Semin Neurol 2020; 40(01): 040-048
DOI: 10.1055/s-0039-3402066
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Bilateral Vestibular Dysfunction

Sun-Uk Lee
1   Department of Neurology, Korea University Anam Hospital, Seoul, South Korea
,
Hyo-Jung Kim
2   Research Administration Team, Seoul National University Bundang Hospital, Seongnam, South Korea
,
Ji-Soo Kim
3   Department of Neurology, Seoul National University College of Medicine, Seoul, South Korea
4   Dizziness Center, Clinical Neuroscience Center, and Department of Neurology, Seoul National University Bundang Hospital, Seongnam, South Korea
› Author Affiliations
Funding This study was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science, and Technology (NRF-2016R1D1A1B04935568).
Further Information

Publication History

Publication Date:
14 January 2020 (online)

Abstract

Bilateral vestibular dysfunction (BVD) refers to hypofunction of the vestibular nerves or labyrinths on both sides. Patients with BVD present with dizziness, oscillopsia, and unsteadiness, mostly during locomotion, which worsen in darkness or on uneven ground. Although aminoglycoside ototoxicity, Meniere's disease, infection, and genetic disorders frequently cause BVD, the etiology remains undetermined in up to 50% of the patients. The diagnosis of BVD requires both symptoms and documentation of deficient vestibulo-ocular reflex function using head-impulse, bithermal caloric, and rotatory chair tests. Since various neurologic and systemic disorders may present with BVD, clinicians should be cautious not to overlook the symptoms and signs of central nervous system and systemic involvements. Vestibular rehabilitation, application of vibrotactile and auditory feedbacks, and vestibular prosthesis can aid the patients with BVD along with the correction of the underlying causes.

Author Contributions

Dr. Lee wrote the manuscript. Dr. H. J. Kim revised the manuscript. Dr. J. S. Kim designed and conceptualized the study and revised the manuscript.


Disclosure

J. S. Kim serves as an associate editor of Frontiers in Neurology – Neuro-otology and is on the editorial boards of the Journal of Clinical Neurology, Frontiers in Neurology – Neuro-Ophthalmology, Journal of Neuro-Ophthalmology, Journal of Vestibular Research, Journal of Neurology, and Medicine.


