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Interest of vestibular evaluation in sequentially implanted children: Preliminary results
European Annals of Otorhinolaryngology, Head and Neck diseases 133S (2016) S7–S11
Available online at
ScienceDirect www.sciencedirect.com
Original article
Interest of vestibular evaluation in sequentially implanted children: Preliminary results B. Devroede ∗ , I. Pauwels , S.-D. Le Bon , J. Monstrey , A.-L. Mansbach Department of Otolaryngology Head and Neck Surgery, Hôpital Universitaire des Enfants Reine Fabiola, Université Libre de Bruxelles (ULB), Bruxelles, Belgium
a r t i c l e
i n f o
Article history: Received 28 October 2015 Accepted 28 April 2016 Keywords: Cochlear implant Vestibular function Caloric test VEMP’s Pediatric
a b s t r a c t Introduction: An early acquired or congenital absence of sensory input of the vestibule will lead to severe delayed posturomotor milestones. Previous studies have proven modifications and even complete ipsilateral loss of vestibular function after unilateral cochlear implantation. The objective of this study was to evaluate whether sequential cochlear implantation has an impact on vestibular function. Methods: Retrospective study from January 2012 to January 2015 including 26 patients. The first stage consisted of determining the vestibular status of 26 hearing impaired children who were candidates for a second cochlear implant. Three months after contralateral implantation, we reevaluated the vestibular function of the same patients. The vestibular evaluation consisted of multiple tests for canal and otolith function. A complete clinical vestibular evaluation was performed, including the head thrust test. This was followed by an instrumental assessment composed of the classic bicaloric test and vestibular evoked myogenic potentials testing with tone bursts. Results: A high prevalence of vestibular dysfunction (69%) was found in our group of unilaterally implanted children. Three patients had a unique functional vestibule at the not yet implanted ear. Vestibular evoked myogenic potentials responses stayed present in 15 of the 19 patients with a VEMP-response before contralateral implantation. Results of the caloric test changed for 6 patients after contralateral implantation. Conclusions: After contralateral implantation, 37% of our patients manifested modifications of their vestibular status. Intrasubject comparison of bicaloric and vestibular evoked myogenic potentials testing before and after contralateral cochlear implantation showed that canal function was better preserved than saccular function. Seeing the high prevalence of vestibular dysfunction in our test group of unilateral implanted children, sequential implantation must be preceded by a vestibular assessment to prevent complete bilateral vestibular areflexia and its potential consequences. Presence of hyporeflexia at the yet-to-be implanted ear seems to be a situation particularly at risk. © 2016 Elsevier Masson SAS. All rights reserved.
1. Introduction A complete absence of vestibular information, whether congenital or acquired at very young age, will lead to severely delayed posturomotor milestones, such as stabilizing the head, sitting and walking independently [1–3]. Vestibular end-organs and the cochlea share a common embryological origin and develop thereafter a direct anatomical relationship in the inner ear. As a result, children with profound sensorineural hearing loss may also
∗ Corresponding author. Tel.: +32 2 477 23 55. E-mail address: [email protected] (B. Devroede). http://dx.doi.org/10.1016/j.anorl.2016.04.012 1879-7296/© 2016 Elsevier Masson SAS. All rights reserved.
display vestibular dysfunction, with prevalences ranging from 20 to 85 percent [4–7]. In the last decades, cochlear implants have been the gold standard for treating severe sensorineural hearing loss. At present, bilateral implantation is considered to be of greater value than unilateral implantation, as this gives access to binaural hearing, providing children with better sound localization, better speech detection in noisy environment, and quality of life improvement [8,9]. On the other hand, cochlear implantation has been shown to lead to postoperative modifications of the vestibular function [1,7,10–12]. For instance, Wiener-Vacher et al. reported postoperative vestibular modifications in half of their patients and ipsilateral vestibular areflexia in 10% of them after unilateral
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B. Devroede et al. / European Annals of Otorhinolaryngology, Head and Neck diseases 133S (2016) S7–S11
cochlear implantation. For this reason, implanting both ears instead of one constitutes a significantly greater risk of iatrogenic vestibular dysfunction, as it may cause harm to the entire bilateral vestibular system. Currently most Belgian ENT surgeons favour sequential bilateral cochlear implantation, which means there is a certain time-delay between both surgical procedures. There is however an increasing tendency for simultaneous bilateral implantation. This latter approach may offer operative benefits but it also prevents assessing the child’s vestibular status after the first implantation, which might be an important factor in the decision for a second implantation. The first objective of this study is to identify the percentage of children with a unique functional vestibule at the not yet implanted ear before they receive their second implant. The second objective is to assess the vestibular status of all children after the second implantation to determine the impact of a sequential implantation procedure on the vestibular function. 2. Materials and methods The medical files of all the patients who were candidates for a second cochlear implant between January 2012 and January 2015 in our ENT department were examined. We found 26 first implanted patients corresponding to these criteria (Table 1). The patients had a mean age of 6.75 years at the time of the first vestibular testing (range: 1–13 years old). We could not perform a vestibular assessment after second implantation in two of these patients, as one child’s parents refused the examination, and the other child was diagnosed with a unique functional vestibule on the not yet implanted ear prompting the decision not to implant the second ear. All 24 children with both a pre- and postoperative vestibular evaluation received a Cochlear Nucleus System cochlear implant on the contralateral ear, inserted through an anteroinferior cochleostomy, by the same surgeon. Intramodiolar electrodes were not used in these patients. Hearing loss causes were determined as follows: • • • • • •
as part of a clinical syndrome (n = 7); genetic mutations (n = 7); postmeningitis (n = 1); CMV infection (n = 1); auditory neuropathy spectrum disorder (n = 2); unknown (n = 8).
