- Email: [email protected]
Preliminary results of video Head Impulse Testing (vHIT) in children with cochlear implants
Accepted Manuscript Preliminary Results of Video Head Impulse Testing (vHIT) in Children with Cochlear Implants Nader Nassif, MD, Cristiano Balzanelli, MD, Luca Oscar Redaelli de Zinis, MD PII:
S0165-5876(16)30175-6
DOI:
10.1016/j.ijporl.2016.06.034
Reference:
PEDOT 8141
To appear in:
International Journal of Pediatric Otorhinolaryngology
Received Date: 29 March 2016 Revised Date:
11 June 2016
Accepted Date: 14 June 2016
Please cite this article as: N. Nassif, C. Balzanelli, L.O.R.d. Zinis, Preliminary Results of Video Head Impulse Testing (vHIT) in Children with Cochlear Implants, International Journal of Pediatric Otorhinolaryngology (2016), doi: 10.1016/j.ijporl.2016.06.034. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT
Title: Preliminary Results of Video Head Impulse Testing (vHIT) in Children with Cochlear Implants.
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Authors: Nader Nassif, MD; Cristiano Balzanelli, MD; Luca Oscar Redaelli de Zinis, MD
Affiliations:
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Department of Pediatric Otorhinolaryngology (N.N., L.O.R.D.Z.) and Department of Otorhinolaryngology, Head and Neck Surgery (C.B., L.O.R.D.Z.), Spedali Civili, University of Brescia, Italy
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Corresponding author:
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Nader Nassif Department of Pediatric Otorhinolaryngology, Spedali Civili Piazza Spedali Civili 1 25100 Brescia Italy Te. +390303996226 Fax +390303996009 E-mail: [email protected]
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Abstract Objective: to evaluate the lateral semicircular canal high frequency vestibulo-oculomotor reflex (LSC HF VOR) in children with cochlear implant.
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Methods: 16 children (10 females and 6 males, age range = 5-17 years) receiving a unilateral (n=12) or a bilateral (n=4) cochlear implant were included and compared to a control group of 20 age-matched normal-hearing (NH) children. Both implanted and NH children received a vestibular
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function test battery, including a Vestibulo-Ocular Reflex (VOR) gain assessment by means of a video-Head Impulse Test (vHIT), which represented the main outcome measure. In implanted
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subjects, vHIT was measured on both sides in the “CI-ON” and “CI-OFF” conditions. Results: Overall, no significant LSC HF VOR gain difference was found between CI users and NH peers. In the unilaterally implanted group, the LSC HF VOR gain measured in the “CI-ON” condition was significantly higher than in the “CI-OFF” condition, both in the implanted and in the non-
conditions, on either side.
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implanted ear. In the bilaterally implanted group there was no such a difference between the two
Conclusion: this is the first study investigating the LSC HF VOR gain in children with unilateral and
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bilateral CI. The study demonstrates that the LSC HF VOR of bilaterally implanted children is
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comparable to normal hearing children.
Keywords: cochlear implant; children; video Head Impulse Test; HF VOR
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1. Introduction Cochlear implants (CIs) restore hearing in adults and children affected by profound deafness. In early-treated congenitally deaf children, they allow a near normal development of speech
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understanding and production abilities.
Over the last years, concerns have arisen that CI surgery and CI electrical activity may negatively affect vestibular function, both in adult [1] and child recipients [2], by disrupting the delicate
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endolabyrinthine microenvironment. According to these speculations, bilateral CI surgery could impair the function of both vestibular labyrinths and cause a bilateral vestibular deficit, with
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severe implications on balance, postural control and daily life activities.
However, these studies do not seem to be consistent with routine clinical practice, where children’s balance and neuromotor development is hardly ever affected by CI surgery. Assessing the effect of CI on the vestibular function of pediatric subjects can be a challenging task
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because of poor cooperation, lack of normative data and frequent pre-operative vestibular impairment due to the underlying cause of deafness. The video-Head Impulse Test (vHIT) is a simple bedside test that allows evaluation of lateral semicircular canal (LSC) function, as well as
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the vertical canals, at high frequency stimulation (HF) with high efficiency also for children [3-5]. Its outcome measure is the HF Vestibulo-Ocular Reflex (VOR) gain, i.e. the ratio of eye velocity to
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head velocity, which in a perfectly functioning vestibular system is “1” for constant gaze during head rotation. Healthy subjects typically have a HF LSC VOR gain between 0.8-1.2 according to the normative data [6].