 
  • References

  • 1 Baloh RW, Jacobson K, Honrubia V. Idiopathic bilateral vestibulopathy. Neurology 1989; 39 (2 Pt 1): 272-275
  • 2 McGath JH, Barber HO, Stoyanoff S. Bilateral vestibular loss and oscillopsia. J Otolaryngol 1989; 18 (05) 218-221
  • 3 Zingler VC, Cnyrim C, Jahn K. , et al. Causative factors and epidemiology of bilateral vestibulopathy in 255 patients. Ann Neurol 2007; 61 (06) 524-532
  • 4 Kattah JC. Clinical characteristics and etiology of bilateral vestibular loss in a cohort from central Illinois. Front Neurol 2018; 9: 46
  • 5 Hain TC, Cherchi M, Yacovino DA. Bilateral vestibular weakness. Front Neurol 2018; 9: 344
  • 6 Tarnutzer AA, Bockisch CJ, Buffone E, Weber KP. Hierarchical cluster analysis of semicircular canal and otolith deficits in bilateral vestibulopathy. Front Neurol 2018; 9: 244
  • 7 Kim S, Oh YM, Koo JW, Kim JS. Bilateral vestibulopathy: clinical characteristics and diagnostic criteria. Otol Neurotol 2011; 32 (05) 812-817
  • 8 Rinne T, Bronstein AM, Rudge P, Gresty MA, Luxon LM. Bilateral loss of vestibular function: clinical findings in 53 patients. J Neurol 1998; 245 (6-7): 314-321
  • 9 Brandt T, Dieterich M, Strupp M. Vertigo and Dizziness. 2nd ed. London: Springer-Verlag; 2005
  • 10 Ward BK, Agrawal Y, Hoffman HJ, Carey JP, Della Santina CC. Prevalence and impact of bilateral vestibular hypofunction: results from the 2008 US National Health Interview Survey. JAMA Otolaryngol Head Neck Surg 2013; 139 (08) 803-810
  • 11 Moon M, Chang SO, Kim MB. Diverse clinical and laboratory manifestations of bilateral vestibulopathy. Laryngoscope 2017; 127 (01) E42-E49
  • 12 Lucieer F, Vonk P, Guinand N, Stokroos R, Kingma H, van de Berg R. Bilateral vestibular hypofunction: insights in etiologies, clinical subtypes, and diagnostics. Front Neurol 2016; 7: 26
  • 13 Strupp M, Kim JS, Murofushi T. , et al. Bilateral vestibulopathy: diagnostic criteria consensus document of the classification committee of the Barany Society. J Vestib Res 2017; 27 (04) 177-189
  • 14 van de Berg R, van Tilburg M, Kingma H. Bilateral vestibular hypofunction: challenges in establishing the diagnosis in adults. ORL J Otorhinolaryngol Relat Spec 2015; 77 (04) 197-218
  • 15 Cousins S, Kaski D, Cutfield N. , et al. Vestibular perception following acute unilateral vestibular lesions. PLoS One 2013; 8 (05) e61862
  • 16 Glasauer S, Amorim M-A, Vitte E, Berthoz A. Goal-directed linear locomotion in normal and labyrinthine-defective subjects. Exp Brain Res 1994; 98 (02) 323-335
  • 17 Gresty MA, Hess K, Leech J. Disorders of the vestibulo-ocular reflex producing oscillopsia and mechanisms compensating for loss of labyrinthine function. Brain 1977; 100 (04) 693-716
  • 18 Herdman SJ, Hall CD, Schubert MC, Das VE, Tusa RJ. Recovery of dynamic visual acuity in bilateral vestibular hypofunction. Arch Otolaryngol Head Neck Surg 2007; 133 (04) 383-389
  • 19 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 (03) 301-306
  • 20 Anson ER, Gimmon Y, Kiemel T, Jeka JJ, Carey JP. A tool to quantify the functional impact of oscillopsia. Front Neurol 2018; 9: 142
  • 21 Yacovino DA, Finlay JB, Urbina Jaimes VN, Verdecchia DH, Schubert MC. Acute bilateral superior branch vestibular neuropathy. Front Neurol 2018; 9: 353
  • 22 Brandt T, Schautzer F, Hamilton DA. , et al. Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. Brain 2005; 128 (Pt 11): 2732-2741
  • 23 Kremmyda O, Hüfner K, Flanagin VL. , et al. Beyond dizziness: virtual navigation, spatial anxiety and hippocampal volume in bilateral vestibulopathy. Front Hum Neurosci 2016; 10: 139
  • 24 Halmagyi GM, Curthoys IS. A clinical sign of canal paresis. Arch Neurol 1988; 45 (07) 737-739
  • 25 MacDougall HG, Weber KP, McGarvie LA, Halmagyi GM, Curthoys IS. The video head impulse test: diagnostic accuracy in peripheral vestibulopathy. Neurology 2009; 73 (14) 1134-1141
