G Model
ANL-1859; No. of Pages 4 Auris Nasus Larynx xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
Auris Nasus Larynx journal homepage: www.elsevier.com/locate/anl
Vestibular evoked myogenic potentials in children after cochlear implantation George Psillas MD*, Alexandra Pavlidou MD, Nikos Lefkidis MD, Iosif Vital MD, Konstantinos Markou MD, Stefanos Triaridis MD, Miltiadis Tsalighopoulos MD 1st Academic ENT Department, Aristotle University of Thessaloniki, AHEPA Hospital, 1, Stilponos Kyriakidi St., GR 546 36 Thessaloniki, Greece
A R T I C L E I N F O
A B S T R A C T
Article history: Received 2 February 2014 Accepted 2 May 2014 Available online xxx
Objective: The aim of this study was to report the effect of unilateral cochlear implantation to vestibular system using vestibular evoked myogenic potentials (VEMPs) by air-conduction in a sample of children aged less than 5 years. Materials: This study consisted of 10 children (6 boys and 4 girls), who underwent cochlear implantation surgery at our clinic, and 8 normal hearing children (5 boys and 3 girls) matched for age. The VEMPs were performed before, 10 days, and 6 months after surgery. Both the implanted and unimplanted ears of each child were evaluated, with the cochlear implant both off and on. Results: Preoperatively, six (60%) children had abnormal VEMPs responses on both ears. In the postoperative sessions, no child showed any VEMPs response on the implanted side. The VEMPs were not recorded on the unimplanted side either, except for one case. At 6 months, the VEMPs response on the unimplanted side of three children became normal when the cochlear implant was on, and in two children with the device off. Conclusion: In the postoperative 6-month-period, the disappearance of VEMPs suggests that the saccule of children can be extensively damaged following cochlear implantation. A recovery of VEMPs can take place on the unimplanted side, with the cochlear implant both on and off. Despite this saccular injury, the absence of clinical signs in children could be explained by their ability to effectively compensate for such vestibular deficits. ß 2014 Published by Elsevier Ireland Ltd.
Keywords: Vestibular evoked myogenic potentials Cochlear implantation Saccule Vestibular function Children
1. Introduction Cochlear implantation is currently the procedure of choice to rehabilitate deaf born and postlingually deaf people. Although cochlear implantation is surgically safe, balance disorders in the postoperative period have been reported in 30–75% of the cases [1– 3]. Possible causes for vestibular symptoms after cochlear implantation include direct surgical trauma of vestibular receptors due to the electrode insertion into the cochlea and disturbance of inner ear fluids, with subsequent loss of the afferent vestibular pathways [4,5]. According to the literature, cochlear implant may affect vestibular function in children in a high proportion of cases (50–85% of cases), based on the findings of different vestibular laboratory tests [6–8]. However, unlike adult patients, few vestibular tests are well tolerated by children; for example, the
caloric testing, although very useful for the evaluation of peripheral vestibular system, is not really accepted by children [6]. We therefore used in this study the vestibular-evoked myogenic potentials (VEMPs) testing by air-conduction, which is easily applicable to children. The VEMPs assess the otolith organ and mainly the saccule, and the inferior vestibular nerve function. During VEMPs testing, a high-level, click or short tone-burst acoustic stimulus is presented into the ear, and a short latency electromyogram response is recorded from the tonically contracted sternocleidomastoid muscle. Recorded responses in healthy subjects show a biphasic waveform with a positive peak (p13) and a negative peak (n23) [9]. The purpose of this study was to report the effect of unilateral cochlear implantation to vestibular system using VEMPs by airconduction in a sample of children aged less than 5 years. 2. Materials and methods
* Corresponding author. Tel.: +30 2310 994 762; fax: +30 2310 994 916. E-mail address: [email protected] (G. Psillas).
This study examined 10 children (Table 1), 6 boys and 4 girls, aged 1.5 to 4 years (mean age: 2.85 years), who underwent
http://dx.doi.org/10.1016/j.anl.2014.05.008 0385-8146/ß 2014 Published by Elsevier Ireland Ltd.
