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. Otol Neurotol 32:812Y817, 2011.

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

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.

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 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. 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.).

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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).

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.

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).

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).

TABLE 1.

Proposed diagnostic criteria for bilateral vestibulopathy

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.

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

Rotatory Chair Test

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

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814 RESULTS

S. KIM ET AL.

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).

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.

TABLE 2.
Patients age

Clinical characteristic and causes of bilateral vestibulopathy

Mean T SD Range p value

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

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 nie ` res disease Bilateral Me 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 51 57 21 12 4 4 1 1 14 (3) (2) (2) (3) (2) (2) 47.2 52.8 19.4 11.1 3.7 3.7 0.9 0.9 13.0

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.
Model

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

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)

5.1 64.6 17.7 13.7 63.0

100 100 100 100 100

0.525 0.823 0.589 0.586 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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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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