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Otology & Neurotology

32:812Y817 2011, Otology & Neurotology, Inc.

Bilateral Vestibulopathy: Clinical Characteristics and


Diagnostic Criteria
*Seonhye Kim, *Young-Mi Oh, Ja-Won Koo, and *Ji Soo Kim
*Department of Neurology, Seoul National University College of Medicine, Seoul National University Bundang
Hospital, Gyeonggi-do; Department of Neurology, Pusan National University School of Medicine, Pusan
National University Yangsan Hospital, Yangsan; and Department of Otolaryngology, Seoul National
University College of Medicine, Seoul National University Bundang Hospital, Gyeonggi-do, Korea

Objectives: To define clinical and laboratory characteristics of


bilateral vestibulopathy (BV) and to propose diagnostic criteria
of this disorder based on clinical and laboratory findings.
Study Design: Retrospective case series review.
Materials and Methods: We recruited 108 patients with a clinical suspicion of BV based on presenting symptoms (unsteadiness or oscillopsia during locomotion) and bedside (dynamic
visual acuity or head impulse tests) and laboratory (bithermal
caloric or rotatory chair tests) findings after excluding the patients
with other disorders that may explain the symptoms. Definite
diagnosis of BV was made when the patients showed abnormal
findings on both bedside and laboratory tests in addition to the
symptoms, whereas probable diagnosis was obtained when either
the bedside or laboratory findings were abnormal along with the
symptoms.
Results: All patients had unsteadiness, and 36 (33%) reported
oscillopsia. Diminished vestibulo-ocular responses to head im-

pulse in both horizontal directions were present in 45 of the 100


patients evaluated. Dynamic visual acuity was impaired in 65
(95%) of the 68 patients who underwent testing. Fifty-one
(57%) patients showed bilateral hyporesponsiveness during bithermal caloric tests. Forty-eight (53%) patients had reduced
gain of the vestibulo-ocular reflex during rotatory chair test.
By adopting our diagnostic criteria, 93 patients (86%) were
diagnosed as having BV, definite in 49 (45%), and probable in
44 (41%).
Conclusion: The proposed diagnostic criteria encompass
the symptoms and findings of both bedside and laboratory
evaluations and may provide a valuable tool for investigating BV. Key Words: Bilateral vestibulopathyVOscillopsiaV
UnsteadinessVVertigoVVestibulo-ocular reflex.

Bilateral vestibulopathy (BV) is characterized by oscillopsia and unsteadiness, mostly during locomotion
(1Y5). Although various diagnostic tools have been proposed, BV remains a diagnostic challenge because each
diagnostic test has its own limitation without unified
diagnostic criteria. For example, absent or reduced responses during bithermal caloric stimulation have been

adopted as a diagnostic criterion of BV (6Y8). However,


because caloric stimulation corresponds to a sinusoidal
stimulus frequency of 0.003 Hz and does not reflect
natural rotational frequency of the head during locomotion (8,9), bilateral absence of caloric responses does not
necessarily indicate a complete absence of the vestibular
function (10). Reduced gain, increased phase lead, and
shortened time constants of the vestibulo-ocular reflex
(VOR) in response to low-frequency rotation are characteristic of BV (11Y14). However, the highest rotational
frequency achievable is less than 1.0 Hz in most equipment commercially available for human study (15). A
few studies embraced clinical symptoms and bedside
neurologic examinations, such as head impulse (HIT) or
dynamic visual acuity (DVA) test, for diagnosis of BV
(7,16Y20). HIT is useful in detecting vestibular hypofunction in BV (21). However, covert saccades may
conceal BV even in patients with total vestibular loss
(21). DVA has been used as an indirect indicator for

Otol Neurotol 32:812Y817, 2011.

Address correspondence and reprint requests to Ji Soo Kim, M.D.,


Ph.D., Department of Neurology, College of Medicine, Seoul National
University, Seoul National University Bundang Hospital, 300 Gumi-dong,
Bundang-gu, Seongnam-si, Gyeonggi-do, 463-707, Korea; E-mail: jisookim@
snu.ac.kr
The statistical analyses were conducted by Seonhye Kim, MD,
Department of Neurology, Seoul National University Bundang Hospital,
in consultation with Medical Research Collaborating Center Seoul
National University Hospital.
This study was supported by a grant from the Korea Health 21 R&D
Project, Ministry of Health & Welfare, Republic of Korea (A080750).
The authors report no disclosure.

