Acta Oto-Laryngologica. 2015; 135: 549–556

ORIGINAL ARTICLE

Clinical applications of correlational vestibular autorotation test

LI-CHUN HSIEH1,2*, TE-MING LIN3*, YU-MIN CHANG1, TERRY B.J. KUO1 & GHO-SHE LEE 3,4 Acta Otolaryngol Downloaded from informahealthcare.com by Hacettepe Univ. on 05/11/15 For personal use only.

1

Institute of Brain Science, School of Medicine, National Yang-Ming University, 2Department of Otolaryngology, Mackay Memorial Hospital, 3Faculty of Medicine, School of Medicine, National Yang-Ming University and 4 Department of Otolaryngology, Taipei City Hospital, Ren-Ai Branch, Taipei, Taiwan

Abstract Conclusion: The correlational vestibular autorotation test (VAT) system has the advantages of good test–retest reliability and calibrations of absolute degrees of eye movement are unnecessary when acquiring a cross correlation coefficient (CCC). The approach is able to efficiently detect peripheral vestibulopathies. Objective: A VAT has some drawbacks including poor test– retest reliability and slippage of sensor. This study aimed to develop a correlational VAT system and to evaluate the reliability and applicability of this system. Methods: Twenty healthy participants and 10 vertiginous patients were enrolled. Vertical and horizontal autorotations from 0 to 3 Hz with either closed or open eyes were performed. A small sensor and a wireless transmission technique were used to acquire the electro-ocular graph and head velocity signals. The two signals were analyzed using CCCs to assess the functioning of the vestibular ocular reflex (VOR). Results: The results showed a significantly greater CCC for open-eye versus closed-eye of head autorotations. The CCCs also increased significantly with head rotational frequencies. Moreover, the CCCs significantly correlated with the VOR gains at autorotation frequencies ‡1.0 Hz. The test– retest reliability was good (intraclass correlation coefficients ‡0.85). The vertiginous participants had significantly lower individual CCCs and overall average CCC than age- and-gender matched controls.

Keywords: Cross correlational analysis, electro-oculography, gyrometry, intraclass correlation

Introduction Clinically, many tests are used to assess vestibular functioning including optokinetic testing, caloric testing, rotational chair testing, and head impulse testing [1–3]. However, the diagnostic procedures often produce discomfort including dizziness, vertigo, and vomiting [4,5]. The bithermal caloric test remains the mainstay of vestibular function testing [6] and is a reliable parameter for treatment [7]. However, caloric testing is a low frequency (0.025 Hz) stimulus [3]. The vestibular autorotation test (VAT) was developed in the 1980s [8]. The test acquires the signals of eye movement and active head rotation simultaneously. The gain and phase between these two signals are used to represent vestibular functioning. This type of vestibular testing is

more physiological, convenient, and has a lower cost. However, the drawbacks of the existing VAT include poor test–retest reliability [9,10] and slippage of the sensor at high-speed rotations. In addition, the calculations of gain and phase value require good calibration of eye movement signals and the conversion to frequency domain using a Fourier transformation [8]. In this study, to reduce slippage during rotation and to increase the test–retest reliability, we first developed a VAT system with a small sensor and wireless data transmission. In part A, cross correlation analysis was applied to evaluate vestibular functioning among healthy participants and then compared with the traditional gain and phase. The test–retest reliability was also evaluated to confirm the efficiency and efficacy of this system. In part B, this correlational

Correspondence: Guo-She Lee, MD PhD, Department of Otolaryngology, National Yang-Ming University, No. 155, Sec. 2, Li-Norng Street, Bei-Tou District, Taipei City 112, Taiwan. Fax: +886 2 28202190. E-mail: [email protected]; or [email protected] *These authors contributed equally to this work.

(Received 13 October 2014; accepted 1 December 2014) ISSN 0001-6489 print/ISSN 1651-2251 online  2015 Informa Healthcare DOI: 10.3109/00016489.2014.999874

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VAT system was used to detect/assess patients with peripheral vestibulopathies.

break was allowed between the different test conditions. The test sequence of the four conditions was arranged randomly and each condition was repeated once for data averaging and analysis of test–retest reliability.