Imaging studies showed normal inner ear anatomy (n = 19), isolated vestibular malformation (n = 3), cochleo-vestibular malformation (n = 3), and isolated cochlear malformation (n = 1). Table 1 Demographics of the 26 patients.
All patients underwent vestibular status assessment before and 3 months after second implantation, which consisted of a complete vestibular clinical evaluation, horizontal canal testing, and otolithic function testing. Clinical evaluation included medical history, short neurological examination and observation of the child’s balance and eye movements. Horizontal canal function was assessed through vestibulo-ocular reflex (VOR) using videoscopy, Halmagyi’s clinical head thrust test, and bicaloric irrigation. Otolithic function was evaluated by vestibular evoked myogenic potential (VEMP) testing with tone bursts. 2.1. Caloric testing Most patients were exposed to alternate bithermal caloric stimulation, which consists of irrigation of each ear during 30 s at 30 ◦ C and at 44 ◦ C. A limited number of patients had insufficient cooperation and received a monothermal caloric stimulation instead. Moreover, patients suspected to be areflective underwent icewater irrigation to confirm their vestibular status. After irrigation, eye movements were observed during 30 s by videonystagmoscopy while the patient lay in supine position with the head at a 30◦ angle relative to the horizontal plane to put the horizontal semicircular canal in a vertical position. Results were classified in 4 categories: normal, weak, elevated or no responses. For a bithermal caloric irrigation, we used Jongkees’ formula and defined unilateral canal paresis as a result higher than 20% [13]. When a monothermal stimulation was used, unilateral weakness was determined by the following formula: UW % =
(R30 − L30) / (R30 + L30) × 100
The cut-off value is 27% for cold stimulation [14]. 2.2. VEMP testing Vestibular evoked myogenic potentials were recorded using standard auditory brainstem response (ABR) equipment and 500 Hz tonebursts at 74 dB nHl intensity via bone conduction. The potential was recorded ipsilaterally using surface electrodes. Every set of 100 stimuli was averaged and the procedure repeated twice to confirm the reproducibility. Contralateral head turn was used to activate the sternocleidomastoid muscle contraction. Considering that the first generation EMG monitoring used in this study could not monitor the contraction level for each stimulation separately (biofeedback), we therefore decided to interpret responses as either present or absent, without mentioning VEMP amplitudes and latencies. As thresholds could not be measured for every patient, they were excluded from our results. Based on the observed responses to these tests, we defined 3 categories of patients and we compared their vestibular status before and after second implantation:
Population characteristics (n = 26) Mean age at first examination Brand of implants Cochleostomy insertion site Etiology Syndromic Genetic Postmeningitic CMV ANSD Unknown CT scan, NMR Normal Vestibular malformation Cochlea malformation Cochleo-vestibular malformation
6,75 (range: 1–13) Cochlear Antero-inferior 6 7 2 1 2 8 19 3 1 3
• areflective patients who showed a catch-up saccade at the clinical Halmagyi test, no VOR responses on the rotary chair and no responses to caloric and VEMP testing; • hyporeflective patients who displayed either a weak response to caloric testing with normal VEMP testing or an absence of VEMP responses with a normal or weak response to caloric testing. • normal patients when responses to canal and otholithic tests were in the normal range. 2.3. Data analysis Statistical analysis of the data was performed using GraphPad Prism software. Categorical variables were expressed as
B. Devroede et al. / European Annals of Otorhinolaryngology, Head and Neck diseases 133S (2016) S7–S11
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frequencies and percentages. Based on the criteria described above, vestibular status was defined as normal and abnormal. Chi-square test was used to evaluate potential association between categorical variables (postoperative symptoms, inner ear malformation, modifications of the vestibular status). P-values were two-tailed and statistical significance was determined for P-values less than 0.05.
3. Results 3.1. Vestibular status before contralateral implantation (n = 26) In our study group of 26 patients, we find a very high prevalence of vestibular dysfunction: 8% have bilateral areflexia and 61% have hyporeflexia; the other 31% have normal vestibular function (Fig. 1). Amongst the 16 hyporeflective patients, 7 are hyporeflective at the already implanted ear (44%), 4 at the not yet implanted ear (25%) and 5 are bilaterally hyporeflective (31%). We also identify three patients with a unique functional vestibule at the not yet implanted ear. Nevertheless two of them received their second implant. In these patients, postoperative evaluation has shown a complete loss of vestibular function in one of these patients. The second implanted patient maintained his vestibular function.