The aim of this observational, cross-sectional cohort study is to assess lateral semicircular canal (LSC) function in pediatric CI implant users, and to compare it to a control group of normal hearing (NH) children.
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The study hypothesis is that cochlear implantation in pediatric age does not affect HF LSC VOR negatively, and is therefore a safe procedure as far as LSC function is concerned.
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2. Materials and methods 2.1 Ethical considerations
The procedures followed were in accordance with the ethical standards of the Institution’s Review
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informed consent to participation in the study.
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Board and with the Helsinki Declaration. Parents of all included children gave their written
2.2 Study population
Patients were enrolled with the following inclusion criteria:
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pediatric age (< 18 years);
absence of inner ear malformations/ossification as assessed by pre-operative CT scan and MRI;
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parents’ willingness to participate in the study.
2.3 Procedures
Both implanted and NH children received a vestibular function test battery, including: - Basic bedside vestibular examination by means of Infrared Goggles System: spontaneous Nystagmus; positional Nystagmus (left and right side, supine); positioning nystagmus (Dix-Hallpike maneuvre, Roll-supine test); Head-Horizontal Shaking nystagmus; - Basic Bedside balance evaluation: Stretched arms test; Romberg test; Unterberger Fukuda test; 3
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- High frequency stimulation of Horizontal Vestibulo-Ocular Reflex (HF VOR) gain assessment by means of a vHIT, which represented the main outcome measure because of its feasibility in implanted children and high sensitivity in detecting canalar function [4,5]. In implanted subjects,
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vHIT was performed on both sides and in the “CI-ON” and “CI-OFF” conditions.
The vHIT was administered using ICS Impulse, GN Otometrics A/S, Denmark [technological characteristics: Inputs Head: 9 Axis Motion Sensor; Inputs Eye: Monocular (Right eye only);
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Sampling Rate: 250 fps - Impulse; Eye Tracking: 100 x 100 pixels - Impulse; OTOsuite® Vestibular software: Windows Graphical User Interface; High Performance Analysis Software; Database;
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Storage of Test Data; Sophisticated Patient and Test Data Management; Vision Denied for Testing in Complete Darkness; Patient calibration: Goggles have 2 built-in calibration lasers]. Subjects were seated 1 meter from a visual target mounted at eye level on the wall. The examiner stood behind the participant and delivered randomized (timing and direction) head impulses (100°/sec
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to 250°/sec peak head velocity) in the plane of the lateral semicircular canal, until approximately 20 acceptable head impulses were recorded. Responses were considered in terms of gain (eye velocity/head velocity), which was automatically calculated by the device software by dividing the
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area under the curve for eye velocity (with reset saccades removed) by the area under the curve
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for head velocity [7].
2.4 Statistical analysis
A Kolmogorov-Smirnov test was run in order to verify the normal distribution of continuous variables. In order to compare outcome variable changes within and between groups, both Student’s t test and two-way repeated-measures ANOVA (where possible) were conducted, the latter with Greenhouse-Geisser’s sphericity correction for epsilon values < 0.75. Significance was
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accepted for P values <0.05. The Medcalc® statistical software v12 (MedCalc Software bvba, Marienkerke, Beligum) was used.
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3. Results
The CI group consisted of 16 patients, 10 F and 6 M, aged 5-17 years (mean age 10±4 years), receiving their first CI at 6±4 years (range = 1-13 years). In this group, 4 patients were implanted
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bilaterally (3 of them simultaneously and 1 sequentially). Thus, a total of 20 implanted ears were considered. The demographics of implanted children included in the study are detailed in Table 1.
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The control group consisted of 20 subjects aged 10±3 years (range = 6-16 years), for a total 40 ears.
Results of bedside vestibular and balance function tests were normal both in the CI group (both CION and CI-OFF conditions and in the non-implanted ear) and in the NH subjects.
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First, in order to ascertain that implanted and NH subjects were matched well, LSC HF VOR gain was compared between non-implanted ears in deaf children and all ears in the NH group: the difference was not statistically significant (mean gain in the deaf group = 0.93±0.08, mean gain in
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the NH group = 0.89±0.07) (P = 0.2).