812

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BILATERAL VESTIBULOPATHY
effectiveness of the VOR in stabilizing gaze during head
rotation (22,23). DVA may be a better measure of functional vestibular impairments and can be easily performed
(24). However, DVA test can display false-negative results when other mechanisms compensate for the retinal
instability during head movements (7). Accordingly, diagnosis of BV should be based on comprehensive evaluation of the vestibular function using both clinical and
laboratory findings. Nevertheless, no study has attempted
to incorporate all these clinical symptoms, bedside examination, and laboratory tests in diagnosing BV. In this
study, we propose diagnostic criteria of BV that incorporate both clinical and laboratory findings.

813

USA). Detailed methods and normative data were described


elsewhere (26).

Diagnostic Criteria of BV
We proposed our own diagnostic criteria for BV, which
incorporated symptoms (Criteria 1, unsteadiness or oscillopsia
during locomotion), results of bedside evaluation (Criteria 2,
HIT or DVA) and laboratory tests (Criteria 3, bithermal caloric
or rotatory chair tests), and absence of other causes (Criteria 4;
Table 1). Definite diagnosis of BV was made when the patients
met all 4 diagnostic criteria, whereas probable diagnosis was
obtained when the patients experienced the symptoms (Criteria 1)
without other identifiable causes (Criteria 4) and exhibited abnormal results during either the bedside (Criteria 2) or laboratory
tests (Criteria 3).

MATERIALS AND METHODS


Subjects
At the Dizziness Clinic of Seoul National University Bundang
Hospital, 108 consecutive patients with unsteadiness or oscillopsia only during locomotion had been recruited from May
2003 to February 2007. We reviewed the medical records of
the patients and performed an additional telephone interview
in 64 patients whose medical records did not include sufficient
information on the symptoms and possible causes of vestibulopathy. We especially excluded the patients with unsteadiness
or oscillopsia because of cerebellar disorders without bilateral
vestibular failure, intoxication, phobic postural vertigo, vestibular
paroxysmia, perilymph fistula, orthostatic hypotension, hyperventilation syndromes, visual disorders, and unilateral vestibular
loss (16). Most patients underwent evaluation of the vestibular
function, including HIT, bithermal caloric, and rotatory chair tests
in addition to routine neurologic and otologic examinations by the
authors (J. W. K. and J. S. K.). However, DVA was measured
only in 68 (63%) patients because it was applied only by a neurologist (J. S. K.).

Head Impulse Test


HIT was performed manually with rapid rotation of the head
of approximately 20-degree amplitude in the yaw plane. HIT was
considered abnormal if an obvious corrective saccade supplemented the inadequate slow phase in both directions (21,25).

Evaluation of Diagnostic Properties


We also compared the diagnostic yield of our criteria with
those reported previously (2,6,7,10,18,19,27). Selection of these
criteria was based on similarities of the testing methods for
bithermal caloric and rotatory chair tests. To evaluate sensitivity
and specificity of each diagnostic criteria, we plotted receiver
operating characteristic (ROC) curves with true positives on the
vertical axis (sensitivity) and false positives on the horizontal
axis (1-specificity). The area under the curve is a quantitative
measure of the test capacity. The area under the curve value of
0.5 indicates that the true-positive rate equals the false-positive
rate, and the test result is not better than a chance. Because
confirmatory tests are not available for BV, we were unable to
plot the ROC curves for our diagnostic criteria. Instead, we
estimated the sensitivity and specificity of the previously
adopted diagnostic criteria (Models 2Y6) using our own criteria
as a reference standard.

Statistical Analyses
We used t test to compare the continuous variable (age) and
W2 test for dichotomous variable (sex) between the groups.
Spearmans correlation also was used to compare the VOR gain
during rotation at 0.04 Hz and summated SPV during bithermal
caloric tests. All tests were performed using SPSS (version 15;
SPSS, Inc., Chicago, IL, USA), and p G 0.05 was considered
significant.

Dynamic Visual Acuity Test


DVA was measured with a Rosenbaum card which was held
14 inches from the eyes. Reference visual acuity was determined
during head stabilization. After then, the patient was again subjected to measurement of visual acuity, whereas the head was
oscillated approximately at 2.5 Hz in the horizontal plane with
estimated amplitudes of 10 degrees. Loss of 3 or more lines as
compared with the reference level was considered abnormal (1).

