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Access and Polarization Electrode Impedance Changes in Electric-Acoustic Stimulation Cochlear Implant Users with Delayed Loss of Acoustic Hearing

Abstract

Acoustic hearing can be preserved after cochlear implant (CI) surgery, allowing for combined electric-acoustic stimulation (EAS) and superior speech understanding compared to electric-only hearing. Among patients who initially retain useful acoustic hearing, 30–40 % experience a delayed hearing loss that occurs 3 or more months after CI activation. Increases in electrode impedances have been associated with delayed loss of residual acoustic hearing, suggesting a possible role of intracochlear inflammation/fibrosis as reported by Scheperle et al. (Hear Res 350:45–57, 2017) and Shaul et al. (Otol Neurotol 40(5):e518–e526, 2019). These studies measured only total impedance. Total impedance consists of a composite of access resistance, which reflects resistance of the intracochlear environment, and polarization impedance, which reflects resistive and capacitive properties of the electrode–electrolyte interface as described by Dymond (IEEE Trans Biomed Eng 23(4):274–280, 1976) and Tykocinski et al. (Otol Neurotol 26(5):948–956, 2005). To explore the role of access and polarization impedance components in loss of residual acoustic hearing, these measures were collected from Nucleus EAS CI users with stable acoustic hearing and subsequent precipitous loss of hearing. For the hearing loss group, total impedance and access resistance increased over time while polarization impedance remained stable. For the stable hearing group, total impedance and access resistance were stable while polarization impedance declined. Increased access resistance rather than polarization impedance appears to drive the increase in total impedances seen with loss of hearing. Moreover, access resistance has been correlated with intracochlear fibrosis/inflammation in animal studies as observed by Xu et al. (Hear Res 105(1–2):1–29, 1997) and Tykocinski et al. (Hear Res 159(1–2):53–68, 2001). These findings thus support intracochlear inflammation as one contributor to loss of acoustic hearing in our EAS CI population.

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References

  1. Abbas PJ, Tejani VD, Scheperle RA, Brown CJ (2017) Using neural response telemetry to monitor physiological responses to acoustic stimulation in hybrid cochlear implant users. Ear Hear 38(4):409–425. https://doi.org/10.1097/AUD.0000000000000400

    Article  PubMed  PubMed Central  Google Scholar 

  2. Adunka O, Gstoettner W, Hambek M, Unkelbach MH, Radeloff A, Kiefer J (2004) Preservation of basal inner ear structures in cochlear implantation. ORL J Otorhinolaryngol Relat Spec 66(6):306–312. https://doi.org/10.1159/000081887

    Article  PubMed  Google Scholar 

  3. Adunka OF, Pillsbury HC, Buchman CA (2010) Minimizing intracochlear trauma during cochlear implantation. Adv Otorhinolaryngol 67:96–107. https://doi.org/10.1159/000262601

    Article  PubMed  Google Scholar 

  4. Bester C., Razmovski T, Collins A., Mejia O, Foghsgaard S, Mitchell-Innes A., Shaul C, Campbell L, Eastwood H, O’Leary S (2020). Four-point impedance as a biomarker for bleeding during cochlear implantation. Sci Rep 10, 2777. https://doi.org/10.1038/s41598-019-56253-w

  5. Briggs Robert, O’Leary Stephen, Birman Catherine, Plant Kerrie, English Ruth, Dawson Pamela, Risi Frank, Gavrilis Jason, Needham Karina, Cowan Robert (2020) Comparison of electrode impedance measures between a dexamethasone-eluting and standard CochlearTM Contour Advance® electrode in adult cochlear implant recipients. Hear Res 390:107924. https://doi.org/10.1016/j.heares.2020.107924

  6. Brockmeier SJ, Peterreins M, Lorens A, Vermeire K, Helbig S, Anderson I, Skarzynski H, Van de Heyning P, Gstoettner W, Kiefer J (2010) Music perception in electric acoustic stimulation users as assessed by the Mu.S.I.C. test. Adv Otorhinolaryngol 67:70–80. https://doi.org/10.1159/000262598

