Electrical Cochlear Response as an Objective Measure of Hearing Threshold and Hearing Performance Evaluation in Pediatric Cochlear Implant Users

The difficulties of applying the audiometry in pediatric populations and its methodological limitations in implanted patients have spurred the development of new alternative auditory evaluation methods. This study aimed to show an objective method to estimate hearing thresholds in pediatric cochlear implanted patients through Electrical Cochlear Response (ECR) and to quantify the hearing performance by using an Auditory Skills Questionnaire (ASQ) and a Calibrated Sounds Test (CST) designed on purpose. Eighteen implanted patients, 1-6 years old underwent standard audiometry, ECR, and ASQ in two evaluation sessions T1 and T2. At T2, in addition, patients underwent CST. For patients ≤3 years old (G1), Pure Tone Averages (PTA and PTAECR)showed a statistically significant difference between them at T1 and T2. At T2 improvements in audiometric and ECR thresholds were observed (p<0.05), regarding T1. Patients older than 3 years (G2) had significantly better ASQ and CST scores. CST detection scores at 40 dBHL for groups G1 and G2, 36% and 70% respectively, showed a better relationship to ECR thresholds. The relationship observed between ECR thresholds and CST detection scores seems to confirm that ECR brings the feasibility of objective hearing threshold estimation and provides a better frequency resolution than audiometry.


INTRODUCTION
Today, a technological alternative for patients suffering from profound bilateral sensorineural hearing loss is the cochlear implant (CI) which, based on banded spectrum analysis for extraction of significant voice attributes, obtains an electrical stimulation code which, applied to the patient's hearing system, generates an auditory sensation. The FDA (Food and Drug Administration) recommends using CI in children from 12 months of age, due to the difficulty of performing behavioral hearing tests in younger patients. This is a limitation when seeking successful rehabilitation in the implanted patients, considering that the critical period for language acquisition comprises the first years of life [1] [2] [3] .
Four to six weeks following implant surgery, CI is programmed for the first time, starting the process of customizing the device to the patient's needs, in order to achieve useful, safe, and comfortable hearing. The different parameters involved in CI programming include establishing the dynamic range of electrical stimulation current in each intracochlear electrode, delimited by the minimum (T) and maximum (M) levels corresponding to the threshold and maximum tolerable auditory sensation, respectively [4] . In clinical practice these current levels are determined by observing the patient's auditory behavior in response to the electrical stimulation provided for a limited number of electrodes. This behavioral CI fitting can be more difficult in pediatric patients who lack the communication skills needed to obtain reliable feedback information.
Unfortunately, neither ECAP nor other electrophysiological methodologies mentioned previously, allow the estimation of hearing thresholds. The audiometry is the only clinical test available to determine hearing thresholds for a number of standardized frequencies [13] [14] [15] [16] , which requires the conscious participation of the patient.
Audiometry results are reliable in patients older than 4 years old, while in younger patients it is difficult to perform because they frequently do not present perceptible behavioral changes. It is even more difficult to observe the changes in implanted patients, especially in their first CI programming session because they are not familiar with the use of the device [17] .  [18] , as an alternative method for hearing threshold estimation in implanted pediatric patients. ECR measures the electrical response of the auditory nerve due to electric stimulation every time CI processes an incoming external sound. The ECR considers the auditory nerve portion responsiveness to the electrical current involved with each intracochlear electrode.
For a given dynamic range of electrical current in an intracochlear electrode, ECR allows establishing the minimum sound intensity level for which auditory nerve portion near to intracochlear electrode generates a threshold electrical response.
Through individual electrode current adjusting, ECR test can help to estimate the auditory threshold at each of the intracochlear electrodes. This is done by quantifying the change in amplitude of the ECR due to variations in the sound intensity level of the input sound.
Previous ECR results have shown that the activation profile of the intracochlear electrodes follows the audiometric threshold profile [19] . These results have shown the feasibility of estimating the patient's hearing thresholds based on ECR, which is independent of the age, general health condition, previous time of use, or brand of the CI.
On the other hand, considerable efforts have been made in the clinical field to establish an auditory-verbal rehabilitation program for pediatric CI users, by using a standardized set of tests that include questionnaires about child' hearing abilities development, and evaluation of speech and sounds discrimination [20] [21] . However, up to now, there are no standardized methodologies to quantify the patient's hearing performance during the period of adaptation to the device.
The purpose of this work is to show the use of ECR to estimate hearing thresholds in implanted pediatric patients and to evaluate hearing performance through the application of a set of tests designed to assess the patient's hearing abilities (see Table 1).

