Simultaneous Bilateral Cochlear Implantation in Very Young Children Improves Adaptability and Social Skills: A Prospective Cohort Study

Abstract

Objectives: 

To investigate the value of using the Gesell Development Diagnosis Scale (GDDS) to predict developmental outcomes in very young children who undergo simultaneous bilateral cochlear implantation.

Design: 

In this prospective cohort study, a repeated-measures investigation was conducted in a tertiary referral hospital. A total of 62 children receiving simultaneous bilateral cochlear implantations were enrolled from April 2017 to August 2018. They were divided into 2 groups depending on the operative age: “Infants” group (6 to 12 months, N = 38) or “Children” group (12 to 36 months, N = 24). Data on the surgical outcomes, auditory development, speech production, and developmental indicators were collected until 2 years after the initial fitting. The primary outcome measure was the GDDS, a neuropsychological development examination. Secondary outcomes included the following: complication rate, aided pure-tone average, Infant-Toddler Meaningful Auditory Integration Scale, Categories of Auditory Performance-II, Meaningful Use of Speech Scale, Speech Intelligibility Rating, and the LittlEARS Auditory Questionnaire.

Results: 

The mean ages at implantation in infants and children groups were 9.2 ± 1.17 and 16.6 ± 3.60 months, respectively. Significant differences were found in the social skills (p = 0.001) and adaptability (p = 0.031) domains of GDDS. The younger the age of bilateral cochlear implants surgery, the higher developmental quotient of language, social skills, and adaptability the child could achieve after 2 years. The complication rates in the infants and children groups were 0% versus 2.1% (p = 0.57). There was no surgical complication in the infants group. In the children group, 1 case with enlarged vestibular aqueduct and Mondini malformation had a receiver-implant misplacement on the right side (2%, 1/48). In the two groups, auditory performance and speech production had improved similarly. In the infants group, social skills developmental quotient at baseline had a significant positive relationship with Meaningful Use of Speech Scale after 2 years.

Conclusions: 

Simultaneous bilateral cochlear implantation in younger children improves adaptability and social skills. GDDS is a sensitive tool of evaluating short-term effect of bilateral cochlear implants in neuropsychological development and constitutes a reliable predictor of speech production for the very younger pediatric cochlear implant users.

INTRODUCTION

Universal newborn hearing screening (UNHS) has been in place in many countries and indicates the incidence of congenital hearing loss to be 0.1 to 0.3% (^{Mehl & Thomson 2002; Morton & Nance 2006}). As a result of the UNHS, diagnosis before three months of age and intervention before 6 months can be achieved for pediatric hearing loss (^{Expert Group on Universal Newborns Hearing Screening of the National et al. 2018}). To maximize the opportunity for spoken language, cochlear implant (CI) surgery is the most effective method of hearing rehabilitation for children with severe to profound sensorineural hearing loss (SNHL) (^{Brookhouser et al. 1990; Iseli & Buchman 2015}). The Food and Drug Administration candidacy criteria have expanded to include profound SNHL in children as young as 9 months old in 2020 (^{FDA (U.S. Food & Drug Administration) 2020}). In France, CI surgery is proposed before 12 months of age for children with congenital bilateral profound hearing loss (^{Simon et al. 2019}). However, CI surgery is recommended only for children older than 12 months in British and Chinese guidelines (^{Editorial Board of Chinese Journal of Otorhinolaryngology Head and Neck Surgery et al. 2014; NICE (National Institute for Health and Care Excellence) 2019}). The Australian guideline has removed the minimum age limit for children and recommended that cochlear implantation should proceed as early as possible once audiological information is verified and consistent (^{Leigh et al. 2016}).

There have already been many studies focusing on the safety and outcomes of early intervention for pediatric hearing loss. Application of CIs in children as young as 12 months began in the early 21st century to minimize the duration of auditory deprivation (^{Govaerts et al. 2002; Hammes et al. 2002; Miyamoto et al. 2003; Colletti et al. 2005}). In the literature, although most studies were retrospective, CI surgery risks in very young children were similar to those expected with older pediatric patients with regard to anesthetic and surgical course, and device-related complications (^{Valencia et al. 2008; Roland et al. 2009; Colletti et al. 2012; Holman et al. 2013; Hoff et al. 2019; Karltorp et al. 2020}). CIs in children younger than 6 or 9 months were shown to achieve better auditory and language outcomes than children older than 12 months without a higher rate of complications (^{Colletti et al. 2012; Karltorp et al. 2020}). In contrast, ^{Franchella et al. (2018}) found that undergoing surgery before 2 years of age achieved a satisfactory audiometric performance, with no particular benefits from surgery performed before 12 months of age.

