Acta Oto-Laryngologica. 2013; 133: 1278–1284

ORIGINAL ARTICLE

Feasibility of simultaneous recording of cervical and ocular vestibular-evoked myogenic potentials via galvanic vestibular stimulation

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CHIH-MING CHANG1,4, YI-HO YOUNG2 & PO-WEN CHENG1,3 1

Department of Otolaryngology, Far Eastern Memorial Hospital, 2Department of Otolaryngology, National Taiwan University Hospital, 3Oriental Institute of Technology, Taipei, Taiwan and 4Institute of Biomedical Engineering, National Taiwan University

Abstract Conclusion: Simultaneous galvanic vestibular stimulation (GVS)-cervical vestibular-evoked myogenic potential (cVEMP) and GVS-ocular (oVEMP) tests yielded similar information to that obtained in individual tests. Objective: This study compared the characteristic parameters of cVEMPs and oVEMPs via GVS between individual and simultaneous recording patterns in healthy and elderly subjects. Consequently, the effectiveness of simultaneous GVS-cVEMP and GVS-oVEMP tests was assessed. Methods: A total of 24 healthy and 16 elderly subjects were enrolled in this study. All participants underwent individual cVEMP, individual oVEMP, and simultaneous cVEMP and oVEMP testing via GVS mode in a random order. The response rates and characteristic parameters of cVEMPs and oVEMPs between individual and simultaneous tests, including latencies, intervals, and amplitudes, were measured. Results: The VEMP parameters, including latencies, intervals, and amplitudes, all demonstrated no significant differences between individual and simultaneous tests (p > 0.05, paired t test), either in healthy or elderly subjects. Pearson’s correlation analyses also revealed significant positive correlations in all parameters between these two tests (p < 0.05).

Keywords: Elderly subjects, latencies, intervals, amplitudes

Introduction The cervical vestibular-evoked myogenic potential (cVEMP) test recorded from tonically contracted cervical muscles has become an important part of the neuro-otological test battery to examine the saccule function and the integrity of the descending sacculo-collic reflex (SCR) pathway since the mid1990s [1]. During recent years, the ocular vestibularevoked myogenic potential (oVEMP) test recorded on extraocular muscles has also been successfully demonstrated [2] for assessing the utricle function and the ascending crossed vestibulo-ocular reflex (VOR) pathway [3]. Three stimulation modes have been widely administered for eliciting VEMP responses in clinical use, including acoustic (air-conducted sound, ACS), mechanical (bone-conducted vibration, BCV), and galvanic (galvanic vestibular

stimulation, GVS) modes [4,5]. Through acoustic or mechanical stimulation, VEMP responses are assumed to originate from the otolithic organs and recorded on the differential muscles (i.e. neck and extraocular muscles). However, it is difficult to discriminate between labyrinthine and retrolabyrinthine lesions by the ACS- or BCV-VEMP results alone. Since the presence of a response to galvanic stimulation shows that there must be vestibular afferents activated [6], combined ACS- or BCV-VEMPs with GVS-VEMPs may further clarify the lesion site in the reflex pathway. In other words, a retrolabyrinthine lesion may cause absent VEMP responses in all stimulation modes, while a labyrinthine lesion may only affect ACS- or BCV-VEMPs [5,7]. Because galvanic VEMPs offer additional topographic information and serve as a supplementary tool for evaluating the severity and for predicting the prognosis of

Correspondence: Po-Wen Cheng MD, Department of Otolaryngology, Far Eastern Memorial Hospital, 21, Sec.2, Nanya S. Rd, Banqiao Dist, New Taipei City, Taiwan. Tel: + 886 2 89667000 ext 2833. Fax: + 886 2 77282149. E-mail: [email protected]

(Received 14 May 2013; accepted 20 June 2013) ISSN 0001-6489 print/ISSN 1651-2251 online  2013 Informa Healthcare DOI: 10.3109/00016489.2013.820345

