대한평형의학회지 제 4 권 1 호 2005 ; 145-158

Update on the Bedside Evaluation of the Dizzy Patient: the Angular and Transalational Vestibuloocular Reflex

David Zee The Johns Hopkins University, USA

Basic Physiological Principles

• Two types of acceleration sensors: angular (semicircular canals) and linear (otoliths) • Two reflexes: vestibulo-ocular reflex (VOR) and vestibulo-spinal reflex (VSR) • Functions: Assure clear vision during head motion (rotation and translation) and maintain upright posture during standing and walking

145 Update on the Bedside Evaluation of the Dizzy Patient: the Angular and Transalational Vestibuloocular Reflex

Central labyrinthine projections Innervation and Blood Supply of the Labyrinth: Clinical points SCC – rostral vestibular complex • Anterior vestibular artery is an end artery (hence most susceptible to ischemia). Thus posterior circulation hypoperfusion with isolated vertigo is a possibility albeit unusual to recur over the long term without other signs or symptoms. • Cochlear branch of the common cochlear -- posterior vestibular artery supplies the basal turn of the cochlea (high frequencies). Hence hearing loss in association with ischemic (and inflammatory) processes on the vestibular nerve is usually high OTOLITH – caudal frequency while with Ménière's disease vestibular complex (endolymphatic hydrops) the hearing loss with vertigo is usually low frequency. SCC / Otolith VESTIBULOCEREBELLUM

SCC Organization: a guide to nystagmus Central projections from the labyrinth Arrows indicate direction of • SCC projections are primarily to the rostral slow phase with stimulation portions of the vestibular complex. • Otolith projections are primarily to the caudal portions of the vestibular complex. Beware infarct in lateral medulla (Wallenberg’s syndrome) when symptoms and signs are isolated otolith (tilt, vertical diplopia due to skew (vertical misalignment of eyes). • SCC and otoliths also project directly to the cerebellum. Beware of cerebellar hemorrhage and Central Patterns infarct in elderly presenting as ‘labyrinthitis’, especially if they CANNOT walk, even with assistance. Peripheral Pattern

Why do vestibular patients complain so much in Visual-Vestibular Interaction: supermarkets, while driving, watching action movies? convergence of labyrinthine and visual inputs within the vestibular nuclei There is a strong convergence between vestibular and visual signals in the brainstem (vestibular nuclei) and cerebrum (vestibular cortex). Rotation in the In pathological circumstances, the visual and dark vestibular signals become incongruent, leading to abnormal sensations of motion and tilt, and discomfort, anxiety and phobias.

Pure visual (optokinetic) input

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Psychiatric disease and vertigo A physiological based exam • Disabling psychological effects of vestibular disease. – Phobic behavior. • Static disturbances due to a tone imbalance – Anxiety and panic attacks. with head still. – Depression and withdrawal. • Psychiatric disease presenting with vestibular • Dynamic disturbances due to abnormal responses symptoms during motion of the head – Somatization and psychosomatic disorders. – Obsessive compulsive behavior. – Panic attacks. – Depression.

Evaluation and treatment of psychiatric symptoms in vestibular patients should proceed in parallel with the ‘organic’ evaluation and treatment

Bedside Examination of the SCC – static disturbances LOCALIZATION OF NYSTAGMUS

– Peripheral lesions – Nystagmus is increased or brought out by removal of fixation (Romberg sign of VOR) – Mixed horizontal-torsional nystagmus is characteristic for complete loss of function on one side – Central lesions – Fixation has little effect on nystagmus – Pure vertical or pure torsional nystagmus

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Dynamic Visual Acuity (DVA)

Normal subjects lose only 1 line of acuity with head shaking. Patients with no vestibular function lose about 5 lines with horizontal or vertical rotation but not with rotation in ‘roll’ (ear to shoulder) since the image is still on the fovea. Patients who lose DVA in ‘roll’ are malingering!

Head-thrust sign in bilateral labyrinthine Technique to elicit thrusts (rotational VOR) loss and heaves (translational VOR) Catch-up saccades during brief, high- acceleration, head rotation (bilateral loss)

Remember: Patients who lose vestibular function bilaterally do NOT have vertigo since there is no tone imbalance or nystagmus. E.g., ototoxicity of antibiotics

Vestibular responses on the ‘head sled’ Quantification of t-VOR: ‘Head sled’ Normal subject

Cerebellar patient

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Pursuit -- Cerebellar patient

Head-shaking induced nystagmus

• Peripheral pattern: slow phase toward affected ear after horizontal head shaking • Central pattern: vertical nystagmus (usually DB) after horizontal head shaking (cross coupling) • Note that in Ménières disease the initial slow phase may be toward the intact ear. Can not use the direction of nystagmus to decide the affected ear in Ménières disease. Must use audiogram and hearing.

