Introduction. Sung Wook Jeong 1 Seung Hyun Chung 1 Lee Suk Kim 1

Transcription

1 OTOLOGY P1 cortical auditory evoked potential in children with unilateral or bilateral cochlear implants; implication for the timing of second cochlear implantation Sung Wook Jeong 1 Seung Hyun Chung 1 Lee Suk Kim 1 Received: 2 March 2018 / Accepted: 26 May 2018 / Published online: 31 May 2018 Springer-Verlag GmbH Germany, part of Springer Nature 2018 Abstract Objective To examine maturation of the central auditory pathway, using P1 cortical auditory evoked potential (CAEP), in children who had received unilateral or bilateral cochlear implantation (CI). Study design Prospective study. Setting Tertiary referral hospital. Methods Twenty children who had received CI due to congenital, or prelingual, deafness participated in the study. Participants had received the 1st implant at a mean age of 3.4 ± 0.7 years; 16 had also received a 2nd CI for the contralateral ear, at a mean age of 11.1 ± 2.1 years. P1 CAEP was recorded while using the 1st implant and, for those who received contralateral CI, within 2 weeks of switching on the 2nd implant. Relations between P1 latency and duration with the 1st implant, and between age at 1st CI and P1 latency, were investigated. Relations between P1 latency with the 1st and 2nd implants, and between the interstage interval and difference between P1 latencies with the 1st and 2nd implants, were also examined. Results P1 CAEP with the 1st implant was present in 16 of the 20 children. Mean P1 latency was shorter in the early CI group compared with the late CI group, but this difference was not statistically significant (p = 0.154). There was a significant negative correlation between the duration with the 1st implant and P1 latency (r = 0.783, p < 0.001). Among the 16 children with sequential bilateral CI, P1 CAEP with the 2nd implant was present in 10. There was a significant negative correlation between the duration with the 1st implant before receiving the 2nd implant and P1 latency with the 2nd implant (r = 0.710, p = 0.021); there was also a significant positive correlation between P1 latency with the 1st and 2nd implants (r = 0.722, p = 0.018). There was not a significant correlation between interstage interval and the difference between the two P1 latencies (r = 0.430, p = 0.248). Conclusion Longer cochlear implant use is associated with shorter P1 latency. Unilateral hearing with the 1st implant may positively affect P1 latency with the 2nd CI ear. These findings imply that increased auditory experience may influence central auditory pathway maturation and that the degree of central auditory pathway maturation before the 2nd CI, rather than the timing when the surgery is received, may influence 2nd CI outcome in children with sequential bilateral cochlear implants. Keywords Cochlear implants Cortical auditory evoked potential Central auditory pathway Child Introduction * Lee Suk Kim klsolkor@chol.com 1 Department of Otolaryngology Head and Neck Surgery, College of Medicine, Dong-A University, 3 1 Dongdaeshin dong, Seo gu, Busan , South Korea Auditory deprivation during early development in children with congenital hearing loss causes devolution of the central auditory pathway and poor development of oral speech and language functions [1, 2]. Among prelingual deaf patients, a smaller functioning auditory cortex volume is found in older subjects compared with those who are younger, and is positively correlated with speech perception after cochlear implantation (CI) [1]. A period of auditory deprivation from 6.5 to 7.5 years causes significant loss of functioning Vol.:( )