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Simultaneous recording of GVS-cVEMPs and GVS-oVEMPs vestibular diseases [8,9], the addition of this examination to a routine vestibular function test battery might be recommended. To shorten the test time and reduce patients’ discomfort caused by galvanic stimulation, it is valuable to clarify whether the combined test can replace individual cVEMP and oVEMP tests. Previously, individual GVS-cVEMP and GVS-oVEMP tests have been widely applied in many studies [4–14], whereas recording GVS-cVEMP and GVS-oVEMP tests simultaneously has never been investigated. Hence, the present study compared the results of the simultaneous and individual GVS-cVEMP and GVS-oVEMP tests in healthy and elderly subjects to evaluate the practicability of the simultaneous GVS-cVEMP and GVS-oVEMP test. Material and methods Healthy subjects Twenty-four subjects (48 ears) younger than 60 years (12 men and 12 women; ages ranged from 20 to 56 years, with a mean of 38 years) without previous vestibular/neurotological disorders were prospectively enrolled in this study. All subjects underwent individual cVEMP, oVEMP, and simultaneous cVEMP and oVEMP testing via GVS mode in a random order. The galvanic stimulation was 5 mA in intensity and 1 ms in duration [11]. The response rate and characteristic parameters of VEMP tests were further analyzed. The characteristic parameters included latencies, intervals, and amplitudes. Elderly subjects Another 16 subjects (32 ears) older than 60 years (8 men and 8 women; ages ranged from 61 to 71 years, with a mean of 65 years) were enrolled in this study. All of them received the same aforementioned VEMP testing. Individual cVEMP test via GVS mode The examinee was in a sitting position. Electrodes for administering galvanic stimuli were placed on the mastoid process (cathode) of the tested side and forehead (anode) in all participants. Surface potentials, predominantly electromyographic (EMG) activities, were recorded (Medelec Synergy N-EP, Oxford Instrument Medicals, Surrey, UK) with Ag/AgCl electrodes. The active electrodes were placed on the upper half of the bilateral SCM muscles, with a reference electrode on the suprasternal notch, and a ground electrode on the sternum. The electrode impedance was kept under 8 kW. EMG signals were

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amplified, bandpass-filtered between 20 and 2000 Hz and monitored to maintain background muscle activity of at least 50 mV. An intensity of 5 mA with the duration of 1.0 ms was given with and without contraction of the SCM muscles. The stimulation rate was 5 Hz and the analytical period for each response was 50 ms. Responses to 128 galvanic stimuli were averaged for each run. Because the original GVS-cVEMP waveform contained large electrical artifacts, the responses obtained without muscle contraction were subsequently subtracted from those with SCM muscle contraction to provide the final GVS-cVEMP [5,11]. Individual oVEMP test via GVS mode The examinee was in a sitting position. Electrodes for delivering galvanic stimuli were placed in the same locations as for cVEMP settings. Each active electrode was placed on the face inferior to each eye, around 1 cm below the center of the lower eyelid. The reference electrodes were positioned 1–2 cm below the corresponding active ones. One ground electrode was placed over the sternum. The electrode impedance was kept under 8 kW. The EMG signals were amplified and bandpass-filtered between 1 and 1000 Hz. The participants received galvanic stimuli (5 mA, 1 ms) while they gazed up or down. The stimulation rate and analytical period were 5 Hz and 50 ms, respectively. The average of 128 responses obtained upon gazing downward was subtracted from that upon gazing upward to provide the final GVS-oVEMP [7,14]. Simultaneous cVEMP and oVEMP test via GVS mode The participant was in a sitting position. Electrodes for administering galvanic stimuli were placed as before for the individual VEMP tests. For right-sided galvanic stimulation, two electrodes were placed on the ‘right’ corresponding sites of the neck for recording right cVEMPs, while another two electrodes were situated on the ‘left’ corresponding sites of the cheek for recording right oVEMPs (Figure 1). The recording electrodes were arranged in the opposite direction for left-sided stimulation. All stimulation and recording settings were identical for simultaneous and individual tests. When the simultaneous cVEMP and oVEMP test via GVS mode was conducted, examinees were instructed to rotate their heads away from the stimulated side and gaze upward to obtain the evoked responses. Then, they were asked to keep gazing down without neck rotation to get the background responses. The background responses were subtracted from the evoked responses to provide the final GVScVEMPs and GVS-oVEMPs. Two consecutive final responses were acquired to verify the reproducibility of

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C.-M. Chang et al. Continuous variables (VEMP parameters) were evaluated by Student’s t test. Pearson’s correlation analysis was conducted for analyzing the correlation of VEMP parameters between individual and simultaneous VEMP tests. A difference was regarded as significant if p < 0.05. This study was approved by the institutional review board. Results

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Individual tests in healthy vs elderly subjects

individual and simultaneous tests, and the results of each test were averaged for further statistical analysis.