Bithermal Caloric Tests


The caloric stimuli comprised alternate irrigation for 25 seconds
with 50 ml of cold and hot water (30-C and 44-C) (25). Nystagmus
was recorded binocularly using video-oculography (NCI-480; ICS
Medical, Schaumburg, IL, USA). BV was defined by summated
slow phase velocity (SPV) of the nystagmus of less than 20 degrees
per second during 4 stimulation conditions.

Rotatory Chair Test


Rotatory chair test were performed in darkness using a
rotatory chair system (CHARTR; ICS Medical, Dallas, TX,

TABLE 1.

Proposed diagnostic criteria for


bilateral vestibulopathy

Criteria 1. Symptoms only during locomotion (either A or B)


A. Unsteadiness
B. Oscillopsia
Criteria 2. Findings of bedside evaluations (either A or B)
A. Positive head impulse test in both horizontal directions
B. Impaired dynamic visual acuity
Criteria 3. Results of laboratory tests (either A or B)
A. Reduced responses (summated slow phase velocity of the
nystagmus G20 degrees per second) during bithermal caloric
tests
B. Reduced vestibulo-ocular reflex gain during rotatory chair test
Criteria 4. Other causes excluded
Definite diagnosis: met all 4 diagnostic criteria.
Probable diagnosis: met the criteria 2 or 3 in addition to Criteria 1
and 4.
Otology & Neurotology, Vol. 32, No. 5, 2011

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814

S. KIM ET AL.
RESULTS

Demographic and Clinical Characteristics


Patients included 60 women and 48 men without difference in age between women and men (Table 2). There
was no difference in age and sex between the idiopathic
and secondary groups (Table 2). Other clinical characteristics and causes were summarized in Table 2.
Bedside and Laboratory Vestibular Function Tests
Horizontal HIT was performed in 100 patients, and 45
of them showed corrective catch-up saccades in both
directions, whereas 17 patients exhibited positive results
only unilaterally. DVA was impaired in 65 (96%) of the
68 patients tested.
Bithermal caloric tests showed reduced response in 51
(57%) of 89 patients, including no response in 4 of them.
Results of rotatory chair test were abnormal in 48 (53%)
of 91 patients (Fig. 1). All the patients with abnormal
rotatory responses exhibited reduced gain and increased
phase leads during lower (0.02 and 0.04 Hz) frequency
rotations, and most of them (n = 42 [88%]) also showed
abnormalities during higher (0.08, 0.16, and 0.32 Hz)
frequency rotations (Fig. 1). The summated SPV of the
nystagmus induced during bithermal caloric stimuli
showed a positive linear correlation with the VOR gain at
0.04 Hz during rotatory stimulation (Spearmans correlation, r = 0.670, p G 0.001; Fig. 2).

TABLE 2.

Clinical characteristic and causes of


bilateral vestibulopathy

Patients age

Mean T SD

Total (n = 108)
Men (n = 48)
Women (n = 60)
Idiopathic group (M:W = 23:21)
Secondary group (M:W = 37:27)
Clinical symptoms
Unsteadiness
Oscillopsia
Transient vertigo
Bilateral hearing loss
Tinnitus
Causes
Idiopathic
Secondary
Ototoxicity
Bilateral Menie`res disease
Bilateral sequential vestibular
neuritis
Head trauma
Bilateral chronic otitis media
Autoimmune disorder
Neurologic diseases
Central nervous system
infection
Cerebellar infarction
Cerebellar degeneration
Superficial siderosis
Tumor
Neuropathy

62.9 T 16.4
12Y88
62.7 T 17.8
12Y88
90.05
63.2 T 15.4
18Y88
65.4 T 16.5
15Y86
90.05
61.3 T 16.3
12Y88
No.
Percentage (%)
108
100
36
33
30
28
20
19
13
12

Range

51
57
21
12
4

47.2
52.8
19.4
11.1
3.7

4
1
1
14
(3)

3.7
0.9
0.9
13.0

(2)
(2)
(3)
(2)
(2)

p value

FIG. 1. Gains of the VOR in 48 patients that exhibited reduced


gains during sinusoidal harmonic accelerations. All of them
showed reduced gain at lower (0.02 and 0.04 Hz) frequency
rotations, and most of them (n = 42 [88%]) also exhibited diminished gain at higher (0.08, 0.16, and 0.32 Hz) frequency rotations.
The gray box indicates reference ranges (mean, T2 standard
deviation) of the VOR gain at each frequency.

