Analysis of vestibular-evoked myogenic potentials in the vestibular migraine

Belgin Tutar; Güler Berkiten; Onur Akan; Ziya Saltürk; Berk Gürpinar; Semih Karaketir; Tolgar Lütfi Kumral; Yavuz Uyar; Ömür Biltekin Tuna

doi:10.4103/NSN.NSN_4_20

ORIGINAL ARTICLE

Year : 2020 | Volume : 37 | Issue : 2 | Page : 63-69

Analysis of vestibular-evoked myogenic potentials in the vestibular migraine

Belgin Tutar¹, Güler Berkiten¹, Onur Akan², Ziya Saltürk¹, Berk Gürpinar¹, Semih Karaketir¹, Tolgar Lütfi Kumral¹, Yavuz Uyar¹, Ömür Biltekin Tuna¹
¹ Department of ENT (Ear, Nose and Throat), Okmeydani Education and Research Hospital, Istanbul, Turkey
² Department of Neurology, Okmeydani Education and Research Hospital, Istanbul, Turkey

Date of Submission	12-Sep-2019
Date of Decision	31-Mar-2020
Date of Acceptance	06-Apr-2020
Date of Web Publication	29-Jun-2020

Correspondence Address:
Belgin Tutar
Department of ENT (Ear, Nose and Throat), Okmeydani Education and Research Hospital, Istanbul
Turkey

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/NSN.NSN_4_20

Abstract

Objectives: The objective of this study is to determine the subclinical vestibular dysfunction of patients with vestibular migraine (VM) in the interattack period who had no vestibular symptoms. We assessed ascending utricular and descending saccular pathways using cervical vestibular-evoked myogenic potentials (cVEMP) and ocular vestibular-evoked myogenic potentials (oVEMP) in patients with VM and a healthy control group and then compared the electrophysiologic findings with each other. Materials and Methods: Between January 2017 and January 2018, 116 patients (aged 18–62 years) were enrolled in the study. The study group consisted of 68 women with VM and the control group comprised 48 healthy women. Results: For cVEMP findings, the mean left ear P1 latency of the VM group was statistically significantly longer than that of the control group (P = 0.024; P < 0.05). No statistical significance was found in left ear N1 latency, P1-N1 interpeak intervals and mean amplitudes between the VM and the control groups (P > 0.05). Amplitude asymmetry ratios (AARs) were not statistically significantly different between the two groups in cVEMP (P > 0.05). In terms of oVEMP findings, no statistically significant difference was found in the right ear parameters of N1, P1, P1-N1 intervals, and amplitudes of the VM and the control groups (P > 0.05). The left ear oVEMPs of the VM group showed absent responses in 12 cases and were statistically significant compared with the control group (P = 0.037; P < 0.05). The AARs were significantly greater for the the VM group than the control group in oVEMP (P = 0.006; P < 0.05). Conclusion: These electrophysiologic findings suggest that peripheral vestibular structures such as the utricle, saccule and also other central vestibular structures might be affected in VM. Patients with VM had subclinical vestibular dysfunction despite being in the interattack period. To support the diagnosis of VM, VEMPs are easy and cost-effective tests.

Keywords: Electrophysiology, evoked potentials, migraine

How to cite this article:
Tutar B, Berkiten G, Akan O, Saltürk Z, Gürpinar B, Karaketir S, Kumral TL, Uyar Y, Tuna &B. Analysis of vestibular-evoked myogenic potentials in the vestibular migraine. Neurol Sci Neurophysiol 2020;37:63-9

How to cite this URL:
Tutar B, Berkiten G, Akan O, Saltürk Z, Gürpinar B, Karaketir S, Kumral TL, Uyar Y, Tuna &B. Analysis of vestibular-evoked myogenic potentials in the vestibular migraine. Neurol Sci Neurophysiol [serial online] 2020 [cited 2023 May 29];37:63-9. Available from: http://www.nsnjournal.org/text.asp?2020/37/2/63/288420

