Acta Oto-Laryngologica. 2014; 134: 1128–1133

ORIGINAL ARTICLE

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The vestibulo-ocular reflex assessment in patients with Ménière’s disease: examining all semicircular canals

CRISTINA ZULUETA-SANTOS1, BARBARA LUJAN2, RAQUEL MANRIQUE-HUARTE1 & NICOLAS PEREZ-FERNANDEZ1 1

Department of Otorhinolaryngology, Clínica Universidad de Navarra, University Hospital and Medical School, University of Navarra, Pamplona, Navarra, Spain and 2Instituto Nacional de Rehabilitación, Mexico City, Mexico

Abstract Conclusion: The distribution of abnormal results is not uniform between different canals in each patient; the most frequent gain reduction is obtained for the posterior canal. Gain reduction reflects the disease duration and amount of hearing loss. Objective: To test the hypothesis that the vestibulo-ocular reflex (VOR) evoked after stimulation of each semicircular canal behaves in a different manner in patients with unilateral definite Ménière’s disease. Methods: We studied the VOR evoked by rapid head-impulses in the plane of the 6 semicircular canals in 36 patients. It was evaluated with a video system that analyzes the head and eye velocity and the gain was the objective measure. Results: In 12 (33.3%) patients the examination of both ears was normal for all the semicircular canals, in 12 patients the results from the affected ear were abnormal in at least 1 of the semicircular canals, in 11 (30.5%) patients the results were abnormal in at least 1 of the semicircular canals in both the affected and unaffected ears, and in 1 (2.9%) patient the results were abnormal only in the unaffected ear. The most frequent abnormal result was obtained from the posterior canal of the affected ear and from the coupled superior canal of the unaffected ear. The distribution of abnormal findings was dependent on the disease duration and hearing loss.

Keywords: dizziness, inner ear, video head-impulse, vertigo

Introduction Ménière’s disease (MD) is an idiopathic inner ear disorder characterized by episodic vertigo, aural fullness, tinnitus, and fluctuating hearing loss [1]. The natural course of the disease is characterized by a reduction of the number of vertigo spells (in particular of those that last less than 6 h) in such a way that the possibility of experiencing an episode-free year increases as the disease evolves. As such, after a period of exacerbations and remissions the patient enters into a situation of chronic disequilibrium without vertigo spells [2]. Auditory and vestibular examinations are correlated to some extent but not uniformly in all the studies, which reflects not only differences in evaluation but also in the natural history of the disease

between patients. This is very relevant for the bedside and instrumental examination of vestibular function [3]. In general, in the initial stage of the disease the main damage occurs in the saccule and as the disease progresses the damage extends to the utricle and semicircular canals [4]. It is important to take into account how recent the last vertigo spell was, as results in the vestibular test will reflect this issue in particular when saccular [5] or horizontal semicircular canal function [6] are evaluated. Also, as the disease progresses a marked hearing deterioration occurs (once hearing loss is corrected to age of the patient) for the low frequencies [7]. We were interested in performing a detailed assessment of the vestibulo-ocular reflex (VOR) in patients with MD, analyzing the eye response to sudden head thrusts in the different planes in which each

Correspondence: Dr Nicolas Perez, Dpto de ORL-Clínica Universitaria, Pio XII 36, 31008 Pamplona, Navarra, Spain. Tel: +34 948 255400. Fax: +34 948 296588. E-mail: [email protected]

(Received 11 February 2014; accepted 13 April 2014) ISSN 0001-6489 print/ISSN 1651-2251 online  2014 Informa Healthcare DOI: 10.3109/00016489.2014.919405

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Ménière’s disease six canals semicircular canal is situated. Recently, in the clinical setting new video-based equipment has been introduced that enables registration of the eye in response to sudden head impulses [8,9]; this is called the video head-impulse test (vHIT). This system mimics the performance of the scleral search coil in a magnetic field installation. Previous work with the scleral coil has been aimed at correlating the findings with those of the caloric test and they have shown a clear dichotomy, as it is more frequent to obtain an abnormal response in the caloric than in the head-impulse or head-thrust test [10]. Regarding the amount of affected to non-affected side asymmetry in gain of the VOR it was found to be 0.8 for lateral canals and >0.7 for the vertical canals, according to previous clinical published experiences [13]. Disability measures. These were performed with the Dizziness Handicap Inventory Test using the total

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score (DHITS) and patients were classified by functional level scale (FLS) [1].

