AM ER IC AN JOUR NA L OF OTOLARY NG OLOG Y H EA D A N D N E CK ME D I CI NE AN D SUR G E RY 3 4 ( 2 0 13 ) 49 04 9 5

Available online at www.sciencedirect.com

ScienceDirect
www.elsevier.com/locate/amjoto

Clinical characteristics associated with isolated unilateral

utricular dysfunction,,
Stanley Pelosi, MD a,, Daniel Schuster, MD a , Gary P. Jacobson, PhD b ,
Matthew L. Carlson, MD a , David S. Haynes, MD a , Marc L. Bennett, MD a ,
Alejandro Rivas, MD a , George B. Wanna, MD a
a
b

Department of Otolaryngology Head and Neck Surgery, Vanderbilt University Medical Center, Nashville, TN 37232
Department of Hearing and Speech Sciences, Vanderbilt University Medical Center, Nashville, TN 37232

ARTI CLE I NFO

A BS TRACT

Article history:

Purpose: The ocular vestibular evoked myogenic potential (oVEMP) represents the sound-

Received 8 April 2013

induced activation of extraocular muscles and is believed to originate from the utricle and
superior vestibular nerve. Isolated unilateral oVEMP abnormalities with otherwise normal
balance function test (BFT) results have not yet been characterized in a large patient series,
and their clinical significance remains unclear.
Materials and Methods: Retrospective review of adult patients with vestibular complaints at
a tertiary academic neurotologic referral center was performed. Patients with isolated
unilateral oVEMP abnormalities were identified. The prevalence of vestibular symptoms
and results of the Dizziness Handicap Inventory (DHI) and Hospital Anxiety and Depression
Scale (HADS) were compared between these patients and those with normal BFT results.
Results: Thirty-one adult patients with isolated unilateral oVEMP abnormalities were
identified (71% female, mean age 48 14 years). Presenting complaints included vertigo in
53%, non-vertiginous dizziness in 68%, postural instability in 52%, and swaying/rocking
sensation in 13%. Significant differences were observed in the percentage of patients with
postural instability (p = 0.046) and swaying/rocking sensation (p = 0.04) when comparing
the abnormal oVEMP group to patients with a normal BFT battery. No differences were
observed when comparing other symptoms, age, gender, diagnoses, and DHI/HADS scores
between groups.
Conclusion: This is the largest series to date reporting on patients with isolated unilateral
oVEMP abnormalities. Our results suggest this population may demonstrate an increased
prevalence of postural instability and swaying/rocking sensation. Other measures of
postural stability may further characterize the vestibular impairments associated with
isolated unilateral utricular dysfunction.
2013 Elsevier Inc. All rights reserved.

Outside funding?: No outside funding was provided for this project.

Conflict of interest: No conflicts of interest related to this manuscript exist amongst the authors.

Publication statement: Data from this manuscript will be presented at the 2013 Combined Otolaryngology Spring Meetings, Orlando,
Florida. The material in this manuscript is not under consideration for publication in another journal. IRB approval number: 120131.
Corresponding author. Department of Otolaryngology Head and Neck Surgery, Vanderbilt University Medical Center, Nashville, TN
37232. Tel.: + 1 615 322 6180.
E-mail address: stanley.pelosi@vanderbilt.edu (S. Pelosi).

0196-0709/$ see front matter 2013 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.amjoto.2013.04.008

AM ER IC AN JOUR NA L OF OTOLARY NG OLOG Y H EA D A N D N E CK ME D I CI N E AN D SUR G E RY 3 4 ( 2 0 13 ) 49 04 9 5

1.

