Impact of otolith dysfunction on postural stability and quality of life: A prospective,case-control study

Abstract

Background

Vestibular evoked myogenic potentials (VEMPs) are widely used to assess the otolith organs; however, the clinical significance of otolith organ dysfunction is unclear.

Objective

The primary purpose was to determine the functional consequences of otolith dysfunction on postural stability and quality of life in U.S. Veterans.

Methods

A prospective case-control design was used, and 124 participants (21–84 years) were grouped based on comprehensive vestibular testing. Caloric and vertical canal video head impulse testing were used to determine semicircular canal function. Cervical and ocular VEMP testing determined otolith organ function. Three vestibular site-of-lesion groups (Otolith Only, Otolith + Canal, and Canal Only) and two control groups (Dizzy Control and Non-Dizzy Control) completed measures of quality of life and multiple measures of postural control.

Results

ANCOVAs indicated significant group differences for measures of quality of life and postural stability. All vestibular groups (Otolith Only, Otolith + Canal, and Canal Only) reported significantly worse quality of life than Non-Dizzy Controls. The Otolith + Canal group performed significantly worse than the Otolith Only group and both control groups on the functional gait assessment and preferred gait speed.

Conclusions

Similar to isolated semicircular canal dysfunction, isolated otolith dysfunction may negatively impact quality of life, and in conjunction with semicircular canal dysfunction, may also negatively impact postural stability.

Keywords

vestibular diseases vestibular function tests utricle and saccule postural equilibrium traumatic brain injury

Introduction

Otolith organ testing is becoming more widely used in vestibular clinics throughout the world, yet the clinical significance of otolith organ dysfunction is unclear. Vestibular evoked myogenic potentials (VEMPs) are short-latency myogenic responses to loud sound or vibration that are used clinically to assess the otolith organs and their pathways. Cervical VEMPs (cVEMPs) are recorded from surface electrodes over the tonically contracted sternocleidomastoid (SCM) muscle and are mediated predominately by the saccule/inferior vestibular nerve (IVN).^1,2 Ocular VEMPs (oVEMPs) are recorded from surface electrodes over the inferior oblique extra-ocular muscles and are mediated predominately by the utricle/superior vestibular nerve (SVN).^3,4 Peripheral vestibular loss can occur in one or both labyrinths, in one or both branches of the vestibular nerve, and in one or more vestibular sensory end-organs. In addition, otolith organ abnormalities do not always correlate with semicircular canal (SCC) involvement.⁵ For example, unilateral utricular dysfunction can occur in isolation, which is intriguing because both the horizontal and anterior SCC and utricle are innervated by the SVN.^6,7 In addition to abnormality isolated to one organ, vestibular pathology may affect both otolith organ and SCC function.^8,9 The clinical use of VEMPs in conjunction with the ability to test each of the six SCCs allows for the identification of specific vestibular end-organ dysfunction and potential differentiation of vestibular end-organ from vestibular nerve dysfunction.

The contribution of otolith organ dysfunction to postural instability and the incidence of falls is unclear. There is substantial evidence that uncompensated peripheral vestibular loss results in postural instability, visual blurring, and subjective complaints of dizziness and/or imbalance.^10,11 Moreover, the incidence of falls is greater in individuals with unilateral or bilateral vestibular hypofunction than in healthy individuals of the same age living in the community.¹² Many studies examining the effect of vestibular loss on postural stability, however, have used tests of vestibulo-ocular reflex (VOR) function (caloric and rotational tests, or more recently the video head impulse test) that measure hSCC and SVN function to determine vestibular loss [e.g., Refs. 11–14]; therefore, the interpretation of these studies concerning the association between vestibular site-of-lesion and postural stability was based on only a partial assessment of vestibular function.

The functional impact of otolith dysfunction is a critical healthcare issue because there are emerging data that suggest the otolith organs and pathways may be particularly vulnerable to the effects of aging, mild traumatic brain injury (mTBI), and noise and blast exposure.^5,15–18 The standard of care for patients with peripheral vestibular dysfunction is vestibular rehabilitation, which includes gaze stabilization exercises based primarily upon principles of vestibular adaptation of the angular VOR. There is some evidence that combined otolith and canal dysfunction does not negatively impact rehabilitation outcomes¹⁹; however, individuals with isolated otolith organ dysfunction were not included in the study. Therefore, determining the effect of otolith organ dysfunction on postural stability may have implications for rehabilitation strategies in patients with isolated loss of otolith organ function. The purpose of this study was to determine the functional consequences of otolith dysfunction on quality of life and postural stability.

Methods

Participants

A prospective case-control study design was used to determine the effect of otolith organ dysfunction on balance, gait, and quality of life. Three vestibular groups (n = 49 combined) and two control groups (n = 75 combined) were enrolled with participants ranging in age from 18 to 84 years. The three vestibular groups included individuals with chronic (>3 months) complaints of dizziness and/or imbalance with: (1) otolith organ dysfunction only (Otolith Only), (2) SCC and otolith organ dysfunction (Otolith + Canal), and (3) SCC dysfunction only (Canal Only). The two control groups included individuals with normal canal and otolith organ function and (1) complaints of dizziness and/or imbalance (Dizzy Control) or (2) no complaints of dizziness and/or imbalance and no history of mTBI (Non-Dizzy Control).

Veterans and Servicemembers in the Reserves or National Guard with and without mTBI/blast exposure were recruited from the James H. Quillen Veterans Affairs Medical Center and via flyers to local National Guard armories and college Veteran organizations in eastern Tennessee. The protocol was approved by VA/East Tennessee State University IRB (0814.15sw) and participants provided written consent prior to initiating the study protocol.

Exclusion criteria included progressive neurological disorders (including severe peripheral neuropathy based on sensory and strength testing), benign paroxysmal positional vertigo (BPPV), superior semicircular canal dehiscence, middle-ear pathology with conductive hearing loss, abnormal ocular motor function (gaze evoked nystagmus, saccades, smooth pursuit, and optokinetic nystagmus) suggesting central pathology, lower extremity joint replacement or amputation, cognitive impairment, severe depression and anxiety, and best-corrected visual acuity worse than 20/40 in the better eye²⁰ because these factors can impact postural control independent of vestibular function. All participants were screened for cognitive impairment with the mini-mental state examination²¹ based on age and education criteria.²²

Protocol

Hearing evaluation

Behavioral audiometric assessment was performed by an audiologist in a double-walled sound-attenuated booth. Pure-tone air conduction audiometry was performed at octave and inter-octave frequencies from 0.25 to 8 kHz, and bone conduction audiometry was performed at octave frequencies from 0.5 to 4 kHz using ER-3A insert earphones. Acoustic immittance testing was performed and included 226-Hz tympanometry and ipsilateral acoustic reflex thresholds. High frequency pure-tone average (HFPTA) of the worst ear at 2, 4, and 8 kHz frequencies were calculated and used to quantify hearing sensitivity. If there was no response at a pure-tone frequency, then the limit of the audiometer at that frequency was used in the calculation of HFPTA.

Vestibular test battery

To determine the site-of-lesion for each vestibular group and to rule out vestibular dysfunction for the two control groups, comprehensive vestibular site-of-lesion testing was performed on individuals with and without dizziness and/or imbalance, and participants were grouped according to patterns of vestibular site-of-lesion test findings. Caloric testing was used as the primary measure of hSCC function, and results were obtained for all participants. Rotary chair and lateral canal video head impulse testing were used as secondary measures of hSCC pathway function; thus, test findings were only available for a portion of the participants. To rule out vertical SCC dysfunction in the Otolith only, all participants underwent video head impulse testing (vHIT) of all four vertical canals (Micromedical Technologies, Chatham, IL, USA).

