Edited by: Mikhail Lebedev, Duke University, USA
Reviewed by: Silvestro Micera, Sant’Anna School of Advanced Studies, Italy; Enrique Soto, Universidad Autónoma de Puebla, Mexico; Timothy G. Constandinou, Imperial College London, UK
Specialty section: This article was submitted to Neuroprosthetics, a section of the journal Frontiers in Neurology
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The vestibular implant seems feasible as a clinically useful device in the near future. However, hearing preservation during intralabyrinthine implantation remains a challenge. It should be preserved to be able to treat patients with bilateral vestibulopathy and (partially) intact hearing. This case study investigated the feasibility of hearing preservation during the acute phase after electrode insertion in the semicircular canals.
A 40-year-old woman with normal hearing underwent a translabyrinthine approach for a vestibular schwannoma Koos Grade IV. Hearing was monitored using auditory brainstem response audiometry (ABR). ABR signals were recorded synchronously to video recordings of the surgery. Following the principles of soft surgery, a conventional dummy electrode was inserted in the lateral semicircular canal for several minutes and subsequently removed. The same procedure was then applied for the posterior canal. Finally, the labyrinthectomy was completed, and the schwannoma was removed.
Surgery was performed without complications. No leakage of endolymph and no significant reduction of ABR response were observed during insertion and after removal of the electrodes from the semicircular canals, indicting no damage to the peripheral auditory function. The ABR response significantly changed when the semicircular canals were completely opened during the labyrinthectomy. This was indicated by a change in the morphology and latency of peak V of the ABR signal.
Electrode insertion in the semicircular canals is possible without acutely damaging the peripheral auditory function measured with ABR, as shown in this proof-of-principle clinical investigation.
Bilateral vestibulopathy is the disease resulting in a reduced or absent function of the vestibular organs, the vestibular nerves, or a combination of both (
This implant, in a concept analogous to the cochlear implant, captures motion and processes this information into an electrical stimulus that is delivered by electrodes to the vestibular nerves (
At this moment, two surgical strategies have been described: the intralabyrinthine approach (
A 40-year-old woman who had to undergo a planned partial resection followed by radiosurgery of a vestibular schwannoma Koos Grade IV on her right side was selected. She still had normal hearing, with a Pure Tone Average tone threshold (averaged over 1,000, 2,000, and 4,000 Hz) of 10 dB on the right side and 5 dB on the left side (Figure
Functionality of the cochleovestibular neuronal pathways was peroperatively monitored by ABR (
Video recordings of the surgery and of the ABR signals were made by capturing the images of the surgical microscope and the images of the computer screen of the ABR equipment. The recordings of the surgery and the ABR signals were synchronized.
Surgery involved a routine translabyrinthine approach. However, after the mastoidectomy and identifying the semicircular canals, the labyrinth was not immediately opened, and the additional study procedure started. This procedure involved the following steps. First, the lateral semicircular canal (LSCC) and posterior semicircular canal (PSCC) were bluelined, and the peripheral auditory function was monitored. Second, the LSCC was opened first, without disrupting the membranous labyrinth, and the peripheral auditory function was monitored again. Third, a conventional dummy electrode (made of silicone, with a diameter of 0.4 mm apical and 0.6 mm basal) was inserted in the LSCC approximately up to the cupula, and the peripheral auditory function was monitored. Following the principles of soft tissue surgery, the insertion was performed extra slowly to avoid strong hydraulic forces that could be transmitted throughout the inner ear. The electrode was inserted until a resistance was met, and from insertion depth it was deduced that the tip of the electrode was adjacent to the ampulla (Figure
Time | |
---|---|
End of bluelining semicircular canals | 0:00 |
Auditory brainstem response audiometry (ABR) | 0:59 |
Lateral semicircular canal (LSCC) opened | 5:00 |
ABR | 5:53 |
LSCC electrode inserted | 8:25 |
ABR | 9:33 |
ABR | 11:42 |
LSCC electrode taken out | 12:19 |
ABR | 14:13 |
Posterior semicircular canal (PSCC) opened | 15:42 |
ABR | 16:31 |
PSCC electrode inserted | 18:29 |
ABR | 19:25 |
PSCC electrode taken out | 19:44 |
ABR | 20:52 |
All 3 semicircular canals completely opened | 24:20 |
ABR | 25:19 |
Vestibulum opened | 30:04 |
ABR | 30:59 |
ABR | 32:12 |
ABR | 33:48 |
ABR | 34:40 |
The synchronized ABR video recordings of the surgery were analyzed in consensus by three authors (Erwin George, Raymond van de Berg, and Joost van Tongeren). Regarding surgery, special attention was paid to the observation of damage to the membranous labyrinth and leakage of endolymph.
All surgical steps of the study procedure and removal of the vestibular schwannoma were performed without complications. When opening the LSCC and PSCC, the membranous labyrinth was not disrupted at the point of fenestration. After insertion of the electrode and taking it out again, damage to the membranous labyrinth was observed in the lateral as well as the PSCC. However, no leakage of endolymph was observed, until the semicircular canals were opened completely as a part of the translabyrinthine surgery of the schwannoma.
