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. 2023 Jun 15;149(8):670–680. doi: 10.1001/jamaoto.2023.1275

Association of Bilateral Vestibulopathy With and Without Hearing Loss With Cognitive-Motor Interference

Maya Danneels 1,✉, Ruth Van Hecke 1, Laura Leyssens 1, Raymond van de Berg 2,3, Ingeborg Dhooge 1,4, Dirk Cambier 1, Vincent Van Rompaey 5,6, Leen Maes 1,4
PMCID: PMC10273132  PMID: 37318799

Key Points

Question

Do people with bilateral vestibulopathy (BV) have more cognitive and motor deficits, as well as more cognitive-motor interference, than healthy control participants?

Findings

In this prospective case-control study that included 41 persons with BV, persons with an isolated BV had impaired cognitive function in several cognitive domains in a single-task condition. However, persons with BV and hearing loss were affected in even more cognitive domains in a single-task condition, and this could only be elicited in the dual-task condition in the isolated BV group.

Meaning

The results of this case-control study potentially support the deprivation (that a lack of vestibular input may be associated with accelerated brain atrophy in regions important in different cognitive processes) and attentional capacity (associated with an increased cognitive-motor interference) theories.

Abstract

Importance

The past years, evidence suggested that the primary symptoms traditionally associated with bilateral vestibulopathy (BV) do not represent the full picture of this patient population. Recent literature also demonstrated cognitive impairment. However, although multitasking and dual-tasking are widely present in everyday activities, most of these studies assessed cognitive function only in single-task conditions.

Objective

To uncover the association of BV with and without hearing loss with cognitive and motor performance and cognitive-motor interference.

Design, Setting, and Participants

This prospective case-control study assessed persons with an isolated BV and persons with BV and a concomitant hearing loss compared with a healthy control group. Data were analyzed in December 2022. The study was conducted at Ghent University (Ghent, Belgium). Data collection took place between March 26, 2021, and November 29, 2022.

Main Outcomes and Measures

All participants completed the 2BALANCE dual-task protocol, comprising a static and a dynamic motor task that was combined with 5 visual cognitive tasks. These cognitive tasks assessed mental rotation, visuospatial memory, working memory, response inhibition (executive function), and processing speed. All cognitive tasks were performed in a single-task condition (while seated) and in a dual-task condition (combined with a static and a dynamic motor task). The static task comprised balancing on a force platform with foam pad, and the dynamic task comprised walking at a self-selected speed on the GAITRite Walkway. Both motor tasks were performed in the single-task and dual-task condition.

Results

Nineteen persons with BV and hearing loss (mean [SD] age, 56.70 [10.12] years; 10 women [52.6%]), 22 persons with an isolated BV (mean [SD] age, 53.66 [13.35] years; 7 women [31.8%]), and 28 healthy control participants were included (mean [SD] age, 53.73 [12.77] years; 12 women [42.9%]). Both patient groups had mental rotation and working memory impairment in a single-task condition and slower processing speed when walking (ie, during the dynamic dual-task condition). Additionally, the patient group with hearing loss had impaired visuospatial memory and executive function deficits in single-task and dual-task conditions, while this could only be elicited when performing a motor task in persons with isolated BV (ie, when dual-tasking).

Conclusion and Relevance

The findings of this case-control study suggest an association between vestibular function and cognitive and motor performance, even greater in persons with a concomitant hearing loss than in persons with an isolated BV.

This case-control study examines the association of bilateral vestibulopathy with and without hearing loss with cognitive and motor performance and cognitive-motor interference.

Introduction

A growing body of literature suggests that impaired vestibular function is involved in far more than postural control and gaze stability.1,2 Various symptoms and complaints, including compromised cognitive function, have also been demonstrated.3 The different cognitive processes and domains that might be affected by vestibular lesions are summarized in the widely cited review by Bigelow and Agrawal.1 During the past few years, this study was endorsed by more recent findings.2,4,5,6,7,8,9,10,11 The most compelling and strongest evidence shows an association between vestibular function and visuospatial cognition, including visuospatial memory, visuospatial navigation, and mental rotation. Dysfunctions in all 3 subdomains were identified in persons with vestibular dysfunction and were associated with decreased hippocampal volume.1,5,8,9,11,12,13,14,15 This brain region is involved in spatial representations and creates cognitive maps based on place cells, border cells, grid cells, and head direction cells.14,16 These findings aligned with the deprivation theory, which states that a lack of vestibular input may be associated with accelerated brain atrophy in regions important in different cognitive processes. Similar evidence also exists for nonspatial cognition. Deficits in attention, memory, and executive function were described in persons with vestibular impairment.1,4,10,17 However, this evidence is scarce, and studies show methodological shortcomings and heterogeneous or small study samples, which consequently also result in heterogeneous findings. Research in this area is bidirectional, as not only cognitive assessment was performed in persons with vestibular dysfunction, but also vestibular function in persons with cognitive impairment. This research suggests a contribution of vestibular (dys)function in the development of dementia, including Alzheimer disease.18,19,20,21 Agrawal et al19 observed a 3-fold prevalence of vestibular dysfunction in persons with Alzheimer disease compared with healthy control (HC) participants.

Notwithstanding the evidence that strongly suggests the contribution of vestibular impairment in cognitive dysfunction, some studies proposed that the involvement of the vestibular system might be confounded by hearing loss (HL).22,23 Because of the close anatomical association between the vestibular organ and the cochlea, a high comorbidity between HL and vestibular dysfunction exists. An association between HL and cognitive function was demonstrated in numerous studies, in which impaired global cognition, processing speed, executive function, and memory were observed.24,25 These studies were mainly performed in older persons in whom HL appeared to be an independent risk factor for developing mild cognitive impairment and dementia.24,26,27,28,29 While cognitive studies in persons with vestibular deficits are increasingly accounting for hearing status, studies focusing on HL generally do not include information about vestibular function.23 However, these fields of study would benefit from a more multifactorial approach that accounts for both input systems.

It was hypothesized that assessing cognitive performance in a single-task condition (ST) while the vestibular system is not challenged would not represent everyday activities, during which multitasking often occurs.30 Keeping balance is a fairly automatic process in healthy persons. However, when faced with a vestibular disorder, a certain amount of mental capacity is required to maintain postural control and avoid falls.1,31 Given the established motor and cognitive difficulties in persons with bilateral vestibulopathy (BV), the total amount of cognitive capacity might be surpassed. As described in Kahneman’s attentional capacity theory,32 this may be associated with an increased cognitive-motor interference. This study was part of the 2BALANCE study, in which cognitive and motor performance and cognitive-motor interference were assessed in persons with BV. This article specifically focuses on persons with BV and a combined HL compared with an isolated BV.

