10.14639/0392-100X-N1951
Objective. The aim of this study is to evaluate vestibular functions with video head impulse test (VHIT) and to understand the value of VHIT in differential diagnosis in patients with vestibular migraine (VM) during dizziness attack. Materials and methods. Two groups were enrolled in this study. The first consisted of 84 vestibular migraine patients, and second group of 74 healthy subjects. VHIT was applied to patients with VM during vertigo attack and the results were compared with the VHIT values applied to subjects in the control group. Results. The mean vestibulo-ocular reflex (VOR) in all semicircular canals in the VM group was lower than healthy individuals, but the results were not statistically significant. Refixation saccades were found in 52.3% of VM patients and in 10.2% of healthy individuals. Conclusions. When patients with VM were evaluated with VHIT during vertiginous attack, VOR gain values were not different from healthy individuals, but the number of catch-up saccades were higher in VM patients, which indicates peripheral vestibular involvement. For differential diagnosis in patients with VM, vestibular tests should be performed during the vertigo attack. When evaluating VHIT results, the presence of refixation saccades should also be evaluated.
text/xml
1827-675X
1951
en
Elvan Cevizci Akkılıç
http://creativecommons.org/licenses/by-nc-nd/4.0
ACTA Otorhinolaryngologica Italica
head impulse test
Evaluation of video head impulse test during vertiginous attack in vestibular migraine
Text.Serial.Journal
https://www.actaitalica.it/
42
Vestibology
2022-06-30
2021-12-02
2022-07-26
2022-07-26
281-286
1
Elvan Cevizci Akkılıç
2022/06/30
10.14639/0392-100X-N1951
281
Acıbadem Health Group, Acıbadem Kozyatagi Hospital, Neurology Department, Istanbul, Turkey
1827-675X
head impulse test
en
286
Evaluation of video head impulse test during vertiginous attack in vestibular migraine
https://www.actaitalica.it/article/download/1951/832
42
ACTA OTORHINOLARYNGOLOGICA ITALICA 2022;42:281-286; doi: 10.14639/0392-100X-N1951




Vestibology


Evaluation of video head impulse test during
vertiginous attack in vestibular migraine
Valutazione dell’head impulse test eseguito durante l’attacco vertiginoso acuto
nella emicrania vestibolare
Ahmet Koç1, Elvan Cevizci Akkılıç2
1
 Acıbadem University, School of Medicine, Department of ENT, Istanbul, Turkey; 2 Acıbadem Health Group, Acıbadem Kozyatagi
Hospital, Neurology Department, Istanbul, Turkey


