International Journal of Pediatric Otorhinolaryngology 79 (2015) 660–665

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Effect of cochlear implant electrode array design on auditory nerve and behavioral response in children Laila M. Telmesani a, Nithreen M. Said b,c,* a

Otology & Neuro-Otology, Otorhinolaryngology Department, Faculty of Medicine, Dammam University, Dammam, Saudi Arabia Audiology Unit, Otorhinolaryngology Department, Faculty of Medicine, Dammam University, Dammam, Saudi Arabia c Audiology Unit, Otorhinolaryngology Department, Faculty of Medicine, Ain Shams University, Cairo, Egypt b

A R T I C L E I N F O

A B S T R A C T

Article history: Received 7 January 2015 Accepted 5 February 2015 Available online 14 February 2015

Aim: To study the effect of change in the array design of cochlear implant electrode on electrophysiological, and behavioral functional measures of cochlear implant users. Method: A total of 33 children using cochlear implants were included in this study. Subjects were implanted with different electrode types including Slim Straight (CI422) and Freedom Contour Advance (CI24RE) electrode arrays. The electrically evoked compound action potential (ECAP) thresholds were evoked by stimulation of basal, mid, and apical electrodes. The behavioral aided responses using the implant were obtained about 6–12 months post fitting of implant. Results: ECAP thresholds decreased significantly postoperatively in both electrode arrays. Slim straight electrode (CI422) had higher thresholds than Freedom Contour Advance (CI24RE) electrode at most recording sites, but the differences were only significant at basal site. This is a direct consequence of a perimodiolar electrode versus a lateral wall electrode, i.e., the neurons are further away requiring more current (higher threshold) to record the NRT. Conclusion: Although the curved electrode array appeared to evoke responses at lower thresholds, effect on patient performance was not obvious. ß 2015 Elsevier Ireland Ltd. All rights reserved.

Keywords: Electric compound action potential ECAP Neural response telemetry Cochlear implant electrodes Objective assessment

1. Introduction Multichannel cochlear implants have been highly successful in restoring speech understanding in individuals with severe-toprofound hearing loss. Most individuals are able to obtain postoperative improvement in word recognition scores with cochlear implants [1]. One factor that may limit performance after cochlear implantation is the broad spread of electrical current within the cochlea, which may result in greater channel interaction, higher current needs, and less opportunity to take advantage of newer speech processing strategies [2]. One way to improve patient performance is to manipulate the anatomical placement of the electrode array within the scala tympani of the cochlea. Various cochlear implant manufacturers have concentrated on changing the electrode design to direct the

* Corresponding author at: Ain Shams University, Audiology-Otorhinolaryngology, Cairo, Egypt. Tel.: +00201002500123. E-mail addresses: [email protected], [email protected] (N.M. Said). http://dx.doi.org/10.1016/j.ijporl.2015.02.008 0165-5876/ß 2015 Elsevier Ireland Ltd. All rights reserved.

contacts toward the modiolus and place the electrode array in a peri-modiolar position [3]. To achieve medial placement, Cochlear Limited (Sydney, Australia) uses a pre-curved electrode array, the Nucleus freedom Contour advance (CI24RE). Many studies have reported that the peri-modiolar position decreases threshold levels, increases dynamic range and improves spatial selectivity of neural activation [4–9]. These changes could contribute to more effective channels within the implant system, which may improve the understanding of speech in both quiet and noisy listening situations [9–11]. Another way of improving the performance of cochlear implants is to increase the likelihood and degree of preservation of hearing through improved surgical techniques and technological developments [1]. Even though the perimodiolar electrode allows significant preservation of residual hearing, its greater volume and stiffness produces a higher degree of residual hearing loss as a result of the possibility of mechanical trauma [1]. The Nucleus Slim Straight cochlear implant (CI422) which was recently developed by Skarzynski et al. [1] together with Cochlear Ltd., Sydney, Australia, has an electrode array with a total length of 25 mm, and smaller dimensions than the Nucleus Contour Advance electrode arrays (diameter 0.3–0.6 vs. 0.5–0.8 mm).