Fig. 2. Comparison of VEMP responses before and after contralateral implantation (n = 24).
3.2. Otolithic function: VEMP testing (n = 24) Before contralateral implantation, VEMP responses are present in 19 of the 24 patients (79%) (Fig. 2). After receiving a second implant, only 15 patients (62%) still show a VEMP response. To put it differently, four patients out of 19 with VEMP responses (21%) lose their VEMP response after their second implantation. 3.3. Horizontal canal function: bicaloric testing (n = 24) We can confirm that the five patients who had no reactions to caloric stimulation before the second implant keep the same status postoperatively. For this reason, we exclude them from our data analysis (Fig. 3). Preoperative and postoperative bicaloric test results are compared and show different responses in 6 patients (32%): decreased reactions (n = 3), increased reactions–possibly resulting from canal hyperexcitability (n = 2) [1], and absent reactions (n = 1). The complete test results for each patient are detailed in Appendix 1.
Fig. 1. Vestibular status of the 26 first implanted children.
Fig. 3. Evolution of the horizontal canal function after contralateral implantation (n = 24).
4. Discussion Our results confirm that cochlear implantation can damage vestibular function, as shown in previous studies [1,7,10–12,15]. Damage to the vestibular end-organs can be due to direct trauma from insertion of the electrode with possible misplacement in the scala vestibuli, electrical stimulation of the vestibular organs by the implant, intraoperative loss of perilymph, disturbance of the endolymph flow causing endolymphatic hydrops, foreign body reaction with labyrinthitis, or intravestibular fibrosis [10–12,16–18]. Histopathological studies of temporal bones after cochlear implantation revealed in more than half of the cases a cochlear hydrops with saccular collapse [19]. Another frequent finding is bad insertion of the electrode array in the scala vestibuli. [16]. Other authors have concluded that it is the electrode array insertion site in the cochlea that influences the vestibular outcome [20,21]. As of today, we found no consensus whether antero-inferior cochleostomy or round window approach should be preferred to minimize vestibular loss [20–22]. In all the patients included in this study, an antero-inferior cochleostomy was performed. Inner ear surgery in malformed ears is expected to bring about a higher percentage of postoperative vestibular damage, as it entails more surgical difficulties. No significant correlation between the presence of inner ear malformation and the risk of developing
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postoperative vestibular dysfunction could be found due to the limited number of patients fulfilling these criteria. Moreover 2 of the patients with inner ear malformations (n = 5) already presented an areflexia before contralateral implantation. The presence of a functional vestibule at the not yet implanted ear in three of these patients is insufficient to give significant conclusions about the impact of contralateral implantation. Before contralateral implantation, 27% of the entire study group of patients had hyporeflexia at the first implanted ear. Unfortunately, a link between these findings and the first implantation surgery could not be established, as most children were implanted before a systematic vestibular testing was implemented in our ENT department. Concerning otolithic testing, we only considered the presence or absence of VEMP responses. Amplitude of response is highly dependent on the level of the sternocleidomastoid muscle contraction [23,24]. So, amplitudes can only be compared interaurally if we consider muscle contractions of the same level, which requires an accurate EMG feedback monitoring of the muscle contraction. As we did not use this monitoring in the beginning of the study, we decided not to draw conclusions based on amplitude alone and treat all data as on-off results. Therefore our findings of VEMP responses impairment are underestimated since we did not take into account hypofunction of the otolith function. However, some changes in amplitude were striking: two children showed an important decrease in response amplitude, even with a good muscle contraction monitored by biofeedback. Further research is needed to determine whether these are hyporeflectic responses. Immediately after contralateral implantation, one third of our patients with postoperative vestibular modifications experienced nausea, dizziness and vertigo. In contrast, patients with no modifications did not manifest any of these symptoms. Although, we did not find a statistically significant correlation between postoperative vestibular modifications and postoperative symptoms (P = 0.07), there seems to be a trend. This finding goes against what is found in the literature [11]. One possible explanation for this difference may be age-related. Our test group is older than the ones mentioned in other studies, mainly because contralateral cochlear implants were reimbursed in Belgium only since 2010. In total, nine patients (37%) manifested modifications of their vestibular function after second implantation. These patients deteriorated from normal function to hyporeflexia (8 patients) or from hyporeflexia to areflexia (1 patient). No cases of normal preoperative vestibular status resulted in areflexia postoperatively. As previously mentioned we implanted 2 patients with a unique functional vestibule at the not yet implanted ear. One patient presented a complete bilateral areflexia after the second implantation. This patient was 8 years old with a normal posturomotor development at the time of surgery. She experienced vomiting and dizziness during the first postoperative month. After this period she became totally asymptomatic and resumed her sports activities. In this study, canal function was better preserved than saccular function after sequential implantation. This result is consistent with previous studies [25–27]. Several authors stated that saccular function is easily affected after cochlear implantation. On histopathological studies saccule is the most frequently damaged followed by the utricle and the semi-circular canals [27]. This saccular impairment on the implanted side is due to the insertion of the electrode array into the inner ear and is demonstrated in our patients by a disappearance of the VEMP responses. As previously said, reduction of VEMP response amplitudes and threshold elevations were not taken in account. Compliance for VEMP testing was high, in contrast to compliance for caloric testing. Especially irrigation at 44◦ and ice water