Introduction

The otolith organs are sensitive to changes in linear acceleration and head tilt and are thought to play a role in postural
stability. The otoliths also have sound sensitivity, and their
activation in response to acoustic stimulation is the basis for
the vestibular evoked myogenic potential (VEMP). The cervical
VEMP (cVEMP) represents the sound-evoked attenuation of
the tonically activated sternocleidomastoid muscle (SCM)
following a high-intensity acoustic stimulus. The response is
thought to originate from the saccule [1], and it assesses the
vestibulocollic reflex (VCR), which coordinates neck muscle
contraction for head stabilization in response to movement.
Ocular VEMP (oVEMP) testing is another method of using
myogenic potentials to assess the vestibular system. The
oVEMP represents the sound-induced activation of extraocular muscles and is best recorded from beneath the contralateral eye (i.e. contralateral to the stimulated ear). This response
assesses the integrity of the vestibulo-ocular reflex (VOR),
which is mediated by the medial longitudinal fasciculus.
VEMPs have an evolving role in the diagnosis of several
vestibular disorders. Decreased or unilaterally absent cVEMP
responses may be seen in Mnire's disease, vestibular neuritis,
and vestibular schwannomas, while unilateral increased amplitudes and abnormally reduced response thresholds may be
seen in superior semicircular canal dehiscence syndrome [2].
oVEMPs can also be altered in various peripheral vestibular
disorders [2], although these responses are frequently dissociated from cVEMP abnormalities in patients with peripheral
vestibular dysfunction [36]. Both cVEMP and oVEMP responses
may be reduced or eliminated by advanced age [7].
The origin of the oVEMP has been a topic of considerable
discussion. The most recent evidence suggests that the
oVEMP in response to air-conducted sound and recorded
with strategically placed infraorbital electrodes is generated
from the utricle and superior vestibular nerve [8]. Several
anatomic studies have demonstrated that air conduction
stimuli can activate utricular afferents [9,10], and the utricle
has been shown to possess stronger projections to the
extraocular muscles than the saccule [11,12]. Additionally,
abnormalities in the static subjective visual horizontal, a
psychophysical test believed to assess utricular function, have
been found to correlate with oVEMP abnormalities [13].
Since caloric testing evaluates the function of the lateral
semicircular canal and superior vestibular nerve, while oVEMP
tests the status of the utricle and superior nerve, the presence
of a unilateral oVEMP abnormality and normal caloric responses suggests dysfunction of the utricle alone. Isolated
oVEMP abnormalities with otherwise normal balance function
test results have not yet been well-characterized, and their
clinical significance remains unclear.
We wish to further characterize the clinical presentation of
patients who are found to have isolated unilateral oVEMP
abnormalities on vestibular function testing. Other reports
have examined isolated unilateral utricle dysfunction as
tested by abnormalities in the SVV during eccentric rotation
[14,15], but to date no large series have specifically reported on
clinical symptoms in patients with isolated unilateral oVEMP
abnormalities. Our hypothesis was that because of compen-

491

sation from the contralateral utricle and central mechanisms,

vestibular symptoms and self-report measures would not
suggest a greater severity of impairment that other dizzy
patients with normal balance function test (BFT) results.

2.

