The cellular response to cochlear implants, a study in a person undergoing implant replacement

Abstract

Aim: cochlear implantation is a highly successful technology. However, a small but consistent proportion of people do not achieve optimal outcomes. This needs to be addressed. In some cases it appears the tissue response to cochlear implantation is responsible1,2, however this largely remains uncharacterised. We propose a method to study the tissue response to an array in individuals experiencing underperformance or soft failure that require explantation and reimplantation. We aim to determine factors contributing to the tissue response and consequently how well an implant performs. We describe a case study of an electrode migration-related soft failure. Clinical indicators leading to explantation included a decline in hearing performance, rapid changes in impedance and migration of the array. Using this method, we aimed to characterise the tissue composition and cellular environment of the extra-cochlear fibrotic sheath that forms around an array to gain a better understanding of the mechanisms behind soft failures. 
Method: a female was implanted in her 50s due to progressive sensorineural hearing loss over the previous decade. Over 10 months of implantation, she developed non-auditory sensations, poor loudness growth, changes in electrode impedance and required electrodes to be deactivated. Her cochlear implant (CI) performance was lower than expected and the decision was made to remove the device and reimplant a new one resulting in a unique opportunity to characterise the tissue response associated with the soft failure. The array and tissue attached was collected at explantation. The fibrotic sheath was removed, preserving the orientation of the tissue. Histological staining was used to analyse the gross morphology and cellular organisation of the tissue. Immunohistochemistry using a panel of markers was used to investigate the cellular sub-types across the tissue. 
Results: the results indicate ongoing chronic inflammation. There is evidence of growth of new blood vessels and active proliferation across the tissue, with no resolution of the wound healing response. The tissue composition, pattern of collagen deposition and cellularity showed regional differences across the fibrotic tissue. Histological evidence of active inflammation included eosinophils and neutrophils; cells typically involved in the early stages of an acute inflammatory response. Pro- and anti-inflammatory macrophage populations, as well as clusters of T cells were identified across the tissue suggesting a role of the innate and adaptive immune response. Cytokine, interleukin 1 beta (Il-1B), expression provided evidence of pro-inflammatory signalling between immune cells. 
Conclusion: the analysis shows characteristics of unresolved wound healing response despite the time since implantation. This study is the first to characterise the tissue response to a CI array in a user undergoing explantation and reimplantation3. The tissue obtained is from relatively early stages post-implantation (when compared to post-mortem analysis) and close to the time of underperformance or failure - two advantages of this method. The tissue analysis is considered within the context of the users clinical and performance measures, collected across the period of implantation. This is beneficial in understanding factors that contribute to underperformance and soft failure. Detailed cellular and immunological analysis through immunohistochemical investigation of the tissue allows for a fuller understanding of the wound healing response to cochlear implantation. Characterising the tissue response on explanted devices, from multiple individuals, would further our understanding of the factors contributing to the tissue response and its association with performance outcomes. References 1.Nadol, J. B., Eddington, D. K. & Burgess, B. J. Foreign body or hypersensitivity granuloma of the inner ear after cochlear implantation: one possible cause of a soft failure? Otol. Neurotol. 29, 1076–1084 (2008).2.Seyyedi, M. & Nadol, J. B. Intracochlear inflammatory response to cochlear implant electrodes in humans. Otol. Neurotol. 35, 1545–1551 (2014).3.Hough, K. et al. Inflammation at the tissue-electrode interface in a case of rapid deterioration in hearing performance leading to explant after cochlear implantation. Otol. Neurotol. 42, e445–e450 (2021).

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Identifiers

ORCID for Kate Hough: orcid.org/0000-0002-5160-2517

ORCID for Tracey Newman: orcid.org/0000-0002-3727-9258

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