, where all three stimuli had response rates of 100%. There were 5 participants with absent cVEMP responses across all three stimuli: 3 in group 4, 1 in group 6 and 1 in group 7. There were 16 participants with absent responses to IH only, 3 to B81 only, and 1 to B81 and IH. There were only 3 participants with absent responses to ACS only, indicating an added benefit of performing BCV in these participants.

Figure 1:

Figure 1:

Figure 1:

Figure 1:

Figure 1:

Figure 1:

Figure 1:

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Representative responses from a 67-year old subject: A) Air-conduction (ACS) cVEMP, B) B81 cVEMP, C) Impulse hammer (IH) cVEMP, D) ACS oVEMP, E) B81 oVEMP, and F) IH oVEMP.

Table 2.

Cervical VEMP Mean (SD) P13 and N23 latencies, EMG and P13/N23 corrected amplitude (cAmp) for the right and left ears across age group.

P13 N23 EMG cAmp
Group Left Right Left Right Left Right Left Right
10-19 years ACS 12.9 (.77) 12.9 (.79) 20.9 (1.55) 21.0 (1.59) 231.37 (74.42) 213.33 (56.68) 1.5 (.66) 1.60 (.73)
B81 14.1 (1.14) 14.0 (1.2) 21.8 (1.6) 22.2 (1.48) 243.69 (85.24) 236.5 (70.61) 1.89 (.69) 1.80 (.82)
IH 15.3 (1.57) 15.7 (1.20) 22.4 (2.04) 22.8 (1.76) 292.32 (87.97) 313.27 (105.3) 1.4 (.72) 1.3 (.77)
20-29 years ACS 13.2 (1.4) 13.1 (.91) 21.88 (2.02) 22.4 (2.27) 163.35 (44.07) 172.89 (54.47) 1.40 (.37) 1.50 (.43)
B81 13.49 (1.83) 13.30 (.87) 22.46 (1.96) 23.84 (2.46) 167.69 (55.9) 172.07 (54.13) .96 (.43) 1.22 (.62)
IH 15.06 (2.09) 14.78 (1.91) 21.74 (3.46) 22.31 (4.15) 212.31 (77.39) 214.18 (77.58) 1.09 (.78) 1.27 (.67)
30-39 years ACS 13.23 (1.85) 13.32 (1.75) 21.97 (2.15) 21.98 (2.33) 182.24 (44.12) 210.86 (63.38) 1.13 (.44) 1.31 (.50)
B81 13.78 (1.85) 13.67 (2.08) 22.88 (2.63) 22.08 (2.49) 194.56 (57.9) 200.63 (76.04) .73 (.51) 1.08 (.62)
IH 15.71 (2.80) 15.60 (2.67) 21.97 (2.95) 21.00 (3.41) 275.53 (75.79) 279.13 (92.03) 1.01 (1.01) .91 (1.04)
40-49 years ACS 13.10 (1.46) 13.24 (1.10) 21.53 (1.87) 21.65 (2.20) 180.29 (80.91) 171.56 (50.93) .73 (.51) .68 (.32)
B81 14.74 (2.18) 12.85 (1.26) 22.46 (2.59) 21.76 (2.36) 195.75 (83.11) 168.39 (84.42) .73 (.58) .82 (.90)
IH 15.42 (1.37) 15.58 (1.07) 21.37 (2.46) 21.72 (3.28) 223.75 (77.1) 251.25 (127.08) .91 (.57) .93 (.58)
50-59 years ACS 13.69 (1.49) 13.27 (1.06) 22.44 (1.74) 22.00 (1.13) 194.68 (62.58) 182.30 (58.87) .86 (.45) .88 (1.13)
B81 14.50 (2.21) 14.24 (1.86) 23.17 (3.02) 23.13 (2.13) 184.29 (67.21) 167.9 (98.11) .57 (.28) .86 (.45)
IH 15.51 (.83) 15.54 (1.29) 21.41 (2.65) 21.97 (1.67) 257.21 (115.62) 270.39 (136.51) .63 (.35) .78 (.37)
60-69 years ACS 14.02 (1.80) 13.17 (.62) 21.62 (1.22) 21.08 (1.05) 188.48 (86.84) 187.82 (73.01) .80 (.43) .88 (.51)
B81 14.86 (2.10) 14.64 (1.32) 23.26 (1.18) 23.09 (1.59) 212.55 (112.22) 154.48 (51.96) .42 (.21) .61 (.30)
IH 16.16 (1.95) 15.63 (2.15) 22.73 (1.66) 22.24 (1.88) 254.37 (77.11) 239.32 (85.15) .87 (.45) .64 (.40)
70+ years ACS 13.54 (.66) 13.83 (1.37) 21.47 (1.04) 22.03 (2.47) 249.61 (85.32) 269.89 (113.2) .63 (.35) .55 (.19)
B81 13.55 (2.64) 14.85 (1.74) 21.47 (3.33) 22.97 (1.67) 266.95 (79.55) 123.87 (74.17) .34 (.11) .85 (.47)
IH 14.84 (1.12) 16.17 (1.21) 21.20 (1.54) 21.88 (2.27) 287.73 (96.73) 305.49 (124.95) .51 (.14) .48 (.26)
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ACS = air-conduction stimuli, IH = impulse hammer, EMG = electromyographic