Introduction

Migraine is a frequent disease characterized by unilateral, recurrent and pulsatile headaches. Published data support the concomitance of vestibular disorders and migraines.^[1] Sometimes, vertigo may be the first symptom; hence, the term vestibular migraine (VM) is used to refer to this disease.^[2] VM has gained importance as a frequent cause of episodic vertigo, affecting up to 1% of the general population with a female preponderance.^[3],[4]

The pathophysiology of VM is uncertain. The pathology can be anywhere in the vestibular system, such as the inner ear receptor organs, eight nerve, medulla oblongata, thalamus, vestibular cortex, vestibulocerebellum and/or central pathways to the vestibular and oculomotor nuclei. Vertigo may be caused by an over- or under-activation of the peripheric or central vestibular system resulting from a tonic imbalance between those structures.^[5],[6],[7]

An abnormal brain sensitization leading to the dislocation of the multimodal sensory integration in the thalamocortical interpretation may interact with the trigeminovascular reflex. Abnormal processing of the vestibular and nociceptive inputs may determine transient vestibular dysfunction with the properties of migraines.^[8]

Vertiginous symptoms of VM are initiated spontaneously or positionally and are visually induced or exacerbated by the movements of the head. Episodes are variable; in 30% of cases, the attacks last for minutes, in 30% for hours and in 30% for days. Ten percent have symptoms that last for only several seconds after visual stimulation or a change in the head position.^{[2],[3],[4],[5]} Phonophobia, visual aura, and related symptoms may occur before with or after vestibular symptoms. Phonophobia is always bilateral and transient, whereas visual auras are characterized by bright lights or zigzag patterns. Both last approximately 5–20 min and never exceed 60 min.^[7],[8] In the interattack period, patients usually do not have vestibular symptoms. VM is diagnosed according to the International Classification of Headache Disorders (ICHD; 3^rd edition updated in 2013).^[9]

Vestibular-evoked myogenic potentials (VEMPs) are electrophysiologic tests used to describe the sacculo-collic (cervical VEMP [cVEMP]) or the utriculo-ocular (ocular VEMP [oVEMP]) reflex pathways. Currently, VEMP is accepted as a reliable method to assess subclinical vestibular involvement.^{[10],[11],[12],[13]}

The aim of our study was to analyze electrophysiologic parameters (oVEMP and cVEMP) in patients with VM during the interattack period and to reveal misdiagnosed cases.

Materials and Methods

Patients

Between January 2017 and January 2018, 116 patients (aged 18–62 years) were enrolled in the study. The study group consisted of 68 women with VM and the control group comprised 48 healthy women.

Inclusion criteria

Sixty-eight women who were diagnosed as having VM according to the diagnostic criteria of the Barany Society and the International Headache Society (2013 ICHD appendix, 3^rd edition) were enrolled in the study. All patients with VM were newly diagnosed and were not under the treatment of any kind. The patients with VM were in the interattack interval and had no vestibular symptoms.

Exclusion criteria

Patients with benign paroxysmal positional vertigo, Meniere's disease, neurologic disease, and chronic otitis media were excluded from the study.

The control group had no neurologic or vestibular symptoms. All patients received a detailed otolaryngologic examination and had normal otoscopic and audiologic findings. The VM characteristics of the patients were determined [Table 1]. Patients were initially examined using video nystagmography and VEMP.

Table 1: Distribution of the symptoms according to the characteristics of migraine

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The local ethics committee approved this study (25.12.2017, 48670771-000-19293), and verbal consent was obtained from the participants.

Vestibular-evoked myogenic potential protocol

All patients received cVEMP and oVEMP to assess their vestibular symptoms (ICS-Chartr EP 200 evoked potentials system, Otometrics North America, Schaumburg, IL, USA). The VM and control groups were compared using VEMP waves: cVEMP (P1, N1), oVEMP (N1, P1) latencies, amplitudes, and amplitude asymmetry ratio (AAR, determined as AAR =100 × (Ar − Al)/(Ar + Al) (Ar: Right amplitude; Al: Left amplitude). An ICS medical insert earphone (ER 3A/5A Insert Earphone, 300 ohms) was used in both oVEMP and cVEMPs for acoustic stimulation). The AAR peak limit has been defined as 34.2% in cVEMP, and as 35% in oVEMPand values greater than this limit were defined as abnormal.^[14],[15] Impedance differentiation was held below 3 kOhm between the electrodes. Air conductive 97 db, rarefaction polarity, and 500 Hz tone-burst stimuli (2 ms rise/fall time, 0 ms plateau) were used on all patients and controls. The band permeability was 2 Hz-500 Hz filtered, 5/s frequency.