irrigation–to confirm bilateral areflexia–were badly tolerated in some patients. Another possibility for testing the canal function would be to use a Video Head Impulse Test (v-HIT). This is a more recent objective test that detects correction saccades during rapid head rotations in case of semicircular canal dysfunction. It also provides quantification of the vestibulo-ocular reflex gain and allows–in theory–evaluation of all six semicircular canals [28]. Sadly we did not have access to this material at the beginning of our study in 2012. The test was less widespread at that time and was not available in our hospital. However, v-HIT is a well-tolerated test in pediatric patients, unlike caloric stimulation, since it does not require irrigation of the ear canal, does not provoke vertigo and is much quicker. This test can be performed as soon as the child is able to fixate a target, which generally corresponds to the age of three. Today, v-HIT is included in our daily practice to assess at least the horizontal canal function before and after cochlear implant surgery. 5. Conclusion Before contralateral implantation we identified 3 patients with a unique functional vestibule at the not yet implanted ear. In these cases, the decision whether or not to implant the contralateral side was taken after long and careful discussion considering the age of the patient, potential risks and benefits of the procedure with the parents and the whole implant team. After assessing the vestibular status of all of our patients implanted on the contralateral side, we can conclude that canal function seems more preserved than saccular function. In total, 37% of our patients manifested modifications of their vestibular status. This study confirms that cochlear implant surgery can strongly interfere with vestibular function. We want to emphasize the importance of vestibular assessment before the second implantation to prevent bilateral vestibular areflexia, especially if there is already areflexia present in the first implanted ear and hyporeflexia in the yet-to-be implanted ear. Clinical and instrumental evaluation of vestibular function in children remains a challenge and it is necessary to use a childfriendly protocol in order to obtain a high test-retest reliability. Unlike with adults, a certain loss of accuracy of some test results cannot be avoided in order to accomplish a complete vestibular evaluation in young subjects. Future goals in this domain should focus on gathering more quantitative results without sacrificing the child’s acceptance of the procedure. Disclosure of interest The authors declare that they have no competing interest. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.anorl. 2016.04.012. References [1] Jacot E, Van Den Abbeele T, Wiener-Vacher SR. Vestibular impairments pre- and post-cochlear implant in children. Int J Pediatr Otorhinolaryngol 2009;73:209–17. [2] Kaga K. Vestibular compensation in infants and children with congenital and acquired vestibular loss in both ears. Int J Pediatr Otorhinolaryngol 1999;49:215–24. [3] Admiraal RJC, Huygen PLM. Vestibular areflexia as a cause of delayed motor skill development in children with the CHARGE association. Int J Pediatr Otorhinolaryngol 1997.
B. Devroede et al. / European Annals of Otorhinolaryngology, Head and Neck diseases 133S (2016) S7–S11 [4] Cushing SL, Papsin BL, Rutka JA, James AL, Gordon KA. Evidence of vestibular and balance dysfunction in children with profound sensorineural hearing loss using cochlear implants. Laryngoscope 2008;118:1814–23. [5] Cushing SL, Papsin BC, Rutka JA, James AL, Blaser SL, Gordon KA. Vestibular end-organ and balance deficits after meningitis and cochlear implantation in children correlate poorly with functional outcome. Otol Neurotol 2009;30:488–95. [6] De Kegel A, Maes L, Baetens T, Dhooghe I, Van Waelvelde H. The influence of a vestibular dysfunction on the motor development of hearing-impaired children. Laryngoscope 2012;122:2837–43. [7] Arena Abramides P, Ferreira Bento R, Moreira Bittar RS, de Brito Neto RV, Koji Tsuji R. How can the cochlear implant interfere with the vestibular function? Intl Arch Otorhinolaryngol 2009;2:195–200. [8] Ramsden JD, Papsin BC, Leung R, James A, Gordon KA. Bilateral simultaneous cochlear implantation in children: our first 50 cases. Laryngoscope 2009;119:2444–8. [9] Laszig R, et al. Benefits of bilateral electrical stimulation with the nucleus cochlear implant in adults: 6-month postoperative results. Otol Neurotol 2004;25(6):958–68. [10] Licameli G, Zhou G, Kenna MA. Disturbance of vestibular function attributable to cochlear implantation in children. Laryngoscope 2009;119:740–5. [11] Katsiari E, Balatsouras DG, Sengas J, Riga M, Korres GS, Xenelis J. Influence of cochlear implantation on the vestibular function. Eur Arch Otorhinolaryngol 2013;270:489–95. [12] Buchman CA, Joy J, Hodges A, Telischi FF, Balkany TJ. Vestibular effects of cochlear implantation. Laryngoscope 2004;114;1–22 [Supplement]. [13] Jongkees LB. The caloric test and its value in evaluation of the patient with vertigo. Otolaryngol Clin North Am 1973;6(1):73–93. [14] Sameh AF, Shereen ME, Maha HA. Monothermal caloric test its value in assessment of vestibular function. Int Congr Ser 2003;1240:1319–24. [15] Huygen PL, et al. The risk of vestibular function loss after intracochlear implantation. Acta Otolaryngol Suppl 1995;520(2):270–2. [16] O’leary MJ, House WF, Fayad J, Linthicum Jr FH. Electrode insertion trauma in cochlear implantation. Ann otol rhinol laryngol 1991;100(9):695–9.