Table 3.

cVEMP Response Rates for ACS, B81 and IH for each age group.

Group (age range) ACS B81 IH
1 (10-19 years) 100% 100% 100%
2 (20-29 years) 100% 100% 82%
3 (30-39 years) 100% 95% 90%
4 (40-49 years) 95% 90% 85%
5 (50-59 years) 95% 100% 75%
6 (60-69 years) 83% 88% 83%
7 (70+ years) 80% 74% 53%
All subjects 92% 92% 79%
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ACS = air-conduction stimuli, IH = Impulse Hammer

To examine the relationship between age, gender and stimulus (ACS, B81 and IH) on cVEMP corrected amplitude, a linear mixed-effects model as described above was completed. The minimal random effects structure that supported best model fit included a random intercept for participant. The minimal fixed effects structure that best supported model fit included age and stimulus, but not gender (Table 4). All interactions were excluded from the model as they did not improve model fit. As age increased, amplitude decreased (t = −7.47, p < .001, Figure 2). Specifically, for every one year increase in age, there was a 0.02 decrease in amplitude. For stimulus, corrected cVEMP amplitudes from ACS were significantly different from B81 (t = −2.06, p = .04) and IH (t = −2.41, p = .02) with ACS corrected amplitudes being on average .11 and .14 larger compared to B81 and IH, respectively. Corrected cVEMP amplitudes for B81 and IH did not differ significantly (t = −0.48, p = .63).

Table 4.

Model predicting the cVEMP amplitude

Estimate Standard error t-value Pr(>|z|)
Intercept 1.03 0.05 19.58 <.0001
Age −0.02 0.002 −7.47 <.0001
Stimulus, B81 a −0.11 0.05 −2.06 0.04
Stimulus, IH a −0.14 0.06 −2.41 0.02
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ACS = air-conduction stimuli; IH = impulse hammer

a

Reference group was ACS

Figure 2.

Figure 2.

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Mixed effects modeling revealed a significant effect of age and stimulus on cVEMP corrected amplitude. As age increased, cVEMP corrected amplitude decreased (p < .001). Air-conduction stimuli (ACS) corrected amplitudes were significantly larger than B81 (p = .04) and impulse hammer (IH) (p = .02). B81 and IH corrected amplitudes did not differ significantly (p = .63).

