The modified ampullar approach for vestibular implant surgery: feasibility and its first application in a human with a long-term vestibular loss

Raymond van de Berg, Nils Guinand, Jean-Philippe Guyot, Herman Kingma, Robert J Stokroos, Raymond van de Berg, Nils Guinand, Jean-Philippe Guyot, Herman Kingma, Robert J Stokroos

Abstract

Objective: To assess, for the first time in a human with a long-term vestibular loss, a modified approach to the ampullae and the feasibility of evoking a VOR by ampullar stimulation.

Materials and methods: Peroperative stimulation of the ampullae, using the ampullar approach, was performed under full anesthesia during cochlear implantation in a 21-year-old female patient, who had experienced bilateral vestibular areflexia and sensorineural hearing loss for almost 20 years.

Results: The modified ampullar approach was performed successfully with as minimally invasive surgery as possible. Ampullar stimulation evoked eye movements containing vectors congruent with the stimulated canal. As expected, the preliminary electrophysiological data were influenced by the general anesthesia, which resulted in current spread and reduced maximum amplitudes of eye movement. Nevertheless, they confirm the feasibility of ampullar stimulation.

Conclusion: The modified ampullar approach provides safe access to the ampullae using as minimally invasive surgery as possible. For the first time in a human with long-term bilateral vestibular areflexia, it is shown that the VOR can be evoked by ampullar stimulation, even when there has been no vestibular function for almost 20 years. This approach should be considered in vestibular surgery, as it provides safe access to one of the most favorable stimulus locations for development of a vestibular implant.

Keywords: acclimation; adaptation; ampullar approach; bilateral vestibular areflexia; bilateral vestibulopathy; neural prosthesis; vestibular implant; vestibular prosthesis.

Figures

Figure 1
Figure 1
Lateral view of a right temporal bone. It shows the superior canal (SC), lateral canal (LC), and posterior canal (PC) which are fenestrated near the ampullary ends and marked with inserted plastic wires. Line X is the imaginary line through the stapes footplate, which indicates the location of the posterior ampulla, medial to the facial nerve.
Figure 2
Figure 2
Anterolateral view of a right temporal bone using cone beam CT-scan. It shows the fenestration and insertion of the cochleovestibular electrodes in the superior ampulla (SA), lateral ampulla (LA), and cochlea (C).
Figure 3
Figure 3
Anterolateral view of a right temporal bone using cone beam CT-scan. It shows the fenestration and insertion of the electrode (*) in the posterior ampulla (PA). (LC = lateral canal).
Figure 4
Figure 4
Maximum vertical and horizontal amplitudes of the eye during ampullar nerve stimulation of each canal.
Figure 5
Figure 5
(A) VOR vertical component during suprathreshold stimulation of the SAN. Vertical bars indicate the start and end of stimulation. (B) VOR horizontal component during suprathreshold stimulation of the SAN. Vertical bars indicate the start and end of stimulation.