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Mechanisms for hyperventilation-induced Congenital Epidermoids nystagmus

• Usually appear in adolescence • Improved conduction on demyelinated fibers • Males > females (alkalosis, calcium). • Change in intracranial pressure mediated • Hemifacial spasms may precede frank through a fistula. facial palsy • Seizures. • Ischemia (decreased blood flow).

Recovery nystagmus

• After a unilateral peripheral loss of vestibular function there is a central rebalancing to eliminate the spontaneous nystagmus. • If peripheral function suddenly “recovers” (e.g., by improved conduction on demyelinated nerves because of pH changes due to hyperventilation), a new imbalance is created causing a recovery nystagmus with slow phases directed away from the affected ear.

Fistula due to dehiscence of the roof of the superior SCC

Intact side Abnormal side Lloyd minor CT temporal bone 0.5mm slices with 3D reconstruction

Beldon, Radiology 2003

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Audiograms in superior canal dehiscence Vestibular-evoked myogenic potentials (VEMPS)

Air-bone gap • Short-latency, relaxation potentials measured from tonically-active sterno- cleido-mastoid muscle that relax with Case1 Lowered threshold ipsilateral loud clicks. for bone-conducted • Originate from the sacculus (inferior hearing division of vestibular nerve) • 10 Hz, 0.1ms, 60-103 dB

Case2

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Syndrome of dehiscence of the roof of the superior canal

• Vertigo, oscillopsia, and/or dysequilibrium related to noise, altered middle ear pressure, exercise and/or altered intracranial pressure (e.g., Valsalva maneuvers, jugular vein compression). • Changes in symptoms with head position; chronic dysequilibrium. • Auditory findings – Gaze-evoked and pulsatile tinnitus – Hyperacusis – lowered thresholds for bone conduction with air-bone but with normal tympanogram – ‘Malleolus sign’ (hears vibration at ankle!) – Lowered threshold for click-induced EMG of sternocleidomastoid (VEMPs)

Syndrome of dehiscence of the roof of the superior canal Migraine and • Induced vertical-torsional eye movements (with the vestibular sound or valsava maneuvers) that can be system explained by activation of the superior canal. • Temporal bone CT scans identify dehiscence of bone overlying the affected superior semicircular canal. • Beware some normals without symptoms have thin bone. Von Brevern, Brain, 2004; Neurology 2004 • Beware false positives (especially with > 0.5mm Furman, JNNP,2005 sections). Neuhauser, Cephalgia, 2004 • Symptoms relieved by plugging of the superior canal (if necessary). Crevitz, Clinical Neurology Neurosurgery, 2005 Brantberg, Acta Otolaryngologica, 2005

Some ‘facts’ about vestibular migraine Some ‘facts’ about vestibular migraine

• In a “dizziness clinic” 38% of patients were • The mean onset of vertigo in migraine is about 40 diagnosed with migraine (24% in an orthopedics clinic); 7%, with migrainous vertigo, and in a yrs of age, and headaches precede vertigo by “migraine clinic”, 9% diagnosed with migrainous almost 10 years. Women much more likely to be vertigo. (Neuhauser). diagnosed with vertigo and migraine. • Other studies suggest that more than 50% of • Duration of symptoms is usually minutes to a day migraineurs have vestibular symptoms (including but ‘low-level’ symptoms may last days to weeks – dizziness)! imbalance and extreme motion sensitivity • In patients with dizziness and migraine, • Patient may have hearing symptoms; muffled abnormalities on vestibular lab testing are common, sounds, ear pressure or pain, tinnitus. but often nonspecific. – up to 25% of migraineurs with dizziness have been • Patients overall often have chronic motion reported to have a reduced caloric response. (CAUTION sensitivity. (Syndrome of mal de debarquement). ADVISED HERE). • Migraine headaches are often an infrequent or – Interictal, central eye movement abnormalities (e.g., gaze-evoked nystagmus, impaired pursuit) have been long-forgotten symptom in vestibular migraine. reported in as many as 65% of patients with migraine • Migraine headaches may occur independently of and vestibular symptoms. (CAUTION ADVISED HERE but note reports of subclinical cerebellar dysfunction vestibular symptoms and vice versa. Often they (limb dysmetria) in migraine.) never occur together.

