REVIEW ARTICLES
Vestibular Implants: A Literature Review
Vestibüler Ä°mplantlar: Literatür Derlemesi
Received Date : 08 Sep 2022
Accepted Date : 23 Sep 2022
Available Online : 26 Sep 2022
Mustafa KARABULUTa, Banu MÃœJDECÄ°b
aMaastricht Üniversitesi Tıp Merkezi, Kulak Burun Boğaz Hastalıkları ABD, Maastricht, Hollanda
bAnkara Yıldırım Beyazıt Üniversitesi Sağlık Bilimleri Fakültesi, Odyoloji Bölümü, Ankara, Türkiye
Doi: 10.24179/kbbbbc.2022-93282 - Makale Dili: TR
KBB ve BBC Dergisi. 2022;30(4):224-31
Copyright © 2020 by Turkey Association of Society of Ear Nose Throat and Head Neck Surgery. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)
ABSTRACT
Vestibular implant (VI) is a prosthesis that aims to restore
bilaterally damaged peripheral vestibular function. VI fundamentally
consists of three key components. (1) Gyroscopes and/or
accelerometers, (2) An external processor, and (3) implanted stimulator.
VI is applied to patients with bilateral vestibulopathy (BVP). In
order to restore peripheral vestibular function, a new artificial (electrical)
baseline stimulation needs to be created as the peripheral vestibular
physiology is bilaterally damaged in patients with BVP. After
adjusting the new artificial baseline stimulation with the vestibular implant,
motion modulations are applied in order to adapt the individuals
to the new electrical stimulation. VI research-based implantation criteria
basically consist of 2 main processes: Bilaterally reduced or absent
peripheral vestibular function as a result of the caloric test, rotational
chair test (video) head impulse test and (2) the presence of severe
vestibular function with the chronic symptoms such as imbalance and
oscillopsia. However, one should pay attention to the existence of extra
criteria. Regarding VI surgery, two different types of surgical approaches,
intralabyrinthine and extralabyrinthine, can be used. Although
both approaches have pros and cons, the most preferred
approach is the intralabyrinthine approach. Intraoperative measurements
are also performed during the surgery in order to assess the integrity
of the implant and the appropriateness of the placement of the
electrodes. The VI started with animal experiments and has been currently
continuing with research based on humans. The aim of this review
is to address fundamental knowledge and convey the scientific
results on vestibular implants.
Keywords: Vestibular implant; bilateral vestibulopathy; bilateral vestibular loss; electrical stimulation; vestibular prosthesis; vestibulo-ocular reflex
ÖZET
Vestibüler implant (Vİ), bilateral olarak fonksiyonu bozulmuş
periferik vestibüler sistemi tekrar onarmayı amaçlayan bir protezdir.
Temel olarak 3 bileşenden oluşmaktadır: (1) Jiroskoplar ve/veya ivmeölçerler
(2) dış işlemci ve (3) implante edilmiş bir uyarıcıdır. VI bilateral
vestibülopatisi (BVP) olan hastalara uygulanmaktadır. BVP’si
olan bireylerde, vestibüler fizyolojinin bozulması nedeniyle sistemi restore
edebilmek için, yapay olarak (elektriksel) yeni bir temel ateşleme
hızının oluşturulması gerekmektedir. Vestibüler implant ile yeni temel
ateşleme hızı ayarlanmasının ardından, baş hareket modülasyonları uygulanarak,
bireyin yeni elektriksel uyarıma uyumu sağlanmaktadır. Vİ
araştırma bazlı implantasyon kriterleri temelde 2 ana süreçten oluşmaktadır:
(1) Kalorik test, rotasyonel sandalye testi (video), baÅŸ savurma
testi sonucunda her iki kulakta azalmış veya mevcut olmayan
vestibüler fonksiyonun saptanması ve (2) kronik dengesizlik ve osilopsi
gibi kronik semptomların var olduğu ileri derecede vestibüler
fonksiyon kaybıdır. Ancak ekstra kriterlerin varlığına dikkat edilmelidir.
VI cerrahisinde intralabirentin ve ekstralabirentin olmak üzere iki
farklı cerrahi yaklaşım kullanılabilir. Her iki yaklaşımın avantaj ve dezavantajları
olmasına rağmen en çok tercih edilen intralabirentin yaklaşımıdır.