  • 26 Yip CW, Glaser M, Frenzel C, Bayer O, Strupp M. Comparison of the bedside head-impulse test with the video head-impulse test in a clinical practice setting: a prospective study of 500 outpatients. Front Neurol 2016; 7: 58
  • 27 Tarnutzer AA, Bockisch CJ, Buffone E, Weiler S, Bachmann LM, Weber KP. Disease-specific sparing of the anterior semicircular canals in bilateral vestibulopathy. Clin Neurophysiol 2016; 127 (08) 2791-2801
  • 28 Baloh RW, Honrubia V, Kerber K. Baloh and Honrubia's Clinical Neurophysiology of the Vestibular System. New York: Oxford University Press; 2010
  • 29 Grossman GE, Leigh RJ, Abel LA, Lanska DJ, Thurston SE. Frequency and velocity of rotational head perturbations during locomotion. Exp Brain Res 1988; 70 (03) 470-476
  • 30 Fife TD, Tusa RJ, Furman JM. , et al. Assessment: vestibular testing techniques in adults and children: report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology. Neurology 2000; 55 (10) 1431-1441
  • 31 Matsuzaki M, Murofushi T. Vestibular evoked myogenic potentials in patients with idiopathic bilateral vestibulopathy. Report of three cases. ORL J Otorhinolaryngol Relat Spec 2001; 63 (06) 349-352
  • 32 Rosengren SM, Welgampola MS, Taylor RL. Vestibular-evoked myogenic potentials in bilateral vestibulopathy. Front Neurol 2018; 9: 252
  • 33 Zingler VC, Weintz E, Jahn K. , et al. Saccular function less affected than canal function in bilateral vestibulopathy. J Neurol 2008; 255 (09) 1332-1336
  • 34 Agrawal Y, Bremova T, Kremmyda O, Strupp M. Semicircular canal, saccular and utricular function in patients with bilateral vestibulopathy: analysis based on etiology. J Neurol 2013; 260 (03) 876-883
  • 35 Ruehl RM, Guerkov R. Amiodarone-induced gait unsteadiness is revealed to be bilateral vestibulopathy. Eur J Neurol 2017; 24 (02) e7-e8
  • 36 Fife TDF, Robb MJA, Steenerson KK, Saha KC. Bilateral vestibular dysfunction associated with chronic exposure to military jet propellant type-eight jet fuel. Front Neurol 2018; 9: 351
  • 37 Jen JC. Bilateral vestibulopathy: clinical, diagnostic, and genetic considerations. Semin Neurol 2009; 29 (05) 528-533
  • 38 Sánchez-Sellero I, Soto-Varela A. Instability due to drug-induced vestibulotoxicity. J Int Adv Otol 2016; 12 (02) 202-207
  • 39 Hain TC, Cherchi M, Yacovino DA. Bilateral vestibular loss. Semin Neurol 2013; 33 (03) 195-203
  • 40 Park HK, Kim JS, Strupp M, Zee DS. Isolated floccular infarction: impaired vestibular responses to horizontal head impulse. J Neurol 2013; 260 (06) 1576-1582
  • 41 Kim HJ, Lee SH, Park JH, Choi JY, Kim JS. Isolated vestibular nuclear infarction: report of two cases and review of the literature. J Neurol 2014; 261 (01) 121-129
  • 42 Lee SU, Park SH, Park JJ. , et al. Dorsal medullary infarction distinct syndrome of isolated central vestibulopathy. Stroke 2015; 46 (11) 3081-3087
  • 43 Migliaccio AA, Halmagyi GM, McGarvie LA, Cremer PD. Cerebellar ataxia with bilateral vestibulopathy: description of a syndrome and its characteristic clinical sign. Brain 2004; 127 (Pt 2): 280-293
  • 44 Szmulewicz DJ, Roberts L, McLean CA, MacDougall HG, Halmagyi GM, Storey E. Proposed diagnostic criteria for cerebellar ataxia with neuropathy and vestibular areflexia syndrome (CANVAS). Neurol Clin Pract 2016; 6 (01) 61-68
  • 45 Huh YE, Kim JS, Kim HJ. , et al. Vestibular performance during high-acceleration stimuli correlates with clinical decline in SCA6. Cerebellum 2015; 14 (03) 284-291
  • 46 Gordon CR, Zivotofsky AZ, Caspi A. Impaired vestibulo-ocular reflex (VOR) in spinocerebellar ataxia type 3 (SCA3): bedside and search coil evaluation. J Vestib Res 2014; 24 (5-6): 351-355
  • 47 Luis L, Costa J, Muñoz E. , et al. Vestibulo-ocular reflex dynamics with head-impulses discriminates spinocerebellar ataxias types 1, 2 and 3 and Friedreich ataxia. J Vestib Res 2016; 26 (03) 327-334
