The development of auditory performance and speech perception in CI children after long-period follow up

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The development of auditory performance and speech perception in CI children after long-period follow up Qianqian Guoa,b, Jing Lyua,b, Ying Konga,b, Tianqiu Xua,b, Ruijuan Donga,b, Beier Qia,b, ⁎ Shuo Wanga,b, Xueqing Chena,b, a b

Beijing Tongren 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

ARTICLE INFO

ABSTRACT

Keywords: Categorical auditory performance Speech intelligibility rating Cochlear implantation Children

Purpose: The main purpose of the current study was to assess the development of auditory and speech perception and the effects of the age at implantation in CI children after long-period follow up. Materials and methods: Five hundred and forty-four young children participated in this study (339 males and 205 females). The age at implantation ranged from 6 months to 36 months. All subjects were prelingually bilateral profound sensorineural hearing loss. They were divided into 3 groups according to the implant ages: group 1 (age at implantation < 12 months, n = 109); group 2 (12 months < age at implantation < 24 months, n = 284); and group 3 (24 months < age at implantation < 36 months, n = 151). The categorical auditory performance (CAP) was used to assess auditory abilities and the speech intelligibility rating (SIR) was used to assess the speech intelligibility of these CI children. The tests were administered at pre-surgery and 1, 3, 6, 12, 24, 36, 48- and 60-months post-surgery. Results: All the subjects demonstrated improvements of auditory abilities and speech intelligibility after CI surgery. The auditory ability developed quickly in 12 months after implantation. However, the speech intelligibility scores show rapid improvement within 24 months post implantation. Significant difference was found between group 1 and group 3, group 2 and group 3 before 12 months post-implantation for CAP and SIR. The three groups of children showed similar development pattern for their auditory abilities and speech intelligibility. Conclusion: The results of this study suggested dramatic and continuous improvement of the auditory and speech abilities post implantation in these CI children. Furthermore, the age at implantation played a considerably smaller role in the improvement of hearing and speech abilities. However, earlier implantation still benefits the language development.

1. Introduction In the whole world, approximately 10% of the population suffers from hearing loss [1]. In China, there are about 27.8 million deaf populations. For the infants with hearing loss, they are at risk of delayed speech and language development and other social problems [2–6]. However, with the implementation of universal hearing screening program, early identification and intervention of the hearing loss become possible [7,8]. For the individuals with profoundly hearing loss, the most common amplification choice is Cochlear Implant. It can facilitate speech and language development by bypassing the non-functional cochlea [9,10]. There are approximately 200,000 cochlear

implant users worldwide, including approximately 80,000 infants and children [11]. In clinical practice, there are many conventional methods to assess the effectiveness of CI use and rehabilitation outcomes such as pure tone audiometry, aided threshold, and speech perception test, etc. However, because the children may be too young to respond to these assessments [12], parental questionnaires have been widely used to evaluate the effectiveness of CI use and rehabilitation outcomes [13–16]. Among these questionnaires (e.g. MAIS, IT-MAIS, MUSS, CAP, SIR, PEACH etc.), the categorical auditory performance (CAP)was developed by the Nottingham group. It is not a closed-set laboratory type test but an assessment for everyday auditory performance. This test used an

⁎ Corresponding author at: Beijing Tongren Hospital, Capital Medical University and Beijing Institute of Otolaryngology, 17 Hougou Lane, Chongnei Street, Dongcheng District, Beijing 100005, China. E-mail address: [email protected] (X. Chen).

https://doi.org/10.1016/j.amjoto.2020.102466 Received 25 February 2020 0196-0709/ © 2020 Elsevier Inc. All rights reserved.

Please cite this article as: Qianqian Guo, et al., Am J Otolaryngol, https://doi.org/10.1016/j.amjoto.2020.102466

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Meanwhile, the effect of age at implantation on the auditory and speech intelligibility scores was also examined.