Methods

After institutional review board (IRB) approval, a retrospective

chart review was performed evaluating all patients who were
diagnosed with isolated oVEMP abnormalities on vestibular
function evaluation at a tertiary academic referral center (2006
2011). These patients were compared to a group of 30 subjects
having dizziness symptoms but demonstrating normal BFT
results. All patients underwent a complete vestibular testing
battery, including electronystagmography (ENG), rotational
chair evaluation, and testing for cVEMP/oVEMP responses.
Additionally, gender, co-morbidities, nature of vestibular complaints, associated otologic symptoms (e.g. pain, hearing loss,
tinnitus), clinical diagnoses, imaging results, and scores on selfreport questionnaires (see below) were also collected. Patients
with anatomic imaging abnormalities that could potentially
account for vestibular complaints were excluded. Because airconducted stimuli alone were used to elicit the cVEMP/oVEMP
responses, patients with audiometric evidence of conductive
hearing loss were also excluded.
Electronystagmography (ENG) or videonystagmography
(VNG) assessments included ocular motility testing (e.g. tests
of gaze, pursuit, saccade and optokinetic system function),
positional and positioning tests, and either the monothermal
warm or alternate binaural, bithermal (ABBT) caloric test
using techniques previously described [16]. A significant
interaural asymmetry in monothermal testing was defined
as 10% between ears, and a significant ABBT interaural
asymmetry was 22% [16].
Rotational chair testing was similarly performed using
previously described techniques [17]. Patients were seated in a
commercially available, sinusoidal harmonic acceleration
chair (Micromedical Technologies System 2000). The chair
was in a light-proof room, and infrared VNG or ENG
techniques were used to record eye position. Rotational
chair testing was conducted at frequencies of 0.01 Hz,
0.08 Hz, and 0.32 Hz, with a maximum angular velocity of 50
degrees per second. Vestibulo-ocular reflex (VOR) gain, phase,
and symmetry were measured.
Both oVEMP and cVEMP testing was performed using a
clinical evoked potentials system (GN Otometrics ICS Charter)
and recording techniques similar to those previously described
[8,18]. For cVEMP recordings, active electrodes were applied to
the ipsilateral middle sternocleidomastoid (SCM) muscle, a
reference electrode was placed on the chin [19], and a ground
electrode was placed at the mid-frontal site. The patient was
positioned in a semi-recumbent position with the head elevated
and turned away from the stimulated ear; 500 Hz tone bursts
presented monaurally at 95 dB HL and at a rate of 5/sec were
routed through an Etymotic ER-3A insert earphone to elicit the
response from each ear. Electromyogenic (EMG) recordings
were amplified (5000), bandpass filtered (i.e. between 10 and
1500 Hz), and signal averaged (i.e. 100 msec averaging window).
A minimum of 80 samples were averaged for each waveform,

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and each tracing was replicated at least one time. The amplitude
of the P13-N23 response was then measured, and an amplitude
asymmetry greater than 47% between ears was considered to
be abnormal [20]. Background EMG activity of the SCM muscle
was not recorded, although an optimal positioning technique
for eliciting consistent cVEMP responses was used [21].
oVEMP testing was performed with active electrodes
placed in the infraorbital region 1 cm below each eye.
Reference electrodes were placed approximately 3 cm beneath the active electrode, and a ground electrode was placed
on the forehead. The patients were tested in a semirecumbent position. During signal averaging patients were
asked to stare at a target on the ceiling that forced them to
elevate their gaze ~ 30 degrees, and to maintain this gaze for
2030 seconds. The same acoustic stimulus used to record the
cVEMP was also employed for oVEMP testing. The resulting
myoelectrical activity was amplified by 100,000, bandpass
filtered between 10 and 1500 Hz, and signal-averaged over 100
milliseconds. Each oVEMP tracing represented the average of
~ 150 individual samples. A significant oVEMP N10-P15
amplitude asymmetry was defined as > 34% [19].
The Dizziness Handicap Inventory (DHI) was completed by
all patients using a paper-pencil administration format to
assess self-reported disability/handicap. The DHI asks a
patient to answer yes (4 points), sometimes (2 points),
or no (0 points) to a list of 25 questions relating how
dizziness symptoms affect their daily lives [22]. Also performed was the Hospital Anxiety and Depression Scale
(HADS), a questionnaire with seven items assessing the extent
of depression and seven which relate to anxiety. Each item on
the questionnaire is scored 03, with a score between 11 and
21 indicating significant levels of anxiety or depression [23].

Data analysis was performed using STATA software

(StataCorp LP, College Station, TX). Frequency and proportion
calculations were made for categorical variables, while
continuous variables were reported as mean and standard
deviation (SD). The chi-square test of independence (p < 0.05)
was used to compare proportions between patient and control
groups, and the Student t test (p < 0.05) was used to compare
continuous variables.

