Video head impulse test (vHIT) versus videonystagmography (VNG) in migraine with dizziness

Background Migraine disease is a chronic headache disorder characterized by recurrent attacks. Migraine and vestibular disorders are common associations. The exact pathophysiology is still unknown. Objectives To study the results of vHIT and VNG in dizzy migraineurs. Methods This is a case-control study that included 140 subjects 70 of them were migraine patients with vestibular symptoms, while the other 70 were a control group of healthy subjects matched in age. A full history with pure tone audiometry and tympanogram for hearing evaluation was done for both groups then videonystagmography and the video head impulse tests were done. Results The vHIT results showed that there were no significant differences among control and study groups regarding the VOR gain and gain asymmetry with no corrective saccades recorded in patients or control groups that denote the VOR is intact. The VNG test revealed in OPK and saccade tests that there was a significant difference between the control and the study groups. A positive weak correlation between vHIT and caloric test results in the left lateral and posterior canal gain in the study group. Conclusion The migraine disease with vestibular symptoms does not affect the VOR gain in vHIT and affects the oculomotor tests in VNG.


Background
Migraine is a chronic headache disorder characterized by recurrent attacks with a time varying from around 5 min to 72 h.Migraine has a pulsating quality of moderate or severe intensity in nature which is aggravated by routine physical activity.It is commonly associated with nausea, vomiting, photophobia, or phonophobia.It could be also associated with an aura (transient focal neurological symptoms) whose origin is believed to involve the brain stem, and cortex [14].Migraine and vestibular disorders are a common association.The exact pathophysiology is still unknown.The most common terms to describe the combination of migraine and vestibular symptoms are vestibular migraine, migrainous vertigo, migraine-associated vertigo, and vertiginous migraine.Migraine vertigo can be rotational or non-rotational, spontaneously or in association with a change of position [11].The vestibuloocular reflex (VOR) is a reflex responsible for maintaining eye fixation during head rotation by moving the eyes in the opposite direction of head rotation at approximately the same speed.The VOR incorporates both the visual and the vestibular systems, gathering input information from the semicircular canals and eye fixation.This reflex serves to allow gaze fixation during movement to keep an image on the fovea [10].An abnormal VOR could result in the inability to maintain an image on the fovea and manifests clinically as subjective vertigo reported by the patient or objective nystagmus that could be observed by functional methods in the form of clinical office tests or electrophysiological methods by using videonystagmography (VNG) or recently developed video head impulse test (vHIT) [24].The introduction of the vHIT provides a new dimension in vestibular diagnostics.The vHIT test allows a quantitative tool for the assessment of the SCC function by measuring the saccadic count (both overt and covert saccades) and evaluating the VOR gain in each canal of the six semicircular canals separately.The vHIT provides a new objective measurement system that is fast and accurate enough to detect not only overt saccades but also covert saccades [6].The vHIT detects abnormalities in all six canals, and it tests the high frequency (3-6 Hz) also clinician has the ability to test patients even if they have middle ear disorders and patients who cannot tolerate calorics.While the caloric subtest of VNG detects only lateral canal abnormalities and evaluates low frequency (0.003 Hz) [28].