    CAS  Article  PubMed  Google Scholar 

  7. Brown CJ, Abbas PJ, Gantz BJ (1998) Preliminary experience with neural response telemetry in the nucleus CI24M cochlear implant. Am J Otol 19:320–327

    CAS  PubMed  Google Scholar 

  8. Busby PA, Plant KL, Whitford LA (2002) Electrode impedance in adults and children using the Nucleus 24 cochlear implant system. Cochlear Implants Int 3(2):87–103. https://doi.org/10.1179/cim.2002.3.2.87

    CAS  Article  PubMed  Google Scholar 

  9. Choi CH, Oghalai JS (2005) Predicting the effect of post-implant cochlear fibrosis on residual hearing. Hear Res 205(1–2):193–200. https://doi.org/10.1016/j.heares.2005.03.018

    Article  PubMed  PubMed Central  Google Scholar 

  10. Choi J, Payne MR, Campbell LJ, Bester CW, Newbold C, Eastwood H, O’Leary SJ (2017) Electrode impedance fluctuations as a biomarker for inner ear pathology after cochlear implantation. Otol Neurotol 38(10):1433–1439. https://doi.org/10.1097/mao.0000000000001589

    Article  PubMed  Google Scholar 

  11. Di Lella FA, Parreño M, Fernandez F, Boccio CM, Ausili SA (2020) Measuring the electrical status of the bionic ear. Re-thinking the impedance in cochlear implants. Front Bioeng Biotechnol 8:568690. https://doi.org/10.3389/fbioe.2020.568690

  12. Dorman MF, Smith LM, Dankowski K, McCandless G, Parkin JL (1992) Long-term measures of electrode impedance and auditory thresholds for the Ineraid cochlear implant. J Speech Hear Res 35(5):1126–1130. https://doi.org/10.1044/jshr.3505.1126

    CAS  Article  PubMed  Google Scholar 

  13. Dunn CC, Perreau A, Gantz B, Tyler RS (2010) Benefits of localization and speech perception with multiple noise sources in listeners with a short-electrode cochlear implant. J Am Acad Audiol 21(1):44–51. https://doi.org/10.3766/jaaa.21.1.6

    Article  PubMed  PubMed Central  Google Scholar 

  14. Dunn CC, Etler C, Hansen MR, Gantz BJ (2015) Successful hearing preservation after reimplantation of a failed hybrid cochlear implant. Otol Neurotol 36(10):1628–1632. https://doi.org/10.1097/MAO.0000000000000867

    Article  PubMed  PubMed Central  Google Scholar 

  15. Dunn CC, Oleson J, Parkinson A, Hansen MR, Gantz BJ (2020) Nucleus Hybrid S12: multicenter clinical trial results. Laryngoscope 130(10):E548–E558. https://doi.org/10.1002/lary.28628

    Article  PubMed  PubMed Central  Google Scholar 

  16. Dymond AM (1976) Characteristics of the metal-tissue interface of stimulation electrodes. IEEE Trans Biomed Eng 23(4):274–280. https://doi.org/10.1109/tbme.1976.324585

    CAS  Article  PubMed  Google Scholar 

  17. Fontenot TE, Giardina CK, Dillon MT, Rooth MA, Teagle HF, Park LR, Brown KD, Adunka OF, Buchman CA, Pillsbury HC, Fitzpatrick DC (2019) Residual Cochlear Function in Adults and Children Receiving Cochlear Implants: Correlations With Speech Perception Outcomes. Ear & Hearing 40(3):577–591. https://doi.org/10.1097/AUD.0000000000000630

  18. Gantz BJ, Dunn CC, Oleson J, Hansen MR, Parkinson A, Turner C (2016) Multicenter clinical trial of the Nucleus Hybrid S8 cochlear implant: final outcomes. Laryngoscope 126:962–973. https://doi.org/10.1002/lary.25572