To determine otolith organ function, each participant underwent cVEMP and oVEMP testing. Two-channel cervical VEMP (cVEMP) and ocular VEMP (oVEMP) recordings were performed with a clinical evoked potential system (Otometrics EP200, Taastrup, Denmark). We used air conduction (AC) cVEMPs and bone conduction (BC) oVEMPS because these tests have high response prevalence rates in normal individuals and there is substantial neurophysiologic evidence that the cVEMP is produced by activation of the saccular macula and the oVEMP results from activation of the utricular macula.²³

The procedures described below were used to determine the site-of-lesion for each vestibular group and to rule out vestibular dysfunction for the two control groups (Tables 1 and 2). The Otolith Only group included individuals with saccular and/or utricular dysfunction and no anterior SCC (aSCC), posterior SCC (pSCC), or hSCC dysfunction. The Otolith + Canal group included individuals with either saccular and/or utricular dysfunction, and aSCC, pSCC, and/or hSCC dysfunction. The Canal Only group included individuals with aSCC, pSCC, and/or hSCC dysfunction and normal otolith function.

Table 1.

Number of abnormal vestibular site-of-lesion test findings for the vestibular and control groups.

Vestibular tests	Otolith Only^* (n = 18)	Otolith + Canal^* (n = 19)	Canal Only^* (n = 12)
Caloric	0	19 (100%)	12 (100%)
cVEMP	14 (78%)	13 (68%)	0
oVEMP	6 (33%)	13 (68%)	0
Vertical vHIT	0	6 (32%)	2 (17%)

cVEMP: cervical vestibular evoked myogenic potential; oVEMP: ocular vestibular evoked myogenic potential; vHIT: video head impulse test.

^*Within a vestibular group, participants may have more than one test abnormality, thus the sum of the abnormalities does not equal 100%.

Table 2.

Summary of vestibular test findings for the three vestibular groups.

Tests of semicircular canal function						Tests of otolith function
Age	mTBI	Calorics	Rotary chair	Lateral vHIT	Vertical vHIT	cVEMP	oVEMP
Otolith Only
68	No	Normal	Normal	Normal	Normal	Unilateral	Normal
29	Yes	Normal	Normal	Normal	Normal	Unilateral	Unilateral
37	Yes	Normal	Normal	Normal	Normal	Normal	Unilateral
51	No	Normal	Normal	Normal	Normal	Unilateral	Normal
75	No	Normal	Normal	Normal	Normal	Normal	Unilateral
70	No	Normal	Normal	Normal	Normal	Normal	Unilateral
66	Yes	Normal	Normal	Normal	Normal	Unilateral	Normal
49	No	Normal	Normal	Normal	Normal	Unilateral	Normal
66	No	Normal	Normal	Normal	Normal	Unilateral	Normal
38	Yes	Normal	Normal	Normal	Normal	Unilateral	Normal
34	Yes	Normal	DNT	Normal	Normal	Unilateral	Normal
59	No	Normal	Normal	Normal	Normal	Unilateral	Normal
75	No	Normal	DNT	Normal	Normal	Unilateral	Normal
68	No	Normal	DNT	Normal	Normal	Unilateral	Normal
46	Yes	Normal	DNT	Normal	Normal	Unilateral	Normal
74	No	Normal	DNT	Normal	Normal	Bilateral	Normal
66	No	Normal	DNT	Normal	Normal	Bilateral	Bilateral
64	No	Normal	DNT	Normal	Normal	Normal	Bilateral
Otolith + Canal
64	No	Unilateral	Normal	DNT	Normal	Normal	Unilateral
64	No	Unilateral	Abnormal	DNT	RP	Unilateral	Normal
70	No	Unilateral	Abnormal	DNT	Normal	Normal	Unilateral
66	No	Unilateral	Abnormal	DNT	Normal	Unilateral	Unilateral
67	No	Unilateral	Abnormal	DNT	Normal	Unilateral	Unilateral
82	No	Unilateral	Abnormal	Normal	Normal	Unilateral	Normal
37	Yes	Bilateral	DNT	Normal	Normal	Bilateral	Normal
81	No	Bilateral	Abnormal	RL and LL	Normal	Bilateral	Bilateral
73	No	Unilateral	Normal	Normal	Normal	Bilateral	Normal
67	No	Unilateral	Abnormal	DNT	Normal	Unilateral	Unilateral
51	No	Unilateral	Normal	DNT	Normal	Normal	Unilateral
47	Yes	Unilateral	Abnormal	RL	Normal	Normal	Unilateral
55	No	Unilateral	Abnormal	Normal	Normal	Unilateral	Unilateral
47	No	Bilateral	Abnormal	RL and LL	RP	Bilateral	Bilateral
67	Yes	Unilateral	DNT	Normal	Normal	Unilateral	Normal
74	No	Unilateral	DNT^*	RL and LL	LA, RP, RA, and LP	Normal	Bilateral
53	No	Unilateral	DNT^*	Normal	Normal	Bilateral	Normal
72	No	Unilateral	DNT	LL	LA, RP, RA, and LP	Normal	Bilateral
80	No	Bilateral	DNT	RL	Normal	Unilateral	Bilateral
Canal Only
73	No	Unilateral	Abnormal	Normal	Normal	Normal	Normal
26	Yes	Unilateral	Normal	Normal	RA	Normal	Normal
79	Yes	Bilateral	Abnormal	RL and LL	Normal	Normal	Normal
64	No	Unilateral	Abnormal	Normal	Normal	Normal	Normal
67	No	Unilateral	Abnormal	DNT	Normal	Normal	Normal
59	No	Unilateral	Normal	Normal	Normal	Normal	Normal
68	No	Unilateral	DNT	RL	Normal	Normal	Normal
35	Yes	Unilateral	DNT	Normal	Normal	Normal	Normal
68	No	Unilateral	DNT	Normal	Normal	Normal	Normal
73	No	Unilateral	DNT	Normal	Normal	Normal	Normal
33	Yes	Unilateral	DNT	Normal	Normal	Normal	Normal
67	Yes	Unilateral	DNT	Normal	Normal	Normal	Normal

^*Previous clinical testing revealed abnormal rotary chair findings.

DNT: did not test; mTBI: history of mild traumatic brain injury; vHIT: video head impulse test cVEMP: cervical vestibular evoked myogenic potential; oVEMP: ocular vestibular evoked myogenic potential; LL: abnormal left lateral semicircular canal function; RL: abnormal right lateral semicircular canal function; LA: abnormal left anterior semicircular canal function; RP: abnormal right posterior semicircular canal function; RA: abnormal right anterior semicircular canal function; LP: abnormal left posterior semicircular canal function.

Pre-test instructions included refraining from the use of alcohol, recreational drugs, over-the-counter antihistamines, anti-vertigo medications, and central nervous system suppressants. The Dix-Hallpike and roll tests were performed to rule out the presence of BPPV. Abnormal acoustic immittance and air-bone gap (>10 dB) during pure-tone audiometry were used to exclude participants with middle-ear pathology. Vestibular audiologists performed the audiometric and vestibular assessments.

The binaural bithermal water caloric test was performed using videonystagmography as described previously.²⁴ Abnormal response was defined as ≥ 25% asymmetry of the slow component eye velocity (SCEV), which suggests unilateral hSCC dysfunction.²⁵ Bilateral hSCC dysfunction was indicated by total warm SCEV <11°/s and total cool SCEV <11°/s.²⁴

For the rotary chair test (Micromedical System 2000), slow harmonic acceleration at frequencies ranging from 0.01 to 0.64 Hz were used.²⁴ Rotary chair was considered abnormal when phase, gain, or asymmetry was >2 SD of our laboratory normative values, and abnormal at two or more adjacent frequencies.

The vHIT was performed (Micromedical) with participants seated and eye position was calibrated prior to testing. To perform the lateral canal vHIT, the examiner stood behind the participant and manually rotated the head abruptly and unpredictably to the left or right through a small angle (10 to 20°) in the horizontal plane. To test either of the co-planar vertical canal pairs, the participant’s head was turned either to the right (LARP) or to the left (RALP) ∼30 to 40° relative to the trunk prior to rotating the head either downward (stimulates the anterior canal) or upward (stimulates the posterior canal). The vHIT software recorded both overt and covert catch-up saccades and calculated VOR gain using a wide window method of calculating gain based on position. Gain is calculated as the ratio of head and eye position at the start of the head thrust to an end point. The end point is usually when the head velocity returns to 0 deg/s. However, if covert saccades are detected, the end point is moved to base of the first saccade. Abnormal canal function was defined as low VOR gain (<0.7 for lateral canal and <0.6 for vertical canal) and/or the presence of catch-up saccades.²⁶

Air conduction cervical VEMPs were obtained using 500-Hz Blackman-gated tone bursts (rarefaction onset phase; rise/fall time = 1 cycle and plateau = 3 cycles) presented monaurally via insert earphones at 90 dB nHL (GN Otometrics EP200; version 6.2.1). The SCM muscle was activated unilaterally in the sitting position for a target EMG level (50–90 µV), and participants were tested in supine with the head rotated laterally if the target EMG range could not be obtained in the sitting position. If cVEMPs were absent at the 50–90 μV-EMG level, then recordings were obtained at maximum voluntary contraction (MVC) of the sSCM muscle, and cVEMP amplitude was normalized for EMG level. Participants who had absent cVEMPs at 500 Hz with MVC were then tested with a 1000-Hz tone burst and at MVC to verify that the cVEMPs were absent. Cervical VEMPs were also recorded at 64 dB nHL to rule out SSCD.

