AbstractIntroduction: The assessment of the vestibulo-ocular reflex (VOR) is one of the main steps inclinically evaluating patients with dizziness. It can be performed at the bedside with commonhead-impulse test in which eye position is analysed at the end of the head-thrust. It is animportant test due to its high specificity but low sensitivity.Material and methods: We studied 179 patients with different types of balance-affecting dis-orders. The results were analysed in contingency tables. The clinical test was classified asnormal or abnormal according to the absence or existence, respectively, of fixation saccadesonce the head-thrust was finished. The video head-impulse test (vHIT) was classified accordingto vestibulo-ocular reflex (VOR) gain and presence of fixation saccades. The speed of the slowphase of spontaneous nystagmus was also quantified, in addition to the caloric test results.Results: There were significant differences (Chi-square test, P=.00) for the findings in the clin-ical evaluation and with the vHIT: 32.1% of the tests performed yielded different findings inboth tests. In the vHIT, the differences were due to the finding of normal gain with saccades;in these patients, the mean canal paresis was significantly abnormal: 39%±10%.Conclusions: The distribution of findings for the VOR bedside examination and for that with thehelp of a video system are significantly different; as such, the video head-impulse examinationis not simply an added VOR detection and registration system. The difference relies mainlyon a vHIT response characterised as of normal gain but with fixation saccades. These have
� Please cite this article as: Pérez-Fernández N, et al. Exploración clínica y videoasistida del reflejo vestíbulo-oculomotor: análisiscomparativo. Acta Otorrinolaringol Esp. 2012;63:429---35.
∗ Corresponding author.E-mail address: [email protected] (N. Pérez-Fernández).
he response elicited by vestibular stimulation during headovements is, among others, an ocular movement with ainimal compensating delay, in the opposite direction andith the same speed. These characteristics perfectly define
he vestibulo-ocular reflex (VOR) whose study and assess-ent can be made from each of the 5 vestibular receptors
n the inner ear. In fact, the most common method is toxplore this response by stimulating the horizontal semicir-ular canal receptor, as in the caloric and rotatory tests.1
The clinical examination of each receptor in the semi-ircular canals can be individualised in the head impulseest systematised by Halmagyi and Curthoys.2 In such a clin-cal environment, the test evaluates ocular position, thats, the location of the eye at the end of the head impulsehen patients are asked to look forward to a point at a dis-
ance of 1 m, or whether saccades appear during or afteread impulse. It is an extremely useful test despite theubjectivity-entailed differences both in the stimulus and inhe response assessment. In acute vertigo crises, a normalesponse is the strongest predictor against a suspected cere-ellar stroke.3 In chronic peripheral condition, specificity isigh but sensitivity is low.4
The instrumental examination of this head impulse reflexs performed in an extremely detailed manner, with aorneal coil in a magnetic field test.5 The recording of posi-ion during this test is accurate and fast, thus enabling a
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etailed study of eye velocity during head movement. Unfor-unately, this test is impractical in a clinical environmentith a high workload and even more in an emergency situa-
ion.The development of techniques based on high definition
nd speed recordings has led to ocular velocity recordingests which have solved almost all the difficulties imposedy the corneal coil study.6 The method is named after theevice employed (video head-impulse test [vHIT]) and therere currently 2 different approaches, one with an externalamera facing the patient and one with the camera attachedo the head of the patient. The second method, employedn our study, has been validated against the corneal coilest and has shown an almost complete correspondence ofesults: the velocity profile recorded was identical and repli-ability between tests with each system was greater than.9.7
The aim of this work is to analyse the results in a broadopulation of patients with various types of balance disor-ers (referred for evaluation due to dizziness, vertigo ornstability) and to carry out a comparative study with easilybtained data during clinical examination.
aterials and Methods
atients included in this study were those who attendedonsultation due to suffering dizziness, vertigo or instability.
431
Table 1 Number of Patients Per Type of Disease Studied.