    Article  PubMed  PubMed Central  Google Scholar 

  19. Gantz BJ, Dunn CC, Oleson J, Hansen MR (2018) Acoustic plus electric speech processing: long-term results. Laryngoscope 128(2):473–481. https://doi.org/10.1002/lary.26669

    Article  PubMed  Google Scholar 

  20. Gfeller KE, Olszewski C, Turner C, Gantz B, Oleson J (2006) Music perception with cochlear implants and residual hearing. Audiol Neurootol 11(Suppl 1):12–15. https://doi.org/10.1159/000095608

    Article  PubMed  Google Scholar 

  21. Giardina CK, Krause ES, Koka K, Fitzpatrick DC (2018) Impedance measures during in vitro cochlear implantation predict array positioning. IEEE Trans Biomed Eng 65(2):327–335. https://doi.org/10.1109/TBME.2017.2764881

    Article  PubMed  PubMed Central  Google Scholar 

  22. Gifford RH, Dorman MF, Spahr AJ, Bacon SP, Skarzynski H, Lorens A (2008) Hearing preservation surgery: psychophysical estimates of cochlear damage in recipients of a short electrode array. J Acoust Soc Am 124(4):2164–2173. https://doi.org/10.1121/1.2967842

    Article  PubMed  PubMed Central  Google Scholar 

  23. Gifford RH, Dorman MF, Brown CA (2010) Psychophysical properties of low-frequency hearing: implications for perceiving speech and music via electric and acoustic stimulation. Adv Otorhinolaryngol 67:51–60. https://doi.org/10.1159/000262596

    Article  PubMed  Google Scholar 

  24. Helbig S, Van de Heyning P, Kiefer J, Baumann U, Kleine-Punte A, Brockmeier H, Anderson I, Gstoettner W (2011) Combined electric acoustic stimulation with the PULSARCI100 implant system using the FLEXEAS electrode array. Acta Otolaryngol 131(6):585–595. https://doi.org/10.3109/00016489.2010.544327

    Article  PubMed  Google Scholar 

  25. Huang CQ, Tykocinski M, Stathopoulos D, Cowan R (2007). Effects of steroids and lubricants on electrical impedance and tissue response following cochlear implantation. Cochlear Implants Int. 8(3):123-147. https://doi.org/10.1179/cim.2007.8.3.123

  26. Hughes ML, Vander Werff KR, Brown CJ, Abbas PJ, Kelsay DM, Teagle HF, Lowder MW (2001) A longitudinal study of electrode impedance, the electrically evoked compound action potential, and behavioral measures in Nucleus 24 cochlear implant users. Ear Hear 22(6):471–486. https://doi.org/10.1097/00003446-200112000-00004

    CAS  Article  PubMed  Google Scholar 

  27. Hunter JB, Gifford RH, Wanna GB, Labadie RF, Bennett ML, Haynes DS, Rivas A. Hearing Preservation Outcomes With a Mid-Scala Electrode in Cochlear Implantation (2016). Otol Neurotol. 37(3):235-240. https://doi.org/10.1097/mao.0000000000000963

    Article  Google Scholar 

  28. Klabbers TM, Huinck WJ, Heutink F, Verbist BM, Mylanus E (2021) Transimpedance matrix (TIM) measurement for the detection of intraoperative electrode tip foldover using the slim modiolar electrode: a proof of concept study. Otol Neurotol 42(2):e124–e129. https://doi.org/10.1097/MAO.0000000000002875

    Article  PubMed  Google Scholar 

  29. Konrad S, Framke T, Kludt E, Büchner A, Lenarz T, Paasche G (2020). Ear Hear. (Online ahead of print). https://doi.org/10.1097/aud.0000000000000914

  30. Kopelovich JC, Reiss LA, Etler CP, Xu L, Bertroche JT, Gantz BJ, Hansen MR (2015) Hearing loss after activation of hearing preservation cochlear implants might be related to afferent cochlear innervation injury. Otol Neurotol 36(6):1035–1044. https://doi.org/10.1097/MAO.0000000000000754