Ocular VEMPs were recorded using a 500-Hz Blackman-gated tone burst (rarefaction onset phase; rise/fall time = 1 cycle and no plateau) presented at a repetition rate of 5 Hz at 155 dB peak force level (re: 1 µNewton). Stimuli were generated by a commercial evoked potential instrument (GN Otometrics EP200; version 6.2.1), amplified (Bruel and Kjaer power amplifier, model 2810), and delivered by a hand-held vibrator (Bruel and Kjaer Mini-Shaker, model 4810) fitted with a custom acrylic rod. The Mini-Shaker was held by the examiner such that the axis of the acrylic rod was approximately perpendicular to the subject’s skull at Fz. Surface electrodes were placed below the center of each pupil and the ground electrode was at Fpz. The EMG was amplified (100,000x), band-pass filtered (1–1000 Hz), and sampled at 12 kHz. The 70-ms recording epoch included a 20-ms pre-stimulus baseline. Each oVEMP waveform consisted of responses to 75 stimuli and waveforms were replicated for each subject.

Peak-to-peak cVEMP amplitude (P1-N1) was calculated from the mean value of the replicated waveforms for each subject, and cVEMP amplitude was normalized for EMG level. Peak-to-peak oVEMP amplitude (N1-P1) was calculated from the mean value of the replicated waveforms for each subject. The criteria for abnormal cVEMP and oVEMP testing were defined as an absent VEMP response (unilateral or bilateral) or a corrected VEMP amplitude asymmetry ratio ≥40%.²⁴

Postural stability and quality of life outcome measures

To evaluate the effect of vestibular site-of-lesion on postural stability and quality of life, patient-reported outcomes and multiple measures of balance and gait were performed within 4 weeks of vestibular laboratory tests. Demographics, medical history, and fall history were assessed using a health history questionnaire. Quality of life outcome measures included: (1) symptom interference, (2) Activities-specific Balance Confidence scale, (3) Dizziness Handicap Inventory, (4) Disability Rating Scale, (5) Vestibular Activities and Participation measure. Postural stability outcome measures included: (6) history of falls, (7) Sensory Organization Test, (8) functional gait assessment, and (9) gait characteristics, including preferred gait speed, with and without head turns. Total time to complete balance and gait assessment was approximately one and a half hours and rest breaks were provided as needed. A research physical therapist who was blinded to group (i.e., vestibular test results) administered questionnaires and performed neurological screening and gait and balance testing.

Symptom interference incorporates visual analogue scales to assess perception of the percent of time that dizziness interferes with activities. This technique employs a 10-cm horizontal line marked in 20% increments (0%–100%) and the score is the percentage distance from zero to the participant’s mark.²⁷

Activities-specific Balance Confidence (ABC) scale was used to measure participants’ self-report of confidence to maintain balance in a variety of situations.²⁸ A lower score indicates worse confidence in balance ability and scores <67% have been associated with a risk for falling.²⁹

The Dizziness Handicap Inventory (DHI) is a 25-item scale used to measure the impact of dizziness or unsteadiness on daily activities.³⁰ The DHI total scores can range from 0 to 100 with higher scores indicating greater self-perceived handicap due to dizziness or imbalance. Scores greater than 30 indicate moderate to severe handicap.³¹

The Disability Rating Scale (DRS) is a six-point scale from 0 to 5 with 0 indicating no disability and five indicating long-term severe disability.³² Participants were instructed to check the one descriptive phrase to describe the impact of their symptoms.

The Vestibular Activities and Participation (VAP) measure is a disease-specific measure to examine the impact of vestibular disorders on activities and participation.³³ A composite score was calculated as the average of the item scale values after excluding the N/A items and a lower score indicates less difficulty.

History of falls in the past year was extracted from the health history questionnaire and based on self-report. Participants responded to whether they had “fallen (including a slip or trip) in which [they] unexpectedly lost [their] balance and landed on the floor or ground or lower level within the past year.” If they responded yes, then they recorded how many times they had fallen.

Sensory Organization test (SOT) assessed the use of sensory information by measuring postural sway under altered visual and somatosensory conditions.³⁴ The SOT was performed as described previously [3; NeuroCom SMART Equitest]. Patterns of use of sensory information for balance were calculated from ratios of the equilibrium scores from the different conditions. The Visual Ratio is the ratio of the equilibrium score for condition four (eyes open, sway-referenced surface) relative to the equilibrium score for condition 1 (eyes open, firm surface), the Somatosensory Ratio is condition 2 (eyes closed, firm surface) relative to condition 1 and the Vestibular Ratio is condition five (eyes closed, sway-referenced surface) relative to condition 1.

Functional gait assessment (FGA) is a 10-item clinical test that incorporates gait items that are particularly difficult for people with vestibular disorders (e.g., walking with head turns, narrow base of support, backwards, and with eyes closed).³⁵

Gait characteristics were measured using an electronic walkway (GAITRite® System).³⁶ Participants were instructed to walk at their preferred gait speed with and without head turns to quantify the temporal and spatial parameters of gait. The electronic walkway is 9 m long and 1 m wide, and the active area of the mat is 8 m long and 0.6 m wide with 12.7 mm between sensors. Temporal resolution of the system is 12.5 ms. Gait characteristics examined included average velocity, stride length, step width, double support time, stride velocity, and variability of stride velocity.

In addition to the outcome measures, we recorded the following personal factors that may impact postural stability: total number of comorbidities that impact mobility (Functional Comorbidity Index),³⁷ depression (15-item Geriatric Depression Scale),³⁸ anxiety (20-item Geriatric Anxiety Inventory),³⁹ physical activity level (Physical Activity Scale for the Elderly),⁴⁰ lower extremity strength (30-s chair stand test)⁴¹ and symptoms of post-traumatic stress disorder (PTSD) (PTSD Checklist – Civilian Version, PCL-C)⁴² via self-report questionnaires.

Data analyses

The sample size was based on power calculations that assumed equal group sizes for the Otolith Only (n = 32), Dizzy Control (n = 32), and Non-Dizzy Control (n = 32) groups, and half the size for the Otolith + Canal group (n = 16). To obtain an adequate sample size for group comparisons, we oversampled the Canal Only group to ensure that the Canal Only group (n = 12) would be 10% of the total sample. The original power analysis was based on preliminary site-of-lesion findings from 262 patients and informed by group means and standard deviations for balance and gait data. Using these data, an effect size of f = 0.421 was estimated, and a total sample size of 124 was calculated to yield 95% power at α = 0.05 for planned group comparisons (e.g., vestibular vs control).

All data were summarized by study group (three vestibular groups and the two control groups) using descriptive statistics. Separate one-way ANOVAs were utilized to determine group differences in the covariates (alpha = 0.05). For significant main effects, post-hoc pairwise comparisons using the least significant differences method were performed. Each outcome measure was analyzed independently as each involves a distinct domain. Missing data were not imputed; thus, participants with missing data were removed from these analyses.

To determine the functional consequences of vestibular site-of-lesion on postural stability, the study groups were compared using linear and generalized linear models for continuous outcomes while adjusting for covariates that may impact postural stability. The covariates included age, mTBI status (yes/no), depression, lower extremity strength, and hearing sensitivity (highest, i.e., worst, HFPTA of the left or right ear). To reduce multicollinearity, for any pair of covariates that had a correlation greater than 0.80, one of the covariates was excluded from the analysis depending on which covariate had a higher correlation with the other five covariates. To determine differences on the Disability Rating Scale among the study groups a Kruskal-Wallis test was used due to the non-normal distribution of the data and the need to compare multiple independent groups.