Table 1 Category of Auditory Performance (CAP). 7 Use of the telephone with the known speaker 6 Understanding conversation without lip-reading with a familiar listener 5 Understanding common phrases without lip-reading 4 Discrimination of speech sounds 3 Identification of environmental sounds 2 Response to speech sounds (e.g. go) 1 Awareness of environmental sounds 0 No awareness of environmental sounds

2. Materials and methods 2.1. Subjects A total of 544 young children (339 boys and 205 girls) participated in this study. They all received cochlear implantation before the age of 36 months (from 6 months to 36 months, mean 20.45) at Beijing Tongren Hospital, Capital Medical University. All subjects were diagnosed with bilateral profound sensorineural hearing loss prelingually by audiological tests like pediatric behavioral audiometry, tympanometry, distortion product otoacoustic emissions (DPOAEs), auditory brainstem response (ABR) and auditory steady-state response (ASSR). None of them had inner ear malformation or other physical and mental diseases. These subjects were divided into 3 groups according to their implant ages, the children who received the CI surgery before 1 year old were in group 1 (n = 109), those who received the CI surgery between 1 and 2 years old were in group 2 (n = 284), and those who received the CI surgery between 2 and 3 years old were in group 3 (n = 151). A summary of the subject characteristics in the three groups, including gender, types of device, age at implantation and other information, are presented in Table 3.

Table 2 Speech Intelligibility Rating (SIR). 5 Connected speech is intelligible to all listeners; the child is understood easily in everyday contexts 4 Connected speech is intelligible to a listener who has 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

eight-point scale (Table 1, Category of performance criteria (CAP)) to evaluate the auditory performance ranging from ‘no awareness of environmental sound’ to the ‘use of the telephone with known users’. It was designed to reflect the real-life auditory condition of children and has been extensively used to assess the auditory ability in CI children [17–21]. The speech intelligibility rating (SIR) was developed in 1989 and was designed to measure the intelligibility of CI children's spontaneous speech. The SIR is composed of five hierarchical ratings (Table 2, Category Speech intelligibility rating criteria (SIR)) describing various degrees of speech intelligibility, with the lowest level for unintelligible speech and the highest level for intelligible to all listeners. It was developed as a time-effective general outcome assessment for speech production in real-life situation [22]. CAP and SIR are simple, easy to learn and implement for clinicians, audiologists, rehabilitation teachers and parents who have no experience about the tests or other assessment tools for CI children. Moreover, the inter observer reliability of these two scales have been formally tested. These two scales cover a wide range of hearing abilities in implanted children [17,19]. They can be applied to a variety of age ranges varying from very young children to adults. The choice of these questionnaires maintains the continuity of hearing evaluation for the young children, hence performing an unbiased assessment. Wu, C.-M did a long-term investigation with CAP and SIR on Mandarin-speaking prelingually deaf children in Taiwan. The results revealed that the score of the CAP changed from 4 after one-year post implantation to 7 after three years post implantation; the score of the SIR changed from 4 after two years post implantation to 5 after three years post implantation. However, not all the subjects reached the highest level of CAP and SIR. Huang's study indicated that SIR in CI children was negatively correlated with the age at implantation but positively correlated with the duration of CI use [23]. The study by Beadle found that after 10 years' follow-up of 30 profoundly deaf children, 87% of the children understood a conversation without lip reading and 60% used the telephone with a familiar speaker, 77% of the subjects were intelligible to an average listener or a listener with little experience of a deaf person's speech [24]. However, so far, there has been no reported data about the development of hearing performance and speech intelligibility in large sample size Mandarin-speaking children with cochlear implants. To fill this gap, the goal of the current study was to use CAP and SIR to examine the development of auditory and speech intelligibility in a large number (544) of CI children up to 5 years post implantation.