Secondly, in order to assess the effect of surgery, LSC HF VOR gain was compared between
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implanted and non-implanted ears in the 12 unilaterally implanted children, and the difference was not statistically significant (t=1.32, P= 0.2), as shown by figure 1. Last, the effect of CI switch-on and laterality were assessed by means of a two-way ANOVA model with Bonferroni correction, considering VOR gain in all the 20 implanted ears (12 of the unilateral CI users and 8 of bilateral CI users) as the continuous outcome variable, CI status (“ON” vs “OFF”) as within-subject factor and laterality of CI (unilateral vs bilateral) as between-subject factor. Results are illustrated in figure 2. While no effect of “laterality” on LSC HF VOR gain was observed 5
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[F (1.36) = 0.07, P = 0.8)], a significant effect of “CI configuration” was found [F (1.36) = 6.63, P = 0.01]; no significant interaction resulted between the within-subject and the between-subject factor (P = 0.3). Specifically, in the “CI ON” condition LSC HF VOR gain was higher than with the “CI
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OFF” condition both in unilaterally (1.02±0.17 vs. 0.89±0.08, P = 0.01) and bilaterally (0.97±0.05 vs. 0.92±0.08, P = 0.08) implanted children.
4. Discussion
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Changes in vestibular function after cochlear implantation have been investigated by several
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studies in the literature. In adults, changes are reported to occur in 20-40% of cases [1,8,9], while in children the prevalence ranges from 9 up to 50% [2,7,10-12]. This variability seems to be independent from surgical technique [13,14] even though minimally invasive electrode insertion techniques are now considered mandatory also for vestibular function preservation [15,16]. However, as far as pediatric age is concerned data are available mainly for school-aged children
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and adolescents, due to better cooperation during vestibular examination, while very little is known on implant-related vestibular function changes in younger prelingually deaf babies. Moreover, most studies report vestibular outcome many years after CI [2,7], so that it is not
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possible to establish whether the higher prevalence of vestibular dysfunction in CI children as
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compared to NH ones is an effect of CI or is due to the underlying disease. Post-mortem temporal bone studies suggest that CI does cause structural damage to the inner ear, including the posterior labyrinth [17,18]. Finally, studied populations generally include both unilaterally and bilaterally implanted children, but numbers are so small that it is impossible to say whether unilateral or bilateral CI represents an additional risk factor for vestibular dysfunction.
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This is the first study investigating function LSC HF VOR as measured by means of vHIT also in bilaterally implanted children, comparing the “CI-ON” and “CI-OFF” configurations, i.e. performing the test with the CI switched on and switched off, respectively.
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Our results show that deaf children’s non-implanted ear has a LSC HF VOR, which does not differ significantly from NH children’s.
This finding is not consistent with some past studies reporting that the prevalence of vestibular
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dysfunction in children with sensorineural hearing loss is higher than in NH subjects due to the mechanisms of disease underlying deafness. For example, it has been demonstrated that up to
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70% of children with sensorineural hearing loss have some degree of vestibular end-organ dysfunction [19], and that the prevalence of dysfunction is higher in children with profound hearing loss [20]. More recently, rotatory and collic Vestibular Evoked Myogenic Potential abnormalities have been described in children with sensorineural hearing loss compared to
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healthy peers [21-23]. These findings may seem discordant from ours, but in the above mentioned studies the cohort with hearing loss included several cases of Pendred syndrome, enlarged vestibular aqueduct and other cochlear malformations, together with cases of post-meningitis and
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Cytomegalovirus-related hearing loss. Children with these clinical pictures were excluded from our study, in order to avoid bias deriving from conditions that are well-known to affect vestibular
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function. Moreover, the aim of our study was to investigate only LSC HF VOR function, which is the most explored part of the posterior labyrinth. As second relevant finding in our study, there was no statistically significant difference in LSC HF VOR gain between the implanted and the non-implanted side in the unilaterally implanted children. This is consistent with studies in adult, unilaterally implanted patients [24,25], and also with research in children: investigating low frequencies of LSC function stimulation by means of
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caloric testing in unilaterally implanted children, Cushing et al [21,26,27] found no significant differences between implanted and contralateral ear. The increased LSC HF VOR gain in the “CI-ON” condition compared to the “CI-OFF” one supports
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the hypothesis of a direct effect of the electrical stimulation on vestibular receptors and vestibular nerve afferent neurons. This is consistent with preliminary studies on vestibular implants, suggesting that LSC HF VOR gain can be increased by means of electrodes stimulating the
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semicircular canals in adult patients with bilateral vestibular loss [28,29]. Possibly, the spread of excitation of electrodes in the basal turn of the cochlea, which are the nearest to the vestibule,
physiologic mechanism is still unknown.