Analysis of covariance (ANCOVA) models were fit to investigate group differences (alpha = 0.05) in outcomes. Adjusted means and 95% confidence intervals were estimated for each study group, and pairwise comparisons of the adjusted means were completed using the Fisher’s LSD method to adjust for pairwise multiple comparisons within each outcome analysis.

To examine the effect of vestibular site-of-lesion on specific gait characteristics (velocity, stride length, step width, double support time, and stride velocity SD), separate one-way ANOVAs compared the study groups (alpha = 0.05). For significant main effects, post-hoc pairwise comparisons using the least significant differences method were performed. IBM SPSS v28 was used for statistical analyses.

Results

Participant characteristics

A total of 921 Veterans and Reservists were screened for eligibility, and 158 were enrolled in this study (Figure 1). Of these, 124 Veterans completed the study protocol, 10 withdrew, and 24 were disqualified. Reasons for disqualification were central vestibular dysfunction (n = 6), neurological abnormalities (n = 2), positive lateral canal vHIT or no vHIT test for the Otolith Only group (n = 3), positive vestibular findings for participants recruited for the Dizzy Control group (n = 1) and Non-Dizzy Control group (n = 7), musculoskeletal abnormality (n = 3), and severe anxiety during testing (n = 2).

Figure 1.

Consolidated standards of reporting trials flow diagram of trial enrollment.

The three vestibular groups included Veterans with dizziness and/or imbalance and vestibular test findings consistent with: Otolith Only (n = 18), Otolith + Canal (n = 19), and Canal Only (n = 12). The two control groups included Veterans with dizziness and/or imbalance and normal vestibular test findings (Dizzy Control; n = 50) and Veterans without dizziness or imbalance and normal vestibular test findings (Non-Dizzy Control; n = 25). Results from the specific vestibular test findings (Table 2) revealed that the majority of individuals with otolith only dysfunction had abnormal cVEMP tests (14 of 18) suggesting saccular dysfunction; whereas, only one-third of these participants had abnormal oVEMP tests suggesting utricular dysfunction. For the group with both otolith and canal dysfunction, there was an equal number of participants with cVEMP and oVEMP abnormalities. All participants in the Canal Only and Otolith + Canal groups had abnormal caloric test findings suggesting hSCC dysfunction, and there were no participants with isolated vertical canal dysfunction (i.e., low gain on vertical vHIT).

Participant demographics and covariates for each group are summarized in Table 3. There were no significant group differences for age, race, ethnicity, gender, education or occupational status. Overall, the mean age was 56.4 ± 16.8 years, 99% were male, 90% were Caucasian and 6% were African American. There was a significant group difference in the total number of comorbidities based on FCI (p = 0.003, η_p2 = 0.123). Post-hoc testing revealed that the Non-Dizzy Control group had significantly fewer comorbidities than the other groups except the Canal only group (p ≤ 0.04) and the Dizzy Control group had significantly fewer comorbidities than the Otolith + Canal group (p = 0.02). Excluding the Non-Dizzy Control group who did not have a history of mTBI, there was no significant difference in the proportion of participants with history of mTBI/blast (χ² test: p = 0.098) among the vestibular and the Non-Dizzy Control groups. Nearly one-third of participants (n = 38) reported a history of mTBI, and 27 of these were related to blast exposure. In the Otolith Only group 33% reported a history of mTBI, 16% in Otolith + Canal group, 42% in the Canal Only group and 48% in the Dizzy Control group.

Table 3.

Demographics and covariates by study group.

	Study group
	Vestibular			Control		Total (N = 124)
	Otolith Only (N = 18)	Otolith + Canal (N = 19)	Canal Only (N = 12)	Dizzy (N = 50)	Non-Dizzy (N = 25)	Total (N = 124)
Age (years)
Mean (SD)	57.4 (15.2)	64.1 (12.6)	59.3 (17.7)	51.7 (16.9)	58.0 (18.1)	56.4 (16.8)
Range (min–max)	29–75	37–82	26–79	26–84	21–82	21–84
Male, n (%)	18 (100.0%)	19 (100.0%)	12 (100.0%)	50 (100.0%)	24 (96.0%)	126 (99.2%)
Race/ethnicity
Caucasian	16 (88.9%)	19 (100.0%)	12 (100.0%)	43 (86.0%)	19 (76.0%)	112 (88.2%)
African-American	1 (5.6%)	0 (0.0%)	0 (0.0%)	3 (6.0%)	3 (12.0%)	7 (5.5%)
Hispanic or Latino	1 (5.6%)	0 (0.0%)	0 (0.0%)	1 (2.0%)	0 (0.0%)	2 (1.6%)
Other	0 (0.0%)	0 (0.0%)	0 (0.0%)	1 (2.0%)	2 (8.0%)	3 (2.4%)
Unknown	0 (0.0%)	0 (0.0%)	0 (0.0%)	2 (4.0%)	1 (4.0%)	3 (2.4%)
Highest education
High school	6 (33.3%)	7 (36.8%)	3 (25.0%)	9 (18.0%)	4 (16.0%)	29 (22.8%)
Vocational training/some college/associate degree	10 (55.6%)	8 (42.1%)	5 (41.7%)	21 (42.0%)	11 (44.0%)	58 (44.6%)
Bachelor’s degree	1 (5.6%)	2 (10.5%)	2 (16.7%)	13 (26.0%)	6 (24.0%)	24 (18.9%)
Post-graduate training	1 (5.6%)	2 (10.5%)	2 (16.7%)	7 (14.0%)	4 (16.0%)	16 (12.6%)
Occupational status
Employed	4 (22.2%)	1 (5.3%)	4 (33.3%)	21 (42.0%)	6 (24.0%)	36 (28.3%)
Unemployed	2 (11.1%)	1 (5.3%)	0 (0.0%)	4 (8.0%)	4 (16.0%)	11 (8.7%)
Retired	8 (44.4%)	13 (68.4%)	7 (58.3%)	19 (38.0%)	11 (44.0%)	60 (47.2%)
Disabled	3 (16.7%)	4 (21.1%)	1 (8.3%)	4 (8.0%)	2 (8.0%)	15 (11.8%)
Other	1 (5.6%)	0 (0.0%)	0 (0.0%)	2 (4.0%)	2 (8.0%)	5 (3.9%)
Functional Comorbidity Index (/18)**
Mean (SD)	4.4 (2.3)	5.9 (2.1)	4.4 (2.4)	4.3 (2.6)	2.9 (2.4) †	4.3 (2.6)
Arthritis n (%)	12 (67%)	12 (63%)	6 (50%)	23 (46%0)	10 (40%)	63 (51%)
Depression n (%)	7 (39%)	10 (53%)	7 (58%)	24 (48%)	6 (24%)	54 (44%)
Obesity n (%)	10 (56%)	4 (21%)	3 (25%)	20 (40%)	6 (24%)	41 (33%)
Heart disease n (%)	3 (17%)	8 (42%)	4 (33%)	9 (18%)	3 (12%)	27 (22%)
Diabetes n (%)	3 (17%)	10 (53%)	3 (25%)	7 (14%)	3 (12%)	26 (21%)
PTSD severity score (range: 17–85)
Mean (SD)	39.6 (15.9)	35.3 (17.3)	38.8 (16.1 0	43.5 (17.3)	29.2 (13.8) †	38.4 (16.8)
Range	19–67	17–74	17–67	18–83	17–58	17–83
Anxiety (/20)
Mean (SD)	5.9 (5.6)	4.8 (5.8)	6.2 (6.2)	8.0 (7.2)	1.9 (2.8) †	5.9 (6.4)
Physical Activity Level (units)
Mean (SD)	190.5 (102.7)	127.5 (89.5)	187.5 (92.4)	199.3 (116.8)	173.5 (87.6) †	179.3 (104.4)
Covariates: mTBI History
No	12 (66.7%)	16 (84.2%)	7 (58.3%)	26 (52.0%)	25 (100.0%)	87 (68.5%)
Yes	6 (33.3%)	3 (15.8%)	5 (41.7%)	24 (48.0%)	0 (0.0%)	40 (31.5%)
Depression (/15)***
Mean (SD)	5.1 (4.1)	4.7 (3.8)	3.4 (2.3)	5.6 (4.0)	1.6 (1.6) †	4.4 (3.8)
Lower extremity strength (n)***
Mean (SD)	14.3 (3.0)	10.2 (3.8)	13.8 (3.6)	15.3 (5.6)	16.8 (3.6)	14.5 (4.9)
HFPTA (dB HL)**
Mean (SD)	39.6 (23.5)	63.2 (24.6)	50.6 (19.4)	38.2 (24.4)	38.7 (28.5)	43.5 (26.0)

mTBI: mild traumatic brain injury; PTSD: post-traumatic stress disorder; HFPTA (dB HL): high frequency pure-tone average (dB hearing loss) of the worst ear †One participant did not complete the self-report questionnaires.