Please cite this article in press as: Psillas G, et al. Vestibular evoked myogenic potentials in children after cochlear implantation. Auris Nasus Larynx (2014), http://dx.doi.org/10.1016/j.anl.2014.05.008
G Model
ANL-1859; No. of Pages 4 G. Psillas et al. / Auris Nasus Larynx xxx (2014) xxx–xxx
2
cochlear implantation surgery at our clinic. These children were affected by congenital idiopathic deafness without inner ear dysplasia or syndrome. All the children received cochlear implant in the right ear by our cochlear implant team (consisting of three surgeons); six children were implanted with Freedom implant (Cochlear Contour) (subjects 1–5, 8) and four with Medel Sonata (subjects 6, 7, 9, 10). Our routine procedure consisted of a cortical mastoidectomy, posterior tympanotomy and electrode insertion through the classic cochleostomy located anteroinferior to the round window. A control group of eight normal hearing children, five boys and three girls, matched for age (mean age: 3 years, range 2–5 years) were also used. Informed consent was obtained from the parents of all participating children. The study was approved by the Bioethics Committee of the Medical School of Thessaloniki. The VEMPs were recorded in a soundproof room by means of an Amplaid MK 12 with the children lying supine on a comfortable bed at an approximately 308 angle from the floor. Electrodes were located at the junction middle and upper third of the sternocleidomastoid muscle for each side stimulated, with the reference electrode placed on the middle of the clavicle and a third electrode was placed on the forehead as a ground. During the recording session the children were instructed to stretch their arms right to front of them and simultaneously to turn their heads in the direction contralateral to the stimulated ear in order to unilaterally contract the sternocleidomastoid muscle; at the same time, pendulous oscillating toys were used over their head to distract them and to keep them still and lying during the test. The electrode impedance checked before each recording was below 5 kV. Monoaural stimulation was induced using a 500 Hz positive logon of negative polarity in the earphone (TDH 49). The electromyographic signals were amplified and band-pass filtered from 10 to 2000 Hz and recorded at a constant level for each child. The intensity of the signal was fixed at 130 dB sound pressure level (SPL) at a rate of four signals per second. VEMPs were obtained in a 100 ms-window with a 25 mV/div-amplitude scale, in response to 200 stimuli; a second recording was made to check the reliability of the response. A normal VEMPs tracing was considered as a biphasic waveform with a positive peak (p13) and a negative peak (n23). In order to establish the VEMPs’ normal parameters, the amplitude of the first positive–negative peak (p13–n23) and the latencies of p13 and n23 were assessed in both ears in the control group. However, an
amplitude less than 65 mV was considered as decreased; an absent reflex was defined as an amplitude less than 20 mV or if an unrecognizable tracing was obtained. In order to evaluate the VEMPs reproducibility, the children of the control group were retested with VEMPs after a time of 3 months. For the study group, the VEMPs were first recorded just before the operation. In the postoperative period, VEMPs were evaluated at 10 days and 6 months after surgery, when the cochlear implant was both off and on. Statistical analysis was performed using Student’s t-test (p > 0.05; SPSS 10.0).
3. Results In the control group, the mean amplitude was 142 (SD, 51 mV) and the mean latency of p13 and n23 was 15.6 2.2 ms and 24.1 3.3 ms, respectively. In the same group, 3 months later, no statistically significant difference was found, as the mean amplitude was 154 (SD, 46) (p > 0.05), the mean latency of p13 and n23 was 16.1 2.4 ms (p > 0.05), and 23.6 3.5 ms (p > 0.05), respectively; thus, although our sample was small, the VEMPs could be considered as a reliable diagnostic testing for the young children. It should also be mentioned that the VEMPs were recorded in all ears in this group in both sessions. Preoperatively, in the study group, 4 (40%) out of 10 children showed normal VEMPs in at least one ear (Table 1, Figs. 1A and 2A). In three children, VEMPs amplitude was reduced and in other three children, VEMPs were not elicited on both sides. The mean p13 latency was found normal (16.3 1.6 ms) compared to the control group (p > 0.05). The mean n23 latency was found significantly increased (26.5 2.5 ms) compared to the control group (p < 0.05). Postoperatively, on the 10th day and 6 months after cochlear implantation, no VEMPs were produced in any child on the operated side (Table 1 and Fig. 1B–E). However, no child suffered from dizziness, vertigo, or instability, and no nystagmus was observed. Interestingly, the VEMPs were not recorded on the 10th postoperative day not only on the implanted side but also on the contralateral unimplanted side either (Fig. 2B–C), except for cases 4 and 10; in those children, the VEMPs amplitude was normal (case 4) or reduced (case 10), when the cochlear implant was off
Table 1 Children characteristics and pre-, postoperative results of VEMPs on both sides (R: right, L: left). CI: cochlear implantation –: no VEMPs elicited. Patient/sex
Age (year) of CI
Before CI
Post-10 days CI off
CI on
CI off
CI on
R: normal L: normal R: – L: – R: normal L: normal R: normal L: normal R: – L: normal R: – L: – R: decreased L: – R: – L: – R: decreased L: decreased R: decreased L: decreased
R: – L: – R: – L: – R: – L: – R: – L: normal R: – L: – R: – L: – R: – L: – R: – L: – R: – L: – R: – L: decreased
R: – L: – R: – L: – R: – L: – R: – L: normal R: – L: – R: – L: – R: – L: – R: – L: – R: – L: – R: – L: decreased
R: – L: – R: – L: – R: – L: decreased R: – L: – R: – L: normal R: – L: – R: – L: – R: – L: – R: – L: – R: – L: normal
R: – L: – R: – L: – R: – L: normal R: – L: – R: – L: normal R: – L: – R: – L: – R: – L: – R: – L: – R: – L: normal
1.