Ménière’s disease 68Benign paroxysmal positional vertigo 35Vestibular migraine 25Chronic otitis media 16Vestibular neuritis (sequelae) 10Posttraumatic 8Otosclerosis 5Secondary chronic instability 4Vertigo in patients with cochlear implants 3
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Clinical and video-assisted examination of the VOR
Additionally, we selected those in whom the cause was clari-fied unequivocally following diagnostic criteria proven in theliterature.8 We conducted an initial study of spontaneousnystagmus and nystagmus induced by positional changes,with and without visual fixation. Nystagmus was recordedby a VN415® (Interacoustics, Denmark) videonystagmogra-phy device. The Dix---Hallpike test was analysed under directvision, without visual fixation, with conventional Frenzelgoggles. Additional vestibular studies were conducted whenconsidered necessary (caloric or rotational testing).
Clinical Exploration of the Vestibulo-OcularReflex
The clinical vestibulo-ocular reflex (cVOR) was studiedusing the instructions of Halmagyi2 as described in otherarticles.4,9 We did not use additional recording devices inour work, but rather used visual examination; the clinicalassessment addressed the existence of re-fixation saccadesat the time of completing the head impulse. We performed3 impulses towards the left and right sides, randomly. Thetest was considered normal if there were no ocular saccadesjust at the end of head movement in at least 2 impulsestowards each side.
Video-Assisted Exploration of theVestibulo-Ocular Reflex
The study was conducted with a vHIT® device (video Head-Impulse Testing, GN Otometrics, Denmark). This deviceconsisted of a portable mask containing the camera whichrecorded eye movement, a gyroscope and a laser projector.Placement of the mask was a crucial step, as it had to befirm enough to provide stability and prevent sliding duringhead movements. Calibration was performed using the laser,which projected 2 points from one side of the mask whichswitched on and off alternately and subtended a 20◦ angleat a distance of 1 m from a comfortably sitting patient. Thetest consisted of small impulses to the right and left sides,firmly grasping the head of the patient from behind withboth hands placed on the temporal and parietal areas, whilstavoiding contact with the tape holding the mask or its cable.
We performed at least 20 impulses towards the right andleft. The normal response in a series of impulses towardsthe right is shown in Fig. 1. The final response was analysedbased on 2 key aspects of the impulses towards each side:the reflex gain and the existence of re-fixation saccades.Based on previous studies,7 gain values below 0.6 were con-sidered abnormal and re-fixation saccades were divided intocovert or overt. The former were re-fixation saccades occur-ring during the head impulse and the latter when this hadconcluded.
Since this exploration yielded detailed information onthe VOR, findings were divided into 4 groups: group 1 ornormal (gain>0.6, with no re-fixation saccades), group 2, inwhich the gain was normal (>0.6) but re-fixation saccades
were recorded (Fig. 2), group 3, in which the gain was lowand there were re-fixation saccades (covert and/or overt)(Fig. 2), and group 4, in which the gain was >1.3 either inisolation or due to the existence of covert saccades (Fig. 3).
he information was stored and analysed using the sta-istical package SPSS® 15.0. The result of each test wasivided into normal and pathological for the left and rightmpulses in each of the study methodology modes, clini-al and instrumental. We studied the relationship betweenoth evaluations through contingency tables, using the Chi-quare data (�2) and Fisher’s exact test, and consideringhe right and left impulses conducted on each patients individual assessments. This resulted in a study with58 tests. Firstly, we classified the findings of both scans asormal/abnormal according to the criteria mentioned pre-iously and secondly, we subclassified the findings of theideo-assisted study into the 4 categories defined previously.ext, each patient was classified according to the degree ofoncordance between cVOR and vVOR. These were classifieds identical if the results following both methods were simi-ar (normal or abnormal in both cases) and different if thereere differences (one normal and the other one abnormal).
n the latter case, we distinguished between VOR studiesonducted towards the right and left sides and conducted
study of differences towards either side. We used theann---Whitney U-test to analyse the differences in valuesf canalicular paresis between groups 1 and 2.
esults
e studied 179 patients distributed according to their dis-ases as described in Table 1. Of these, 69 (38.5%) patientsere male and 110 (61.5%) were female.