**p < 0.01; ***p < 0.001 for group differences.

There were significant study group differences for three of the covariates. There was a significant main effect of group for lower extremity strength (p < 0.001, η_p2 = 0.181) and post-hoc testing revealed that the Otolith + Canal group had significantly lower strength than the other groups (p ≤ 0.036). There was a significant main effect of group for depression (p < 0.001, η_p2 = 0.160) and post-hoc testing revealed that the Non-Dizzy Control group had significantly lower depression scores than the Otolith Only, Otolith + Canal, and Dizzy Control groups (p ≤ 0.005). There was a significant main effect of group for hearing sensitivity (p = 0.004, η_p2 = 0.122) and post-hoc testing revealed that the Otolith + Canal group had significantly worse hearing than the Otolith Only and both control groups (p ≤ 0.005).

Consequences of vestibular dysfunction on quality of life

ANCOVAs determined that there were significant differences in the quality of life outcome measures between the groups, while accounting for age, hearing sensitivity, depression, lower extremity strength, and mTBI status (p ≤ 0.009, η_p² ≥ 0.117). The results are summarized in Table 4 (see Supplemental Table 1 for details). There were significant differences among the five groups (see below), but there were no significant differences among the three vestibular groups (Otolith Only, Otolith + Canal, and Canal Only).

Table 4.

Descriptive statistics (unadjusted means (SD)) and group comparisons (ANCOVA^†) for quality of life, balance, and gait measures by study group.

	Study Group					Significant group differences
	Vestibular			Control
	Otolith Only (N = 18)	Otolith + Canal (N = 19)	Canal Only (N = 11)	Dizzy (N = 49)	Non-Dizzy (N = 24)
Symptom interference (%)	28.6 (26.8)	33.2 (29.0)	35.9 (26.3)	21.5 (22.1)	1.9 (5.6)	^{f,g,h*,i}
Activities-specific Balance Confidence Scale (%)	66.3 (28.5)	60.2 (24.1)	70.5 (20.5)	73.1 (24.5)	96.4 (4.2)	^{f,g,h,i}
Dizziness Handicap Inventory (/100)	30.9 (21.4)	41.8 (22.1)	33.8 (22.3)	32.9 (22.0)	1.0 (2.1)	^{f,g,h,i*}
Disability Rating Scale (n, %)						^{f*,g,h,i*}
No disability (0)	1, 6%	0, 0%	0, 0%	7, 14%	22, 92%
No disability (1)	4, 22%	4, 21%	3, 25%	5, 10%	2, 8%
Mild disability (2)	4, 22%	4, 21%	3, 25%	18, 36%	0, 0%
Moderate disability (3)	9, 50%	6, 32%	5, 42%	14, 28%	0, 0%
Severe disability (4)	0, 0%	0, 0%	0, 0%	2, 4%	0, 0%
Long-term disability (5)	0, 0%	5, 26%	1, 8%	4, 8%	0, 0%
Vestibular Activities and Participation Measure (/4)	0.81 (0.56)	1.34 (0.79)	1.02 (0.73)	0.93 (0.76)	0.09 (0.15)	^g,h,i**
SOT Composite score (/100)	68.0 (14.9)	45.6 (19.5)	64.5 (11.7)	71.7 (12.6)	74.5 (9.5)
SOT Visual Ratio score	0.80 (0.23)	0.60 (0.37)	0.83 (0.15)	0.85 (0.17)	0.89 (0.09)
SOT Somatosensory Ratio score	0.92 (0.15)	0.85 (0.23)	0.93 (0.06)	0.94 (0.06)	0.96 (0.02)
SOT vestibular Ratio score	0.52 (0.26)	0.19 (0.24)	0.47 (0.27)	0.59 (0.23)	0.63 (0.16)
Functional gait assessment (/30)	23.1 (4.8)	17.4 (5.0)	21.4 (5.1)	23.9 (5.0)	25.2 (3.9)	^a,d,g**
Preferred gait speed (m/s)	1.26 (0.22)	1.04 (0.23)	1.17 (0.23)	1.19 (0.22)	1.29 (0.21)	^{a*,d,g**,i}
History of falls (#)	6.1 (13.2)	2.4 (3.1)	0.9 (1.6)	3.2 (5.0)	0.0 (0.2)

SOT: Sensory organization test.

^aOtolith Only versus Otolith + Canal.

^bOtolith + Canal versus Canal Only.

^cOtolith Only versus Canal Only.

^dOtolith + Canal versus Dizzy Control.

^eCanal Only versus Dizzy Control.

^fOtolith Only versus Non-Dizzy Control.

^gOtolith + Canal versus Non-Dizzy Control.

^hCanal Only versus Non-Dizzy Control.

ⁱDizzy Control versus Non-Dizzy Control.

^†Covariates included age, mTBI status (yes/no), depression, lower extremity strength, and hearing sensitivity (highest HFPTA of the left or right ear).

*p < 0.05; **p < 0.01; ***p < 0.001.

There was a significant effect of group on symptom interference (p = 0.007, η_p2 = 0.122), balance confidence (p = 0.003, η_p2 = 0.137), and dizziness handicap (p < 0.001, η_p2 = 0.162). Post-hoc testing revealed that the three vestibular groups and the Dizzy Control group had significantly worse scores (i.e., greater symptom interference, lower balance confidence, and greater perceived handicap) than the Non-Dizzy Control group (p ≤ 0.014). There was a significant effect of group (p = 0.008, η_p2 = 0.119) on the Vestibular Activities and Participation measure. Post-hoc testing revealed that the Canal + Otolith (p = 0.006), Canal Only (p = 0.003), and Dizzy Control groups (p = 0.003) had significantly higher scores (i.e., greater interference with activities due to dizziness) than the Non-Dizzy Control group. There was a significant difference in the proportional odds (p < 0.001; Kruskal-Wallis test for ordinal data) between groups. Using a bootstrap approach, the three vestibular groups and the Dizzy Control group had significantly (p < 0.001) greater odds of higher scores (i.e., greater disability) than the Non-Dizzy Control group.

Consequences of vestibular dysfunction on postural control

ANCOVAs determined differences in the postural control outcome measures between groups, while accounting for age, hearing loss, depression, lower extremity strength and mTBI status. The results are summarized in Table 4.

There was not an overall significant difference between groups (p = 0.185) for the number of falls in the previous year. There were no overall significant differences found for the SOT Composite score (p = 0.097), Visual Ratio score (p = 0.656), Somatosensory Ratio score (p = 0.810), or Vestibular Ratio score (p = 0.052). There was a significant effect of group for FGA (p = 0.039, η_p2 = 0.089). The covariates age (p = 0.001), depression (p = 0.022), and lower extremity strength (p < 0.001) showed significance, but no significant effect was found for hearing loss (p = 0.304) or mTBI status (p = 0.702). Post-hoc testing revealed the Otolith + Canal group performed significantly worse than the Otolith Only group (p = 0.013) and significantly worse than the Non-Dizzy and Dizzy Control groups (p = 0.004 and p = 0.006, respectively).

The Otolith + Canal group walked significantly slower than the Otolith Only group (p = 0.003), and both Control groups (p ≤ 0.018). Furthermore, the Dizzy Control group walked significantly slower than the Non-Dizzy Control group (p = 0.047). See Supplemental Table 2 for group comparisons of additional gait characteristics.