L.M. Telmesani, N.M. Said / International Journal of Pediatric Otorhinolaryngology 79 (2015) 660–665

Being half-banded, it provides a ‘smooth’ side which may reduce trauma when it is moved along the lateral wall of the scala. CI422 is an improvement on the existing full-banded Nucleus Straight array both in terms of insertion trauma and the potential to conserve residual hearing. Electrophysiological recordings of the auditory system such as the electrically evoked compound action potential (ECAP) provide useful objective measures of neural response to auditory stimulation [12,13]. A system of measuring the ECAP, first developed by Cochlear Corporation for the Nucleus 24 device (CI24), is known as neural response telemetry (NRT). Researchers and clinicians have investigated the feasibility of using the ECAP threshold to objectively predict psychophysical measurements and facilitate the programming of the speech processor [14]. Consequently, it is important to determine whether electrophysiological responses in children change with different designs of cochlear implant electrode arrays as these are sometimes the only measures available to set cochlear implant stimulation levels especially in young children or individuals who are difficult to test. Saunders et al. [4] studied the radial distance of the electrode from the modiolus and concluded that ECAP thresholds and impedance levels would be lower for electrodes closer to the modiolus as a lower current would be needed to stimulate neurons that are in close proximity to an electrode. Gordin et al. [14] reported lower ECAP levels for the perimodiolar 24RE device compared with the older straight electrode 24 M device. Very few studies have compared different generations of electrode arrays and non have compared the slim straight electrode (CI422) to previous generations. In the present study, we were specifically interested in comparing the ECAP thresholds evoked by the recent slim straight (CI422) electrode with those evoked by Freedom contour advance (CI24RE) electrode.

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sleeve, and the transmitter coil was placed over the skin. Impedance levels were measured after which the measurement of ECAP thresholds were done. A fast stimulation rate of 250 Hz was used for ECAP recording to reduce test time in the operating room. Threshold search begins with a relatively high current level. 2.2.2. Postoperative recordings A speech processor was fitted 4 weeks after surgery. Programming was based on objective ECAP thresholds in the first sessions till behavioral programming levels could be achieved. A slow-rate (80 Hz) was used to record ECAP thresholds. The current stimulation levels begin at low levels to prevent overstimulation and ensure that the patient is comfortable [15] For intra and postoperative ECAP recordings, biphasic electrical current pulses, 25 ms pulse width, were used to stimulate the electrodes. The amplifier gain ranged from 40 to 60 dB, and recording delays were 50 to 125 ks. AutoNRT ‘‘searches’’ for threshold by presenting a series of ascending and descending current levels. Threshold is defined as the mean of the lowest positive response measurement and the highest negative response measurement [15]. Thresholds from apical (typically no. 22), mid (typically nos. 16 and 11), and basal (typically nos. 6 and 1) sites were selected and analyzed in the study. Impedance was measured using the standard clinical method for recording impedance in the Custom sound software. Monopolar 1 + 2 mode electrode impedances were analyzed. Electrode impedance levels were measured intra-operatively and at the beginning of the fitting session before ECAP measurement. A decrease in impedance levels was observed after the beginning of electrical stimulation and the use of the device. Measurement of impedance levels was repeated 1 month after the device was fitted and these levels were used to compare the two groups postoperatively.

2. Methodology 2.1. Subjects Thirty-three children were included in the study. All subjects received Nucleus 24 cochlear implant system at King Fahad University Hospital—Dammam University. They had used hearing aids for at least three months prior to cochlear implant surgery and had received auditory verbal rehabilitation. The age at implantation ranged from 1.2 to 5 years old. Subjects were classified into two groups according to the type of implanted electrode array. Group (A) was implanted with Nucleus Freedom Contour Advance array (CI24RE) and group (B) with the Nucleus Slim Straight electrode array (CI422). 2.2. Procedure All patients were operated on by the same surgeon (the first author). Trans-mastoid posterior tympanotomy approach was used. CI24RE electrode was introduced in group A via a cochleostomy while slim straight electrode (CI422) was introduced in group B via round window. Electrode impedance and auditory nerve response measures were recorded in the operating room immediately after the cochlear implantation and at the time of fitting. Cochlear Corporation’s Custom sound EP software version 3.2 was used for the recording. The Neural response telemetry (AutoNRT) feature was used to record the ECAP. 2.2.1. Intraoperative recordings Measurements were done in the operating room after the insertion of the electrode into the cochlea and during the closing of the incision. The processor and coil were placed in a sterile camera