References

    1. Cass S. P., Davidson P., Goshgarian H. (1989). Survival of the vestibular nerve after labyrinthectomy in the cat. Otolaryngol. Head Neck Surg. 101, 459–465
    1. Dai C., Fridman G. Y., Chiang B., Davidovics N. S., Melvin T. A., Cullen K. E., Della Santina C. C. (2011). Cross-axis adaptation improves 3D vestibulo-ocular reflex alignment during chronic stimulation via a head-mounted multichannel vestibular prosthesis. Exp. Brain Res. 210, 595–60610.1007/s00221-011-2591-5
    1. Dai C., Fridman G. Y., Della Santina C. C. (2010). Effects of vestibular prosthesis electrode implantation and stimulation on hearing in rhesus monkeys. Hear. Res. 277, 204–21010.1016/j.heares.2010.12.021
    1. Davidovics N. S., Fridman G. Y., Chiang B., Della Santina C. C. (2011). Effects of biphasic current pulse frequency, amplitude, duration, and interphase gap on eye movement responses to prosthetic electrical stimulation of the vestibular nerve. IEEE Trans. Neural Syst. Rehabil. Eng. 19, 84–9410.1109/TNSRE.2010.2065241
    1. Della Santina C. C., Migliaccio A. A., Patel A. H. (2007). A multichannel semicircular canal neural prosthesis using electrical stimulation to restore 3-D vestibular sensation. IEEE Trans. Biomed. Eng. 54, 1016–103010.1109/TBME.2007.894629
    1. Epley J. M. (1980). Singular neurectomy: hypotympanotomy approach. Otolaryngol. Head Neck Surg. 88, 304–309
    1. Feigl G. C., Fasel J. H., Anderhuber F., Ulz H., Rienmüller R., Guyot J. P., Kos I. M. (2009). Superior vestibular neurectomy: a novel transmeatal approach for a denervation of the superior and lateral semicircular canals. Otol. Neurotol. 30, 586–59110.1097/MAO.0b013e3181ab9164
    1. Fridman G. Y., Davidovics N. S., Dai C., Migliaccio A. A., Della Santina C. C. (2010). Vestibulo-ocular reflex responses to a multichannel vestibular prosthesis incorporating a 3D coordinate transformation for correction of misalignment. J. Assoc. Res. Otolaryngol. 11, 367–38110.1007/s10162-010-0208-5
    1. Gacek R. R. (1974). Transection of the posterior ampullary nerve for the relief of benign paroxysmal positional vertigo. Ann. Otol. Rhinol. Laryngol. 83, 596–605
    1. Gacek R. R., Gacek M. R. (2002). Results of singular neurectomy in the posterior ampullary recess. ORL J. Otorhinolaryngol. Relat. Spec. 64, 397–40210.1159/000067572
    1. Gong W., Haburcakova C., Merfeld D. M. (2008). Vestibulo-ocular responses evoked via bilateral electrical stimulation of the lateral semicircular canals. IEEE Trans. Biomed. Eng. 55, 2608–261910.1109/TBME.2008.2001294
    1. Gong W., Merfeld D. M. (2000). Prototype neural semicircular canal prosthesis using patterned electrical stimulation. Ann. Biomed. Eng. 28, 572–58110.1114/1.293
    1. Gong W., Merfeld D. M. (2002). System design and performance of a unilateral horizontal semicircular canal prosthesis. IEEE Trans. Biomed. Eng. 49, 175–18110.1109/10.979358
    1. Guyot J. P., Sigrist A., Pelizzone M., Feigl G. C., Kos M. I. (2011a). Eye movements in response to electrical stimulation of the lateral and superior ampullary nerves. Ann. Otol. Rhinol. Laryngol. 120, 81–87
    1. Guyot J. P., Sigrist A., Pelizzone M., Kos M. I. (2011b). Adaptation to steady-state electrical stimulation of the vestibular system in humans. Ann. Otol. Rhinol. Laryngol. 120, 143–149
    1. Janssen M., Stokroos R., Aarts J., van Lummel R., Kingma H. (2010). Salient and placebo vibrotactile feedback are equally effective in reducing sway in bilateral vestibular loss patients. Gait Posture 31, 213–21710.1016/j.gaitpost.2009.10.008
    1. Kudo Y., Nomura Y. (1996). The vestibular nerve: its course to the anterior and lateral ampullae. ORL J. Otorhinolaryngol. Relat. Spec. 58, 208–21210.1159/000276838
    1. Lacour M., Dutheil S., Tighilet B., Lopez C., Borel L. (2009). Tell me your vestibular deficit, and i’ll tell you how you’ll compensate. Ann. N. Y. Acad. Sci. 1164, 268–27810.1111/j.1749-6632.2008.03731.x
    1. Leake P. A., Hradek G. T., Snyder R. L. (1999). Chronic electrical stimulation by a cochlear implant promotes survival of spiral ganglion neurons after neonatal deafness. J. Comp. Neurol. 412, 543–56210.1002/(SICI)1096-9861(19991004)412:4<543::AID-CNE1>;2-3