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may reach the vestibular labyrinth and it could elicit an increase of LSC HF VOR gain, although the
The most important limitation of our study is that the analysis of LSC function has not been compared with caloric testing since there are evidences, during the initial attempts to validate
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vHIT comparing with caloric testing, that LSC HF VOR gain results abnormal only when vestibular deficit on caloric testing of the canal is higher than 40% [30]. The decision to perform vHIT without comparison with caloric testing was based on validation of vHIT testing in children made by other
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investigators who pointed out also the unpleasant sensations often caused by caloric and
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rotational testing in children [4,5,7].
5. Conclusion
Overall, testing vestibular function in children before and after CI is becoming increasingly important, in order to be able to formulate a prognosis for vestibular function itself and to choose the CI side. Our preliminary results on implanted children do not show a significant impairment of LSC HF VOR function compared to NH subjects. This suggests that both unilateral and simultaneous bilateral CI 8
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is a procedure that does not impair HF LSC function as far as it is analyzed by vHIT. Further studies are needed to confirm our preliminary results with complete vestibular testing (calorics, saccular-
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[9] A. Batuecas-Caletrio, M. Klumpp, S. Santacruz-Ruiz, F.B. Gonzalez, E.G. Sánchez, M. Arriaga. Vestibular function in cochlear implantation: Correlating objectiveness and subjectiveness. Laryngoscope. 125 (2015) 2371-5.
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[10] T. Jacot, E. Van Den Abbeele, H.R. Debre, S.R. Wiener-Vacher. Vestibular impairments preand post-cochlear implant in children. Int. J. Pediatr. Otorhinolaryngol. 73 (2009) 209-17.
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[13] J. Louza, L. Mertes, T. Braun, R. Gürkov, E. Krause. Influence of insertion depth in cochlear implantation on vertigo symptoms and vestibular function. Am J Otolaryngol. 36 (2015) 254-8. [14] Y.C. Rah, J.H. Park, J.H. Park, B.Y. Choi, J.W. Koo. Dizziness and vestibular function before and
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[19] J. Arnvig. Vestibular function in deafness and severe hardness of hearing. Acta Otolaryngol Head Neck Surg. 45 (1955) 283–8.
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[20] L. Sandberg, K. Terkildsen. Caloric tests in deaf children. Arch Otorhinolaryngol. 81 (1965)
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[24] A.A. Migliaccio, C..C Della Santina, J.P. Carey, J.K. Niparko, L.B. Minor. The vestibulo-ocular reflex response to head impulses rarely decreases after cochlear implantation. Otol Neurotol. 26
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[28] A. Perez Fornos, N. Guinand, R. van de Berg, R. Stokroos, S. Micera, H. Kingma, M Pelizzone, J.P. Guyot. Artificial balance: restoration of the vestibulo-ocular reflex in humans with a prototype vestibular neuroprosthesis. Front Neurol. (2014) 295-66.
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[29] N. Guinand, R. van de Berg, S. Cavuscens, R.J. Stokroos, M. Ranieri, M. Pelizzone, H. Kingma, J.P. Guyot, A. Perez-Fornos. Vestibular implants: 8 years of experience with electrical stimulation of the vestibular nerve in 11 patients with bilateral vestibular loss. ORL J Otorhinolaryngol Relat
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[30] M. Bartolomeo, R. Biboulet, G. Pierre, M. Mondain, A. Uziel, F. Venail. Value of the video head
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Otorhinolaryngol. 271 (2014) 681-8.
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impulse test in assessing vestibular deficits following vestibular neuritis. Eur Arch
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Figure legend Figure 1. Bars represent mean ± SEM of VOR gain in the implanted (left) and in the non-implanted (right) ear.
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bars: “CI OFF” configuration; black bars: “CI ON” configuration.