  • 48 Naoshima-Ishibashi Y, Murofushi T. A case of Cronkhite-Canada syndrome with vestibular disturbances. Eur Arch Otorhinolaryngol 2004; 261 (10) 558-559
  • 49 Chen L, Halmagyi GM, Todd MJ, Aw ST. Vestibular and saccadic abnormalities in Gaucher's disease. JIMD Rep 2014; 13: 111-118
  • 50 Ell J, Prasher D, Rudge P. Neuro-otological abnormalities in Friedreich's ataxia. J Neurol Neurosurg Psychiatry 1984; 47 (01) 26-32
  • 51 Lee SH, Kim SH, Kim JM, Tarnutzer AA. Vestibular dysfunction in Wernicke's encephalopathy: predominant impairment of the horizontal semicircular canals. Front Neurol 2018; 9: 141
  • 52 Choi KD, Oh SY, Kim HJ, Kim JS. The vestibulo-ocular reflexes during head impulse in Wernicke's encephalopathy. J Neurol Neurosurg Psychiatry 2007; 78 (10) 1161-1162
  • 53 Kattah JC, Dhanani SS, Pula JH, Mantokoudis G, Tehrani ASS, Toker DEN. Vestibular signs of thiamine deficiency during the early phase of suspected Wernicke encephalopathy. Neurol Clin Pract 2013; 3 (06) 460-468
  • 54 Kattah JC, Guede C, Hassanzadeh B. The medial vestibular nuclei, a vulnerable target in thiamine deficiency. J Neurol 2018; 265 (01) 213-215
  • 55 Hughes JT, Oppenheimer DR. Superficial siderosis of the central nervous system. A report on nine cases with autopsy. Acta Neuropathol 1969; 13 (01) 56-74
  • 56 Tarlov I. Structure of the nerve root: II. Differentiation of sensory from motor roots; observations on identification of function in roots of mixed cranial nerves. Arch Neurol Psychiatry 1937; 37: 1338-1355
  • 57 Lee SY, Lee DH, Bae YJ, Song JJ, Kim JS, Koo JW. Bilateral vestibulopathy in superficial siderosis. Front Neurol 2018; 9: 422
  • 58 Jeong SH, Kim YS, Lee JH, Jo H, Lee AY, Kim JM. Transient positive horizontal head impulse test in pregabalin intoxication. J Epilepsy Res 2015; 5 (02) 101-103
  • 59 Lee SU, Jung IE, Kim HJ, Kim JS. Metronidazole-induced combined peripheral and central vestibulopathy. J Neurol Sci 2016; 365: 31-33
  • 60 Lunardi C, Bason C, Leandri M. , et al. Autoantibodies to inner ear and endothelial antigens in Cogan's syndrome. Lancet 2002; 360 (9337): 915-921
  • 61 Arnold W, Pfaltz R, Altermatt H-J. Evidence of serum antibodies against inner ear tissues in the blood of patients with certain sensorineural hearing disorders. Acta Otolaryngol 1985; 99 (3-4): 437-444
  • 62 Haynes BF, Kaiser-Kupfer MI, Mason P, Fauci AS. Cogan syndrome: studies in thirteen patients, long-term follow-up, and a review of the literature. Medicine (Baltimore) 1980; 59 (06) 426-441
  • 63 Kessel A, Vadasz Z, Toubi E. Cogan syndrome--pathogenesis, clinical variants and treatment approaches. Autoimmun Rev 2014; 13 (4-5): 351-354
  • 64 Kleffner I, Dörr J, Ringelstein M. , et al; European Susac Consortium (EuSaC). Diagnostic criteria for Susac syndrome. J Neurol Neurosurg Psychiatry 2016; 87 (12) 1287-1295
  • 65 Greco A, De Virgilio A, Gallo A. , et al. Idiopathic bilateral vestibulopathy: an autoimmune disease?. Autoimmun Rev 2014; 13 (10) 1042-1047
  • 66 Kim HJ, Park SH, Kim JS. , et al. Bilaterally abnormal head impulse tests indicate a large cerebellopontine angle tumor. J Clin Neurol 2016; 12 (01) 65-74
  • 67 Kim SH, Kim HJ, Kim JS. Rapid progression of bilateral vestibulopathy due to metastatic lung cancer. J Clin Neurol 2018; 14 (01) 104-106
  • 68 Lee SU, Kim HJ, Choi JY, Kim JS. Lower brainstem melanocytoma masquerading as vestibular paroxysmia. J Neurol 2018; 265 (05) 1222-1225
  • 69 Lee SU, Kim HJ, Choi JY, Yang X, Kim JS. Isolated acute vestibular syndrome due to presumed primary central nervous system lymphoma involving the dorsal medulla. J Neurol 2018; 265 (08) 1937-1939
  • 70 Staecker H, Praetorius M, Baker K, Brough DE. Vestibular hair cell regeneration and restoration of balance function induced by math1 gene transfer. Otol Neurotol 2007; 28 (02) 223-231
  • 71 Zingler VC, Weintz E, Jahn K. , et al. Follow-up of vestibular function in bilateral vestibulopathy. J Neurol Neurosurg Psychiatry 2008; 79 (03) 284-288
