Intelligence development of pre-lingual deaf children with unilateral cochlear implantation

International Journal of Pediatric Otorhinolaryngology 90 (2016) 264e269

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Intelligence development of pre-lingual deaf children with unilateral cochlear implantation Mo Chen, Zhaoyan Wang, Zhiwen Zhang, Xun Li, Weijing Wu, Dinghua Xie, Zi-an Xiao* Department of Otorhinolaryngology Head & Neck Surgery, The Second Xiangya Hospital of Central South University, Changsha, Hunan, China

a r t i c l e i n f o

a b s t r a c t

Article history: Received 6 July 2016 Received in revised form 21 September 2016 Accepted 22 September 2016 Available online 28 September 2016

Objective: The present study aims to test whether deaf children with unilateral cochlear implantation (CI) have higher intelligence quotients (IQ). We also try to find out the predictive factors of intelligence development in deaf children with CI. Methods: Totally, 186 children were enrolled into this study. They were divided into 3 groups: CI group (N ¼ 66), hearing loss group (N ¼ 54) and normal hearing group (N ¼ 66). All children took the HiskeyNebraska Test of Learning Aptitude to assess the IQ. After that, we used Deafness gene chip, Categories of Auditory Performance (CAP) and Speech Intelligibility Rating (SIR) methods to evaluate the genotype, auditory and speech performance, respectively. Results: At baseline, the average IQ of hearing loss group (HL), CI group, normal hearing (NH) group were 98.3 ± 9.23, 100.03 ± 12.13 and 109.89 ± 10.56, while NH group scored higher significantly than HL and CI groups (p < 0.05). After 12 months, the average IQ of HL group, CI group, NH group were99.54 ± 9.38,111.85 ± 15.38, and 112.08 ± 8.51, respectively. No significant difference between the IQ of the CI and NH groups was found (p > 0.05). The growth of SIR was positive correlated with the growth of IQ (r ¼ 0.247, p ¼ 0.046), while no significant correlation were found between IQ growth and other possible factors, i.e. gender, age of CI, use of hearing aid, genotype, implant device type, inner ear malformation and CAP growth (p > 0.05). Conclusions: Our study suggests that CI potentially improves the intelligence development in deaf children. Speech performance growth is significantly correlated with IQ growth of CI children. Deaf children accepted CI before 6 years can achieve a satisfying and undifferentiated short-term (12 months) development of intelligence. © 2016 Published by Elsevier Ireland Ltd.

Keywords: Cochlear implantation Non-verbal IQ Pre-lingual deaf children Auditory and speech performance

1. Introductions The development of multichannel cochlear implant (CI) and the improvement in surgical skills have made cochlear implantation an accepted and standard treatment for severe to profound sensorineural hearing loss in children and adults. The primary effect of CI is to enable speech perception [1], and improvements in speech perception are often accompanied by gains in oral language development [2]. The outcome of CI varies over a wide range among pediatric patients. Some prelingually deafened children show outstanding

* Corresponding author. Department of Otolaryngology Head & Neck Surgery, The Second Xiangya Hospital, Central South University, No. 139 Renmin Road, Changsha, Hunan Province, 410011, China. E-mail address: [email protected] (Z.-a. Xiao). http://dx.doi.org/10.1016/j.ijporl.2016.09.031 0165-5876/© 2016 Published by Elsevier Ireland Ltd.

behavioral performance, such as the rapid acquisition of spoken language and the production of intelligible speech after years of CIassisted rehabilitative effort, while other children develop awareness of environmental or speech sounds but never catch up with normal age-appropriate auditory language [3]. Previous studies have provided the evidence that the younger age at implantation, the better outcomes of spoken language and speech perception [4,5]. Some studies indicated that children with CI who had GJB2related deafness displayed better auditory and speech performance [6,7]. A great deal of researches have been devoted to understanding hearing and spoken language development in deaf children with CI, very little has been performed to investigate general intelligence development after CI. As we known, children with even mild or unilateral hearing loss tend to score lower on intelligence tests than normal hearing peers [8,9]. Studies of some aspects of cognitive capabilities in children with and without normal hearing have revealed that the latter