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Figure 2. Bars represent mean ± SEM of VOR gain in the unilateral and bilateral CI groups; gray
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Patient
Age at CI (years)
Sex
Etiology of deafness
CI model
CI side
right
1
F
Unknown, non syndromic
2
8
M
Cx26 homozygous
Cochlear (Nucleus Freedom)
3
6
F
Cx26 homozygous
Cochlear (Straight)
4
4
F
Cx26 homozygous
Cochlear (Soft Straight)
5
3
F
Prematurity
Cochlear (Soft Straight)
6
10
F
Unknown, non syndromic
Cochlear (Soft Straight)
left
7
6
M
Unknown, non syndromic
Cochlear (Soft Straight)
left
8
12
F
Unknown, non syndromic
9
7
F
Cx26 homozygous
10
10
M
11
13
M
12
2
M
13
1
15
16
Prematurity
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Unknown, non syndromic Unknown, non syndromic
Unknown, non syndromic
left
left
left
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14
F
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1
Cochlear (Nucleus Freedom)
AB (Hires120k)
right
left
Cochlear (Nucleus Freedom)
left
Cochlear (Nucleus Freedom)
right
Cochlear (CI512)
left
Cochlear (Nucleus Straight)
right
Cochlear (Nucleus Freedom)
bilateral
MED-EL (Synchrony 28 mm)
3
M
1
F
Cx26 homozygous
Cochlear (Freedom)
bilateral
2
F
Unknown, non syndromic
Cochlear (Freedom)
bilateral
Legend: CI, cochlear implant; F, female; M, male; Cx, Connexin Table 1 heading. Demographics of children included in the study.
bilateral
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S0165-5876(16)30175-6
DOI:
10.1016/j.ijporl.2016.06.034
Reference:
PEDOT 8141
To appear in:
International Journal of Pediatric Otorhinolaryngology
Received Date: 29 March 2016 Revised Date:
11 June 2016
Accepted Date: 14 June 2016
Please cite this article as: N. Nassif, C. Balzanelli, L.O.R.d. Zinis, Preliminary Results of Video Head Impulse Testing (vHIT) in Children with Cochlear Implants, International Journal of Pediatric Otorhinolaryngology (2016), doi: 10.1016/j.ijporl.2016.06.034. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT
Title: Preliminary Results of Video Head Impulse Testing (vHIT) in Children with Cochlear Implants.
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Authors: Nader Nassif, MD; Cristiano Balzanelli, MD; Luca Oscar Redaelli de Zinis, MD
Affiliations:
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Department of Pediatric Otorhinolaryngology (N.N., L.O.R.D.Z.) and Department of Otorhinolaryngology, Head and Neck Surgery (C.B., L.O.R.D.Z.), Spedali Civili, University of Brescia, Italy
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Corresponding author:
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Nader Nassif Department of Pediatric Otorhinolaryngology, Spedali Civili Piazza Spedali Civili 1 25100 Brescia Italy Te. +390303996226 Fax +390303996009 E-mail: [email protected]
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Abstract Objective: to evaluate the lateral semicircular canal high frequency vestibulo-oculomotor reflex (LSC HF VOR) in children with cochlear implant.
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Methods: 16 children (10 females and 6 males, age range = 5-17 years) receiving a unilateral (n=12) or a bilateral (n=4) cochlear implant were included and compared to a control group of 20 age-matched normal-hearing (NH) children. Both implanted and NH children received a vestibular
SC
function test battery, including a Vestibulo-Ocular Reflex (VOR) gain assessment by means of a video-Head Impulse Test (vHIT), which represented the main outcome measure. In implanted
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subjects, vHIT was measured on both sides in the “CI-ON” and “CI-OFF” conditions. Results: Overall, no significant LSC HF VOR gain difference was found between CI users and NH peers. In the unilaterally implanted group, the LSC HF VOR gain measured in the “CI-ON” condition was significantly higher than in the “CI-OFF” condition, both in the implanted and in the non-
conditions, on either side.
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implanted ear. In the bilaterally implanted group there was no such a difference between the two
Conclusion: this is the first study investigating the LSC HF VOR gain in children with unilateral and
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bilateral CI. The study demonstrates that the LSC HF VOR of bilaterally implanted children is
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comparable to normal hearing children.
Keywords: cochlear implant; children; video Head Impulse Test; HF VOR
1
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1. Introduction Cochlear implants (CIs) restore hearing in adults and children affected by profound deafness. In early-treated congenitally deaf children, they allow a near normal development of speech
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understanding and production abilities.