SUMMARY
Objective. The aim of this study is to evaluate vestibular functions with video head impulse
test (VHIT) and to understand the value of VHIT in differential diagnosis in patients with
vestibular migraine (VM) during dizziness attack.
Materials and methods. Two groups were enrolled in this study. The first consisted of 84
vestibular migraine patients, and second group of 74 healthy subjects. VHIT was applied to
patients with VM during vertigo attack and the results were compared with the VHIT values
applied to subjects in the control group.
Results. The mean vestibulo-ocular reflex (VOR) in all semicircular canals in the VM group
was lower than healthy individuals, but the results were not statistically significant. Refixa-
tion saccades were found in 52.3% of VM patients and in 10.2% of healthy individuals.
Conclusions. When patients with VM were evaluated with VHIT during vertiginous attack,
VOR gain values were not different from healthy individuals, but the number of catch-up
saccades were higher in VM patients, which indicates peripheral vestibular involvement.
For differential diagnosis in patients with VM, vestibular tests should be performed dur-
ing the vertigo attack. When evaluating VHIT results, the presence of refixation saccades
should also be evaluated.
KEY WORDS: vertigo, migraine, head impulse test
                                                                                                  Received: December 2, 2021
                                                                                                  Accepted: March 20, 2022
RIASSUNTO
Obiettivo. Lo scopo di questo studio è valutare la funzione vestibolare con il Video Head         Correspondence
Impulse Test (VHIT) e valutare il valore della VHIT nella diagnosi differenziale dei pazienti     Ahmet Koç
con emicrania vestibolare (VM) durante l’attacco vertiginoso acuto.                               Acıbadem Kozyatağı Hastanesi, Kbb Kliniği,
Materiali e metodi. Ci sono due gruppi arruolati in questo studio. Il primo Gruppo è com-         19 Mayıs Mah Begonya Sok No:12, Kozyatağı
posto da 84 pazienti con emicrania vestibolare e il secondo gruppo da 74 soggetti sani. La        Kadıköy, İstanbul, Türkiye
                                                                                                  Tel. +90 216 5714203. Fax +90 216 5714000
VHIT è stata applicata ai pazienti con VM durante l’attacco di vertigini e i risultati sono
                                                                                                  E-mail: ahmet.koc@acibadem.com
stati confrontati con i valori VHIT applicati ai soggetti nel gruppo di controllo.
Risultati. Il guadagno medio del riflesso oculo vestibolare (VOR) in tutti i canali semi-
circolari nel gruppo VM era inferiore rispetto agli individui sani, ma i risultati non erano        How to cite this article: Koç A, Akkılıç EC.
statisticamente significativi. I movimenti saccadici sono stati riscontrati nel 52,3% nei pa-       Evaluatıon of video head impulse test during
zienti con VM e nel 10,2% negli individui sani.                                                     vertiginous attack in vestibular migraine. Acta
Conclusioni. Quando i pazienti con VM sono stati valutati con VHIT durante un attacco               Otorhinolaryngol Ital 2022;42:281-286. https://
                                                                                                    doi.org/10.14639/0392-100X-N1951
vertiginoso, i valori di guadagno di VOR non erano diversi dagli individui sani, ma il nu-
mero di movimenti saccadici di recupero era più alto nei pazienti con VM, il che indica un
                                                                                                  © Società Italiana di Otorinolaringoiatria
coinvolgimento vestibolare periferico. Per la diagnosi differenziale nei pazienti con VM,         e Chirurgia Cervico-Facciale
i test vestibolari devono essere eseguiti durante l’attacco acuto di vertigini. Quando si
valutano i risultati VHIT, deve essere valutata anche la presenza di movimenti saccadici di
                                                                                                                 OPEN ACCESS
rifissazione.
                                                                                                  This is an open access article distributed in accordance with
PAROLE CHIAVE: vertigini, emicrania, head impulse test                                            the CC-BY-NC-ND (Creative Commons Attribution-Non-
                                                                                                  Commercial-NoDerivatives 4.0 International) license. The
                                                                                                  article can be used by giving appropriate credit and mentio-
                                                                                                  ning the license, but only for non-commercial purposes and
                                                                                                  only in the original version. For further information: https://
                                                                                                  creativecommons.org/licenses/by-nc-nd/4.0/deed.en