Cerrahi süreç esnasında implantın bütünlüğünü ve
elektrotların yerleşiminin uygunluğunu değerlendirmek için intraoperatif
ölçümler uygulanmaktadır. Vestibüler implantlar, hayvan deneyleri
ile başlamış olup günümüzde insanlar üzerinde araştırma tabanlı
olarak uygulanmaya devam etmektedir. Bu gözden geçirme yazısında
Vİ’ye yönelik temel bilgilerin ele alınması ve literatür sonuçlarının aktarılması
amaçlanmıştır.
Anahtar Kelimeler: Vestibüler implant; bilateral vestibülopati; bilateral vestibüler bozukluk; elektriksel uyarım; vestibüler protez; vestibülooküler refleks
KAYNAKLAR
- Guyot JP, Perez Fornos A. Milestones in the development of a vestibular implant. Curr Opin Neurol. 2019;32(1):145-53. [Crossref] [PubMed] [PMC]
- Cohen B, Suzuki JI. Eye movements induced by ampullary nerve stimulation. Am J Physiol. 1963;204:347-51. [Crossref] [PubMed]
- Cohen B, Suzuki JI, Bender MB. Nystagmus induced by electric stimulation of ampullary nerves. Acta Oto-Laryngologica. 1965;60(1-6):422-36. [Crossref]
- Gong W, Merfeld DM. Prototype neural semicircular canal prosthesis using patterned electrical stimulation. Ann Biomed Eng. 2000;28(5):572-81. [Crossref] [PubMed]
- Dai C, Fridman GY, Chiang B, Davidovics NS, Melvin TA, Cullen KE, et al. Cross-axis adaptation improves 3D vestibulo-ocular reflex alignment during chronic stimulation via a head-mounted multichannel vestibular prosthesis. Exp Brain Res. 2011;210(3-4):595-606. [Crossref] [PubMed] [PMC]
- Lewis RF, Gong W, Ramsey M, Minor L, Boyle R, Merfeld DM. Vestibular adaptation studied with a prosthetic semicircular canal. J Vestib Res. 2002-2003;12(2-3):87-94. [Crossref] [PubMed]
- Migliaccio AA, Meierhofer R, Della Santina CC. Characterization of the 3D angular vestibulo-ocular reflex in C57BL6 mice. Exp Brain Res. 2011;210(3-4):489-501. [Crossref] [PubMed] [PMC]
- Thompson LA, Haburcakova C, Gong W, Lee DJ, Wall C 3rd, Merfeld DM, et al. Responses evoked by a vestibular implant providing chronic stimulation. J Vestib Res. 2012;22(1):11-5. [Crossref] [PubMed] [PMC]
- Guyot JP, Sigrist A, Pelizzone M, Kos MI. Adaptation to steady-state electrical stimulation of the vestibular system in humans. Ann Otol Rhinol Laryngol. 2011;120(3):143-9. [Crossref] [PubMed]
- van de Berg R, Guinand N, Stokroos RJ, Guyot JP, Kingma H. The vestibular implant: quo vadis? Front Neurol. 2011;2:47. [Crossref] [PubMed] [PMC]
- Guinand N, van de Berg R, Cavuscens S, Stokroos RJ, Ranieri M, Pelizzone M, et al. Vestibular implants: 8 years of experience with electrical stimulation of the vestibular nerve in 11 patients with bilateral vestibular loss. ORL J Otorhinolaryngol Relat Spec. 2015;77(4):227-40. [Crossref] [PubMed]
- Chow MR, Ayiotis AI, Schoo DP, Gimmon Y, Lane KE, Morris BJ, et al. Posture, gait, quality of life, and hearing with a vestibular implant. N Engl J Med. 2021;384(6):521-32. [Crossref] [PubMed] [PMC]
- Guinand N, van de Berg R, Ranieri M, Cavuscens S, DiGiovanna J, Nguyen TA, et al. Vestibular implants: Hope for improving the quality of life of patients with bilateral vestibular loss. Annu Int Conf IEEE Eng Med Biol Soc. 2015;2015:7192-5. [Crossref] [PubMed]
- Ramos de Miguel A, Falcon Gonzalez JC, Ramos Macias A. Vestibular response to electrical stimulation of the otolith organs. implications in the development of a vestibular implant for the improvement of the sensation of gravitoinertial accelerations. J Int Adv Otol. 2017;13(2):154-61. [Crossref] [PubMed]
- Rubinstein JT, Bierer S, Kaneko C, Ling L, Nie K, Oxford T, et al. Implantation of the semicircular canals with preservation of hearing and rotational sensitivity: a vestibular neurostimulator suitable for clinical research. Otol Neurotol. 2012;33(5):789-96. [Crossref] [PubMed] [PMC]