K.A., F
4
2.
K.S., M
3.5
3.
M.K., F
2.5
4.
A.T., M
4
5.
M.A., F
2
6.
M.E., M
3
7.
P.A., M
1.5
8.
I.R., F
3
9.
D.D., M
3
10.
P.V., M
2
Post-6 months
Please cite this article in press as: Psillas G, et al. Vestibular evoked myogenic potentials in children after cochlear implantation. Auris Nasus Larynx (2014), http://dx.doi.org/10.1016/j.anl.2014.05.008
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ANL-1859; No. of Pages 4 G. Psillas et al. / Auris Nasus Larynx xxx (2014) xxx–xxx
3
4. Discussion
Fig. 1. VEMPs of case 1 (right ear, implanted side). (A) Normal VEMPs before cochlear implantation. (B and C) On the 10th postoperative day, absence of VEMPs when the cochlear implant was off and on, respectively. (D and E) Six months later, absence of VEMPs, when the cochlear implant was off and on, respectively.
and on. Six months later, no VEMPs response was produced in child 4, and in child 10 the VEMPs amplitude became normal. Moreover, 6 months after cochlear implantation, the VEMPs response on the unimplanted side of three (30%) children (cases 3, 5, 10) became normal when the cochlear implant was on (Fig. 2E); when the cochlear implant was off, the VEMPs response was normal in children 5 and 10, and reduced in child 3 (Fig. 2D). In the remaining cases, no VEMPs were produced on the unimplanted side.
Fig. 2. VEMPs of case 3 (left side, unimplanted side). (A) Normal VEMPs before cochlear implantation. (B and C) On the 10th postoperative day, absence of VEMPs when the cochlear implant was off and on, respectively. (D and E) Six months later, appearance of reduced VEMPs, when the cochlear implant was off and normal VEMPs when the cochlear implant was on, respectively.
In the preoperative period, six (60%) children showed abnormal VEMPs responses on both sides; in other reports [8,10], approximately half of the severely hearing impaired children presented with pathological VEMPs. After cochlear implantation, no VEMPs could be recorded by airconduction in any of our children on the operated side. Histopathologic studies have demonstrated that during cochlear implantation the saccule is the most frequent site of damage in the vestibular system, followed by the utricle and semicircular canals [11,12]. This is due to the fact that the saccule is more proximal to the inserted electrode than the utricle or semicircular canals, regardless of whether the classical cochleostomy or round window approach was performed [11]. Morphological changes can be present such as saccular membrane distortion, loss of saccular membrane, saccular collapse or hydrops, and local fibrosis [11,12]; these saccular alterations may be induced by the insertion trauma of the cochlear implant electrode [2] or resulted indirectly from obstruction of the ductus reuniens (which connects the endolymphatic space between the cochlear duct and the saccule) by debris surgically produced [12]. Basta et al. [2] also found that no VEMPs responses were elicited up to the 6th postoperative week after cochlear implantation in patients aged 10–75 years. However, a lesser extent of saccular damage was reported in children after cochlear implantation; Jin et al. [13] demonstrated that when the cochlear implant was off just after the operation, 11 (91%) out of 12 children (aged 2–7 years) showed no response in VEMPs and one child showed a decreased VEMPs amplitude; when the device was on, eight (66%) showed no response, three (25%) a normal response and one increased VEMPs amplitude; it was possible that the VEMPs were induced by activation of the device as a result of electrical stimulation on the vestibular nerve [5,14]. This observation did not corroborate our results as in our study the VEMPs remained absent irrespective of device activation. Finally, Licameli et al. [6], in a population of 15 older children (aged 5–22 years) until 6 weeks after cochlear implantation, found that 20% of them had absent VEMPs response, 60% of children had reduced and 20% had normal VEMPs response. According to our results, nine children (except for case 4) had abnormal VEMPs responses not only on the implanted side but also on the unimplanted ear either. This unusual finding was not reported elsewhere in VEMPs studies, but it has already been described for the caloric response, which was reduced after cochlear implantation on the unimplanted ear as on the implanted one [14,15]. However, the underlying mechanism which could explain the saccular suppression in the acute postoperative period on both sides is still unknown. Moreover, our three (30%) children (cases 3, 5, 10) showed recovery of VEMPs responses to the normal range on the unimplanted side 6 months after the cochlear implantation. Similar to VEMPs, the caloric response can also return to normal response on the non-operated side within 3–6 months following cochlear implantation [5,16] or