Discussion

The current study revealed that any vestibular dysfunction, including isolated otolith organ or semicircular canal dysfunction, negatively impacts quality of life. More widespread vestibular damage, which frequently involved multiple end-organs and/or bilateral involvement in the Otolith + Canal group also negatively impacted postural stability. Comorbidities common in military personnel—history of mTBI and hearing loss—were used as covariates in the analyses and were not significantly related to any of the quality of life or postural stability measures. In fact, few of the covariates examined were significantly associated with the outcome measures. Age was associated with FGA, but none of the QoL measures. Depression was associated with one QoL outcome (DHI) and both depression and lower extremity strength were associated with one gait outcome (FGA).

Vestibular site-of-lesion groups

Participants were grouped according to vestibular site-of-lesion and the greatest number of participants were in the Otolith + Canal group and the fewest in the Canal Only group. The majority of individuals in the Otolith Only group had abnormal saccular pathway function, and only 11% had abnormalities in both saccular and utricular pathways. In contrast, nearly 40% of the Otolith + Canal group demonstrated more widespread vestibular pathway dysfunction involving multiple canals and both otolith organs. All participants in the Canal Only and Otolith + Canal groups had abnormal hSCC function, and there were no participants with isolated abnormal vertical SCC function.

Consequences of otolith dysfunction on quality of life

Individuals with vestibular dysfunction demonstrated a poorer quality of life than healthy individuals without dizziness indicating that vestibular dysfunction disrupts performance of daily activities. Overall, participants across vestibular dysfunction groups (Otolith Only, Otolith + Canal, and Canal Only) reported that their dizziness and imbalance resulted in a moderate perceived handicap (DHI) and lower perceived balance confidence (ABC). Furthermore, approximately one-third reported that their symptoms disrupted both household and work activities (DRS).

There were no significant differences in QoL scores among the vestibular groups indicating that otolith dysfunction has a comparable impact on QoL as canal dysfunction. These findings are consistent with previous work showing similar levels of self-reported dizziness handicap across vestibular sites of lesion.^8,9 In contrast to these studies, the current study used oVEMP which provided a measure of utriculo-ocular pathways in addition to sacculo-collic pathways. Our findings were similar to Yip and Strupp⁴³ who used oVEMP and cVEMP to identify otolith dysfunction and reported similar DHI scores across vestibular groups (by vestibular diagnosis, such as vestibular migraine, or main groups of vestibular disorders, such as peripheral, central, or functional). In contrast, two studies have reported differences in QoL among vestibular sites of lesion. Farrell and Rine⁴⁴ reported greater dizziness handicap in patients with otolith dysfunction compared to those with canal dysfunction (and normal otolith function); however, the interpretation of these findings is limited due to the small sample size (otolith dysfunction = 11 and canal dysfunction = 3). Sestak et al.⁴⁵ also reported significant differences among vestibular groups: patients with canal and otolith dysfunction had severe dizziness handicap and patients with isolated vestibular pathway dysfunction (Otolith Only or Canal Only) had moderate dizziness handicap. The current study included participants with chronic symptoms not seeking medical care, in contrast to Sestak et al.⁴⁵ who included clinic patients with more recent symptom onset. The conflicting findings from the two studies may be due to a difference in central compensation.

Consequences of otolith dysfunction on postural control

Overall, the participants in the vestibular dysfunction groups demonstrated deficits in postural stability. Specifically, the mean SOT composite score was below normal (<70) for each vestibular group suggesting poor static balance control. The mean FGA score for the vestibular groups (≤23.1) indicated poor dynamic balance control below normal for age (>26 indicates normal ability up to age of 69 years) and increased fall risk (<23 indicates fall risk) for the Otolith + Canal and Canal Only groups.

Although the mean scores for balance and gait performance suggested reduced static and dynamic balance control for all vestibular groups, only the Otolith + Canal group performed significantly worse than the Non-Dizzy Control group. Furthermore, the Otolith + Canal group performed significantly worse than the isolated Otolith Only group on the FGA and preferred walking speed suggesting that damage to multiple vestibular pathways is more detrimental to postural stability than damage isolated to the otolithic pathways. It is not surprising that the Otolith + Canal group would have impaired balance given the dynamic interplay of otolith and canal contributions to postural control.⁴⁶ There is ambiguity in the otolith signal that is resolved with input from the SCCs. Bermudez-Rey and colleagues⁴⁶ demonstrated that higher (i.e., worse) vestibular perceptual thresholds of roll tilt, a measure of noise in the central integration of canal and otolith input, are strongly associated with postural instability during a “vestibular” balance task (i.e., eyes closed standing on foam). In their study, the mixed model (adjusted for age, gender, and migraine) revealed that the proportion of failures in the balance task was significantly associated with higher roll tilt thresholds.⁴⁶ This is an important finding as failures in the vestibular balance task have been linked to a 3.6-fold increase in the odds of experiencing a fall.⁴⁷ The groups with isolated vestibular dysfunction (Otolith Only and Canal Only) performed similarly to the Non-Dizzy Control group. These findings may reflect the redundancy of vestibular input to the VSR pathway limiting the functional impact of hypofunction isolated to a single vestibular pathway. In contrast, more widespread damage across vestibular pathways resulted in greater balance and gait impairment.

It is interesting that isolated vestibular dysfunction (either otolith or canal) significantly impacted QoL but not postural stability. One possibility is that the perception of dizziness has an emotional impact on the perceived action affordances that may explain the subjective perception of changes without detectable performance changes in balance and gait.⁴⁸ Another possibility is that laboratory measures of postural control are not sensitive enough to identify more subtle balance and gait impairment that could occur with vestibular hypofunction isolated to a single pathway. Additionally, standard laboratory balance testing may inadequately reflect the postural challenges of real-life situations that inform participant’s responses to QoL measures. Future studies may need to include more challenging assessment of postural control in the laboratory, such as tests of reactive balance that can simulate a slip or trip.

Previous work has examined the role of otolith dysfunction on postural control; however, otolith assessment was limited to cVEMP.^8,49 Like the present study, individuals with combined Otolith + Canal dysfunction were less stable (greater sway velocity and sway envelope) than controls on tests of sensory integration for balance. In contrast to the current findings, individuals with isolated vestibular dysfunction (Otolith Only and Canal Only) were also less stable than controls on tests of sensory integration for balance. McCaslin and colleagues⁸ also reported that individuals with canal only dysfunction were less stable than individuals with otolith only dysfunction. Using subjective visual horizontal (SVH) as a measure of utricular pathway function and cVEMP, Murray et al.⁹ reported similar balance and gait performance in a group with hSCC and otolith dysfunction compared to a group with hSCC dysfunction only. There are, however, important distinctions between the current study and the McCaslin and Murray studies. First, a more comprehensive vestibular test battery was used in the present study to categorize participants according to vestibular site-of-lesion. For example, utricular testing (oVEMP) was performed in the current study which ruled out utricular pathway dysfunction in the canal only group. It is noteworthy that the Otolith Only group had four participants with normal cVEMP testing but abnormal oVEMP testing. Further, participants in previous studies who were categorized as having isolated otolith dysfunction may have also had vertical SCC dysfunction. In the current study, abnormal vertical canal function was ruled out using video head impulse testing, and four participants in the Otolith + Canal group had vertical canal dysfunction in addition to horizontal canal dysfunction. Finally, in contrast to Murray et al.,⁹ the current study used oVEMP as a measure of utricular function rather than SVH; oVEMP reflects dynamic otolith function, whereas SVH likely reflects static function.⁵⁰

Previous research has shown that individuals with vestibular disorders have persistent gait deficits. While walking at preferred speed on level surface without and with head turns, individuals with vestibular disorders demonstrate slower gait velocity, lower cadence, and shorter step length compared to healthy controls.^36,51,52 The findings from the current study revealed similar findings and extend the research to specific vestibular deficits. Whereas, isolated vestibular hypofunction did not significantly change gait characteristics compared to the Non-Dizzy Control group, multiple vestibular pathway involvement in the Otolith + Canal group resulted in significant alterations in gait compared to the Otolith Only and Non-Dizzy Control groups.