Material and methods

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Part A: VAT analysis of healthy controls Subjects. Ten healthy participants, six males and four females, aged between 18 and 40 years were enrolled. None of the participants had upper respiratory tract infection 1 week before the test. A past medical history including vertigo, hearing loss, head surgery or ear surgery resulted in exclusion from this study. This study was approved by the Institutional Review Board of National Yang-Ming University (IRB 990045R). Informed consent was obtained for all participants. Hardware settings. The sensor consisted of an electronic two-axis gyrometer and two-channel electro-oculography (EOG) to record the angular velocity of the head’s pitch and yaw and to detect horizontal and vertical eye movements. The sensor was 5  2  1 cm and weighted less than 20 g, fixed to the vertex using a headband. The horizontal electrodes were placed at the outer canthi of bilateral eyes, while the vertical electrodes were placed above and below the right eye along the vertical axis of the right pupil at central gaze. The signals of head rotation and EOG were digitally sampled at the rate of 250, 500 Hz and were transmitted to a computer using wireless transmission. Calibration of gyrometer and EOG. The calibrations of the gyrometer were carried out by placing the sensor in an apparatus rotating at constant speeds of 1 Hz and 2 Hz in both horizontal and vertical plane. For the EOG calibrations, five cycles of 15 horizontal saccades and 10 vertical saccades were used to map the physical eye movement values [11]. Head autorotation. There were four test conditions, including horizontal head autorotations (head shaking) with open eyes (HO), horizontal head autorotations with closed eyes (HC), vertical head autorotations (head nodding) with open eyes (VO), and vertical head autorotations with closed eyes (VC). When the eyes were open, the participants were requested to gaze at a projected bar 1 meter in front of them during the head rotations. The sinusoidal head rotations started at about 3 Hz and then decreased gradually to an entire stop. The range of the velocities of horizontal and vertical head autorotation test were – 250 to 250(/s and –150 to 150(/s, respectively. A 2 min

Signal acquisition and processing. The signals were digitally processed via a customized program developed in LabVIEW 2010 (National Instruments, Austin, TX, USA). The signals were first bandpass filtered between 0.03 and 10 Hz using a digital Butterworth filter. The size of analytical window was 5 s, and the sliding time between windows was 0.5 s. For a single analytical window, the eye velocity was obtained by calculating the differentials of the EOG signals. The head velocity was determined by calculating the maxima of the auto-correlation function of gyrometer signals. The cross correlation coefficient (CCC) between eye velocity and head velocity was then used to evaluate the vestibular function. The CCC equation is provided below:

CCC =

∑ ( x − x )( y − y ) ∑(x − x ) ∑( y − y ) −

i

i

i

2

i

2

where xi is the eye velocity at time i, xis the mean eye velocity of the analytical window, yi is the head rotational velocity at time i, and y is the mean head rotational velocity of the analytical window. Statistical analysis. Based on head rotational speed, all data were divided into six frequency bands, namely 0.0–0.5, 0.5–1.0, 1.0–1.5, 1.5–2.0, 2.0–2.5, and 2.5– 3.0 Hz. A paired sampled t test was used to compare CCC values between the open-eye and closed-eye conditions within the same frequency group. Oneway repeated-measures analysis of variance (ANOVA) with post hoc pair-wise comparisons using the Tukey procedure was used for multiple comparisons between different frequency groups. The correlation between CCC and VOR gain was analyzed using Pearson’s correlation analysis. Intraclass correlation (ICC) analysis was used to evaluate the test–retest reliability. The statistical analysis was carried out using SPSS 12 (SPSS, Chicago, IL, USA). The results are expressed as means ± standard error of the means (SE). Statistical significance was assumed if p < 0.05. Part B: VAT analysis of individuals with peripheral vestibulopathies Subjects. The included individuals with peripheral vestibulopathies had presented at a tertiary referral

VAT using wireless technique and cross correlation analysis

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Table I. Demographic characteristics of patients with peripheral vestibulopathies. Age (years)

Gender

Diagnosis

Caloric test

1

37

F

Left vestibular neuritis

Left CP 58%

2

62

F

Left Meniere’s disease

Left CP 30%

3

61

F

Left Meniere’s disease

Left CP 38%

4

51

F

Right vestibular neuritis

Right CP 57%

5

26

F

Left vestibular neuritis

Left CP 45%

6

33

F

Right vestibular neuritis

Right CP 64%

7

42

F

Right temporal bone fracture

Right CP 74%

8

50

F

Right vestibular neuritis

Right CP 83%

9

40

F

Right vestibular neuritis

Right CP 86%

10

66

F

Left vestibular neuritis

Left CP 52%

CP, canal paresis; F, female; M, male.

were approved by the Institutional Review Board of Mackay Memorial Hospital (IRB: 11MMHIS131).

hospital with acute vertigo. History taking was performed before the tests were carried out. Vestibular neuritis was confirmed when there was a sudden onset of vertigo with observed spontaneous and/or gazeevoked horizontal nystagmus together with canal palsy, as revealed by a caloric test, where the canal paresis (CP) value was (25%. Meniere’s disease was diagnosed when there was acute vertigo and the symptoms fulfilled the criteria of the American Academy of Otolaryngology-Head and Neck Surgery [12]. Patients with cervical spine lesion or who had mental disease such that they were unable to rotate their head randomly or obey the instructions were excluded. Ten females aged from 26 to 66 years were finally enrolled. The demographic characteristics and clinical features of the 10 patients are presented in Table I. Ten ageand-gender matched healthy volunteers were included as the control group. The research protocols

A

EOG calibration, head autorotation, and signal acquisition/processing. The calibration of the EOG, head autorotation, signal acquisition, and signal processing were performed as described earlier in part A. Average CCC was defined as the mean of the CCC of the four frequency bands of (1.0 Hz. Statistical analysis. The CCCs and average CCC of the patient group were compared to those of the control group using independent samples t test for HO, HC, VO, and VC. The software used for the statistical analysis was SPSS 12. The results are expressed as means ± SE. Statistical significance was assumed if p < 0.05.