3.

Results

Thirty-one adult patients with vestibular complaints and

complete medical records were found to have isolated
unilateral oVEMP abnormalities (Table 1). Episodic spinning
vertigo was present in 55% of patients; episodes lasted
anywhere between minutes to days. Other vestibular symptoms included non-vertiginous dizziness in 68%, postural
instability (described by patients as unsteadiness, poor
balance, or imbalance) in 52%, and swaying/rocking sensation in 13% of patients. The total duration of vestibular
symptoms prior to presentation was less than 2 months in 5
patients, while the remainder had symptoms for monthsyears. Otologic symptoms were present in 26 patients (81%),
the most commonly reported being tinnitus in 21 (67%).
Amongst clinical diagnoses, the most common was migraine
in 35% of patients, followed by benign positional vertigo
(BPV), Mnire's disease, viral neurolabyrinthitis, and mal de
debarquement syndrome. In 29% of patients, no diagnosis
was assigned.
Thirty patients had normal bithermal caloric testing
results, and 1 could not be tested due to the presence of a

Table 1 Clinical characteristics of dizzy patients with abnormal oVEMP test results v. normal vestibular function tests
results.
Patient group

Gender
Age, years (mean SD)
Vestibular symptoms
Vertigo
Non-vertiginous dizziness
Postural instability
Swaying/rocking sensation
Otologic symptoms
Tinnitus
Diagnoses
Migraine
BPV
Menieres disease
Viral labyrinthitis
Mal de debarquement
No diagnosis rendered
DHI score (mean SD)
HADS score (mean SD)
Depression
Anxiety

Abnormal oVEMP results

(n = 31)

Normal vestibular function

testing battery
(n = 30)

p value

71% F
48 14

77% F
49 16

0.61 (chi-square = 0.26, df = 1)

0.47 (t-test, = 0.73, df = 55)

55%
68%
52%
13%
81%
67%

63%
60%
27%
63%
50%

0.5 (chi-square = 0.46, df = 1)

0.53 (chi-square = 0.4, df = 1)
0.046 (chi-square = 3.98, df = 1)
0.04 (chi-square = 4.14, df = 1)
0.13 (chi-square = 2.27, df = 1)
0.16 (chi-square = 1.99, df = 1)

35%
13%
13%
6%
3%
29%
32 23

23%
13%
7%
3%
53%
36 19

0.30 (chi-square = 1.08, df = 1)

1 (chi-square = 0.002, df = 1)
0.41 (chi-square = 0.67, df = 1)
0.57 (chi-square = 0.32, df = 1)

54
12% abnormal
84
36% abnormal
(n = 25)

54
12% abnormal
75
24% abnormal
(n = 25)

0.95 (t-test, t = 0.07, df = 48)

1 (chi-square = 0, df = 1)
0.35 (t-test, t = 0.95, df = 48)
0.23 (chi-square = 0.86, df = 1)

0.05 (chi-square = 3.72, df = 1)

0.48 (t-test, t = 0.71, df = 57)

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AM ER IC AN JOUR NA L OF OTOLARY NG OLOG Y H EA D A N D N E CK ME D I CI N E AN D SUR G E RY 3 4 ( 2 0 13 ) 49 04 9 5

Table 2 Clinical characteristics of patients with reduced oVEMP v. absent oVEMP responses.
Patient group
Gender
Age, years (mean SD)
Vestibular symptoms
Vertigo
Non-vertiginous dizziness
Postural instability
Swaying/rocking sensation
Otologic symptoms
Tinnitus
Diagnoses
Migraine
BPV
Menieres disease
DHI score (mean SD)
HADS score (mean SD)
Depression
Anxiety

Reduced oVEMP
(n = 13)

P value

85% F
49 12

61% F
47 16

0.16 (chi-square = 2.02, df = 1)

0.73 (t-test, t = 0.35, df = 29))