Methods

Study Design

The protocol of this case-control study was reported in Danneels et al.30 The main objective was to assess persons with BV and HL (BV-HL) and BV and normal hearing (NH; BV-NH) compared with an HC group. Testing was performed by a certified audiologist (M.D.) and took place in the morning to limit the effect of fatigue. Different randomization sets were used to control a learning effect. This work followed the ‘Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) reporting guidelines.33 This study was approved by the ethics committee of Ghent University Hospital. Written informed consent was given prior to assessment in accordance with the Declaration of Helsinki.

Patient Data

Persons between the ages of 18 and 70 years who met the Bárány Society diagnostic criteria for BV were recruited.34 For the BV-HL group, moderate-to-profound bilateral HL was also premised. The degree of HL was based on the pure-tone average, which was measured at 1000, 2000, and 4000 Hz.35 For each person with BV, an HC participant was recruited via convenience sampling and was matched for age, sex, and education level. The absence of audiovestibular impairment was verified based on pure-tone averages and horizontal video head impulse testing (vHIT) gain values. Exclusion criteria for all groups were diagnosed neurodevelopmental and neurological deficits. A demographic questionnaire, the dizziness handicap inventory,36 the tinnitus handicap inventory,37 the activities-specific balance confidence scale,38 and the falls efficacy scale39 were administered.

2BALANCE Test Protocol

A detailed description of the 2BALANCE protocol was reported previously.30 The 2BALANCE protocol comprised 2 motor tasks and 7 cognitive tasks. As persons with HL are faced with an increased listening effort, auditory tasks were not included for this study. All instructions were given in oral and visual formats to ensure correct understanding. The participants with HL were tested while wearing their hearing devices. Testing was conducted in a well-lit and quiet room that was free of any environmental noise. All cognitive and motor tasks were performed separately, in an ST and combined in static and dynamic dual-task conditions (SDT and DDT, respectively).

Cognitive Tasks

The 5 visual cognitive tasks each assessed a different cognitive domain. Visuospatial skills were investigated using a mental rotation task (mental rotation skills) and the Corsi block task (visuospatial memory). Processing speed, working memory, and executive function (response inhibition) were investigated using the coding task, visual backward digit recall test, and visual Stroop task, respectively.

Motor Tasks

Static motor performance was observed by balancing with the feet at hip width on a force platform (Nintendo Wii Fit balance board), which was destabilized using a foam pad (AirEx Balance-Pad Solid). To collect center of pressure (CoP) data, CU BrainBLoX software was used.40 The surface of the 95% confidence ellipse (cm2), sway path length (cm), and average velocity of the CoP displacement (cm/s) were analyzed using a custom-made code in MATLAB (The MathWorks Inc). Dynamic motor performance was assessed by analyzing velocity (cm/s), step length (cm), and base of support (cm) while walking at a self-selected speed on an 8.8 m–long GAITRite Walkway (CIR System Inc). To normalize the walking pattern, all participants were asked to start 1.5 m before and stop 1.5 m after the walkway. A minimum of 5 lengths was walked during each condition.

Audiovestibular Test Protocol

Rotatory chair testing and caloric assessment by means of electronystagmography, vHIT testing, and pure-tone audiometry were part of the standard of care in the participating hospitals. At the time of participation, these data were acquired a year prior or less. Only vHIT, cervical and ocular vestibular-evoked myogenic potentials (cVEMPs and oVEMPs), and unaided pure-tone audiometry were performed at the time of participation. The vHIT was performed using the ICS Impulse system (GN Otometrics). For the assessment of the lateral and vertical semicircular canals, the velocity of the head thrusts was between 150 and 250 °/s and 120 and 250 °/s, respectively. The VEMPs were conducted using the neuro-audio software (Neurosoft). The stimulus parameters for the cVEMP and oVEMP were, respectively, air-conducted 500-Hz tone bursts, with an intensity of 95 dBnHL presented using insert earphones, and bone-conducted 500-Hz stimuli, with an intensity of a 140-dB force level presented using a minishaker at Fz position (type 4810; Brüel & Kjaer).

Statistical Analysis

Data were analyzed using the SPSS package, 28th edition (IBM). To investigate group differences for all cognitive and motor outcome measures, a generalized estimating equations model was used. Main effects and interaction effects between the groups (BV-HL, BV-NH, and HC) and conditions (ST, SDT, and DDT) were assessed. This model corrected for sex, age, education level, and randomization set. For count data, a negative binomial regression model was used. A linear model was used for the remaining continuous outcome variables. The estimated marginal means, odds ratios (ORs) and their 95% CIs, and effect sizes (Cramér V) were calculated. For the backward digit recall test, the mean, standard deviation, and effect sizes (Cohen d) were calculated using a 1-way repeated measures of analysis variance. Effect sizes with values greater than 0.1, 0.3, and 0.5 indicated a weak, medium, and large association, respectively.

Results

Demographic Data and Clinical Features

Each person with a diagnosis of BV who agreed to participate in the 2BALANCE study was assessed between March 2021 and September 2022. Nineteen persons with BV and HL (mean [SD] age, 56.70 [10.12] years) and 22 persons with BV and normal hearing (mean [SD] age, 53.66 [13.35] years) were included. Of this sample, 13 pairs were matched for age, sex, and education level. A third group of 13 HC participants was matched based on the same matching criteria. For the remaining participants with BV with (6 [27%]) and without (9 [47%]) HL, additional HC participants were recruited, amounting to a total of 28 HC participants (mean [SD] age, 53.73 [12.77] years). The control participants all had age-appropriate hearing bilaterally and lateral vHIT gain values of 0.8 and higher. The HC participants in whom VEMPs were absent were older than 65 years. Demographic data and audiovestibular data are presented in Table 1 and the eTable in Supplement 1, respectively.

Table 1. Demographic Data and Clinical Features of the Patient Groups With Bilateral Vestibulopathy and the Healthy Control Group.