after vestibular nerve section [15]. Riba´ry et al. [5] attributed the recovery of caloric response in the implanted and unimplanted ear to the effect of chronic electrical stimulation on the labyrinth. Despite the VEMPs findings, none of our children seemed to postoperatively suffer from dizziness or vertigo and no nystagmus was observed. In adults, approximately 50% of the cases with total loss of VEMPs complained of dizziness for more than 3 months after cochlear implantation [2]. This difference could be attributed on the important capacity of children to better compensate and rapidly adapt to vestibular injury compared to adults [7,17]. In a previous work, Tahara et al. [18] have demonstrated that in children suffering from vestibular neuritis the nystagmus disappeared earlier compared
Please cite this article in press as: Psillas G, et al. Vestibular evoked myogenic potentials in children after cochlear implantation. Auris Nasus Larynx (2014), http://dx.doi.org/10.1016/j.anl.2014.05.008
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to adults, and caloric paresis remained over a longer period in adults than in children. It is evident that our findings were based on a small sample and there was a great variability among the children of this study; however, according to our results, the sacculi of children were easily affected following cochlear implantation. Although this vestibular damage occurred not only in the implanted ear, but also on the unimplanted side, the children had no vestibular complaint and did not show vestibular symptoms. Nonetheless, the potential of negative effect on vestibular function following cochlear implantation should be explained to parents and that vestibular disturbances may appear in long-term. Conflict of interest None. References [1] Fina M, Skinner M, Goebel JA, Piccirillo JF, Neely JG, Black O. Vestibular dysfunction after cochlear implantation. Otol Neurotol 2003;24:234–42. [2] Basta D, Todt I, Goepel F, Ernst A. Loss of saccular function after cochlear implantation: the diagnostic impact of intracochlear electrically elicited vestibular evoked myogenic potentials. Audiol Neurootol 2008;13:187–92. [3] Steenerson RL, Cronin GW, Gary LB. Vertigo after cochlear implantation. Otol Neurotol 2001;22:842–3. [4] Todt I, Basta D, Ernst A. Does the surgical approach in cochlear implantation influence the occurrence of postoperative vertigo. Otolaryngol Head Neck Surg 2008;138:8–12.
[5] Riba´ri O, Ku¨stel M, Szirmai A, Re´pa´ssy G. Cochlear implantation influences contralateral hearing and vestibular responsiveness. Acta Otolaryngol 1999;119:225–8. [6] Licameli G, Zhou G, Kenna MA. Disturbance of vestibular function attributable to cochlear implantation in children. Laryngoscope 2009;119:740–5. [7] Jacot E, Van Den Abbeele T, Debre HR, Wiener-Vacher SR. Vestibular impairments pre- and post-cochlear implants in children. Int J Pediatr Otorhinolaryngol 2009;73:209–17. [8] Shinjo Y, Jin Y, Kaga K. Assessment of vestibular function of infants and children with congenital and acquired deafness using the ice-water caloric test, rotational chair test and vestibular-evoked myogenic potential recording. Acta Otolaryngol 2007;127:736–47. [9] Maes L, Vinck BM, De Vel E, D’haenens W, Bockstael A, Keppler H, et al. The vestibular evoked myogenic potential: a test–retest reliability study. Clin Neurophysiol 2009;120:594–660. [10] Cushing SL, Gordon KA, Rutka JA, James AL, Papsin BC. Vestibular end-organ dysfunction in children with sensorineural hearing loss and cochlear implants: an expanded cohort and etiologic assessment. Otol Neurotol 2013;34:422–8. [11] Tien HC, Linthicum Jr FH. Histopathologic changes in the vestibule after cochlear implantation. Otolaryngol Head Neck Surg 2002;127:260–4. [12] Handzel O, Burgess BJ, Nadol Jr JB. Histopathology of the peripheral vestibular system after cochlear implantation in the human. Otol Neurotol 2006;27:57– 64. [13] Jin Y, Nakamura M, Shinjo Y, Kaga K. Vestibular-evoked myogenic potentials in cochlear implant children. Acta Otolaryngol 2006;126:164–9. [14] Buchman CA, Joy J, Hodges A, Telischi FF, Balkany TJ. Vestibular effects of cochlear implantation. Laryngoscope 2004;114(Suppl. 103):1–22. [15] Cass SP, Kartush JM, Graham MD. Patterns of vestibular function following vestibular nerve section. Laryngoscope 1992;102:388–94. [16] Vibert D, Ha¨usler R, Kompis M, Vischer M. Vestibular function in patients with cochlear implantation. Acta Otolaryngol Suppl 2001;545:29–34. [17] Cushing SL, Chia R, James AL, Papsin BC, Gordon KA. A test of static and dynamic balance function in children with cochlear implants: the vestibular olympics. Arch Otolaryngol Head Neck Surg 2008;134:34–8. [18] Tahara T, Sekitani T, Imate Y, Kanesada K, Okami M. Vestibular neuronitis in children. Acta Otolaryngol Suppl 1993;503:49–52.