54%
85%
46%
23%
77%
77%

56%
56%
56%
6%
83%
61%

0.93
0.09
0.61
0.15
0.66
0.35

(chi-square
(chi-square
(chi-square
(chi-square
(chi-square
(chi-square

46%
15%
36 22

28%
22%
11%
29 25

0.29
0.07
0.73
0.44

(chi-square = 1.11, df = 1)
(chi-square = 3.32, df = 1)
(chi-square = 0.12, df = 1)
(t-test, t = 0.78, df = 29)

44
9% abnormal
84
36% abnormal
(n = 11)

64
14% abnormal
84
36% abnormal
(n = 14)

0.38
0.69
0.82
0.97

(t-test, t = 0.91, df = 23)

(chi-square = 0.16, df = 1)
(t-test, t = 0.22, df = 23)
(chi-square = 0.001, df = 1)

tympanic membrane perforation. All 31 patients had normal

positional/positioning tests on ENG, and all patients had
normal rotational chair testing. cVEMP response amplitudes
and thresholds were normal in all patients. Abnormal oVEMP
responses were recorded in 18 left (59%) and 13 right ears
(41%). Abnormalities included absent unilateral responses in
18 patients and reduced unilateral oVEMP amplitudes (> 34%
interaural amplitude asymmetry) in 13. The mean DHI score
for the cohort was 32 23points, indicating a moderate
dizziness-related handicap. Twelve percent and 36% of
patients scored abnormally on the depression domain and
anxiety portion of the HADS, respectively.
Twenty-seven patients had MRI available for review.
Reported abnormalities included one patient with a left
temporal lobe vascular malformation, another with evidence
of a prior left temporoparietal lobe ischemic infarct (but with
sparing of the parieto-insular vestibular cortex), and 2 patients
with mild diffuse white matter changes. No patients had MRI
abnormalities localized to the temporal bone, brainstem, or
cerebellum, which could account for vestibular symptoms.
Clinical characteristics were also recorded for 30 patients
with normal BFT results. Significant differences in the percentage of patients complaining of postural instability and swaying/
rocking sensation were observed between the isolated unilateral oVEMP response group and patients with a normal BFT
battery (Table 1). No other differences were observed when
comparing other symptoms, age, gender, diagnoses, and DHI/
HADS scores between groups. Similarly, neither symptoms nor
self-report questionnaire responses could distinguish patients
with reduced versus absent unilateral VEMP responses (Table 2).

4.

Absent oVEMP
(n = 18)

Discussion

The purpose of this study was to define the clinical

characteristics in a large population of patients with isolated
unilateral oVEMP abnormalities, and to determine whether

=
=
=
=
=
=

0.01, df
2.92, df
0.27, df
2.06, df
0.20, df
0.86, df

=
=
=
=
=
=

1)
1)
1)
1)
1)
1)

these characteristics were different from those in dizzy

patients with normal BFT results. Our results demonstrate
that patients with isolated unilateral oVEMP abnormalities
exhibit a wide range of vestibular complaints, and also that
these patients may exhibit a greater preponderance to
postural instability and swaying/rocking sensation. These
findings are in agreement with the demonstrated sensitivity
of otolith organs to head tilt [24] and their role in affecting
postural stability through contributions to the vestibuloocular and vestibulo-spinal pathways [14].
Also suggested by our results is that vestibular compensatory mechanisms in response to a loss of utricular function (or
to ongoing dysfunction) may be incomplete. Outcomes from
testing measures such as the subjective visual vertical (SVV)
have also implied that only partial compensation may occur
after a utricular insult. One study demonstrated that unilateral peripheral vestibular deafferentation (ie. labyrinthectomy) will create acute disruption of the static SVV, and while
improvement in tilt perception occurs over time, deficits may
still be evident at 6 weeks [25]. Hence in an analogous fashion,
postural instability and swaying sensation in our group of
patients with abnormal oVEMP responses may be a result of
incomplete vestibular compensation from a static utricular
defect, ongoing utricular dysfunction, or some combination of
the two.
Other clinical findings were not found to be significantly
different between patients with abnormal oVEMP responses
and those with normal BFTs. This may be explained in part by
the presence of underdiagnosed conditions not easily distinguished by BFTs in both groups. Chronic subjective dizziness
(CSD) is one such disorder which may not have been
recognized as a cause of symptoms, especially given the
high prevalence of non-vertiginous dizziness complaints and
co-morbid anxiety in each group (both symptoms of which are
hallmarks of CSD) [26]. Other clinical diagnoses may have
played a role in limiting the ability to distinguish between
patient groups as well. Vestibular migraine was the most