Characteristic BV-HL (n = 19) BV-NH (n = 22) HC (n = 28)
Age (mean), y 56.70 (10.12) 53.66 (13.35) 53.73 (12.77)
Sex (male:female) 9:10 15:7 16:12
Hearing loss of the better ear, No. (%)
Moderate (41-55 dB HL) 2 (11) 0 0
Moderately severe (56-70 dB HL) 6 (32) 0 0
Severe (71-90 dB HL) 3 (16) 0 0
Profound (>91dB HL) 8 (42) 0 0
FIhigh, best ear unaided, mean (SD)b >84.21 (26.41) 15.30 (9.24) 10.48 (9.27)
Hearing devices, No. (%) 19 (100) 0 0
Bilateral hearing aid 8 (42) NA NA
Brainstem implant 1 (5)
Cochlear implant 5 (26)
Unilateral hearing aid 1 (5)
Unilateral hearing aid + cochlear implant 4 (21)
BMI, mean (SD) 27.95 (7.00) 25.53 (3.92) 26.93 (4.32)
Diabetes, No. (%) 2 (11) 0 1 (4)
Mean (SD) weekly physical activity, h 4.06 (3.15) 5.81 (7.46) 5.81 (10.51)
Noise exposure, No. (%) 3 (16) 6 (27) 4 (14)
Bilingualism, No. (%) 0 (0) 3 (14) 1 (4)
Tinnitus presence, No. (%) 14 (74) 10 (45) 7 (25)
Mean (SD) tinnitus handicap inventory score 26.53 (25.03) 13.24 (19.17) 1.25 (2.75)
Mean (SD) dizziness handicap inventory score 58.11 (21.19) 46.60 (23.83) 1.84 (4.43)
Mean (SD) ABC scale scorea 6.32 (2.31) 7.96 (1.78) 10.53 (0.82)
Mean (SD) falls efficacy scale score 35.05 (9.82) 28.11 (7.35) 17.42 (1.81)
BV etiologies, No. (%)
Autoimmune 0 2 (9) NA
Bilateral vestibular schwannoma 1 (5) 0
DFNA9 10 (53) 0
Idiopathic 6 (32) 18 (82)
Ototoxicity 0 1 (5)
Oxygen deprivation at birth 1 (5) 0
Post-resection astrocytoma 1 (5) 0
Suspicion of bilateral vestibular neuritis 0 1 (5)
Specifications degree of BV, No. (%)
All 3 Bárány criteria met 12 (63) 13 (59) NA
Two Bárány criteria met 6 (32) 7 (32)
One Bárány criterion met 1 (5) 2 (9)
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Abbreviations: ABC, activities-specific balance confidence; BMI, body mass index (calculated as weight in kilograms divided by height in meters squared); BV-HL, bilateral vestibulopathy and hearing loss; BV-NH, bilateral vestibulopathy and normal hearing; HC, healthy control participants; FI, Fletcher Index; NA, not applicable; VEMPs, vestibular-evoked myogenic potentials.

a

For the ABC, a higher score indicates more confidence performing daily activities. For the other questionnaires, a higher score indicates a greater association of dizziness with daily life, more difficulties of tinnitus on daily life, or less confidence to perform activities without falling.

b

For the FI in the BV-HL group, thresholds of >120 dB HL were analyzed as 120 dB HL.

Cognitive Tasks

Descriptive data and each cognitive test are reported in Table 2. Error bars are reported in Figure 1.

Table 2. Descriptive Data for the Cognitive Tasks.

Task ST SDT DDT
Mental rotation task, percentage of incorrect responses, estimated marginal means (95% CI)
BV-HL 7.60 (4.28-13.51) 6.02 (3.61-10.02) 6.86 (4.34-10.86)
BV-NH 5.25 (3.30-8.35) 4.94 (2.99-8.17) 8.16 (4.91-13.57)
HC 1.90 (1.03-3.49) 5.00 (3.13-7.99) 3.54 (2.02-6.20)
Effect size, BV-HL and HCa .48 .08 .26
Effect size, BV-NH and HC .39 .01 .35
Effect size, BV-HL and BV-NH .16 0.09 0.08
Mental rotation task, response time, s, estimated marginal means (95% CI)
BV-HL 2.26 (1.65-2.87) 2.40 (1.37-3.42) 2.07 (1.35-2.79)
BV-NH 2.71 (2.15-3.27) 2.67 (2.10-3.23) 2.50 (1.94-3.06)
HC 2.25 (1.80-2.70) 2.25 (1.68-2.83) 1.98 (1.51-2.45)
Effect size, BV-HL and HC .01 .04 .03
Effect size, BV-NH and HC .18 .14 .20
Effect size, BV-HL and BV-NH .18 .07 .15
Corsi block, percentage of incorrect responses, estimated marginal means (95% CI)
BV-HL 27.35 (19.07-39.22) 23.86 (15.09-37.73) 30.00 (21.28-42.31)
BV-NH 17.57 (11.18-27.63) 18.58 (11.98-28.81) 25.92 (17.32-38.79)
HC 17.48 (12.33-24.77) 11.81 (8.22-16.97) 20.59 (15.02-28.22)
Effect size, BV-HL and HC .30 .38 .30
Effect size, BV-NH and HC .01 .30 .19
Effect size, BV-HL and BV-NH .27 .14 .10
Coding task, responses per minute, estimated marginal means (95% CI)
BV-HL 39.15 (36.28-42.03) 37.47 (33.70-41.24) 33.25 (30.61-35.90)
BV-NH 38.37 (35.69-41.05) 37.31 (34.84-39.77) 33.87 (31.10-36.64)
HC 41.00 (39.09-42.92) 39.71 (37.54-41.89) 37.20 (35.52-38.88)
Effect size, BV-HL and HC .16 .15 .38
Effect size, BV-NH and HC .24 .22 .30
Effect size, BV-HL and BV-NH .06 .01 .05
Visual Stroop task, response time, s, estimated marginal means (95% CI)
BV-HL 0.87 (0.81-0.94) 0.93 (0.84-1.02) 0.89 (0.80-0.98)
BV-NH 0.84 (0.77-0.92) 0.84 (0.76-0.92) 0.83 (0.75-0.90)
HC 0.79 (0.73-0.86) 0.82 (0.76-0.89) 0.75 (0.69-0.82)
Effect size, BV-HL and HC .33 .37 .45
Effect size, BV-NH and HC .19 .06 .30
Effect size, BV-HL and BV-NH .10 .29 .20
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Abbreviations: BV-HL, bilateral vestibulopathy and hearing loss; BV-NH, bilateral vestibulopathy and normal hearing; DDT, dynamic dual task; HC, healthy control participants; ST, single task; SDT, static dual task.

a

All effect sizes are presented using Cramér V.

Figure 1. Measurements of Participant Cognitive Data.

Figure 1.

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These data are presented for the single-task (ST), static dual-task (SDT), and dynamic dual-task (DDT) conditions. The error bars signify the 95% CIs of the estimated marginal means. BV indicates bilateral vestibulopathy; HC, healthy control; HL, hearing loss; NH, normal hearing.