Over the last years, concerns have arisen that CI surgery and CI electrical activity may negatively affect vestibular function, both in adult [1] and child recipients [2], by disrupting the delicate
SC
endolabyrinthine microenvironment. According to these speculations, bilateral CI surgery could impair the function of both vestibular labyrinths and cause a bilateral vestibular deficit, with
M AN U
severe implications on balance, postural control and daily life activities.
However, these studies do not seem to be consistent with routine clinical practice, where children’s balance and neuromotor development is hardly ever affected by CI surgery. Assessing the effect of CI on the vestibular function of pediatric subjects can be a challenging task
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because of poor cooperation, lack of normative data and frequent pre-operative vestibular impairment due to the underlying cause of deafness. The video-Head Impulse Test (vHIT) is a simple bedside test that allows evaluation of lateral semicircular canal (LSC) function, as well as
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the vertical canals, at high frequency stimulation (HF) with high efficiency also for children [3-5]. Its outcome measure is the HF Vestibulo-Ocular Reflex (VOR) gain, i.e. the ratio of eye velocity to
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head velocity, which in a perfectly functioning vestibular system is “1” for constant gaze during head rotation. Healthy subjects typically have a HF LSC VOR gain between 0.8-1.2 according to the normative data [6].
The aim of this observational, cross-sectional cohort study is to assess lateral semicircular canal (LSC) function in pediatric CI implant users, and to compare it to a control group of normal hearing (NH) children.
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The study hypothesis is that cochlear implantation in pediatric age does not affect HF LSC VOR negatively, and is therefore a safe procedure as far as LSC function is concerned.
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2. Materials and methods 2.1 Ethical considerations
The procedures followed were in accordance with the ethical standards of the Institution’s Review
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informed consent to participation in the study.
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Board and with the Helsinki Declaration. Parents of all included children gave their written
2.2 Study population
Patients were enrolled with the following inclusion criteria:
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pediatric age (< 18 years);
absence of inner ear malformations/ossification as assessed by pre-operative CT scan and MRI;
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parents’ willingness to participate in the study.
2.3 Procedures
Both implanted and NH children received a vestibular function test battery, including: - Basic bedside vestibular examination by means of Infrared Goggles System: spontaneous Nystagmus; positional Nystagmus (left and right side, supine); positioning nystagmus (Dix-Hallpike maneuvre, Roll-supine test); Head-Horizontal Shaking nystagmus; - Basic Bedside balance evaluation: Stretched arms test; Romberg test; Unterberger Fukuda test; 3
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- High frequency stimulation of Horizontal Vestibulo-Ocular Reflex (HF VOR) gain assessment by means of a vHIT, which represented the main outcome measure because of its feasibility in implanted children and high sensitivity in detecting canalar function [4,5]. In implanted subjects,
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vHIT was performed on both sides and in the “CI-ON” and “CI-OFF” conditions.
The vHIT was administered using ICS Impulse, GN Otometrics A/S, Denmark [technological characteristics: Inputs Head: 9 Axis Motion Sensor; Inputs Eye: Monocular (Right eye only);
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Sampling Rate: 250 fps - Impulse; Eye Tracking: 100 x 100 pixels - Impulse; OTOsuite® Vestibular software: Windows Graphical User Interface; High Performance Analysis Software; Database;
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Storage of Test Data; Sophisticated Patient and Test Data Management; Vision Denied for Testing in Complete Darkness; Patient calibration: Goggles have 2 built-in calibration lasers]. Subjects were seated 1 meter from a visual target mounted at eye level on the wall. The examiner stood behind the participant and delivered randomized (timing and direction) head impulses (100°/sec
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to 250°/sec peak head velocity) in the plane of the lateral semicircular canal, until approximately 20 acceptable head impulses were recorded. Responses were considered in terms of gain (eye velocity/head velocity), which was automatically calculated by the device software by dividing the
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area under the curve for eye velocity (with reset saccades removed) by the area under the curve
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for head velocity [7].
2.4 Statistical analysis
A Kolmogorov-Smirnov test was run in order to verify the normal distribution of continuous variables. In order to compare outcome variable changes within and between groups, both Student’s t test and two-way repeated-measures ANOVA (where possible) were conducted, the latter with Greenhouse-Geisser’s sphericity correction for epsilon values < 0.75. Significance was
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accepted for P values <0.05. The Medcalc® statistical software v12 (MedCalc Software bvba, Marienkerke, Beligum) was used.