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The HL group consisted of 25girls and 29 boys, with mean age 3.94 ± 0.89 (range 3e6 years). The NH group consisted of 66 healthy children, 32 girls and 34 boys, with mean age 4.09 ± 1.02 (range 3e6 years). No statistically significant difference among three groups on gender (p ¼ 0.125), age (p ¼ 0.964) and family incomes (p ¼ 0.461) were found (Table 1). Informed consent was obtained in all cases, and protocols were approved by scientific ethical committee of the Second Xiangya Hospital.

experience difficulties at the cognitive level [10,11]. We wonder that, as long as deaf children provided with sufficient language and communication access by CI, could they obtain a better outcome of intelligence development? And what are the predictive factors of their intelligence development? A few studies stated that children with CI display distinctive developmental patterns in cognitive function, compared with normal hearing children and deafness children [12,13], and implant age was a predictive factor of intelligent development of children with CI [14]. There is still a need for a greater understanding of CI users' intelligence development and the predictive factors. Thus, this study aims to evaluate the intelligence quotients diversity among CI children, deaf children and normal-hearing children. We also try to find out the related factors that influence the outcomes of intelligence development in deaf children with CI.

2.2. Research procedures and content Table 2 shows the research procedures and content of this study. All patients took the IQ test in the first and 12th month, respectively. Children in CI group had the auditory and speech tests in the first and 12th month. Besides, CI group had underwent Magnetic Resonance Imaging (MRI) and Computed Tomography (CT) of ears, deaf related gene test and cochlear implantation in the first month.

2. Methods 2.1. Subjects

2.3. Assessments We recruited 66 children (cochlear implantation group, CI group) with profound hearing loss who received unilateral CI at the Department of Otolaryngology Head and Neck Surgery, the Second Xiangya Hospital, Central South University in China. The inclusion criteria were: bilateral pre-verbal profound sensorineural hearing loss, and age between 3 and 6 years. Exclusion criteria included a history of a seizure disorder, learning disability, progressive neurological problem or traumatic brain injury, additional significant disabilities (e.g., blindness, autism), not using mandarin as the primary mode of communication or any other serious medical condition. The CI group consist of 32 girls and 34 boys, mean age 4.35 ± 0.98 (range 3e6 years). All children were implanted with unilateral CI at a mean age of 3.35 ± 0.98 months (range 2e5 years). Thirty four (51.5%) children used hearing aid while thirty two (48.5%) children did not. CI children were implanted with unilateral CI of CI24R (Cochlear Corperation, Australia) (n ¼ 27), Combi40þ (MED-EL Corperation, Austria) (n ¼ 30) or Hires90k (AB Corperation, America) (n ¼ 41). Eight (12.1%) children were found Large Vestibular Aqueduct Syndrome (LVAS), while fifty eight (87.9%) were not. We also recruited 66 healthy children with normal hearing (normal-hearing group, NH group) and 54 deaf children without CI (hearing loss group, HL group) who were matched with children with CI in CI group by their chronological ages, hearing loss degree, hearing aid experiences, genders and family incomes. The same exclusion criteria used in the CI group were used to select the control group.