8  FLS = 2; 8  FLS = 3; 8  FLS = 4; 4  FLS = 5; and 1  FLS = 6. The mean DHITS was 35 ± 19.

Statistical analysis

Analysis of vHIT

All analyses were performed using the SPSS 12.0 statistical software, and a p value < 0.05 was considered to be statistically significant. In the data analysis, we looked for possible relations between vHIT parameters and the disease duration and the PTA. From audiometric data patients were classified in four groups: 1 if PTA 70 dB HL. A Kaplan–Meier time to event (abnormal result) method was used to analyze the responses in each canal from both sides. This method evaluates the percentage of patients who show a normal (gain >0.8) or abnormal (gain 0.05). The distribution of findings by patients was the following: (a) in 12 (33.3%) the examination was normal as gain of the VOR after head impulses in the plane of the 6 semicircular canals w above normal limits, (b) in 12 the results from the affected ear were abnormal in at least 1 of the semicircular canals, (c) in 11 (30.5%) the results were abnormal in at least 1 of the semicircular canals in both the affected and unaffected ears and, (d) in 1 (2.9%) the results were abnormal only in the unaffected ear. According to our results the most frequent abnormal result was from the stimulation of the vertical canals and in particular the posterior canal (PSC) in the symptomatic ear. The horizontal canal (HSC) in both the symptomatic and asymptomatic ears displayed very few abnormal results and in particular the latter in just one patient. Canal function in the six canals was significantly different when disease duration (log rank, p = 0.002, c2 = 18.4) and PTA (log rank, p = 0.003, c2 = 18) were analyzed (Figures 2 and 3).

Results Patients The study subjects comprised 36 patients (20 females and 16 males; mean age 53 years, range 21–79 years) with unilateral MD. The affected ear was the right ear in 20 (55.5%) and the left ear in 16 (44.5%) patients. The mean disease duration was 7 years (95% confidence interval (CI95%): 4–9) and the mean time since the last vertigo spell was 33 days (CI95%: 17–50). On vestibular examination, spontaneous nystagmus was evident in 17 (47.2%). In audiometry, the mean PTA was 45 ± 19 dB; the distribution was the following: 7  PTA 70 dB. The FLS results were distributed as follows: 7  FLS = 1;

Discussion The immediate eye response to high velocity head impulses or thrusts in the plane of a given semicircular canal depends on the adequate function of the vestibular end organ and the integrity of the corresponding neurological pathway. As such the VOR can be quantified and, in case of deficit, the immediate eye corrective movement (refixation saccade) can also be registered. With the use of high speed and high velocity cameras this method of vestibular examination is becoming the preferred routine office-based

Table I. Gain (mean ± standard deviation, SD) of the vestibulo-ocular reflex (VOR) according to the ear and canal plane of stimulation. Asymptomatic ear

Symptomatic ear

Superior

Horizontal

Posterior

Superior

0.85 ± 0.2

1.02 ± 0.13

0.79 ± 0.14

0.89 ± 0.26

Horizontal 1 ± 0.15

Posterior 0.74 ± 0.14

Ménière’s disease six canals

CONTRA SUP

1131

IPSI SUP 22.8

22.8

2.58

CONTRA HOR

14.2

IPSI HOR

40

CONTRA POST

IPSI POST

Figure 1. Distribution of abnormal results in the population. Data are percentage of abnormal result by ear affected (IPSI) and normal ear (CONTRA) and canal (superior, SUP; horizontal, HOR; posterior, POST).

practice at the bedside [14], as occurs in acute unilateral vestibulopathy to disclose central vestibular damage [15]. In a group of patients with unilateral MD, by examining the VOR elicited by the stimulation of each semicircular canal we found a completely normal response from the affected and unaffected ears in 33.3% of the patients, the affected ear showed abnormal results in 63.8% and the unaffected in 33.3%, of which in only 2.9% was there an abnormal result. No correlation was seen with any of the clinical

parameters (taken independently) of the disease here evaluated. In patients with MD, previous experimental work with the scleral search coil led to the conclusion that a lower than normal gain of the VOR for head impulses in the plane of the horizontal semicircular canal of the diseased side was found in only 13.2% of patients, and abnormal gain asymmetry (between the affected and unaffected ears) in 29%. This value is much lower than the number of patients with abnormal unilateral caloric weakness as seen in 42.1% of the patients [10].

