Advertisement

Diagnosing and localizing the acute vestibular syndrome – Beyond the HINTS exam

Published:October 08, 2022DOI:https://doi.org/10.1016/j.jns.2022.120451

      Highlights

      • Brainstem and cerebellar strokes cause ocular motor findings beyond the HINTS exam.
      • Review central patterns of saccades, smooth pursuits, ocular tilt reaction and nystagmus.
      • Ocular lateropulsion (ipsipulsion) in Wallenberg is highly localizing.
      • Flocculus, Nodulus, Midbrain, Pons and Medullary stroke syndromes are reviewed.
      • Diagnose central causes of Acute Vestibular syndrome (AVS) with the bedside exam.

      Abstract

      When assessing the acutely dizzy patient, the HINTS ‘Plus’ (Head Impulse, Nystagmus, Test of Skew, ‘Plus’ a bedside assessment of auditory function) exam is a crucial component of the bedside exam. However, there are additional ocular motor findings that can help the clinician distinguish peripheral from central etiologies and enable accurate localization, especially when the patient has acute dizziness, vertigo and/or imbalance but without spontaneous nystagmus. We will review the literature on these findings which are ‘beyond HINTS’ and include saccades/ocular lateropulsion, smooth pursuit, and provocative maneuvers including head-shaking and positional testing (not part of the HINTS exam). Additionally, we will expound on the localizing value of nystagmus, ocular alignment and the ocular tilt reaction (parts of the HINTS exam). The paper has been organized neuroanatomically, based on brainstem and cerebellar structures that have been reported to cause the acute vestibular syndrome.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Journal of the Neurological Sciences
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Kattah J.C.
        • Talkad A.V.
        • Wang D.Z.
        • Hsieh Y.H.
        • Newman-Toker D.E.
        HINTS to diagnose stroke in the acute vestibular syndrome: three-step bedside oculomotor examination more sensitive than early MRI diffusion-weighted imaging.
        Stroke. 2009 Nov; 40: 3504-3510
        • Leigh R.J.
        • Zee D.S.
        The Neurology of Eye Movements [Internet].
        5th ed. Oxford University Press, 2015https://doi.org/10.1093/med/9780199969289.001.0001/med-9780199969289 ([cited 2022 May 8]. Available from:)
        • Gold D.R.
        Neuro-Ophthalmology and Neuro-Otology: A Case-Based Guide for Clinicians and Scientists.
        Springer Nature, 2021
        • Shemesh A.A.
        • Zee D.S.
        Eye movement disorders and the cerebellum.
        J. Clin. Neurophysiol. 2019 Nov; 36: 405-414
        • Spooner J.W.
        • Sakala S.M.
        • Baloh R.W.
        Effect of aging on eye tracking.
        Arch. Neurol. 1980 Sep 1; 37: 575-576
        • Zwergal A.
        • Rettinger N.
        • Frenzel C.
        • Dieterich M.
        • Brandt T.
        • Strupp M.
        A bucket of static vestibular function.
        Neurology. 2009 May 12; 72: 1689-1692
        • Baier B.
        • Bense S.
        • Dieterich M.
        Are signs of ocular tilt reaction in patients with cerebellar lesions mediated by the dentate nucleus?.
        Brain. 2008 Jan 29; 131: 1445-1454
        • Choi J.Y.
        • Kim H.J.
        • Kim J.S.
        Recent advances in head impulse test findings in central vestibular disorders.
        Neurology. 2018 Mar 27; 90: 602-612
        • Kim J.S.
        • Kim H.G.
        • Chung C.S.
        Medial medullary syndrome: report of 18 new patients and a review of the literature.
        Stroke. 1995 Sep; 26: 1548-1552
        • Kim J.S.
        • Choi K.D.
        • Oh S.Y.
        • Park S.H.
        • Han M.K.
        • Yoon B.W.
        • et al.
        Medial medullary infarction: abnormal ocular motor findings.
        Neurology. 2005 Oct 25; 65: 1294-1298
        • Tyler K.L.
        • Sandberg E.
        • Baum K.F.
        Medial medullary syndrome and meningovascular syphilis: a case report in an HTV-infected man and a review of the literature.
        Neurology. 1994 Dec 1; 44 (2231–2231)
        • Isenberg-Grzeda E.
        • Rahane S.
        • DeRosa A.P.