Cervical-vestibular-evoked myogenic potential

All patients were positioned in the sitting position. Active electrodes were placed over the mid-third of the sternocleidomastoid muscle, the reference electrode was placed over their sternum, and the ground electrode was aligned with the nasion, close to the hairline along the midline. Participants rotated their heads toward the contralateral side of the stimulated ear. If they felt fatigued, they were allowed a short rest. As the stimulus was given, the initial negative-positive biphasic waveform comprised peaks P1 (positive) and N1 (negative) [Figure 1]a.

Figure 1: (a) Cervical vestibular-evoked myogenic potential showing normal responses in both sides. (b) Ocular-vestibular-evoked myogenic potential showing normal responses in both sides

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Ocular-vestibular-evoked myogenic potential

Tests were performed in the sitting position. Patients were asked not to contract their facial muscles but to keep them relaxed while looking at a 30°–40° in an upward direction. As the stimulus was given, they were asked to gaze at a predetermined point two meters away while keeping their head position constant. Concurrently, recordings were made from their contralateral eyes. Active electrodes were placed 1 cm infraorbital, the reference electrode 3 cm infraorbital and the ground electrode on the forehead. As the stimulus was given, the peaks of the first biphasic waveform were determined as negative (N1) and positive (P1) [Figure 1]b.

Statistical analysis

Statistical analysis was performed using the Statistical Package for the Social Sciences v22.0 (IBM SPSS, Turkey) software package. Continuous data are presented as mean ± standard deviation, and statistical significance was accepted when P < 0.05. Intergroup quantitative normal parametric data were evaluated using Student's t-test. Intragroup left and right ear data were compared using the paired sample t-test. Qualitative data were evaluated using Fisher's exact test continuity (Yates) and McNemar's test.

Results

The average age was 40.59 ± 9.06 years in the study group and 44.75 ± 8.86 years in the control group. There was no statistical difference in age between the VM and control groups.

Cervical-vestibular-evoked myogenic potential findings

There were absent responses in 8 (11.8%) right ears and in 4 (5.9%) left ears in the VM group [Table 2] [Figure 2]a. The mean left ear P1 latency of the VM group was significantly longer than that of the control group (P = 0.024; P < 0.05). No statistically significant results were found for left ear N1 latency, P1-N1 interpeak intervals and mean amplitudes between the VM and the control groups (P > 0.05). AARs were not statistically significant between the two groups in cVEMP (P > 0.05) [Table 3].

Table 2: Vestibular-evoked myogenic potentials responses in vestibular migraine and control groups

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Figure 2: (a) Cervical-vestibular-evoked myogenic potential showing no response in the right side of a patient with vestibular migraine. (b) Ocular vestibular-evoked myogenic potential showing no response in the right and left sides of a patient with vestibular migraine

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Table 3: Vestibular migraine and control group cervical-vestibular-evoked myogenic potentials and ocular-vestibular-evoked myogenic potentials findings

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Ocular-vestibular-evoked myogenic potential findings

No significance was found for the right and left parameters N1, P1, and P1-N1 intervals and amplitudes of the VM and control groups (P > 0.05) [Table 3]. The left ear oVEMPs of the VM group showed absent responses in 12 patients and were statistically significant compared with the control group (P = 0.037; P < 0.05) [Figure 2]b. The AARs were significantly greater for the VM group than for the control group in oVEMP (P = 0.006; P < 0.05).

Although a cVEMP AAR higher than 34% was measured in 41.17% (n = 28) of patients, there was no statistically significant difference between the two groups in terms of cVEMP AAR (P > 0.05). An oVEMP AAR higher than 35% was measured in 55.8% (n = 38) of patients. No unilateral potential was detected in 17.6% (n = 12) of the patients and eight patients had no bilateral response. The AAR in the VM group was significantly higher than in the control group in oVEMP (P = 0.006; P < 0.05) [Table 4].