- Golub JS, Ling L, Nie K, Nowack A, Shepherd SJ, Bierer SM, et al. Prosthetic implantation of the human vestibular system. Otol Neurotol. 2014;35(1):136-47. [Crossref] [PubMed] [PMC]
- Ramos Macias A, Ramos de Miguel A, Rodriguez Montesdeoca I, Borkoski Barreiro S, Falcón González JC. Chronic electrical stimulation of the otolith organ: preliminary results in humans with bilateral vestibulopathy and sensorineural hearing loss. Audiol Neurootol. 2020;25(1-2):79-90. [Crossref] [PubMed]
- Goldberg JM, Fernandez C. Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. 3. Variations among units in their discharge properties. J Neurophysiol. 1971;34(4):676-84. [Crossref] [PubMed]
- Guyot JP, Sigrist A, Pelizzone M, Feigl GC, Kos MI. Eye movements in response to electrical stimulation of the lateral and superior ampullary nerves. Ann Otol Rhinol Laryngol. 2011;120(2):81-7. [Crossref] [PubMed]
- Faan RWBM, Dmsc VHM, Kerber K. Baloh and Honrubia's Clinical Neurophysiology of the Vestibular System. 4th ed. New York: Oxford University Press; 2010.
- Brontë-Stewart HM, Lisberger SG. Physiological properties of vestibular primary afferents that mediate motor learning and normal performance of the vestibulo-ocular reflex in monkeys. J Neurosci. 1994;14(3 Pt 1):1290-308. [Crossref] [PubMed] [PMC]
- Lucieer F, Duijn S, Van Rompaey V, Pérez Fornos A, Guinand N, Guyot JP, et al. Full spectrum of reported symptoms of bilateral vestibulopathy needs further investigation-a systematic review. Front Neurol. 2018;9:352. [Crossref] [PubMed] [PMC]
- Perez Fornos A, Guinand N, van de Berg R, Stokroos R, Micera S, Kingma H, et al. Artificial balance: restoration of the vestibulo-ocular reflex in humans with a prototype vestibular neuroprosthesis. Front Neurol. 2014;5:66. [Crossref] [PubMed] [PMC]
- Guyot JP, Perez Fornos A, Guinand N, van de Berg R, Stokroos R, Kingma H. Vestibular assistance systems: promises and challenges. J Neurol. 2016;263 Suppl 1:S30-5. [Crossref] [PubMed] [PMC]
- Davidovics NS, Fridman GY, Della Santina CC. Co-modulation of stimulus rate and current from elevated baselines expands head motion encoding range of the vestibular prosthesis. Exp Brain Res. 2012;218(3):389-400. [Crossref] [PubMed]
- Boutros PJ, Schoo D, Rahman M, Valentin NS, Chow M, Gimmon Y, et al. First-in-human safety and preliminary efficacy results for the MVIâ„¢ Multichannel Vestibular Implant. Journal of Hearing Science. 2018;8(2):195-6. [Link]
- Gong W, Haburcakova C, Merfeld DM. Vestibulo-ocular responses evoked via bilateral electrical stimulation of the lateral semicircular canals. IEEE Trans Biomed Eng. 2008;55(11):2608-19. [Crossref] [PubMed] [PMC]
- Merfeld DM, Gong W, Morrissey J, Saginaw M, Haburcakova C, Lewis RF. Acclimation to chronic constant-rate peripheral stimulation provided by a vestibular prosthesis. IEEE Trans Biomed Eng. 2006;53(11):2362-72. [Crossref] [PubMed]
- Guinand N, Guyot JP, Kingma H, Kos I, Pelizzone M. Vestibular implants: the first steps in humans. Annu Int Conf IEEE Eng Med Biol Soc. 2011;2011:2262-4. [Crossref] [PubMed]
- Gong W, Merfeld DM. System design and performance of a unilateral horizontal semicircular canal prosthesis. IEEE Trans Biomed Eng. 2002;49(2):175-81. [Crossref] [PubMed]
- Lewis RF, Haburcakova C, Gong W, Makary C, Merfeld DM. Vestibuloocular reflex adaptation investigated with chronic motion-modulated electrical stimulation of semicircular canal afferents. J Neurophysiol. 2010;103(2):1066-79. [Crossref] [PubMed] [PMC]
- Hain TC, Helminski JO. Anatomy and physiology of the normal vestibular system. Vestibular Rehabilitation. 2007;1(1):2. [Link]
- Halmagyi GM, Curthoys IS. Otolith function tests. In: Herdman SJ, Clendaniel RA, eds. Vestibular Rehabilitation. 4th ed. New York, NY: F. A. Davis Company; 2014.