These findings suggest that comprehensive vestibular assessment (including otolith testing) is important for clinical management of patients with dizziness and imbalance, as isolated otolith dysfunction has a negative impact on quality of life and may negatively impact postural stability. Vestibular assessment limited to the horizontal semicircular canal pathway may miss important information about otolith function, and reduces the likelihood that these patients would be referred for vestibular rehabilitation. Furthermore, comprehensive vestibular assessment may reveal damage to multiple vestibular pathways which may have more severe consequences to postural stability than isolated vestibular pathway damage. A recent study determined that some individuals with combined hSCC and saccular pathway dysfunction may have less robust recovery of subjective dizziness following vestibular rehabilitation than individuals with only hSCC dysfunction.⁵³ It is unclear if treatment approaches should be adjusted based on vestibular site-of-lesion or the extent of damage to the vestibular pathways. Future work should examine more carefully the role that vestibular site-of-lesion plays on vestibular rehabilitation treatment outcomes.

Dizzy controls (normal vestibular function)

A unique aspect of this study was the inclusion of a dizzy control group comprised of individuals with symptoms of dizziness and/or imbalance but normal vestibular function. In general, the dizzy control group reported greater impact of dizziness or imbalance on quality of life compared to the Non-Dizzy Control group although their balance and gait performance was similar. Compared to the three vestibular groups, the dizzy control group reported similar impact of dizziness on quality of life but generally performed better on balance and gait tasks. These findings are consistent with a previous study that demonstrated that patients with dizziness and normal vestibular function report similar dizziness handicap as patients with vestibular dysfunction, although, balance measures in the previous work were not provided.⁶

Although the demographics were not significantly different across groups, the dizzy control group tended to be younger, employed, and more physically active than the other groups. The reduced quality of life for the dizzy control group may be explained by the greater impact of PTSD, anxiety, and depression compared to the other groups. Additionally, a larger percentage of participants in the dizzy control group (48%) had a history of mTBI compared to the vestibular groups (29%) or the Non-Dizzy Control group (0%). These findings are consistent with previous studies that suggest symptoms associated with TBI, including dizziness and imbalance, are often mediated by PTSD or depression and anxiety [e.g., Ref. 54]. It is important to note that history of mTBI was used as a covariate in the analyses and was not significantly related to any of the quality of life or postural stability measures.

Limitations

A limitation of this study was the use of the caloric test alone rather than both calorics and lateral canal vHIT for classification of hSCC dysfunction. Lateral vHIT was performed on 70 of 75 control participants (93%) and the results were normal for these participants. It is possible, therefore, that up to five of the participants in the control groups had abnormal lateral canal vHIT gain in conjunction with normal caloric test results. The low proportion of participants with a potential combination of abnormal lateral canal vHIT and normal calorics (<7%) is consistent with the literature. Specifically, two studies of large series of consecutive patients identified abnormal lateral canal vHIT and normal calorics in less than 5% of patients.^55,56

Another limitation of this study is that the Otolith + Canal group had a greater number of participants with bilateral vestibular involvement compared to the isolated end-organ groups (Otolith Only and Canal Only). This grouping difference was unexpected and may suggest that having more widespread vestibular involvement (i.e., otolith and canal) is associated with greater incidence of bilateral deficits. It is unclear if the performance deficits in the Otolith + Canal group were driven by additional organ involvement (i.e., otolith) or bilateral involvement. We provide information about unilateral versus bilateral loss, but the low sample size limits statistical comparisons. Compared to unilateral semicircular canal loss bilateral loss results in greater postural instability, higher incidence of falls and lower quality of life [e.g., 12,57]; however, we do not know the functional impact of unilateral versus bilateral otolith organ dysfunction which should be the focus of future research.

The power analysis was based on planned comparisons using simplified groupings (e.g., vestibular vs control) and did not account for the full complexity of the final ANCOVA model involving five groups and four covariates. As such, the analysis may be underpowered for detecting smaller effects between all five individual groups. The sample size was further influenced by the anticipated distribution of diagnostic subtypes, which informed the decision to oversample the Canal Only group. While the sample is sufficient to characterize the control groups and larger vestibular subgroups, comparisons involving the smallest groups should be interpreted with appropriate caution.

Conclusions

Similar to isolated canal dysfunction, isolated otolith organ dysfunction may negatively impact quality of life but not postural stability. In contrast, more widespread vestibular damage, which frequently involves multiple end-organs and/or bilateral involvement of both the otolith and semicircular canal pathways has a negative impact on postural stability. These findings suggest that inclusion of otolith organ assessment (VEMPs) is critical in the management of individuals with vestibular disorders. Future work should examine whether treatment approaches should be adjusted based on vestibular site-of-lesion or the extent of damage to the vestibular pathways.

Supplemental Material

Supplemental Material - Distinguishing Pedohebephebophilic Actors and Non-Actors: A Meta-Analysis

Supplemental Material for Impact of otolith dysfunction on postural stability and quality of life: A prospective, case-control study by Courtney D. Hall, Mark Dula, and Faith W. Akin in Journal of Vestibular Research

Footnotes

Acknowledgments

RTI International provided statistical support and data analyses were performed by Barry S. Eggleston, MS, Elizabeth V. Fogleman, BSPH, and Tracy L. Nolen, DrPH. Additional statistical analyses were performed by Mark Dula, PhD. We acknowledge the efforts of the entire CENC Study 8 core team members with special thanks for their dedication to Richard Atlee, DPT and Jennifer Sears, AuD. This material is based upon work supported with resources and the use of facilities at James H. Quillen VAMC, Mountain Home, TN. We appreciate the participants who volunteered their time to contribute to this study.

ORCID iD

Courtney D. Hall

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This material is based upon work supported by the U.S. Army Medical Research and Material Command and from the U.S. Department of Veterans Affairs [Chronic Effects of Neurotrauma Consortium] under Award No. W81XWH-13-2-0095. The views, opinions, and/or findings expressed in this publication are those of the authors and should not be construed as an official Veterans Affairs or Department of Defence position, policy, or decision.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Data Availability Statement

The dataset generated during the study protocol may be available by request from the Chronic Effects of Neurotrauma Consortium (CENC) at CENC_Research@rtiresearch.org in accordance with the policy established by the CENC Research Committee.

Supplemental Material

Supplemental material for this article is available online.

References

Colebatch

Halmagyi

. Vestibular evoked potentials in human neck muscles before and after unilateral vestibular deafferentation. Neurology 1992; 42: 1635–1636.

Sheykholeslami

Kaga

. The otolithic organ as a receptor of vestibular hearing revealed by vestibular-evoked myogenic potentials in patients with inner ear anomalies. Hear Res 2002; 165: 62–67.

Iwasaki

Chihara

Smulders

, et al. The role of the superior vestibular nerve in generating ocular vestibular-evoked myogenic potentials to bone conducted vibration at Fz. Clin Neurophysiol 2009; 120: 588–593.

Todd

NPM

Rosengren

Colebatch

. A utricular origin of frequency tuning to low-frequency vibration in the human vestibular system? Neurosci Lett 2009; 451: 175–180.

Ernst

Basta

Seidl

, et al. Management of posttraumatic vertigo. Otolaryngol Head Neck Surg 2005; 132: 554–558.

Pelosi

Schuster

Jacobson

, et al. Clinical characteristics associated with isolated unilateral utricular dysfunction. Am J Otolaryngol 2013; 34(34): 490–495.

Schönfeld

Helling

Clarke

. Evidence of unilateral isolated utricular hypofunction. Acta Otolaryngol 2010; 130: 702–707.

McCaslin

Jacobson

Grantham

, et al. The influence of unilateral saccular impairment on functional balance performance and self-report dizziness. J Am Acad Audiol 2011; 22: 542–549.

Murray

Hill

Phillips

, et al. The influence of otolith dysfunction on the clinical presentation of people with a peripheral vestibular disorder. Phys Ther 2007; 87: 143–152.

10.

Jacobson

Piker

Hatton

, et al. Development and preliminary findings of the dizziness symptom profile. Ear Hear 2019; 40: 568–576.

11.

Karabulut

Van Laer

Hallemans

, et al. Chronic symptoms in patients with unilateral vestibular hypofunction: systematic review and meta-analysis. Front Neurol 2023; 14: 1177314.