Methods
A case-control study was conducted at the Audio-vestibular Unit of Al-Zahraa Hospital, Al-Azhaar University in Egypt the period from March 2020 to June 2022.Subjects in this study were composed of two groups the control and the study group both matched in age (20-50 years).
1-The control group consisted of 70 normal-hearing adults not complaining of dizziness, migraine, any audio-vestibular disorders, neck problems, any systemic diseases, or neurological or visual disorders.They were collected from the associates of the patients and the hospital colleagues' volunteers.
2-The study group consisted of 70 migraine patients with dizziness according to ICHD-3 and Barrany society classification with normal hearing not complaining of neurological disease, neck problems, visual problems, or systemic diseases.They were referred from the neurology and ENT clinics and were previously diagnosed as having migraine within the last 5 years according to [18].Most of the patients were examined between 2 days and 1 week after their last dizziness attack, while the others were examined after 1 week.Patient consent was taken and the patients were submitted for audiological evaluation to exclude any audiological problems and vestibular evaluation by vHIT and VNG battery tests.All subjects included in the study were submitted to the following: by using the Interacoustics Eye See Cam.The vHIT system consists of a lightweight pair of goggles integrated with a video-oculography camera that was fixed to the head tightly by using a rubber band.The vHIT was recorded from the right eye by a mirror to reflect the image of the patient's right eye into the camera and an inertial system to measure head movements.In the test, subjects were seated wearing goggles with their head and body facing a target located 1 m distance on the wall.The eye movements and the head movements were recorded by using processing algorithms and calibration was done.The Video head impulse test was performed to evaluate lateral semicircular canal gain.The examiner was standing behind the subject in the study held his head and gave him the instructions to look at a dot located on the wall all through the lateral canal test [26].
A lateral small movement to the head of the patient by amplitude (5-15°) and high peak velocity (150-200°/s).Each subject was subjected to 10 head impulses at least in the horizontal plane to each side (left or right) with unpredictable timing and direction.LARP canals were studied with the head 30° to the right of the fixation point.RALP canals were studied with the head turned to the left 30°.Passive back-and-forth movements were done to the subject's head with an amplitude of (5-15°) with high peak velocity (60-120°/s).Each subject was subjected to at least 10 head impulses unpredictable in timing and direction in the vertical plane to each side back or forth [3].The vHIT measures the VOR gain for each of the semi-circular canals on both sides [26].The VOR gain is the ratio of the eye velocity to the head impulse velocity from the onset of the head impulse to the moment when the head velocity returns to zero.It is defined as normal if they are within the calculated gain-reference range and no corrective saccades occur [1].The Gain Asymmetry (GA) was calculated using a general formula: VOR gain asymmetry (%) = [(larger − smaller)/ (larger + smaller)] × 100 .The normal values of vHIT gain > 0.7 without saccades [15].The normal range of vHIT gain asymmetry is from 0 to 13.3% and it is considered to be abnormal if it is greater than 13.3% [7].

The statistical analysis
Data were collected, tabulated, and statistically analyzed by using an IBM-compatible personal computer with Statistical Package for the Social Sciences (SPSS) version 26 (SPSS Inc.Released 2018.IBM SPSS Statistics for Windows, version 26.0, Armnok, NY: IBM Corp.).Two types of statistical analysis were performed [23]: a) Descriptive statistics, e.g., qualitative data were expressed as number (N), and percentage (%), while quantitative data were expressed as mean (x̅ ), standard deviation (SD) b) Analytic statistics, e.g., ▪ Chi-squared (χ2): it is used for qualitative variables.▪ Mann-Whitney's test (U): was used for the comparison of quantitative variables between two groups of not normally distributed data [17].▪ One-way ANOVA (F): test is a test used for comparison between more than two groups having quantitative normally distributed variables.▪ Least significant difference (LSD): test is used for post hoc analysis.▪ Spearman correlation: was used for not normally distributed data with interpretation guidelines as follows: [1] r = 0.0: no correlation 0.0 < r < 0.2: very weak correlation 0.2 ≤ r < 0.4: weak correlation 0.4 ≤ r < 0.6: moderately strong correlation 0.6 ≤ r < 0.8: strong correlation 0.8 ≤ r < 1.0: very strong correlation r = 1.0: perfect correlation.