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Introduction                                                      healthy control group were evaluated. VM patients were
                                                                  included in the first group. 84 patients were identified with
Migraine is an episodic headache disease with diagnostic
                                                                  a retrospective evaluation who were diagnosed with VM
criteria described by the International Headache Society
                                                                  according to Barany Society and International Headache
(IHS). Vestibular symptoms are more common in patients
                                                                  Society criteria between September 2018 and September
with migraine than in the general population. In about half
                                                                  2020. The diagnosis of VM was made in collaboration with
of patients, dizziness has also been reported 1,2. Vestibular
                                                                  the authors, who are ENT and Neurology specialists. The
migraine (VM) is considered as a separate entity because
                                                                  second group consisted of healthy volunteers without diz-
of case-controlled studies 3. It is the most common cause
                                                                  ziness or migraine headache complaints. There were 84
of vertigo after benign paroxysmal positional vertigo 3. The
                                                                  patients in the VM group, mean age was 40 (18-65), 72
lifetime prevalence is estimated to be 1% 4. It can be seen at
                                                                  were female (85.7%) and 12 were male (14.3%). There
any age and is more common in women 5 with the highest
                                                                  were 78 individuals in the healthy control group. The mean
prevalence in middle-aged women 2. There is no objective
                                                                  age of individuals in this group was 38 (22-63), 68 were
diagnostic test or biomarker for vestibular migraine. Diag-
                                                                  female (87.1%) and were male (12.9%). Individuals un-
nostic criteria were described by Neuhauser in 2001 6. In
                                                                  der 18 years of age, those with current or previous neuro-
2012, the Barany Society and International Headache So-
                                                                  logical disease and patients using vestibular sedative drugs
ciety published the first consensus on diagnostic criteria 3.
                                                                  were excluded from the study. Healthy individuals did not
Symptoms are variable in patients with VM; the most fre-
                                                                  have a history of episodic or chronic headache, no hearing
quent is recurrent episodes of spontaneous vertigo, but po-
                                                                  problems or dizziness complaints, did not use any medi-
sitional vertigo and vertigo triggered by head movements
                                                                  cations, and had normal ENT physical examination. The
may also be seen. Vestibular symptoms may occur during
                                                                  groups were homogeneous in terms of gender (p = 1.000)
a migraine headache attack or in the attack-free period 5,7.
                                                                  and age (p = 0.998). A detailed history was taken from all
Thus, VM is difficult to diagnose, as vestibular symptoms
                                                                  patients, and standard ENT and neurological examinations
are also common in patients with migraine.
Vestibular tests may show abnormal findings during or im-         were performed. All patients were evaluated on the day of
mediately after vertigo attacks 5. It is not known exactly how    vertigo attack.
vestibular functions are affected in vestibular migraine. Ves-    Subjects in both groups were examined with VHIT by two
tibular functions can be measured indirectly by the physio-       investigators (by an ENT physician with experience in neu-
logical vestibulo-ocular, vestibulo-spinal and vestibulo-colic    rotology, and an audiologist with experience in VHIT ap-
reflexes. Measurement methods are electronystagmography,          plications). The investigators were blinded to this process.
videonystagmography, vestibular evoked myogenic poten-            VHIT Ulmer was used for VHIT testing (VHIT ULMER,
tials and video head impulse test (VHIT). VHIT provides ob-       Synapsys, Marseille, France). In the VHIT test, the subject
jective evaluation for all semicircular canals, and is a physi-   was placed on the examination chair 90 cm away from the
ological and easy-to-apply test. With VHIT, vestibulo ocular      VHIT device (the distance between the lens of the cam-
(VOR) gain (ratio between head velocity and eye velocity),        era and the patient’s external orbital cantus). Three fixation
compensatory eye movements (covert and overt saccades)            dots were placed on the wall 1 m away from the device, one
and the time required for correcting gaze can be determined.      in the central gaze axis and the others at ± 15-20°. Patients
VHIT can provide information that help to better under-           were asked to keep their neck muscles relaxed, open their
stand the pathophysiology of VM. In the literature, studies       eyes wide and not blink. Head impulses were applied to
reporting VHIT results in VM patients are examinations            stimulate each semicircular canal. For lateral canal stimula-
made during the vertigo attack-free period. To our knowl-         tion, passive lateral head impulses were applied. For verti-
edge, there is no study in the literature evaluating the re-      cal canal stimulation, the patient’s head was turned left (for
sults of VHIT measurements during a vertigo attack for            right anterior - left posterior stimulation) and right (for left
VM patients. The aim of this study is to evaluate vestibular      anterior - right posterior stimulation), 30-40° lateral from
functions during vertigo attack in vestibular migraine pa-        the midline and fixed to the fixation points. Next, unexpect-
tients with VHIT and to understand the value of VHIT in           ed passive head movements were applied at an amplitude
differential diagnosis.                                           of 10-15°, a duration of 150-200 msec and a peak speed of
                                                                  150-200°/sec. At least 20 impulses were delivered for each
                                                                  canal.
Materials and methods                                             VHIT gain was calculated as the ratio of the area under the
This case control study was carried out in the Vestibular         curve of eye movement versus the curve of the head move-
Diseases Unit. VHIT test results of patients with VM and          ment. Gain was classified as 1 when the graph of head move-