Mental Rotation Task

The BV-HL and BV-NH groups made more mistakes on the mental rotation task than the HC group in single-task condition, with estimated mean mistakes rates 4.01 and 2.77 times higher than the HC group, respectively (95% CI, 1.76-9.15; Cramér V, 0.48; 95% CI, 1.33-5.74; Cramér V, 0.39, respectively). Additionally, the mistake rate of the BV-NH group was 2.31 times higher in the DDT condition compared with the HC group (95% CI, 1.20-4.44; Cramér V,0.35). When performing the static motor task, the mistake rate increased in the HC group, while a decrease was observed in both patient groups (interaction: BV-HL and HC, Cramér V, 0.38; BV-NH and HC, Cramér V, 0.36). By contrast, when performing the dynamic motor task, the mistake rate decreased in the HC group but increased in the BV-NH group (Cramér V, 0.30). Differences in reaction times between groups were not clinically meaningful.

Corsi Block Test

The BV-HL group had the overall lowest visuospatial memory scores. Their mistake rates were 1.57, 2.02, and 1.46 times higher than the HC group in the ST, SDT, and DDT conditions, respectively (ST: 95% CI, 1.02-2.41; Cramér V, 0.30, SDT: 95% CI, 1.19-3.44; Cramér V, 0.38; and DDT: 95% CI, 1.01-2.10; Cramér V, 0.30). For the BV-NH group, the difference in mistake rates was only clinically meaningful in the SDT condition, with an estimated mean mistake rate 1.57 times higher compared with the HC group (95% CI, 1.04-2.39; Cramér V, 0.30). A medium interaction effect was observed between the BV-NH and HC group, as the former showed an increase of 0.49% between the ST and SDT conditions, while the latter showed a decrease of 5.67% between these conditions (Cramér V, 0.37).

Coding Task

The number of responses per minute were 1.12 and 1.10 times higher in the control group compared with the BV-HL and BV-NH groups in the DDT condition, respectively (BV-HL: Cramér V, 0.38; BV-NH: Cramér V, 0.30). No interaction effects nor any clinically meaningful differences between both patient groups were observed.

Visual Stroop Task

The reaction times of the BV-HL group were 1.08, 1.12, and 1.15 times longer compared with the HC group for the ST, SDT, and DDT conditions, respectively (ST: 95% CI, 1.00-1.16; Cramér V, 0.33; SDT: 95% CI, 1.03-1.21; Cramér V, 0.37; and DDT: 95% CI, 1.05-1.25; Cramér V, 0.45). For the BV-NH subgroup, this was only the case while walking (Cramér V, 0.30). No interaction effects were observed.

Visual Backward Digit Recall Test

Before performing the 2BALANCE protocol, a baseline measurement was performed for the backward digit recall test. The maximum number of correctly responded items while seated was noted and used during the dual-task conditions. Because of this difference in baseline score, group comparison for the dual-task conditions was not possible. The mean (SD) number of correctly repeated digits was 4.37 (1.01), 4.45 (1.22), and 5.36 (1.03) for the BV-HL, BV-NH, and HC groups, respectively. The differences between both patient groups and the HC group were large (BV-HL: Cohen d, 0.97; BV-NH: Cohen d, 0.81). No interaction effects were observed.

Motor Tasks

Descriptive data for the motor tasks are presented in Table 3. Error bars are presented in Figure 2.

Table 3. Descriptive Data for the Static and Dynamic Postural Tasks.

Task ST SDT-MR SDT-CB SDT-Coding SDT-vSTR SDT-vBDRT
Static postural task
Surface, cm2, estimated marginal means (95% CI)
BV-HL 21.03 (10.89-31.16) 21.00 (10.68-31.33) 25.37 (9.24-41.50) 20.60 (8.08-33.13) 30.65 (14.04-47.26) 25.37 (15.19-35.56)
BV-NH 18.28 (12.37-24.18) 13.91 (8.81-19.02) 13.55 (6.95-20.14) 13.83 (7.90-19.76) 12.11 (7.14-17.07) 16.43 (11.73-21.14)
HC 9.28 (5.57-12.99) 7.83 (3.78-11.88) 7.42 (3.21-11.64) 10.03 (5.37-14.68) 6.78 (2.63-10.92) 10.90 (6.48-15.32)
Effect size, BV-HL and HCa .31 .34 .24 .22 .40 .37
Effect size, BV-NH and HC .37 .27 .29 .14 .25 .24
Effect size, BV-HL and BV-NH .07 .18 .20 .14 .32 .24
Path length, cm, estimated marginal means (95% CI)
BV-HL 135.53 (110.58-160.48) 136.74 (116.36-157.13) 143.00 (117.53-168.47) 142.96 (122.55-163.36) 160.19 (134.44-185.95) 142.57 (121.25-163.90)
BV-NH 141.05 (115.25-166.85) 127.20 (107.57-146.83) 138.05 (118.76-157.34) 135.62 (118.36-152.89) 136.38 (117.81-154.95) 153.77 (135.25-172.29)
HC 83.29 (75.91-90.67) 83.76 (74.90-92.62) 83.21 (75.23-91.20) 98.66 (85.20-112.11) 86.13 (75.68-96.57) 96.28 (81.48-111.07)
Effect size, BV-HL and HC .60 .69 .64 .52 .76 .51
Effect size, BV-NH and HC .60 .56 .74 .47 .67 .68
Effect size, BV-HL and BV-NH .05 .10 .05 .08 .23 .12
Velocity, cm/s, estimated marginal means (95% CI)
BV-HL 4.48 (3.62-5.35) 4.53 (3.81-5.26) 4.74 (3.87-5.62) 4.73 (4.05-5.42) 5.31 (4.43-6.19) 4.72 (4.00-5.43)
BV-NH 4.64 (3.81-5.47) 4.16 (3.53-4.79) 4.54 (3.91-5.17) 4.46 (3.88-5.03) 4.48 (3.88-5.09) 5.06 (4.49-5.64)
HC 2.75 (2.50-3.00) 2.77 (2.46-3.08) 2.77 (2.48-3.04) 3.03 (2.70-3.36) 2.85 (2.49-3.20) 3.19 (2.71-3.66)
Effect size, BV-HL and HC .55 .64 .63 .64 .75 .51
Effect size, BV-NH and HC .61 .55 .73 .63 .65 .70
Effect size, BV-HL and BV-NH .04 .12 .06 .09 .24 .12
Dynamic postural task
Velocity, cm/s, estimated marginal means (95% CI)
BV-HL 105.86 (97.81-113.90) 89.02 (78.41-99.63) 92.67 (83.57-101.77) 93.86 (84.20-103.52) 97.45 (88.49-106.42) 95.93 (86.94-104.93)
BV-NH 113.57 (106.42-120.72) 94.61 (86.86-102.37) 93.78 (86.68-100.88) 97.25 (89.79-104.72) 102.91 (95.64-110.18) 99.47 (91.97-106.97)
HC 114.25 (107.61-120.89) 96.77 (89.93-103.62) 98.00 (91.05-104.95) 101.74 (94.49-102.40) 102.40 (95.64-109.16) 102.23 (95.46-109.00)
Effect size, BV-HL and HC .27 .21 .17 .24 .16 .20
Effect size, BV-NH and HC .24 .07 .15 .16 .02 .10
Effect size, BV-HL and BV-NH .26 .16 .04 .11 .18 .12
Step length, cm, estimated marginal means (95% CI)
BV-HL 56.89 (53.76-60.02) 50.57 (46.38-54.76) 52.34 (48.71-55.97) 52.48 (48.86-56.09) 53.77 (50.11-57.44) 54.21 (50.42-57.99)
BV-NH 61.05 (58.64-63.46) 54.36 (51.61-57.12) 53.53 (50.16-56.89) 54.58 (51.53-57.63) 57.55 (54.91-60.20) 56.50 (53.61-59.39)
HC 62.93 (60.38-65.48) 56.29 (53.83-58.76) 57.10 (54.58-59.62) 58.23 (55.44-61.01) 58.76 (56.17-61.35) 58.78 (56.10-61.45)
Effect size, BV-HL and HC .45 .37 .34 .41 .34 .31
Effect size, BV-NH and HC .19 .18 .28 .29 .11 .20
Effect size, BV-HL and BV-NH .32 .24 .08 .14 .26 .15
Base of support, cm, estimated marginal means (95% CI)
BV-HL 13.34 (10.97-15.72) 14.60 (12.16-17.03) 14.02 (11.63-16.41) 13.64 (11.26-16.02) 13.17 (10.72-15.61) 14.04 (11.64-16.45)
BV-NH 10.81 (8.52-13.10) 12.53 (9.11-15.96) 12.57 (9.06-16.07) 12.31 (8.50-16.11) 10.92 (8.66-13.18) 12.46 (9.01-15.90)
HC 9.52 (7.58-11.47) 9.45 (7.47-11.44) 9.76 (7.76-11.76) 9.43 (7.44-11.41) 9.46 (7.49-11.42) 9.51 (7.52-11.50)
Effect size, BV-HL and HC .34 .42 .36 .36 .32 .40
Effect size, BV-NH and HC .19 .23 .20 .19 .21 .21
Effect size, BV-HL and BV-NH .26 .21 .15 .14 .24 .18
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Abbreviations: BV-HL, bilateral vestibulopathy and hearing loss; BV-NH, bilateral vestibulopathy and normal hearing; CB, Corsi block; DDT, dynamic dual-task; HC, healthy control participants; MR, mental rotation; SDT, static dual-task; ST, single-task; vBDRT, visual backward digit recall test; vSTR, visual Stroop task.