3.2. oVEMP

Descriptive statistics for oVEMP characteristics including n10 and p16 latencies as well as peak-to-peak amplitude can be found in Table 5. oVEMP response rates for each stimuli across the seven groups can be found in Table 6. Between groups, response rates decreased with age regardless of stimulus type. Similar to cVEMPs, the youngest group, 10-19 years, was the only group with 100% response rates for each stimuli. Overall response rates were comparable between stimuli, with the IH (93%) slightly outperforming ACS (90%) and B81 (89%). Between stimulus types, conversely to cVEMPs, IH response rates were better or equal to the response rates of both ACS and B81 for 5/7 of the groups. Response rates were comparable amongst stimuli in the younger groups with the largest disparity in response rates occurring in the oldest group (70+ years) with IH outperforming both ACS and B81. There were no participants with absent oVEMP responses across all three stimuli.There were 6 participants with absent oVEMP responses to B81 only, 5 to IH only and 1 to B81 and IH. There were 6 participants with absent responses to ACS only, indicating an added benefit of performing BCV in these participants.

Table 5.

Ocular VEMP Mean (SD) N10 and P16 latencies and N10/P16 amplitude for right and left ears across age group.

ACS N10 ACS P16 ACS Amp
Group Left Right Left Right Left Right
1 ACS 9.32 (.40) 9.07 (.47) 13.58 (.75) 13.50 (.82) 16.61 (11.83) 16.85 (12.32)
B81 9.32 (.50) 9.28 (.59) 13.82 (1.01) 13.93 (1.12) 31.58 (16.71) 22.87 (12.90)
IH 11.42 (.83) 11.44 (1.06) 16.05 (.99) 16.07 (1.66) 24.10 (17.00) 26.08 (21.66)
2 ACS 9.02 (.33) 8.95 (.26) 12.88 (1.15) 12.80 (.99) 19.14 (9.75) 22.60 (8.25)
B81 9.58 (.55) 9.26 (.36) 13.64 (1.39) 13.27 (.82) 17.69 (14.71) 19.10 (14.61)
IH 11.57 (.42) 11.47 (.65) 15.63 (.86) 15.66 (.86) 28.85 (22.37) 26.66 (16.88)
3 ACS 9.47 (.61) 9.32 (.55) 13.97 (1.47) 13.42 (1.18) 14.09 (14.58) 13.42 (1.18)
B81 9.88 (.58) 9.83 (.71) 14.50 (1.55) 14.81 (1.51) 8.08 (10.83) 13.31 (11.52)
IH 11.90 (.78) 11.87 (.61) 15.97 (1.52) 15.97 (1.34) 22.54 (24.03) 25.90 (19.19)
4 ACS 9.76 (.57) 9.65 (.51) 13.91 (1.32) 14.03 (1.30) 7.37 (3.17) 7.52 (3.20)
B81 10.09 (.95) 10.22 (.51) 13.98 (1.42) 14.65 (1.54) 5.66 (5.19) 6.69 (4.16)
IH 11.65 (1.10) 11.61 (.85) 16.28 (1.36) 15.92 (1.22) 23.05 (15.47) 23.30 (14.42)
5 ACS 9.80 (.79) 9.65 (.61) 14.3 (1.35) 14.15 (1.31) 8.78 (4.05) 10.37 (6.66)
B81 10.67 (.97) 10.69 (.79) 15.69 (.65) 14.83 (1.92) 4.51 (2.09) 4.99 (2.11)
IH 12.16 (.59) 11.92 (.67) 16.60 (.88) 16.53 (1.01) 26.36 (16.77) 33.09 (17.86)
6 ACS 9.76 (.55) 10.06 (.68) 13.55 (1.27) 13.56 (.72) 12.73 (12.40) 12.18 (11.86)
B81 10.40 (1.52) 10.38 (.77) 14.12 (2.40) 14.30 (1.37) 4.59 (2.71) 4.03 (1.74)
IH 12.20 (1.10) 12.13 (.82) 16.02 (.82) 15.85 (.49) 22.08 (11.21) 20.26 (12.63)
7 ACS 10.31 (.67) 10.55 (.61) 14.24 (.89) 14.65 (.92) 6.11 (2.87) 6.91 (3.33)
B81 11.78 (1.60) 10.72 (1.23) 15.34 (2.35) 15.67 (1.13) 4.34 (3.52) 5.51 (3.88)
IH 12.25 (.91) 12.06 (.70) 16.47 (1.45) 15.97 (1.27) 14.51 (6.43) 16.10 (7.18)
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ACS = air-conduction stimuli; IH = impulse hammer