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[17] Bance ML, O’Driscoll M, Giles E, Ramsden RT. Vestibular stimulation by multichannel cochlear implants. Laryngoscope 1998;108(2):291–4. [18] Kubo T, Yamamoto K, Iwaki T, Doi K, Tamura M. Different forms of dizziness occurring after cochlear implant. Eur Arch Otorhinolaryngol 2001;258: 9–12. [19] Handzel O, Burgess B, Nadol JBJr. Histopathology of the peripheral vestibular system after cochlear implantation in the human. Otol Neurotol 2006;27(1):57–94. [20] Briggs RJ, Tykocinski M, Stidham K, Roberson JB. Cochleostomy site: implications for electrode placement and hearing preservation. Acta Otolaryngol 2005;125(8):870–6. [21] 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(1):8–12. [22] Adunka OF, Pillsbury HC, Buchman CA. Minimizing intracochlear trauma during cochlear implantation. Adv Otorhinolaryngol 2010;67:96–107. [23] Kelsch TA, Schaefer LA, Esquivel CR. Vestibular evoked myogenic potentials in young children: test parameters and normative data. Laryngoscope 2006;116:895–900. [24] Vanspauwen R, Wuyts FL, Van de Heyning PH. Improving vestibular evoked myogenic potential reliability by using a blood pressure manometer. Laryngoscope 2006;116(1):131–5. [25] Jin Y, Nakamura M, Shinjo Y, Kaga K. Vestibular evoked myogenic potentials in cochlear implant children. Acta Oto-laryngologica 2006;126(2): 164–9. [26] Krause E, Louza JP, Hempel Jm, Wechtenbruch J, Rader T, Gürkov R. Effect of cochlear implantation on horizontal semicircular canal function. Eur arch Otorhinolaryngol 2009;266(6):811–7. [27] 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 Neurotol 2008;13:187–92. [28] Hamilton SS, Zhou G, Brodsky JR. Video head impulse testing (VHIT) in the pediatric population. Int J Pediatr Otorhinolaryngol 2015;79:1283–7.
Available online at
ScienceDirect www.sciencedirect.com
Original article
Interest of vestibular evaluation in sequentially implanted children: Preliminary results B. Devroede ∗ , I. Pauwels , S.-D. Le Bon , J. Monstrey , A.-L. Mansbach Department of Otolaryngology Head and Neck Surgery, Hôpital Universitaire des Enfants Reine Fabiola, Université Libre de Bruxelles (ULB), Bruxelles, Belgium
a r t i c l e
i n f o
Article history: Received 28 October 2015 Accepted 28 April 2016 Keywords: Cochlear implant Vestibular function Caloric test VEMP’s Pediatric
a b s t r a c t Introduction: An early acquired or congenital absence of sensory input of the vestibule will lead to severe delayed posturomotor milestones. Previous studies have proven modifications and even complete ipsilateral loss of vestibular function after unilateral cochlear implantation. The objective of this study was to evaluate whether sequential cochlear implantation has an impact on vestibular function. Methods: Retrospective study from January 2012 to January 2015 including 26 patients. The first stage consisted of determining the vestibular status of 26 hearing impaired children who were candidates for a second cochlear implant. Three months after contralateral implantation, we reevaluated the vestibular function of the same patients. The vestibular evaluation consisted of multiple tests for canal and otolith function. A complete clinical vestibular evaluation was performed, including the head thrust test. This was followed by an instrumental assessment composed of the classic bicaloric test and vestibular evoked myogenic potentials testing with tone bursts. Results: A high prevalence of vestibular dysfunction (69%) was found in our group of unilaterally implanted children. Three patients had a unique functional vestibule at the not yet implanted ear. Vestibular evoked myogenic potentials responses stayed present in 15 of the 19 patients with a VEMP-response before contralateral implantation. Results of the caloric test changed for 6 patients after contralateral implantation. Conclusions: After contralateral implantation, 37% of our patients manifested modifications of their vestibular status. Intrasubject comparison of bicaloric and vestibular evoked myogenic potentials testing before and after contralateral cochlear implantation showed that canal function was better preserved than saccular function. Seeing the high prevalence of vestibular dysfunction in our test group of unilateral implanted children, sequential implantation must be preceded by a vestibular assessment to prevent complete bilateral vestibular areflexia and its potential consequences. Presence of hyporeflexia at the yet-to-be implanted ear seems to be a situation particularly at risk. © 2016 Elsevier Masson SAS. All rights reserved.