2.2.3. Hearing evaluation Regular follow-up assessment was done for the patient every three months after fitting. Aided sound field with the cochlear implant was tested using two channel audiometer model AC40. Aided threshold levels were achieved in a sound treated room using warble tones at zero degree azimuths at a distance of one meter from the loudspeaker at the frequencies (250–8000 Hz). Best aided responses after setting the proper map were presented in the study. At the time of the study, most of our subjects had recently had implants (within the first year) so their language abilities did not allow for an assessment of speech perception. 2.2.4. Data analysis Statistical analysis was done using the SPSS statistical software program. Simple descriptive analysis was performed in order to calculate arithmetic mean, standard deviation and range. Data were expressed as means and standard deviation for quantitative measures, and as a number for qualitative data. Multi-variant analysis of variances (MANOVA) and t test were used for comparison. Comparative statistics were performed either by Student’s t-test (t value) for normally distributed two-independent samples or Mann–Whitney U test (Z value) for nonparametric distribution. P-values less than 0.05 were considered significant, while at 0.01 or 0.001 were highly significant. 3. Results Table 1 shows demographic data of both study groups comprising 15 males and 18 females. Age at implantation ranged between 1.2 and 5 years old and the subjects had used hearing aids for at least 3 months before implantation. Fig. 1 shows gender distribution of both study groups. The most common

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Table 1 Demographic details of each study group (group A implanted with CI24RE electrode, group B implanted with CI422 electrode).

Age at implantation

Group A Group B Group A Group B

HA use duration

Mean  SD

Range

P

4.1 y  3.4 1.2 y  1.6 1.8 y  1.4 0.9 y  0.7

2–5 y 1.2–5 y 3 m–4 y 3 m–2 y

0.201 0.324

y = Years old, m = months.

Fig. 1. Gender distribution in both groups.

etiology in our studied subjects was heredo-familial hearing loss (Fig. 2). As regards electrode impedance measures, it was observed that impedance levels dropped significantly after the use of the device and start of electric stimulation. At the time of fitting before the start of electrical stimulation, impedances remained at higher levels that did not differ significantly from intra-operative measure (Fig. 3). Impedance levels did not show significant differences between the two electrode arrays intraoperatively except at apical site E22 where CI422 had higher impedance level (14.9 kV + 3.3) than CI24 RE (11.7 kV + 4.7). No significant differences were observed between the two electrode arrays one month post-fitting (Table 2 and Fig. 4). However, intraoperative ECAP thresholds were higher in CI422 than CI24RE at most recording sites although this difference was statistically significant at the basal site E6 only. This finding was persistent postoperatively at fitting time (Table 3, Fig. 5). It was observed that ECAP thresholds were higher at basal relative to apical recording sites in both electrode arrays. A significant decrease in ECAP thresholds was observed in both electrode arrays postoperatively, at the time of fitting. This was evident for all recording sites in CI422 (group B) and only for the mid array (E16 and E11) in CI24RE (group A) (Fig. 6).

Fig. 3. Changes of impedance levels intra and postoperatively (at fitting time before use of the device and 1 month post fitting).

Fig. 7 revealed no significant differences in the aided sound field responses in both groups.

4. Discussion Our main interest in the present study was to compare impedance levels and auditory nerve compound action potential (ECAP) response thresholds evoked by the Freedom contour advance (CI24RE) electrode and the recent slim straight (CI422) electrode. CI24RE is a pre-curled electrode designed to be placed in a peri-modiolar position, and the CI422 is a straight electrode designed to reduce trauma when moved along the lateral wall of the scala. The most common etiology in our study was heredo-familial hearing loss (Fig. 2). All the subjects had had hearing loss since birth. A comparison of the two groups revealed no statistically

Table 2 Mean  SD of intraoperative and postoperative impedance levels in both groups. Intraoperative impedance levels Implant array Group A Group B P

E22 11.7 + 4.7 14.9 + 3.3 0.04*

E16 13.8 + 6.4 10.8 + 2.2 0.05

Postoperative impedance levels (measured Implant array E22 E16 Group A 9.8 + 1.9 8.5 + 1.3 Group B 10.0 + 1.8 9.2 + 1.8 P 0.81 0.45 Fig. 2. Etiology of hearing loss.

*

Significant.

E11 11.5 + 4.6 10.8 + 2.7 0.58

E6 10.6 + 4.5 10.1 + 2.7 0.68

one month post fitting) E11 E6 7.6 + 1.5 9.6 + 3.3 7.8 + 1.3 7.7 + 1.5 0.80 0.09

E1 8.4 + 5.1 9.0 + 2.9 0.65

E1 8.8 + 2.7 9.4 + 1.5 0.56

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Fig. 4. Intraoperative and one month post fitting impedance levels in both groups.