The results
The participants in this study were divided into two groups: Group 1: normal (control) 70 subjects.Group 2: the study cases 70 patients of migraine with dizziness.
The control group was composed of 70 persons 49(68.8%) of them were females and the others 21(31.2%)were males, with a mean age of 31.9 ± 8.4 years.The age range was between 20 and 48 years, while the study group consisted of 70 patients with 23(32.9%)males and 47(67.1%)females, with mean age 32.6 ± 8.5 years, the range of age varied from 21 to 47 years.The two groups showed no statistically significant difference between them regarding age and sex (P > 0.05) by using Student's t-test and the chi-square test respectively as shown in Table 1.Most of the patients (72.9%) were examined between 2 days and 1 week from their last dizzy spell, one of the patients couldn't tolerate the examination tests, so its data was not computed in the analysis.
Dizziness complaints varied among patients as 54.3% imbalance, 34.2% sense of spinning of surroundings, 8.4% lightheadedness, and 3.1% presyncope of the patient's complaint.The positional tests revealed positional vertical nystagmus in 12.8% of patients, 8.5% showed horizontal nystagmus and 4.2% showed pure torsional nystagmus (Table 2).In the vHIT test, the lateral canal gain range was 0.85-1.3 on the right side with a mean of 0.88 ± 0.11 while in the left side gain range was 0.82-0.98 with a mean of 0.90 ± 0.2.The right anterior canal gain range (0.91-1.39) with a mean of 1.2 ± 0.2 and the left side gain range (0.94-1.13) with a mean of 0.98 ± 0.2.The right posterior canal gain range (0.84-1.17) with a mean of 0.91 ± 0.21.In the left posterior canal gain range was (0.82-1.15) with a mean of 0.92 ± 0.34.There was no statistically significant Table 1 The demographic data of the control and the study groups difference between the control and the study groups as the p value is > 0.05 in each canal gain (Table 3).The gain asymmetry did not exceed 13% in both groups with no corrective saccade recorded.Both the saccade (regarding latency and precision) and the optokinetic test revealed significant statistical differences among the control and the migraine groups (Tables 4  and 5) while the pursuit test showed no significant difference among the study groups (Table 6).The caloric test showed that there were no significant differences between the control group and the migraine patients group as the p value is > 0.05 (Table 7).The study revealed a positive correlation between the vHIT and the caloric test results in left lateral canal gain as the p value is < 0.05 (Table 8).