Please cite this article in press as: Psillas G, et al. Vestibular evoked myogenic potentials in children after cochlear implantation. Auris Nasus Larynx (2014), http://dx.doi.org/10.1016/j.anl.2014.05.008
ANL-1859; No. of Pages 4 Auris Nasus Larynx xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
Auris Nasus Larynx journal homepage: www.elsevier.com/locate/anl
Vestibular evoked myogenic potentials in children after cochlear implantation George Psillas MD*, Alexandra Pavlidou MD, Nikos Lefkidis MD, Iosif Vital MD, Konstantinos Markou MD, Stefanos Triaridis MD, Miltiadis Tsalighopoulos MD 1st Academic ENT Department, Aristotle University of Thessaloniki, AHEPA Hospital, 1, Stilponos Kyriakidi St., GR 546 36 Thessaloniki, Greece
A R T I C L E I N F O
A B S T R A C T
Article history: Received 2 February 2014 Accepted 2 May 2014 Available online xxx
Objective: The aim of this study was to report the effect of unilateral cochlear implantation to vestibular system using vestibular evoked myogenic potentials (VEMPs) by air-conduction in a sample of children aged less than 5 years. Materials: This study consisted of 10 children (6 boys and 4 girls), who underwent cochlear implantation surgery at our clinic, and 8 normal hearing children (5 boys and 3 girls) matched for age. The VEMPs were performed before, 10 days, and 6 months after surgery. Both the implanted and unimplanted ears of each child were evaluated, with the cochlear implant both off and on. Results: Preoperatively, six (60%) children had abnormal VEMPs responses on both ears. In the postoperative sessions, no child showed any VEMPs response on the implanted side. The VEMPs were not recorded on the unimplanted side either, except for one case. At 6 months, the VEMPs response on the unimplanted side of three children became normal when the cochlear implant was on, and in two children with the device off. Conclusion: In the postoperative 6-month-period, the disappearance of VEMPs suggests that the saccule of children can be extensively damaged following cochlear implantation. A recovery of VEMPs can take place on the unimplanted side, with the cochlear implant both on and off. Despite this saccular injury, the absence of clinical signs in children could be explained by their ability to effectively compensate for such vestibular deficits. ß 2014 Published by Elsevier Ireland Ltd.
Keywords: Vestibular evoked myogenic potentials Cochlear implantation Saccule Vestibular function Children
1. Introduction Cochlear implantation is currently the procedure of choice to rehabilitate deaf born and postlingually deaf people. Although cochlear implantation is surgically safe, balance disorders in the postoperative period have been reported in 30–75% of the cases [1– 3]. Possible causes for vestibular symptoms after cochlear implantation include direct surgical trauma of vestibular receptors due to the electrode insertion into the cochlea and disturbance of inner ear fluids, with subsequent loss of the afferent vestibular pathways [4,5]. According to the literature, cochlear implant may affect vestibular function in children in a high proportion of cases (50–85% of cases), based on the findings of different vestibular laboratory tests [6–8]. However, unlike adult patients, few vestibular tests are well tolerated by children; for example, the
caloric testing, although very useful for the evaluation of peripheral vestibular system, is not really accepted by children [6]. We therefore used in this study the vestibular-evoked myogenic potentials (VEMPs) testing by air-conduction, which is easily applicable to children. The VEMPs assess the otolith organ and mainly the saccule, and the inferior vestibular nerve function. During VEMPs testing, a high-level, click or short tone-burst acoustic stimulus is presented into the ear, and a short latency electromyogram response is recorded from the tonically contracted sternocleidomastoid muscle. Recorded responses in healthy subjects show a biphasic waveform with a positive peak (p13) and a negative peak (n23) [9]. The purpose of this study was to report the effect of unilateral cochlear implantation to vestibular system using VEMPs by airconduction in a sample of children aged less than 5 years. 2. Materials and methods
* Corresponding author. Tel.: +30 2310 994 762; fax: +30 2310 994 916. E-mail address: [email protected] (G. Psillas).
This study examined 10 children (Table 1), 6 boys and 4 girls, aged 1.5 to 4 years (mean age: 2.85 years), who underwent
http://dx.doi.org/10.1016/j.anl.2014.05.008 0385-8146/ß 2014 Published by Elsevier Ireland Ltd.