In the healthy group, all (100%) of 48 ears had clear cVEMPs and oVEMPs. In the elderly group, two subjects had bilateral absent cVEMPs and another two had bilateral absent oVEMPs. Hence, both response rates of cVEMPs and oVEMPs were 88% (28/32 ears) in the elderly group. There was a significant difference between the two age groups in terms of VEMP response rates (p < 0.05, Fisher’s exact test). After excluding 4 subjects with either absent GVScVEMPs or absent GVS-oVEMPs, the characteristic parameters of individual GVS-cVEMP and GVSoVEMP tests were compared between healthy (48 ears) and elderly (24 ears) groups. There was a significant difference in the latencies and amplitudes (p < 0.05, unpaired t test, Table I) of GVSVEMPs between both groups, but not for the interval (p > 0.05, unpaired t test, Table I).

Statistical methods

Individual vs simultaneous tests

Categorical variables (response rates) were compared either by Fisher’s exact test or by McNemar test.

Considering GVS-cVEMPs of 48 healthy ears, the response rates of individual and simultaneous tests

Figure 1. Illustration of simultaneous GVS-cVEMP and GVSoVEMP tests (with the permission of the subject). The positions for stimulating and recording electrodes are shown. cVEMP, cervical vestibular-evoked myogenic potential; GVS, galvanic vestibular stimulation; oVEMP, ocular vestibular-evoked myogenic potential.

Table I. Comparison of characteristic parameters of GVS-cVEMPs and GVS-oVEMPs between (A) healthy and (B) elderly groups of individual recordings. cVEMP Group

n (ears)

p13 latency (ms)

n23 latency (ms)

p13-n23 interval (ms)

p13-n23 amplitude (mV)

(A)

48

10.7 ± 0.8

18.6 ± 1.4

8.2 ± 1.6

121.5 ± 45.3

(B)

24

11.8 ± 1.3

19.5 ± 1.7

7.6 ± 1.4

97.1 ± 48.9

0.14

0.04

< 0.01

p value*

0.03 oVEMP

Group

n (ears)

nI latency (ms)

pI latency (ms)

nI-pI interval (ms)

nI-pI amplitude (mV)

(A)

48

7.9 ± 0.5

11.4 ± 0.7

3.5 ± 0.8

7.2 ± 4.8

(B)

24

8.9 ± 0.7

12.1 ± 1.0

3.2 ± 1.0

4.2 ± 2.9

0.14

0.01

p value*

< 0.01

< 0.01

Data are expressed as mean ± SD. cVEMP, cervical vestibular-evoked myogenic potential; GVS, galvanic vestibular stimulation; oVEMP, ocular vestibular-evoked myogenic potential. *Unpaired t test.

Simultaneous recording of GVS-cVEMPs and GVS-oVEMPs

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Table II. Comparison of characteristic parameters of GVS-cVEMPs and GVS-oVEMPs between (A) individual and (B) simultaneous recordings in healthy subjects. cVEMP Group

n (ears)

p13 latency (ms)

n23 latency (ms)

p13-n23 interval (ms)

p13-n23 amplitude (mV)

(A)

48

10.7 ± 0.8

18.6 ± 1.4

8.2 ± 1.6

121.5 ± 45.3

(B)

48

10.8 ± 1.2

18.8 ± 1.4

8.1 ± 1.5

112.0 ± 55.5

0.24

0.48

0.49

0.20

p value*

0.61

0.56

0.73

0.51

< 0.01

< 0.01

< 0.01 oVEMP

< 0.01

n (ears)

nI latency (ms)

pI latency (ms)

nI-pI interval (ms)

nI-pI amplitude (mV)

(A)

48

7.9 ± 0.5

11.4 ± 0.7

3.5 ± 0.8

7.2 ± 4.8

(B)

48

8.0 ± 0.5

11.5 ± 0.8

3.6 ± 0.8

7.5 ± 6.7

p value*

0.42

0.23

0.56

0.54

r

0.90

0.89

0.83

0.83

< 0.01

< 0.01

< 0.01

< 0.01

r

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p value†

Group

#

p value

Data are expressed as mean ± SD. cVEMP, cervical vestibular-evoked myogenic potential; GVS, galvanic vestibular stimulation; oVEMP, ocular vestibular-evoked myogenic potential; r, Pearson’s correlation coefficient. *Paired t test. †Pearson’s correlation analysis.