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Table I. Results of VOR gains in both groups (data was expressed in mean ± SD, median (min-max) and compared with Mann Whitney test).
                                                         VM Group                                   Control Group                                   P
                                                          N = 84                                       N = 78
 Right anterior SCC
   Mean ± SD                                                    0.97 ± 0.12                                     0.98 ± 0.095                       0.39
   Median (min-max)                                           0.98 (0.56-1.16)                                 0.99 (0.67-1.23)
 Left anterior SCC
   Mean ± SD                                                    0.88 ± 0.15                                     0.97 ± 0.088                       0.43
   Median (min-max)                                           0.95 (0.52-1.29)                                 0.98 (0.74-1.28)
 Right lateral SCC
   Mean ± SD                                                    0.85 ± 0.11                                     0.91 ± 0.085                       0.57
   Median (min-max)                                           0.92 (0.52-1.08)                                 0.94 (0.64-1.12)
 Left lateral SCC
   Mean ± SD                                                    0.87 ± 0.13                                     0.90 ± 0.091                       0.45
   Median (min-max)                                           0.90 (0.24-1.05)                                 0.92 (0.64-1.07)
 Right posterior SCC
   Mean ± SD                                                    0.90 ± 0.11                                     0.92 ± 0.088                       0.35
   Median (min-max)                                           0.94 (0.48-1.06)                                 0.95 (0.64-1.16)
 Left posterior SCC
   Mean ± SD                                                    0.89 ± 0.11                                     0.92 ± 0.0928                      0.45
   Median (min-max)                                           0.91 (0.53-1.10)                                 0.93 (0.67-1.08)
VOR: vestibulo-ocular reflex; VM Group: vestibular migraine group; SCC: semicircular canal.



ment and eye movement was equal (i.e., normal condition).                                     present for less than 5 years in 24 patients (28.5%), it was
If the eye movement during head movement is less than nec-                                    present for more than 5 years in 60 patients (71.5%). The
essary to fix the gaze on the target, the gain will be less than 1                            frequency of migraine headache was one or more attacks
and the second eye movement will occur; correction saccade                                    per week in 12 patients (14.2%), 1-3 attacks per month
(CS). This corrective eye movement puts the gaze on the tar-                                  in 34 patients (40.5%) and less than once a month in 38
get. If the impulse delivered to the head does not provide                                    (45.2%) patients. While headache and vertigo were ob-
an appropriate stimulus, the device will automatically reject                                 served together in 16 patients (19%), in 27 patients (32.2%)
this impulse. Possible VHIT results: gain (normal, lower, or                                  vertigo was seen just before or just after the headache. In
higher than normal), presence and number of correction sac-                                   41 patients (48.8%), the relationship was uncertain. Vertigo
cades. In VHIT analysis, VOR gain and presence of refixa-                                     was present for less than 5 years in 73 patients (87%), and
tion saccades were evaluated. Normal VOR gain was taken                                       more than 5 years in 11 patients (13%).
as > 0.8 for the lateral canal and > 0.7 for the vertical canals.
Mann-Whitney Test was used to determine the significance                                      VHIT analysis
of any difference for VOR gain values between groups. A                                       Table I shows the average VOR gains for each semicircular
p value < 0.05 was considered significant. The number and                                     canal in both groups. In the VM group, the mean VOR gains
percentage of saccades depending on VOR gains in both                                         in all semicircular canals were lower than the healthy group,
groups (VM group and control group) was analysed by chi-                                      but the results were not significant. Refixation saccades were
square test (Tab. II).                                                                        seen in 44 patients (52.3%) in the VM group, and only in
                                                                                              8 patients (10.2%) in the healthy group, all of these were
Results                                                                                       covert saccades. This difference was significant (Tab. II).
                                                                                              The amplitudes and latencies of the saccades seen in the VM
In patients with VM, 4 (4.7%) of 84 patients with VM de-                                      group are shown in Table III.
scribed migraine with aura, while 80 (95.3%) described mi-
graine without aura. The number of patients who described
spontaneous vertigo was 29 (34.5%), while 55 (65.5%)
                                                                                              Discussion
patients described positional vertigo. While migraine was                                     The fixation of the visual image in the retina during head