    Article  PubMed  PubMed Central  Google Scholar 

  31. Lenarz T, James C, Cuda D, Fitzgerald O’Connor A, Frachet B, Frijns JH, Klenzner T, Laszig R, Manrique M, Marx M, Merkus P, Mylanus EA, Offeciers E, Pesch J, Ramos-Macias A, Robier A, Sterkers O, Uziel A (2013) European multi-centre study of the Nucleus Hybrid L24 cochlear implant. Int J Audiol 52(12):838–848. https://doi.org/10.3109/14992027.2013.802032

    Article  PubMed  Google Scholar 

  32. Lenarz T, Buechner A, Lesinski-Schiedat A, Timm M, Salcher R (2020) Hearing preservation with a new atraumatic lateral wall electrode. Otol Neurotol 41(8):e993–e1003. https://doi.org/10.1097/mao.0000000000002714

    Article  PubMed  Google Scholar 

  33. Li Q, Lu T, Zhang C, Hansen MR, Li S (2020) Electrical stimulation induces synaptic changes in the peripheral auditory system. J Comp Neurol 528(6):893–905. https://doi.org/10.1002/cne.24802

    Article  PubMed  Google Scholar 

  34. Mesnildrey Q, Macherey O, Herzog P, Venail F (2019) Impedance measures for a better understanding of the electrical stimulation of the inner ear. J Neural Eng 16(1):016023. https://doi.org/10.1088/1741-2552/aaecff

    Article  PubMed  Google Scholar 

  35. Newbold C, Mergen S, Richardson R, Seligman P, Millard R, Cowan R, Shepherd R (2014) Impedance changes in chronically implanted and stimulated cochlear implant electrodes. Cochlear Implants Int 15(4):191–199. https://doi.org/10.1179/1754762813y.0000000050

    Article  PubMed  Google Scholar 

  36. O’Leary SJ, Monksfield P, Kel G, Connolly T, Souter MA, Chang A, Marovic P, O’Leary JS, Richardson R, Eastwood H (2013) Relations between cochlear histopathology and hearing loss in experimental cochlear implantation. Hear Res 298:27–35. https://doi.org/10.1016/j.heares.2013.01.012

    CAS  Article  PubMed  Google Scholar 

  37. Parreño M, Di Lella FA, Fernandez F, Boccio CM, Ausili SA (2020). Toward Self-Measures in Cochlear Implants: Daily and “Homemade” Impedance Assessment. Front Digit Health 2:582562. https://doi.org/10.3389/fdgth.2020.582562

  38. Pillsbury HC 3rd, Dillon MT, Buchman CA, Staecker H, Prentiss SM, Ruckenstein MJ, Bigelow DC, Telischi FF, Martinez DM, Runge CL, Friedland DR, Blevins NH, Larky JB, Alexiades G, Kaylie DM, Roland PS, Miyamoto RT, Backous DD, Warren FM, El-Kashlan HK, Slager HK, Reyes C, Racey AI, Adunka OF (2018) Multicenter US clinical trial with an electric-acoustic stimulation (EAS) system in adults: final outcomes. Otol Neurotol 39(3):299–305. https://doi.org/10.1097/MAO.0000000000001691

    Article  PubMed  PubMed Central  Google Scholar 

  39. Quesnel AM, Nakajima HH, Rosowski JJ, Hansen MR, Gantz BJ, Nadol JB Jr (2016) Delayed loss of hearing after hearing preservation cochlear implantation: human temporal bone pathology and implications for etiology. Hear Res 333:225–234. https://doi.org/10.1016/j.heares.2015.08.018

    Article  PubMed  Google Scholar 

  40. Rauch SD, Halpin CF, Antonelli PJ, Babu S, Carey JP, Gantz BJ, Goebel JA, Hammerschlag PE, Harris JP, Isaacson B, Lee D, Linstrom CJ, Parnes LS, Shi H, Slattery WH, Telian SA, Vrabec JT, Reda DJ (2011) Oral vs intratympanic corticosteroid therapy for idiopathic sudden sensorineural hearing loss: a randomized trial. JAMA 305(20):2071–2079. https://doi.org/10.1001/jama.2011.679