In 1998, the first pediatric patient to receive bilateral CIs underwent cochlear implantation on their second ear after receiving their first CI in 1996 at 2 years of age. From then on, there were thousands of children across the world who would have benefitted from the bilateral CIs (BiCIs). For children with severe to profound SNHL, the benefit of binaural hearing restoration is well documented. Considering the importance of bilateral cochlear implantation, the BiCIs surgery option should become the gold standard in treating children with severe to profound SNHL. BiCIs improve sound localization, language development, speech perception in noise, and subjective benefits (^{Johnston et al. 2009; Ramsden et al. 2012; Lammers et al. 2014; van Schoonhoven et al. 2013; Kraaijenga et al. 2017; van Zon et al. 2017}). Compared with sequential BiCIs, simultaneous BiCIs promote the development of bilateral auditory pathways in tandem and are less resource consuming for rehabilitation (^{Peters et al. 2010}). A recent study about sequential bilateral cochlear implantation with prolonged time intervals manifested that a significant improvement in the speech recognition scores was observed with the first implanted ear, and much slower progress was observed with the second implanted ear. However, the “poorer” second implanted ear could provide a considerable beneficial effect on the improved speech recognition and health-related quality of life with the bilateral CIs (^{Zhang et al. 2020}). The European Consensus Statement declared in 2012 that an infant or child with an unambiguous CI candidacy should receive BiCIs simultaneously as soon as possible after definitive diagnosis of deafness to permit optimal auditory development (^{Ramsden et al. 2012}).

Despite the large number of studies illustrating the benefits of early cochlear implantation on audiological and speech development, speech evaluation tools are unlikely to be sensitive enough for these very young children. To evaluate short-term outcomes for them, speech assessment such as speech recognition score is challenging. Open-set or closed-set speech recognition tests are not developmentally appropriate for children younger than 12 months of age. Instead, current methods of evaluating short-term speech outcomes for these children include subjective scales such as the Meaningful Use of Speech Scale (MUSS) and Parents’ Evaluation of Aural/oral performance of Children. For long-term outcome tracking, the Mandarin Early Speech Perception (MESP) can be performed as an objective speech assessment for older children (^{Zhong et al. 2017; Zhang et al. 2022}). After 12 months or longer of wearing CIs, MESP can be performed for children 2 to 5 years of age (^{Zheng et al. 2010}).

However, for children with CIs, many studies in the literature have focused on hearing and speech development, but few studies have focused on neuropsychological development. The Gesell Development Diagnosis Scale (GDDS) was developed in 1925 and widely used (^{Gesell 1925}). The GDDS is a classic neuropsychological development examination and widely used in children aged 0 to 60 months, including 5 domains: gross motor, fine motor, adaptability, language, and social skills (^{Jin et al. 2007; You et al. 2019; Wei et al. 2021}). The GDDS was used in a retrospective study of pediatric recipients and the results showed that preoperative developmental levels were related to improvements in auditory perception and speech production by parent-report scales after CI surgery (^{Yang et al. 2017}). Older children who were recipients of CI might face more serious developmental delays. The older children are more serious developmental delay occur, so the CI operation should be finished as early as possible (^{Yang et al. 2017}). Therefore, we hypothesized that the GDDS is a suitable tool to evaluate the neuropsychological development for children younger than 12 months who undergo simultaneous BiCIs.

The objective of the present study was to investigate the value of GDDS in children with simultaneous BiCIs in a group of infants implanted at 6 to 12 months compared with a group implanted at 12 to 36 months. This study is unique in that it prospectively captures a comprehensive group of overall developmental outcome measures including neuropsychological development, auditory outcomes, and speech production. Our results have practical implications for determining the ideal age of CI surgery and appropriate assessment tools for short-term outcomes in very young pediatric recipients.

MATERIALS AND METHODS

Study Design

In this prospective cohort study, a repeated-measures investigation was conducted at Shanghai Ninth People’s Hospital which is affiliated with Shanghai Jiao Tong University School of Medicine (2016-139-T88). There were 90 participants aged 6 to 36 months with profound SNHL who were assessed for inclusion in the study (Fig. 1). A total of 63 participants were implanted by simultaneous BiCIs as part of this study. A 13-month-old boy assigned to the children group was not included in the final analysis because he was diagnosed with autism 10 months after surgery by a pediatrician in another hospital. Finally, 38 participants were included in the “Infants” group aged 6 to 12 months and 24 in the “Children” group aged 12 to 36 months with data of all time points for the participants during the 2-year period of follow-up (Fig. 1). The study protocol was approved by the local institutional review boards. Written informed consent was obtained from each individual’s parents after explaining the details of the study.