Evaluation of Diagnostic Properties


According to our diagnostic criteria, 44 (40.7%)
patients met the definite criteria of BV, whereas 49
(45.4%) had the diagnosis of probable BV (Table 3).
Overall, definite or probable diagnosis of BV could be

FIG. 2. The summated SPV of the nystagmus induced during


bithermal caloric stimuli shows a positive linear correlation with
the gain of the VOR during sinusoidal harmonic acceleration at
0.04 Hz with a peak velocity of 50 degrees per second (r = 0.670,
p G 0.001).

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BILATERAL VESTIBULOPATHY
TABLE 3.

815

Diagnostic accuracy of our own and previously proposed criteria for bilateral vestibulopathy
Diagnosis of BV (%) Sensitivity (%)a

Model

Model 1
93/108 (86.1)
1. Unsteadiness or oscillopsia
2. DVA or HIT
3. Caloric test (reduced caloric responses G20 degrees per second)
Definite (n = 44)
or rotatory chair test (decreased gain at lower frequency stimulation: G0.2)
Probable (n = 49)
h Definite: 1 + 2 + 3 and other causes were excluded
h Probable: 1 + either 2 or 3 when other causes were excluded
Model 2 (6,7)
3/87 (3.4)
Absent caloric response
Model 3 (27)
51/87 (58.6)
Reduced caloric response (G24 degrees per second)
Model 4 (2)
4/77 (5.2)
Absent or reduced caloric response (SPV, G5 degrees per second)
+Decreased gain at low-frequency rotatory chair test
Model 5 (10)
10/77 (13.0)
Absent or reduced caloric response (SPV, G10 degrees per second)
+Decreased gain (0.1) at low-frequency rotational chair test
Model 6 (18,19)
46/79 (58.2)
HIT + absent or reduced caloric response (SPV, G5 degrees per second)
h Complete: pathologic HIT + absence of caloric response
h Incomplete;
Complete (n = 3)
1. Bilateral pathologic HIT + reduced caloric response
Incomplete (n = 43)
(SPV, G5 degrees per second)
2. Bilateral pathologic HIT + caloric responses 95 degrees per second
on 1 or both sides
3. Normal HIT + absence or reduced caloric responses (G5 degrees per second)

Specificity (%)a

AUC

5.1

100

0.525

64.6

100

0.823

17.7

100

0.589

13.7

100

0.586

63.0

100

0.815

AUC indicates area under the curve; BV, bilateral vestibulopathy; DVA, dynamic visual acuity; HIT, head impulse test; SPV, slow phase velocity.
a
Receiver operating characteristic curves were used to measure the sensitivities and specificities of the previously reported diagnostic criteria using our
own criteria as reference standards.

made using our criteria in 93 (86.1%) of 108 patients


that experienced unsteadiness or oscillopsia only during
locomotion without other identifiable disorders. When
applying the previously reported diagnostic criteria,
diagnosis of BV could be made in 3.4% to 58.6% of the
patients that underwent the tests adopted in those criteria
(Table 3). We also determined the sensitivity and specificity of the previously reported criteria using our criteria
as a reference standard (2,6,7,10,18,19,27). The sensitivity of the previous criteria ranged from 3.0 to 64.6%,
whereas the specificity was uniformly 100% (Table 3).
DISCUSSION
In this study, we proposed diagnostic criteria of BV
that incorporated clinical symptoms and results of both
bedside examination and laboratory tests. Using our criteria, we were able to diagnose BV in 86% of the patients
with oscillopsia and unsteadiness only during locomotion
after excluding the patients with other disorders that may
explain the symptoms.
In BV, the most common and most important complaints are unsteadiness and oscillopsia during locomotion. The unsteadiness typically worsens in darkness or
on uneven surfaces (5,16). Unsteadiness is a reflection
of impaired vestibulo-spinal reflex, hindering the multisensory process of postural control (28). Unsteadiness also
occurs with high-frequency head movements because detection of high-frequency head rotation is a domain of the
vestibular apparatus (28,29). Oscillopsia also occurs in BV