2.3.1. The Hiskey-Nebraska Test of Learning Aptitude For the evaluation of intelligence, all the children in 3 groups were assessed the first time in the first month after recruited into this study and the second time 12 months later at the Deaf Children Rehabilitation Center of Hunan Province. The Hiskey-Nebraska Test of Learning Aptitude (H-NTLA) is among the most widely used measures of non-verbal intellectual ability with hearing impaired youngster, and has been described as one of the best individual tests for this population [15]. It is widely used all over the world [16]. The H-NTLA consists of measure aspects of visual memory, visual organization, visual discrimination, and visual association. Administration is through pantomimed directions, and responses are given nonverbally. It includes 12 subtests which are sort from easy to difficult: (1) beads stringing; (2) color remembering; (3) figure identification; (4) picture association; (5) paper folding; (6) short-term visual memory; (7) building blocks; (8) picture finishing; (9) number remembering; (10) building mazy blocks; (11) picture analogy; (12) spatial reasoning. Subjects age 3e8 take the former 8 subtests while age 9e17 take the later 7 subtests. Subjects in this study range from 3 to 6 years old, thus, we used the former 8 subtests. Two experienced psychologists conducted all subtests separately. Each subtest score is converted to learning age. From 8 subtests, we got 8 learning ages, and the median learning age is used to determine each participant's ratio intelligence quotient (RIQ). RIQ ¼ (median age/chronological age)  100. According to two psychologists, we got 2 RIQ scores for every subject. We used

Table 1 General information about the participants. CI (n ¼ 66)

HL (n ¼ 54)

NH (n ¼ 66)

Gender Male Female

34 32

29 25

34 32

16 19 23 8

19 23 8 4

16 19 23 8

9 35 22

9 29 16

10 36 20

Age 3 years 4 years 5 years 6 years Family incomes (RMB/year) <30,000 30,000e80,000 >80,000

CI ¼ cochlear implant; HL ¼ hearing loss; NH ¼ normal hearing.

c2

p

0.074

0.964

9.990

0.125

1.548

0.461

266

M. Chen et al. / International Journal of Pediatric Otorhinolaryngology 90 (2016) 264e269

Table 2 Research procedures and content.

HL and NH group: CI group:

Month1

Month12

IQ test IQ test Auditory test Speech test MRI and CT of ears Deaf related gene test Cochlear implant

IQ test IQ test Auditory test Speech test

CI ¼ cochlear implant; HL ¼ hearing loss; NH ¼ normal hearing; IQ ¼ intelligence quotients; MRI ¼ magnetic resonance imaging; CT ¼ computed tomography.

the mean RIQ score as the final RIQ of every subject. 2.3.2. Deafness related gene detection of CI group CI group children's genes were assayed at the Otology Research Institute of the Second Xiangya Hospital before implantation. Allele-specific PCR-based universal arrays (ASPUAs) were used to simultaneously screen for nine mutations that cause hereditary hearing loss, including GJB2 (35delG, 176dell6bp, 235delC and 299delAT), GJB3 (5380T), SLC26A4 (IVS7-2A > G2168A > G) and mitochondrion 12SrRNA (14940T, 1555A > G). The detection rates of GJB2 and SLC26A4 were 20 (30.3%) and 5 (7.6%) respectively. No GJB3 and 12SrRNA related mutations were found. 2.3.3. Auditory and speech performance of CI group Auditory and speech performance of CI group were assessed before and 12 months after cochlear implantation with Categories of Auditory Performance (CAP) scale and Speech Intelligibility Rating (SIR) scale at Deaf Children Rehabilitation Center of Hunan Province. The CAP is a nonlinear hierarchical scale that assesses the auditory performance of deaf patients and consists of 8 categories (from 0 to 7) [17]. The SIR classifies the intelligibility of patients' spontaneous speech into 5 categories (from 1 to 5) [18] (Table 3). Higher ratings indicate better performances. The reliability of both scales has been confirmed. CAP and SIR were rated by 2 speech therapists preoperatively then we took the mean score of 2 therapists.

Graph 1. Intelligence development of 3 groups during 12 months (*p < 0.05).

