Preoperative variables affecting outcome of cochlear implant

Abstract

Background

Cochlear implants made a great impact in the management of severe-to-profound hearing loss in both children and adults. Its greatest impact is in helping children born with a profound hearing loss and implanted early to attend mainstream education and using spoken language to communicate. However, the final outcome in pediatric implantation is not predictable as there are large number of factors which will affect the outcome of cochlear implantation. Studying these determinants increases the ability of clinicians to offer educated preoperative prognosis and might potentially allow for manipulation of variables in an attempt to achieve the best possible outcome.

Objective

The aim of this study was to assess the preoperative factors affecting the audiological, speech, and language outcomes achieved by the recipients of cochlear implants.

Methodology

A total of 39 children with severe-to-profound sensory neural hearing loss were implanted with cochlear implants. Children had received their implants before age of 5 years. Tests of receptive, expressive language quotient, aided cortical auditory-evoked potential using speech stimulus, aided free field audiometry, and aided speech reception thresholds were administered. Characteristics of the child and the family (age before implant and duration of implant use, cause of hearing loss, preimplant use of hearing aids and language therapy, and sociodemographic characteristics of their families) were the preoperative variables. These variables were considered predictors of audiological and language outcomes achieved by children and were determined using statistical analysis by univariate and multivariate analyses.

Results

Age of the studied children at time of cochlear implantation was statistically significant predictor for CI outcome as regard receptive language quotient and also for N1 latency. Hearing age of the studied children was a statistically significant predictor for CI outcome as regards P1 latency.

Conclusion

Based on our findings, two most important factors affecting outcome of cochlear implantation were the age at implantation and the hearing age. Other factors were important but did not affect the outcome significantly.

Background

Cochlear implants (CIs) have enabled hundreds of thousands of individuals worldwide to restore their hearing. Even though the majority of those will benefit after implantation, it is still challenging to estimate exactly how much a person’s hearing will improve. The end result in pediatric implantation is still not totally predicted because there are numerous factors that, either individually or collectively, will determine how well the cochlear implant works [1].

Factors that are known to influence outcomes include three main categories: patient characteristics, the patient’s environment, and the baseline status of the auditory system.

Patient characteristics including age at implantation, duration of auditory deprivation, relationship with common causes of SNHL, and patient’s environment include education level of parents and rural v/s urban population [2]. The age in which the children are implanted is the most essential and often noted factor that affects abilities for auditory-only communication [3].

By classifying these factors, practitioners are able to provide informed preoperative prognosis and may be willing to manipulate factors in an effort to get the best results [4]. Recent studies on cochlear implantation in pediatrics have primarily concentrated on documenting language development among these individuals as well as identifying potential influencing variables that may have an impact on the results.

Poor performance has been linked to a number of known factors, including implantation at a late age, minimal nerve survival, inappropriate fitting, insufficient cognitive ability, social and educational circumstances that stress interpersonal interaction, and little parental support [5].

The vast variety of speech perception qualities seen by cochlear implant users may be partially due to individual variances in their capacity for central auditory processing. Assessing cortical potentials that represent auditory discrimination in particular may provide an understanding of the primary neural mechanisms that underlies speech perception [5].

Cortical auditory-evoked potentials (CAEPs) are used to assess the auditory perception of the electrical stimuli, since the auditory cortex processes the cochlea’s signals. Therefore, by measuring (CAEPs) at the “final stage” of the auditory pathway, acoustic processes can be quantified [6].

The presence of cortical auditory-evoked potentials (CAEPs) in response to a speech signal may indicate that speech is audible to the individual. Kelly et al. [7] showed that CI users with good speech understanding had similar amplitudes and latencies of the CAEPS compared to normal-hearing individuals. Rance et al. [8] demonstrated a clear relationship between speech perception scores and the presence of CAEPs.

Further studies have investigated the potential benefits of using the P1-N1-P2 complex as an objective tool in assessment of CI performance [9], to monitor maturation processes [10], to verify the integrity of the auditory system [3], to estimate threshold levels by loudness scaling [6], and to determine the auditory refractory effects [11].