Out of these patients, the head impulse response studiedlinically (cVOR) was normal in 118 (65.9%), showed rightypofunction in 26 cases (14.5%), left in 26 and bilateral in
(5%).With respect to the stimulus (impulse), the results of the
nstrumented study (vVOR) were as follows: normal towardshe right side in 101 patients (56.4%) and abnormal in 7843.6%), whereas towards the left side it was normal in02 patients (57%) and abnormal in 77 (43%).
The results for the total tests conducted (n=358) arehown in Table 2. We observed that there was an overlap
f findings (normal or abnormal) in 67.9% of examinationserformed, and discordance in the rest. In most cases, thelinical examination was normal, whereas the instrumentedest was abnormal. The result of the Chi-square test was
Figure 1 Characteristics of a normal vVOR. The registry
4.1 (P=.001), and the significance in Fisher’s exact test was
=.001. Since all subjects were patients and no normal sub-ects were included, taking the vVOR as ‘‘gold standard’’,he sensitivity of the cVOR was 35% and specificityas 92%.
tivt
300
200
100
0
–100 –100
–100 –100
0 50 100 175150
Lateral impulse samples
300
200
100
0
0 50 100
Lateral impulse samp
Normal gain and re-fixation saccades
Low gain
Vel
ocity
300
200
100
Vel
ocity
0
0 50 100 150Lateral impulse samples
175
300
200
100
0
0 50 100 Lateral impulse samples
Figure 2 Class 2 (normal gain and saccades) and class 3 (low gai
own in 2D and 3D, scaling the results by stimulus velocity.
Table 3 displays the results of the contingency table when
he result of the vVOR study was detailed by abnormal find-ngs, as mentioned in the previous section. In this case, thealue of Chi-square was 135.287 (P=.00). We observed thathe most frequent cause of disparity occurred in tests in
175150
les
150 175
n and re-fixation saccades) according to the vVOR recording.
Clinical and video-assisted examination of the VOR 433
300
200
100
0
–1000 50 100
Vel
ocity
150 175
300
Covert saccades
Covert drawn from low gain and reattachment
200
100
0
–1000 50 100
Vel
ocity
150 175
300
200
100
0
–1000 50 100 15 0 175
300
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–1000 50 100 150 175
Figure 3 Class 4 (normal gain and saccad
Table 2 Findings Per Exploration Towards the Left andRight Sides in the 179 Patients Included in the Study.
cVOR vVOR
Normal Abnormal
Normal 188 100Abnormal 15 55
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cVOR: clinically assessed head impulse test; vVOR: head impulsetest with video-assisted assessment.
which the vVOR showed a correct gain but re-fixation sac-cades were recorded.
In 66 patients (36.8%), the vVOR study was normal in
both directions (group 1), and in 37 (20.6%) it was nor-mal towards one side whereas towards the other side gainwas also normal but there were re-fixation saccades (group
Table 3 Findings Per Exploration Towards the Left andRight Sides in the 179 Patients Included in the Study.
cVOR vVOR
Normal Class 2 Class 3 Class 4
Normal 188 77 6 17Abnormal 15 20 25 10
cVOR: clinically assessed head impulse test; vVOR: head impulsetest with video-assisted assessment. The latter is divided intothe different classes mentioned in the work.
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es) according to the vVOR recording.
). There were significant differences between both groupsMann---Whitney U, P=.02) regarding the value of canaliculararesis in the caloric test: in group 1 it was 17±2 and inroup 2 it was 39±10.
Finally, we selected patients in whom there was no doubtbout the affected side from the moment of anamnesis,hich left us with 157 patients. Of these, we excluded
hose with an abnormal result on both sides in the cVORnd/or vVOR tests. The comparative results are presentedn Table 4. The value of Chi-square was 23.613 (P=.01).
iscussion
he results of this work support the conclusion that the studyf VOR with a video-assisted recording system (vHIT, GNtometrics) may provide different findings in comparison tohose obtained through conventional clinical studies. In theontext of a specialist consultation, it provides additionalnformation which can improve the diagnostic accuracy ofhe study in admitted patients.