Table 4 CAP development. Level

7 6 5 4 3 2 1 0 Total

0 month

12 months

n

Pct

Cum.Pct

n

Pct

Cum.Pct

0 0 0 1 4 4 49 8 66

0 0 0 1.5 6.1 6.1 74.2 12.1 100

0 0 0 1.5 7.6 13.7 87.9 100 100

6 7 22 20 3 2 6 0 66

9.1 10.6 33.3 30.3 4.5 3.0 9.1 0 100

9.1 19.7 53.0 83.3 87.8 90.8 100 100 100

CAP ¼ categories of auditory performance.

relationship between the growth of IQ and possible factors. All statistical analyses were conducted by SPSS (version 17.0, SPSS Inc., Chicago, IL) and the significance level was set at p < 0.05. 3. Results

2.4. Data analysis

3.1. Intelligence development

We firstly calculated proportions, means and standard deviations of descriptive variables. T tests and one-way ANOVAs were used for comparison among different groups. The Pearson and Spearman correlation coefficient were used to examine the

Before implantation, the average IQ of HL group, CI group, NH group were 98.3 ± 9.23, 100.03 ± 12.13 and 109.89 ± 10.56, respectively. After 12 months, the average IQ of HL group, CI group, NH group were99.54 ± 9.38,111.85 ± 15.38, and 112.08 ± 8.51,

Table 3 Criteria of CAP and SIR. Rating scale

Criteria

Categories of Auditory Performance 7 Use of telephone with known listener 6 Understanding of conversation without lip-reading 5 Understanding of conversation without lip-reading 4 Discrimination of some speech sounds without lip-reading 3 Identification of environmental sounds 2 Response to speech sounds 1 Awareness of environmental sounds 0 No awareness of environmental sounds Speech Intelligibility Rating 5 Connected speech is intelligible to all listeners. Child is understood easily in everyday contexts. 4 Connected speech is intelligible to a listener who has a little experience of a deaf person's speech 3 Connected speech is intelligible to a listener who concentrates and lip-reads 2 Connected speech is unintelligible. Intelligible speech is developing in single words when context and lip-reading cues are available 1 Connected speech is unintelligible. Pre-recognizable words in spoken language, primary mode of communication may be manual CAP ¼ categories of auditory performance; SIR ¼ speech intelligibility rating.

M. Chen et al. / International Journal of Pediatric Otorhinolaryngology 90 (2016) 264e269 Table 5 SIR development. Level

5 4 3 2 1 Total

267

Table 7 Spearman correlations for children with CI.

0 month

12 months

n (%)

n

Pct.

Cum.Pct.

n

Pct.

Cum.Pct.

0 0 1 3 62 66

0 0 1.5 4.5 93.9 100

0 0 1.5 6 100 100

9 12 21 21 3 66

13.6 18.2 31.8 31.8 4.5 100

13.6 31.8 63.6 95.4 100 100

SIR ¼ speech intelligibility rating.

IQ growth

Gender Male Female

34 (51.5) 32 (48.5)

11.94 ± 13.37 11.69 ± 16.49

2 3 4 5

16 (24.2) 19 (28.8) 23 (34.8) 8 (12.1)

9.69 ± 17.79 11.53 ± 16.39 15.17 ± 12.22 7.12 ± 11.72

Yes No

34 (51.5) 32 (48.5)

14.71 ± 15.74 8.75 ± 13.41

GJB2 SLC26A4 Wild

20 (30.3) 5 (7.6) 41 (62.1)

10.21 ± 12.34 21.21 ± 12.03 11.46 ± 16.10

CI24R Combi40þ Hires90k

27 (40.9) 33 (50.0) 6 (9.1)

11.56 ± 15.08 11.30 ± 14.43 15.83 ± 18.14

Yes No

8 (12.1) 58 (87.9)

13.75 ± 10.98 11.55 ± 15.37

Age of CI years years years years

Use of hearing aid

respectively. Tukey-Kramer post-hoc multiple comparison was used to access the difference between 3 groups. At the beginning of this study, HL group and CI group's IQ scores were obviously lower than NH group (p < 0.05), after 12 months, CI group's IQ scores had increased dramatically. The IQs of the children in the NH and CI groups were significant higher than those of the children in the HL group (p < 0.05), while no significant difference between the CI and NH groups (p > 0.05) (Graph 1).