Fig. 1.: Participation eligibility criteria flowchart.

All of the participants received simultaneous BiCIs surgery with a standard mastoid-facial recess approach through the round window. The primary outcome was the GDDS, which was examined at 5 time points: T₀ (at initial activation of the CIs), T_0.5y (0.5 year ± 30 days postactivation), T_1y (1 year ± 30 days postactivation), T_1.5y (1.5 years ± 30 days post-activation), and T_2y (2 years ± 30 days postactivation). The secondary outcome measures included the following: operative safety (complication rate, intraoperative bleeding, operation duration), aided pure-tone average (PTA) measured by visual reinforcement audiometry (VRA), three auditory scales including the Infant-Toddler Meaningful Auditory Integration Scale (IT-MAIS), the Categories of Auditory Performance-II (CAP-II), and the LittlEARS Auditory Questionnaire (LEAQ); two speech scales including the MUSS and the Speech Intelligibility Rating (SIR). Aided PTA was performed at 1 year after the initial activation, which was obtained in the sound field using warble tones by VRA. The IT-MAIS, CAP-II, LEAQ, MUSS, and SIR outcomes were examined at 7 time points: T₀, T_1m (1 month ± 7 days), T_3m (3 months ± 14 days), T_0.5y, T_1y, T_1.5y, and T_2y.

Eligibility Criteria of Participants

Inclusion criteria:

• 1. Age: 6 to 36 months.
• 2. Otoscopy: bilateral external auditory canals clear.
• 3. Bilateral profound SNHL diagnosed as follows:
  • Tympanograms: bilateral normal (pressure >−150 daPa; compliance 0.3 to 1.6 cm³).
  • Click-auditory brainstem response: bilateral ≥ 90 dB nHL.
  • Distortion product otoacoustic emission: the value of signal to noise ratio <3 dB at each frequency point for 500, 1000, 2000, 3000, 4000, 6000, and 8000 Hz (Diagnostic measure by Otometrics, Capella, Denmark).
• 4. Normal cochlear anatomy or enlarged vestibular aqueduct confirmed by computed tomography scan and magnetic resonance imaging.
• 5. Term newborns (≥37 weeks) with normal weight (2500 to 4000 g).
• 6. Participants living with their parents and having speech rehabilitation after BiCIs surgery. Each participant received speech rehabilitation in the local rehabilitation organization affiliated to the Disabled Persons’ Federation. The rehabilitation courses were offered by the speech-language pathologists in the form of group and individual lessons which were offered 5 days a week.
• 7. Bilateral hearing aids fitting for at least 3 months and limited benefit.
• 8. The guardian agrees to the child participating in the study, signs the informed consent, and promises to bring the child to our center at each visit.

Exclusion criteria:

1. Global developmental delay defined as a delay in two or more developmental domains of gross/fine motor, speech/language, cognition, and social skills (^{Mithyantha et al. 2017}).
2. Diagnosed with autism during recruitment and follow-up.
3. Participants admitted to the neonatal intensive care unit due to premature birth.
4. White matter disease or demyelinating disease.
5. Other contraindications for surgery under a general anesthetic.
6. Unable to return to participating institute as required.

Cochlear Implantation and Mapping

Implantations were performed by experienced surgeons having over 10 years of experience in cochlear implantation surgery. A standard mastoid-facial recess approach through the round window was used. The “Soft surgery” protocol was followed (^{Jia et al. 2011}). Postoperative cranial x ray was conducted to confirm the placement of the electrodes. Our criteria for good placement were (1) all electrodes were in the inner ear, (2) no misplacement into vestibule, or semicircular canals was observed; (3) no fold-over of array was observed. The duration of surgery, intraoperative bleeding, and complications such as misplacement or failure of implants, wound infection, facial paralysis, and cerebrospinal fluid leakage were recorded. The CI brands comprised Advanced Bionics (USA), Cochlear (Australia), and Med-El (Austria).

Device activation was performed 1 month ± 7 days after surgery using a combination of behavioral procedures and electrically evoked compound action potentials (ECAP) measurements for device setting. The impedance of all electrodes, and ECAPs of particular electrodes were measured at each follow-up point. The stimulation threshold and upper stimulation level of electrodes were determined by ECAP and VRA results to program the CIs. Mapping was carried out by the audiologist who had 15 years of experience. The clinicians communicated frequently with the speech-language pathologists of the rehabilitation organization to ensure the mapping was appropriate for speech development.