2 1760 European Archives of Oto-Rhino-Laryngology (2018) 275: auditory cortex due to cross-modal reorganization [2]. However, audition restoration through CI in children with congenital deafness promotes maturation of the central auditory pathway and leads to higher levels of oral speech and language skills. Maturation of the central auditory pathway can be objectively assessed using cortical auditory evoked potential (CAEP) [3]. CAEP response is composed of P1, N1 and P2 components. P1 originates from the primary auditory cortex and thalamus [4] and N1 and P2 reflect higher levels of auditory cortical processing including secondary auditory cortex [5]. P1 is present in newborns with normal hearing, but N1 and P2 cannot be reliably recorded until about age 7 years [6]. Thus, the P1 component of the CAEP response can be used to assess central auditory pathway maturation in young children. P1 latency at birth is about 300 ms and decreases gradually with age, finally reaching 60 ms [7]. This change reflects the increased speed of synaptic transmission along the ascending auditory pathway and is why P1 latency can serve as a biomarker of central auditory pathway maturation [3, 7]. There have been several studies of P1 CAEP in children with cochlear implants [3, 5, 8, 9]. One described P1 latencies in 245 congenitally deaf American children who received CI at various ages [3]. In that study, the P1 latency of children with cochlear implants was plotted against the 95% confidence interval of normative, age-appropriate values. The authors claimed that there is a sensitive period, ending at age 3.5 years, during which the central auditory pathway is maximally plastic; children who received CI before this age had a P1 latency within normal limits for their age. Other studies have demonstrated a gradual decrease in P1 latency with increased duration of hearing experience with cochlear implants [10, 11]. Most published studies of P1 CAEP in children who have received CI have been with children who received unilateral CI; P1 CAEP studies including children with bilateral cochlear implants are rare, and research including Asian children who have received CI is lacking. As such, this study examined maturation of the central auditory pathway, using P1 CAEP, in Korean children who had received unilateral or bilateral CI. Subjects and methods Subjects The participants were 20 children who had received CI (Table 1). Inclusion criteria were congenital or prelingual deafness, the absence of cochlea or cochlear nerve malformations and absence of any additional handicap. Participants were 15 boys and five girls who had received their 1st implant at a mean age of 3.4 ± 0.7 years. Sixteen of these Table 1 The demographic findings of subjects No. of patient Sex Onset of deafness Age at 1st CI (years) 1st CI device Duration of 1st CI use at 1st P1 recording (years) Age at 2nd CI (years) 2nd CI device 1 M Congenital 1.1 CI M Congenital 1.1 CI M Congenital 0.9 CI M Congenital 4.5 CI24RECA M Congenital 3.0 CI24RECA CI422 6 F Congenital 6.5 CI24RCS CI422 7 M Congenital 9.8 CI24RCS CI422 8 F Congenital 2.3 CI CI422 9 M Prelingual 10.1 CI24RCS CI F Congenital 1.0 CI CI M Congenital 1.0 CI CI F Congenital 1.8 CI CI M Prelingual 4.9 CI24RCS CI M Congenital 2.0 CI CI M Prelingual 2.9 CI24RCS CI M Congenital 6.9 CI24RCS CI M Congenital 1.0 CI CI M Congenital 2.0 CI24RECA CI F Congenital 2.5 CI24RECA CI M Congenital 2.5 CI24RCA CI422

3 children received a 2nd CI for the contralateral ear at a mean age of 11.1 ± 2.1 years. Methods P1 CAEP was recorded in response to a 1.0-kHz tone burst sound. The duration of sound stimulus was 100 ms (10-ms rise/fall time, 80-ms plateau). Stimulation intensity was 80 db nhl and stimulation rate was 0.7/s. The stimulus was presented via a speaker placed 1 m in front of the child while wearing their cochlear implant. Subjects were seated in a comfortable reclining chair, or seated on a parent s lap, in a sound-treated booth. Children watched a cartoon movie on a laptop monitor or smartphone. The electroencephalographic response was collected using Viking IV (Nicolet Biomedical, Fenton, MO, USA). Scalp recordings were made with silver-coated surface recording electrodes at midline (Fz; upper forehead) referenced to the contralateral mastoid. An electrode positioned at Fpz (lower forehead) was used as a ground. Eyeblink was monitored using electrodes located above and below the eye contralateral to the test ear. Responses were amplified with a gain of 10,000 and filtered from 1 Hz (high-pass filter) to 30 Hz (low-pass filter). The recording window included a 50-ms prestimulus period and a 450-ms poststimulus period, and over 200 sweeps were obtained for each stimulus. P1 CAEP was defined as the first robust positivity and P1 latency was measured to the peak of the response or, if the peak was broad, the midpoint. Two waveforms for each stimulus were obtained to check reproducibility and the mean P1 CAEP latency was calculated. P1 CAEP recordings were collected twice. The first recording was while using the 1st implant. The duration of use of the implant at the time of the recording varied from 1 month to 14.6 years and their ages when they received CI also varied. As such, the relation between the duration of 1st implant use and P1 latency, as well as between age at CI and P1 latency were investigated. Sixteen of the 20 children received a 2nd CI for the contralateral ear, and for these participants, a second P1 CAEP recording was collected using the 2nd implant ear immediately or within 2 weeks after switching on the 2nd implant. The duration of 1st implant use before the 2nd CI varied, so the relation between the duration of 1st implant use and P1 latency of the 2nd implant was investigated. The relation between P1 latencies of the 1st and 2nd implants and the relation between the interstage interval and difference between the P1 latencies of the 1st and 2nd implants was also examined. The data are presented as mean ± SEM. Analyses were performed using independent samples t test, paired samples t test, Mann Whitney U test and simple linear regression analysis, using SPSS version 21.0 statistical software (IBM Corp., Armonk, NY, USA). p values < 0.05 were considered 1761 statistically significant. This study was approved by the institutional review board of the Dong-A University Hospital. Results Age at 1st CI and P1 CAEP latency P1 CAEP was present in 16 of the 20 children at the first recording (Fig. 1). Mean P1 CAEP latency among those who had a P1 response was ± 12.0 ms. The relationship between age at 1st CI and P1 latency was investigated in the 12 children who had used their 1st implant for at least 12 months. These children were divided into two groups according to age at CI: the early implant group received CI before age 5 years (n = 8); the late implant group received CI after age 5 years (n = 4). Mean P1 latency in the early implant group was shorter than with the late implant group (114 and 133 ms, respectively), but the mean latency difference was not statistically significant (p = 0.154, Mann Whitney U test) (Fig. 2). Duration of 1st implant use and P1 CAEP latency The mean durations of 1st implant use in children with and without a P1 response were 8.8 and 0.4 years, respectively (p = 0.016, Mann Whitney U test). There was also a significant, negative correlation between the duration of cochlear implant use and P1 latency (r = 0.783, p < 0.001, simple linear regression analysis) (Fig. 3). Duration of 1st implant use and P1 latency with 2nd implant Sixteen children who received a 2nd CI for the contralateral ear had a second P1 CAEP recording with the 2nd implant. These recordings were made immediately or within 2 weeks after the 2nd implant was switched on. P1 CAEP was present in 10 of these 16 children, and among those 10, mean P1 CAEP latency was ± 7.4 ms. A significant negative correlation was found between duration of 1st implant use before 2nd CI and P1 latency with the 2nd implant (r = 0.710, p = 0.021, simple linear regression analysis) (Fig. 4). P1 latencies of the 1st and 2nd implants Though the mean P1 latency with the 1st implant was slightly shorter than with the 2nd implant, this difference was not statistically significant (p = 0.220, paired t test), despite the 1st implant having been used significantly longer than the 2nd implant (8.5 years and 2 days, respectively) (Fig. 5a). In addition, there was a significant