Please cite this article in press as: Psillas G, et al. Vestibular evoked myogenic potentials in children after cochlear implantation. Auris Nasus Larynx (2014), http://dx.doi.org/10.1016/j.anl.2014.05.008
G Model
ANL-1859; No. of Pages 4 G. Psillas et al. / Auris Nasus Larynx xxx (2014) xxx–xxx
2
cochlear implantation surgery at our clinic. These children were affected by congenital idiopathic deafness without inner ear dysplasia or syndrome. All the children received cochlear implant in the right ear by our cochlear implant team (consisting of three surgeons); six children were implanted with Freedom implant (Cochlear Contour) (subjects 1–5, 8) and four with Medel Sonata (subjects 6, 7, 9, 10). Our routine procedure consisted of a cortical mastoidectomy, posterior tympanotomy and electrode insertion through the classic cochleostomy located anteroinferior to the round window. A control group of eight normal hearing children, five boys and three girls, matched for age (mean age: 3 years, range 2–5 years) were also used. Informed consent was obtained from the parents of all participating children. The study was approved by the Bioethics Committee of the Medical School of Thessaloniki. The VEMPs were recorded in a soundproof room by means of an Amplaid MK 12 with the children lying supine on a comfortable bed at an approximately 308 angle from the floor. Electrodes were located at the junction middle and upper third of the sternocleidomastoid muscle for each side stimulated, with the reference electrode placed on the middle of the clavicle and a third electrode was placed on the forehead as a ground. During the recording session the children were instructed to stretch their arms right to front of them and simultaneously to turn their heads in the direction contralateral to the stimulated ear in order to unilaterally contract the sternocleidomastoid muscle; at the same time, pendulous oscillating toys were used over their head to distract them and to keep them still and lying during the test. The electrode impedance checked before each recording was below 5 kV. Monoaural stimulation was induced using a 500 Hz positive logon of negative polarity in the earphone (TDH 49). The electromyographic signals were amplified and band-pass filtered from 10 to 2000 Hz and recorded at a constant level for each child. The intensity of the signal was fixed at 130 dB sound pressure level (SPL) at a rate of four signals per second. VEMPs were obtained in a 100 ms-window with a 25 mV/div-amplitude scale, in response to 200 stimuli; a second recording was made to check the reliability of the response. A normal VEMPs tracing was considered as a biphasic waveform with a positive peak (p13) and a negative peak (n23). In order to establish the VEMPs’ normal parameters, the amplitude of the first positive–negative peak (p13–n23) and the latencies of p13 and n23 were assessed in both ears in the control group. However, an
amplitude less than 65 mV was considered as decreased; an absent reflex was defined as an amplitude less than 20 mV or if an unrecognizable tracing was obtained. In order to evaluate the VEMPs reproducibility, the children of the control group were retested with VEMPs after a time of 3 months. For the study group, the VEMPs were first recorded just before the operation. In the postoperative period, VEMPs were evaluated at 10 days and 6 months after surgery, when the cochlear implant was both off and on. Statistical analysis was performed using Student’s t-test (p > 0.05; SPSS 10.0).
3. Results In the control group, the mean amplitude was 142 (SD, 51 mV) and the mean latency of p13 and n23 was 15.6 2.2 ms and 24.1 3.3 ms, respectively. In the same group, 3 months later, no statistically significant difference was found, as the mean amplitude was 154 (SD, 46) (p > 0.05), the mean latency of p13 and n23 was 16.1 2.4 ms (p > 0.05), and 23.6 3.5 ms (p > 0.05), respectively; thus, although our sample was small, the VEMPs could be considered as a reliable diagnostic testing for the young children. It should also be mentioned that the VEMPs were recorded in all ears in this group in both sessions. Preoperatively, in the study group, 4 (40%) out of 10 children showed normal VEMPs in at least one ear (Table 1, Figs. 1A and 2A). In three children, VEMPs amplitude was reduced and in other three children, VEMPs were not elicited on both sides. The mean p13 latency was found normal (16.3 1.6 ms) compared to the control group (p > 0.05). The mean n23 latency was found significantly increased (26.5 2.5 ms) compared to the control group (p < 0.05). Postoperatively, on the 10th day and 6 months after cochlear implantation, no VEMPs were produced in any child on the operated side (Table 1 and Fig. 1B–E). However, no child suffered from dizziness, vertigo, or instability, and no nystagmus was observed. Interestingly, the VEMPs were not recorded on the 10th postoperative day not only on the implanted side but also on the contralateral unimplanted side either (Fig. 2B–C), except for cases 4 and 10; in those children, the VEMPs amplitude was normal (case 4) or reduced (case 10), when the cochlear implant was off
Table 1 Children characteristics and pre-, postoperative results of VEMPs on both sides (R: right, L: left). CI: cochlear implantation –: no VEMPs elicited. Patient/sex
Age (year) of CI
Before CI
Post-10 days CI off
CI on
CI off
CI on
R: normal L: normal R: – L: – R: normal L: normal R: normal L: normal R: – L: normal R: – L: – R: decreased L: – R: – L: – R: decreased L: decreased R: decreased L: decreased
R: – L: – R: – L: – R: – L: – R: – L: normal R: – L: – R: – L: – R: – L: – R: – L: – R: – L: – R: – L: decreased
R: – L: – R: – L: – R: – L: – R: – L: normal R: – L: – R: – L: – R: – L: – R: – L: – R: – L: – R: – L: decreased
R: – L: – R: – L: – R: – L: decreased R: – L: – R: – L: normal R: – L: – R: – L: – R: – L: – R: – L: – R: – L: normal
R: – L: – R: – L: – R: – L: normal R: – L: – R: – L: normal R: – L: – R: – L: – R: – L: – R: – L: – R: – L: normal
1.
