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 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 35  |  Issue : 3  |  Page : 1593-1599

Assessment of oculomotor and vestibulo-ocular function in vestibular-migraine patients


1 Department of Otolaryngology, Faculty of Medicine, Menoufia University, Menoufia, Egypt
2 Department of Neurology, Faculty of Medicine, Menoufia University, Menoufia, Egypt
3 Department of Otolaryngology, Benha Teaching Hospital, Qalyubia, Egypt

Date of Submission05-Feb-2022
Date of Decision22-Feb-2022
Date of Acceptance27-Feb-2022
Date of Web Publication29-Oct-2022

Correspondence Address:
Marwa A Allam
Nasr City, Cairo
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/mmj.mmj_48_22

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  Abstract 


Objectives
To assess the vestibulo-ocular and oculomotor functions in vestibular-migraine (VM) patients in-between and during the attacks using video head-impulse test (vHIT) and oculomotor-function tests.
Background
Dizziness and migraine are very common complaints.
Patients and methods
This case–control study included two groups: 1 – control group consisted of 60 normal participants not complaining of any vestibular symptoms. 2 – study group consisted of 30 VM patients, which were subdivided into two subgroups: subgroup 1 was examined in-between attacks (nine patients) and subgroup 2 was examined during the attack (21 patients). The vHIT and oculomotor tests were used to assess both groups.
Results
Oculomotor abnormalities were reported in 20/30 of VM patients (67%): four (44%) patients in subgroup 1 and 16 (76%) patients in subgroup 2. vHIT abnormalities were reported in 20/30 of patients (67%): three (33%) patients in subgroup 1 and 17 (81%) patients in subgroup 2. In total, 18 patients from subgroup 2 were reevaluated after treatment, 3-month interval, and showed improvement in duration of headache, frequency of attacks, and duration of vertigo. The number of abnormalities in vHIT results decreased after treatment.
Conclusion
Abnormalities either in oculomotor-function tests or vHIT are common in VM, which were more pronounced during the attacks than in-between the attacks. The high gain was the most frequent vHIT abnormality during the attack, which shows improvement after treatment in more than half of the patients in the current study. vHIT can be used as a monitoring tool during the management of VM patients.

Keywords: vertigo, vestibular migraine, vestibulo-ocular reflex, video head-impulse test


How to cite this article:
Moaty AS, Afifi KH, Allam MA, Kabel AE. Assessment of oculomotor and vestibulo-ocular function in vestibular-migraine patients. Menoufia Med J 2022;35:1593-9

How to cite this URL:
Moaty AS, Afifi KH, Allam MA, Kabel AE. Assessment of oculomotor and vestibulo-ocular function in vestibular-migraine patients. Menoufia Med J [serial online] 2022 [cited 2024 Mar 29];35:1593-9. Available from: http://www.mmj.eg.net/text.asp?2022/35/3/1593/359509




  Introduction Top


Migraine is the most frequent neurological disease observed in clinical practice. It is defined as a primary headache disorder characterized by unilateral pulsating pain and generally produces several symptoms that can occur with or without aura[1]. Dizziness and migraine are very common complaints and a strong connection exists between them[2]. Vestibular-migraine (VM) is regarded as the second most frequent cause of recurrent vertigo and is estimated to occur in 9% of migraine patients[3].

VM patients frequently report sensitivity to head motion and visual surroundings or disabling misperceptions such as a sudden feeling of imbalance or tilt[4].

Based on the Barrany Society's Vestibular Symptom Classification, vestibular symptoms in VM patients included spontaneous vertigo, positional vertigo, visually induced vertigo, head-movement-induced vertigo, and head-movement-induced dizziness with nausea[5].

The video head-impulse test (vHIT) is a technology that measures eye movement, provides a quick and objective measure of the vestibulo-ocular reflex (VOR) in response to head movements in the natural range of daily motions, and thus evaluates the functional integrity of all the six semicircular canals of both sides[6].