  • 72 Han BI, Song HS, Kim JS. Vestibular rehabilitation therapy: review of indications, mechanisms, and key exercises. J Clin Neurol 2011; 7 (04) 184-196
  • 73 Porciuncula F, Johnson CC, Glickman LB. The effect of vestibular rehabilitation on adults with bilateral vestibular hypofunction: a systematic review. J Vestib Res 2012; 22 (5-6): 283-298
  • 74 Krebs DE, Gill-Body KM, Riley PO, Parker SW. Double-blind, placebo-controlled trial of rehabilitation for bilateral vestibular hypofunction: preliminary report. Otolaryngol Head Neck Surg 1993; 109 (04) 735-741
  • 75 Fujimoto C, Murofushi T, Chihara Y. , et al. Effect of severity of vestibular dysfunction on postural instability in idiopathic bilateral vestibulopathy. Acta Otolaryngol 2013; 133 (05) 454-461
  • 76 Allum JH, Honegger F. Vibro-tactile and auditory balance biofeedback changes muscle activity patterns: possible implications for vestibular implants. J Vestib Res 2017; 27 (01) 77-87
  • 77 Wuehr M, Nusser E, Decker J. , et al. Noisy vestibular stimulation improves dynamic walking stability in bilateral vestibulopathy. Neurology 2016; 86 (23) 2196-2202
  • 78 Kingma H, Felipe L, Gerards M-C. , et al. Vibrotactile feedback improves balance and mobility in patients with severe bilateral vestibular loss. J Neurol 2019; 266 (Suppl. 01) 19-26
  • 79 Guinand N, Van de Berg R, Cavuscens S. , et al. Restoring visual acuity in dynamic conditions with a vestibular implant. Front Neurosci 2016; 10: 577
  • 80 Guinand N, Van de Berg R, Cavuscens S. , et al. The video head impulse test to assess the efficacy of vestibular implants in humans. Front Neurol 2017; 8: 600
  • 81 Strupp M, Jahn K, Brandt T. Another adverse effect of aspirin: bilateral vestibulopathy. J Neurol Neurosurg Psychiatry 2003; 74 (05) 691
  • 82 Bayazit Y, Yilmaz M, Mumbuç S, Kanlikama M. Assessment of migraine-related cochleovestibular symptoms. Rev Laryngol Otol Rhinol (Bord) 2001; 122 (02) 85-88
  • 83 Cass SP, Furman JM, Ankerstjerne K, Balaban C, Yetiser S, Aydogan B. Migraine-related vestibulopathy. Ann Otol Rhinol Laryngol 1997; 106 (03) 182-189
  • 84 Radtke A, von Brevern M, Neuhauser H, Hottenrott T, Lempert T. Vestibular migraine: long-term follow-up of clinical symptoms and vestibulo-cochlear findings. Neurology 2012; 79 (15) 1607-1614
  • 85 Song JJ, Lee HM, Chae SW, Hwang SJ. Bilateral otosyphilis in a patient with HIV infection. Eur Arch Otorhinolaryngol 2005; 262 (12) 972-974
  • 86 van Leeuwen RB, van Kooten B, de Cock AF. Bilateral vestibular hypofunction and Lyme disease: a causal link?. Acta Neurol Belg 2017; 117 (01) 367-368
  • 87 Kagoya R, Iwasaki S, Chihara Y. , et al. Cephalic tetanus presenting as acute vertigo with bilateral vestibulopathy. Acta Otolaryngol 2011; 131 (03) 334-336
  • 88 Pollak L, Milo R, Kossych V, Rabey MJ, Shapira E. Bilateral vestibular failure as a unique presenting sign in carcinomatous meningitis: case report. J Neurol Neurosurg Psychiatry 2001; 70 (05) 704-705
  • 89 Schulz P, Arbusow V, Strupp M, Dieterich M, Sautier W, Brandt T. Sympathetic contralateral vestibulopathy after unilateral zoster oticus. J Neurol Neurosurg Psychiatry 1999; 66 (05) 672-676
  • 90 Fischer CS, Bayer O, Strupp M. Transient bilateral vestibular dysfunction caused by intoxication with low doses of styrene. Eur Arch Otorhinolaryngol 2014; 271 (03) 619-623
  • 91 Jen JC, Wang H, Lee H. , et al. Suggestive linkage to chromosome 6q in families with bilateral vestibulopathy. Neurology 2004; 63 (12) 2376-2379
  • 92 Weegerink NJ, Schraders M, Leijendeckers J. , et al. Audiometric characteristics of a Dutch family with Muckle-Wells syndrome. Hear Res 2011; 282 (1-2): 243-251
  • 93 Jung J, Seo YW, Choi JY, Kim SH. Vestibular function is associated with residual low-frequency hearing loss in patients with bi-allelic mutations in the SLC26A4 gene. Hear Res 2016; 335: 33-39