K.A., F
4
2.
K.S., M
3.5
3.
M.K., F
2.5
4.
A.T., M
4
5.
M.A., F
2
6.
M.E., M
3
7.
P.A., M
1.5
8.
I.R., F
3
9.
D.D., M
3
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4. Discussion
Fig. 1. VEMPs of case 1 (right ear, implanted side). (A) Normal VEMPs before cochlear implantation. (B and C) On the 10th postoperative day, absence of VEMPs when the cochlear implant was off and on, respectively. (D and E) Six months later, absence of VEMPs, when the cochlear implant was off and on, respectively.
and on. Six months later, no VEMPs response was produced in child 4, and in child 10 the VEMPs amplitude became normal. Moreover, 6 months after cochlear implantation, the VEMPs response on the unimplanted side of three (30%) children (cases 3, 5, 10) became normal when the cochlear implant was on (Fig. 2E); when the cochlear implant was off, the VEMPs response was normal in children 5 and 10, and reduced in child 3 (Fig. 2D). In the remaining cases, no VEMPs were produced on the unimplanted side.
Fig. 2. VEMPs of case 3 (left side, unimplanted side). (A) Normal VEMPs before cochlear implantation. (B and C) On the 10th postoperative day, absence of VEMPs when the cochlear implant was off and on, respectively. (D and E) Six months later, appearance of reduced VEMPs, when the cochlear implant was off and normal VEMPs when the cochlear implant was on, respectively.
In the preoperative period, six (60%) children showed abnormal VEMPs responses on both sides; in other reports [8,10], approximately half of the severely hearing impaired children presented with pathological VEMPs. After cochlear implantation, no VEMPs could be recorded by airconduction in any of our children on the operated side. Histopathologic studies have demonstrated that during cochlear implantation the saccule is the most frequent site of damage in the vestibular system, followed by the utricle and semicircular canals [11,12]. This is due to the fact that the saccule is more proximal to the inserted electrode than the utricle or semicircular canals, regardless of whether the classical cochleostomy or round window approach was performed [11]. Morphological changes can be present such as saccular membrane distortion, loss of saccular membrane, saccular collapse or hydrops, and local fibrosis [11,12]; these saccular alterations may be induced by the insertion trauma of the cochlear implant electrode [2] or resulted indirectly from obstruction of the ductus reuniens (which connects the endolymphatic space between the cochlear duct and the saccule) by debris surgically produced [12]. Basta et al. [2] also found that no VEMPs responses were elicited up to the 6th postoperative week after cochlear implantation in patients aged 10–75 years. However, a lesser extent of saccular damage was reported in children after cochlear implantation; Jin et al. [13] demonstrated that when the cochlear implant was off just after the operation, 11 (91%) out of 12 children (aged 2–7 years) showed no response in VEMPs and one child showed a decreased VEMPs amplitude; when the device was on, eight (66%) showed no response, three (25%) a normal response and one increased VEMPs amplitude; it was possible that the VEMPs were induced by activation of the device as a result of electrical stimulation on the vestibular nerve [5,14]. This observation did not corroborate our results as in our study the VEMPs remained absent irrespective of device activation. Finally, Licameli et al. [6], in a population of 15 older children (aged 5–22 years) until 6 weeks after cochlear implantation, found that 20% of them had absent VEMPs response, 60% of children had reduced and 20% had normal VEMPs response. According to our results, nine children (except for case 4) had abnormal VEMPs responses not only on the implanted side but also on the unimplanted ear either. This unusual finding was not reported elsewhere in VEMPs studies, but it has already been described for the caloric response, which was reduced after cochlear implantation on the unimplanted ear as on the implanted one [14,15]. However, the underlying mechanism which could explain the saccular suppression in the acute postoperative period on both sides is still unknown. Moreover, our three (30%) children (cases 3, 5, 10) showed recovery of VEMPs responses to the normal range on the unimplanted side 6 months after the cochlear implantation. Similar to VEMPs, the caloric response can also return to normal response on the non-operated side within 3–6 months following cochlear implantation [5,16] or after vestibular nerve section [15]. Riba´ry et al. [5] attributed the recovery of caloric response in the implanted and unimplanted ear to the effect of chronic electrical stimulation on the labyrinth. Despite the VEMPs findings, none of our children seemed to postoperatively suffer from dizziness or vertigo and no nystagmus was observed. In adults, approximately 50% of the cases with total loss of VEMPs complained of dizziness for more than 3 months after cochlear implantation [2]. This difference could be attributed on the important capacity of children to better compensate and rapidly adapt to vestibular injury compared to adults [7,17]. In a previous work, Tahara et al. [18] have demonstrated that in children suffering from vestibular neuritis the nystagmus disappeared earlier compared