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common diagnosis attributed to symptoms in both groups,

although its true incidence may be called into question since
only one patient met criteria for definitive vestibular
migraine as originally described [27]. Other diagnoses attributed to patients in both groups included BPV, Mnire's
disease, viral neurolabyrinthitis. Again, however, the presence of normal ENG results in all patients suggests that these
peripheral vestibular disorders were not the primary etiology
of symptoms at the time of testing.
We did not find a significant difference between groups in
self-report measures of dizziness. It has previously been
suggested that the DHI lacks precision in distinguishing the
functional impairments associated with specific BFT abnormalities. For example, one report has shown that poorer
scores on the DHI (indicating greater dizziness-related dizziness/handicap) do not correlate with more severe BFT
abnormalities (uncompensated versus compensated peripheral vestibular weakness) [28]. Rather, DHI scores have often
been shown to correlate with factors other than objective
testing abnormalities, including somatic/autonomic complaints, anxiety and depressive symptoms, and coping
mechanisms [29]. As such, the impact of isolated utricular
dysfunction on functional handicap may be mitigated by
factors of non-vestibular origin.
To summarize, the competing influence of multiple factors
(both vestibular and non-vestibular) on dizziness complaints
limits the ability to identify functional deficits associated with
unilateral dysfunction of one vestibular end-organ based on
clinical symptoms and/or self-report questionnaires alone. It
is therefore necessary to develop and utilize more precise
indicators of the functional deficit resulting from unilateral
loss of utricular input, both acutely and following vestibular
compensation. One such measure that holds promise is
posturography, an indicator of vestibulospinal function and
postural stability. Posturography has previously been demonstrated to highlight balance deficits in patients with isolated
unilateral cVEMP abnormalities (suggesting unilateral saccular impairment) relative to healthy subjects without vestibular
impairment and normal BFTs [18]. Application of a similar
testing protocol in patients with isolated unilateral utricular
dysfunction could better characterize the functional deficits
that are likely to also exist in these patients.
Despite mounting evidence demonstrating a utricular
origin for oVEMP responses, this assertion remains controversial. It has been argued that the oVEMP response may
evaluate the utricle, utricle and saccule, or saccular afferents
in the superior vestibular nerve [8]. One potential future
investigation would be useful to determine if oVEMP abnormalities correlate with abnormal results in other known tests
of unilateral utricular dysfunction, such as subjective visual
vertical evaluation during eccentric rotation [15]. Another
potential limitation is that our population of patients with
normal balance function testing results may have been
underdiagnosed, and if other objective measures had been
performed (for instance, video head impulse testing), it is
possible that additional vestibular deficits would have been
identified. Finally, further clinical follow-up to evaluate the
efficacy of treatment strategies in this population, and also to
potentially distinguish these outcomes from other patients
with balance complaints, would also be of interest.

5.

Conclusion

This is the largest series to date reporting on patients with a

rare clinical entity, isolated unilateral oVEMP abnormalities.
Our results suggest this population demonstrates an increased prevalence of postural instability and swaying/rocking sensation. Other measures of postural stability may
further characterize the vestibular impairments associated
with isolated unilateral utricular dysfunction.

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