a

All effect sizes are presented using Cramér V.

Figure 2. Measurements of Participants’ Performance of Static Motor and Dynamic Motor Tasks.

Figure 2.

Open in a new tab

These data are presented for the single-task (ST), mental rotation task (MR), Corsi block (CB), coding task, visual Stroop task (vSTR), and the visual backward digit recall test (vBDRT). The error bars signify the 95% CIs of the estimated marginal means. BV indicates bilateral vestibulopathy; HC, healthy control; HL, hearing loss; NH, normal hearing.

Static Motor Performance

The difference of the CoP between the patient groups and the control group was clinically meaningful for path length and velocity. The magnitude of this association was moderate to large (Cramér V, 0.47-0.76). For the parameter surface, this was only the case for the BV-HL group in the ST and SDT conditions while performing the mental rotation task, visual Stroop task, and visual backward digit recall test (Cramér V, 0.31-0.40). No clinically meaningful interaction effects between the ST and any DT condition were observed.

Dynamic Motor Performance

Only the BV-HL subgroup had a different walking pattern from the HC group. This was translated as a smaller step length and wider base of support during all conditions. The magnitude of this association was moderate (Cramér V, 0.31-0.45). This association was not observed between the BV-NH and HC groups. Interaction effects were observed. First, step length decreased by 12.32% in the BV-NH group, while a decrease of only 8% was observed in the BV-HL group between ST and the Corsi block DT condition (Cramér V, 0.34). Second, the base of support increased by 9.4% in the BV-HL group, while a decrease of 0.7% was observed in the HC group between ST and mental rotation DT condition (Cramér V, 0.30).

Discussion

This case-control study aimed to assess the association of BV and HL with cognitive and motor function and cognitive-motor interference. A second patient group of persons with BV and NH was also included to enable differentiation between isolated BV and combined BV with HL.

Mental rotation, visuospatial memory, working memory, response inhibition, and processing speed were affected in patients with BV with and without HL. However, the observed cognitive differences between the patient and control groups could not be generalized across patient groups, as dysfunction in several of these cognitive domains could only be elicited in the NH subgroup when dual-tasking. Both patient groups had a longer path length and a higher velocity than the HC group while balancing on the force platform. The difference in surface of the CoP between the patient and control groups was only clinically meaningful in most conditions in the BV-HL subgroup. Only the subgroup with HL had a significantly smaller step length and a wider base of support while walking compared with the HC group.

Kahneman’s attentional capacity theory proposes that each individual has a limited amount of cognitive resources.32 When dual-tasking, the performance of 1 or both tasks will decrease if the available amount of cognitive capacity is surpassed. Consequently, in persons with BV and NH, postural and cognitive deficits might be associated with an increased cognitive-motor interference. In the case of a concomitant HL, the cognitive burden and cognitive-motor interference might even further increase. The results of the current study suggest that, for several cognitive tasks, a combined BV and HL elicits impairment in an ST condition, while in persons with an isolated BV, impairment will only arise when adding a motor task. This statement was true for the Corsi block and visual Stroop tasks. The lower scores in persons with HL compared with an isolated BV could be caused by the established association between HL and cognitive impairment and might be associated with an additional cognitive burden.25 Popp et al10 reported impaired visual Stroop performance in persons with BV. However, they did not provide information on participants’ hearing status. Ahmad et al5 only assessed persons with BV and NH and did not observe any impairment during the visual Stroop task. Another possible explanation for the difference in cognitive function between both groups might be found in the degree of BV. Sixty-three percent of participants with HL, compared with 59% of participants with NH, met all 3 diagnostic criteria, indicating a similar vestibulo-ocular reflex function between both groups.34 However, although not used to define the diagnosis of BV, the importance of the otolith organs in cognitive function should not be overlooked.11 In the BV-HL group, 79% had bilaterally absent cVEMPS and oVEMPs, while in the BV-NH group, this was only 27%. Several studies have provided evidence that a loss of otolith function may be association with spatial memory impairment. The otolith organs sense linear acceleration with respect to gravity and provide a gravitational frame of reference.11,41 Harun et al42 found a 3-fold odds of Alzheimer disease in persons with bilaterally absent cVEMPs. No difference in vestibulo-ocular reflex gain between the group with cognitive impairment and the HC group was observed, emphasizing the importance of the otolith organs.