Population
We included a group of 25 pre-lingual CI users Two evaluation sessions were considered, T1: 1.5 to 9 months after CI implantation, and T2: 7 months after T1. The Figure 1 shows a flow diagram of the procedure used for patient´s hearing evaluation in each session.

Tests
Tests were performed at the INR audiology service in a 2.5x2.5x3.0 m audiometric test booth. The free field was calibrated according to ISO 389-7 Standard using a B&K 2235 sound meter, B&K 1625 filter, and a B&K 4230 microphone calibrator. The free field audiometry and ECR test were obtained in two different and successive days. Audiometry was performed using an Interacoustics clinical audiometer AC-40, while the patient was wearing the CI, seated a meter away from the loudspeaker. Pure Tone Average (PTA) was calculated in the frequency range of 500 to 2000 Hz to determine the patient's hearing level [15] . and FPz(GND) according to 10-20 system [22] , observing an electrode-skin impedance < 5 kΩ at 100 Hz were used. One hundred 50 ms EEG epochs were averaged, previously filtered with a second-order Butterworth low-pass filter of 0.1 to 300 Hz with cutoff slope of 12 dB/Octave, zero phase, ±10 μV artifact rejection window, and a sampling frequency of 20 kHz.
Once ECR test finished, patients' parents answered the ASQ to provide information about the child's ability to use the CI in daily situations and the ability to detect, identify, and repeat 18 ambient sounds, as indicated in Table 1. Items evaluated were taken from the IT-MAIS/MAIS scale and the LiP Profile [20] [23] . The CST was designed to evaluate the patient's ability to detect, identify, and repeat 6 seconds duration real sounds and two-syllable Spanish words (Table 1).
All the CST items were normalized in amplitude and grouped in the following five groups: 1. An extended version of Ling sounds, which include eight representative phonemes of the speech spectrum [1] [24] ; 2.

Statistical analysis
The dependent t-test was used to evaluate changes in audiometry and ECR thresholds for all the patients between sessions T1 and T2. The independent t-test was   [26] , considering p<0.05 as significant value. Results are presented in terms of mean ± standard deviation (SD) and percentages.

RESULTS AND DISCUSSION
Of the 25 patients initially included, seven were eliminated because they did not complete the follow-up period. Two of them experienced problems with the implant and five did not complete the battery of tests.
The average age of the 18 patients included in the analysis (9 girls and 9 boys) was 3.2±0.9 (1.8-5.7) years.
The average auditory age (elapsed time between CI activation and ECR recording) was 7.2 months.
Information about the patients is presented in Table 2.        The largest changes between the two groups (G1 and G2) were found in animal sounds, environmental sounds, and two-syllable Spanish words at 40 dB HL (Table 4).For group G1, the PTA ECR of 38±6 dB HL seems to show better relationship with CST detection scores at 40 dB HL than PTA of 51 ±17 dB HL showed in Table 3.
Below is an example of a patient (S2) older than 3 years, who is already familiar with the use of his CI, which has the audiometric and ECR thresholds of Figure 5 and the CST detection scores of Table 5.
According to audiometry patient S2 should detect all sounds at 40 dB HL , however he is not. His CST detection scores are more related to ECR, where thresholds are below 40 dB HL only at some frequencies.
A common practice for CI fitting purposes is to use ECAP threshold to establish M and T levels of the dynamic range of electrical current for a limited number of intracochlear electrodes, without considering the CI sound processor operation. Unfortunately, ECAP is not a predictor of post-operative performance [27] .
Some studies had shown that ECAP threshold tends to fall over time [11] , and is absent in approximately 5% of

Tabla 5
patients [12] [28] . ECAP thresholds profile does not fully coincide with M levels profile [12] , Additionally, ECR thresholds showed less dispersion than audiometry, probably due to its objective nature compared to the subjectivity of the audiometry which generated greater deviations.
The high variability found in the audiometry of the youngest patients, G1, may be due to their short age, limited experience using the CI, and the difficulty they presented in performing the test.