Few studies assessed the VOR in VM patients during and in-between the attacks.

So, this study aimed to assess the VOR in addition to oculomotor functions in VM patients during and in-between the attacks using vHIT and oculomotor-function tests.


  Patients and methods Top


This case–control study was carried out in an Audiovestibular Clinic in Menoufia University Hospital in the period between September 2018 and September 2020. Ethical approval from the hospital committee and written consent from all the participating patients were obtained. Patients included in this study were divided into two groups: 1 – control group: consisted of 60 normal participants not complaining of any vestibular symptoms in the age range of 20–40 years. 2 – Study group (VM case group) consisted of 30 patients in the age range of 20–40 years diagnosed as VM according to International Headache Society guidelines[7]. The study group was subdivided into two subgroups: subgroup 1 was examined in-between attacks (nine patients) at least after 1 week from the last migraine or vertiginous episode and subgroup 2 was examined during the attack (21 patients), with the exclusion of patients suffering from other neurological diseases, systemic disorders, congenital nystagmus, poor vision, and cervical problems in addition to a history of the otovestibular disease.

All VM patients in the study group were subjected to the following: full history taking (1 – migraine criteria: duration of migraine attack, frequency of attack, the character of headache, association, and the received treatment. 2 – auditory symptoms: hearing loss, tinnitus, or aural fullness. 3 – vestibular symptoms: vertigo and imbalance. 4 – concurrent illness), vestibular office tests (posture and gait tests), otoscopic examination, basic audiological assessment, including pure-tone audiometry (model Madsen, Orbiter 922) and immittancemetry (Interacoustic AT235), and vestibular assessment using videonystagmography (NysStar VNG, Difra System, EUPEN, Belgium) and vHIT (HeadStar vHIT, Difra System).

Oculomotor tests included random saccades, smooth pursuit, optokinetic nystagmus testing, spontaneous nystagmus, and gaze-evoked nystagmus testing. The technique of the tests and interpretation of the results were done according to the British Society of Audiology[8].

The vHIT was used to test the function of all six semicircular canals. The results beyond the range of the normal values in our laboratory for the same age group were considered abnormal, which are 0.7–1.4 in the vertical and horizontal canals. The lateral canal was stimulated by a passive lateral head impulse at 10–20° and a velocity of 200°/s, in a neutral position, the head was inclined downward by ∼20°. Vertical-canal stimulation was achieved while the patient's head was rotated to the left for right anterior–left posterior stimulation position, and to the right for left anterior–right posterior stimulation position, 30–40° from the fixation target. Then, unpredictable passive backward and forward movements of the head with a peak head velocity of 150°/s were done. At least 20 impulses were performed for each canal. vHIT analysis depends mainly on VOR gain and the presence of refixation saccades[9].

On routine follow-up visit: patients were reevaluated after treatment, 3 months after the initial visit by history taking (duration, frequency, and intensity of attacks) and vHIT.

Statistical analysis

The results were analyzed using SPSS (SPSS Inc. Released 2015. IBM SPSS Statistics for Windows, Version 23.0; IBM Corp., Armonk, New York, USA), in which qualitative data were expressed as numbers and percentages and quantitative data were expressed as mean and SD. Student t test was used for comparison between groups having quantitative variables. χ2 test was used to study the association between two qualitative variables. Fisher exact test was used for 2 × 2 tables when the expected cell count of more than 25% of cases was less than 5. Mann–Whitney test was used for comparison between two groups having quantitative variables and independent nonparametric data. A P value of less than or equal to 0.05 was considered statistically significant.