Genotype

Implant type

Inner ear malformation

t/F

P

2.256

0.138

0.762

0.520

1.650

0.104

0.379

0.686

0.238

0.789

1.313

0.256

3.2. Auditory and speech development of CI group

CI ¼ cochlear implant; IQ ¼ intelligence quotients.

Before CI, the majority of children were categorized as level 1 of auditory (74.2%) and speech performance (93.9%) according to CAP and SIR, respectively. After 12 months with CI, most of children had at least level 3 of auditory (87.9%) and speech performance (63.6%) (Table 4 and Table 5).

Clearly. Previous study about outcomes of CI users focus on auditory and speech rehabilitation, this study provide us a more comprehensive understand of the benefits that CI users can get. 4.1. Intelligence development

3.3. Correlation between IQ and auditory and speech performance developing The change of auditory and speech were significantly associated with each other (r ¼ 0.604, p ¼ 0.000). The speech change was correlated with the growth of IQ (r ¼ 0.247, p ¼ 0.046), while no association was found between the change of auditory and IQ (r ¼ 0.193, p ¼ 0.121) (Table 6). 3.4. Related factors of IQ in children with CI As shown in Table 7, we compared the means of IQ growth by different factors, i.e. gender, age of CI, use of hearing aid, genotype, implant device type, inner ear malformation, and no significant difference was found (p > 0.05). 4. Discussions The results of this study provide evidence consistent with previous work for an improvement of CI children's intelligence development. CI children with lower intelligence scores were consistently related worse on a speech performance measure.

This study demonstrated that CI might play a very important role in the intelligence development of deaf children. The intelligence development of children with CI was significantly better than that of deaf children without CI; even reach the level of normalhearing peers. This was consistent with a previous study that used the Wechsler Intelligence Scale for Children (WISC) in 30 children with CI [19]. Children's mental development is a process in which their brain and nervous system assimilate and adapt to their external environment. Because of hearing impairment in the infantile period, the nervous system cannot obtain enough information from the external environment, which may affect intelligence development. CI provides deaf children with exposure to sound, enrich their knowledge, boost their confidence, thus promoting their intelligence development. Therefore, for deaf children, the earlier the diagnosis and intervention, the better the intelligence development. CI was found to be the preferred and most effective intervention. Using hearing aids and receiving educations in schools will also help these children increase their chances of connecting with the outside world and obtaining more information, which help the intelligence development as well.

Table 6 Pearson correlations for children with CI.

Growth of IQ pearson correlation p. (2-tailed) Growth of CAP pearson correlation p. (2-tailed) Growth of SIR pearson correlation p. (2-tailed)

Growth of IQ

Growth of CAP

Growth of SIR

1

0.193 0.121 1

0.247* 0.046* 0.604** 0.000** 1

0.193 0.121 0.247* 0.046*

0.604** 0.000**

CI ¼ cochlear implant; IQ ¼ intelligence quotients; CAP ¼ categories of auditory performance; SIR ¼ speech intelligibility rating. *p < 0.05. **p < 0.001.