This study was carried out to gain a better understanding of the prognostic factors that promote language development and auditory abilities after cochlear implantation. This could help in resolving the controversy in selection of CI candidates and in implementation of a rehabilitation program for better language and learning outcome after cochlear implantation.

This issue will be addressed in this work through studying speech-evoked cortical auditory-evoked potentials (S-CAEPs) and language test quotient; this combination between objective and subjective tests may be useful in assessment of efficacy of language therapy that was applied to children with CI and help these children develop language normally and to be enrolled in mainstream education.

Methods

Thirty-nine children with a cochlear implant who were prelingually deaf and aged 3 to 12 years participated in this cross-sectional research. All participants were recruited from the Audiovestibular Unit (Assiut University Hospital) between January 2021 and January 2022. Consent was obtained from each participant’s parents, after explaining the test and its purpose to them. The studied children had the following criteria:

• a) Children fitted with cochlear implant

• b) Less than 5 years of age at the time of implantation

• c) Prelingual deafness

• d) Average intelligence

• e) Exclude cases with abnormal middle ear status

All of the studied children underwent the following:

• A. Detailed audiological history

  Full history was obtained (personal, prenatal, natal, postnatal, family, sociodemographic, and rehabilitation history).

• B. Device check

  The electrical compound action potentials (ECAPs), impedance, CI microphone, map settings, cables, and batteries were checked.

• C. Audiological evaluation in the form of the following:

  • i. Otoscopic examination

  • ii. Tympanometry

  • iii. Aided free field audiometry

    • 1. Every participant was situated in a soundproof chamber and positioned 1-m distant and at a 45° azimuth angle to the left and right loudspeakers, for an aided sound field test. Warble tones were presented at 500-, 1000-, 2000-, and 4000-Hz frequencies, and each child was instructed to identify anytime he or she heard until reaching the threshold, and in younger children, aided play audiometry was done.

    • 2. This was followed by speech reception threshold (SRT) using bisyllabic words. Speech discrimination scores were tested at 40 dBSL.

  • iv. Aided cortical auditory-evoked potentials (A-CAEPs)

    The procedure was performed in an acoustically treated room and was recorded using Smart EP (Intelligent Hearing Systems, Miami, FL, USA).

    • a. Stimulus parameters

      Cortical auditory-evoked potentials were recorded in response to consonant vowel syllables /da/ of 206-ms duration. This stimulus was selected as the linguo-dental plosive consonants (/d/) are characterized by energy at 3–4 kHz which is an important speech frequency range [12]. The /da/ stimulus was presented at 40-dB SL or at their most comfortable level at 1/s repetition rate (RR) using alternating polarity.

    • b. Recording parameters

      Four disposable electrodes were used: One high frontal Fz (positive electrode) and one low frontal Fpz (ground electrode). The last two electrodes were placed on the left and right mastoids (as negative electrode or reference electrode) depending on the recording side.

      The filter setting was 1–30 Hz, the time window was set at 0–450 ms, and the total number of sweeps was 30.

      Speech stimuli were presented via loudspeaker at 45° azimuth angle to either left or right side according to the azimuth angle to either left or right side according to the tested side at distance of 1 m.

      The children remained alert, sitting comfortably in a reclining chair, and they were told to watch a silent video on a tablet during the procedure.

      Three averages were recorded, and the responses were considered to be present if components of S-CAEPs were identified in at least two out of the three averages.