Gesell Development Diagnosis Scale

The GDDS assesses the developmental abilities of infants and children at the age of 0 to 60 months including domains of adaptability, fine motor, gross motor, language, and social skills (^{Gesell 1925}). Adaptability refers to the ability of perception objects and the environment, as well as the ability to solve practical problems. Fine motor refers to fine movements such as grasping, pinching and so on. Gross motor refers to sitting, walking, running and other postures. Language refers to the ability of pronunciation, understanding words, and spoken language. Social skills refer to their personal reaction to social culture, reflecting their ability to interact and communicate with people. The GDDS was designed as the primary outcome measure because of its suitable age range and widely used to evaluate the neuropsychological development in children. A developmental quotient (DQ) was calculated using the following formula: (developmental age/actual age) × 100 (^{Gesell 1932; Meinzen-Derr et al. 2017}). The DQ of each domain was calculated. The mean DQ is 100 with 1 standard deviation (SD) of 15 points. DQ ≥85 is regarded as average development. A developmental score between 1 and 2 SD below the average (85 to 70) is regarded as borderline development delay and below 2 SD (<70) as a significant developmental delay (^{Dror et al. 2009}). The GDDS was carried out by experienced clinicians: a technician and a specialist in child health care who had over 5 years of experience working with children with hearing loss. Each measure took about 30 min.

Auditory and Speech Development

Aided PTA was performed in the sound field using warble tones by VRA by calculating the mean hearing threshold levels at 0.5, 1, 2, and 4 kHz. The IT-MAIS is composed of 10 categories assessing three aspects of speech perception: vocalization, attention to sounds, and identification of sounds (^{Chen et al. 2020}). The maximum score is 40 points. The CAP-II scale is a modified version of CAP. The CAP was first established in 1995 and consisted of 8 performance categories (0 to 7) arranged in order of increasing difficulty to measure the daily hearing performance (^{Archbold et al. 1995}). This extended the CAP-II scale which consists of 10 categories (0 to 9) and has given the examiner the ability to fully assess the maximum benefit of CI (^{Al-Shawi et al. 2020}). The LEAQ consists of 35 yes-or-no questions designed for the parents to test the observed receptive, semantic and early expressive language skills of very young children (^{Wang et al. 2013}). The total score was the sum of all “yes” answers. The MUSS comprises 10 categories assessing areas such as: vocal control, use of speech without gestures or signs, and use of communication strategies in daily situations (^{Chen et al. 2020}). The maximum score is 40 points. The SIR scale is used to classify children’s global speech production according to five performance categories arranged (from one to five points) in order (^{Chen et al. 2020}).

Statistical Analysis

SAS version 9.4 (SAS Institute, Cary, NC, USA) was used for statistical analysis. When describing baseline data for the two groups, the classification variables were represented by frequency and the Chi-squared test was used. The continuous variables conforming to normal distributions were represented by means ± SD and the t tests were used. To compare the postoperative outcomes, repeated-measures analysis of variance (ANOVA) and mixed effects model were used and correction was made for multiple comparisons. The ordinal logit model and linear regression were used to explore the results of GDDS. Two-tailed p values <0.05 were considered statistically significant.

RESULTS

Participants and Surgery

All 62 patients failed in UNHS and were diagnosed with bilateral profound SNHL. Before BiCIs surgery, they wore bilateral hearing aids for over 3 months. During the surgery, all of them had full insertions of the electrode arrays via round window approach. The duration of surgery for the infants and children groups was not significantly different (119 ± 13.9 versus 118 ± 15.6 min, respectively; p = 0.72). However, the estimated quantity of bleeding was 6.0 ± 1.53 and 7.2 ± 2.54 mL in infants and children, respectively (p = 0.02), a difference which had no influence on the immediate outcome. There were no perioperative anesthetic complications. There was no surgical complication in the infants group. In the children group, only 1 case with enlarged vestibular aqueduct and Mondini malformation had a complicated outcome (2%, 1/48): a receiver-implant misplacement on the right side in a 13-month-old girl readjusted 3 days later.

