The relationship between cortical auditory evoked potentials (CAEPs) and speech perception in children with Nurotron® cochlear implants during four years of follow-up

International Journal of Pediatric Otorhinolaryngology 85 (2016) 170–177

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The relationship between cortical auditory evoked potentials (CAEPs) and speech perception in children with Nurotron1 cochlear implants during four years of follow-up Qianqian Guo a,b, Yuling Li a,b, Xinxing Fu a,b, Hui Liu a,b, Jing Chen a,b, Chao Meng a,b, Mo Long c,1,*, Xueqing Chen a,b,1,** a

BeijingTongren Hospital, Capital Medical University, Beijing 100730, China Beijing Institute of Otolaryngology, Key Laboratory of Otolaryngology Head and Neck Surgery(Capital Medical University), Ministry of Education, Beijing, China c China Rehabilitation Research Center for Deaf Children, Beijing 100029, China b

A R T I C L E I N F O

A B S T R A C T

Article history: Received 15 December 2015 Received in revised form 21 March 2016 Accepted 24 March 2016 Available online 11 April 2016

Objective: The purpose of the current study was to evaluate the relationship between the presence or absence of cortical auditory evoked potentials (CAEPs) to speech stimuli and the performance of speech perception in Chinese pediatric recipients of the Nurotron1 cochlear implant (CI).We also wanted to determine how the CAEPs might be used as an indicator for predicting early speech perception and could provide objective evidence for clinical applications of CAEPs. Methods: 23 pediatric unilateral CI recipients participated in this study. 15 males 8 females, and their ages at implantation ranged from 13 to 68 months, with a mean age of 36 months. CAEPs and Mandarin Early Speech Perception (MESP) tests were used to evaluate the audibility and speech perception of these CI users. The tests were administered at the first, second, third, and fourth year after the CI surgery. Results: All the subjects demonstrated improvements in detection of speech sounds with CI. The percentages of participants who could detect all three stimuli were 26% (6/23) at first year, to 100% (23/23) at the fourth year post-implantation. The percentages of participants who passed the Category 6 of MESP were from 9% (2/23) at first year, to 91% (21/23) at the fourth year post-implantation. Significant correlations (p < 0.05) were found between CAEP scores and MESP at the first, second, third year after the CI surgery. The multiple regression equation for prediction of MESP categories from CAEP scores and hearing ages was MESP = 1.088 + (0.504  CAEP score) + (0.964  hearing ages) (F = 72.919, p < 0.001, R2 = 0.621). Conclusion: The results of this study suggested that aided cortical assessment was a useful tool to evaluate the outcomes of cochlear implantation. Cortical outcomes had a significant positive relationship with the MESP, which predicted the early speech perception of CI recipients. ß 2016 Elsevier Ireland Ltd. All rights reserved.

Keywords: Cortical auditory evoked potentials Cochlear implants Children Speech perception

1. Introduction In China, there are about 27.8 million individuals with hearing loss. Hearing loss is a common, disabling disease, particularly for

* Corresponding author at: China Rehabilitation Research Center for Deaf Children, A8 Huixinli, Chaoyang District, Beijing100029, China. Tel.: +86 10 84632997. ** Corresponding author at: Beijing Tongren Hospital, Capital Medical University and Beijing Institute of Otolaryngology, 17 Hougou Lane, Chongnei Street, Dongcheng District, Beijing 100005, China. Tel.: +86 10 58265805; fax: +86 10 85115988. E-mail addresses: [email protected] (M. Long), [email protected] (X. Chen). 1 These authors contributed equally to this work. http://dx.doi.org/10.1016/j.ijporl.2016.03.035 0165-5876/ß 2016 Elsevier Ireland Ltd. All rights reserved.

children where it causes delayed speech and language development, scholastic underachievement and social difficulties [1–6]. However, with the introduction of newborn hearing screening, it is possible to make an early diagnosis of children’s hearing loss, and then recommend appropriate interventions which may include hearing aids or cochlear implants(CI) [7,8]. For children with profound sensorineural hearing loss, CI may be the best solution for them. When hearing loss is detected with infants or young children, they are unable to respond to behavioral threshold measurements, and aided outcome hearing threshold estimations are hard to obtain [9,10]. In clinical practice, parental questionnaires have been extensively used in assessing the effectiveness of CI use, but they are restricted by many factors like parents’ attention to details of their child’s auditory