    1. Lewis R. F., Gong W., Ramsey M., Minor L., Boyle R., Merfeld D. M. (2002). Vestibular adaptation studied with a prosthetic semicircular canal. J. Vestib. Res. 12, 87–94
    1. Lewis R. F., Haburcakova C., Gong W., Makary C., Merfeld D. M. (2010). Vestibuloocular reflex adaptation investigated with chronic motion-modulated electrical stimulation of semicircular canal afferents. J. Neurophysiol. 103, 1066–107910.1152/jn.00241.2009
    1. McCall A. A., Ishiyama G. P., Lopez I. A., Bhuta S., Vetter S., Ishiyama A. (2009). Histopathological and ultrastructural analysis of vestibular end organs in Meniere’s disease reveals basement membrane pathology. BMC Ear Nose Throat Disord. 9, 4.10.1186/1472-6815-9-4
    1. Merfeld D. M., Gong W., Morrissey J., Saginaw M., Haburcakova C., Lewis R. F. (2006). Acclimation to chronic constant-rate peripheral stimulation provided by a vestibular prosthesis. IEEE Trans. Biomed. Eng. 53, 2362–237210.1109/TBME.2006.883645
    1. Merfeld D. M., Haburcakova C., Gong W., Lewis R. F. (2007). Chronic vestibulo-ocular reflexes evoked by a vestibular prosthesis. IEEE Trans. Biomed. Eng. 54, 1005–101510.1109/TBME.2007.891943
    1. Nie K., Bierer S. M., Ling L., Oxford T., Rubinstein J. T., Phillips J. O. (2011). Characterization of the electrically evoked compound action potential of the vestibular nerve. Otol. Neurotol. 32, 88–9710.1097/MAO.0b013e3181f6ca45
    1. Parnes L. S., McClure J. A. (1990). Posterior semicircular canal occlusion for intractable benign paroxysmal positional vertigo. Ann. Otol. Rhinol. Laryngol. 99, 330–334
    1. Parnes L. S., McClure J. A. (1991). Posterior semicircular canal occlusion in the normal hearing ear. Otolaryngol. Head Neck Surg. 104, 52–57
    1. Poon C. C., Irwin M. G. (2009). Anaesthesia for deep brain stimulation and in patients with implanted neurostimulator devices. Br. J. Anaesth. 103, 152–16510.1093/bja/aep179
    1. Rauch S. D., Velazquez-Villasenor L., Dimitri P. S., Merchant S. N. (2001). Decreasing hair cell counts in aging humans. Ann. N. Y. Acad. Sci. 942, 220–22710.1111/j.1749-6632.2001.tb03748.x
    1. Rubinstein J. T., Della Santina C. C. (2002). Development of a biophysical model for vestibular prosthesis research. J. Vestib. Res. 12, 69–76
    1. Rubinstein J. T., Phillips J. O., Nie K., Ling L., Bierer S., Golub J. (2011). Feasibility Studies of the UW/Nucleus Vestibular Implant for Meniere’s Disease: First Human Data Collegium Oto-Rhino-Laryngologicum Amicitae Sacrum. Brugge
    1. Schuknecht H. F. (1982). Behavior of the vestibular nerve following labyrinthectomy. Ann. Otol. Rhinol. Laryngol. Suppl. 97, 16–32
    1. Shkel A. M., Zeng F. G. (2006). An electronic prosthesis mimicking the dynamic vestibular function. Audiol. Neurootol. 11, 113–12210.1159/000090684
    1. Tang S., Melvin T. A., Della Santina C. C. (2009). Effects of semicircular canal electrode implantation on hearing in chinchillas. Acta Otolaryngol. 129, 481–48610.1080/00016480802252243
    1. Tsuji K., Velazquez-Villasenor L., Rauch S. D., Glynn R. J., Wall C., III, Merchant S. N. (2000a). Temporal bone studies of the human peripheral vestibular system. Aminoglycoside ototoxicity. Ann. Otol. Rhinol. Laryngol. Suppl. 181, 20–25
    1. Tsuji K., Velazquez-Villasenor L., Rauch S. D., Glynn R. J., Wall C., III, Merchant S. N. (2000b). Temporal bone studies of the human peripheral vestibular system. Meniere’s disease. Ann. Otol. Rhinol. Laryngol. Suppl. 181, 26–31
    1. Velazquez-Villasenor L., Merchant S. N., Tsuji K., Glynn R. J., Wall C., III, Rauch S. D. (2000). Temporal bone studies of the human peripheral vestibular system. Normative Scarpa’s ganglion cell data. Ann. Otol. Rhinol. Laryngol. Suppl. 181, 14–19
    1. Wall C., III, Kos M. I., Guyot J. P. (2007). Eye movements in response to electric stimulation of the human posterior ampullary nerve. Ann. Otol. Rhinol. Laryngol. 116, 369–374
    1. Wall C., III, Merfeld D. M., Rauch S. D., Black F. O. (2002). Vestibular prostheses: the engineering and biomedical issues. J. Vestib. Res. 12, 95–113
    1. World Medical Association General Assembly (2000). World medical association declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA 284, 3043–304510.1001/jama.284.23.3043

Source: PubMed

Sponsors et collaborateurs

Les conditions médicales

Interventions en matière de drogue

3
S'abonner