Table 6.

oVEMP Response Rates for ACS, B81 and IH for each age group.

Group (age range) ACS B81 IH
1 (10-19 years) 100% 100% 100%
2 (20-29 years) 96% 100% 100%
3 (30-39 years) 100% 85% 100%
4 (40-49 years) 95% 100% 90%
5 (50-59 years) 95% 80% 90%
6 (60-69 years) 92% 83% 96%
7 (70+ years) 67% 80% 87%
All subjects 90% 89% 93%
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ACS = air-conduction stimuli, IH = Impulse hammer

To examine the relationship between age, gender, and stimulus (ACS, B81, and IH) on oVEMP amplitude, a linear mixed-effects model as described above, was completed. The minimal random effects structure that supported the best model fit included a random intercept for ear nested within the participant. The minimal fixed effects structure that supported the best model fit included fixed effects for age, gender, and stimulus, as well as a gender by stimulus interaction (Table 7). All other interactions were excluded from the model as they did not significantly improve model fit. For stimulus, IH oVEMP amplitudes were significantly larger than ACS (t = 2.68, p < .01) and B81 (t = 4.26, p < .001). IH amplitudes were, on average, 5.38 μv larger than ACS amplitudes and 8.68 μv larger than B81 amplitudes. No significant difference was observed between ACS and B81 (t = −1.65, p = .10).

Table 7.

Model predicting the oVEMP amplitude

Estimate Standard error t-value Pr(>|z|)
Intercept 13.19 1.52 8.68 <.0001
Age −0.22 0.03 −6.77 <.0001
Gender −0.24 2.10 −0.12 0.91
Stimulus, B81 a −3.29 1.99 −1.66 0.10
Stimulus, IH a 5.38 2.01 2.68 <.01
Gender x B81 2.46 2.73 0.90 0.37
Gender x IH 9.13 2.71 3.37 <.001
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ACS = air-conduction stimuli; IH = impulse hammer

a

Reference group was ACS

oVEMP amplitude decreased as age increased (t = −6.77, p < .001) (Figure 3). The gender by stimulus interaction revealed that the effect of gender was significantly different between IH and ACS (t = 3.37, p < .001) and IH and B81 (t = 2.45, p = .02). However, the effect of gender was not significantly different between ACS and B81 (t = −0.90, p = .36). Figure 4 illustrates the nature of gender by stimulus interaction. For IH, females demonstrated significantly larger oVEMP amplitudes than males. Age is included in Figure 4 for illustrative purposes. However, note that the age by gender by stimulus interaction was not included in the final model as its inclusion did not significantly improve model fit.

Figure 3.

Figure 3.

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Mixed effects modeling revealed a significant effect of age on oVEMP amplitude. As age increased, oVEMP amplitude decreased (p < .001). Impulse hammer (IH) oVEMP amplitudes were significantly larger than air-conduction stimuli (ACS) (p < .01) and B81 (p < .001). ACS and B81 amplitudes did not differ significantly (p = .10).

Figure 4.

Figure 4.

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Mixed effects modeling revealed a gender by stimulus interaction on oVEMP amplitude in that the effect of gender differed significantly between impulse hammer (IH) and ACS (p < .001) and B81 (p = .02). Specifically, for impulse hammer (IH), females demonstrated larger oVEMP amplitudes compared to males.