1. Introduction A complete absence of vestibular information, whether congenital or acquired at very young age, will lead to severely delayed posturomotor milestones, such as stabilizing the head, sitting and walking independently [1–3]. Vestibular end-organs and the cochlea share a common embryological origin and develop thereafter a direct anatomical relationship in the inner ear. As a result, children with profound sensorineural hearing loss may also
∗ Corresponding author. Tel.: +32 2 477 23 55. E-mail address: [email protected] (B. Devroede). http://dx.doi.org/10.1016/j.anorl.2016.04.012 1879-7296/© 2016 Elsevier Masson SAS. All rights reserved.
display vestibular dysfunction, with prevalences ranging from 20 to 85 percent [4–7]. In the last decades, cochlear implants have been the gold standard for treating severe sensorineural hearing loss. At present, bilateral implantation is considered to be of greater value than unilateral implantation, as this gives access to binaural hearing, providing children with better sound localization, better speech detection in noisy environment, and quality of life improvement [8,9]. On the other hand, cochlear implantation has been shown to lead to postoperative modifications of the vestibular function [1,7,10–12]. For instance, Wiener-Vacher et al. reported postoperative vestibular modifications in half of their patients and ipsilateral vestibular areflexia in 10% of them after unilateral
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cochlear implantation. For this reason, implanting both ears instead of one constitutes a significantly greater risk of iatrogenic vestibular dysfunction, as it may cause harm to the entire bilateral vestibular system. Currently most Belgian ENT surgeons favour sequential bilateral cochlear implantation, which means there is a certain time-delay between both surgical procedures. There is however an increasing tendency for simultaneous bilateral implantation. This latter approach may offer operative benefits but it also prevents assessing the child’s vestibular status after the first implantation, which might be an important factor in the decision for a second implantation. The first objective of this study is to identify the percentage of children with a unique functional vestibule at the not yet implanted ear before they receive their second implant. The second objective is to assess the vestibular status of all children after the second implantation to determine the impact of a sequential implantation procedure on the vestibular function. 2. Materials and methods The medical files of all the patients who were candidates for a second cochlear implant between January 2012 and January 2015 in our ENT department were examined. We found 26 first implanted patients corresponding to these criteria (Table 1). The patients had a mean age of 6.75 years at the time of the first vestibular testing (range: 1–13 years old). We could not perform a vestibular assessment after second implantation in two of these patients, as one child’s parents refused the examination, and the other child was diagnosed with a unique functional vestibule on the not yet implanted ear prompting the decision not to implant the second ear. All 24 children with both a pre- and postoperative vestibular evaluation received a Cochlear Nucleus System cochlear implant on the contralateral ear, inserted through an anteroinferior cochleostomy, by the same surgeon. Intramodiolar electrodes were not used in these patients. Hearing loss causes were determined as follows: • • • • • •
as part of a clinical syndrome (n = 7); genetic mutations (n = 7); postmeningitis (n = 1); CMV infection (n = 1); auditory neuropathy spectrum disorder (n = 2); unknown (n = 8).
Imaging studies showed normal inner ear anatomy (n = 19), isolated vestibular malformation (n = 3), cochleo-vestibular malformation (n = 3), and isolated cochlear malformation (n = 1). Table 1 Demographics of the 26 patients.
All patients underwent vestibular status assessment before and 3 months after second implantation, which consisted of a complete vestibular clinical evaluation, horizontal canal testing, and otolithic function testing. Clinical evaluation included medical history, short neurological examination and observation of the child’s balance and eye movements. Horizontal canal function was assessed through vestibulo-ocular reflex (VOR) using videoscopy, Halmagyi’s clinical head thrust test, and bicaloric irrigation. Otolithic function was evaluated by vestibular evoked myogenic potential (VEMP) testing with tone bursts. 2.1. Caloric testing Most patients were exposed to alternate bithermal caloric stimulation, which consists of irrigation of each ear during 30 s at 30 ◦ C and at 44 ◦ C. A limited number of patients had insufficient cooperation and received a monothermal caloric stimulation instead. Moreover, patients suspected to be areflective underwent icewater irrigation to confirm their vestibular status. After irrigation, eye movements were observed during 30 s by videonystagmoscopy while the patient lay in supine position with the head at a 30◦ angle relative to the horizontal plane to put the horizontal semicircular canal in a vertical position. Results were classified in 4 categories: normal, weak, elevated or no responses. For a bithermal caloric irrigation, we used Jongkees’ formula and defined unilateral canal paresis as a result higher than 20% [13]. When a monothermal stimulation was used, unilateral weakness was determined by the following formula: UW % =
(R30 − L30) / (R30 + L30) × 100
The cut-off value is 27% for cold stimulation [14]. 2.2. VEMP testing Vestibular evoked myogenic potentials were recorded using standard auditory brainstem response (ABR) equipment and 500 Hz tonebursts at 74 dB nHl intensity via bone conduction. The potential was recorded ipsilaterally using surface electrodes. Every set of 100 stimuli was averaged and the procedure repeated twice to confirm the reproducibility. Contralateral head turn was used to activate the sternocleidomastoid muscle contraction. Considering that the first generation EMG monitoring used in this study could not monitor the contraction level for each stimulation separately (biofeedback), we therefore decided to interpret responses as either present or absent, without mentioning VEMP amplitudes and latencies. As thresholds could not be measured for every patient, they were excluded from our results. Based on the observed responses to these tests, we defined 3 categories of patients and we compared their vestibular status before and after second implantation:
Population characteristics (n = 26) Mean age at first examination Brand of implants Cochleostomy insertion site Etiology Syndromic Genetic Postmeningitic CMV ANSD Unknown CT scan, NMR Normal Vestibular malformation Cochlea malformation Cochleo-vestibular malformation
6,75 (range: 1–13) Cochlear Antero-inferior 6 7 2 1 2 8 19 3 1 3
• areflective patients who showed a catch-up saccade at the clinical Halmagyi test, no VOR responses on the rotary chair and no responses to caloric and VEMP testing; • hyporeflective patients who displayed either a weak response to caloric testing with normal VEMP testing or an absence of VEMP responses with a normal or weak response to caloric testing. • normal patients when responses to canal and otholithic tests were in the normal range. 2.3. Data analysis Statistical analysis of the data was performed using GraphPad Prism software. Categorical variables were expressed as
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frequencies and percentages. Based on the criteria described above, vestibular status was defined as normal and abnormal. Chi-square test was used to evaluate potential association between categorical variables (postoperative symptoms, inner ear malformation, modifications of the vestibular status). P-values were two-tailed and statistical significance was determined for P-values less than 0.05.