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behaviors,the abilities of the researchers to extract relevant information from what the parents say, and the lifestyle of the children.[11]. Audiologists usually use simple Ling6 to elicit responses or a drum to test the children’s audibility and tolerance after they receive their cochlear implantation. Unfortunately, the accuracies of these approaches are affected by the infants’ awareness, and the audiologists’ control of their own voice intensity [12]. Therefore, objective methods to verify the outcomes and effectiveness of the cochlear implant are of great importance. There are about 40,000 CI recipients in China, and accurate, objective, and convenient clinical tools to evaluate the success of cochlear implantation are critical. Electrophysiological methods are useful measurements to understand infants’ CI performance. For example, cortical auditory evoked potentials (CAEPs) generated from primary auditory cortex and associative cortical areas can provide objective sensation, cognition, memory, speech perception and other information of the central auditory nervous system [13,14].CAEP was first put forward by Davis in 1939[15], and progressed through 1960s and early 1970s [16], then as the appearance of ABR [17] and the difficulty of judging the CAEP waveforms, CAEP seldom used for a period. But in the mid-1990s, CAEPs was revived for indicating sound discrimination abilities [18]. CAEP waveforms can now be judged by automated statistical detection techniques (e.g. Hotelling’s T2) [19,20], and gradually can be used in clinical work. Speech language perception tests are also useful measurements to assess the outcomes of CI. Several speech language perception test materials exist for children, including the early speech perception (ESP) test [21]; the Pediatric Speech Intelligibility (PSI) test [22], the Lexical Neighbor Test (LNT) [23] and pediatric Hearing In Noise Test (HINT) [24]. For young children in China, the Mandarin Early Speech Perception (MESP) test was developed by Zheng and her colleagues for normal developmentally 2–5 years old Mandarin-speaking children to evaluate early speech perception based on the English version [25]. Several studies have demonstrated the relationship between CAEP components and speech perception. Alvarenga et al. [26] used a Smart EP USB Jr. system to record CAEPs and the tests 5 and 6 of the Glendonald Auditor Screening Procedure (GASP) to evaluate speech perception respectively in 14 pediatric (4–11 years of age) CI users with ANSD, results revealed that P1 component correlated with speech perception and can be a predictor of the speech perception outcome in implanted children. Raince et al. [27] also investigated 18 children with ANSD ranging in age from 6 to 92 months, found that the occurrence of cortical potentials was closely related to PBK open-set speech perception assessment in subjects with hearing aids. The study by Narne [28] showed that speech identification scores had a good relationship with the amplitude of cortical potentials in ANSD subjects andmight offer a way for predicting perceptual skills in these individuals. Maryanne’s [11] research indicated the presence of cortical responses had a good relationship with functional measures of real-world listening behaviors with hearing aids. In addition, many previous studies revealed P1 parameters (latency and amplitude) correlated with speech perception performance in children and adults [29–33]. But the previous researches tested the relationship between cortical responses and speech perception for just one time, not a long period. In our study, in light of the difference of CAEPs recording equipment and characteristics of the mandarin Chinese, we examined the relationship between the occurrence of CAEPs and MESP performances in CI users with profound sensorineural hearing loss during four years of follow-up. The goal of the current study was to examine the clinical applications of CAEPs. We would investigate the relationship between CAEPs and outcomes of speech language perception tests in children with CI.

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2. Materials and methods 2.1. Subjects 23 unilateral CI recipients participated in this study, 15 males 8 females; they had their CI surgery at Beijing Tongren Hospital, Capital Medical University. Their ages at implantation ranged from 13 to 68 months with a mean of 36 months. The tests were administered at the first, second, third, and fourth year after the CI surgery. All subjects were diagnosed with bilateral profound sensorineural hearing loss prelingually by audiological tests like paediatric behavioral audiometry, tympanometry, distortionproduct otoacoustic emissions (DPOAEs), auditory brainstem response (ABR) and auditory steady-state response (ASSR). They were all without inner ear malformation and other physical and mental diseases. All the participants were fitted with Nurotron1 VenusTM (NSP60B strategy) CI. A summary of the subject characteristics, including gender, etiology, age at implantation and other information, are presented in Table 1. 2.2. Procedures The parents of the participants were informed of the test protocol and agreed to participate in the research. The study received approval by the Beijing Tongren Hospital Institutional Research Ethics Board. The children were fitted with their CI before test protocol began, with their threshold (T) levels being measured by visual reinforcement audiometry (VRA), play auditometry (PA), or conventional audiometry according to their ages. Comfort (C) levels were measured by picture pointing tasks or behavioral observation methods during the CI mapping process. The assessment procedure included objective recording of CAEPs as well as subjective speech perception measurements with the Mandarin Early Speech Perception (MESP) test. All the measurements were tested in a free sound field with ambient noise level below 30 dB (A). 2.3. Measures 2.3.1. Measurement of cortical auditory evoked potentials (CAEPs) The cortical auditory evoked potentials (CAEPs) were recorded using the HEARLabTM system (Frye Electronics) [34] with the active electrode attached to the vertex position (Cz), referenced to the non-surgical ear mastoid (Ref), and the forehead as ground (Gnd).The test stimuli /m/,/g/,/t/ were extracted from a running speech of a female. They had little vowel transition and represented a spectral emphasis in the low-, mid-, high-frequency regions respectively and closely equaled to the International Long-Term Average Speech Spectrum (ILTASS). Their durations were 30, 30, 20 ms, separately, the interstimulus interval was 1125 ms. Speech stimuli were presented from a loudspeaker positioned at 0˚ azimuth, approximately 1.5 m from the test position, and the child sitting in a reclining chair and watching a silent cartoon. Prior to testing, CAEP equipment had been calibrated, and both Ref and Cz electrodes had an impedance of <5 kV.The recording window contained a 200 ms pre-stimulus baseline, and a 600 ms poststimulus, and artifact reject level was 150 mV. Online EEG band pass filter settings were 0.2–30 Hz. The speech stimuli were presented at 65 dB SPL, and at least 200artifact-freeepochs were accepted for each stimulus. The probability of detecting the cortical response was automatically analyzed by the statistical procedure (Hotelling’s T2) on the HEARLabTM system, with a system-generated significance level (p-value), a p-value 0.05 indicating a significant result.