4. Discussion

BCV may produce more efficient stimulation to the otolith organs (Curthoys et al., 2006) and be less affected by age (Rosengren et al., 2011; Cheng et al., 2009; Welgampola & Colebatch, 2001), thus making it a more useful stimulus for VEMPs due to limitations with ACS VEMPs. Therefore, the purposes of this study were to examine the effect of age on c- and oVEMP responses using the B81, and to compare ACS, B81 and IH VEMP response characteristics in healthy participants. We hypothesized that BCV stimuli would be less susceptible to age as compared to ACS; thus, c- and oVEMP response rates and amplitudes would be larger for BCV stimuli (B81 and IH) compared to ACS, especially in older participants.

4.1. cVEMP

Contrary to our hypothesis, all three stimul showed decreased cVEMP response rates and corrected amplitudes with age (Figure 2). ACS corrected amplitudes were larger than B81 and IH stimuli across all age groups. Furthermore, ACS response rates were higher or similar to the B81 in almost all age groups while the IH produced the lowest response rates. Our findings suggest that any of the stimuli are appropriate for eliciting cVEMP in our youngest population (10 – 19 years). While ACS resulted in higher cVEMP corrected amplitudes overall, either ACS or B81 are appropriate stimuli for older individuals given their similar performances. We hypothesized that BCV would demonstrate less susceptibility to age; however, both B81 and IH resulted in susceptibility to age, similar to ACS.

Comparison of cVEMP responses across studies can vary due to stimulus level, type, and EMG contraction level, all of which contribute to the diversity of response rates in the literature. Rosengren et al. (2011) evaluated BCV cVEMP response rates via B71 stimulation at the mastoid, and found that 93% of normal participants aged 18-80 years elicited cVEMPs with this lower output bone osillator. The response rate was not broken down by age category; however, a significant decline in B71 cVEMP corrected amplitude with age was noted. This is consistent with our B81 findings. Our overall response rate was 92% and we demonstrated a decline in both response rates and cVEMP corrected amplitude with age. While we hypothesized that some degree of susceptibility to age would be offset by the increased output of the B81, the overall output of the B71 reported by Rosengren et al. (2011; 136 dB pFL) was similar to the overall output of the B81 (136 – 138 dB pFL). The B81 was designed to have higher output and less distortion (Freden Jansson et al., 2014); however, recent work by Clinard et al. (2019) found the maximal output at 500 Hz to be similar to the B71, which was also confirmed in this study. It has been proposed that 135 dB pFL is an effective stimulus level for the B-71 when placed at the mastoid (Rosengren et al., 2009), which was also found in our current study with the B81.

Using reflex hammer taps, Rosengren et al. (2011) reported a response rate of 98% and failed to demonstrate a significant relationship between reflex hammer tap cVEMP corrected amplitude and age. Similarly, Welgampola and Colebatch (2001) reported a response rate of 78.5%. While a weak correlation was noted between reflex hammer tap cVEMP corrected amplitude and age, there were no mean differences between age groups (Welgampola & Colebatch, 2001). This reduced susceptibility to age has been attributed to reflex hammer taps activating a different group of vestibular afferents compared to ACS (Rosengren et al., 2011), or more effectively activating a broader range of afferents (Welgampola & Colebatch, 2001; Halmagyi et al., 1995). Unexpectedly, both ACS and the B81 outperformed the IH in the current study. Ignoring age, there were 16 participants with absent cVEMP responses to IH only. The higher response rates of ACS and B81 could be due to an interaction of two factors: 1) differences in stimulus delivery, and 2) differences in electrode montage. Between B81 and IH stimulation, the B81 was delivered ipsilaterally (i.e., with right mastoid stimulation, responses were measured on the right SCM), while IH stimulation was delivered at the midline (i.e., with midline stimulation, responses were measured bilaterally). While the nearfield placement of the B81 could have overcome the difference in overall output between the two devices (B81: 136 – 138; IH: 144.8 dB pFL), this is not likely as similar findings would have been noted by Rosengren et al. (2011). However, one distinct methodological difference between the current study and both Rosengren et al. (2011) and Welgampola et al. (2001) was the placement of the reference electrode. In the current study, the reference electrode was placed on the manubrium of the sternum, while both Rosengren et al. (2011) and Welgampola et al. (2001) referenced the medial ends of the clavicle. There has been some speculation regarding whether the manubrium of the sternum is an active recording site (Li et al., 1999). When the active electrode is placed on the manubrium of the sternum an inverted response can be recorded in response to bilateral SCM activation (Li et al., 1999). It could be that the higher output stimulus (IH) resulted in a larger inverted response at the manubrium of the sternum, thus resulting in reference electrode contamination. Smith et al. (2019) found no difference in ACS cVEMP amplitudes comparing a bipoloar recording, with the reference electrode on the suprasternal notch, and a monopolar recording, using no reference electrode, suggesting the presence of an inverted response at the sternum does not significantly affect cVEMP amplitude using unilateral ACS stimulation. However, the effect of bilateral stimulation with bone conduction is unknown. The authors are unaware of BCV VEMP response comparisons with the reference electrode at the clavicle versus sternum versus no reference to determine the presence of reference electrode contamination using bilateral stimulation.