2.2. Outcome measures The categorical auditory performance (CAP) was used to assess auditory abilities. It is a nonlinear, hierarchical scale of auditory perception ranging from 0 to7. The speech intelligibility rating (SIR) was used to assess the speech intelligibility of CI children. It consists of five hierarchical categories ranging from 0 to 5 [25]. The auditory and speech intelligibility of all participants were evaluated at pre-surgery and at 1, 3, 6, 12, 24, 36, 48, and 60 months post implantation with CI program switched on. The CAP and SIR are parent questionnaires, the questions involve mainly about the child's spontaneous auditory behaviors in their daily living conditions. Trained audiologists engaged in the process with the parents face-to-face. The parents were asked to provide as many examples as possible of their young child's auditory and speech skill related behaviors. A score is assigned based on the parents' responses in detail [26]. 2.3. Statistical analysis ANOVA was conducted to determine the difference between each two test time points in each group for the CAP and SIR, respectively. Two-sided p values ≤.05 were considered to indicate statistical significance in all tests. Table 3 Demographic and clinical characteristics of the three groups' children. Items

Group 1 (n = 109)

Group 2 (n = 284)

Group 3 (n = 151)

Type of implants Nucleus (n) 25 Medel (n) 52 Clarion (n) 32

122 108 54

38 89 24

Gender Male (n) Female (n)

176 108

95 56

18.37 ± 3.41

30.11 ± 3.43

69 40

Age at implantation (months) Mean ± SE 9.99 ± 1.61

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no significant difference was found between each two intervals before 6 months post implantation (P > 0.05), but between 6 months till 36 months, there was significant difference between each two test intervals (P ≤ 0.05), except 6 months and 12 months, 24 months and 36 months. In group 2, no significant difference was found between presurgery and 1, 3 months post-implantation, 1 and 3 months, 24 and 36 months, 48 and 60 months after switch-on but all other interval contrasts were significantly different. In group 3, the scores of the SIR were significantly different except for the intervals between pre-operation and 1 months after implantation, 1 and 3 months, 3 and 6 months, 24 and 36 months, 48- and 60-months post-surgery. These results suggested that the mean scores of speech intelligibility improved as the hearing ages increased. In addition, the SIR score improved quickly before 24 months post-implantation, especially between 12 and 24 months, and then grew slowly and steadily till 60 months post implantation. 3.2. The differences among the three groups at each test time As shown in Fig. 1, all the three groups showed increased CAP scores as the time increased post implantation. The independent-sample t-test between each two groups for the same test time (results summarized in Table 10) showed that the mean scores of the CAP were not significantly different between group 1 and group 2 at any test points (p > 0.05). Significant difference was found between group 2 and group 3 at pre-surgery and 1, 3 months post-implantation surgery (P ≤ 0.05) and between group 1 and group 3 at pre-surgery and 3, 12 months postsurgery (P ≤ 0.05). As shown in Fig. 2 for SIR scores, the greatest improvement occurred between 12 and 24 months post implantation for group 1, and between 6 and 24 months post implantation for group 2 and 3. The independent - sample t-test (results summarized in Table 11) revealed that the mean scores of SIR were not significantly different between group 1 and 2 at any test session except for 12 months (P ≤ 0.05) postimplantation. Significant difference was found between group 2 and 3 at 1, 3 and 12 months post-implantation surgery (P ≤ 0.05), and between group 1 and 3 at 3, 12 months post-surgery (P ≤ 0.05).

Fig. 1. The development of CAP and speech intelligibility in different groups as the hearing ages increased after long periods of follow-up.

3. Results 3.1. Within group analysis of CAP and SIR over time Fig. 1 shows the scores of auditory performances at different test intervals. The statistical results between each two test intervals in different groups were shown in Tables 4–6. In group 1, before 24 months post implantation, the scores of the CAP were significantly different between each two test intervals (P ≤ 0.05), except for 6 months and 12 months, but between 24 months and 60 months post-implantation, there was not significant difference between each two intervals (P > 0.05). In group 2, before 36 months post implantation, the scores of the CAP were significantly different between each two test intervals (P ≤ 0.05), except for 24 months and 36 months. No significant difference was found between any two intervals after 36 months post implantation. In group 3, the pattern was the same as group 1, but the significant difference was not found between 3 months and 6 months (P > 0.05). These results suggested that the auditory performances improved as the hearing ages increased, meanwhile, the CI children's auditory performance developed rapidly before 24 months post-implantation. Fig. 2 shows the development of speech intelligibility at different test intervals for each group. The statistical results between each two test intervals in different groups were shown in Tables 7–9. In group 1,