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4.2. Correlations between IQ and possible factors In this study, we explored eight possible predictive factors, including auditory and speech performance, gender, age at CI, genotype, implant device type, inner ear malformation and use of hearing aid. According to our data, only speech performance was significantly correlated with growth of IQ. 4.2.1. Auditory and speech performance Although, a research in Korea observed 13 CI users for 1e2 years and found that there was a strong correlation between the performance IQ and postoperative CAP scores [20]. But the present study didn't shown auditory performance was one of the IQ predictive factors. The recovery of auditory is the most intuitive benefits to CI users with minimum variability when compare to speech and intelligence development, which means most CI users' auditory performance would reach a relative consistency level, but speech and intelligence developing had a noticeable individual differences. This shown language ability and IQ developing didn't fully synchronous with the auditory recovery. According to our data, only speech performance was significantly correlated with growth of IQ. It was consistent with the previous study indicated that intelligence performance, especially social cognition, is correlated with the postoperative speech outcome in CI users [20]. In another study, language ability and behavior problem of 11,506 children in USA range 4e12 yeas old were measured, suggested that language ability predicted later behavior problems in children [21]. Some researchers observed 62 children with CI in Australia claimed intelligence development was correlated with auditory and verbal ability recovery [22]. We supposed that better language ability result in better intelligence development, which means more attention should be paid to speech training before and after CI in order to gain a satisfying intelligence development. 4.2.2. Implanted age It was claimed that the optimal time to implant a young deaf child is within a sensitive period of age 0e3.5 years in childhood (best by the first two years of life), cochlear implantation in the early years allows for normal auditory cortical maturation and provides ample opportunities for the appropriate acquisition of speech and oral language skills [23]. Deaf Children also gain better cognitive skills, adaptive behaviors, social and emotional skills from earlier CI [24,25]. In order to help children gain exposure to as much external stimulation as possible during there sensitive period, some researchers suggested deaf children accept CI as earlier as possible without regards to the increasing risk of anesthesia and surgery [26,27]. This study demonstrated that deaf children accepted CI before 6 years old can achieve a satisfying and undifferentiated short-term (12months) development of intelligence. 4.2.3. Genotype and use of hearing aids With the advances in molecular genetics, the chance to detect the underlying gene defect in childhood deafness has increased rapidly. In many countries, mutations of the GJB2 gene account for the majority of hereditary pre-lingual deafness, while mutations of the gene SLC26A4 also play an important role. Patients carrying causal biallelic mutations in either of the two genes seem to strongly benefit from CI [28]. However, the impact of GJB2 gene on CI users'auditory and speech outcomes, when compared to other deafness etiologies, is rather controversial [7]. Few research focuses on the influence of etiology to IQ developing of CI child. As we known, previous researches demonstrated clearly the benefits of early fitting of hearing aids. CI users with early fitting of hearing aid not only gain better auditory and speech recovery, but also better

cognitive development [14,29]. In the present study, No evidence has yet shown that hearing aid use and genotypes, two factors associated with auditory and verbal ability recovery in children with CI, are involved in intelligence improvement. This may partially due to the function of protein coded by deaf related gene, or the limitation of sample quantity. Getting effective hearing is the first step to learn language and accept more outside information. If deaf child can get effective hearing by wearing hearing aid, he could gain an improvement in verbal ability and intelligence through hearing and speech training. In the present study, we recruited children with bilateral pre-verbal profound sensorineural hearing loss, which means all of the subjects have merely residual hearing. Hearing aid is an effectively treatment for people who have residual hearing, the more residual hearing, the better outcome with hearing aid. Some of the subjects used hearing aid, but almost all of them were not satisfied with the effect of it and gave up in one year. Due to their extremely poor hearing even with hearing aid and limitation of follow up observation, no evidence has yet shown that hearing aid are involved in intelligence improvement of children with bilateral pre-verbal profound sensorineural hearing loss in this study. 4.2.4. Inner ear malformation Recently, due to improvements in technology, inner ear deformities are no longer an absolute contraindication to cochlear implantation. However the more severe the deformity, the more challenging the surgery and the outcomes. In the present study, there were 8 (12.1%) children in CI group were found Large Vestibular Aqueduct Syndrome (LVAS), shown no IQ difference from other normal implantees. Numerous studies showed that LAVS patients could acquire satisfying hearing and speech improvements [30,31]. We considered, cochlear implantation in deaf children with LVAS is feasible and effective. While other inner ear disorders may not reach similar outcomes, children with Cochlear Nerve Deficiency (CND) obtained limited substantial benefits from cochlear implantation, and their auditory and speech outcomes were extremely worse than children with normal cochlear nerves [32]. 4.3. Limitations There were some limitations in this study. First of all, a sample bias was unavoidable by such a sample size of 66 subjects in this study due to size of CI populations and the difficulty of follow-up of this special population. But it was still the largest sample among similar researches. So, the guiding significance of this research should not be underestimated. Secondly, the follow-up time was too short to find the complete rehabilitation regulation of CI users. A larger sample of CI users from a multi-center with a longer follow-up period for a more extensive evaluation of the effectiveness of CI is recommended. Meanwhile, no studies of post-CI intelligence in deaf adults have been reported, this rather prominent gap in this field might offer an area for productive investigation. 5. Conclusions Our study suggests that CI potentially improves the intelligence development in deaf children. Speech performance growth is significantly correlated with IQ growth of CI children. Deaf children accepted CI before 6 years can achieve a satisfying and undifferentiated short-term (12 months) development of intelligence. Benefits of CI include not only better abilities to hear and to develop speech and language skills but also improved intelligence development, academic attainment, quality of life and better employment status.