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Table 1 Audiological and demographic characteristics of the subject sample. Nr

Gender

Etiology

AAI (years)

Pre-implant use of hearing aids

Bimodal stimulation

Implant side

Year of reaching max level of CAEP

Year of reaching max level of MESP

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23

F F F M M F M M M M M F M M M F M M F M M F M

Family history Unknown Unknown Unknown Rubella Rubella Unknown Unknown Family history Unknown Unknown Unknown Unknown Unknown Unknown Unknown Unknown Unknown Unknown Unknown Hypoxia Rubella Unknown Unknown

2.6 1.8 3.1 2.2 2.6 2.4 2.2 1.4 3.2 2.4 2.5 2.1 5.3 1.5 5.4 4.6 1.4 2.8 3.8 5.6 2.6 1.1 3.5

No No No No No No No Yes No No No Yes Yes Yes Yes No No No Yes No Yes No No

No No No No No No No No No No No No No No No No No No Yes No No Yes No

L L L L L L L L L L R L L L L L L L L L L L L

First Second Third Third First Second First Second Fourth Third Third Second Third Fourth Second First Fourth Third Second First First Fourth Second

Second Third Third Third Second Second Fourth Third Fourth Third Fourth — Third Fourth Third First — Fourth Second First Fourth Fourth Third

Abbreviations: F = Female, M = Male, AAI = Age at implantation, L = left, R = right. ‘‘First’’ means the first year after CI implantation; ‘‘Second’’ means the second year after CI implantation; ‘‘Third’’ means the third year after CI implantation; ‘‘Fourth’’ means the fourth year after CI implantation. ‘‘—’’ means the subject did not reach the max level of MESP at the last test time.

The recording of CAEPs was taken as objective evidence of the detection of speech stimuli at average conversational level (65 dB SPL). In this study, the presence or absence of P1 wave represented the presence or absence of cortical auditory evoked potentials. The scores of CAEPs were ranged from 0 to 3 for each child; a score of ‘‘0’’ was obtained when no CAEPs was elicited to any of the speech stimuli, while ‘‘3’’ was considered as evidence of CAEPs to all three speech stimuli presented at 65 dB SPL [11]. 2.3.2. Mandarin Early Speech Perception (MESP) test The MESP test was a closed-set evaluation measure of early speech perception abilities using picturable words as stimuli for children 2 or more years of age. It paralleled the English version early speech perception (ESP) but was not exactly the same as ESP. MESP included two additional subtests. The first three items (Speech Detection, Pattern Perception, Spondee Perception) of MESP were as same as the ESP, the fourth category Monosyllable Perception of ESP was split into the later three categories Vowel Perception, Consonant Perception, and Tone Perception in the MESP test. According to the characteristics of the mandarin Chinese, the six subtests were with increasing difficulty, only when the subject reached a threshold percentage, could he/she pass the category, and then went on the next subtest. Threshold percentage were referred as the lowest percentage for a category that was obviously higher than chance performance which were 54.5%, 30.3%, 63.6%, 63.6%, and 63.8% for Category 2, 3, 4, 5, and 6 respectively [25]. In our study, we used the standard version of MESP test. If the subject could not meet Category 1 (speech detection) criterion, the test was stopped; otherwise, the next category Pattern Perception, Spondee Perception, Vowel Perception, Consonant Perception, and Tone Perception was administered until the child did not reach the threshold scores of the testing category, the final passed category was written down. The result of MESP for a certain subject was displayed by the highest category that he/she finally passed. The Comparison of ESP and MESP test structures are shown in Table 2 [25].

2.4. Statistical analysis The relationship between the CAEP scores and MESP categories was analyzed by the Spearman correlation test. Multiple linear regression analysis was performed to investigate the relationship among CAEP scores, hearing ages and MESP categories. Statistical calculations were performed with SPSS 16.0 version. Two-sided pvalues 0.05 were considered to indicate statistical significance in all tests.