3.3. The changes of CAP and SIR in different groups as the physical ages grew Figs. 3 and 4 show the development of CAP and SIR in different groups based on the physical ages. From the figures, we could see that as the physical ages increased, the scores of CAP and SIR also increased, and the three groups of different implant age children had the same development strategy. However, at the same physical age, the children in group 1 acquired higher scores than the other two groups, similarly, the children in group 2 acquired higher scores than group 3. A linear regression was used to analyze the relationship between the CAP scores and physical ages in different group, the statistical test of regression equation was performed by ANOVA, so the regression

Table 4 Statistical differences at any two intervals during the 5-year follow-up based on the mean scores of CAP in group 1. Test intervals (months)

Pre-0

Post -1

Post-3

Post-6

Post-12

Post-24

Post-36

Post-48

1 3 6 12 24 36 48 60

0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000

– 0.000 0.000 0.000 0.000 0.000 0.000 0.000

– 0.000 0.000 0.000 0.000 0.000 0.000

– 0.122 0.000 0.000 0.000 0.000

– 0.000 0.000 0.000 0.000

– 1.000 0.180 0.054

– 1.000 1.000

– 1.000

Note: “pre” means pre-surgery, “post” means post-surgery. Bold and italics indicates significant difference and non-significant difference of the intervals. 3

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Table 5 Statistical differences at any two intervals during the 5-year follow-up based on the mean scores of CAP in group 2. Test intervals (months)

Pre-0

Post -1

Post-3

Post-6

Post-12

Post-24

Post-36

Post-48

1 3 6 12 24 36 48 60

0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000

– 0.000 0.000 0.000 0.000 0.000 0.000 0.000

– 0.000 0.000 0.000 0.000 0.000 0.000

– 0.000 0.000 0.000 0.000 0.000

– 0.000 0.000 0.000 0.000

– 0.104 0.000 0.000

– 1.000 0.250

– 1.000

Bold and italics indicates significant difference and non-significant difference of the intervals.

equation in group 1 was obtained, the scores of CAP = 0.22 + 0.12*physical age, the linear regression equation in group 2 was the scores of CAP = 0.59 + 0.11*physical age, the linear regression equation in group 3 was the scores of CAP = −1.5 + 0.11*physical age. And also, a linear regression equation analyzes the relationship between the SIR scores and physical ages in different group could be obtained, the regression equation in group 1 was obtained, the scores of SIR = 0.30 + 0.07*physical age, the linear regression equation in group 2 was the scores of SIR = −0.02 + 0.07*physical age, the linear regression equation in group 3 was the scores of SIR = −0.86 + 0.07*physical age. 4. Discussion The main goal of pediatric cochlear implantation is to help children partially restore hearing which promotes the development of speech and language and acquisition of communication skills at an early age. The present study was carried out to track the development of auditory performance and speech intelligibility and to evaluate the effects of age at implantation on the auditory and speech abilities in pediatric CI users. In particular, CAP and SIR were selected to assess the auditory and speech abilities of the CI children because CAP has been widely used to evaluate the general auditory performance of children in their daily life and SIR measures the progress of speech production from the occurrence of first word to the establishment of connected speech. As shown in Fig. 1, the CAP scores in all three groups increased with the length of CI use increased. More importantly, the CAP performance improved to a greater extent between 0 and 24 months than between 24 and 60 months post implantation. For all the subjects combined, the score of the CAP for 78% (424/544) of the subjects were 0 pre-implantation, which suggested that most of them were not aware of any environmental sounds. After 24 months of device use, the median score of the CAP reached 6. At the 36 months after the surgery, the median CAP performance reached the highest score 7, which means that they could communicate with the known speaker use of the telephone. This observation reflected that the development of auditory abilities in the CI children mainly occurred in the first two years after implantation. However, some advanced hearing abilities need more time to develop,