Please cite this article in press as: Psillas G, et al. Vestibular evoked myogenic potentials in children after cochlear implantation. Auris Nasus Larynx (2014), http://dx.doi.org/10.1016/j.anl.2014.05.008
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to adults, and caloric paresis remained over a longer period in adults than in children. It is evident that our findings were based on a small sample and there was a great variability among the children of this study; however, according to our results, the sacculi of children were easily affected following cochlear implantation. Although this vestibular damage occurred not only in the implanted ear, but also on the unimplanted side, the children had no vestibular complaint and did not show vestibular symptoms. Nonetheless, the potential of negative effect on vestibular function following cochlear implantation should be explained to parents and that vestibular disturbances may appear in long-term. Conflict of interest None. References [1] Fina M, Skinner M, Goebel JA, Piccirillo JF, Neely JG, Black O. Vestibular dysfunction after cochlear implantation. Otol Neurotol 2003;24:234–42. [2] Basta D, Todt I, Goepel F, Ernst A. Loss of saccular function after cochlear implantation: the diagnostic impact of intracochlear electrically elicited vestibular evoked myogenic potentials. Audiol Neurootol 2008;13:187–92. [3] Steenerson RL, Cronin GW, Gary LB. Vertigo after cochlear implantation. Otol Neurotol 2001;22:842–3. [4] Todt I, Basta D, Ernst A. Does the surgical approach in cochlear implantation influence the occurrence of postoperative vertigo. Otolaryngol Head Neck Surg 2008;138:8–12.
[5] Riba´ri O, Ku¨stel M, Szirmai A, Re´pa´ssy G. Cochlear implantation influences contralateral hearing and vestibular responsiveness. Acta Otolaryngol 1999;119:225–8. [6] Licameli G, Zhou G, Kenna MA. Disturbance of vestibular function attributable to cochlear implantation in children. Laryngoscope 2009;119:740–5. [7] Jacot E, Van Den Abbeele T, Debre HR, Wiener-Vacher SR. Vestibular impairments pre- and post-cochlear implants in children. Int J Pediatr Otorhinolaryngol 2009;73:209–17. [8] Shinjo Y, Jin Y, Kaga K. Assessment of vestibular function of infants and children with congenital and acquired deafness using the ice-water caloric test, rotational chair test and vestibular-evoked myogenic potential recording. Acta Otolaryngol 2007;127:736–47. [9] Maes L, Vinck BM, De Vel E, D’haenens W, Bockstael A, Keppler H, et al. The vestibular evoked myogenic potential: a test–retest reliability study. Clin Neurophysiol 2009;120:594–660. [10] Cushing SL, Gordon KA, Rutka JA, James AL, Papsin BC. Vestibular end-organ dysfunction in children with sensorineural hearing loss and cochlear implants: an expanded cohort and etiologic assessment. Otol Neurotol 2013;34:422–8. [11] Tien HC, Linthicum Jr FH. Histopathologic changes in the vestibule after cochlear implantation. Otolaryngol Head Neck Surg 2002;127:260–4. [12] Handzel O, Burgess BJ, Nadol Jr JB. Histopathology of the peripheral vestibular system after cochlear implantation in the human. Otol Neurotol 2006;27:57– 64. [13] Jin Y, Nakamura M, Shinjo Y, Kaga K. Vestibular-evoked myogenic potentials in cochlear implant children. Acta Otolaryngol 2006;126:164–9. [14] Buchman CA, Joy J, Hodges A, Telischi FF, Balkany TJ. Vestibular effects of cochlear implantation. Laryngoscope 2004;114(Suppl. 103):1–22. [15] Cass SP, Kartush JM, Graham MD. Patterns of vestibular function following vestibular nerve section. Laryngoscope 1992;102:388–94. [16] Vibert D, Ha¨usler R, Kompis M, Vischer M. Vestibular function in patients with cochlear implantation. Acta Otolaryngol Suppl 2001;545:29–34. [17] Cushing SL, Chia R, James AL, Papsin BC, Gordon KA. A test of static and dynamic balance function in children with cochlear implants: the vestibular olympics. Arch Otolaryngol Head Neck Surg 2008;134:34–8. [18] Tahara T, Sekitani T, Imate Y, Kanesada K, Okami M. Vestibular neuronitis in children. Acta Otolaryngol Suppl 1993;503:49–52.
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