3. Results 3.1. The progress of cortical responses and speech perception Table 3 shows the numbers of subjects detecting the stimuli of CAEPs at different test intervals. The percentages of participants who could detect all three stimuli were from 26% (6/23) at first year to 100% (23/23) at fourth year post-implantation. From the scores of CAEP in Table 3, we also found that only 4 subjects could not detect speech sounds after 1 year of CI use, but all subjects demonstrated improvements throughout 2 years of observation post-implantation, and at the fourth year postimplantation, all children obtained the highest score 3. The category scores of MESP are shown in Table 4. The percentages of participants who passed the Category 6 were from 9% (2/23) at first year to 91% (21/23) at the fourth year post-implantation. Table 5 shows the detail scores of CAEP and MESP at different test intervals. 3.2. The changes of P1 latency Table 6 shows the changes of P1 latency during the test procedure. From the table we could see that there was no significant difference of P1 latency between the children who were fitted with cochlear implants before age 3.5 years and after age 3.5 years but before 7 years.

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Table 2 Comparison of ESP and MESP test structures. ESP

MESP

Category 1 Description

Speech Sound Detection Live voice determination of detection and awareness of speech

Speech Sound Detection Same as ESP

Category 2 Description

Speech Pattern Perception 12 words in four different syllable and stress patterns: three each of monosyllables, disyllable trochees, disyllable spondees, and trisyllables

Speech Pattern Perception Similar to ESP, Mandarin spondees have same tone in each syllable, and tone 3 is excluded

Category 3 Description

Spondee Identification 12 disyllabic spondees with widely differing consonants and vowels

Spondee Perception Similar to ESP, Mandarin spondees have the same tone in each syllable

Category 4 Description

Monosyllabic Word Identification 12 monosyllable words that begin with/b/and vary in medial vowel and final consonant

Vowel Perception 4 groups of 3 monosyllable words with same consonant and tone but different vowels

Category 5 Description

Consonant Perception 4 groups of 3 monosyllable word with same vowel and tone but different consonants

Category 6 Description

Tone Perception 6 subtests consisting of 4 pairs of monosyllabic words with same consonant and vowel but different tones

ESP: early speech perception; MESP: Mandarin Early Speech Perception.

3.3. The relationship between CAEP and MESP Fig. 1 shows the categories of MESP as a function of CAEP outcomes over four years post-implantation for all participants combined. A significant relationship was found between the categories of MESP andCAEP scores (rs = 0.757; n = 23; p = 0.000). The detailed relationships between the categories of MESP and the CAEP scores for the first, second and third year post-implantation are shown in Fig. 2 (rs = 0.622; n = 23; p = 0.002), 3 (rs = 0.701; n = 23; p = 0.000), and 4 (rs = 0.437; n = 23; p = 0.037), respectively. The fourth year post-implantation, the scores of CAEP presented a ceiling effect that all the participants got the highest CAEP score 3, so the relationship between CAEP and MESP at this year was not shown (Figs. 3 and 4). The relationship between the CAEP scores at the first year and MESP categories at the second, third year after surgery was shown

Table 3 Numbers of children in each CAEP scores at different test intervals. Score

Pre-operation

1 year

0 1 2 3

23

4 8 5 6

2 years

3 years

5 5 13

4 19

23

Total

23

23

23

23

23

Pre-operation

0 1 2 3 4 5 6

17 6

Total

23

1 year

2 years

3 years

Table 5 The score of CAEP and MESP at every test year. Nr

Gender

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23

F F F M M F M M M M M F M M M F M M F M M F M

4 years

Table 4 Numbers of children in each MESP category at different test intervals. Category

in Fig. 5 (rs = 0.747; n = 23; p = 0.000), and 6 (rs = 0.552; n = 23; p = 0.006). The relationship between the CAEP scores at the first year and MESP categories at the fourth year after surgery was not significant (rs = 0.320; n = 23; p = 0.136). A multiple linear regression was used to analyze the CAEPs that could reflect early speech perception. The MESP outcomes were the dependent variable, and the two independent variables were CAEP scores and years. The statistical test of regression equation was performed by ANOVA (F = 91.808, p < 0.001), so the multiple regression equation was obtained, the categories of MESP = 0.915 + (1.104  CAEP score) + (0.424  years post-implantation) (R2 = 0.674) (Fig. 6).

4 years

5 4 7 3 2 2

1 2 2 4 8 6

2 1 6 14

1 21

23

23

23

23

1

First year postimplantation

Second year postimplantation

Third year postimplantation

Fourth year postimplantation

CAEP

MESP

CAEP

MESP

CAEP

MESP

CAEP

MESP

3 2 2 0 3 1 2 3 1 1 0 1 1 0 1 3 0 2 2 3 3 1 1

3 1 2 1 3 3 4 5 3 3 3 2 4 2 2 6 1 3 5 6 4 1 1

3 3 2 1 3 3 2 3 1 2 2 3 1 3 3 3 1 2 3 3 3 1 3

6 5 5 2 6 6 5 5 4 5 3 5 4 3 5 6 2 4 6 6 5 1 4

3 3 2 3 3 3 3 3 2 3 3 3 3 3 3 3 2 3 3 3 3 2 3

6 6 6 4 6 6 6 5 5 6 5 5 6 5 6 6 3 5 6 6 6 3 6

3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3

6 6 6 6 6 6 6 6 6 6 6 5 6 6 6 6 3 6 6 6 6 6 6

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Table 6 Mean P1 latencies (ms) are shown for different age-implanted children. Stimuli