Fig. 2. The development of SIR in different groups as the hearing ages increased after long periods of follow-up.

so continuous but steady improvement of CAP scores can still be observed after 24 months. As shown in Fig. 2, all three groups demonstrated increased SIR scores as the length of device use increased. However, different from CAP scores that showed quick improvement in the first 12 months, the SIR scores showed relatively steady improvement in the first 12 months and a dramatic improvement between 12 and 24 months. Approximately 95% (517/544) of the CI children scored 1 for SIR pre-implantation, which represented that most participants had unintelligible speech and unrecognizable words. They used gesture as the most common communication method. The median score of the SIR was 2 at

Table 6 Statistical differences at any two intervals during the 5-year follow-up based on the mean scores of CAP in group 3. Test intervals (months)

Pre-0

Post -1

Post-3

Post-6

Post-12

Post-24

Post-36

Post-48

1 3 6 12 24 36 48 60

0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000

– 0.000 0.000 0.000 0.000 0.000 0.000 0.000

– 0.482 0.000 0.000 0.000 0.000 0.000

– 0.000 0.000 0.000 0.000 0.000

– 0.000 0.000 0.000 0.000

– 1.000 0.095 0.061

– 1.000 1.000

– 1.000

Bold and italics indicates significant difference and non-significant difference of the intervals.

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Table 7 Statistical differences at any two intervals during the 5-year follow-up based on the mean scores of SIR in group 1. Test intervals (months)

Pre-0

Post -1

Post-3

Post-6

Post-12

Post-24

Post-36

Post-48

1 3 6 12 24 36 48 60

1.000 1.000 0.349 0.000 0.000 0.000 0.000 0.000

– 1.000 0.058 0.000 0.000 0.000 0.000 0.000

– 1.000 0.019 0.000 0.000 0.000 0.000

– 1.000 0.000 0.000 0.000 0.000

– 0.000 0.000 0.000 0.000

– 1.000 0.030 0.027

– 1.000 0.922

– 1.000

Bold and italics indicates significant difference and non-significant difference of the intervals. Table 8 Statistical differences at any two intervals during the 5-year follow-up based on the mean scores of SIR in group 2. Test intervals (months)

Pre-0

Post -1

Post-3

Post-6

Post-12

Post-24

Post-36

Post-48

1 3 6 12 24 36 48 60

1.000 0.249 0.000 0.000 0.000 0.000 0.000 0.000

– 0.520 0.000 0.000 0.000 0.000 0.000 0.000

– 0.011 0.000 0.000 0.000 0.000 0.000

– 0.000 0.000 0.000 0.000 0.000

– 0.000 0.000 0.000 0.000

– 0.106 0.000 0.000

– 0.000 0.000

– 1.000

Bold and italics indicates significant difference and non-significant difference of the intervals. Table 9 Statistical differences at any two intervals during the 5-year follow-up based on the mean scores of SIR in group 3. Test intervals (months)

Pre-0

Post -1

Post-3

Post-6

Post-12

Post-24

Post-36

Post-48

1 3 6 12 24 36 48 60

1.000 0.046 0.000 0.000 0.000 0.000 0.000 0.000

– 0.155 0.000 0.000 0.000 0.000 0.000 0.000

– 1.000 0.000 0.000 0.000 0.000 0.000

– 0.000 0.000 0.000 0.000 0.000

– 0.000 0.000 0.000 0.000

– 0.671 0.001 0.000

– 1.000 0.032

– 1.000

Bold and italics indicates significant difference and non-significant difference of the intervals. Table 10 The differences of CAP in different groups at the same test interval. Test groups