M. Chen et al. / International Journal of Pediatric Otorhinolaryngology 90 (2016) 264e269

Conflicts of interest and source of funding The authors declare that they have no conflict of interest. We acknowledge the financial support of the project of Natural Science Foundation of China (30572021), Hunan Provincal Natural Science Foundation (11JJ6087) and the Fundamental Research Funds for the Central Universities of Central South University (2015ZZTS121). Acknowledgement The authors thank the children and families who participated in this research. We thank the second Xiangya hospital of central south university, the Deaf Children Rehabilitation Center of Hunan Province. References [1] V. Vincenti, A. Bacciu, M. Guida, et al., Pediatric cochlear implantation: an update, Ital. J. Pediatr. 40 (2014) 72. [2] J.K. Niparko, E.A. Tobey, D.J. Thal, et al., Spoken language development in children following cochlear implantation, JAMA 303 (2010) 1498e1506. [3] H.J. Lee, E. Kang, S.H. Oh, et al., Preoperative differences of cerebral metabolism relate to the outcome of cochlear implants in congenitally deaf children, Hear Res. 203 (2005) 2e9. [4] E.A. Tobey, D. Thal, J.K. Niparko, et al., Influence of implantation age on schoolage language performance in pediatric cochlear implant users, Int. J. Audiol. 52 (2013) 219e229. [5] C.C. Dunn, E.A. Walker, J. Oleson, et al., Longitudinal speech perception and language performance in pediatric cochlear implant users: the effect of age at implantation, Ear Hear. 35 (2014) 148e160. [6] S. Janeschik, M. Teschendorf, H. Bagus, et al., Influence of etiologic factors on speech perception of cochlear-implanted children, Cochlear Implants Int. 14 (2013) 190e199. [7] L. Varga, Z. Kabatova, I. Masindova, et al., Is deafness etiology important for prediction of functional outcomes in pediatric cochlear implantation? Acta oto-laryngologica 134 (2014) 571e578. [8] P.L. Purcell, J.R. Shinn, G.E. Davis, et al., Children with unilateral hearing loss may have lower intelligence quotient scores: a meta-analysis, Laryngoscope 126 (2016) 746e754. [9] T.W. Teasdale, M.H. Sorensen, Hearing loss in relation to educational attainment and cognitive abilities: a population study, Int. J. audiology 46 (2007) 172e175. [10] S. Fukuda, K. Fukushima, Y. Maeda, et al., Language development of a multiply handicapped child after cochlear implantation, Int. J. Pediatr. Otorhinolaryngol. 67 (2003) 627e633. [11] P. Kushalnagar, T.D. Topolski, B. Schick, et al., Mode of communication, perceived level of understanding, and perceived quality of life in youth who are deaf or hard of hearing, J. deaf Stud. deaf Educ. 16 (2011) 512e523. [12] M.T. Le Normand, C. Ouellet, H. Cohen, Productivity of lexical categories in French-speaking children with cochlear implants, Brain Cogn. 53 (2003) 257e262. [13] G. Le Maner-Idrissi, S. Barbu, G. Bescond, et al., Some aspects of cognitive and social development in children with cochlear implant, Dev. Med. child

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