Both patient groups had lower scores for the coding task in the DDT condition and the baseline backward digit recall measurement. Similar to the current study, Popp et al10 could not identify poorer processing speed in the BV population in the ST condition. However, using the 2BALANCE protocol, difficulties in this cognitive subdomain were elicited while dual-tasking. Ahmad et al5 assessed auditory working memory and could not find any differences between participants with BV and HC participants. For the mental rotation task, both patient groups had significantly lower scores in the ST setting compared with healthy participants. The subgroup of patients with NH also had poorer mental rotation skills than the HC group while walking (ie, DDT). Hearing loss did not appear to be a contributing factor to mental rotation difficulties. These findings aligned with Grabherr et al,12 in which higher error rates were observed in the BV group compared with the HC group. In contrast to the current study, that study’s BV population also had significantly slower response times.

Although no difference in gait speed could be observed, the smaller step length and wider base of support in the HL compared with the HC group was noteworthy. An association between sensorineural hearing loss and gait alterations has previously been reported.43,44 This might be explained by the lack of stationary auditory cues. These cues can be used as a reference to compare our position in space, which is important in maintaining postural balance.45,46,47,48 However, these studies did not include any vestibular assessment. Given the high comorbidity between HL and vestibular dysfunction, the independent causal factor for the gait alterations cannot be identified. Nonetheless, because of a lack of vestibular information, persons with BV are known to rely more on other input systems, such as vision, proprioception, and even hearing. When one of these input systems is affected, postural imbalance will increase.3 Consequently, auditory cues might be used as an important point of reference to remain balanced in persons with BV. The difference in gait pattern between both patient groups aligns with the activities-specific balance confidence scale and falls efficacy scale, for which scores indicating a lower confidence not to fall were observed in the HL group compared with the NH subgroup (Table 1). Analogous to the cognitive test results, the motor performance might also be associated with the degree of BV, as loss of otolith function has been associated with an increased postural sway and a higher fall risk.49,50

Not only the degree, but also the etiology of BV might be associated with cognitive and motor performance differently. Most of the patient group with HL comprised persons with a heterozygous dominant-negative COCH gene variant, causing DFNA9 (53%).51,52 This disorder has a progressive sensorineural HL and vestibular dysfunction that eventually evolves toward BV.53,54,55,56,57 Eighty-three percent of the participants with BV with NH had an idiopathic BV, often with a sudden onset. The progressive vs sudden disease onset might lead to different coping strategies to remain balanced.

Limitations and Future Perspectives

This study had several limitations. First, a group of participants with an isolated HL and normal vestibular function would enable defining the contribution of both input systems separately. Second, a sample size of 22 persons per group was defined based on the dual-task study by Bessot et al,58 while the current BV-HL group comprised 19 participants. However, with a total of 41 included patients, this study sample still surpassed the dual-task studies already reported in BV. Third, the BV-HL group wore hearing devices that (partially) compensated the HL. However, only visual cognitive tests were included.

Conclusions

The results of this case-control study suggest that persons with BV have cognitive and motor impairment. These data support the deprivation and attentional capacity theories. Persons with an isolated BV have impaired mental rotation and working memory skills in an ST condition, while visuospatial memory, processing speed, and response inhibition impairment solely arose while dual-tasking. Persons with a combined BV and HL also have poorer visuospatial memory and response inhibition skills in an ST condition. Finally, gait differences were observed between both patient groups, possibly associated with a lack of auditory cues to position oneself in space. However, the differences in the degree and etiology of BV between patient groups could also have been associated with cognitive and motor performance.

Supplement 1.

eTable. Audiovestibular data

Click here for additional data file. (269.4KB, pdf)
Supplement 2.

Data sharing statement

Click here for additional data file. (15.5KB, pdf)