- Merfeld DM, Haburcakova C, Gong W, Lewis RF. Chronic vestibulo-ocular reflexes evoked by a vestibular prosthesis. IEEE Trans Biomed Eng. 2007;54(6 Pt 1):1005-15. [Crossref] [PubMed]
- Nguyen TA, DiGiovanna J, Cavuscens S, Ranieri M, Guinand N, van de Berg R, et al. Characterization of pulse amplitude and pulse rate modulation for a human vestibular implant during acute electrical stimulation. J Neural Eng. 2016;13(4):046023. [Crossref] [PubMed]
- Fernandez C, Goldberg JM. Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. II. Response to sinusoidal stimulation and dynamics of peripheral vestibular system. J Neurophysiol. 1971;34(4):661-75. [Crossref] [PubMed]
- DiGiovanna J, Nguyen TA, Guinand N, Pérez-Fornos A, Micera S. Neural network model of vestibular nuclei reaction to onset of vestibular prosthetic stimulation. Front Bioeng Biotechnol. 2016;4:34. [Crossref] [PubMed] [PMC]
- van de Berg R, Ramos A, van Rompaey V, Bisdorff A, Perez-Fornos A, Rubinstein JT, et al. The vestibular implant: opinion statement on implantation criteria for research. J Vestib Res. 2020;30(3):213-23. [Crossref] [PubMed] [PMC]
- Strupp M, Kim JS, Murofushi T, Straumann D, Jen JC, Rosengren SM, et al. Bilateral vestibulopathy: diagnostic criteria consensus document of the Classification Committee of the Bárány Society. J Vestib Res. 2017;27(4):177-89. [Crossref] [PubMed] [PMC]
- van de Berg R, Guinand N, Guyot JP, Kingma H, Stokroos RJ. The modified ampullar approach for vestibular implant surgery: feasibility and its first application in a human with a long-term vestibular loss. Front Neurol. 2012;3:18. [Crossref] [PubMed] [PMC]
- Fridman GY, Davidovics NS, Dai C, Migliaccio AA, Della Santina CC. Vestibulo-ocular reflex responses to a multichannel vestibular prosthesis incorporating a 3D coordinate transformation for correction of misalignment. J Assoc Res Otolaryngol. 2010;11(3):367-81. [Crossref] [PubMed] [PMC]
- Rubinstein JT, Bierer S, Kaneko C, Ling L, Nie K, Oxford T, Newlands S, Santos F, Risi F, Abbas PJ, Phillips JO. Implantation of the semicircular canals with preservation of hearing and rotational sensitivity: a vestibular neurostimulator suitable for clinical research. Otology & Neurotology. 2012 Jul 1;33(5):789-96. [Crossref] [PubMed] [PMC]
- Feigl GC, Fasel JH, Anderhuber F, Ulz H, Rienmüller R, Guyot JP, et al. Superior vestibular neurectomy: a novel transmeatal approach for a denervation of the superior and lateral semicircular canals. Otol Neurotol. 2009;30(5):586-91. [Crossref] [PubMed]
- Wall C 3rd, Kos MI, Guyot JP. Eye movements in response to electric stimulation of the human posterior ampullary nerve. Ann Otol Rhinol Laryngol. 2007;116(5):369-74. [Crossref] [PubMed]
- Dai C, Fridman GY, Della Santina CC. Effects of vestibular prosthesis electrode implantation and stimulation on hearing in rhesus monkeys. Hear Res. 2011;277(1-2):204-10. [Crossref] [PubMed] [PMC]
- Tang S, Melvin TA, Della Santina CC. Effects of semicircular canal electrode implantation on hearing in chinchillas. Acta Otolaryngol. 2009;129(5):481-6. [Crossref] [PubMed] [PMC]