12.

Herdman

Blatt

Schubert

, et al. Falls in patients with vestibular deficits. Am J Otol 2000; 21: 847–851.

13.

Karabulut

Avci

Yalçınkaya

, et al. Chronic unilateral vestibular hypofunction: a qualitative study exploring the full spectrum of symptoms and impacts through the ICF framework. Front Neurol 2025; 16: 1589404.

14.

Patel

Arshad

Roberts

, et al. Chronic symptoms after vestibular neuritis and the high-velocity vestibulo-ocular reflex. Otol Neurotol 2016; 37: 179–184.

15.

Akin

Murnane

Tampas

, et al. The effect of noise exposure on the cervical vestibular evoked myogenic potential. Ear Hear 2012; 33: 458–465.

16.

Scherer

Burrows

Pinto

, et al. Evidence of central and peripheral vestibular pathology in blast-related traumatic brain injury. Otol Neurotol 2011; 32: 571–580.

17.

Serrador

Lipsitz

Gopalakrishnan

, et al. Loss of otolith function with age is associated with increased postural sway measures. Neurosci Lett 2009; 465: 10–15.

18.

Stewart

Holt

Altschuler

, et al. Effects of noise exposure on the vestibular system: a systematic review. Front Neurol 2020; 11: 593919.

19.

Murray

Hill

Phillips

, et al.

Does otolith organ dysfunction influence outcomes after a customized program of vestibular rehabilitation?

J Neurol Phys Ther 2010; 34: 70–75.

20.

Vitale

Cotch

Sperduto

. Prevalence of visual impairment in the United States. JAMA 2006; 295: 2158–2163.

21.

Folstein

McHugh

. “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975; 12: 189–198.

22.

Crum

Anthony

Bassett

, et al. Population-based norms for the mini-mental state examination by age and educational level. JAMA 1993; 269: 2386–2391.

23.

Curthoys

. A critical review of the neurophysiological evidence underlying clinical vestibular testing using sound, vibration and galvanic stimuli. Clin Neurophysiol 2010; 121: 132–144.

24.

Akin

Murnane

Hall

, et al. Vestibular and balance function in veterans with chronic dizziness associated with mild traumatic brain injury and blast exposure. Front Neurol 2022; 13: 930389.

25.

Jongkees

LBW

. Value of the caloric test of the labyrinth. Arch Otolaryngol Head Neck Surg 1948; 48: 402–417.

26.

Chen

Halmagyi

. Video head impulse testing: from bench to bedside. Semin Neurol 2020; 40: 005–017.

27.

Hall

Herdman

. Reliability of clinical measures used to assess patients with peripheral vestibular disorders. J Neurol Phys Ther 2006; 30: 74–81.

28.

Powell

Myers

. Activities-specific balance confidence scale. J Gerontol A Biol Sci Med Sci 1995; 50A: M28–M34.

29.

Lajoie

Gallagher

. Predicting falls within the elderly community: comparison of postural sway, reaction time, the berg balance scale and the Activities-specific balance Confidence (ABC) scale for comparing fallers and non-fallers. Arch Gerontol Geriatr 2004; 38: 11–26.

30.

Jacobson

Newman

. The development of the dizziness handicap inventory. Arch Otolaryngol Head Neck Surg 1990; 116: 424–427.

31.

Whitney

Wrisley

Brown

, et al.

Is perception of handicap related to functional performance in persons with vestibular dysfunction?

Otol Neurotol 2004; 25: 139–143.

32.

Telian

Shepard

Smith-Wheelock

, et al. Habituation therapy for chronic vestibular dysfunction: preliminary results. Otolaryngol Head Neck Surg 1990; 103: 89–95.

33.

Alghwiri

Whitney

Baker

, et al. The development and validation of the vestibular activities and participation measure. Arch Phys Med Rehabil 2012; 93: 1822–1831.

34.

Nashner

Peters

. Dynamic posturography in the diagnosis and management of dizziness and balance disorders. Neurol Clin 1990; 8: 331–349.

35.

Wrisley

Marchetti

Kuharsky

, et al. Reliability, internal consistency, and validity of data obtained with the functional gait assessment. Phys Ther 2004; 84(84): 906–918.

36.

Marchetti

Whitney

Blatt

, et al. Temporal and spatial characteristics of gait during the dynamic gait index in people with and without balance or vestibular disorders. Phys Ther 2008; 88: 640–651.

37.

Groll

Bombardier

, et al. The development of a comorbidity index with physical function as the outcome. J Clin Epidemiol 2005; 58: 595–602.

38.

Sheikh

Yesavage

. Geriatric depression scale (GDS). Recent evidence and development of a shorter version in clinical gerontology. Clin Gerontol 1986; 5: 165–173.

39.

Pachana

Byrne

Siddle

, et al. Development and validation of the geriatric anxiety inventory. Int Psychogeriatr 2007; 19(19): 103–114.

40.

Washburn

Smith

Jette

, et al. The Physical Activity Scale for the Elderly (PASE): development and evaluation. J Clin Epidemiol 1993; 46: 153–162.

41.

Jones

Rikli

Beam

. A 30-s chair-stand test as a measure of lower body strength in community-residing older adults. Res Q Exerc Sport 1999; 70: 113–119.

42.

Blanchard

Jones-Alexander

Buckley

, et al. Psychometric properties of the PTSD checklist (PCL). Behav Res Ther 1996; 34: 669–673.

43.

Yip

Strupp

. The dizziness handicap inventory does not correlate with vestibular function tests: a prospective study. J Neurol 2018; 265: 1210–1218.

44.

Farrell

Rine

. Differences in symptoms among adults with canal versus otolith vestibular dysfunction: a preliminary report. ISRN Rehabil 2014; 2014: 1–10.

45.

Sestak

Maslovara

Zubcic

, et al. Influence of vestibular rehabilitation on the recovery of all vestibular receptor organs in patients with unilateral vestibular hypofunction. NeuroRehabilitation 2020; 47: 227–235.

46.

Bermúdez Rey

Clark

Wang

, et al. Vestibular perceptual thresholds increase above the age of 40. Front Neurol 2016; 7: 162.

47.

Agrawal

Carey

Della Santina

, et al. Disorders of balance and vestibular function in US adults: data from the National Health and Nutrition Examination Survey, 2001-2004. Arch Intern Med 2009; 169: 938–944.

48.

Kaski

Herron

Nachev

. Deconstructing dizziness. Front Neurol 2021; 12: 664107.

49.

Fujimoto

Murofushi

Chihara

, et al. Effects of unilateral dysfunction of the inferior vestibular nerve system on postural stability. Clin Neurophysiol 2010; 121: 1279–1284.

50.

Curthoys

MacDougall

Vidal

, et al. Sustained and transient vestibular systems: a physiological basis for interpreting vestibular function. Front Neurol 2017; 8: 117.

51.

Grove

Whitney

Pyle

, et al. Instrumented gait analysis to identify persistent deficits in gait stability in adults with chronic vestibular loss. JAMA Otolaryngol Head Neck Surg 2021; 147: 729–738.

52.

Krebs

Goldvasser

Lockert

, et al.

Is base of support greater in unsteady gait?

Phys Ther 2002; 82: 138–147.

53.

Jeong

Jung

Lee

, et al. Effects of saccular function on recovery of subjective dizziness after vestibular rehabilitation. Otol Neurotol 2017; 38: 1017–1023.

54.

Hoge

McGurk

Thomas

, et al. Mild traumatic brain injury in U.S. soldiers returning from Iraq. N Engl J Med 2008; 358: 453–463.

55.

Rambold

. Prediction of short-term outcome in acute superior vestibular nerve failure: three-dimensional video-head-impulse test and caloric irrigation. Int J Otolaryngol 2015; 2015: 639024.

56.

van Esch

Nobel-Hoff

van Benthem

, et al. Determining vestibular hypofunction: start with the video-head impulse test. Eur Arch Otorhinolaryngol 2016; 273: 3733–3739.

57.

Sun

Ward

Semenov

, et al. Bilateral vestibular deficiency: quality of life and economic implications. JAMA Otolaryngol Head Neck Surg 2014; 140: 527–534.

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