    CAS  Article  PubMed  Google Scholar 

  41. Reiss LA, Stark G, Nguyen-Huynh AT, Spear KA, Zhang H, Tanaka C, Li H (2015) Morphological correlates of hearing loss after cochlear implantation and electro-acoustic stimulation in a hearing-impaired guinea pig model. Hear Res 327:163–174. https://doi.org/10.1016/j.heares.2015.06.007

    Article  PubMed  PubMed Central  Google Scholar 

  42. Roland JT Jr, Gantz BJ, Waltzman SB, Parkinson AJ (2018) Long-term outcomes of cochlear implantation in patients with high-frequency hearing loss. Laryngoscope 128(8):1939–1945. https://doi.org/10.1002/lary.27073

    Article  PubMed  PubMed Central  Google Scholar 

  43. Roland JT Jr, Gantz BJ, Waltzman SB, Parkinson AJ, Multicenter Clinical Trial Group (2016) United States multicenter clinical trial of the Cochlear Nucleus hybrid implant system. Laryngoscope 126(1):175–181. https://doi.org/10.1002/lary.25451

    Article  Google Scholar 

  44. Sainz M, Roldan C, de la Torre A, Gonzalez M, Ruiz J (2003) Transitory alterations of the electrode impedances in cochlear implants associated to middle and inner ear diseases. Int Congr Ser 1240:407–410. https://doi.org/10.1016/S0531-5131(03)00774-X

  45. Scheperle RA, Tejani VD, Omtvedt JK, Brown CJ, Abbas PJ, Hansen MR, Gantz BJ, Oleson JJ, Ozanne MV (2017) Delayed changes in auditory status in cochlear implant users with preserved acoustic hearing. Hear Res 350:45–57. https://doi.org/10.1016/j.heares.2017.04.005

    Article  PubMed  PubMed Central  Google Scholar 

  46. Shaul C, Bester CW, Weder S, Choi J, Eastwood H, Padmavathi KV, Collins A, O’Leary SJ (2019) Electrical impedance as a biomarker for inner ear pathology following lateral wall and peri-modiolar cochlear implantation. Otol Neurotol 40(5):e518–e526. https://doi.org/10.1097/mao.0000000000002227

    Article  PubMed  Google Scholar 

  47. Tanaka C, Nguyen-Huynh A, Loera K, Stark G, Reiss L (2014) Factors associated with hearing loss in a normal-hearing guinea pig model of Hybrid cochlear implants. Hear Res 316:82–93. https://doi.org/10.1016/j.heares.2014.07.011

    Article  PubMed  PubMed Central  Google Scholar 

  48. Tejani VD, Brown CB (2020) Speech masking release in Hybrid cochlear implant users: roles of spectral and temporal cues in electric-acoustic hearing. J Acoust Soc Am 147(5):3667–3683. https://doi.org/10.1121/10.0001304

    Article  PubMed  PubMed Central  Google Scholar 

  49. Tejani VD, Kim JS, Oleson JJ, Abbas PJ, Brown CJ, Hansen MR, Gantz BJ (2021). Residual hair cell responses in electric-acoustic stimulation cochlear implant users with complete loss of acoustic hearing post-implant. J Assoc Res Otolaryngol. 22(2):161-176. https://doi.org/10.1007/s10162-021-00785-4

  50. Thompson NJ, Dillon MT, Buss E, Park LR, Pillsbury HC 3rd, O’Connell BP, Brown KD (2020) Electrode array type and its impact on impedance fluctuations and loss of residual hearing in cochlear implantation. Otol Neurotol 41(2):186–191. https://doi.org/10.1097/mao.0000000000002457

    Article  PubMed  Google Scholar 

  51. Turner CW (2006) Hearing loss and the limits of amplification. Audiol Neurootol 11(Suppl 1):2–5. https://doi.org/10.1159/000095606