Table 3 Mean + SD of intra and postoperative ECAP thresholds at different electrode sites measured in both groups. Intraoperative ECAP thresholds Implant array Group A Group B P

E22 161.6 + 26.5 174.4 + 23.5 0.17

Postoperative ECAP thresholds (measured at time of fitting) Implant array E22 Group A 159.2 + 26.3 Group B 167.5 + 19.0 P 0.31 **

E16 178.7 + 20.0 175.7 + 15.3 0.66

E11 184.2 + 15.9 194.0 + 15.2 0.10

E6 167.9 + 32.0 197.4 + 13.6 0.0001**

E1 190.8 + 12.5 200.8 + 18.7 0.15

E16 172.2 + 18.0 166.9 + 12.4 0.33

E11 178.7 + 18.9 184.7 + 12.9 0.30

E6 162.2 + 23.7 181.9 + 12.6 0.0001**

E1 183.3 + 15.9 185.3 + 13.3 0.72

Highly significant.

Fig. 5. ECAP thresholds at intra and postoperative (fitting time) in both groups.

significant differences in age at implantation or the duration of the use of a hearing aid before implantation (Table 1). 4.1. Electrode impedance levels Electrode impedance measurements can detect circumstances under which certain electrodes should not be used, such as openor short-circuits. In addition impedance measurements facilitate the estimation of voltage compliance levels for the comfort Clevels used with a cochlear implant system. Exceeding the compliance levels, will deny the patient the ability to perceive the growth of loudness as the current level is increased, the result of which is loudness ‘saturation’ [16]. In the present study, all impedance levels were below 15 kV. No open or short circuits were observed in the studied subjects. In both electrode arrays (CI422 and CI24RE), there was a significant decrease in impedance levels after the fitting of the device and the start of electric stimulation. Significantly higher impedance levels were noticed at the time of surgery and before

fitting (Fig. 3). These findings agreed with such previous studies as Henkin et al. [13] who reported that electrode impedance values decreased significantly after initial stimulation. Henkin et al. [13] reported that stabilization of values was evident after 1 month post fitting. Previous studies with the Nucleus 24 M implant [4, 17] and Ineraid device [18] had shown similar results. Therefore, in the present study, we used the impedance levels measured one month postfitting for the purpose of comparison. Hughes et al. [17] suggested that the initial decrease in impedance of current carrying electrodes may be attributed to the notion that stimulation of electrodes causes the formation of a hydride layer on the surface of the electrode, resulting in lower electrode impedance. Impedances could vary in different electrode sites across the array since each site has its own local environment that change on account of its position in the cochlea (e.g. proximity to bone) and degree of tissue formation on the surface of the electrode. In the present study, CI422 had significantly higher impedance level than CI24 RE at the apical electrode site (E22). This finding was observed

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Fig. 6. Changes in ECAP threshold levels intra and postoperatively (at fitting time) in both electrode arrays.

A comparison of ECAP thresholds in the two electrodes, revealed no significant difference except at basal site (E6), which was higher in CI422. This finding was persistent at fitting time postoperatively (Table 3; Fig. 5), and can be explained by the proximity of CI24RE to the modiolus at the base which agreed with previous findings [14] that compared CI24RE to straight arrays (24 M). These studies were consistent with the conclusions of Huang et al. [21] (based on X-ray measurements in adult cochlear implant users) that the Contour advance (24RE) sits closer to the modiolus than straight arrays. The differences in ECAP thresholds in the two electrode arrays at basal recording sites did not seem to have affected our patients’ performance and there was no significant effect on sound field behavioral responses in the two groups (Fig. 7). Spivak et al. [22] reported a consistent pattern in ECAP threshold in patients implanted with Nucleus freedom implant. Thresholds are highest for electrode 1 (basal end) and lowest for electrode 22 (apical end). The gradual progression from high to low threshold from basal to apical end is interrupted by a slight increase in threshold at electrode 11. Our data shows that stimulation from the apical implant electrode produced the lowest ECAP threshold in both arrays, and this was consistent with previous results [14, 23, 24]. On the other hand, differences between ECAP levels evoked by the basal versus midarray electrode were dependent upon the device. CI24RE showed lower thresholds at the basal sites (E6) relative to the mid array sites (E11 and 16). However, in CI422, there was no difference between mid and basal sites. Similar results were obtained by Gordin et al. [14] but in a comparison of the precurved CI24RE to the straight array 24 M. Differences in ECAP thresholds as a function of electrode position have been attributed to density and integrity of surviving spiral ganglion cells at different positions within the cochlea, and the proximity of the electrodes to neural elements [21, 25, 26]. Data shown in Fig. 6 indicates a decrease in ECAP thresholds in both electrode arrays at fitting time. This drop was significant for all recording sites in CI422 and only for the mid array (E16 and E11) in the CI24RE electrode array. In our opinion, this can be attributed to changes in the cochlea in the 1st month of using a cochlear implant. Gordon et al. 27] and Hughes et al. [17] added the chronic electric stimulation as a factor for the change in ECAP thresholds. There are no reports of differences in ECAP threshold stability over time as a function of electrode position or electrode design. 5. Conclusion

Fig. 7. Sound field behavioral responses in both groups.

at the time of surgery only. Post-fitting, impedance levels did not show significant differences between the two arrays and between different electrode positions (Table 2 and Fig. 4). This finding agreed with previous studies which revealed no significant differences in impedance levels at different cochlear segments [13, 17]. 4.2. ECAP thresholds Both electrode impedance values and ECAP thresholds reflect the anatomical and physiological status of the cochlea [19, 20]; however, ECAP thresholds reflect cognitive-behavioral processes as well.