Another source of possible contamination is the presence of the crossed, contralateral response (Taylor et al., 2019; Murofushi et al., 2004; Welgampola & Colebatch 2001). In response to unilateral stimulation, a low amplitude, contralateral response of opposite polarity has been noted in 38 - 53% of normal individuals (Taylor et al., 2019; Welgampola & Colebatch, 2001; McNerney & Burkard, 2011). When completing cVEMP with bilateral stimulation, this contralateral reponse can potentially reduce the peak-to-peak amplitude (Taylor et al., 2019). In fact, Wang et al. (2003), noted a 15 – 19% reduction in cVEMP amplitudes with bilateral ACS stimulation. Therefore, it is unknown whether this contralateral response impacted BCV amplitudes in the current study, particularly when referencing on the sternum.

4.2. oVEMP

Contrary to our hypothesis, all three stimuli showed decreased oVEMP amplitudes with age, suggesting that BCV using either stimulus (B81 or IH) was still susceptible to age effects (Figure 3). However, the IH produced the largest amplitudes overall. Furthermore, while response rates were comparable amongst stimuli, both the B81 and IH had higher response rates compared to ACS for the oldest group (age 70+), consistent with our hypothesis. Similar to cVEMP corrected amplitude, any of the stimuli are appropriate for eliciting oVEMP in our younger populations (10-49 years) given comparable response rates. While the B81 had similar response rates compared to both ACS and the IH for younger participants, ACS and IH performed best for oVEMP in individuals over the age of 50, and IH is preferred for individuals over age 70.

In their control population, Rosengren et al. (2011) reported oVEMP response rates of 97% to 500 Hz tonebursts, 63% to B71 and 96% to reflex hammer taps, which are somewhat consistent with our overall response rates of 90%, 89%, and 93%, respectively. Most notably, response rates using the B81 outperformed the B71. As noted above, this difference cannot be attributed to output as Rosengren et al. (2011) reported an output of 136 dB pFL, which equals the force output of the B81. While both the B71 and B81 were placed at the mastoid, small variations in placement can result in reduced or absent responses (Rosengren et al., 2019), and placement of the bone oscillator on each mastoid can result in differences in eye movements between the eyes (Curthoys et al., 2016). Another potential source could be differences in electrode montage. Rosengren et al. (2011) used a traditional electrode montage, which has been shown to result in reference electrode contamination (Piker et al., 2011), while a modified belly tendon montage was used in the current study (Sandhu et al., 2013). However, if this were the case, we would have expected similar reductions in response rates for all stimuli, not just the B71.