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Some ‘facts’ about vestibular migraine Differential diagnosis of vestibular migraine • Vestibular neuritis, neuronitis, labyrnthitis, • Family history is usually positive and neurolabyrinthits attacks of vertigo may be the predominant – Isolated attack of acute vertigo, nausea, symptom in some family members. dysequilibrium, previous URI. • Light sensitivity is common in migraineurs – Head thrust sign with abnormal caloric response. – May be viral (Rx, with prednisone and antivirals) or during their attacks of vertigo. ischemic (relative poor collateral circulation to the • Panic, anxiety and phobic behavior are structures perfused by the anterior vestibular artery common in patients with vertigo and (supplies the lateral semicircular canal)). – Remember inflammatory disorders (e.g., Lyme, migraine. Syphilis). – (A first and severe attack of vestibular migraine may be difficult to distinguish from above) • Benign Paroxysmal Positional Vertigo (BPPV); perhaps triple the incidence in migraine patients.

Differential diagnosis of vestibular migraine Differential diagnosis of vestibular migraine • Ménière's disease – Pain, pressure, fullness in ear, loss of hearing • Remember episodic ataxia 2 (EA2) – familial, which may precedes vertigo and aural symptoms periodic, diamox-responsive vertigo and ataxia may disappear with vertigo (Lermoyez syndrome). (calcium channel on chromosome 19, as is – Fluctuating tinnitus, low-pitched, sea-shell. familial hemiplegic migraine). – Fluctuating hearing loss, often low-frequency. – Onset relatively young in life. GET AUDIOGRAMS – Precipitated by emotion or exercise. – Eventually develop interictal downbeat nystagmus and – Attacks of vertigo, hours to a day or two. other cerebellar eye signs. – Otolithic crises of Tumarkin – patient is suddenly • Temporal lobe epilepsy (tornado epilepsy), thrown to the ground. especially in children. – May be due to autoimmune disease or as a late • Variety of central disorders sequela of inner ear viral infection. – Tumors in the posterior fossa, – Transtympanic electrocochleography (ECOG). – Cranio-cervical junction anomalies (Chiari Increased co-morbidity with migraine (Radtke). malformation) – Valsalva-induced symptoms. – Vertigo attacks can be effectively treated with intratympanic gentamicin BUT be sure of dx. – Demyelination. – “Vestibular Ménière's” is commonly migraine. – Posterior circulation ischemia – Vertebral artery dissection.

Differential diagnosis of vestibular migraine Differential diagnosis of vestibular migraine

• Microvascular compression (VIII) • Perilymphatic fistula syndrome – post-traumatic or spontaneous and also associated with congenital temporal bone – paroxysms (seconds) of tinnitus or vertigo, anomalies (e.g., Mondini). – sustained motion sensitivity, – Hearing loss is usually prominent. Chronic – chronic dysequilibrium, dysequilibrium. – positionally-induced symptoms, – May have positional symptoms. – hyperventilation-induced nystagmus, • Large vestibular aqueduct syndrome – abnormal BAER. – early onset hearing loss recurrent vertigo. – respond to AED. – often precipitated by exercise or mild head trauma. – diagnosed by MRI or CT.

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DDx of Vestibular Migraine Treatment of vestibular migraine

• Meniere’s syndrome • EDUCATION (e.g., educational video) • Acute labyrinthitis (viral,ischemic) • Appropriate physical therapy – e.g., Tai Chi • BPPV (high incidence in migraine) exercises. • Episodic ataxia and vertigo (EA1) • Eliminate provocatives, e.g. diet?? • ‘Tornado epilepsy’ • Psychological management (stress, depression) • Miscellaneous – MS, vestibular schwannoma, autoimmune, • The usual migraine prophylactics (AEDs) infection, posterior circulation (dissection, tia), temporal – Neurontin, topiramate, depakote, oxycarbamazepine?? bone abnormalities (dehiscence and large vestibular – Triptans ?? aqueduct syndrome), microvascular compression, – Tricyclics, beta blockers, calcium channel blockers?? perilymphatic fistula, Chiari malformation and other • Acetazolamide?? posterior fossa lesions • Benzodiazepams??