3. Results 3.1. Vestibular status before contralateral implantation (n = 26) In our study group of 26 patients, we find a very high prevalence of vestibular dysfunction: 8% have bilateral areflexia and 61% have hyporeflexia; the other 31% have normal vestibular function (Fig. 1). Amongst the 16 hyporeflective patients, 7 are hyporeflective at the already implanted ear (44%), 4 at the not yet implanted ear (25%) and 5 are bilaterally hyporeflective (31%). We also identify three patients with a unique functional vestibule at the not yet implanted ear. Nevertheless two of them received their second implant. In these patients, postoperative evaluation has shown a complete loss of vestibular function in one of these patients. The second implanted patient maintained his vestibular function.
Fig. 2. Comparison of VEMP responses before and after contralateral implantation (n = 24).
3.2. Otolithic function: VEMP testing (n = 24) Before contralateral implantation, VEMP responses are present in 19 of the 24 patients (79%) (Fig. 2). After receiving a second implant, only 15 patients (62%) still show a VEMP response. To put it differently, four patients out of 19 with VEMP responses (21%) lose their VEMP response after their second implantation. 3.3. Horizontal canal function: bicaloric testing (n = 24) We can confirm that the five patients who had no reactions to caloric stimulation before the second implant keep the same status postoperatively. For this reason, we exclude them from our data analysis (Fig. 3). Preoperative and postoperative bicaloric test results are compared and show different responses in 6 patients (32%): decreased reactions (n = 3), increased reactions–possibly resulting from canal hyperexcitability (n = 2) [1], and absent reactions (n = 1). The complete test results for each patient are detailed in Appendix 1.
Fig. 1. Vestibular status of the 26 first implanted children.
Fig. 3. Evolution of the horizontal canal function after contralateral implantation (n = 24).
4. Discussion Our results confirm that cochlear implantation can damage vestibular function, as shown in previous studies [1,7,10–12,15]. Damage to the vestibular end-organs can be due to direct trauma from insertion of the electrode with possible misplacement in the scala vestibuli, electrical stimulation of the vestibular organs by the implant, intraoperative loss of perilymph, disturbance of the endolymph flow causing endolymphatic hydrops, foreign body reaction with labyrinthitis, or intravestibular fibrosis [10–12,16–18]. Histopathological studies of temporal bones after cochlear implantation revealed in more than half of the cases a cochlear hydrops with saccular collapse [19]. Another frequent finding is bad insertion of the electrode array in the scala vestibuli. [16]. Other authors have concluded that it is the electrode array insertion site in the cochlea that influences the vestibular outcome [20,21]. As of today, we found no consensus whether antero-inferior cochleostomy or round window approach should be preferred to minimize vestibular loss [20–22]. In all the patients included in this study, an antero-inferior cochleostomy was performed. Inner ear surgery in malformed ears is expected to bring about a higher percentage of postoperative vestibular damage, as it entails more surgical difficulties. No significant correlation between the presence of inner ear malformation and the risk of developing
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postoperative vestibular dysfunction could be found due to the limited number of patients fulfilling these criteria. Moreover 2 of the patients with inner ear malformations (n = 5) already presented an areflexia before contralateral implantation. The presence of a functional vestibule at the not yet implanted ear in three of these patients is insufficient to give significant conclusions about the impact of contralateral implantation. Before contralateral implantation, 27% of the entire study group of patients had hyporeflexia at the first implanted ear. Unfortunately, a link between these findings and the first implantation surgery could not be established, as most children were implanted before a systematic vestibular testing was implemented in our ENT department. Concerning otolithic testing, we only considered the presence or absence of VEMP responses. Amplitude of response is highly dependent on the level of the sternocleidomastoid muscle contraction [23,24]. So, amplitudes can only be compared interaurally if we consider muscle contractions of the same level, which requires an accurate EMG feedback monitoring of the muscle contraction. As we did not use this monitoring in the beginning of the study, we decided not to draw conclusions based on amplitude alone and treat all data as on-off results. Therefore our findings of VEMP responses impairment are underestimated since we did not take into account hypofunction of the otolith function. However, some changes in amplitude were striking: two children showed an important decrease in response amplitude, even with a good muscle contraction monitored by biofeedback. Further research is needed to determine whether these are hyporeflectic responses. Immediately after contralateral implantation, one third of our patients with postoperative vestibular modifications experienced nausea, dizziness and vertigo. In contrast, patients with no