4 1762 European Archives of Oto-Rhino-Laryngology (2018) 275: Fig. 1 Representative P1 cortical auditory evoked response in two children with cochlear implants. a Example of a P1 response from a boy age 1 year, 9 months. b Example of the absence of a P1 response from a boy age 1 year Fig. 2 P1 latency according to age at cochlear implantation (CI). Mean P1 latency in the early CI group was shorter than with the late CI group; the mean difference was not statistically significant (p = 0.154, Mann Whitney U test). Values are mean and SEM positive correlation between P1 latency with the 1st and 2nd implants (r = 0.722, p = 0.018, simple linear regression analysis) (Fig. 5b). Fig. 3 Scatterplot showing the significant negative association between duration of 1st implant use and P1 latency (r = 0.783, p < 0.001, simple linear regression analysis) Interstage intervals between the 1st and 2nd CIs, and P1 latency difference between 1st and 2nd implants The mean interstage interval between the 1st and 2nd CIs was 8.5 ± 1.7 years, and the mean P1 latency difference between the 1st and 2nd implants was 13.9 ± 3.2 ms. There

5 1763 Fig. 4 Scatterplot showing the significant negative association between duration of 1st implant use before 2nd CI and P1 latency of 2nd implant (r = 0.710, p = 0.021, simple linear regression analysis) was not a significant correlation between the interstage interval and the difference between the two P1 latencies (r = 0.255, p = 0.477, simple linear regression analysis) (Fig. 6). Discussion Early intervention leads to better speech-language outcomes in children with congenital hearing loss, and intervention within 6 months of age is strongly recommended [12]. Fortunately, with newborn hearing screenings, congenital hearing loss is now detected very early. As such, intervention using hearing aids or CI can be provided in early infancy. However, it is difficult to determine whether devices provide sufficient benefits to allow infants with hearing loss to achieve age-appropriate development, because subjective monitoring of infants auditory development is unreliable [13]. P1 CAEP can help monitor the auditory development of infants with hearing loss objectively [3, 7]. Maturation of the central auditory pathway in hearing-impaired children who use hearing aids or cochlear implants can be determined by monitoring whether P1 latency decreases over time and whether the absolute value of P1 latency falls within a normal range. In this study, the duration of 1st implant use was negatively correlated with P1 latency (r = 0.783, p < 0.001), suggesting that experience-driven plasticity occurs in children who have received CI [14]. In other words, auditory experience following CI may promote maturation of the central auditory pathway and decreases in P1 latency over time. The P1 latencies of children in this study who had received CI could not be evaluated in relation to normative values, because these Fig. 5 Comparison of P1 latencies with 1st and 2nd implants. a Mean P1 latency with the 1st implant was shorter than the 2nd implant; this difference was not statistically significant (p = 0.220, paired t test). Values are mean and SEM. b Significant positive correlation between P1 latencies of 1st and 2nd implants (r = 0.722, p = 0.018, simple linear regression analysis) have not yet been fully established in Korean children with normal hearing. One of the most important studies of P1 CAEP in children with a cochlear implant was performed by Sharma et al. [3] and included 245 congenitally deaf children who received CI at various ages. The children who received CI before 3.5 years had normal P1 latencies. Only half of the children who received CI between the ages 3.5 and 7 years, and nearly none who received CI after age 7 years, had normal P1 latencies. This supports the notion of a sensitive period, during which the central auditory pathway may be maximally plastic; it also emphasizes that hearing should be restored before 3.5 years to achieve normal central auditory pathway maturation. Likewise, the early CI group in the present study showed a shorter P1 latency than the late CI