Canal function 1.0

0.8

Survivial

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11.42

0.6

0.4

0.2

0.0 0

5

10

15

20

25

Disease duration (years) Figure 2. Kaplan–Meier survival plot of the results in the video head-impulse test (vHIT) for each of the semicircular canals: in red for the ipsilesional side and in green for the contralesional side; circles represent the horizontal canal, upward triangles the posterior canal, and downward triangles the superior canal. The time domain is years since the definite diagnosis was given to the patient.

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Survivial

0.8

0.6

0.4

0.2

0.0 0

20

40

60

80

100

PTA Figure 3. Kaplan–Meier survival plot of the results in the video head-impulse test (vHIT) for each of the semicircular canals: red indicates the ipsilesional side and green the contralesional side; circles represent the horizontal canal, upward triangles the posterior canal, and downward triangles the superior canal. The time domain is pure-tone average (PTA).

We agree in that finding but did not perform a comparative evaluation with the caloric test here, because the aim of the study was to evaluate all the semicircular canals and in the case of the verticals a comparison would not be possible. However, previous work comparing the vHIT and the caloric test in patients with MD has shown similar differences for the ratio of normal to abnormal gain asymmetry in the vHIT and canal paresis [16]. The amount of abnormalities for the HSC found in the present study is very similar to those mentioned with the scleral search coil technique but lower when, in the definition of normal and abnormal vHIT, the appearance of refixation saccades is added [17]. There is not an in-depth analysis of refixation saccades in patients according to age either when saccades occur in patients with normal gain VOR: because of this, we did not include that finding in our classification of vHIT results. As we increase the number of semicircular canals to examine, the number of abnormalities also increases. With respect to other work with the scleral coil, gains of the VOR from the affected ear are not very similar, as ours are a little higher for the superior canal (SCC) and HSC but lower for the PSC [10]. The PSC response from the affected ear is most frequently abnormal and in the case of the unaffected ear the SSC; interestingly, the most frequently normal response is obtained from HSC testing. The significance of this finding is not clear, as in histopathologic reports of the affected ear of patients with MD the number of type I hair cells is not different from

normative data in all the five vestibular receptors [18]. Type I hair cells have specific properties and it is tempting to speculate that this may be where transduction of head impulses and the VOR response, as evaluated with high-frequency and high-velocity impulses, takes place. However, when analyzed in more detail some differences were found at the ultrastructural level in the end organs of the inner ear, as follows [19]. Between semicircular canals (loss of stereocilia is slightly more frequent in the HSC, but cellular vacuolization and increased intercellular stromal spaces is in the SSC) and between semicircular canal and otolithic: a monolayer of columnar shaped epithelial cells with a uniform-appearing cytoplasm, homogeneously staining nuclei aligned at the same level between the apical and basal surfaces of the cell substituting the neuroepithelium, and basement membrane thickening are more frequent in the semicircular canals and sacculus than in the utricle. Unfortunately the number of PSC specimens in that study was very low, but in two cases disclosed findings similar to the HSC and SSC. Monolayer formation and basement membrane thickening are correlated with the amount of vestibular deficit as measured with the caloric test but not with the disease duration. Differential effects of senescence in the vestibular end organs are another possible cause for our findings; however, still there is not a work to answer this possibility. We selected two clinical issues of interest to evaluate whether or not the vHIT characterization of the inner ear function in patients with MD could provide

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Ménière’s disease six canals insight into the progression or activity of the disease. We have seen that as the disease and hearing loss progress the number of abnormalities increase in the six semicircular canals, more in the ipsilesional side and in particular for the verticals and especially in the posterior. A trend to a predominant dysfunction of the posterior semicircular canal in the ipsilesional ear is clear; however, this needs a more detailed assessment coupled with the need to consider the time since the last vertigo attack (in days), as the gain of the VOR has been shown to change according to this factor [20]. In patients with early MD, while in the quiescent period the gain of the VOR for ipsilesional impulses was seen as normal or slightly enhanced, in crisis it typically became lower [6]. Interestingly, in patients who suffer Lermoyez-type vertigo attacks, the VOR gain on the affected side does not change during the crisis, but on the normal side is significantly reduced compared with pre-attack values [21]. As with several other measures of inner ear function in patients with unilateral MD, a proportion of abnormal results is obtained from the supposedly normal and unaffected ear. This amount is in the range of the proportion we have found, and establishes a new prospective assessment as to whether it may be an indication of a probable MD in the normal side. In conclusion, the distribution of abnormal results is not uniform between different canals in each patient; the most frequent gain reduction is obtained for the posterior canal. Gain reduction depends on the disease duration and amount of hearing loss. Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.