were identical (100%, p > 0.05, McNemar test). The p13 latencies (mean ± SD) of individual and simultaneous tests were 10.7 ± 0.8 and 10.8 ± 1.2 ms, respectively, also exhibiting a non-significant difference (p > 0.05, paired t test, Table II). The n23 latency, p13-n23 interval, and p13-n23 amplitude also had no significant difference between the two types of test (p > 0.05, paired t test, Table II). Pearson’s correlation analyses revealed a significant

positive correlation between the two VEMP tests in terms of all VEMP parameters (p < 0.05, Table II). Similarly, the parameters of GVS-oVEMPs displayed no significant difference between individual and simultaneous tests, but exhibited a significant positive correlation (Table II, Figure 2). In 32 elderly ears, the response rates of individual and simultaneous tests were also identical (88%, p > 0.05, McNemar test). The ears with absent

n23 nl Individual test pl

p13 n23

nl

Simultaneous test

pl 5 µV

50 µV

p13

5 ms cVEMP

5 ms oVEMP

Figure 2. Cervical and ocular vestibular-evoked myogenic potentials configurations triggered by galvanic stimulation (5 mA, 1 ms) in individual and simultaneous tests of a 45-year-old man.

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C.-M. Chang et al.

Table III. Comparison of characteristic parameters of GVS-cVEMPs and GVS-oVEMPs between (A) individual and (B) simultaneous recordings in elderly subjects. cVEMP Group

n (ears)

p13 latency (ms)

n23 latency (ms)

p13-n23 interval (ms)

p13-n23 amplitude (mV)

(A)

24

11.8 ± 1.3

19.5 ± 1.7

7.6 ± 1.4

97.1 ± 48.9

(B)

24

11.6 ± 1.3

19.4 ± 1.9

7.8 ± 1.5

89.5 ± 41.3

0.34

0.95

0.43

0.30

p value*

0.68

0.91

0.69

0.72

< 0.01

< 0.01

< 0.01 oVEMP

< 0.01

n (ears)

nI latency (ms)

pI latency (ms)

nI-pI interval (ms)

nI-pI amplitude (mV)

(A)

24

8.9 ± 0.7

12.1 ± 1.0

3.2 ± 1.0

4.2 ± 2.9

(B)

24

8.8 ± 0.7

12.0 ± 0.9

3.1 ± 1.0

3.8 ± 2.5

p value*

0.41

0.35

0.62

0.12

r

0.88

0.82

0.86

0.86

< 0.01

< 0.01

0.01

< 0.01

r

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p value†

Group

p value†

Data are expressed as mean ± SD. cVEMP, cervical vestibular-evoked myogenic potential; GVS, galvanic vestibular stimulation; oVEMP, ocular vestibular-evoked myogenic potential; r, Pearson’s correlation coefficient. *Paired t test. †Pearson’s correlation analysis.

GVS-VEMPs in the individual test were the same as those in the simultaneous test. After excluding 8 ears with absent GVS-VEMPs, 24 ears showed no significant differences between individual and simultaneous tests concerning all VEMP parameters (p > 0.05, paired t test), but revealed a significant positive correlation (p < 0.05, Pearson’s correlation analyses, Table III). cVEMPs vs oVEMPs In 48 ears of healthy subjects, the values of latencies, intervals, and amplitudes of GVS-cVEMPs were all significantly larger than those of GVS-oVEMPs in either individual tests or simultaneous tests (p < 0.05, paired t test). Likewise, these elevated values of GVS-cVEMP parameters over those of GVS-oVEMP were also found in 24 ears of elderly subjects (p < 0.05, paired t test). Discussion Repeated and above-threshold stimuli, including ACS, BCV, and GVS, are required for generation of VEMPs. The former two stimulate otolithic receptors and the latter activates vestibular afferents to elicit these responses [12,13]. Evoked either via ACS or BCV modes, it is suggested that cVEMPs mainly probe saccular function due to the strong projection

of saccular neurons to neck muscles, whereas oVEMPs predominantly assess utricular function because of the major projection of utricular neurons to the oculomotor system [15]. Since galvanic stimuli directly activate the vestibular afferents to generate responses, GVS-VEMPs may be applied to help define retrolabyrinthine lesions and to determine the residual function of vestibular afferents in patients with vestibular loss [16]. GVS-VEMP responses may be decreased by physiological aging deteriorations of the vestibular system. Previous studies had shown prolonged latencies and decreased amplitudes of GVS-cVEMPs and GVSoVEMPs in subjects over 60 years of age [17,18], probably attributed to age-related morphologic degenerations in the vestibular afferents, such as the decrease in the number and their caliber. To further clarify the clinical applicability of simultaneous GVS-VEMP tests in patients with retrolabyrinthine lesions, elderly subjects were enrolled in the present study because of their ongoing retrolabyrinthine degeneration [17,18]. The results of individual GVS-VEMP testing in this study reinforce evidence that aging could lead to impaired retrolabyrinthine function. To investigate whether correct GVS-cVEMP and GVS-oVEMP information could be obtained simultaneously, comparative analysis between GVS-VEMPs in both individual and simultaneous recordings was conducted. Consequently, no