6 1764 European Archives of Oto-Rhino-Laryngology (2018) 275: Fig. 6 The relation between interstage interval and P1 latency in children with sequential bilateral CI. The X-axis is the interstage interval between 1st and 2nd CIs; the Y-axis is the P1 latency with the 2nd implant minus the latency with the 1st implant. The correlation coefficient was not statistically significant (r = 0.255, p = 0.477, simple linear regression analysis) group; although the difference was not statistically significant, this may have been due to a small sample size. Success of the 1st CI in children with congenital deafness depends largely on the age at which the child receives surgery [15 17]. Because the human brain has sensitive periods for development, during which experience-dependent alteration is maximal, the final outcome of the 1st CI is optimal when performed during the sensitive period for auditory cortex development: within the first 1 3 years of life [5, 18, 19]. Accordingly, the approved age for CI surgery by the US FDA was lowered to 24 months in 1990 and then to 12 months in Recent studies have shown that a 1st CI before age 12 months leads to significantly better speech production and language abilities than when surgery is performed between age months [15, 16]. However, optimal timing of a 2nd CI in the contralateral ear of children with a unilateral cochlear implant has not been established. Research has shown that the 2nd CI timing does not seem as critical as it is for the 1st CI [20 24]. A shorter interstage interval (i.e., earlier 2nd CI) has resulted in better outcomes, but there are small differences in speech perception abilities between children with short and long interstage intervals [20, 21] and correlations between interstage interval and speech perception ability with the 2nd implant are weak [22 24]. Kim et al. studied 42 children with sequential bilateral CI who achieved excellent speech perception with their 1st implant before receiving a 2nd CI and found that there was not a significant difference in speech perception between their 1st and 2nd implant ears after the 2nd CI [21]. Even children with an interstage interval of 7 or more years had good speech perception with their 2nd CI ear, which was comparable to their 1st CI ear. Furthermore, there was no difference in speech perception with the 2nd CI ear between children with short and long interstage intervals, showing that speech perception ability with the 1st CI ear, rather than the timing of a 2nd CI surgery, influences 2nd CI outcome. Findings from the present study are in agreement with those of previous studies. This study demonstrates that P1 latency of the 1st implant is positively correlated with P1 latency of the 2nd implant (r = 0.722, p = 0.018) and that duration of 1st implant use is negatively correlated with P1 latency of the 2nd implant (r = 0.710, p = 0.021). In addition, there was not a significant correlation between interstage interval and the difference between P1 latencies with the 1st and 2nd implants. These findings suggest that the success of 2nd CI depends on the maturational status of central auditory pathway gained with use of the 1st implant rather than the timing of 2nd CI surgery. Conclusion Longer duration of hearing experience using a cochlear implant is associated with shorter P1 latency. Shorter P1 latency with a 1st implant is also correlated with shorter P1 latency with a 2nd implant, and longer duration of 1st implant use is correlated with shorter P1 latency with a 2nd implant. These cumulate results suggest that central auditory pathway maturation is achieved with increasing hearing experience using cochlear implant and that the degree of central auditory pathway maturation before a 2nd CI, rather than the timing of the surgery, may influence the 2nd CI outcome in children with sequential bilateral CI. Acknowledgements This study was supported by research funds from Dong-A University. Compliance with ethical standards Conflict of interest All the authors certify that they have no conflict of interest. Ethical approval All procedures performed in this study were in accordance with the ethical standards of the institutional review board of the Dong-A University Hospital. References 1. Lee HJ, Kang E, Oh SH, Kang H, Lee DS, Lee MC et al (2004) Preoperative differences of cerebral metabolism relate to the outcome of cochlear implants in congenitally deaf children. Hear Res 203:2 9

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