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[5] Kuo SW, Yang TH, Young YH. Change of vestibular evoked myogenic potentials after Meniere attack. Ann Otol Rhinol Laryngol 2005;114:717–21. [6] Manzari L, MacDougall HG, Burgess AM, Curthoys IS. New, fast, clinical vestibular tests identify whether a vertigo attack is due to early Ménière’s disease or vestibular neuritis. Laryngoscope 2013;123:507–11. [7] Belinchon A, Perez-Garrigues H, Tenias JM, Lopez A. Hearing assessment in Menière’s disease. Laryngoscope 2011; 121:622–6. [8] Weber KP, MacDougall HG, Halmagyi GM, Curthoys IS. Impulsive testing of semicircular-canal function using videooculography. Ann N Y Acad Sci 2009;1164:486–91. [9] Bartl K, Lehnen N, Kohlbecher S, Schneider E. Head impulse testing using video-oculography. Ann N Y Acad Sci 2009;1164:331–3. [10] Park HJ, Migliaccio AA, Della Santina CC, Minor LB, Carey JP. Search-coil head-thrust and caloric tests in Ménière’s disease. Acta Otolaryngol 2005;125:852–7. [11] Carey JP, Minor LB, Peng GC, Della Santina CC, Cremer PD, Haslwanter T. Changes in the three-dimensional angular vestibulo-ocular reflex following intratympanic gentamicin for Ménière’s disease. J Assoc Res Otolaryngol 2002;3:430–43. [12] Migliaccio AA, Cremer PD. The 2D modified head impulse test: a 2D technique for measuring function in all six semicircular canals. J Vestib Res 2011;21:227–34. [13] MacDougall HG, McGarvie LA, Halmagyi GM, Curthoys IS, Weber KP. Application of the video head impulse test to detect vertical semicircular canal dysfunction. Otol Neurotol 2013;34:974–9. [14] Agrawal Y, Schubert MC, Migliaccio AA, Zee DS, Schneider E, Lehnen N, et al. Evaluation of quantitative head impulse testing using search coils versus videooculography in older individuals. Otol Neurotol 2014;35: 283–8. [15] Newman-Toker DE, Kerber KA, Hsieh YH, Pula JH, Omron R, Saber Tehrani AS, et al. HINTS outperforms ABCD2 to screen for stroke in acute continuous vertigo and dizziness. Acad Emerg Med 2013;20:986–96. [16] Mahringer A, Rambold HA. Caloric test and video-headimpulse: a study of vertigo/dizziness patients in a community hospital. Eur Arch Otorhinolaryngol 2014;271:463–72. [17] Blödow A, Pannasch S, Walther LE. Detection of isolated covert saccades with the video head impulse test in peripheral vestibular disorders. Auris Nasus Larynx 2013;40:348–51. [18] Tsuji K, Velázquez-Villaseñor L, Rauch SD, Glynn RJ, Wall C 3rd, Merchant SN. Temporal bone studies of the human peripheral vestibular system. Meniere’s disease. Ann Otol Rhinol Laryngol Suppl 2000;181:26–31. [19] McCall AA, Ishiyama GP, Lopez IA, Bhuta S, Vetter S, Ishiyama A. Histopathological and ultrastructural analysis of vestibular endorgans in Meniere’s disease reveals basement membrane pathology. BMC Ear Nose Throat Disord 2009; 9:4. [20] Manzari L, Burgess AM, MacDougall HG, Bradshaw AP, Curthoys IS. Rapid fluctuations in dynamic semicircular canal function in early Ménière’s disease. Eur Arch Otorhinolaryngol 2011;268:637–9. [21] Manzari L, Burgess AM, Curthoys IS. Vestibular function in Lermoyez syndrome at attack. Eur Arch Otorhinolaryngol 2012;269:685–91.

The vestibulo-ocular reflex assessment in patients with Ménière's disease: examining all semicircular canals.

Abstract Conclusion: The distribution of abnormal results is not uniform between different canals in each patient; the most frequent gain reduction is...
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