    • c. Analysis of the response

      At the end of recording, analysis of the response was done with identification of different components of S-CAEPs: P1 (a positive wave at 80–120 ms), N1 (negative wave that follows P1 and peaks at 100–150 ms), P2 (large positive peak at 150–250 ms), and their latencies were calculated automatically by the device once the waves of S-CAEPs were identified and marked by the examiner (Fig. 1)

• D. Phoniatric assessment

  All of the studied children were referred to Phoniatric Unit, ENT Department, Assiut University Hospitals where a language test utilizing the Arabic language test was conducted [13]. All children were subjected to the protocol of language assessment and articulation test through the following steps:

  • a. Parents’ interview: Complaint and analysis of symptoms, personal history (age, birth order), family history (father’s and mother’s job, degree of mother’s education, parental consanguinity, and similar conditions in the family), developmental history (prenatal, neonatal, and postnatal), milestones of development, and illness of early childhood

  • b. Patient examination: Including general examination, neurological examination, and vocal tract examination to exclude any cases with associated disorders

  • c. Psychometric evaluation: To assess cognitive age (mental age) evaluation using Stanford-Binet Intelligence Scale [14]

  • d. Language evaluation: Using the Arabic language test [15]. It is valid and reliable test for evaluation of language development for Arabic-speaking children. The language test items include assessment of the following:

    • a. Attention of the child by observation

    • b. Receptive part of semantics that includes the following:

       ▪ Examining the ability of the child to recognize different semantic groups as body parts, cloths, fruits, vegetables, animals, furniture, transportation means, food utensils, colors, plants, and money, to categorize things into semantic groups, to make matching or pairing, to understand opposites, and to recognize time concept

    • c. Expressive part of semantics that includes the following:

       ▪ Examining the ability of the child to name different semantic groups and to say opposites

    • d. Receptive part of syntax: Which includes testing the ability of the child to understand the following:

       ▪ A sentence composed of two words: A noun and a verb

       ▪ A sentence containing a preposition or a spatial indicator as above, under, beside, right, left, behind, in the middle, around, and inside

       ▪ A sentence composed of three words (noun, verb, and object)

       ▪ A complete sentence

       ▪ Time indicators as before and after

       ▪ Different verb tenses “past, present, and future”

       ▪ Orders increasing in length

       ▪ Singular and plural

       ▪ Pronouns: Personal, subject, object, and possessives

       ▪ Adjectives: Big/small and tall/short

       ▪ Adverbs: Quickly/slowly and strongly/weakly

       ▪ Conjunctions: and, or

       ▪ Numbers

       ▪ Negative forms

       ▪ Comparatives and superlatives

       ▪ Passive voice sentence

       ▪ Action-agent use (the use of objects)

    • e. The expressive part of syntax: Testing the ability of the child to produce or utter the following:

       ▪ His name and many

       ▪ To respond to question whose answer is one word, either a name or a verb

       ▪ The various verb tenses: Past, present, and future

       ▪ Prepositions or spatial indicators

       ▪ A sentence composed of three words (noun, verb, and object).

       ▪ Singular and plural

       ▪ Pronouns: Personal, subject, object, and possessives

       ▪ Adjectives: Big/small and tall/short

       ▪ Adverbs: Quickly/slowly and strongly/weakly.

       ▪ Conjunctions: and, or

       ▪ Counting

       ▪ Negation

       ▪ Comparatives and superlatives

       ▪ Passive voice sentences

       ▪ Action agent (the use of different objects)

       ▪ Time indicators: Before and after

       ▪ Repetition

       ▪ A sample of spontaneous speech is elicited and written as such, and a comment on its length and degree of intelligibility is written.

    • f. Pragmatics

       ▪ Testing the ability of the child to initiate a dialogue, continue it, maintain topic, and end it

    • g. Testing phonology by the articulation test [13]

      Detailed assessment of articulation skill is carried out with the aid of general, extensive, and systemic articulation test that covers all the Arabic sounds. This test is composed of 24 bands; each band composed of three to four subitems. It examines the different Arabic phonemes at the beginning, middle, and the end of a familiar word. In young children, each word is accompanied by a picture that facilitates the use of this test.

Fig. 1

Example of CAEPs in response to /da/ stimulus (P1 at 90 ms, N1 at 166 ms, & P2 at 189 ms)

Results

Statistical analysis

• ▪ The collected data were revised, organized, tabulated, and statistically analyzed using Statistical Package for Social Sciences (SPSS) version 22.0 for Windows. Data are presented as the mean ± standard deviation (SD), frequency, and percentage. Categorical variables were compared using the chi-square (χ²) test and Fisher’s exact test (if required). Continuous normally distributed data were compared by the Student t-test (two-tailed) and one-way ANOVA test with Bonferroni post hoc test to detect the differences between the studied groups.