    Article  PubMed  Google Scholar 

  52. Turner CW, Gantz BJ, Vidal C, Behrens A, Henry BA (2004) Speech recognition in noise for cochlear implant listeners: benefits of residual acoustic hearing. J Acoust Soc Am 115(4):1729–1735. https://doi.org/10.1121/1.1687425

    Article  PubMed  Google Scholar 

  53. Tykocinski M, Duan Y, Tabor B, Cowan RS (2001) Chronic electrical stimulation of the auditory nerve using high surface area (HiQ) platinum electrodes. Hear Res 159(1–2):53–68. https://doi.org/10.1016/s0378-5955(01)00320-3

    CAS  Article  PubMed  Google Scholar 

  54. Tykocinski M, Cohen LT, Cowan RS (2005) Measurement and analysis of access resistance and polarization impedance in cochlear implant recipients. Otol Neurotol 26(5):948–956. https://doi.org/10.1097/01.mao.0000185056.99888.f3

    Article  PubMed  Google Scholar 

  55. Van Abel KM, Dunn CC, Sladen DP, Oleson JJ, Beatty CW, Neff BA, Hansen M, Gantz BJ, Driscoll CL (2015) Hearing preservation among patients undergoing cochlear implantation. Otol Neurotol 36(3):416–421. https://doi.org/10.1097/mao.0000000000000703

    Article  PubMed  PubMed Central  Google Scholar 

  56. Vanpoucke FJ, Zarowski AJ, Peeters SA (2004) Identification of the impedance model of an implanted cochlear prosthesis from intracochlear potential measurements. IEEE Trans Biomed Eng 51(12):2174–2183. https://doi.org/10.1109/tbme.2004.836518

    Article  PubMed  Google Scholar 

  57. Wilk M, Hessler R, Mugridge K, Jolly C, Fehr M, Lenarz T, Scheper V. (2016). Impedance Changes and Fibrous Tissue Growth after Cochlear Implantation Are Correlated and Can Be Reduced Using a Dexamethasone Eluting Electrode. PLoS One. 2016;11(2):e0147552. https://doi.org/10.1371/journal.pone.0147552

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  58. Xu J, Shepherd RK, Millard RE, Clark GM (1997) Chronic electrical stimulation of the auditory nerve at high stimulus rates: a physiological and histopathological study. Hear Res 105(1–2):1–29. https://doi.org/10.1016/s0378-5955(96)00193-1

    CAS  Article  PubMed  Google Scholar 

  59. Zierhofer CM, Hochmair IJ, Hochmair ES (1997) The advanced Combi 40+ cochlear implant. Am J Otol 18(6 Suppl):S37–S38

    CAS  PubMed  Google Scholar 

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Acknowledgements

Electrode Voltage Telemetry research software was provided by Cochlear Ltd. Linjie Shu, Alexandra Watts, and Sushun (Albert) Zhang assisted in compiling the dataset. Audiologists on the University of Iowa Cochlear Implant team contributed audiometric and clinical impedance datasets, provided expert care for our cochlear implant patients, and shared valuable insights regarding impedance fluctuations and relevant clinical pathologies in our EAS population.

Funding

This study was funded by National Institutes of Health/National Institute on Deafness and Other Communicative Disorders P50 DC 00242 (PI: Gantz).

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Correspondence to Viral D. Tejani.

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BJG is a consultant for Cochlear Ltd. MRH is co-founder and Chief Medical Officer for iotaMotion, Inc. VDT is a consultant for iotaMotion, Inc. All other authors declare that they have no conflict of interest.

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Tejani, V.D., Yang, H., Kim, JS. et al. Access and Polarization Electrode Impedance Changes in Electric-Acoustic Stimulation Cochlear Implant Users with Delayed Loss of Acoustic Hearing. JARO (2021). https://doi.org/10.1007/s10162-021-00809-z

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Keywords

  • impedance
  • polarization impedance
  • access resistance
  • hearing preservation
  • electric-acoustic stimulation
  • Hybrid