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3. Results
The CI group consisted of 16 patients, 10 F and 6 M, aged 5-17 years (mean age 10±4 years), receiving their first CI at 6±4 years (range = 1-13 years). In this group, 4 patients were implanted
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bilaterally (3 of them simultaneously and 1 sequentially). Thus, a total of 20 implanted ears were considered. The demographics of implanted children included in the study are detailed in Table 1.
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The control group consisted of 20 subjects aged 10±3 years (range = 6-16 years), for a total 40 ears.
Results of bedside vestibular and balance function tests were normal both in the CI group (both CION and CI-OFF conditions and in the non-implanted ear) and in the NH subjects.
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First, in order to ascertain that implanted and NH subjects were matched well, LSC HF VOR gain was compared between non-implanted ears in deaf children and all ears in the NH group: the difference was not statistically significant (mean gain in the deaf group = 0.93±0.08, mean gain in
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the NH group = 0.89±0.07) (P = 0.2).
Secondly, in order to assess the effect of surgery, LSC HF VOR gain was compared between
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implanted and non-implanted ears in the 12 unilaterally implanted children, and the difference was not statistically significant (t=1.32, P= 0.2), as shown by figure 1. Last, the effect of CI switch-on and laterality were assessed by means of a two-way ANOVA model with Bonferroni correction, considering VOR gain in all the 20 implanted ears (12 of the unilateral CI users and 8 of bilateral CI users) as the continuous outcome variable, CI status (“ON” vs “OFF”) as within-subject factor and laterality of CI (unilateral vs bilateral) as between-subject factor. Results are illustrated in figure 2. While no effect of “laterality” on LSC HF VOR gain was observed 5
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[F (1.36) = 0.07, P = 0.8)], a significant effect of “CI configuration” was found [F (1.36) = 6.63, P = 0.01]; no significant interaction resulted between the within-subject and the between-subject factor (P = 0.3). Specifically, in the “CI ON” condition LSC HF VOR gain was higher than with the “CI
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OFF” condition both in unilaterally (1.02±0.17 vs. 0.89±0.08, P = 0.01) and bilaterally (0.97±0.05 vs. 0.92±0.08, P = 0.08) implanted children.
4. Discussion
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Changes in vestibular function after cochlear implantation have been investigated by several
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studies in the literature. In adults, changes are reported to occur in 20-40% of cases [1,8,9], while in children the prevalence ranges from 9 up to 50% [2,7,10-12]. This variability seems to be independent from surgical technique [13,14] even though minimally invasive electrode insertion techniques are now considered mandatory also for vestibular function preservation [15,16]. However, as far as pediatric age is concerned data are available mainly for school-aged children
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and adolescents, due to better cooperation during vestibular examination, while very little is known on implant-related vestibular function changes in younger prelingually deaf babies. Moreover, most studies report vestibular outcome many years after CI [2,7], so that it is not
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possible to establish whether the higher prevalence of vestibular dysfunction in CI children as
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compared to NH ones is an effect of CI or is due to the underlying disease. Post-mortem temporal bone studies suggest that CI does cause structural damage to the inner ear, including the posterior labyrinth [17,18]. Finally, studied populations generally include both unilaterally and bilaterally implanted children, but numbers are so small that it is impossible to say whether unilateral or bilateral CI represents an additional risk factor for vestibular dysfunction.
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This is the first study investigating function LSC HF VOR as measured by means of vHIT also in bilaterally implanted children, comparing the “CI-ON” and “CI-OFF” configurations, i.e. performing the test with the CI switched on and switched off, respectively.
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Our results show that deaf children’s non-implanted ear has a LSC HF VOR, which does not differ significantly from NH children’s.