  Results Top


There was no significant statistical difference between cases and control groups as regards age and sex distribution [Table 1].
Table 1: Demographic characteristics of the studied groups

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Migraine criteria in the VM group showed that 24 (80%) of patients had a pulsating character of headache and 20 (67%) of patients had nausea, three (10%) of patients had vomiting, and seven (23%) of patients had both nausea and vomiting. Also, 11 (37%) of patients had photophobia, six (20%) of patients had phonophobia, and 13 (43%) of patients had both photophobia and phonophobia. Migraine-attack frequency was 3.80 ± 1.47 per month and the duration of headache was 31.5 ± 24.96 h.

Audiovestibular symptoms in the VM group: six (20%) of the patients had sensorineural hearing loss, 10 (33%) of patients reported tinnitus, and 14 (47%) reported aural fullness. In total, 15 (50%) of the patients had episodes of vertigo [that was spontaneous in six (40%) patients, positional in six (40%) patients, and visually induced in three (20%) patients], also imbalance was reported in 11 (37%) of patients, and four (13%) patients had both vertigo and imbalance. The mean duration of vertiginous attack was 80.28 ± 60.35 min.

Basic audiological assessment: all the participants in this study had normal tympanic membrane and normal middle-ear function with preserved acoustic reflex. In total, 24 (80%) of the patients in this study had normal pure-tone audiometry, except six (20%) cases who had SNHL ranging from mild to a moderate degree.

All the participants in this study had a normal neurological assessment and office tests (posture and gait).

Oculomotor-test results: all the participants in the control group were within normal oculomotor results. There were statistically significant differences between control and VM subgroups regarding latency of saccade test and saccadic pursuit [Table 2]. Oculomotor abnormalities were reported in 20/30 (67%) patients: in subgroup 1: four (44%) patients had abnormalities that were gaze-test abnormality in one (11%) patient, prolonged latency of saccade test in one (11%) patient, and saccadic pursuit in three (33%) patients. But in subgroup 2: 16 (76%) patients had abnormalities that were spontaneous nystagmus in six (29%) patients, gaze-test abnormality in five (24%) patients, prolonged latency of saccade test in four (19%) patients, and saccadic pursuit in 15 (71%) patients. There was a statistically significant difference in the number of cases that showed abnormalities in saccadic pursuit between both subgroups (χ2 test, P = 0.05).
Table 2: Comparison of oculomotor tests results between the control and vestibular-migraine subgroups

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vHIT results: there was no significant statistical difference between right and left ears in both control and case groups, so ears were used in the statistical calculation. In the comparison of the gain between the two subgroups and control group, there was a statistically significant difference regarding vHIT gain of lateral and posterior canals between control versus both subgroups of VM and between both subgroups [Table 3].
Table 3: Comparison of video head-impulse test gain between control and vestibular migraine groups in-between and during the attack

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vHIT abnormalities were reported in 20/30 (67%) patients of the VM group: in subgroup 1: three (33%) patients showed a low gain, and in subgroup 2: 17 (81%) patients showed abnormal gain, either low gain in three (18%) patients or high gain in 14 (82%) patients and three cases showed overt saccades.

The distribution of abnormalities in the gain of vHIT in different canals in VM subgroups is shown in [Figure 1].
Figure 1: Distribution of the abnormalities of the gain of the video head impulse in different canals in the vestibular-migraine groups.

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The distribution of the number of affected canals is shown in [Table 4]. There was no statistically significant difference between abnormal vHIT gain and demographic characteristics: age (Student's t test, P = 0.86), sex (χ2 test, P = 0.17), and audiovestibular symptoms: Hl (Fisher exact test, P = 0.7), tinnitus, aural fullness, vertigo, and imbalance (χ2 test, P = 0.25, 0.91, 0.44, and 0.25, respectively), and migraine criteria: Ch of headache (χ2, P = 0.56), duration, and frequency of attacks (Mann–Whitney test, P = 0.10 and 0.97, respectively).
Table 4: Distribution of the number of affected canals

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In VM group: 14 (47%) patients showed abnormality in both vHIT and oculomotor tests [two (22%) in subgroup 1 and 12 (57%) in subgroup 2], six (20%) patients showed vHIT abnormalities with normal oculomotor tests [one (11%) in subgroup 1 and five (24%) in subgroup 2], six (20%) patients showed normal vHIT results with abnormal oculomotor tests [two (22%) in subgroup 1 and four (19%)] in subgroup 2, and four (13%) patients showed no abnormalities in both tests [all four (44%) patients were in subgroup 1].