GDDS Outcomes

Significant differences were found in the adaptability (Fig. 2A) and social skills (Fig. 2B) domains between the infants and children (p = 0.001 and 0.031 by a repeated-measures ANOVA, respectively). The infants group presented better trends of adaptability and social skills than the children group over time. Thus, the t test was used to compare the DQs between the two groups at each time point. For the adaptability domain, infants had higher DQs than children at 1.5 years (105.9 ± 9.71 versus 97.4 ± 6.98; p < 0.001) and 2 years (102.3 ± 8.11 versus 95.6 ± 7.80, p = 0.002). For the social skills domain, infants had higher DQs than children at 0.5 year (93.71 ± 9.63 versus 88.3 ± 10.38, p = 0.042) and 1 year (92.8 ± 9.30 versus 83.2 ± 8.20; p < 0.001). No significant difference was found in language, gross motor, and fine motor domains (Fig. 2C–E). However, the baseline for language DQs was different between the two groups (p < 0.001; Table 1) because speech developmental delay was nonsynchronous in the different age groups. Repeated-measures ANOVA was used to compare the mean change from baseline and reported no statistically significant difference between infants and children (p = 0.13). Mixed effects models were also applied and came to the same conclusion as the repeated-measures ANOVA: significant differences were found in adaptability and social skills domains between the infants and children groups; no significant difference was found in language, gross motor, and fine motor domains. Results of repeated measures and mixed effects models are listed in Table 2.

TABLE 1. - Patient demographics and preoperative evaluations.

	Infants	Children	p
Demographic
Total	38	24	/
Sex (M/F)	23/15	17/7	0.41
Inner ear (normal/EVA)	32/6	20/4	0.91
Age of implantation (mo)	9.2 ± 1.17 (6.7–11.4)	16.6 ± 3.60 (12.1–25.7)	<0.001
Preoperative auditory and speech scales
IT-MAIS	0.4 ± 1.24	0.7 ± 1.76	0.45
CAP-II	0.1 ± 0.27	0.3 ± 0.53	0.10
MUSS*	0	0	/
SIR†	1	1	/
LEAQ	0.1 ± 0.36	0.5 ± 1.64	0.17
Preoperative Gesell scores
Gross motor	95.0 ± 15.26	102.3 ± 11.89	0.05
Fine motor	95.9 ± 10.19	95.7 ± 13.19	0.93
Adaptability	90.1 ± 11.42	93.5 ± 11.70	0.26
Language	65.1 ± 15.30	45.9 ± 12.88	<0.001
Social skill	93.7 ± 14.23	90.9 ± 11.55	0.41

^*Preoperative MUSS scores of all the patients enrolled were 0.

^†Preoperative SIR scores of all the patients enrolled were 1.

EVA, enlarged vestibular aqueduct; CAP-II, Categories of Auditory Performance-II; IT-MAIS, Infant-Toddler Meaningful Auditory Integration Scale; LEAQ, LittlEARS Auditory Questionnaire; MUSS, Meaningful Use of Speech Scale; SIR, Speech Intelligibility Rating.

TABLE 2. - The GDDS differences in the infant and children groups over time. (Using repeated-measures analysis of variance and mixed effects model separately.)

Domains	Repeated-Measures Analysis of Variance		Mixed Effects Model
	F	p	F	p
Adaptability	5.045	0.001	5.31	0.0010
Social skills	2.870	0.031	3.02	0.0245
Gross motor	1.523	0.208	0.60	0.1854
Fine motor	0.200	0.938	0.19	0.9453
Language	1.478	0.221	1.56	0.1978

GDDS, Gesell Development Diagnosis Scale.

Fig. 2.: The GDDS results in the infant and children groups over time. A–E, The results of adaptability, social skills, language, gross motor, and fine motor DQs over time, respectively. p values of repeated-measures analysis of variance for each scale are indicated below the titles. The areas of normative range and 1 SD below have been presented as dotted lines. CI indicates cochlear implant; DQ, developmental quotient; GDDS, Gesell Development Diagnosis Scale.

The GDDS results were also analyzed considering age as continuous variable instead of dividing into infants and children groups. Relationship of implantation age and GDDS outcomes is shown in Figure 3. For adaptability, social skills and language domains, implantation age had negative relationship with DQs after 2 years (Fig. 3A–C). For gross and fine motors, implantation age had no significant relationship (Fig. 3D, E). In addition, after 2 years of BiCIs use, the number of participants who obtained “Normal” level of each domain obviously increased (DQ ≥85 was regarded as “Normal” according to the clinical diagnostic criteria). A total of 96.8% of the participants reached “Normal” level in adaptability and gross motor domains; 85.5% in social skills and language domains, and 93.5% in fine motor domain (Fig. 4). The proportion of normal participants was compared between T₀ and T_2y points in the five domains. For adaptability, language, and gross motor domains, the proportion of normal participants at T_2y was significantly higher than that of T₀ (p < 0.001, p < 0.001, and p = 0.008, respectively). For social skills and fine motor domains, the proportion of normal participants at two time points presented no significant difference (p = 0.061 and 0.182, respectively). For social skills, 72.6% participants had over 85 DQ before BiCIs surgery, but the percentage decreased to 64.5% after 1 year and returned to 85.5% after 2 years.