modifications did not manifest any of these symptoms. Although, we did not find a statistically significant correlation between postoperative vestibular modifications and postoperative symptoms (P = 0.07), there seems to be a trend. This finding goes against what is found in the literature [11]. One possible explanation for this difference may be age-related. Our test group is older than the ones mentioned in other studies, mainly because contralateral cochlear implants were reimbursed in Belgium only since 2010. In total, nine patients (37%) manifested modifications of their vestibular function after second implantation. These patients deteriorated from normal function to hyporeflexia (8 patients) or from hyporeflexia to areflexia (1 patient). No cases of normal preoperative vestibular status resulted in areflexia postoperatively. As previously mentioned we implanted 2 patients with a unique functional vestibule at the not yet implanted ear. One patient presented a complete bilateral areflexia after the second implantation. This patient was 8 years old with a normal posturomotor development at the time of surgery. She experienced vomiting and dizziness during the first postoperative month. After this period she became totally asymptomatic and resumed her sports activities. In this study, canal function was better preserved than saccular function after sequential implantation. This result is consistent with previous studies [25–27]. Several authors stated that saccular function is easily affected after cochlear implantation. On histopathological studies saccule is the most frequently damaged followed by the utricle and the semi-circular canals [27]. This saccular impairment on the implanted side is due to the insertion of the electrode array into the inner ear and is demonstrated in our patients by a disappearance of the VEMP responses. As previously said, reduction of VEMP response amplitudes and threshold elevations were not taken in account. Compliance for VEMP testing was high, in contrast to compliance for caloric testing. Especially irrigation at 44◦ and ice water
irrigation–to confirm bilateral areflexia–were badly tolerated in some patients. Another possibility for testing the canal function would be to use a Video Head Impulse Test (v-HIT). This is a more recent objective test that detects correction saccades during rapid head rotations in case of semicircular canal dysfunction. It also provides quantification of the vestibulo-ocular reflex gain and allows–in theory–evaluation of all six semicircular canals [28]. Sadly we did not have access to this material at the beginning of our study in 2012. The test was less widespread at that time and was not available in our hospital. However, v-HIT is a well-tolerated test in pediatric patients, unlike caloric stimulation, since it does not require irrigation of the ear canal, does not provoke vertigo and is much quicker. This test can be performed as soon as the child is able to fixate a target, which generally corresponds to the age of three. Today, v-HIT is included in our daily practice to assess at least the horizontal canal function before and after cochlear implant surgery. 5. Conclusion Before contralateral implantation we identified 3 patients with a unique functional vestibule at the not yet implanted ear. In these cases, the decision whether or not to implant the contralateral side was taken after long and careful discussion considering the age of the patient, potential risks and benefits of the procedure with the parents and the whole implant team. After assessing the vestibular status of all of our patients implanted on the contralateral side, we can conclude that canal function seems more preserved than saccular function. In total, 37% of our patients manifested modifications of their vestibular status. This study confirms that cochlear implant surgery can strongly interfere with vestibular function. We want to emphasize the importance of vestibular assessment before the second implantation to prevent bilateral vestibular areflexia, especially if there is already areflexia present in the first implanted ear and hyporeflexia in the yet-to-be implanted ear. Clinical and instrumental evaluation of vestibular function in children remains a challenge and it is necessary to use a childfriendly protocol in order to obtain a high test-retest reliability. Unlike with adults, a certain loss of accuracy of some test results cannot be avoided in order to accomplish a complete vestibular evaluation in young subjects. Future goals in this domain should focus on gathering more quantitative results without sacrificing the child’s acceptance of the procedure. Disclosure of interest The authors declare that they have no competing interest. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.anorl. 2016.04.012. References [1] Jacot E, Van Den Abbeele T, Wiener-Vacher SR. Vestibular impairments pre- and post-cochlear implant in children. Int J Pediatr Otorhinolaryngol 2009;73:209–17. [2] Kaga K. Vestibular compensation in infants and children with congenital and acquired vestibular loss in both ears. Int J Pediatr Otorhinolaryngol 1999;49:215–24. [3] Admiraal RJC, Huygen PLM. Vestibular areflexia as a cause of delayed motor skill development in children with the CHARGE association. Int J Pediatr Otorhinolaryngol 1997.
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