1 2 3

Pre-0

Post -1

Post-3

Post-6

Post-12

Post-24

Post-36

Post-48

Post 60

123

123

123

123

123

123

123

123

123

- - 0.003 1.000 - - 0.000 -

- - 0.229 1.000 - - 0.007 -

- - 0.050 1.000 - - 0.025 -

- - 1.000 1.000 - - 0.468 -

- - 0.037 1.000 - - 0.158 -

- - 1.000 1.000 - - 1.000 -

- - 1.000 1.000 - - 1.000 -

- - 1.000 1.000 - - 0.904 -

- - 0.587 1.000 - - 0.618 -

Note: “pre” means pre-surgery, “post” means post-surgery. Bold and italics indicates significant difference and non-significant difference of the intervals. Table 11 The differences of SIR in different groups at the same test interval. Test groups

1 2 3

Pre-0

Post -1

Post-3

Post-6

Post-12

Post-24

Post-36

Post-48

Post 60

123

123

123

123

123

123

123

123

123

- - 1.000 0.546 - - 0.069 -

- - 0.057 1.000 - - 0.027 -

- - 0.020 1.000 - - 0.010 -

- - 0.611 1.000 - - 0.550 -

- - 0.000 0.006 - - 0.029 -

- - 1.000 1.000 - - 1.000 -

- - 1.000 1.000 - - 0.973 -

- - 1.000 1.000 - - 1.000 -

- - 1.000 1.000 - - 1.000 -

Bold and italics indicates significant difference and non-significant difference of the intervals.

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two years post implantation and 5 after three years post implantation [24]. Our results were similar to those reported in Allen and Wu but different from Calmels'. Regarding the difference among the three groups, the CI children with different age at implantation showed similar development patterns of CAP and SIR scores with varying length of implant use. Meanwhile, group difference at certain time points was yielded. In particular, group 3 showed significantly higher CAP scores than group 1 and 2 at presurgery and 3 months post-surgery. Meanwhile, group 3 showed significantly higher SIR scores than group 1 at 3- and 12-months post implantation. Group 3 also showed significantly higher SIR scores than group 2 at 1, 3- and 12-months post-implantation surgery. We speculate that the significantly higher scores in the children with older age at implantation than those with younger age at implantation could be partially explained by the more advanced cognitive abilities in the older children. With the same length of device use during the first two years post implantation, the older children might benefit more from the restoration of auditory sensation. As the length of implant use continued increasing, the younger children caught up and showed similar performance to the older children. Many studies have found that earlier implantation leads to better language outcomes [28–33], indicating that there was a sensitive period for central auditory system and spoken language development at a younger age. If the auditory system is deprived of sound input during this sensitive period, the central auditory will replaced by another sensory cortex. Therefore, early implantation is necessary to allow normal organization of auditory pathways in congenitally deaf children. In the present study, although the age at implantation played a considerably smaller role in the improvement of hearing and speech abilities, the children with early age implantation still leads to better language outcomes. In sum, results from the present study suggested that the prelingually deafened children with CIs showed a long-term development of their auditory performance and speech intelligibility. Meanwhile, earlier implantation benefits the children with CIs to a greater extent. Although CAP and SIR are simple and easy to manage, they only provide a subjective evaluation of overall categorical performance of CI children's auditory and speech abilities. For future study, objective assessment tools should be used to evaluate the auditory and speech abilities in children with CIs.

Fig. 3. The development of CAP in different groups based on the physical ages.

Funding The project was supported by the capital citizen health program to foster from Beijing Municipal Science and 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). Fig. 4. The development of SIR in different groups based on the physical ages.

Declaration of competing interest

12 months, 3 at 24 months post-implantation, and 5 at 60 months after the surgery. The different development trajectories between CAP and SIR suggested that the development of the speech ability might be slower than the development of the auditory ability. We speculate that the delayed development of speech ability relative to auditory ability is because the acquisition of language requires intensive auditory input as the trigger. Calmels et al. found that median SIR score was 1 at three months post implantation, 2 at one-year post implantation and 3 at two to five years post-implantation. Their subjects did not achieve the highest score of 5 even after five years of implant use [27]. In Allen's research, their subjects scored 3 after three years of CI use, 4 at five years post implantation [22]. Wu's results showed that the children scored 4 after

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