because of bilaterally impaired VOR that reduces stabilization of the images on the retina (retinal slip) during locomotion and head movements (1,16). All our patients
experienced unsteadiness during locomotion. However,
only 36 (33%) of them reported oscillopsia. In the previous reports, the oscillopsia also was described in only 25%
to 50% of the patients with BV (1). In patients with vestibular disorders, the degree of subjective complaints may
not follow the severity of vestibular dysfunction measured
using objective tests (1). Impaired VOR may be compensated by other mechanisms (7,30Y32).
Caloric and rotatory chair tests have been adopted
in diagnosing BV (1,2,4,6,13,14). However, absent responses during bithermal caloric stimulation does not
necessarily indicate a complete loss of the vestibular function (33). To determine any vestibular function remained,
previous studies introduced ice-water stimulation in case of
absent responses during bithermal caloric irrigation (6,7,34).
However, ice-water irrigation is unpleasant and painful and
may produce pseudocaloric nystagmus by activating latent
spontaneous nystagmus (35,36). Furthermore, there has
been no consensus on the range of responses (nystagmus)
required for diagnosis of BV during caloric stimulation
(1,27,37).
Rotatory chair test adopts more physiologic stimuli over a
broad frequency range and has been regarded a better
method for identifying patients with BV (10,13,38Y40).
However, commercially available rotatory chairs for
human study do not readily evaluate the VOR at frequencies above 1 Hz where the head usually oscillates
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816

S. KIM ET AL.

during daily activities (15,41). Thus, it would be inadequate to determine the vestibular dysfunction with only
the results of caloric or rotatory chair test. Indeed, reduced
caloric responses were observed only in 57% and decreased VOR gain in 52% of our patients with unsteadiness and oscillopsia only during locomotion.
HIT and DVA can evaluate the VOR function at the
physiologic head oscillation frequencies during locomotion (20,21,40,42). However, only a few previous studies
adopted the results of HIT or DVA for diagnosis of BV
(16Y18,43). In the present study, the sensitivity of DVA
was 96% during passive head rotation, which was higher
than that (66%Y75%) in the previous studies (1) and was
similar to that of computerized DVA (20). DVA is known
to decline with aging both in healthy persons and in
patients with BV, although there are no reference values
by age for the clinical DVA test (20). Because the average
age of our patients (63 yr) was higher than that of the
previous study (54 yr) (1), inclusion of more aged patients
may explain the higher proportion of abnormal DVA in
this study. Also, false negatives are unknown for the large
number of patients who did not have DVA test.
Our diagnostic criteria for BV improved diagnostic
yields of this disorder (Table 3). Previously, most studies
had adopted the results of only caloric or rotatory chair
test in diagnosing BV (6,7), which would have resulted
in lower sensitivity. Especially, adoption of absent responses or summated SPV below 5 degrees per second
during bithermal caloric stimulation would have lowered
the sensitivity further (Table 3). During caloric stimulation, we estimated the positive likelihood ratio of the
summated SPV using ROC with decreased gains at lower
frequency rotations as a reference standard. We found
that likelihood ratio was highest when the summated SPV
of the nystagmus was below 20 degrees per second. Thus,
we adopted the value of less than 20 degrees per second
as an indicator for decreased VOR function during bithermal caloric tests.
This study had some limitations. First of all, we determined the abnormality of HIT bedside without quantitative analyses. Bedside HIT is less sensitive than
quantitative HIT especially when the vestibular deficits
are partial (44). Also, covert saccades during HIT may
mask the corrective catch-up saccades and prevent accurate identification of the vestibular impairments (21,45).
However, bedside HIT is feasible, and the sensitivity is
clinically acceptable in the hands of both neuro-otologic
experts and nonexperts (46). Second, the function of the
vertical semicircular canals was not investigated. Given
that the vertical HIT and DVA during vertical head oscillation may evaluate the function of the vertical semicircular
canals, the findings and diagnostic use of these tests
should be validated further in BV. Finally, otolithic dysfunction remains an area of further exploration in BV. The
saccular function, as determined by cervical vestibular
evoked myogenic potential, may be impaired in BV (47).
In patients with suspected BV, cervical vestibular evoked
myogenic potential may be abnormal bilaterally in the
presence of normal caloric responses (48).

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Otology & Neurotology, Vol. 32, No. 5, 2011

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