There are some fundamental differences between bothcans which must be recognised before interpreting theesults. Regarding the scanning methodology, firstly we mustention that in the case of the cVOR we only performed
impulses towards each side, while in the vVOR we per-ormed at least 20 impulses towards the right side and the
ame towards the left. Secondly, in the cVOR we did notave a quality assessment of the head movement induc-ng the reflex, while in the vVOR we obtained an accurateonitoring of the impulses performed through the recording
434
Table 4 Findings Per Exploration Towards the Right andLeft Sides in 114 Patients With Unilateral Involvement andWith Normal or Abnormal Result, Unilateral in Both the cVORand the vVOR Studies.
cVOR vVOR
Normal AbnormalTowards theRight
AbnormalTowards theLeft
Normal 46 22 23Abnormal towards
the right4 6 1
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Conflict of Interests
the left
f their speed. Thus, we excluded from the analysis thoseases which we considered had not been done properly.oreover, this also led to a learning curve which succes-
ively enabled us to perform tests in a similar way. This ledo a third difference, which is the possibility of studying dif-erent responses according to the velocity of the stimulus,ince we could induce this voluntarily. Fourth and finally,isual fixation in the case of cVOR took place at a short dis-ance (approximately 30 cm), whereas in the case of vVOR itook place at 1 m. Fixation distance during active movementas a relevant influence in the case of VOR gain, which has
significant cognitive component.10 Finally, and connectingith the following paragraph, the clinical study fixed on thenal position, which was influenced by more elements thanhe vestibular alone. In contrast, the video-assisted methodnalysed displacement during the first 150 ms, which exclu-ively represents the contribution of the vestibular systemo the VOR.
The method of recording and analysis of results alsostablished significant differences between the two pro-edures which should be recognised when comparing theiresults. Knowing the value of VOR gain is crucial when study-ng the functionality of the peripheral vestibular system,ecause during the passive movements undergone by theatient the influence of the peripheral vestibular recep-or in producing a correct reflex is almost exclusive. Weust not forget other elements, such as the monitoring, sac-
adic system and the cervico-ocular reflex, each of whichas a higher latency or a varying influence depending onhe form (active or passive) of producing the head impulsend adaptation mechanisms. A second difference is giveny the possibility of studying the morphology of ocularpeed registration in detail, analysing the characteristicsf re-fixation saccades during or after head movement. Atresent, there is no specific information from studies withorneal coils, but the complexity of these studies has pre-ented extending the knowledge of this phenomenon andharacterising it properly in patients with various types ofestibulopathy.11
We can understand the results of the study based on theifferences described previously. It could be argued that
he information obtained through both methods is not sim-lar and the differences are due to issues inherent to eachest, as described above. A similar study which compared T
N. Pérez-Fernández et al.
he cVOR with VOR gain measured with a corneal coil devicen 15 subjects found similar results.12
The study of cVOR systematised by Halmagyi andurthoys to be performed in any clinical environment isndoubtedly one of the most important pillars in the studyf patients with dizziness, vertigo or instability. Raising aichotomy in the methodology of clinical examination ofatients is far from the intention of the authors of theresent article. In fact, one of the current lines of work iso analyse in detail the reasons for the variations betweenVOR and cVOR, beyond the differences entailed by theechnique, particularly whether these distinctions could beddressed with the results from the caloric and/or rotatoryests. We believe that every patient should be examined inhe most thorough manner, and this includes the study ofOR, at least clinically. Nevertheless, the methodology ofhe study with a vHIT device provides complementary andore detailed information; it is not simply an additional
orm of recording. Moreover, the duration of the test andimplicity of the device employed add a very short time toealthcare, while providing versatility and enabling its usen any environment: outpatient clinics, admissions, emer-encies, etc.