On routine follow-up visits: 18 patients from subgroup 2 were reevaluated and showed improvement in their symptoms after treatment with a statistically significant difference regarding the duration of headache, frequency of attacks, and duration of vertigo (Student's t test, P value was 0.04, less than 0.001, and 0.049, respectively). [Table 5] shows the difference in vHIT gain before and after treatment with a statistically significant difference between canals before and after treatment.
Table 5: Video head-impulse test gain before and after treatment among studied patients

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The number of abnormalities decreased after treatment: 12/18 cases showed improvement and reported normal gain (10 cases changed from high gain to normal gain and two cases changed from low gain to normal gain) in different canals.


  Discussion Top


Migraine is a common chronic intermittent-headache disease that affects 15–18% of the average population. Migraine is a paroxysmal disease characterized by severe headaches, and that severity may interfere with daily activities[10].

VM is now the accepted name for vestibular symptoms that are causally related to migraines[2]. VM is widely accepted in the vestibular community and may be the second leading cause of vertigo after benign positional vertigo[10]. Oraby et al.[11] reported that migraine peaks in the late 30s to early 40s and declines during the 50s. In the current study, the mean age of migrainous patients was 28.8 ± 5.9 in subgroup 1 and 29.7 ± 4.7 in subgroup 2. Females constituted 67% of patients in the current study. Salmito and Ganança[12] reported that VM is mainly in female patients, with a ratio of 1.5: 5.1.

Twenty-four (80%) patients in the current study had a pulsating character of headache and that is in agreement with Menon and Kinnera[13] who reported that the most characteristic headache was pulsatile or throbbing, which was reported in 80% of migrainous patients. In the current study, the mean of attack duration was 31.5 ± 24.96 h. In the study conducted by Stolte et al.[14], the duration of migraine attacks ranged from a few seconds to a few minutes, a few hours, or even a few days. Most of the patients in the current study had normal hearing sensitivity, except 20% of patients who had SNHL, 33% of patients reported tinnitus, and 47% reported aural fullness. Salviz et al.[15] reported that hearing loss ranges from 11 to 18% and the rate of tinnitus varies from 20 to 53% in his VM patients.

In the current study, all the patients in the VM group had vestibular symptoms, either vertigo in 50% of patients or imbalance was in 37% of patients, or both in 13% of patients. Huang et al.[4] reported that 20–85% of VM patients had spontaneous vertigo, 18–60% had positional vertigo, and 30–80% had an imbalance. These symptoms can vary from patient to patient. In the current study, the mean duration of vertigo attacks was 80.28 ± 60.35 min. Zhang et al.[16] reported that the duration of vestibular symptoms in patients with VM varies greatly from several minutes, or several hours, or several days, and some report daily fluctuations in symptoms. The oculomotor function is usually affected in VM patients and the incidence of abnormalities is high, it may be related to the course of the disease, which increases with time[17]. Power et al.[18] reported that 8–60% of VM patients have oculomotor abnormalities. In the current study, two-thirds of VM patients showed abnormal oculomotor-function tests, and the smooth-pursuit abnormalities were the most frequently reported oculomotor abnormalities, it was reported in 60% of VM patients. Fu et al.[19] stated that smooth pursuit is one of the commonest oculomotor abnormalities in VM patients. In the current study, more oculomotor abnormalities were reported during the attacks than in-between the attacks. Lempert et al.[17] reported that the period between VM attacks for the majority of patients is characterized by free symptoms and physical examination, changes are detected during the attacks with marked central and vestibular abnormalities. Baloh[20] suggested that these variabilities of symptoms and clinical findings, both during and between attacks, are due to the interaction of migraine with the vestibular system at various levels. Also, Salmito and Ganança[12] reported that the vestibular findings are more abnormal during or shortly after the onset of migraine attacks.