Auditory brainstem response audiometry results showed a stable morphology and a consistent peak V during the first 11 min after opening the LSCC. That is, the functional status of the cochleovestibular pathway appeared to be stable even after the LSCC was opened and after the electrode was inserted and removed. After opening the PSCC, peak V was still clearly present but it was delayed approximately 0.5 ms compared to baseline. ABR morphology, however, remained normal, and peak V remained present during opening of the PSCC and during insertion and removal of the electrode. Even after completely opening all three semicircular canals, ABR results appeared stable, with still a clearly visible peak V. However, after opening the vestibulum, ABR no longer showed any identifiable peaks, implying that functional hearing was clearly distorted. A largely delayed peak V seemed to return at a later moment, but morphology of the ABR signal and thus functional hearing still appeared to be compromised at this stage of surgery (Figure
The objective of this case study was to evaluate whether hearing can be preserved during the acute phase after electrode insertion in semicircular canals. It was shown that intralabyrinthine electrode insertion is possible without inducing significant damage to the peripheral auditory function measured by ABR, in the first half hour after opening the labyrinth and subsequent electrode insertion and removal. This is congruent with the experience in other intralabyrinthine surgeries such as semicircular canal plugging for intractable benign paroxysmal positional vertigo or superior canal dehiscence syndrome, in which hearing is often preserved (
Major difference between electrodes in this study and “plugs” in previous studies is the fact that electrodes do not immediately close the whole semicircular canal and that they might penetrate the membranous labyrinth. This is important, since leakage of endolymph and perilymph is generally believed to induce loss of cochlear and vestibular function (
However, in another research group, previous vestibular implantations with electrodes designed to be selectively inserted in the perilymphatic space of the semicircular canals, resulted in hearing loss in all four Meniere’s patients following the implantations. Taken this into account, probably multiple factors could influence hearing during intralabyrinthine surgery. First, regarding the leakage of endolymph, patients with a hydrops (such as Meniere’s patients) or a gusher could be more susceptible to hearing loss (
Most of the abovementioned factors remain still partially speculative. Therefore, it should still be investigated which factors contribute to which extent to the occurrence of hearing loss during the acute phase of intralabyrinthine surgery. Until then, it could be advised to use “soft surgical” skills like preservation of the membranous labyrinth as long as possible, slow insertion of the electrodes, and avoiding suction directly on the perilymph or membranous labyrinth. Furthermore, it could be considered to open the labyrinth more far away from the ampulla and to not yet select patients with a suspicion of endolymphatic hydrops or gusher. In these cases, an extralabyrinthine approach might at this point be the safest procedure, since the labyrinth is not opened. Ideally, vestibular implantation surgery should be standardized. This would imply a safe surgical procedure and an optimal electrode design that complement each other, while both taking into account anatomical variabilities. At this moment, no optimal surgical procedure and electrode design are present yet (
Regarding monitoring of hearing, the use of other (complementary) techniques could be considered like electrocochleography, or directly recorded cochlear nerve action potentials, in order to improve specificity. This, since ABR measurements are highly sensitive in detecting auditory damage, but specificity is poor (
Previous unsuccessful attempts for hearing preservation during vestibular implant (
Finally, after a protocol for hearing preservation in the acute stage of intralabyrinthine insertion is established, the long-term effects should still be investigated. For example, delayed neo-osteogenesis, reactive fibrous tissue formation around the array, and delayed inner ear toxicity (blood, irrigation fluids, and device material) might all appear and could lead to delayed hearing loss (
Due to obvious ethical limitations, the time for the study procedure was limited. This resulted in two main limitations. First, not all semicircular canals were inserted with an electrode. At this moment, intralabyrinthine vestibular implants in humans consist of three electrode branches that are inserted in each semicircular canal (
Electrode insertion in the semicircular canals is possible without acutely damaging the peripheral auditory function as measured with ABR and shown in this proof-of-principle clinical investigation.
The procedures in this investigation were in accordance with the legislation and ethical standards on human experimentation in the Netherlands and in accordance with the Declaration of Helsinki (amended version 2013). Approval was obtained from the ethical committee of Maastricht University Medical Center (NL54761.068.15/METC162006). All procedures were performed at Maastricht University Medical Center.
All authors contributed extensively to the work presented in this paper. JT, RS, and YT were the surgeons in this case. EG analyzed the ABR measurements. RB wrote the manuscript. FL created and edited the figures of the manuscript. FL, NG, JT, EG, J-PG, HK, MH, YT, JO, AP-F, and RS reviewed the manuscript and edited the manuscript.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The authors would like to thank Yvonne Extra and Afra Bruinen from the Audiological Center of MUMC+ for performing the ABR measurements.
Med-El has provided the VCI-device and funding for research (not presented here).