It is somewhat surprising to find results with normalain and re-fixation saccades. Saccades occurring duringead impulse (or after its completion) are intended to cor-ect erroneous ocular position when there are variationsetween the ocular reflex velocity and the reflex-inducingead velocity.13 These were identified in 97 tests, of whichhe cVOR was normal in 77 and abnormal in 20. It isnteresting that, precisely the finding of re-fixation sac-ades in the cVOR study enabled us to differentiate aormal result from an abnormal one, and here they wentnnoticed in almost 2/3 of cases. The reason for thisies in their low speed and their proximity to the endf reflex ocular movement. They were intermediate sac-ades, between overt and covert, with an intermediatepeed (they were studied in 23 tests and the value obtainedas 83±9◦/s) and were probably a residue from somerior and properly compensated vestibular damage (hencehe finding of a greater degree of canalicular paresis),ith an almost correct functional restoration. Unfortu-ately, we do not have complementary information on theunction of the receptors from the superior and posterioremicircular canals to produce a more detailed descrip-ion. Moreover, according to some authors, these unnoticedaccades have the most notable influence on the low sen-itivity of the clinical test or cVOR.12 In this work, weave shown for the first time that they obey a pathologicalause, as observed when comparing the values of canalic-lar paresis in the caloric test, which were significantlyigher in patients with normal gain and re-fixation sac-ades.
We believe that this re-exploration system opens a newvenue for the investigation of vestibular function based onhe study of the vestibulo-ocular reflex and improves clinicaltudies.
he authors have no conflict of interests to declare.
1
1
1
Neurosurg Psychiatry. 2007;78:1113---8.
Clinical and video-assisted examination of the VOR
References
1. Pérez N, Martín E, Romero MD, García-Tapia R. Influence ofcanal paresis and compensation on gain and time constantof nystagmus slow-phase velocity to yaw-axis rotation. ActaOtolaryngol. 2001;121:715---23.
2. Halmagyi GM, Curthoys IS. A clinical sign of canal paresis. ArchNeurol. 1988;45:737---9.
3. Newman-Toker DE, Kattah JC, Alvernia JE, Wang DZ. Normalhead impulse test differentiates acute cerebellar strokes fromvestibular neuritis. Neurology. 2008;70:2378---85.
4. Pérez N, Rama-López J. Head-impulse and caloric tests inpatients with dizziness. Otol Neurotol. 2003;24:913---7.
5. Boleas-Aguirre M, Migliaccio AA, Carey JP. Registro del reflejovestibulooculomotor con la técnica de la bobina corneal encampo magnético (scleral search coil). Revisión de afec-ciones vestibulares periféricas. Acta Otorrinolaringol Esp.2007;58:321---6.
6. Weber KP, MacDougall HG, Halmagyi GM, Curthoys IS. Impulsivetesting of semicircular-canal function using video-oculography.
Ann N Y Acad Sci. 2009;1164:486---91.
7. MacDougall HG, Weber KP, McGarvie LA, Halmagyi GM, CurthoysIS. The video head impulse test: diagnostic accuracy in periph-eral vestibulopathy. Neurology. 2009;73:1134---41.
1
435
8. Soto-Varela A, Arán-González I, López-Escámez JA, Morera-Pérez C, Oliva-Domínguez M, Pérez-Fernández N. Clasificaciónde los vértigos periféricos de la Comisión de Otoneurologíade la Sociedad Espanola de Otorrinolaringología: concordanciadiagnóstica y actualización (versión 2, ano 2011). Acta Otorrin-olaringol Esp. 2012;63:125---31.
9. Oliva M, Martín García MA, Bartual J, Ariza A, García Teno M. Eltest de movimientos cefálicos bruscos [head-thrust test (HTT)]:consideraciones fisiopatologicas y utilidad en la clínica diaria.Acta Otorrinolaringol Esp. 1998;49:275---9.
0. Clément G, Maciel F. Adjustment of the vestibulo-ocular reflexgain as a function of perceived target distance in humans. Neu-rosci Lett. 2004;366:115---9.
1. Weber KP, Aw ST, Todd MJ, McGarvie LA, Curthoys IS, Hal-magyi GM. Head impulse test in unilateral vestibular loss:vestibulo-ocular reflex and catch-up saccades. Neurology.2008;70:454---63.
2. Jorns-Häderli M, Straumann D, Palla A. Accuracy of the bedsidehead impulse test in detecting vestibular hypofunction. J Neurol
3. Schubert MC, Hall CD, Das V, Tusa RJ, Herdman SJ. Oculomotorstrategies and their effect on reducing gaze position error. OtolNeurotol. 2010;31:228---31.
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