        • Ellis J.
        • Nicolson S.E.
        Wernicke-Korsakoff syndrome in patients with cancer: a systematic review.
        Lancet Oncol. 2016 Apr; 17 (e142–8)
        • Sechi G.
        • Serra A.
        Wernicke’s encephalopathy: new clinical settings and recent advances in diagnosis and management.
        Lancet Neurol. 2007 May; 6: 442-455
        • Sinha S.
        • Kataria A.
        • Kolla B.P.
        • Thusius N.
        • Loukianova L.L.
        Wernicke encephalopathy—clinical pearls.
        Mayo Clin. Proc. 2019 Jun; 94: 1065-1072
        • Kattah J.C.
        • Tehrani A.S.
        • du Lac S.
        • Newman-Toker D.E.
        • Zee D.S.
        Conversion of upbeat to downbeat nystagmus in Wernicke encephalopathy.
        Neurology. 2018 Oct 23; 91: 790-796
        • Kattah J.C.
        • McClelland C.
        • Zee D.S.
        Vertical nystagmus in Wernicke’s encephalopathy: pathogenesis and role of central processing of information from the otoliths.
        J. Neurol. 2019; 266: 139-145
        • Buttner-Ennevera J.A.
        A review of otolith pathways to brainstem and cerebellum.
        Ann. N. Y. Acad. Sci. 1999 May; 871: 51-64
        • Wallenberg A.
        Acute Bulbaraffection (Embolie der art.cerebellar.post,inf.sinistr?).
        Arch. Psychiatr. Nervenkrankh. 1895; 27: 504-540
        • Currier R.D.
        • Schneider R.C.
        • Preston R.E.
        Angiographic findings in Wallenberg’s lateral medullary syndrome.
        J. Neurosurg. 1962 Dec; 19: 1058-1067
        • Fisher C.M.
        • Karnes W.E.
        • Kubik C.S.
        Lateral medullary infarction—the pattern of vascular occlusion.
        J. Neuropathol. Exp. Neurol. 1961; 20: 323-379
        • Paliwal V.
        • Neyaz Z.
        • Kumar S.
        • Gupta D.
        Ipsipulsion: a forgotten sign of lateral medullary syndrome.
        Ann. Indian Acad. Neurol. 2015; 18: 284
        • Waespe W.
        • Wichmann W.
        Oculomotor disturbances during visual-vestibular interaction in Wallenberg’s lateral medullary syndrome.
        Brain. 1990; 113: 821-846
        • Kim J.S.
        • Moon S.Y.
        • Park S.H.
        • Yoon B.W.
        • Roh J.K.
        Ocular lateropulsion in Wallenberg syndrome.
        Neurology. 2004 Jun 22; 62 (2287–2287)
        • Kattah J.C.
        • Badihian S.
        • Pula J.H.
        • Tarnutzer A.A.
        • Newman-Toker D.E.
        • Zee D.S.
        Ocular lateral deviation with brief removal of visual fixation differentiates central from peripheral vestibular syndrome.
        J. Neurol. 2020 Dec; 267: 3763-3772
        • Choi K.D.
        • Kim H.J.
        • Cho B.M.
        • Kim J.S.
        Saccadic adaptation in lateral medullary and cerebellar infarction.
        Exp. Brain Res. 2008 Jul; 188: 475-482
        • Hayakawa Y.
        • Nakajima T.
        • Takagi M.
        • Fukuhara N.
        • Abe H.
        Human cerebellar activation in relation to saccadic eye movements: a functional magnetic resonance imaging study.
        Ophthalmologica. 2002; 216: 399-405
        • Cho K.H.
        • Kim Y.D.
        • Kim J.
        • Ye B.S.
        • Heo J.H.
        • Nam H.S.
        Contraversive ocular tilt reaction after the lateral medullary infarction.
        Neurologist. 2015 Feb; 19: 79-81
        • Guerrero W.R.
        • Dababneh H.
        • Hedna S.
        • Johnson J.A.
        • Peters K.
        • Waters M.F.
        Vessel wall enhancement in herpes simplex virus central nervous system vasculitis.
        J. Clin. Neurosci. 2013 Sep; 20: 1318-1319
        • Elavarasi A.
        • Mani B.
        Vertical diplopia: skew deviation and medullary lesion.
        Ann. Indian Acad. Neurol. 2019; 0: 0
        • Lee S.U.