One surprising finding was the gender by stimulus interaction, wherein females demonstrated larger oVEMP amplitudes than males for IH. The age by gender by stimulus interaction was excluded from the model because it did not improve model fit. However, male to female differences were most evident in the younger age groups (Figure 4) and also showed a large amount of variability in the females. To our knowledge, there has been no previous effect of gender on c- and oVEMP amplitudes in adults using the B71 (Rosengren et al., 2011) or oVEMPS amplitudes in children using the minishaker (Chou et al., 2012). However, large variability has been found with the IH in younger participants (Rodriguez et al., 2018; Greenwalt et al., in press). Thus, this gender effect may be due to a slight preponderance in females:males (44:34) and the large variability in the young female responses, despite controlling for force range (10-30 N).

Previous literature suggests that the saccule has better specificity to ACS, whereas BCV stimulates the saccule and the utricle equally (Curthoys et al., 2016; Curthoys et al., 2006). The differential effect of stimulus type on c- and oVEMP response rates and amplitudes found in the current study supports this. For cVEMPs, larger corrected amplitudes were noted for ACS; however, for oVEMPs, higher response rates and larger amplitudes were noted for IH. While BCV stimulates both the saccule and utricle, the urticulo-ocular projections are thought to be stronger with BCV compared to the sacculo-ocular projections (Uchino and Kushiro, 2011), thus BCV is speculated to be a more appropriate stimulus for oVEMPs rather than cVEMPs (Rosengren et al., 2019). Findings from the current study are consistent with this. Curthoys et al. (2011) suggested that in response to bilateral stimulation, as is the case with BCV, there is an enhancement of the vertical component eye movement, which could account for the higher oVEMP response rates and amplitudes to BCV noted in the current study.

IH out performed the B81 for oVEMPs in our study, which we attribute to increased force level, mentioned previously, as well as the stimulus location. Stimulation at the forehead produces larger oVEMP amplitudes compared to the mastoid placement (Rosengren et al., 2011; Iwasaki et al., 2008). Thus, it is not surprising that the B81 had lower response rates and amplitudes given the lower force level and not ideal location for eliciting oVEMPs.

4.3. Clinical Use of BCV VEMPs

While BCV VEMPs were still susceptible to age in the current study, BCV was comparable to ACS across the lifespan. Anectodectally, many clinicians report they do not perform VEMP testing in patients over the age of 60-65 years, due to the high likelihood of absent responses. Piker et al. (2015) reported an increased likelihood of absent responses beginning in the 4th and 5th decades of life for o- and cVEMPs, respectively. However, our results suggest that robust c- and oVEMP responses can be seen in the majority of older healthy participants using ACS or BCV stimuli and our electrode montage and stimulus parameters.

Only 3 subjects had absent ACS and present BCV cVEMPs and 6 had absent ACS and present BCV oVEMPs; therefore, results from this study do not suggest that BCV should replace ACS VEMPs at this time. However, there are some advantages of using BCV over ACS. One advantage of BCV is the reduced risk of damage from sound pressure exposure. The high intensity stimuli required for ACS VEMPs, leads to greater risk of damage in smaller ear canals, with ~3 dB higher SPL in smaller ears (≤ .8 ml; Thomas et al, 2017; Rodriguez et al, 2018). Thus, BCV could be used in lieu of ACS to avoid damage related to the loud stimuli. Second, middle ear dysfunction (e.g., otitis media) and/or middle ear surgeries, may present with a CHL and reduce or abolish the ACS VEMP response (Bath et al., 1999; Halmagyi et al., 1994). BCV bypasses the middle ear and avoids absent responses due to middle ear dysfunction. Lastly, cochlear implants may lead to mechanical changes resulting in a stiffening of the auditory system (Merchant et al., 2020). In these cochlear implant participants, BCV VEMP responses rates were higher compared to ACS VEMP response rates, suggesting that absent ACS responses were likely due to the mechanical changes rather than true vestibular loss. Thus, BCV may be a more appropriate stimuli to assess vestibular function post-cochlear implantation.