• ▪ Abnormally distributed continuous data compared using Mann–Whitney U and Kruskal–Wallis tests. Linear regression models were constructed to obtain the significant predictors of auditory and language scores. Pearson and Spearman correlation was used to study the correlation between the continuous variables. The level of significance was accepted if the P-value < 0.05.

Demographic data

• This study was conducted on 39 prelingually deafened children (Fig. 2).

• Their mean age was 7.5 ± 2.1 years, with ages ranging from 3.8 to 12 years.

Fig. 2

Percent of gender distribution among study groups

Sociodemographic characteristics of the studied children

The bulk of the participants included in this study were living in rural areas (74.4%). The rest of cases (25.6%) were living in urban areas in Upper Egypt. As regards the education level of their parents, according to the International Standard Classification of Education (ISCED) 2011, the educational state of the family was classified to poor educational status, those who had secondary level of education or less, and good educational status, those who had post-secondary level of education or higher. About two-thirds (66.7%) of the children’s parents included in the study had good education, and the rest (33.3%) had poor education.

Clinical features of the studied children

The clinical characteristics of the children who participated in this study (Table 1) included the hearing age (the number of months that the child was hearing by his CI), age of receiving CI, cause of hearing loss (either congenital nonsyndromic or congenital syndromic HL as there were two children with syndromic hearing loss (Waardenburg syndrome and achondroplasia)), side of implantation, regular use of HA, and regular speech therapy before CI.

Table 1 Clinical characteristics of the studied children with cochlear implantation. Total N = 39

Outcome measures of the studied children

Results indicated that P1 was detected in all studied children, while N1 was found in 76.9%, and P2 was found in 74.4% of the studied children who aged 8 years or more.

The relation between different preoperative variables and CI outcome of the studied children (univariate analysis)

Significant negative correlation was found between age of the studied children and their hearing age with their outcome measures (aided FFA & S-CAEPS), while statistically significant positive correlation was found between these outcomes and their age of implantation, meaning that with increase in the age and hearing age of the studied children, there was a decrease in average FFA threshold and decrease the latencies of S-CAEPS. Earlier age of implantation was associated with decrease in average FFA threshold and decrease the latencies of S-CAEPS.

There was a positive relationship that was statistically significant among age and hearing age of the studied children and their expressive and receptive language quotients while significant negative relationship between their age of implantation and language quotients.

This means that the increase in the language quotients of the studied children was associated with increase in their age and hearing age and also with decrease in their age of implantation.

In the same time, other variables such as their sex, residence, educational state of their parents, causes of deafness, and regular use of HA and speech therapy before CI had no statistically significant correlation with the measured outcome of the studied children. All of these results were shown in Tables 2 and 3.

Table 2 Correlation of sociodemographic and clinical characteristics of the studied children with average FFA threshold and S-CAEP (P1, N1, & P2 latencies)

Table 3 Correlation of sociodemographic and clinical characteristics of the studied children with expressive and receptive language quotient

Predictors of CI outcome using (multivariate analysis)

We performed multivariable regression analysis of the variables hierarchically proven to be predictors of CI outcome, and we found that the statistically significant predictors of CI outcome as regard p1 latency were hearing age, N1 latency was age at implantation, and as regard receptive language, quotients were age in month and age of implantation, meaning that earlier age of implantation and longer duration of CI use were highly significant predictors of language output.

Correlation between different outcome measures

There was a significant negative association among both expressive and receptive language quotient of the studied children with S-CAEP and average aided FFA threshold, meaning that the increase in receptive and expressive language quotients was associated with decrease in the latency of CAEP parameters and with decrease in the average aided FFA threshold.

In the same time, a statistically significant association existed between average FFA threshold and ACEP latency.