M G T

First year post-implantation

Second year postimplantation

Third year post-implantation

Fourth year postimplantation

AI < 3.5

3.5 < AI < 7

AI < 3.5

3.5 < AI < 7

AI < 3.5

3.5 < AI < 7

AI < 3.5

3.5 < AI < 7

132.1 125.1 123.0

137.7 125.3 129.3

126.6 119.2 121.4

125.3 124.4 128.8

116.5 115.3 117.2

116.2 118.4 117.3

105.0 106.1 112.9

102.6 108.9 108.6

Abbreviations: AI = age at implantation; AI < 3.5 means the age at implantation was younger than 3.5 years old; 3.5 < AI < 7 means the age at implantation was between 3.5 and 7 years old.

4. Discussion The main purpose of pediatric cochlear implantation is to provide hearing that will promote the development of speech and language like their normal hearing peers, allowing them to participate in the mainstream of society. Therefore the evaluation of the outcomes of CI is of great importance. Cortical response is an objective method that can provide information on the functioning of the central auditory nervous system [35]. This study aimed to evaluate the relationship between CAEP outcomes and speech perception over4years observations in pediatric users of the Nurotron1 cochlear implant system and to determine if the CAEPs could be used as an index for predicting outcomes of speech perception. From our results the majority of subjects demonstrated improvements in audibility skills throughout 2 years of observation post-implantation, and at the fourth year post-implantation, the subjects wholly obtained highest CAEP scores. While the presence of CAEPs to speech stimuli could provide early objective indications of the aided child’s ability to access speech by audition [11], the absence of cortical responses suggested that the speech sounds may have not been detected, or might be related to insufficient sensation level of the amplified sounds [36], or the immaturity of the central auditory system. Only four subjects could not detect speech sounds after 1 year of CI use. These four subjects who were insensitive to speech sounds may have not been behaviorally ready for this testing. Because the audiologists also kept the amplified sounds conservative when they adjusted the CI mapping, this may have contributed to the inadequate sensation levels needed to elicit cortical responses. CAEPs also might not be

Fig. 1. Horizontal axis shows the CAEP scores from 0 to 3, vertical axis shows the Category of MESP from 1 to 6. The line reveals MESP outcomes as a function of the overall CAEP scores for all participants over 4 years combined.

detectable in some individuals at low to medium sensation levels [37]. The findings of the current study suggested that cortical assessment was a useful objective tool to assess the effectiveness of amplification for sound detection and guide the CI mapping, rehabilitation training in the future. There were also many other factors that affected P1 wave. There was a sensitive period that influenced the central auditory development in CI children, the age cut-offs were set at 3.5 and 7.0 years (<3.5 years for early-implanted group and >7.0 years for late-implanted group). Many researches revealed that earlyimplanted children showed rapid development in CAEP waveform and P1 latency, but late-implanted children showed aberrant waveform morphology and slower decrease P1 latency after the surgery [38]. Dorman et al. found that if children experienced less than 3.5 years of auditory deprivation, P1 latency fell into the range of normal following 3–6 months stimulation; but if the auditory deprivation was longer than 7 years, P1 waveform would not develop into normal latency [39]. Therefore, the age at implantation was very important to the development of P1 latency, this told us that cochlear implantation should be performed as early as possible. In this study, there were only 7 children accepted their CI surgery after 3.5 years old but younger than 7 years old, and there was no significant difference between these two groups in P1 latency but the P1 latency of all the subjects decreased as their ages increased. Rehabilitation was also a factor that influenced P1 latency. Thabet’s [1] study revealed that prolonged P1 latencies would be recorded in hearing impaired children with inadequate rehabilitation. In our study, most children came from countryside;

Fig. 2. Horizontal axis shows the CAEP scores from 0 to 3, vertical axis shows the Category of MESP from 1 to 6. The line reveals the CAEP scores in relation to the MESP category for all participants at the first year post-implantation.

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Fig. 3. Horizontal axis shows the CAEP scores from 0 to 3, vertical axis shows the Category of MESP from 1 to 6. The line reveals the CAEP scores in relation to the MESP category for all participants at the second year post-implantation.