B 10.0 600 8.0

400 EOG (degree)

Gyrometry (degree/s)

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Patient no.

200 0 –200 –400

6.0 4.0 2.0 0.0

–600 –2.0 0

10

20 Time (s)

30

40

0

10

20

30

40

Time (s)

Figure 1. The horizontal head autorotation signals with closed eyes (A) and parallel electro-oculography results (B) for one participant.

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Results Part A: VAT analysis of the healthy controls

CCC. The CCCs of all participants, HO versus HC and VO versus VC, are presented in Figure 2. The CCCs with open eyes were significantly higher than those with closed eyes for all frequency bands (p < 0.05). The CCCs increased with the head rotational frequencies, especially for HC and VC. For autorotation of (1.0 Hz with both open and A

Gain and phase of VOR. The VOR gain and phase for HO versus HC and VO versus VC for all participants are presented in Figure 3. For HO and VO, the gain was 1.00 ± 0.02, 1.17 ± 0.06 (mean ± SE), respectively. The gains and phases with open eyes (HO and VO) were significantly different from those with closed eyes (HC and VC) (p < 0.05). In particular, the phase lag was >90 for HC when the frequency was 2.5 Hz in clinical

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settings. Finally, one common drawback of VAT is that autorotation usually stimulates both ears simultaneously and the side of vestibular pathologies is not easy to locate using this system.

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Conclusion In conclusion, the VAT system described here and the subsequent data analysis using CCC is able to produce high test–retest reliability and also has high efficacy when detecting peripheral vestibulopathies. Tests involving autorotation with closed eyes may be more representative of VOR function than those with open eyes. Nevertheless, more research is necessary to test the sensitivity and specificity of this system.

Acknowledgment The research was supported by a grant from the National Science Council, Taiwan (NSC 101-2314-B-010-022). Declaration of interest: There are no conflicts of interest to be declared in this research.

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[7] Strupp M, Zingler V, Arbusow V, Niklas D, Maag KP, Dieterich M, et al. Effects of methylprednisolone, valacyclovir, or the combination in vestibular neuritis. N Engl J Med 2004;351:354–61. [8] Fineberg R, O’Leary DP, Davis LL. Use of active head movements for computerized vestibular testing. Arch Otolaryngol Head Neck Surg 1987;113:1063–5. [9] Blatt PJ, Schubert MC, Roach KE, Tusa RJ. The reliability of the Vestibular Autorotation Test (VAT) in patients with dizziness. J Neurol Phys Ther 2008;32:70–9. [10] Guyot J, Psillas G. Test-retest reliability of vestibular autorotation testing in healthy subjects. Otolaryngol Head Neck Surg 1997;117:704–7. [11] Hirvonen T, Aalto H, Juhola M, Pyykkö I. A comparison of static and dynamic calibration techniques for the vestibuloocular reflex signal. Int J Clin Monit Comput 1995;12: 97–102. [12] Committee on Hearing and Equilibrium guidelines for the diagnosis and evaluation of therapy in Menière’s disease. American Academy of Otolaryngology-Head and Neck Foundation, Inc. Otolaryngol Head Neck Surg 1995;113: 181–5. [13] O’Leary DP, Davis LL. Spectral analysis of low-frequency, active-head vestibulo-ocular reflex responses. J Vestib Res 1998;8:313–24. [14] Hirvonen TP, Pyykkö I, Aalto H. A head autorotation test for patients with Meniere’s disease. Auris Nasus Larynx 1998; 25:111–19. [15] Perez N, Martin E, Garcia-Tapia R. Results of vestibular autorotation testing at the end of intratympanic gentamicin treatment for Meniere’s disease. Acta Otolaryngol 2003;123: 506–14. [16] O’Leary DP, Davis LL. Vestibular autorotation testing of Meniere’s disease. Otolaryngol Head Neck Surg 1990;103: 66–71. [17] Ng M, Davis LL, O’Leary DP. Autorotation test of the horizontal vestibulo-ocular reflex in Menière’s disease. Otolaryngol Head Neck Surg 1993;109:399. [18] Corvera J, Corvera-Behar G, Lapilover V, Ysunza A. Objective evaluation of the effect of flunarizine on vestibular neuritis. Otol Neurotol 2002;23:933–7. [19] Iida M, Hitouji K, Takahashi M. Vertical semicircular canal function: a study in patients with benign paroxysmal positional vertigo. Acta Otolaryngol Suppl 2001;545:35–7. [20] Sekine K, Imai T, Nakamae K, Miura K, Fujioka H, Takeda N. Dynamics of the vestibulo-ocular refex in patients with the horizontal semicircular canal variant of benign paroxysmal positional vertigo. Acta Otolaryngol 2004;124:587–94.

Clinical applications of correlational vestibular autorotation test.

The correlational vestibular autorotation test (VAT) system has the advantages of good test-retest reliability and calibrations of absolute degrees of...
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