Table 4: Vestibular migraine and control group amplitude asymmetry ratios

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Discussion

cVEMP and oVEMP are helpful tools for researchers in the search to understand the underlying pathophysiology of the vestibular system. Recent studies are increasingly supportive of electrophysiologic tests in the differentiation of VM from other causes of vestibular dysfunction; however, the etiologies of VM, whether peripheral or central, are controversial.^{[11],[16],[17]} cVEMP and oVEMP may locate and describe the pathology affecting the central and peripheric vestibular areas; the main mechanism is thought to be the divergence of the vestibulo-colic and vestibulo-ocular reflex pathways beyond the nerve root entry.^[18]

In the literature, cVEMP studies outnumber oVEMP studies for VM. VEMP results are controversial because each research group found different results. Murofushi et al.^[19] reported that two types of abnormal findings could be found in patients with VM in cVEMP. The first was latency prolongation, which suggests lesions in the central nervous system or in the Retro labyrinth. The second abnormality was the shift of a preferred frequency (tuning) to 1000 Hz, mainly seen in endolymphatic hydrops in the otolith organ. These findings suggest that vertigo in patients with VM could have both peripheral and central origins. Hong et al.^[17] and Kandemir et al.^[20] found no difference in latency, but Moallemi et al.^[21] reported a prolongation of P13 latency in VM. In our study, we also found that cVEMP P1 latency was prolonged.

Abnormal VEMP amplitudes in patients with VM are also reported in the literature. A decrease in the interpeak amplitude was reported in cVEMP by Baier and Dieterich ^[11] and in oVEMP by Gozke et al.^[18] Zuniga showed a decrease in the amplitude of cVEMP but no pathology in oVEMP.^[13] In our study, we found no significant decrease in either cVEMP or oVEMP amplitude.

One of the overall goals of VEMP analysis is to assess the symmetry of saccular and utricular function by comparing the right versus left sides.^[21] A lack of this symmetry could be a sign of a unilateral deficit in the vestibular system. More than half (79.4%) of the oVEMP profiles in our study included in the VM group were abnormal (absent or asymmetric) (nonresponders in oVEMP were 11.8% [n = 8] in the right ear and 17.6% [n = 12] in the left ear). Moreover, the VM group had a significantly higher rate of absent oVEMP responders compared with the control group.

Several previous reports showed absent oVEMP responses in the VM group. Boldingh et al.^[12] reported that they found an absent VEMP response, either unilateral or bilaterally, in 44% of patients with VM. Gozke et al.^[18] found 18.6% and Zaleski et al.^[22] determined 28% absent oVEMP responders; furthermore, 61% of patients showed VEMP abnormalities (absence or asymmetry). These results suggest a pathology within the oVEMP pathway or the ascending utriculo-ocular reflex in migraineurs.

The AAR peak limit has been defined as 34.2% in cVEMP and 35.3% in oVEMP. If the AAR is greater than the peak limit, the response is categorized as decreased and abnormal.^[14],[15] We accepted these limits in our study. Kandemir et al.^[20] and Utkur et al.^[23] reported no significant difference between the groups in terms of AAR in cVEMP testing. Our results support these findings. oVEMP AAR results were 41% in Hong et al.'s ^[17] and 50% in Zaleski et al.'s ^[22] studies. In our study, AAR was 43% in oVEMP and was statistically significant.

Conclusion

VM is characterized by asymmetric headache and vestibular symptoms associated with attacks and inter-attack periods. Its pathophysiology has not yet been fully elucidated. These electrophysiologic findings suggest that peripheral vestibular structures, such as the utricle and the saccule and other central vestibular structures might be affected in VM. Furthermore, patients with VM may have subclinical vestibular dysfunction even though they are in the inter-attack period. To support the diagnosis of VM, VEMPs are easy and cost-effective tests.

The number of patients was adequate in our study and the tests were performed before treatment started during the inter-attack period. The patients with VM had no vestibular dysfunction.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

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