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Fig. 5. Horizontal axis shows the CAEP scores from 0 to 3, vertical axis shows the Category of MESP from 1 to 6. The line reveals the CAEP scores at the first year in relation to the MESP category at the second year post-implantation for all participants.

their parents did not have enough money to send them to rehabilitation institute, so it was not discussed in this study. Zheng and her colleagues created the MESP for developmentally normal 2–5 years old Mandarin-speaking children to evaluate early speech perception. Zheng demonstrated that all children aged 4–5 years old could reach all MESP categories successfully [25]. She also successfully used the MESP as subjective outcome assessment of speech perception and discrimination in pediatric CI recipients, and that after 4 years CI use, most Mandarin-speaking CI recipients had reached the highest MESP category 6[40]. The MESP outcomes of the participants in present study showed a delayedspeech language development compared with normal children at the same chronological age. Nearly all the recipients eventually reached level 6, the most difficult category in MESP, if the participant could pass this category, he/she might develop the

ability of Monosyllabic Word Identification which was also the most difficult category in ESP. There was a common developmental trajectory in relation to hearing age, which proved that the earlier cochlear implantation was done, the better the results were. The relationship between the categories of MESP and CAEP scores was examined for all participants over 4 years postimplantation and a significant positive correlation was found. There was significant correlation between the categories of MESP and CAEP scores for the first, second, and third year postimplantation. At the fourth year after surgery, the correlation between these two variables was not presented, because at that time the MESP categories and CAEP scores varied little as the audibility skills of all children in this study developed appropriately. While there was significant relationship between MESP

Fig. 4. Horizontal axis shows the CAEP scores from 0 to 3, vertical axis shows the Category of MESP from 1 to 6. The line reveals the CAEP scores in relation to the MESP category for all participants at the third year post-implantation.

Fig. 6. Horizontal axis shows the CAEP scores from 0 to 3, vertical axis shows the Category of MESP from 1 to 6. The line reveals the CAEP scores at the first year in relation to the MESP category at the third year post-implantation for all participants.

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categories and CAEP scores in children who used CI, but the amount of variance in MESP categories that was explained by CAEP was not very high suggesting that there were other factors that impact on the outcomes of MESP test. This could be the result of the abilities of the children improved as they got older individual differences, ages at implantation, duration of deafness, wellness of the family, the language used in daily life, and the education of their parents [41,42]. Therefore, the outcomes of MESP varied a lot. We believe this does not change the importance of CAEP outcomes to speech stimuli and their relationship to speech perception in children. Because the presence of CAEP and progress of speech perception using MESP were both reliant on the audibility of speech, our results were not amazing. For future research, we will consider extending the numbers of subjects, and discuss the relationship to different ages at implantation, different rehabilitation intensity, separately. This study also showed that the CAEP scores at the first year have relationships with the categories of MESP at the second and third year. CAEP could be a predictor of speech perception. For children with CI, better audibility skills were not correlated to excellent speech language performance in the future. However, poor audibility skills indicated low speech language performance. Clinical uses of auditory evoked potentials include threshold estimation and auditory discrimination, and many researchers focused their attention on the obligatory component of CAEPs, which was generally considered as the P1-N1-P2 complex [35]. Previous studies usually used P1 component to evaluate the benefits from cochlear implantation, auditory training, or amplification and the maturation process, plasticity of central nervous system in congenitally hearing-impaired children after they have been fitted with CI. [1,10,39,43–45]. Recently, research has revealed that CAEPs are also a valid tool for assessment of the effectiveness of hearing aids for young children. Maryanne’s [11] research results indicated the presence of cortical responses had a good relationship with functional measures of real-world listening behaviors. Recording CAEPs to speech stimuli could provide objective evidence that these amplified stimuli had reached the cortex and they were potentially audible to the individual with CI. Our findings revealed that significant positive correlation between CAEP scores and the categories of MESP, as for infants and young CI children, they were not able to provide feedback of reliable behavioral responses and could not cooperate with speech language tests, so cortical assessment was an objective method to evaluate the outcomes of cochlear implant, and could be used to assess the early speech perception as time went on. In summary, results from present study suggest that CAEP is a good way to evaluate the outcomes of CI, and a significant correlation exists between CAEP and MESP. CAEP can be used as a predictor of early speech perception in young children. Acknowledgements We were grateful to all the children and their families who participated in this study. The authors would like to gratefully acknowledge Wenfang Wu from Capital Medical University for the statistical analyses. The project was supported by the capital citizen health program to foster from Beijing Municipal Science & Technology Commission (No. Z141100002114033), the Beijing Municipal Administration of Hospitals Clinical Medicine Development of special funding support (No. XMLX201514), the capital health research and development of special from the Beijing Municipal Health Bureau (No. 2011-1017-01), the promotion grant for high level scientific and technological elites in medical science from the Beijing Municipal Health Bureau (No. 2009-3-29), key projects in basic and clinical research cooperation funds from Capital Medical University (No. 12JL12).

We thank our teachers, colleagues, and the Nurotron Company; they all make great contribution to experimental design, clinical guidance, technical support, and paper revision. The authors and their families have no fiscal or other relationship to Nurotron.