Discussion

This study covered a wide range of features, and individuals of both sexes used their implants within 6 months and 9 years and were implanted between the ages of 2 and 5 years. All these variables, causes of hearing loss, early hearing aids fitting and preoperative speech therapy, care and awareness of parents, their educational level, occupation, residence, and socioeconomic status, were studied, to detect whether it was useful in predicting language and auditory capabilities in individuals with CI or not.

In this study, combination of subjective methods such as aided free field audiometry, language tests, and objective methods such as ACEPS using speech stimulus was measured (Tables 4 & 5).

Table 4 Results of the mean and SD of P1, N1, and P2 components of S-CAEPs, aided free field audiometry threshold, aided SRT, and language test (expressive and receptive language quotient) of the study group

Table 5 Correlation between different outcome scores

Cortical auditory-evoked potential was better indicative of optimal speech and language development in the studied children. It was assumed that the existence of a CAEP responses indicates that sound has reached, perceived at the higher regions of the brain and ready for cortical processing [10].

Both morphology and latency of cortical responses change over time, and P1 latency decreases quickly during infancy and childhood and slowly during adolescence [9]. It has been shown to be a biomarker for determining how well children’s central auditory pathways are maturing [10, 16].

Morphology of the response changes from single P1 response in childhood to a P1 and N1 and P2 response with advancing age [9], and our results approved that as further component of CAEP such as N1 and P2 was detected in children 8 years or more.

This study assessed the variables that affect the rate of oral language development, so the evaluation of language development was facilitated by receptive tests for the detection, discrimination, identification, and perception of language samples. Expressive speech production can serve as an alternative criterion [17].

Variables affecting CI outcome

Age at time of cochlear implantation

In this study, we discovered that there was statistically significant association (P < 0.01) between age of implantation and different outcome measures (inversely correlated with receptive and expressive language quotient and positively correlated with aided FFA threshold and aided speech cortical auditory-evoked potential (univariate analysis)).

It was statistically significant predictor for CI outcome as regard receptive language scores and also for N1 latency (multivariate analysis) (Tables 2, 3, 6, & 7).

Table 6 Predictors of CI outcome using N1 latency of S-CAEPS (multivariate analysis)

Table 7 Predictors of CI outcome using receptive language quotient (multivariate analysis)

Our results were in agreement with a study done by Gaurav et al. [18] who found that CI recipients implanted at age of “5 years or below” had considerably better mean auditory perception results than those who implanted at “more than 5 years” of age (rise of 12.29% in CAP and 14.05% in MAIS values).

Noroozi et al. [19] supported this, as their research included 104 participants who were brought to the Khuzestan Cochlear Implant Center in Ahvaz, Iran. Children who received cochlear implants were monitored for a year, and categories of auditory performance (CAP) assessments were kept. They found that implantation age was negatively correlated with speech perception after 1 year.

Age of implantation relates to the survival, physiology, and function of spiral ganglion cells. A critical period for the development of human auditory pathway has not been definitively established, and research in this area is in progress. Effects of deprivation and plasticity on post CI performance can be interpreted to a certain extent to age at which the child receives CI [18].

There is a positive association among low-resting activity and speech perception in the primary auditory cortex (PAC) before CI for the prelingual deaf, suggesting that CI may enable the PAC to mature in a manner that is experience dependent. Given the continuing increase in auditory ability with greater CI experience, this link shows that PAC along with other higher order auditory regions are elastic changeable [18].

Gender of the studied children

We discovered that there was no existed a statistically substantial variation between male and female groups in this study as regards their different outcome measures (P > 0.05) (Tables 2 & 3).

In normal-hearing subjects, females use more integrative and predictive cognitive strategies for speech comprehension than males. However, there is no evidence of a gender difference in speech comprehension performance, and females not always have greater ability to adapt to the changed auditory information provided by a cochlear implant. This shows that men and women use different cognitive that normally result in similar levels of speech comprehension [20].

Our results was in agreement with a study made by Green et al. [21] who did not find any statistically significant difference between male and female and also in agreement of a study done by Lenarz et al. [22] who found that in the speech tracking test and the Freiburger monosyllabic test, both genders performed similarly.