Discussion
In the current study most of the dizzy migraine patients (62.7%) complained from headaches in a duration range 1-5 years, while (37.3%) complained for less than 1 year, with a recurrence of headache attacks which varied between patients from once per week (25.7%) or more (18.7%) to once per month (14.2%) or more (41.4%),which associated with other symptoms like nausea and vomiting (11.4%) or photophobia (82.8%), phonophobia (71.4%) and visual aura in (61.4%) of patients, the dizziness spell may be associated with the headache attack in (11.4%) of patients or proceed the headache in (41.4%) of the patients, while may come after headache in 30% of them.Most of the patients were examined between 2 days and 1 week from their last dizzy spell (72.9%) and they revealed normal  office tests examinations regarding gait, cerebellar tests or head shaking.
In the dizzy migraine patients about (12.8%) they exhibited vertical nystagmus, (8.5%) of the patients revealed horizontal nystagmus, and (4.2%) of them revealed pure torsional nystagmus which was in agreement with Elsherif et al. [9] who found vertical nystagmus in 16% of the study group, Wei et al. [29] who found positional nystagmus in 24% of his study group, and Waissbluth et al. [27] who found positional nystagmus (which varies between vertical, horizontal, and torsional nystagmus) in 33.3% of his study group.While there was no nystagmus in positioning tests, the dizzy migraine patients exhibited a non-paroxysmal type of positional nystagmus which differs from the benign paroxysmal positional nystagmus which is characterized by its paroxysmal form with latency and is usually associated with a sensation of vertigo [8].
It was reported in migraine with dizziness that the horizontal nystagmus is caused by abnormal vestibular signals from the lateral canals and the affection of the flocculi-nodular lobe of the cerebellum is responsible for vertical nystagmus by dis-inhibition of vestibular nuclei in the brainstem [20].In migraine with dizziness pathology, the central vestibular system dysfunction which is either in the vestibular nuclei of the brain  stem or in the multisensory vestibular cortex may be the explanation for this nystagmus [16].
The vHIT evaluates the function of the semicircular canals in response to high-frequency head movements and that is more suitable for the assessment of the real-world vestibular function of the semicircular canals.In the current study, the vHIT results showed that there is no significant difference between the control and study groups as the P value is > 0.05 and these results were in agreement with Salmito and Gananca, [22] who found that the vestibular function measured by the semicircular canals VOR gains were normal in both groups (the study and control groups) of their study while disagreeing with Kang et al. [19] who found abnormal vHIT in approximately 31% of migraine patients in his study.
In this study group, the VOR gain of the vHIT was normal with no re-fixation saccade in all patients, which is in agreement with Elsherif et al. [9] who found that in the majority of the dizzy migraine patients of his study, the VOR gain was normal with no re-fixation saccades.So it is suggested that the vestibule-ocular (VOR) reflex arc is intact in dizzy migraine patients.
In this study, there were no spontaneous or gazeevoked nystagmus while in the oculomotor tests, the smooth pursuit test revealed that there was no significant difference among the study and control groups.These results disagree with Wei et al. [29] who found pursuit abnormalities in half of his study group patients.
The saccade test revealed that there was a significant difference in latency and precision among the study  Apart from central mechanisms, inner ear involvement may explain abnormal findings.Trigeminal vascular reflex-mediated vasodilatation of cranial blood vessels and subsequently plasma extravasation causing meningeal inflammation are the key reason and the trigeminal vascular system also innervates the inner ear [12].These previous test results may be accounted by the central affection in migraine disease by the complex theoretical pathophysiological link between migraine and the vestibular system [4] which is thought to be a combination of neurological and vascular events [25].These may include cortical spreading depression (CSD) which is a slowly propagated wave of depolarization followed by suppression of brain activity.It is a complex event that involves dramatic changes in neural, glial, and vascular function [5].
In the optokinetic (OPK) test it showed that there is a significant difference between OPK test results among the two groups.These results are in agreement with Elsherif et al. [9] and Waissbluth et al. [27] who found that the majority of patients (> 50%) in their studies groups exhibited abnormalities in the OPK nystagmus test.These results may be explained by the hyper-excitable brain state that occurs in migraine patients this leads to a sensory demodulation concept (a deficient potentiation and habituation of sensory responses that occurs in the pathogenesis of migraine) [13].So by exposure to a sensory stimulus that results in hypersensitivity which can extend to other sensory stimuli, migraine patients show a high sensitivity to motion, and they have high variability in spatial orientation this suggests that the visuospatial symptoms in migraine patients are related to altered sensory processing and integration that contribute to the perception of spatial orientation.Regarding the effect of visual motion, migraine patients had large visualinduced errors in spatial orientation during and after optokinetic stimulation [2].
The caloric test revealed no significant difference among the study groups (as the p value is > 0.05) which disagrees with Kang et al. [19] who found that 19% of their study group exhibited abnormal caloric test results.Correlation between the vHIT and caloric test results a positive correlation was found in the left lateral canal, which is in agreement with [21] who found a correlation analysis between vHIT VOR gain and the caloric test in all patients using Spearman's rank test indicated a significant, but only weak correlation.

Conclusion
The VNG battery test is a more dependable tool in assessment of the dizzy migraine patients than the vHIT.

Recommendations
To explore the role of other tests like (posturography and rotatory chair) in the evaluation of migraine with dizziness.

Table 2
Positional and positioning test results among the study and control groups

Table 3
The comparison of the vHIT test results among the cach canal gain and gain asymmetry

Table 4
The comparison between the saccade test results among the study and the control groups regarding velocity, latency and precision *Significant Difference as P ≤ 0.05

Table 5
The comparison between the optokinetic test results among the study and the control groups regarding gain and SPV *Significant Difference as P ≤ 0.05

Table 6
The comparison between the pursuit test gain results among the study and the control groups

Table 7
The comparison between the control and the study groups as regarding the caloric test

Table 8
[27]correlation between the vHIT test and the Caloric test results in the study group groups, as regarding velocity there was no significant difference.These results are in agreement with Waissbluth et al.[27]who found saccade test abnormalities in 70% of his study group patients.These results may be related to the pathological mechanisms of migraine.