        • Park S.H.
        • Park J.J.
        • Kim H.J.
        • Han M.K.
        • Bae H.J.
        • et al.
        Dorsal medullary infarction: distinct syndrome of isolated central vestibulopathy.
        Stroke. 2015 Nov; 46: 3081-3087
        • Brandt T.
        • Dieterich M.
        Skew deviation with ocular torsion: a vestibular brainstem sign of topographic diagnostic value.
        Ann. Neurol. 1993 May; 33: 528-534
        • Keane J.R.
        Ocular skew deviation: analysis of 100 cases.
        Arch. Neurol. 1975 Mar 1; 32: 185
        • Dieterich M.
        • Brandt T.
        Ocular torsion and tilt of subjective visual vertical are sensitive brainstem signs.
        Ann. Neurol. 2004 Oct 16; 33: 292-299
        • Walter E.
        • Trobe J.D.
        The clinical and imaging profile of skew deviation: a study of 157 cases.
        J. Neuroophthalmol. 2021 Mar; 41: 69-76
        • Gold D.R.
        • Schubert M.C.
        Ocular misalignment in dizzy patients—something’s A-skew.
        J. Neurol. Phys. Ther. 2019 Apr; 43: S27-S30
        • Brazis P.W.
        Ocular motor abnormalities in Wallenberg’s lateral medullary syndrome.
        Mayo Clin. Proc. 1992 Apr; 67: 365-368
        • Choi K.D.
        • Oh S.Y.
        • Park S.H.
        • Kim J.H.
        • Koo J.W.
        • Kim J.S.
        Head-shaking nystagmus in lateral medullary infarction: patterns and possible mechanisms.
        Neurology. 2007 Apr 24; 68: 1337-1344
        • Kattah J.C.
        Use of HINTS in the acute vestibular syndrome. An overview.
        Stroke Vasc. Neurol. 2018; 3: 190-196
        • Chang T.P.
        • Zee D.S.
        • Gold D.R.
        Upbeat nystagmus in dorsolateral pontine infarction.
        J. Neuroophthalmol. 2021 Mar; 41 (e94–6)
        • Caplan L.
        • van Gijn J.
        Stroke Syndromes.
        3rd ed. Cambridge University Press, New York2012: 621
        • Strupp M.
        • Kremmyda O.
        • Adamczyk C.
        • Böttcher N.
        • Muth C.
        • Yip C.W.
        • et al.
        Central ocular motor disorders, including gaze palsy and nystagmus.
        J. Neurol. 2014 Sep; 261: 542-558
        • Zee D.S.
        Internuclear ophthalmoplegia: pathophysiology and diagnosis.
        Baillieres Clin. Neurol. 1992 Aug; 1: 455-470
        • Jeong S.H.
        • Kim E.K.
        • Lee J.
        • Choi K.D.
        • Kim J.S.
        Patterns of dissociate torsional-vertical nystagmus in internuclear ophthalmoplegia: jerky seesaw nystagmus in INO.
        Ann. N. Y. Acad. Sci. 2011 Sep; 1233: 271-278
        • Oh K.
        • Chang J.H.
        • Park K.W.
        • Lee D.H.
        • Choi K.D.
        • Kim J.S.
        Jerky seesaw nystagmus in isolated internuclear ophthalmoplegia from focal pontine lesion.
        Neurology. 2005 Apr 12; 64: 1313-1314
        • Bassetti C.
        • Bogousslavsky J.
        • Barth A.
        • Regli F.
        Isolated infarcts of the pons.
        Neurology. 1996 Jan; 46: 165-175
        • Deplanque D.
        • Godefroy O.
        • Guerouaou D.
        • Laureau E.
        • Desaulty A.
        Sudden bilateral deafness: lateral inferior pontine infarction.
        J. Neurol. Neurosurg. Psychiatry. 1998 Jun 1; 64 (817a–8a)
        • Kim H.A.
        • Lee H.
        Isolated vestibular nucleus infarction mimicking acute peripheral vestibulopathy.
        Stroke. 2010 Jul; 41: 1558-1560
        • Kato I.
        • Takeyama I.
        • Watanabe J.
        • Nakamura T.
        • Harada K.
        • Hasegawa Y.
        • et al.
        EOG findings in patients with lesions in cerebellar peduncles.