There were no significant differences in impedance levels in the two studied electrodes (CI24RE and CI422). ECAP thresholds drop significantly at fitting time regardless of the type of electrode. Although the curved electrode array appeared to evoke responses at lower thresholds in the basal stimulation sites, effects on sound field responses or patients’ performance were not apparent. Conflict of interset statement There is no conflict of interest and no financial disclosures. Financial support None. Acknowledgments The authors would like to express their sincere thanks to Prof. Emmanuel B. Larbi, professor of Medicine & Clinical Pharmacology

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Secretary, Principal Committee of Quality & Planning Unit College of Medicine, University of Dammam, for his continuing support. The authors gratefully acknowledge Dr Ammar Hassan Khamis, Associate professor of biostatistics and genetic epidemiology, Dubai college of dental medicine, UAE, and Dr. Osama Majdalawieh (Ph.D.), Cochlear AG, Basel Switzerland who helped us in data analysis in this study. We wish to thank Dr. Salma Al Sharhan, Specialist otolaryngology, ENT Department, Dammam University who helped in collecting patients’ data. References [1] H. Skarzynski, A. Lorens, M. Matusiak, M. Porowski, P. Skarzynski, C. James, Partial deafness treatment with the nucleus straight research array cochlear implant, Audiol. Neurotol. 17 (2012) 82–91. [2] J.B. Firszt, P.A. Wackym, G.W. Wolfgang, L.S. Burg, R.M. Reeder, Electrically evoked auditory brain stem responses for lateral and medial placement of the clarion hifocus electrode, Ear Hear. 24 (2) (2003) 184–190. [3] J.J. Briaire, H.M. Frijns, The consequences of neural degeneration regarding optimal cochlear implant position in scala tympani: a model approach, Hear. Res. 214 (2006) 17–27. [4] E. Saunders, L. Cohen, A. Aschendorff, W. Shapiro, M. Knight, M. Stecker, et al., Threshold, comfortable level and impedance changes as a function of electrodemodiolar distance, Ear Hear. 23 (1) (2002) 28S–40S. [5] M. Tykocinski, E. Saunders, L. Cohen, C. Treaba, R. Briggs, P. Gibson, et al., The contour electrode array: safety study and initial patient trials of a new perimodiolar design, Otol. Neurotol. 22 (2001) 33–41. [6] G. Donaldson, M. Peters, M. Ellis, B. Friedman, S. Levine, F. Rimell, Effects of the clarion electrode positioning system on auditory thresholds and comfortable loudness levels in pediatric patients with cochlear implants, Arch. Otolaryngol. Head Neck Surg. 127 (8) (2001) 956–960. [7] L. Cohen, E. Saunders, G. Clark, Psychophysics of a prototype peri-modiolar cochlear implant electrode array, Hear. Res. 155 (1–2) (2001) 63–81. [8] S. Cords, G. Reuter, P. Issing, A. Sommer, J. Kuzma, T. Lenarz, A silastic positioner for a modiolus-hugging position of intracochlear electrodes: electrophysiologic effects, Am. J. Otol. 21 (2) (2000) 212–217. [9] R. Shepherd, S. Hatsushika, G. Clark, Electrical stimulation of the auditory nerve: the effect of electrode position on neural excitation, Hear. Res. 66 (1993) 108–120. [10] L. Cohen, L. Richardson, E. Saunders, R. Cowan, Spatial spread of neural excitation in cochlear implant recipients: comparison of improved eCAP method and psychophysical forward masking, Hear. Res. 179 (1–2) (2003) 72–87. [11] J. Frijns, S. de Snoo, R. Schoonhoven, Potential distributions and neural excitation patterns in a rotationally symmetric model of the electrically stimulated cochlea, Hear. Res. 87 (1995) 170–186.

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Effect of cochlear implant electrode array design on auditory nerve and behavioral response in children.

To study the effect of change in the array design of cochlear implant electrode on electrophysiological, and behavioral functional measures of cochlea...
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