Fig. 3.: Relationship of implantation age and GDDS outcomes after 2 yrs. A–E, The linear correlation results of implantation age and adaptability, social skills, language, gross motor, and fine motor DQs, respectively. The regression equation of age and GDDS results at T _2y as well as its p value are indicated below the titles. DQ indicates developmental quotient; GDDS, Gesell Development Diagnosis Scale.

Fig. 4.: The three grades of GDDS results before BiCIs surgery (T ₀), after 1 (T _1y) and 2 years (T _2y) in all 62 participants. The 3 grades of GDDS results are “Normal” (DQ ≥85), “Borderline” (70 ≤ DQ < 85), and “Delay” (DQ < 70), respectively. The number of “Normal” participants and their percentages are indicated within the column. BiCIs indicates bilateral cochlear implants; DQ, developmental quotient; GDDS, Gesell Development Diagnosis Scale.

Auditory and Speech Outcomes

The aided PTA after 1 year in infants was 32.5 ± 1.09 dB HL, which was not different compared with children (31.6 ± 0.97 dB HL; P = 0.55). The results of IT-MAIS, CAP-II, LEAQ, MUSS, and SIR presented no significant differences between infants and children using a repeated-measures ANOVA (Fig. 5). The baselines for these scales also showed no significant differences (Table 1). At the end of the 2-year follow-up, the results of IT-MAIS, CAP-II, LEAQ, SIR, and MUSS of the infants group were 39.9 ± 0.49, 6.9 ± 1.07, 34.7 ± 0.97, 3.6 ± 0.97, and 29.1 ± 6.77, respectively. The results of the children group were 39.8 ± 0.57, 7.3 ± 1.24, 34.7 ± 0.92, 3.8 ± 1.15, and 30.9 ± 9.44, respectively. There were no significant differences between two groups.

Fig. 5.: Auditory and speech development in the infants and children groups over time. A–E, The results for the IT-MAIS, CAP-II, LEAQ, MUSS, and SIR over time. p values of repeated-measures analysis of variance for each scale are indicated below the titles. CAP-II indicates Categories of Auditory Performance-II; IT-MAIS, Infant-Toddler Meaningful Auditory Integration Scale; LEAQ, LittlEARS Auditory Questionnaire; MUSS, Meaningful Use of Speech Scale; SIR, Speech Intelligibility Rating.

Relationship of Baseline GDDS and Auditory/Speech Outcomes

The effects of GDDS baseline DQs on CAP-II and SIR 2 years after the initial activation were analyzed by the ordinal logistic regression because CAP-II and SIR are performance categories (ranked ordinal data). The group information was taken into consideration as a factor in the logistic regression. The results showed no relationship between them (Table 3).

TABLE 3. - Effects of baseline GDDS results on CAP-II and SIR after 2 yr (ordinal logistic regression results adjusted for group).

Dependent Variable	Independent Variable	Wald Chi-Square	p Value	OR	95% CI
CAP-II (T 2y)	Gross motor (T 0)	0.28	0.60	0.99	0.96–1.02
	Fine motor (T 0)	1.03	0.31	1.02	0.98–1.06
	Adaptability (T 0)	0.53	0.48	1.02	0.98–1.06
	Language (T 0)	0.05	0.82	1.00	0.97–1.03
	Social skill (T 0)	3.00	0.08	1.03	1.00–1.07
SIR (T 2y)	Gross motor (T 0)	1.53	0.22	0.98	0.95–1.01
	Fine motor (T 0)	1.40	0.24	1.03	0.98–1.07
	Adaptability (T 0)	0.37	0.54	1.01	0.97–1.05
	Language (T 0)	0.08	0.78	1.00	0.96–1.03
	Social skill (T 0)	1.07	0.31	1.02	0.98–1.06

CAP-II, Categories of Auditory Performance-II; CI, confidence interval; GDDS, Gesell Development Diagnosis Scale; OR, odds ratio; SIR, Speech Intelligibility Rating.