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A Koç, E.C. Akkılıç




Table II. The number and percent of saccades depending on VOR gains in both groups.
                                                            VM group (n = 84)                               Control group (n = 78)
                                                                         n                   %               n                 %
 No saccades                                                             40                47.6             70                89.8              p < 0.001c
 Saccades with normal VOR gain                                           24                28.5             8                 10.2              p < 0.001c
 Saccades with low VOR gain                                              20                23.8             0                  0                p < 0.001c
VOR: vestibulo-ocular reflex; VM Group: vestibular migraine group; c: chi-square test.



Table III. Amplitude (°/s) and latency (msn) of saccades in VM group.
 VM group                                                                                Amplitude (°/s)                        Latency (msn)
 Saccades with normal VOR gain                                                           203 (116-250)                           121 (63-190)
 Saccades with low VOR gain                                                              151 (111-189)                           139 (84-188)
VM Group: vestibular migraine group; VOR: vestibulo-ocular reflex.



movement is achieved by the VOR. The relationship be-                                     dependent functional magnetic resonance (fMR) studies
tween head and eye movements is called VOR gain 8,9. If,                                  have shown structural and functional changes in brain ar-
due to vestibular hypofunction, the velocity of the eyes is                               eas responsible for central vestibular control and vestibular
lower than head velocity, the eyes pause in the orbit, de-                                compensation in patients with VM 21. Vestibular findings
lay and the eye slips off the target. In this case, eye move-                             are thought to be explained by a wave of depression that
ments called catch-up saccades (CS) are used to stabilise                                 spreads from the occipital lobe to the cerebral cortex 1.
the gaze to compensate for the impaired eye movement 10,11.                               The fact that the clinical appearance of VM varies according
CSs can be covert or overt depending on whether they are                                  to age creates difficulties in differential diagnosis. There is
seen during head movements or after head movements are                                    no laboratory test or biomarker that gives a definitive diag-
terminated 12. VHIT, one of the newest tests in the vestibu-                              nosis for VM 2. Therefore, vestibular tests in patients with
lar laboratory, evaluates VOR by measuring eye deviations                                 VM are investigated to obtain information that will help in
during rapid head acceleration in each semicircular canal                                 differential diagnosis 2. Most patients with VM do not have
(SCC) plan. VHIT calculates vestibulo-ocular reflex gain,                                 any complaints during the attack-free periods. Nystagmus
determines the presence and amplitude of covert and overt                                 can be detected on physical examination during an attack.
catch-up saccades and records eye and head movements 8-13.                                Performing vestibular tests during the vertiginous attack
Unlike the caloric test, it is a physiological test, each semi-                           may be more useful for differential diagnosis.
circular canal can be evaluated, gives a more comprehen-                                  Studies evaluating VHIT results in patients with VM have
sive assessment and is better tolerated by the patient 2,14,15.                           shown VHIT abnormalities (low gain and/or saccades) in
In migraine, not only headache but also other complaints                                  11-36% of cases 2,15,22. Only gain abnormalities were de-
such as dizziness, hearing loss and tinnitus can be found.                                tected between 8-11% 15,23,24. In a study on 31 patients with
These are thought to be due to chemical changes in synap-                                 VM, Salmito found similar VOR gain values for lateral ca-
tic transmission and subsequent imbalance between neural                                  nals between the VM and control groups, but found higher
excitation and inhibition 16. VM is the second most com-                                  VOR gain values for vertical canals in the VM group 5. Sal-
mon cause after BPPV in many studies evaluating patients                                  mito argued that this difference in vertical canals may be
with vertigo complaints 3,7. VM occurs with central or pe-                                due to artifacts, incorrect head positioning, improper po-
ripheral vestibular dysfunction during headache attacks 17.                               sitioning of the VHIT device, or head impulses at different
There are some hypotheses about how the inner ear dis-                                    velocities. In the study by Mahringer, VHIT had abnormal
orders occur in patients with migraine. Sterile inflamma-                                 results in 11% of patients with VM 25. In Blödow’s study,
tory response in intracranial vessels with activation in the                              9% abnormal gain was found in patients with VM, and the
trigeminovascular system 18, cortical spreading depression                                average VOR gain in these cases was 0.73 ± 0.04 23. In two
affecting the brain stem 3, peripheral vestibular dysfunction                             studies by Elsherif, VHIT abnormality in the VM group
because of vasospasm in the internal auditory artery 19 and                               was 36% in 25 patients and 26.3% in 80 patients 1,22. In the
plasma extravasation because of trigeminal neurogenic in-                                 mean VOR gains between the VM and control groups, a sta-
flammation in the labyrinth have been invoked 20. Positron                                tistically significant difference was found only in the right
emission tomography (PET) and blood oxygenation level                                     posterior canal measurements, and was found to be lower