In the current study, two-thirds of VM patients reported vHIT abnormalities (one-third in subgroup 1 and more than two-thirds in subgroup 2). Salmito and Ganança[12] and Yilmaz et al.[21] reported that abnormal vHIT was found in ∼10–18% of VM patients tested in interictal periods. Fu et al.[19] reported vHIT abnormalities in 32% of VM patients tested in interictal periods. In the current study, vHIT abnormalities were more reported during the attacks than in-between the attacks.

Migraineurs may show different VOR gain according to the presence of associated dizziness/vertigo or the frequency of attacks[6]. In the current study, high VOR gain was frequently reported in VM during the attacks: lateral canal 19 (46%) ears, posterior canal five (12%) ears, and anterior canal four (10%) ears. Lewis et al.[22] reported a possibility for increased VOR gain in VM patients as one of the pathophysiological mechanisms of migraine is the increased sensitivity of patients to sensory stimuli. Salmito and Ganança[12] reported that another possibility for increased VOR gain in VM patients is that vestibular sensitivity is normal, but the response is increased due to central migraine changes in the vestibular-efferent pathway. In the current study, low VOR gain was also reported in both subgroups [three (17%) ears in subgroup 1 and nine (21%) ears in subgroup 2]. Young et al.[23] reported that vHIT results demonstrated a reduced gain in VM patients in 2.5% of patients. But Blödow et al.[24] and Anson et al.[25] reported a reduced gain in VM patients in 9–11% of patients.

Another outcome of vHIT is the presence of corrective saccades (CS). With vHIT, both gain and CS can be objectively measured[25]. In the current study, three cases in subgroup 2 showed CS. Janky et al.[26] supposed that interpreting vHIT using both gain and CS would increase the sensitivity of vHIT for identifying vestibular loss. Adding CS improved diagnostic accuracy. CS is only present in peripheral disorders, whereas saccades did not appear in central disorders[27]. Huang et al.[4] have reported a higher incidence of central, peripheral vestibular dysfunction, or a combination of both in VM patients.

Arkink et al.[28], Shin et al.[29], and Obermann and Strupp[30] reported that activation of the dorsal brainstem nucleus and increase in the metabolism of the cerebellum and temporal areas lead to repetitive physiological and biochemical changes and also vascular and neural changes during migraine attacks. These functional and structural alterations in different areas of vestibular systems lead to peripheral and central vestibular abnormalities or a mixture of both, which explain the difference between both subgroups in the current study.

VM patients in the current study reported abnormal vestibular-function tests in more than 80% of them, either in vHIT only or oculomotor only or in both tests. In the current study, most patients of subgroup 2 were reevaluated during the routine follow-up visits at 3 months after their first visit to the clinic to assess the improvement in the migraine, vHIT as a quick test was done to assess the improvement. Most of the reevaluated patients reported improvement in their symptoms and more than half of the patients with a high gain had normal gain after treatment, two patients had gain improvement from low to normal, and six patients did not show any improvement in vHIT-gain results after treatment, so vHIT can be used as an easy quick monitoring tool during the management of VM patients. One of the limitations of the current study is the small number of participants, so large-scale studies are recommended on vHIT in VM patients, and the use of vHIT on follow-up of the patients during management.


  Conclusions Top


Abnormalities either in oculomotor-function tests or vHIT are common in VM, which were more pronounced during the attacks than in-between the attacks. The high gain was the most frequent vHIT abnormality during the attack, which shows improvement after treatment in more than half of the patients in the current study. vHIT can be used as a monitoring tool during management of VM patients.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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