The effects of GDDS baseline DQs on MUSS/IT-MAIS/LEAQ 2 years after the initial activation were analyzed by linear regression because they are quantitative data. The results for GDDS on MUSS are shown in Figure 6. In infants, social skills DQ had a positive relationship with MUSS outcomes: Y = 10.78 + 0.20X, p = 0.011 (Fig. 6B). In children, language DQ had a positive relationship with MUSS outcomes: Y = 16.65 + 0.31X, p = 0.04 (Fig. 6C). The results indicated that the higher the baseline social skills DQs, the better the speech outcomes after 2 years in infants; the better the preoperative linguistic basis, the better the speech outcomes after 2 years in children. Unexpectedly, gross motor DQ at baseline had a negative relationship with MUSS scores in children: Y = 66.18–0.35X, p = 0.04 (Fig. 6D). A similar result was found for the relationship between baseline gross motor DQ and LEAQ outcomes in children: Y = 38.44–0.04X, p = 0.02 (Table 4).

TABLE 4. - Effects of baseline GDDS results on IT-MAIS and LEAQ after 2 yr (linear regression analysis).

	Independent Variable (X)	Gross Motor (T 0)	Fine Motor (T 0)	Adaptability (T 0)	Language (T 0)	Social Skill (T 0)
Dependent variable (Y1) = IT-MAIS (T 2y)	All	Y1 = 39.86 + 0.0002X (p = 0.96)	Y1 = 40.12 − 0.003X (p = 0.68)	Y1 = 40.09 − 0.002X (p = 0.70)	Y1 = 39.78 + 0.002X (p = 0.63)	Y1 =39.92 − 0.0004X (p = 0.94)
	Infants	Y1 = 39.58 + 0.004X (p = 0.50)	Y1 = 39.88 − 0.0004X (p = 0.96)	Y1 = 39.61 + 0.003X (p = 0.63)	Y1 = 40.26 − 0.005X (p = 0.32)	Y1 = 39.66 + 0.003X (p = 0.63)
	Children	Y1 = 40.43 − 0.006X (p = 0.57)	Y1 = 40.34−0.005X (p = 0.56)	Y1 = 40.72 − 0.01X (p = 0.36)	Y1 = 39.19 + 0.01X (p = 0.13)	Y1 = 40.68 − 0.009X (p = 0.37)
Dependent variable (Y2) = LEAQ (T 2y)	All	Y2 = 34.98 − 0.003X (p = 0.70)	Y2 = 35.13 − 0.005X (p = 0.65)	Y2 = 33.69 + 0.01X (p = 0.31)	Y2 = 34.28 + 0.007X (p = 0.36)	Y2 = 33.91 + 0.008X (p = 0.37)
	Infants	Y2 = 33.79 + 0.009X (p = 0.39)	Y2 = 34.85 − 0.002X (p = 0.90)	Y2 = 32.64 + 0.02X (p = 0.11)	Y2 = 34.47 + 0.003X (p = 0.78)	Y2 = 32.72 + 0.02X (p = 0.06)
	Children	Y2 = 38.44 − 0.04X (p = 0.02)	Y2 = 35.40 − 0.008X (p = 0.61)	Y2 = 35.32 − 0.007X (p = 0.68)	Y2 = 33.53 + 0.025X (p = 0.10)	Y2 = 36.66 − 0.02X (p = 0.19)

GDDS, Gesell Development Diagnosis Scale; IT-MAIS, Infant-Toddler Meaningful Auditory Integration Scale; LEAQ, LittlEARS Auditory Questionnaire.

Fig. 6.: Linear regression of GDDS results before BiCIs surgery (T ₀) and MUSS scores after 2 yr (T _2y) in infants and children groups. A–E, The results for adaptability, social skills, language, gross motor, and fine motor. The baseline social skills DQ in the infants group and language DQ in the children group had positive relationship with MUSS scores, respectively. BiCIs indicates bilateral cochlear implants; DQ, developmental quotient; GDDS, Gesell Development Diagnosis Scale; MUSS, Meaningful Use of Speech Scale.

DISCUSSION

In this study, we present the results of overall developmental benefits in very young children with BiCIs to evaluate the value of the GDDS. As a result, the GDDS is proven to be sensitive material for short-term evaluation in the very young pediatric CIs users. The infants group presented significantly better social skills and adaptability DQs than the children group. In addition, the younger the child had BiCIs, the higher DQ of language, social skills, and adaptability he or she could achieve after 2 years.

The strength of this study included using a metrics sensitive enough for reflecting the short-term effectiveness of BiCIs in the very young pediatric users aged 6 to 12 months. Evaluation materials for short-term outcomes mainly consisted of subjective hearing and speech questionnaire for parents before (^{Chen et al. 2020}). However, besides hearing and speech development, cognitive function and other abilities are drawing increasing attention in recent years (^{Park et al. 2015; Kral et al. 2016}). The GDDS is a classic diagnostic development scale. The GDDS is clinician-administered on the spot, which accurately reflects a child’s level of neuropsychological development. It was carried out by experienced clinicians in this study. The GDDS was proven to be sensitive material for short-term evaluation in the very young pediatric users. Particularly there are not many measures (aside from speech discrimination testing such as visual habituation, preferential looking, and visual reinforcement infant speech discrimination) that evaluate speech perception before word onset for the pre-lexical children.