        Acta Otolaryngol. (Stockh.). 1991 Jan; 111: 260-261
        • Lee S.U.
        • Bae H.J.
        • Kim J.S.
        Ipsilesional limb ataxia and truncal ipsipulsion in isolated infarction of the superior cerebellar peduncle.
        J. Neurol. Sci. 2015 Feb; 349: 251-253
        • Kim S.H.
        • Kim J.S.
        Eye movement abnormalities in middle cerebellar peduncle strokes.
        Acta Neurol. Belg. 2019 Mar; 119: 37-45
        • Chen L.
        • Todd M.
        • Halmagyi G.M.
        • Aw S.
        Head impulse gain and saccade analysis in pontine-cerebellar stroke and vestibular neuritis.
        Neurology. 2014 Oct 21; 83: 1513-1522
        • Zhang Q.
        • Li J.
        Seesaw nystagmus with internuclear ophthalmoplegia from bilateral dorsomedial pons and left thalamus infarction: a case report.
        J. Med. Case Rep. 2019 Dec; 13: 352
        • Ogawa K.
        • Suzuki Y.
        • Oishi M.
        • Kamei S.
        Clinical study of twenty-one patients with pure midbrain infarction.
        Eur. Neurol. 2012; 67: 81-89
        • Kremmyda O.
        • Glasauer S.
        • Guerrasio L.
        • Büttner U.
        Effects of unilateral midbrain lesions on gaze (eye and head) movements.
        Ann. N. Y. Acad. Sci. 2011 Sep; 1233: 71-77
        • Saber Tehrani A.S.
        • Kattah J.C.
        • Mantokoudis G.
        • Pula J.H.
        • Nair D.
        • Blitz A.
        • et al.
        Small strokes causing severe vertigo: frequency of false-negative MRIs and nonlacunar mechanisms.
        Neurology. 2014 Jul 8; 83: 169-173
        • Makki A.A.
        • Newman N.J.
        A trochlear stroke.
        Neurology. 2005 Dec 27; 65 (1989–1989)
        • Walker A.E.
        • Botterell E.H.
        The syndrome of the superior cerebellar peduncle in the monkey.
        Brain. 1937; 60: 329-353
        • De Schutter E.
        • Adham Z.O.
        • Kattah J.C.
        Central positional vertigo: A clinical-imaging study.
        in: Progress in Brain Research [Internet]. Elsevier. 2019: 345-360 ([cited 2022 May 15]. Available from:)
        • Marti S.R.
        • Straumann D.
        • Glasauer S.E.
        The origin of downbeat nystagmus: an asymmetry in the distribution of on-directions of vertical gaze-velocity Purkinje cells.
        Ann. N. Y. Acad. Sci. 2005 Apr; 1039: 548-553
        • Park H.K.
        • Kim J.S.
        • Strupp M.
        • Zee D.S.
        Isolated floccular infarction: impaired vestibular responses to horizontal head impulse.
        J. Neurol. 2013 Jun; 260: 1576-1582
        • Lee H.
        • Yi H.A.
        • Lee S.R.
        • Lee S.Y.
        • Park B.R.
        Ocular torsion associated with infarction in the territory of the anterior inferior cerebellar artery: frequency, pattern, and a major determinant.
        J. Neurol. Sci. 2008 Jun; 269: 18-23
        • Yacovino D.A.
        • Akly M.P.
        • Luis L.
        • Zee D.S.
        The floccular syndrome: dynamic changes in eye movements and vestibulo-ocular reflex in isolated infarction of the cerebellar flocculus.
        Cerebellum. 2018 Apr; 17: 122-131
        • Lee S.H.
        • Park S.H.
        • Kim J.S.
        • Kim H.J.
        • Yunusov F.
        • Zee D.S.
        Isolated unilateral infarction of the cerebellar tonsil: ocular motor findings: tonsillar infarction.
        Ann. Neurol. 2014 Mar; 75: 429-434
        • Ogawa K.
        • Suzuki Y.
        • Akimoto T.
        • Morita A.
        • Hara M.
        • Yoshihashi H.
        • et al.
        Clinical study on 3 patients with infarction of the vermis/tonsil in the cerebellum.
        J. Stroke Cerebrovasc. Dis. 2018 Nov; 27: 2919-2925
        • Choi S.Y.
        • Jang J.Y.
        • Oh E.H.
        • Choi J.H.