Benign Paroxysmal Positional Vertigo (BPPV) Benign Paroxysmal Positional Vertigo (BPPV) • Posterior SCC becomes gravity sensitive due to • Easily diagnosed by history and exam floating debris (otoconia • Pathophysiology well understood dislodged from the • Easily treated macula of the utricle) • Patients gratified • Otoconia get trapped in the posterior SCC on the cupula (CUPULOLITHIASIS) or are free-floating in the long arm of the canal (CANALOLITHIASIS).

Otoconia in BPPV (CUPULOLITHIASIS) Otoconia in BPPV (CANALOLITHIASIS)

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BPPV: Otoconia in posterior SCC

From SCC in BPPV patient From intact at the time of surgery otolith

BPPV -- Symptoms BPPV -- Etiology

• Transient vertigo precipitated by a change in • Idiopathic (especially elderly) attitude of the head relative to gravity • Post traumatic (may be mild, e.g. (offending ear down, e.g., turning over in bed, whiplash, riding a bicycle on rough looking to a high shelf, getting out of or into bed), or by exposure to imposed linear terrain) acceleration (elevator, car) • Prolonged bed rest or unusual postures • Tumbling, rolling, cartwheeling sensation, with (hair dresser, dentist, working under nausea, vomiting and imbalance one’s car) • Chronic unsteadiness • Post labyrinthitis (viral or ischemic) which • Symptoms typically maximum for days to weeks, spares the inferior division of the usually resolves in months, but often recurs vestibular nerve (posterior SCC intact)

BPPV -- Signs Nystagmus in BPPV from right SCC

• Mixed vertical-torsional nystagmus, slow phases Direction of downwards and top of eyes roll away from Slow-phase offending (dependent) posterior SCC. • Elicited in the Dix-Hallpike maneuver (head turned 45 deg then body and head moved en bloc straight back). • Nystagmus more vertical when looking toward the up ear, and more torsional when looking toward the down ear. • Latency (up to 30sec), transient (usually less than 15sec), decreases with repetitive testing. • Reverses direction on sitting up. • If cupulolithiasis, more sustained, less ‘habituation’ with repetitive testing.

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BPPV – Treatment for posterior SCC variant

• Do nothing -- avoid offending position • Epley maneuver -- Roll of head from offending ear down to offending ear up. • Semont maneuver – 180 deg cartwheel of torso from offending ear down and nose up to offending ear up and nose down, slow rise.

Post-treatment instructions

• Do not bend over or look up for rest of the day. Keep head in neutral position • Watch for sudden transient imbalance immediately after treatment • Sit still in clinic for about 20 minutes before walking away • Avoid sleeping on offending side for several nights. • Retreatment in one week for 20-30% of cases • Home exercise program – Web site http:www.charite.de/ch/neuro/vertigo.htm • Almost never necessary is surgery -- canal plugging, singular nerve section

Treatment exercises for left BPPV Treatment exercises for right BPPV

http://www.charite.de/ch/neuro/vertigo.html http://www.charite.de/ch/neuro/vertigo.html

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Lateral canal BPPV Lateral canal BPPV

• Elicit in ‘Barany position”, right or left ear down. • Geotropic, direction-changing (beats to the ground) (usually canalolithiasis). More intense with affected ear down. • Apogeotropic, direction changing (beats to the sky) (occasionally cupulolithiasis). Von Brevern More intense with affected ear up. Neurology, 2001

Lateral canal BPPV Treatment -- Lateral canal BPPV

• If canalolithiasis (on cupula) may have – Log rolling (toward intact side). small spontaneous nystagmus with eyes in – Single, repositioning maneuver. straight ahead position (slow phase – Lie for 11 hours with affected side up. toward affected ear) with head upright. – Note, if ‘iatrogenic’, i.e., after repositioning • There may be a null with head slightly maneuver for posterior canal BPPV, usually disappears spontaneously in a day or two. pitched forward. • If supine and turn to either side, the null is toward the affected side.

Treatment of lateral canal (geotropic, beats toward the ground) BPPV Tilt OPPOSITE the affected side

Appiani, ONO, 2001

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Orientation of canals in left labyrinth with Rx of right-sided head upright* apogeotropic (beats toward the sky) lateral canal BPPV Tilt TOWARD the affected side

Bertholon JNNP 2002

Casini, Laryng, 2002

Anterior canal BPPV producing vertical nystagmus with head in either Dix-Hallpike Anterior canal BPPV position*

• Downbeat nystagmus with torsional component (may be small). • Elicited in both Dix-Hallpike positions and especially with head hanging. • Exclude central problems (cerebellar lesions and multisystem atrophy (MSA)). Bertholon • Treatment?? JNNP 2002

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