References

  • 1.Bigelow RT, Agrawal Y. Vestibular involvement in cognition: visuospatial ability, attention, executive function, and memory. J Vestib Res. 2015;25(2):73-89. doi: 10.3233/VES-150544 [DOI] [PubMed] [Google Scholar]
  • 2.Dobbels B, Peetermans O, Boon B, Mertens G, Van de Heyning P, Van Rompaey V. Impact of bilateral vestibulopathy on spatial and nonspatial cognition: a systematic review. Ear Hear. 2019;40(4):757-765. doi: 10.1097/AUD.0000000000000679 [DOI] [PubMed] [Google Scholar]
  • 3.Lucieer FMP, Van Hecke R, van Stiphout L, et al. Bilateral vestibulopathy: beyond imbalance and oscillopsia. J Neurol. 2020;267(1)(suppl 1):241-255. doi: 10.1007/s00415-020-10243-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Bosmans J, Gommeren H, Mertens G, et al. Associations of bilateral vestibulopathy with cognition in older adults matched with healthy controls for hearing status. JAMA Otolaryngol Head Neck Surg. 2022;148(8):731-739. doi: 10.1001/jamaoto.2022.1303 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Ahmad M, Bola L, Boutabla A, King S, Lewis RF, Chari DA. Visuospatial cognitive dysfunction in patients with vestibular loss. Otol Neurotol. 2022;43(10):e1140-e1147. doi: 10.1097/MAO.0000000000003696 [DOI] [PubMed] [Google Scholar]
  • 6.Zhang X, Huang Y, Xia Y, et al. Vestibular dysfunction is an important contributor to the aging of visuospatial ability in older adults—data from a computerized test system. Front Neurol. 2022;13:1049806. doi: 10.3389/fneur.2022.1049806 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Bosmans J, Jorissen C, Gilles A, et al. Vestibular function in older adults with cognitive impairment: a systematic review. Ear Hear. 2021;42(5):1119-1126. doi: 10.1097/AUD.0000000000001040 [DOI] [PubMed] [Google Scholar]
  • 8.Guidetti G, Guidetti R, Manfredi M, Manfredi M. Vestibular pathology and spatial working memory. Acta Otorhinolaryngol Ital. 2020;40(1):72-78. doi: 10.14639/0392-100X-2189 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Kremmyda O, Hüfner K, Flanagin VL, et al. Beyond dizziness: virtual navigation, spatial anxiety and hippocampal volume in bilateral vestibulopathy. Front Hum Neurosci. 2016;10:139. doi: 10.3389/fnhum.2016.00139 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Popp P, Wulff M, Finke K, Rühl M, Brandt T, Dieterich M. Cognitive deficits in patients with a chronic vestibular failure. J Neurol. 2017;264(3):554-563. doi: 10.1007/s00415-016-8386-7 [DOI] [PubMed] [Google Scholar]
  • 11.Smith PF. The growing evidence for the importance of the otoliths in spatial memory. Front Neural Circuits. 2019;13:66. doi: 10.3389/fncir.2019.00066 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Grabherr L, Cuffel C, Guyot JP, Mast FW. Mental transformation abilities in patients with unilateral and bilateral vestibular loss. Exp Brain Res. 2011;209(2):205-214. doi: 10.1007/s00221-011-2535-0 [DOI] [PubMed] [Google Scholar]
  • 13.Dobbels B, Mertens G, Gilles A, et al. The virtual Morris water task in 64 patients with bilateral vestibulopathy and the impact of hearing status. Front Neurol. 2020;11:710. doi: 10.3389/fneur.2020.00710 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Brandt T, Schautzer F, Hamilton DA, et al. Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. Brain. 2005;128(Pt 11):2732-2741. doi: 10.1093/brain/awh617 [DOI] [PubMed] [Google Scholar]
  • 15.Candidi M, Micarelli A, Viziano A, Aglioti SM, Minio-Paluello I, Alessandrini M. Impaired mental rotation in benign paroxysmal positional vertigo and acute vestibular neuritis. Front Hum Neurosci. 2013;7:783. doi: 10.3389/fnhum.2013.00783 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Hitier M, Besnard S, Smith PF. Vestibular pathways involved in cognition. Front Integr Neurosci. 2014;8:59. doi: 10.3389/fnint.2014.00059 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Smith L, Wilkinson D, Bodani M, Bicknell R, Surenthiran SS. Short-term memory impairment in vestibular patients can arise independently of psychiatric impairment, fatigue, and sleeplessness. J Neuropsychol. 2019;13(3):417-431. doi: 10.1111/jnp.12157 [DOI] [PubMed] [Google Scholar]
  • 18.Previc FH. Vestibular loss as a contributor to Alzheimer’s disease. Med Hypotheses. 2013;80(4):360-367. doi: 10.1016/j.mehy.2012.12.023 [DOI] [PubMed] [Google Scholar]
  • 19.Agrawal Y, Smith PF, Rosenberg PB. Vestibular impairment, cognitive decline and Alzheimer’s disease: balancing the evidence. Aging Ment Health. 2020;24(5):705-708. doi: 10.1080/13607863.2019.1566813 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Wei EX, Oh ES, Harun A, et al. Increased prevalence of vestibular loss in mild cognitive impairment and Alzheimer’s disease. Curr Alzheimer Res. 2019;16(12):1143-1150. doi: 10.2174/1567205016666190816114838 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Wei EX, Oh ES, Harun A, Ehrenburg M, Agrawal Y. Vestibular loss predicts poorer spatial cognition in patients with Alzheimer’s disease. J Alzheimers Dis. 2018;61(3):995-1003. doi: 10.3233/JAD-170751 [DOI] [PubMed] [Google Scholar]
  • 22.Dobbels B, Mertens G, Gilles A, et al. Cognitive function in acquired bilateral vestibulopathy: a cross-sectional study on cognition, hearing, and vestibular loss. Front Neurosci. 2019;13:340. doi: 10.3389/fnins.2019.00340 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Smith PF. Hearing loss versus vestibular loss as contributors to cognitive dysfunction. J Neurol. 2022;269(1):87-99. doi: 10.1007/s00415-020-10343-2 [DOI] [PubMed] [Google Scholar]
  • 24.Lin FR, Yaffe K, Xia J, et al. ; Health ABC Study Group . Hearing loss and cognitive decline in older adults. JAMA Intern Med. 2013;173(4):293-299. doi: 10.1001/jamainternmed.2013.1868 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Claes AJ, Van de Heyning P, Gilles A, Hofkens-Van den Brandt A, Van Rompaey V, Mertens G. Impaired cognitive functioning in cochlear implant recipients over the age of 55 years: a cross-sectional study using the Repeatable Battery for the Assessment of Neuropsychological Status for Hearing-Impaired Individuals (RBANS-H). Front Neurosci. 2018;12:580. doi: 10.3389/fnins.2018.00580 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Gurgel RK, Ward PD, Schwartz S, Norton MC, Foster NL, Tschanz JT. Relationship of hearing loss and dementia: a prospective, population-based study. Otol Neurotol. 2014;35(5):775-781. doi: 10.1097/MAO.0000000000000313 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Michalowsky B, Hoffmann W, Kostev K. Association between hearing and vision impairment and risk of dementia: results of a case-control study based on secondary data. Front Aging Neurosci. 2019;11:363. doi: 10.3389/fnagi.2019.00363 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Golub JS, Brickman AM, Ciarleglio AJ, Schupf N, Luchsinger JA. Association of subclinical hearing loss with cognitive performance. JAMA Otolaryngol Head Neck Surg. 2020;146(1):57-67. doi: 10.1001/jamaoto.2019.3375 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Liu CM, Lee CT. Association of hearing loss with dementia. JAMA Netw Open. 2019;2(7):e198112. doi: 10.1001/jamanetworkopen.2019.8112 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Danneels M, Van Hecke R, Leyssens L, et al. 2BALANCE: a cognitive-motor dual-task protocol for individuals with vestibular dysfunction. BMJ Open. 2020;10(7):e037138. doi: 10.1136/bmjopen-2020-037138 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Lajoie Y, Teasdale N, Bard C, Fleury M. Attentional demands for static and dynamic equilibrium. Exp Brain Res. 1993;97(1):139-144. doi: 10.1007/BF00228824 [DOI] [PubMed] [Google Scholar]