        • Park J.Y.
        • Lee S.H.
        • et al.
        Persistent geotropic positional nystagmus in unilateral cerebellar lesions.
        Neurology. 2018 Sep 11; 91 (e1053–7)
        • Lee H.
        • Sohn S.I.
        • Cho Y.W.
        • Lee S.R.
        • Ahn B.H.
        • Park B.R.
        • et al.
        Cerebellar infarction presenting isolated vertigo: frequency and vascular topographical patterns.
        Neurology. 2006 Oct 10; 67: 1178-1183
        • Kim S.H.
        • Kim H.J.
        • Kim J.S.
        Isolated vestibular syndromes due to brainstem and cerebellar lesions.
        J. Neurol. 2017 Oct; 264: 63-69
        • Toudou-Daouda M.
        • Alecu C.
        • Chausson N.
        • Aminou-Tassiou N.R.
        • Smadja L.
        • Soumah D.
        • et al.
        Isolated cerebellar nodulus infarction: two case reports and literature review.
        J. Clin. Neurosci. 2021 Jul; 89: 161-164
        • Moon I.S.
        • Kim J.S.
        • Choi K.D.
        • Kim M.J.
        • Oh S.Y.
        • Lee H.
        • et al.
        Isolated nodular infarction.
        Stroke. 2009 Feb; 40: 487-491
        • Huh Y.E.
        • Kim J.S.
        Patterns of spontaneous and head-shaking nystagmus in cerebellar infarction: imaging correlations.
        Brain. 2011 Dec; 134: 3662-3671
        • Kim H.A.
        • Yi H.A.
        • Lee H.
        Apogeotropic central positional nystagmus as a sole sign of nodular infarction.
        Neurol. Sci. 2012 Oct; 33: 1189-1191
        • Young A.S.
        • Lechner C.
        • Bradshaw A.P.
        • MacDougall H.G.
        • Black D.A.
        • Halmagyi G.M.
        • et al.
        Capturing acute vertigo: a vestibular event monitor.
        Neurology. 2019 Jun 11; 92 (e2743–53)
        • Carmona S.
        • Martínez C.
        • Zalazar G.
        • Moro M.
        • Batuecas-Caletrio A.
        • Luis L.
        • et al.
        The Diagnostic Accuracy of Truncal Ataxia and HINTS as Cardinal Signs for Acute Vestibular Syndrome. Front Neurol [Internet].
        2016 Aug 8https://doi.org/10.3389/fneur.2016.00125/abstract ([cited 2022 Aug 17];7. Available from:)
        • Kim J.S.
        • Kim H.J.
        Inferior vestibular neuritis.
        J. Neurol. 2012 Aug; 259: 1553-1560
        • Green K.E.
        • Gold D.R.
        HINTS examination in acute vestibular neuritis: do not look too hard for the skew.
        J. Neuroophthalmol. 2021 Dec; 41 (e672–8)
        • Gold D.R.
        Brainstem Ocular Motor Machinery [Internet].
        ([cited 2022 Jun 10]. Available from:)
        • Gold D.R.
        The Utriculo-Ocular Motor Pathways - Physiologic and Pathologic Ocular Tilt Reaction: Physiologic Ocular Tilt Reaction (OTR) (Figure 1) [Internet].
        ([cited 2022 Jun 10]. Available from:)
        • Lance S.
        • Thomson T.
        Cerebellar nodulus infarction secondary to vertebral artery dissection.
        BMJ Case Rep. 2019 Apr; 12e229876
        • Ogawa K.
        • Suzuki Y.
        • Takahashi K.
        • Akimoto T.
        • Kamei S.
        • Soma M.
        Clinical study of seven patients with infarction in territories of the anterior inferior cerebellar artery.
        J. Stroke Cerebrovasc. Dis. 2017 Mar; 26: 574-581
        • Dieterich M.
        • Glasauer S.
        • Brandt T.
        Why acute unilateral vestibular midbrain lesions rarely manifest with rotational vertigo: a clinical and modelling approach to head direction cell function.
        J. Neurol. 2018 May; 265: 1184-1198
        • Newman-Toker D.E.
        • Kattah J.C.
        • Alvernia J.E.
        • Wang D.Z.
        Normal head impulse test differentiates acute cerebellar strokes from vestibular neuritis.
        Neurology. 2008 Jun 10; 70: 2378-2385