4.4. Limitations

One limitation of using the B81 is that small variations in placement can result in reduced or absent responses (Rosengren et al., 2019). The variability in the skin and underlying tissues are largest at the mastoid compared to anywhere else on the head (Studebaker, 1962). However, forehead placement is not recommended with the B71 for VEMPs due to limited force output (Iwasaki et al., 2007) . Since output of the B81 is similar to the B71, B81 output is likely not strong enough for forehead placement. Additionally, audiometric thresholds are lower when stimulation is at the mastoid process compared to the forehead (Studebaker, 1962; Weatherton & Goetzinger, 1971). While others have controlled for the exact placement on the mastoid (i.e., measuring 3 cm posteriorly from the external acoustic meatus, Welgamopola et al., 2003), we did not standardize placement. Rather we placed the B81 where it seemed most stable throughout testing, most consistent with routine clinical testing. Movement of the head (i.e., lifting for cVEMPs) and differences in mastoid anatomy occasionally made the bone oscillator move slightly. If the movement was obvious by the participant and/or the examiner, the trial was stopped, the bone oscillator was repositioned and testing was repeated; however, it should be noted that some participants had mastoids that were difficult to position the bone oscillator on without some movement throughout testing (i.e., large protruding mastoid processes), which could have influenced results. Conversely, forehead placement produces larger VEMP amplitudes compared to the mastoid placement for IH (Rosengren et al., 2011; Iwasaki et al., 2008).

A second limitation is the non-linear nature of the B81. Stimuli were initially delivered at 70 dB nHL (136 dB pFL) and increased to 75 dB nHL (138 dB pFL) for 27 participants who had absent responses at 70 dB nHL. Clinard et al. (2019) indicate the maximum output range with minimal to absent harmonic distortion is between 120-128 dB pFL suggesting the peak force levels in the current study (136-138 dB pFL) are outside the linear range, resulting in harmonic distortion. However, Clinard et al. (2019) speculate that any harmonic distortion at 500 Hz is unlikely to be influencing the VEMP response due to the low-freqency nature of VEMPs.

A third limitation of this study was our cVEMP testing position with bilateral SCM contraction (i.e., lying supine and lifting head straight up) in conditions with bilateral stimulation (i.e., B81 and IH). Bilateral stimulation is often used for IH (Rosengren et al., 2011; Nguyen et al., 2010). Therefore, we chose to maintain the same method to make direct comparisons between stimuli. However, bilateral SCM contraction could be causing a crossed vestibulo-collic pathway with the binaural stimulation, as discussed above (Taylor et al., 2019).

5. Conclusions

Age significantly affects c- and oVEMP amplitudes regardless of stimulus type. Contrary to our hypothesis, BCV did not provide any reduced susceptibility to the effect of age; however, there was a differential effect of stimulus type on c- and oVEMP response rates and amplitudes. For both c- and oVEMPs, ACS and BCV performed similarly in younger participants. However, for cVEMPs in older participants, ACS was the superior stimulus followed by B81 and then the IH. Conversely, for oVEMPs in older participants, IH was the superior stimulus, followed by B81 and then ACS. While the IH had superior response rates for oVEMPs in older adults (over the age of 50), the B81 performed better than ACS. Overall, the B81 performed well across the lifespan for c- and oVEMPs and may be a reasonable BCV option for patients with absent ACS VEMPs, but at this time is not recommended as a replacement to ACS.

Acknowledgments

Financial disclosures/conflicts of interest: Research reported in this publication was supported by the National Institute of General Medical Sciences of the National Institutes of Health under award numbers P20GM109023 and 5T32DC00013-36 and the National Institute on Deafness and Other Communication Disorders under award number R03DC015318.

Interacoustics provided Boys Town National Research Hospital with the Eclipse device on loan to collect data for this study.

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