Unlike Hamid et al. [23] who discovered that females do better in language than males, this is evidenced that girls outperform boys verbally in both hearing [24] and hearing-impaired populations [25].

Hearing age of the studied children

In this study, we found that the hearing age was highly significant predictor for language and auditory abilities as regards receptive language quotient and P1 latency (multivariate analysis), and this enhances the significance of cochlear implant usage duration when assessing the device’s advantages (Tables 8 & 7).

Table 8 Predictors of CI outcome using P1 latency of S-CAEPS (multivariate analysis)

Cho et al. [26] showed that among a sample of 61 participants who had implants, the duration of implant usage revealed the most variable in performance. Waltzman et al. [4] examined 81 individuals who had implants at a major academic medical facility and were observed for 5 to 13 years and found that using their CI consistently led to considerable improvements in speech perception, oral language usage, and capacity to function in a mainstream context.

Preoperative regular use of HA and regular enrollment in speech therapy

In this study, we discovered that there was no statistically significant distinction among preoperative regular use of HA and regular enrollment in speech therapy in the studied children and different outcome measures (P > 0.05) (Tables 2 & 3).

These results indicate that postponing cochlear implantation to prolong hearing aid usage for kids with severe-to-profound hearing impairment may be harmful to the development of language and may lead to substantial loss in language development [27].

This was unlike Hamid et al. [23] They discovered that continual language treatment over months and preoperative hearing aid fitting were important indicators of auditory ability; language therapy lasting more than 6 months was a reliable indicator of language outcomes.

The differences between our results and other studies may be attributed to the presence of residual hearing which would benefit from acoustic amplification.

In conclusion, spoken language learning relies on effective hearing. Close monitoring of performance with hearing aids can determine whether speech is effectively amplified to allow spoken language acquisition to progress or not.

Sociodemographic variables

In this study, we discovered that sociodemographic variables cannot significantly affect outcome of CI in the investigated children (P > 0.05) (Tables 2 & 3). This was in agreement with Sharma et al. [28] in which they discovered that socioeconomic status did not appear to have a major influence on the achievement of children following cochlear implantation. Their study aimed to evaluate the effect of specific socioeconomic variables, which included the parents’ level of education, the distance between their house and the auditory verbal treatment facility, the income of their families, and the child’s age upon implantation.

Knutson et al. [29] also noted that there was not much information on how familial characteristics affect how effectively kids who have cochlear implants develop their language and speech skills.

In the same time, many researches examining the connection between socioeconomic characteristics and cochlear implant success had produced a range of findings, and poor socioeconomic situation along with inadequate levels of education within the household is accountable for a delay in cochlear implantation [30]. That might be partially related to a limitation of knowledge about the cochlear implant’s existence and advantages as well as poor accessibility to medical services.

Kids who have a greater socioeconomic position show better progress in spoken language and understanding, according to Niparko et al. [29] research of the development of language after cochlear implantation.

According to our hypothesis, parents from a lower socioeconomic class sacrificed time from their job schedule in order to fulfill the plan laid out for their kid. This might have been one of the elements that enabled children from lower socioeconomic categories to compensate for the gap and perform on line with their counterparts from better socioeconomic groups.

This may have been made easier by providing the parents with comprehensive preoperative counseling in order to educate them on the value of extended postoperative auditory verbal treatment and by providing the maximum amount of aural stimulation at home.

Conclusion

Age of the studied children at time of cochlear implantation and hearing age were the most important predictors that affect speech and language development. Other preoperative variables studied were not significant predictors for CI outcome. However, these variables must be taken in consideration when we select candidate for cochlear implantation.

P1 latency may offer physicians with a method for objectively evaluating maturation and development of central auditory pathways. Combination between objective measures (S-CAEP) and subjective measures (language test) in evaluation of language and speech development of the studied children was valuable in evaluation of electrical stimulation’s impact of CI on hearing and speech centers of the brain and the efficacy of language therapy that was applied to children with CI.