The infants group presented significantly better social skills and adaptability DQs than the children group (Fig. 2). These results indicate that early BiCIs surgery can provide neurobehavioral benefits. Whether it is related to improved central auditory system remains unknown and needs further objective evidence such as functional imaging measures and electroencephalograph analysis. Interestingly, for social skills, the proportion of “Normal” ones decreased to 64.5% after 1 year and returned to 85.5% after 2 years. It might be related to surgical operation and cochlear devices which partly resulted in “social isolation” to the recipients for the short term.

On the other hand, preoperative GDDS results may be reliable predictors of hearing and speech outcomes after 2 years. At the end of follow-up in this study, greater differences were found in speech production outcomes within groups, although none presented differences between infants and children groups (Fig. 5). Therefore, we studied predictive indicators of speech outcomes. A previous retrospective study focused on the value of GDDS in predicting CI outcomes and found that preoperative adaptability DQ had a predictive effect on CAP and SIR outcomes (^{Yang et al. 2017}). In our study, baseline social skills in infants had a positive relationship with MUSS scores 2 years after BiCIs surgery (Fig. 6B). This result suggested that training the ability to communicate with people could improve speech outcomes for infants. However, in children group, language DQ at baseline had a significant positive relationship with MUSS outcomes (Fig. 6C), which indicated the importance of preoperative language level for pediatric CI users older than 12 months. Unexpectedly, gross motor DQ at baseline had a negative relationship with MUSS and LEAQ scores in children group (Fig. 6D and Table 4). From the point of view of overall development, children with profound SNHL tend to communicate with others and explore the world by movements and body language, especially for children older than 12 months. The dissociation of DQs in deaf children has been found in previous studies (^{Rine et al. 2000; Horn et al. 2006; Fiorillo et al. 2017; Hall 2017; Meinzen-Derr et al. 2017; Swanepoel et al. 2020; Kamel et al. 2021; Tsou et al. 2021}). In this study, participants in the children group had relatively high gross motor DQ at baseline (102.3 ± 11.89), although not significantly different from the infants group, p = 0.053 (Table 1). This may have contributed to the negative relationship between gross motor DQ and CI outcomes.

The safety of simultaneous BiCIs surgery in infants aged 6 to 12 months was supported by the current study’s results. It is worth noting that a specialist pediatric CI surgery team of experts, including an audiologist, pediatrician, ear surgeon, and anesthesiologist is critical to achieve proper diagnosis and safe treatment in these children. The speech-language pathologists from local rehabilitation organizations were involved in speech rehabilitation after the first mapping of CIs. Many centers worldwide have reached this broad consensus on CI surgery in infants younger than 12 months. In addition, this study raised the attention of neuropsychological development for pediatric CIs users.

The limitation of this study is the existence of confounding factors which might have influenced the CI outcomes, such as the levels of household income and parental education, and the rehabilitation training after BiCIs surgery. Each participant received speech rehabilitation offered by different speech-language pathologists in local organizations affiliated to the Disabled Persons’ Federation. However, the frequency of each child’s speech training was 5 days a week. These participants received speech rehabilitation by means of auditory-verbal therapy which was characterized by conversational interaction and deep parental involvement. All the speech-language pathologists obtained the qualification certificate after unified training. The audiologist who performed CIs mapping in this study communicated frequently with the speech-language pathologists to ensure the mapping was appropriate for speech development.

In conclusion, simultaneous bilateral cochlear implantation in younger children improves adaptability and social skills. The GDDS is a sensitive tool of evaluating short-term effect which provides a standardized measure to assess progress in pre-lexical children and constitutes a reliable predictor of speech outcomes for the very young pediatric CI users.

ACKNOWLEDGMENTS

This study was supported by grants from Clinical Research Plan of SHDC (16CR1005A to H. W. and SHDC2020CR1044B to H. W.); Shanghai Jiaotong University School of Medicine Multi-centre Clinical Research Programme (DLY201511 to H. W.); Shanghai Rising Stars of Medical Talent Youth Development Program (Youth Medical Talents – Specialist Program to Y. C.) and Foundation of Shanghai Municipal Health Commission (201840052 to J. L.).