This finding is not consistent with some past studies reporting that the prevalence of vestibular
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dysfunction in children with sensorineural hearing loss is higher than in NH subjects due to the mechanisms of disease underlying deafness. For example, it has been demonstrated that up to
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70% of children with sensorineural hearing loss have some degree of vestibular end-organ dysfunction [19], and that the prevalence of dysfunction is higher in children with profound hearing loss [20]. More recently, rotatory and collic Vestibular Evoked Myogenic Potential abnormalities have been described in children with sensorineural hearing loss compared to
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healthy peers [21-23]. These findings may seem discordant from ours, but in the above mentioned studies the cohort with hearing loss included several cases of Pendred syndrome, enlarged vestibular aqueduct and other cochlear malformations, together with cases of post-meningitis and
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Cytomegalovirus-related hearing loss. Children with these clinical pictures were excluded from our study, in order to avoid bias deriving from conditions that are well-known to affect vestibular
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function. Moreover, the aim of our study was to investigate only LSC HF VOR function, which is the most explored part of the posterior labyrinth. As second relevant finding in our study, there was no statistically significant difference in LSC HF VOR gain between the implanted and the non-implanted side in the unilaterally implanted children. This is consistent with studies in adult, unilaterally implanted patients [24,25], and also with research in children: investigating low frequencies of LSC function stimulation by means of
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caloric testing in unilaterally implanted children, Cushing et al [21,26,27] found no significant differences between implanted and contralateral ear. The increased LSC HF VOR gain in the “CI-ON” condition compared to the “CI-OFF” one supports
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the hypothesis of a direct effect of the electrical stimulation on vestibular receptors and vestibular nerve afferent neurons. This is consistent with preliminary studies on vestibular implants, suggesting that LSC HF VOR gain can be increased by means of electrodes stimulating the
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semicircular canals in adult patients with bilateral vestibular loss [28,29]. Possibly, the spread of excitation of electrodes in the basal turn of the cochlea, which are the nearest to the vestibule,
physiologic mechanism is still unknown.
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may reach the vestibular labyrinth and it could elicit an increase of LSC HF VOR gain, although the
The most important limitation of our study is that the analysis of LSC function has not been compared with caloric testing since there are evidences, during the initial attempts to validate
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vHIT comparing with caloric testing, that LSC HF VOR gain results abnormal only when vestibular deficit on caloric testing of the canal is higher than 40% [30]. The decision to perform vHIT without comparison with caloric testing was based on validation of vHIT testing in children made by other
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investigators who pointed out also the unpleasant sensations often caused by caloric and
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rotational testing in children [4,5,7].
5. Conclusion
Overall, testing vestibular function in children before and after CI is becoming increasingly important, in order to be able to formulate a prognosis for vestibular function itself and to choose the CI side. Our preliminary results on implanted children do not show a significant impairment of LSC HF VOR function compared to NH subjects. This suggests that both unilateral and simultaneous bilateral CI 8
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is a procedure that does not impair HF LSC function as far as it is analyzed by vHIT. Further studies are needed to confirm our preliminary results with complete vestibular testing (calorics, saccular-
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impulse test in assessing vestibular deficits following vestibular neuritis. Eur Arch
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Figure legend Figure 1. Bars represent mean ± SEM of VOR gain in the implanted (left) and in the non-implanted (right) ear.
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bars: “CI OFF” configuration; black bars: “CI ON” configuration.
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Figure 2. Bars represent mean ± SEM of VOR gain in the unilateral and bilateral CI groups; gray
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Patient
Age at CI (years)
Sex
Etiology of deafness
CI model
CI side
right
1
F
Unknown, non syndromic
2
8
M
Cx26 homozygous
Cochlear (Nucleus Freedom)
3
6
F
Cx26 homozygous
Cochlear (Straight)
4
4
F
Cx26 homozygous
Cochlear (Soft Straight)
5
3
F
Prematurity
Cochlear (Soft Straight)
6
10
F
Unknown, non syndromic
Cochlear (Soft Straight)
left
7
6
M
Unknown, non syndromic
Cochlear (Soft Straight)
left
8
12
F
Unknown, non syndromic
9
7
F
Cx26 homozygous
10
10
M
11
13
M
12
2
M
13
1
15
16
Prematurity
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Unknown, non syndromic Unknown, non syndromic
Unknown, non syndromic
left
left
left
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14
F
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1
Cochlear (Nucleus Freedom)
AB (Hires120k)
right
left
Cochlear (Nucleus Freedom)
left
Cochlear (Nucleus Freedom)
right
Cochlear (CI512)
left
Cochlear (Nucleus Straight)
right
Cochlear (Nucleus Freedom)
bilateral
MED-EL (Synchrony 28 mm)
3
M
1
F
Cx26 homozygous
Cochlear (Freedom)
bilateral
2
F
Unknown, non syndromic
Cochlear (Freedom)
bilateral
Legend: CI, cochlear implant; F, female; M, male; Cx, Connexin Table 1 heading. Demographics of children included in the study.
bilateral
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