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Simultaneous recording of GVS-cVEMPs and GVS-oVEMPs matter which VEMP parameter was compared, either in healthy or in elderly subjects, a significant correlation existed between individual and simultaneous recording modes. A simultaneous GVS-VEMP test can provide similar results with no significant difference compared to those obtained in individual tests. These findings indicate that GVS-cVEMPs and GVS-oVEMPs were elicited independently during the testing session and did not interfere with one another. Furthermore, both reflex pathways in simultaneous recordings may be identical to those in individual recordings. Parameter differences exist between GVS-cVEMPs and GVS-oVEMPs. In healthy and elderly subjects, wave latencies of GVS-cVEMPs were significantly longer than those of GVS-oVEMPs, possibly because of the fact that the path length of SCR is longer than that of VOR, leading to more signal transmission time causing delayed elicitation in cVEMPs than in oVEMPs. Besides, the amplitude of cVEMPs is larger than that of oVEMPs, which may be associated with the variance in the muscle bulk between neck and extraocular muscles. The use of simultaneous GVS-cVEMP and GVSoVEMP testing as opposed to individual testing has substantial benefits. For example, simultaneous GVSVEMP tests shorten testing time, which allows for patients who have difficulty maintaining steady neck or eye muscle contraction during the repeated trials to complete the examination. Therefore, simultaneous testing can be used for weak and elderly examinees, uncooperative children, or disabled patients [19]. Additional advantages of saving test time include easing the participants’ impatience for the longer testing session, avoiding exhaustion due to sustained muscle contraction, and decreasing skin pain induced by electrical stimulation. Another beneficial outcome resulting from the combination of GVS-cVEMP and GVS-oVEMP testing is its practicality. In the absence of ACSVEMP waveform, it is common to follow with GVS-VEMP testing to clarify the lesion site in the reflex pathway. In a previous study, the feasibility of simultaneous recording of cVEMPs and oVEMPs via ACS mode had been demonstrated [20]. As an ongoing study, this paper shows that simultaneous cVEMP and oVEMP testing via GVS mode not only saves time, but also yields similar results compared to individual testing. Whether the VEMPs are elicited by ACS or GVS mode, the simultaneous test saves half of the recording time when compared with the time it takes to perform both tests individually. Since the recording electrode positions for simultaneous GVS-VEMP and simultaneous ACS-VEMP tests are identical, it is convenient to further generate

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GVS-VEMPs by only substituting acoustic stimulation for galvanic stimulation without changing any electrodes. In other words, the simultaneous cVEMP and oVEMP testing via ACS and GVS mode allows for the administration of four individual examinations with only one recording set-up. To sum up, cVEMP and oVEMP data can be achieved simultaneously by ACS or GVS modes with the advantage of yielding similar results to individual tests while saving time and appealing to a broader demographic. Thus, this combined test for acquiring ACS-VEMP and GVS-VEMP can be widely applied in routine clinical practice. Conclusion The simultaneous cVEMP and oVEMP tests via GVS stimulation yielded similar information to those obtained by the individual tests. It is a convenient electrophysiological tool for accessing the integrity of the ipsilateral SCR and contralateral VOR pathways following the labyrinth with advantages of saving test time and decreasing patients’ discomfort caused by galvanic stimulation.

Acknowledgments This study was supported by a research grant from the Far Eastern Memorial Hospital (grant no. FEMH-2012-C-022). The authors thank Hillary Chiao Lee for manuscript editing. Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.

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Feasibility of simultaneous recording of cervical and ocular vestibular-evoked myogenic potentials via galvanic vestibular stimulation.

Simultaneous galvanic vestibular stimulation (GVS)-cervical vestibular-evoked myogenic potential (cVEMP) and GVS-ocular (oVEMP) tests yielded similar ...
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