References [1] M.T. Thabet, N.M. Said, Cortical auditory evoked potential (P1): a potential objective indicator for auditory rehabilitation outcome, Int. J. Pediatr. Otorhinolaryngol. 76 (2012) 1712–1718. [2] K.R. Bachmann, J.C. Arvedson, Early identification and intervention for children who are hearing impaired, Pediatr. Rev. 19 (1998) 155–165. [3] A.E. Carney, M.P. Moeller, Treatment efficacy: hearing loss in children, J. Speech Lang. Hear. Res. 41 (1998) 61–84. [4] F.H. Bess, J. Dodd-Murphy, R.A. Parker, Children with minimal sensorineural hearing loss: prevalence, educational performance, and functional status, Ear Hear. 19 (1998) 339–354. [5] M.N. Kotby, S. Tawfik, A. Aziz, H. Taha, Public health impact of hearing impairment and disability, Folia Phoniatr. Logop. 60 (2008) 58–63. [6] M. Khairi Md Daud, R.M. Noor, N.A. Rahman, D.S. Sidek, A. Mohamad, The effect of mild hearing loss on academic performance in primary school children, Int. J. Pediatr. Otorhinolaryngol. 74 (2010) 67–70. [7] C. Yoshinaga-Itano, Levels of evidence: universal newborn hearing screening (UNHS) and early hearing detection and intervention systems (EHDI), J. Commun. Disord. 37 (2004) 451–465. [8] C. Yoshinaga-Itano, A.L. Sedey, D.K. Coulter, A.L. Mehl, Language of early- and later-identified children with hearing loss, Pediatrics 102 (1998) 1161–1171. [9] A.F. Snik, K. Neijenhuis, C.C. Hoekstra, Auditory performance of young children with hearing aids: the Nijmegen experience, Scand. Audiol. Suppl. 53 (2001) 61– 67. [10] A. Sharma, K. Martin, P. Roland, P. Bauer, M.H. Sweeney, P. Gilley, et al., P1 latency as a biomarker for central auditory development in children with hearing impairment, J. Am. Acad. Audiol. 16 (2005) 564–573. [11] M. Golding, W. Pearce, J. Seymour, A. Cooper, T. Ching, H. Dillon, The relationship between obligatory cortical auditory evoked potentials (CAEPs) and functional measures in young infants, J. Am. Acad. Audiol. 18 (2007) 117–125. [12] F.H. Bess, L.E. Humes, Audiology: The Fundamentals, Lippincott Williams and Wilkins, Philadelphia, 2003. [13] C.W. Ponton, J.J. Eggermont, Of kittens and kids: altered cortical maturation following profound deafness and cochlear implant use, Audiol. Neurootol. 6 (2001) 363–380. [14] T. McGee, N. Kraus, Auditory development reflected by middle latency response, Ear Hear. 17 (1996) 419–429. [15] P.A. Davis, The electrical response of the human brain to auditory stimuli, Am. J. Physiol. 126 (1939) 475–476. [16] B. Cone-Wesson, J. Wunderlich, Auditory evoked potentials from the cortex: audiology applications, Curr. Opin. Otolaryngol. Head Neck Surg. 11 (2003) 372–377. [17] D.L. Jewett, J.S. Williston, Auditory-evoked far fields averaged from the scalp of humans, Brain 94 (1971) 681–696. [18] N. Kraus, D.B. Koch, T.J. McGee, T.G. Nicol, J. Cunningham, Speech-sound discrimination in school-age children: psychophysical and neurophysiologic measures, J. Speech Lang. Hear. Res. 42 (1999) 1042–1060. [19] L. Carter, M. Golding, H. Dillon, J. Seymour, The detection of infant cortical auditory evoked potentials (CAEPs) using statistical and visual detection techniques, J. Am. Acad. Audiol. 21 (2010) 347–356. [20] M. Golding, H. Dillon, J. Seymour, L. Carter, The detection of adult cortical auditory evoked potentials (CAEPs) using an automated statistic and visual detection, Int. J. Audiol. 48 (2009) 833–842. [21] J.S. Moog, A.E. Geers, Early Speech Perception Test for Profoundly HearingImpaired Children, Central Institute for the Deaf, St. Louis, 1990. [22] L.S. Eisenberg, D.D. Dirks, Reliability and sensitivity of paired comparisons and category rating in children, J. Speech Hear. Res. 38 (1995) 1157–1167. [23] H.M. Yang, J.L. Wu, Y.H. Lin, Y.J. Sher, Development of Mandarin monosyllabic lexical neighbourhood test (LNT), Cochlear Implants Int. 5 (2004) 203–205. [24] M. Nilsson, S.D. Soli, J.A. Sullivan, Development of the Hearing in Noise Test for the measurement of speech reception thresholds in quiet and in noise, J. Acoust. Soc. Am. 95 (1994) 1085–1099. [25] Y. Zheng, Z.L. Meng, K. Wang, Y. Tao, K. Xu, S.D. Soli, Development of the Mandarin early speech perception test: children with normal hearing and the effects of dialect exposure, Ear Hear. 30 (2009) 600–612. [26] K.F. Alvarenga, R.B. Amorim, R.S. Agostinho-Pesse, O.A. Costa, L.T. Nascimento, M.C. Bevilacqua, Speech perception and cortical auditory evoked potentials in cochlear implant users with auditory neuropathy spectrum disorders, Int. J. Pediatr. Otorhinolaryngol. 76 (2012) 1332–1338. [27] G. Rance, B. Cone-Wesson, J. Wunderlich, R. Dowell, Speech perception and cortical event related potentials in children with auditory neuropathy, Ear Hear. 23 (2002) 239–253. [28] V.K. Narne, C. Vanaja, Speech identification and cortical potentials in individuals with auditory neuropathy, Behav. Brain Funct. 4 (2008) 15–22. [29] P.A. Groenen, M. Makhdoum, J.L. van den Brink, M.H. Stollman, A.F. Snik, P. van den Broek, The relation between electric auditory brain stem and cognitive