- Nguyen TAK, Cavuscens S, Ranieri M, Schwarz K, Guinand N, van de Berg R, et al. Characterization of cochlear, vestibular and cochlear-vestibular electrically evoked compound action potentials in patients with a vestibulo-cochlear implant. Front Neurosci. 2017;11:645. [Crossref] [PubMed] [PMC]
- Fishman AJ, Roland JT Jr, Alexiades G, Mierzwinski J, Cohen NL. Fluoroscopically assisted cochlear implantation. Otol Neurotol. 2003;24(6):882-6. [Crossref] [PubMed]
- Stultiens JJA, Postma AA, Guinand N, Pérez Fornos A, Kingma H, van de Berg R. Vestibular implantation and the feasibility of fluoroscopy-guided electrode insertion. Otolaryngol Clin North Am. 2020;53(1):115-26. [Crossref] [PubMed]
- Phillips C, Ling L, Oxford T, Nowack A, Nie K, Rubinstein JT, et al. Longitudinal performance of an implantable vestibular prosthesis. Hear Res. 2015;322:200-11. [Crossref] [PubMed] [PMC]
- Phillips JO, Ling L, Nie K, Jameyson E, Phillips CM, Nowack AL, et al. Vestibular implantation and longitudinal electrical stimulation of the semicircular canal afferents in human subjects. J Neurophysiol. 2015;113(10):3866-92. [Crossref] [PubMed] [PMC]
- Guinand N, Van de Berg R, Cavuscens S, Ranieri M, Schneider E, Lucieer F, et al. The video head impulse test to assess the efficacy of vestibular implants in humans. Front Neurol. 2017;8:600. [Crossref] [PubMed] [PMC]
- van de Berg R, Guinand N, Nguyen TA, Ranieri M, Cavuscens S, Guyot JP, et al. The vestibular implant: frequency-dependency of the electrically evoked vestibulo-ocular reflex in humans. Front Syst Neurosci. 2015;8:255. [Crossref] [PubMed] [PMC]
- Boutros PJ, Schoo DP, Rahman M, Valentin NS, Chow MR, Ayiotis AI, et al. Continuous vestibular implant stimulation partially restores eye-stabilizing reflexes. JCI Insight. 2019;4(22):e128397. [Crossref] [PubMed] [PMC]
- Fornos AP, van de Berg R, Armand S, Cavuscens S, Ranieri M, Crétallaz C, et al. Cervical myogenic potentials and controlled postural responses elicited by a prototype vestibular implant. J Neurol. 2019;266(Suppl 1):33-41. [Crossref] [PubMed] [PMC]
- Phillips C, Defrancisci C, Ling L, Nie K, Nowack A, Phillips JO, et al. Postural responses to electrical stimulation of the vestibular end organs in human subjects. Exp Brain Res. 2013;229(2):181-95. [Crossref] [PubMed]
- Lucieer FMP, Van Hecke R, van Stiphout L, Duijn S, Perez-Fornos A, Guinand N, et al. Bilateral vestibulopathy: beyond imbalance and oscillopsia. J Neurol. 2020;267(Suppl 1):241-55. [Crossref] [PubMed] [PMC]
- Guinand N, Pijnenburg M, Janssen M, Kingma H. Visual acuity while walking and oscillopsia severity in healthy subjects and patients with unilateral and bilateral vestibular function loss. Arch Otolaryngol Head Neck Surg. 2012;138(3):301-6. [Crossref] [PubMed]
- Guinand N, Van de Berg R, Cavuscens S, Stokroos R, Ranieri M, Pelizzone M, et al. Restoring visual acuity in dynamic conditions with a vestibular implant. Front Neurosci. 2016;10:577. [Crossref] [PubMed] [PMC]
- Starkov D, Guinand N, Lucieer F, Ranieri M, Cavuscens S, Pleshkov M, et al. Restoring the high-frequency dynamic visual acuity with a vestibular implant prototype in humans. Audiol Neurootol. 2020;25(1-2):91-5. [Crossref] [PubMed]