284
                                                                                                               VHIT in vestibular migraine




in the group with VM. Kang detected abnormal VHIT find-          should be assessed. Vestibular tests should be performed
ings in 9 (11%) of 81 VM patients 15. In a previous study,       on patients with VM, if possible, during the vertigo attack.
the rate of covert saccades in patients with migraine was
found to be significantly higher than the control group, and     Acknowledgements
it was thought that this high saccade rate may be related to     The authors have no affiliations with or involvement in any
the connection between the trigeminal nerve and vestibular       organisation or entity with any financial interest (such as
nuclei. Like VHIT, recent studies propose using functional       honoraria; educational grants; participation in speakers’
head impulse test (fHIT) to evaluate VM patients 26,27. The      bureaus; membership; employment; consultancies; stock
results of percentage of correct answers in fHIT can sup-        ownership or other equity interest, and expert testimony
port the diagnosis of VM.                                        or patent-licensing arrangements), or non-financial interest
It has been argued that VM occurs because of a deterioration     (such as personal or professional relationships, affiliations,
in the rate of spontaneous neural firing at the level of the     knowledge, or beliefs) in the subject matter or material dis-
vestibular nuclei with the decrease in inhibitory inputs from    cussed in thus manuscript.
the cerebellar flocculus to the vestibular nuclei 22. VHIT has
been found to be useful in evaluating the response to medical    Conflict of interest statement
treatment in patients with VM. Kang reported that cervical       The authors declare no conflict of interest.
vestibular evoked myogenic potential test (cVEMP), ocular
vestibular evoked myogenic potential test (oVEMP) and sen-       Funding
sory organization test (SOT) are not useful when evaluating      This research did not receive any specific grant from fund-
the response to medical treatment in patients with VM, but       ing agencies in the public, commercial, or not-for-profit
that VHIT results are useful. Complete recovery was ob-          sectors.
served in 82% of patients with normal VHIT gains compared
to 44% in patients with abnormal VHIT gains 15. VHIT has         Authors’ contributions
also been found to be useful in differential diagnosis of VM     AK and ECA have equally contributed to the manuscript.
and Meniere’s disease 23,28.
In all these studies, VHIT was performed in patients with        Ethical consideration
VM during the period between attacks (attack-free peri-          This study was approved by Ethics Committee of Univer-
ods). In the current study, the VHIT test was performed          sity of Acıbadem University (approval number/protocol
on the day of vertigo attack. In the VM group, 24 (28.5%)        number 2020-18/4).
patients had normal VOR gain and 20 (23.8%) had low              The research was conducted ethically, with all study pro-
VOR gain. The total VHIT abnormality rate was found to           cedures being performed in accordance with the require-
be 52.3%. In the control group, only 8 patients (10.2%) had      ments of the World Medical Association’s Declaration of
normal VOR gain with saccades.                                   Helsinki.
The episodic character of VM means that tests are per-           Written informed consent was obtained from each partici-
formed in the asymptomatic period in most patients. To           pant/patient for study participation and data publication.
our knowledge, the present study is the only study in the
literature evaluating VHIT results during vertigo/dizzi-
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