Sensitivity of the cochlear nerve to acoustic and electrical stimulation months after a vestibular labyrinthectomy in guinea pigs

Highlights

• Minimal cochlear sensitivity loss 10 months after labyrinthectomy in a guinea pig.

• Cochlear implants are effective months after vestibular labyrinthectomy.

• There is minimal cochlear fibrosis or scaring following labyrinthectomy.

• Support for Cochlear implant in post-labyrinthectomy patients.

Abstract

Single-sided deafness patients are now being considered candidates to receive a cochlear implant. With this, many people who have undergone a unilateral vestibular labyrinthectomy for the treatment of chronic vertigo are now being considered for cochlear implantation. There is still some concern regarding the potential efficacy of cochlear implants in these patients, where factors such as cochlear fibrosis or nerve degeneration following unilateral vestibular labyrinthectomy may preclude their use. Here, we have performed a unilateral vestibular labyrinthectomy in normally hearing guinea pigs, and allowed them to recover for either 6 weeks, or 10 months, before assessing morphological and functional changes related to cochlear implantation. Light sheet fluorescence microscopy was used to assess gross morphology throughout the entire ear. Whole nerve responses to acoustic, vibrational, or electrical stimuli were used as functional measures. Mild cellular infiltration was observed at 6 weeks, and to a lesser extent at 10 months after labyrinthectomy. Following labyrinthectomy, cochlear sensitivity to high-frequency acoustic tone-bursts was reduced by 16 ± 4 dB, vestibular sensitivity was almost entirely abolished, and electrical sensitivity was only mildly reduced. These results support recent clinical findings that patients who have received a vestibular labyrinthectomy may still benefit from a cochlear implant.

Introduction

Despite much research, the etiology of Meniere's syndrome remains unknown and there is no cure. Often in advanced stages of the disorder, where the patient's natural hearing has been completely lost, patients may still experience disabling vertigo. Options at this stage to bring relief to these symptoms include intratympanic gentamicin injections, and if this fails, a surgical unilateral vestibular labyrinthectomy (UVL). While patients undergoing a UVL generally have permanent relief from any future vertiginous attacks, at the same time, they typically irreversibly lose hearing in that ear (Dickins and Graham, 2005, Goksu et al., 2005). In this setting the application of Cochlear Implant (CI) technology has created a lot of interest as it gives new hope for these patients to regain their ability to hear (Fife et al., 2014, Hansen et al., 2013, Lustig et al., 2003, Samy et al., 2014). Since the sanction of single-sided deaf patients as candidates for a CI (some of whom are post UVL patients), there are now many Meniere's patients who stand to benefit from a CI.

Currently, apart from several case studies (Facer et al., 2000, Osborn et al., 2012, Zwolan et al., 1993), little is known about long term hearing outcomes with CI following a labyrinthectomy. Furthermore, the optimal timing of when to perform the labyrinthectomy and CI are unclear, and potential technical and functional challenges remain. With the vestibule open there is a risk that the cochlea, which is partly an immunologically isolated area, may develop adhesions or fibrosis over time. If this were to occur there would be conceivable technical challenges in successful implantation. For this reason many surgeons have advocated implantation at the same time as the labyrinthectomy (Doobe et al., 2015, MacKeith et al., 2014). It is difficult to ascertain the hypothesized risk of fibrosis, although recent studies have utilized MRI to determine severe cochlear fibrosis cases following labyrinthectomy (Charlett and Biggs, 2015). Additionally, there is a risk of cochlear nerve deterioration with time if the cochlea suffers a sensorineural hearing loss (Kujawa and Liberman, 2015), which may significantly decrease the sensitivity of the VIII^th nerve to the electrical stimulation from a CI (Shepherd and Hardie, 2001). That said, histopathological studies from post-UVL patients have suggested there is minimal nerve degeneration in these patients (Chen et al., 1988).

Here, we have used normally hearing guinea pigs as an experimental model to explore, from a first order perspective, the morphological and functional changes that occur months after vestibular labyrinthectomy, and to determine if it decreases the efficacy of a CI. The above mentioned clinical studies examining the outcomes of CI in a small number of post-labyrinthectomy patients lend the strongest level of support to the clinical decision to implant a post-UVL patient, whilst only providing results in a limited number of patients. Our experimental study here is designed to provide additional laboratory-based support to the clinical decision making process in this patient subgroup.