  • 32.Kahneman D. Attention and Effort. Citeseer; 1973. [Google Scholar]
  • 33.Cuschieri S. The STROBE guidelines. Saudi J Anaesth. 2019;13(suppl 1):S31-S34. doi: 10.4103/sja.SJA_543_18 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Strupp M, Kim JS, Murofushi T, et al. Bilateral vestibulopathy: diagnostic criteria consensus document of the classification committee of the Bárány Society. J Vestib Res. 2017;27(4):177-189. doi: 10.3233/VES-170619 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Clark JG. Uses and abuses of hearing loss classification. ASHA. 1981;23(7):493-500. [PubMed] [Google Scholar]
  • 36.Jacobson GP, Newman CW. The development of the Dizziness Handicap Inventory. Arch Otolaryngol Head Neck Surg. 1990;116(4):424-427. doi: 10.1001/archotol.1990.01870040046011 [DOI] [PubMed] [Google Scholar]
  • 37.Newman CW, Jacobson GP, Spitzer JB. Development of the Tinnitus Handicap Inventory. Arch Otolaryngol Head Neck Surg. 1996;122(2):143-148. doi: 10.1001/archotol.1996.01890140029007 [DOI] [PubMed] [Google Scholar]
  • 38.Powell LE, Myers AM. The Activities-Specific Balance Confidence (ABC) scale. J Gerontol A Biol Sci Med Sci. 1995;50A(1):M28-M34. doi: 10.1093/gerona/50A.1.M28 [DOI] [PubMed] [Google Scholar]
  • 39.Tinetti ME, Richman D, Powell L. Falls efficacy as a measure of fear of falling. J Gerontol. 1990;45(6):239-243. doi: 10.1093/geronj/45.6.P239 [DOI] [PubMed] [Google Scholar]
  • 40.Cooper J, Siegfried K, Ahmed A. BrainBLoX: brain and biomechanics lab in a box software (version 1.0). Accessed May 10, 2023. http://www.colorado.edu/neuromechanics/research/wii-balance-board-project
  • 41.Andreescu CE, De Ruiter MM, De Zeeuw CI, De Jeu MT. Otolith deprivation induces optokinetic compensation. J Neurophysiol. 2005;94(5):3487-3496. doi: 10.1152/jn.00147.2005 [DOI] [PubMed] [Google Scholar]
  • 42.Harun A, Oh ES, Bigelow RT, Studenski S, Agrawal Y. Vestibular impairment in dementia. Otol Neurotol. 2016;37(8):1137-1142. doi: 10.1097/MAO.0000000000001157 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Sakurai R, Suzuki H, Ogawa S, Takahashi M, Fujiwara Y. Hearing loss and increased gait variability among older adults. Gait Posture. 2021;87:54-58. doi: 10.1016/j.gaitpost.2021.04.007 [DOI] [PubMed] [Google Scholar]
  • 44.Li L, Simonsick EM, Ferrucci L, Lin FR. Hearing loss and gait speed among older adults in the United States. Gait Posture. 2013;38(1):25-29. doi: 10.1016/j.gaitpost.2012.10.006 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45.Campos J, Ramkhalawansingh R, Pichora-Fuller MK. Hearing, self-motion perception, mobility, and aging. Hear Res. 2018;369:42-55. doi: 10.1016/j.heares.2018.03.025 [DOI] [PubMed] [Google Scholar]
  • 46.Zhong X, Yost WA. Relationship between postural stability and spatial hearing. J Am Acad Audiol. 2013;24(9):782-788. doi: 10.3766/jaaa.24.9.3 [DOI] [PubMed] [Google Scholar]
  • 47.Easton RD, Greene AJ, DiZio P, Lackner JR. Auditory cues for orientation and postural control in sighted and congenitally blind people. Exp Brain Res. 1998;118(4):541-550. doi: 10.1007/s002210050310 [DOI] [PubMed] [Google Scholar]
  • 48.Carpenter MG, Campos JL. The effects of hearing loss on balance: a critical review. Ear Hear. 2020;41(suppl 1):107S-119S. doi: 10.1097/AUD.0000000000000929 [DOI] [PubMed] [Google Scholar]
  • 49.Serrador JM, Lipsitz LA, Gopalakrishnan GS, Black FO, Wood SJ. Loss of otolith function with age is associated with increased postural sway measures. Neurosci Lett. 2009;465(1):10-15. doi: 10.1016/j.neulet.2009.08.057 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50.Basta D, Todt I, Scherer H, Clarke A, Ernst A. Postural control in otolith disorders. Hum Mov Sci. 2005;24(2):268-279. doi: 10.1016/j.humov.2005.04.002 [DOI] [PubMed] [Google Scholar]
  • 51.Verdoodt D, Van Camp G, Ponsaerts P, Van Rompaey V. On the pathophysiology of DFNA9: effect of pathogenic variants in the COCH gene on inner ear functioning in human and transgenic mice. Hear Res. 2021;401:108162. doi: 10.1016/j.heares.2020.108162 [DOI] [PubMed] [Google Scholar]
  • 52.JanssensdeVarebeke SPF, Moyaert J, Fransen E, et al. Genotype-phenotype correlation study in a large series of patients carrying the p.Pro51Ser (p.P51S) variant in COCH (DFNA9) part II: a prospective cross-sectional study of the vestibular phenotype in 111 carriers. Ear Hear. 2021;42(6):1525-1543. doi: 10.1097/AUD.0000000000001070 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 53.Fransen E, Verstreken M, Bom SJ, et al. A common ancestor for COCH related cochleovestibular (DFNA9) patients in Belgium and The Netherlands bearing the P51S mutation. J Med Genet. 2001;38(1):61-65. doi: 10.1136/jmg.38.1.61 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 54.Bom SJ, Kemperman MH, Huygen PL, Luijendijk MW, Cremers CW. Cross-sectional analysis of hearing threshold in relation to age in a large family with cochleovestibular impairment thoroughly genotyped for DFNA9/COCH. Ann Otol Rhinol Laryngol. 2003;112(3):280-286. doi: 10.1177/000348940311200316 [DOI] [PubMed] [Google Scholar]
  • 55.Bischoff AM, Huygen PL, Kemperman MH, et al. Vestibular deterioration precedes hearing deterioration in the P51S COCH mutation (DFNA9): an analysis in 74 mutation carriers. Otol Neurotol. 2005;26(5):918-925. doi: 10.1097/01.mao.0000185048.84641.e3 [DOI] [PubMed] [Google Scholar]
  • 56.Bae SH, Robertson NG, Cho HJ, et al. Identification of pathogenic mechanisms of COCH mutations, abolished cochlin secretion, and intracellular aggregate formation: genotype-phenotype correlations in DFNA9 deafness and vestibular disorder. Hum Mutat. 2014;35(12):1506-1513. doi: 10.1002/humu.22701 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 57.Gommeren H, Bosmans J, Moyaert J, et al. Accelerated cognitive decline associated with hearing loss and bilateral vestibulopathy: insights from a prospective cross-sectional study using the repeatable battery for the assessment of neuropsychological status adjusted for the hearing impaired in the DFNA9 population. Ear Hear. Published online December 20, 2022. doi: 10.1097/AUD.0000000000001315 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 58.Bessot N, Denise P, Toupet M, Van Nechel C, Chavoix C. Interference between walking and a cognitive task is increased in patients with bilateral vestibular loss. Gait Posture. 2012;36(2):319-321. doi: 10.1016/j.gaitpost.2012.02.021 [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplement 1.

eTable. Audiovestibular data

Click here for additional data file. (269.4KB, pdf)
Supplement 2.

Data sharing statement

Click here for additional data file. (15.5KB, pdf)

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