Delayed Auditory Brainstem Responses in Prelingually Deaf and Late-Implanted Cochlear Implant Users

JARO 16: 669–678 (2015) DOI: 10.1007/s10162-015-0532-x D 2015 The Author(s). This article is published with open access at Springerlink.com Research Article JARO Journal of the Association for Research in Otolaryngology Delayed Auditory Brainstem Responses in Prelingually Deaf and Late-Implanted Cochlear Implant Users MARC J. W. LAMMERS,1,2 RUBEN H. M. VAN EIJL,1,2 GIJSBERT A. VAN ZANTEN,1,2 HUIB VERSNEL,1,2 AND WILKO GROLMAN1,2 1 Department of Otorhinolaryngology and Head & Neck Surgery, University Medical Center Utrecht, Room G.02.531P.O. Box 855003508 GA, Utrecht, The Netherlands 2 Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, The Netherlands Received: 16 February 2015; Accepted: 15 June 2015; Online publication: 11 July 2015 ABSTRACT Neurophysiological studies in animals and humans suggest that severe hearing loss during early development impairs the maturation of the auditory brainstem. To date, studies in humans have mainly focused on the neural activation of the auditory brainstem in children treated with a cochlear implant (CI), but little is known about the pattern of activation in adult CI users with early onset of deafness (prelingual, before the age of 2 years). In this study, we compare auditory brainstem activation in prelingually deaf and late-implanted adult CI users to that in postlingually deaf CI users. Electrically evoked auditory brainstem responses (eABRs) were recorded by monopolar stimulation, separately using a middle and an apical electrode of the CI. Comparison of the eABR latencies revealed that wave V was significantly delayed in the prelingually deaf CI users on both electrode locations. Accordingly, when the apical electrode was stimulated, the III–V interwave interval was significantly longer in the prelingually deaf group. These findings suggest a slower neural conduction in the auditory brainstem, probably caused by impairment of maturation during the long duration of severe hearing loss in infancy. Shorter wave V latencies, reflecting a more mature brainstem, appeared to be a predictor for better speech perception. Correspondence to: Huib Versnel & Department of Otorhinolaryngology and Head & Neck Surgery & University Medical Center Utrecht & Room G.02.531P.O. Box 855003508 GA, Utrecht, The Netherlands. email: Keywords: auditory brainstem response, cochlear implant, maturation, humans, prelingual deaf, hearing loss, deafness INTRODUCTION The duration of auditory deprivation before cochlear implantation is an important predictor for hearing with a cochlear implant (CI). Whereas patients with late onset of deafness can obtain good speech perception in quiet, the hearing performance of patients with long-term early-onset deafness is generally poor (Teoh et al. 2004; Lammers et al. 2015). The large difference might be caused by an impaired development of their auditory pathway in combination with cross-modal changes during a prolonged period of auditory deprivation (Doucet et al. 2006; Lee et al. 2007; Kral and O’Donoghue 2010; Kral and Sharma 2012; Lammers et al. 2015). Recently, we demonstrated that prelingually deaf and late-implanted CI users display relatively early and large N1 peaks of the cortical auditoryevoked potential (Lammers et al. 2015). This altered cortical activity raises the question regarding the extent to which the subcortical pathway, particularly the auditory brainstem, is affected in prelingually deaf CI users. It is well documented that after birth, auditory brainstem response (ABR) wave latencies decrease and reach adult levels around the age of 2–3 years (Inagaki et al. 1987; Eggermont and Salamy 1988). This decrease is slower for wave V than for early waves and is hypothesized to result from increasing myelination and/or synaptic efficacy within the auditory brainstem since these developments lead to faster axonal conduction and synaptic 669 670 transmission (Eggermont and Salamy 1988; Moore et al. 1995; Thai-Van et al. 2007). Long periods of deafness affect the subcortical pathway, resulting in gradual spiral ganglion cell degeneration (Spoendlin 1975; Versnel et al. 2007), and a volume reduction of the cochlear nucleus and its cells (Moore 1990; Leake et al. 2008; Ryugo et al. 2010). On the other hand, electrically evoked ABRs (eABRs) in congenitally deaf cats demonstrate latencies decreasing with age, similarly to normal-hearing cats (Tillein et al. 2012). This suggests that auditory brainstem structures and pathways develop even in the absence of auditory stimulation. In humans, development of the auditory brainstem following deafness has been studied by recording eABRs in children with CI (Gordon et al. 2006, 2008; Thai-Van et al. 2007; Sparreboom et al. 2010). These studies demonstrated that in children with early-onset deafness, eABR wave latencies decrease after implantation, irrespective of age at implantation, like they do in normal-hearing children. On the contrary, in bilaterally implanted children, when a response is evoked using a second CI implanted much later than the first, the wave V latency is longer than the responses evoked by the first CI (Gordon et al. 2008; Sparreboom et al. 2010). This suggests impaired maturation of the auditory brainstem of the later implanted ear (Gordon et al. 2008; Sparreboom et al. 2010), or altered neuronal connections induced by the period of unilateral hearing with the first CI. Whereas above-mentioned studies were performed in children and in animal models, we address the effect of early deafness on the auditory brainstem in adults. We compare eABRs in prelingually deaf subjects who had little or no auditory stimulation for more than 20 years to eABRs in postlingually deaf CI users. According to various studies (Eggermont and Salamy 1988; Moore et al. 1995; Thai-Van et al. 2007; Leake et al. 2008; Ryugo et al. 2010), myelination and synapses in the brainstem of the postlingual group should have developed normally because of sufficient auditory input during childhood. In contrast, we expect the coarse structures of the brainstem to develop in the prelingual group but sensory-driven maturation to be impaired reducing axonal myelination and synaptic efficacy among others. Any effect by auditory stimulation after cochlear implantation could only have occurred in the adult system and is expected to be negligible. Therefore, we hypothesize typical eABR waveforms in both groups, but longer wave V latencies in the prelingually deaf. METHODS Participants All adult users of a Cochlear® CI who visited the outpatient clinic from December 2011 to December LAMMERS ET AL.: eABRs in Prelingually Deaf CI Users 2012 were consented to participate in a study which included eABR and cortical auditory-evoked potential (CAEP) recordings. Twenty-three adults, with at least 6 months experience with their CI, agreed to participate in this study. In 20 subjects, eABRs could be recorded, while in the remaining three postlingual subjects, no cl (...truncated)