Q. Guo et al. / International Journal of Pediatric Otorhinolaryngology 85 (2016) 170–177

[30] [31] [32]

[33]

[34]

[35] [36]

[37]

responses and speech perception in cochlear implant users, Acta Otolaryngol. 116 (1996) 785–790. P.R. Kileny, A. Boerst, T. Zwolan, Cognitive evoked potentials to speech and tonal stimuli in children with implants, Otolaryngol. Head Neck Surg. 117 (1997) 161–169. A.J. Beynon, A.F. Snik, P. van den Broek, Evaluation of cochlear implant benefit with auditory cortical evoked potentials, Int. J. Audiol. 41 (2002) 429–435. K.A. Gordon, S. Tanaka, B.C. Papsin, Atypical cortical responses underlie poor speech perception in children using cochlear implants, Neuroreport 16 (2005) 2041–2045. A.S. Kelly, S.C. Purdy, P.R. Thorne, Electrophysiological and speech perception measures of auditory processing in experienced adult cochlear implant users, Clin. Neurophysiol. 116 (2005) 1235–1246. K.J. Munro, S.C. Purdy, S. Ahmed, R. Begum, H. Dillon, Obligatory cortical auditory evoked potential waveform detection and differentiation using a commercially available clinical system: HEARLab, Ear Hear. 32 (2011) 782–786. A. Almeqbel, Speech-evoked cortical auditory responses in children with normal hearing, S. Afr. J. Commun. Disord. 60 (2013) 38–43. V.W. Zhang, T.Y. Ching, P. Van Buynder, S. Hou, C. Flynn, L. Burns, et al., Aided cortical response, speech intelligibility, consonant perception and functional performance of young children using conventional amplification or nonlinear frequency compression, Int. J. Pediatr. Otorhinolaryngol. 78 (2014) 1692–1700. H.W. Chang, H. Dillon, L. Carter, B. van Dun, S.T. Young, The relationship between cortical auditory evoked potential (CAEP) detection and estimated audibility in infants with sensorineural hearing loss, Int. J. Audiol. 51 (2012) 663–670.

177

[38] A. Sharma, M.F. Dorman, A. Karl, The influence of a sensitive period on central auditory development in children with unilateral and bilateral cochlear implants, Hear. Res. 203 (2005) 134–143. [39] M.F. Dorman, A. Sharma, P. Gilley, K. Martin, P. Roland, Central auditory development: evidence from CAEP measurements in children fit with cochlear implants, J. Commun. Disord. 40 (2007) 284–294. [40] Y. Zheng, S.D. Soli, Z.L. Meng, Y. Tao, K. Wang, K. Xu, et al., Assessment of Mandarin-speaking pediatric cochlear implant recipients with the Mandarin Early Speech Perception (MESP) test, Int. J. Pediatr. Otorhinolaryngol. 74 (2010) 920–925. [41] Himanshu Swami, E. James, K. Sabrigirish, S.K. Singh, Meena Ohal, A study to determine factors influencing outcomes of pediatric cochlear implants, Med. J. Armed Forces India 69 (2013) 366–368. [42] Y. Li, R. Dong, Y. Zheng, T. Xu, Y. Zhong, C. Meng, et al., Speech performance in pediatric users of Nurotron1 Venus cochlear implants, Int. J. Pediatr. Otorhinolaryngol. 79 (2015) 1017–1023. [43] S. Jiwani, B.C. Papsin, K.A. Gordon, Central auditory development after long-term cochlear implant use, Clin. Neurophysiol. 124 (2013) 1868–1880. [44] A. Sharma, A.A. Nash, M. Dorman, Cortical development, plasticity and reorganization in children with cochlear implants, J. Commun. Disord. 42 (2009) 272–279. [45] S. Singh, A. Liasis, K. Rajput, A. Towell, L. Luxon, Event-related potentials in pediatric cochlear implant patients, Ear Hear. 25 (2004) 598–610.