Title | Dizziness and Vertigo: The Skillful Examination |
Creator | Ari A. Shemesh; Daniel R. Gold |
Affiliation | Department of Neurology (AAS, DRG), the Johns Hopkins University School of Medicine, Baltimore, Maryland; and Departments of Ophthalmology (DRG), Otolaryngology-Head and Neck Surgery, Neurosurgery and Emergency Medicine, the Johns Hopkins University School of Medicine, Baltimore, Maryland |
Abstract | Background: The visual, ocular motor and vestibular systems have intimate neural and close anatomical relationship that dictates their assessment in a patient with dizziness and vertigo. Results: Recognition of the pearls and pitfalls of a targeted clinical examination HINTS/HINTS 'Plus' allows the clinician to probe at the bedside the most crucial hypothesis in a patient with acute isolated vestibular syndrome, 'Is this a stroke?' Conclusion: By applying a methodical approach to examination of patients with dizziness and vertigo, localization of the offending lesion, management, and even elucidation of the underlying diagnosis is feasible. |
Subject | Dizziness / diagnosis; Dizziness / etiology; Eye Movements / physiology; Humans; Vertigo / complications; Vertigo / diagnosis; Visual Acuity |
OCR Text | Show Trainees' Corner Dizziness and Vertigo: The Skillful Examination Ari A. Shemesh, MD, Daniel R. Gold, DO Background: The visual, ocular motor and vestibular systems have intimate neural and close anatomical relationship that dictates their assessment in a patient with dizziness and vertigo. Results: Recognition of the pearls and pitfalls of a targeted clinical examination HINTS/HINTS "Plus" allows the clinician to probe at the bedside the most crucial hypothesis in a patient with acute isolated vestibular syndrome, "Is this a stroke?" Conclusion: By applying a methodical approach to examination of patients with dizziness and vertigo, localization of the offending lesion, management, and even elucidation of the underlying diagnosis is feasible. Journal of Neuro-Ophthalmology 2020;40:e49-61 doi: 10.1097/WNO.0000000000000980 © 2020 by North American Neuro-Ophthalmology Society T he approach to the clinical examination in patients with dizziness and vertigo is based on functional assessment of 3 systems, which have intimate neural and/or close anatomical relationship-the visual, ocular motor and vestibular systems (Tables 1-4). Here, the emphasis will be on the HINTS (3 step ocular motor examination) and HINTS "Plus" (HINTS + a fourth step where auditory function is evaluated using finger rub) examinations, which are targeted assessments used in the acute vestibular syndrome (AVS). The AVS is defined as continuous dizziness/vertigo for .24 hours, associated with imbalance, head motion intolerance, nausea, vomiting, and spontaneous nystagmus (SN). In the AVS, focused history and general neurologic examinations alone are usually unable to distinguish central (stroke) from peripheral (vestibular neuritis [VN]) disorders, so Department of Neurology (AAS, DRG), the Johns Hopkins University School of Medicine, Baltimore, Maryland; and Departments of Ophthalmology (DRG), Otolaryngology-Head and Neck Surgery, Neurosurgery and Emergency Medicine, the Johns Hopkins University School of Medicine, Baltimore, Maryland. The authors report no conflicts of interest. Address correspondence to Daniel R. Gold, DO, the Johns Hopkins Hospital, 600 N Wolfe Street, Pathology 2-210, Baltimore, MD 21287; E-mail: Dgold7@jhmi.edu Shemesh and Gold: J Neuro-Ophthalmol 2020; 40: e49-e61 HINTS/HINTS "Plus" (referred to below as HINTS+) examinations should be used. The HINTS/HINTS+ examination is superior to even MR with diffusion weighted imaging (DWI) in the first 24-72 hours, with sensitivities to detect an acute stroke using HINTS and HINTS+ of 96.5% and 99.1%, respectively, and specificities using HINTS and HINTS+ of 84.4% and 83.1%, respectively (1,2). The HINTS examination consists of 3 ocular motor/ vestibular signs: head impulse, nystagmus, and test of skew. In the AVS, each individual element can be classified as "peripheral" or "central." However, even if 2 signs appear peripheral (e.g., unidirectional nystagmus and negative test of skew) but one follows a central pattern (e.g., normal head impulse test [HIT]), then the etiology of all HINTS findings must be assumed central until proven otherwise. The internal auditory artery is a branch of anterior inferior cerebellar artery (AICA) that supplies the labyrinth (3). Therefore, in the AVS, a new unilateral hearing loss and/or prominent tinnitus is suspicious for labyrinthine ischemia, particularly in a patient with vascular risk factors. Accordingly, the HINTS+ examination adds a fourth element, which is intended to identify acute unilateral sensorineural hearing loss. The HINTS+ examination can be thought of as a test to differentiate benign peripheral (VN) from dangerous peripheral (labyrinthine ischemia). HEAD IMPULSE TEST: PERIPHERAL PEARLS 1. Per HINTS/HINTS+, an abnormal/positive HIT in the plane of the horizontal canal (HC) must be seen to reassure the clinician that the patient has a peripheral etiology (see example-https://collections.lib.utah.edu/ ark:/87278/s6x398q2) (4). Because VN almost always involves the HC afferents (HC and anterior canal [AC] are innervated by the superior division of the vestibular nerve), the HIT should be abnormal in peripheral etiologies with few exceptions. e49 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Trainees' Corner TABLE 1. Assessing vision, pupils, and eyelids (22) Test Why? Visual function Selecting (and interpreting) the most appropriate bedside test(s) 1. Monocular visual acuity (best corrected) depends on the patient's visual function 2. Visual fields to confrontation Afferent abnormalities can provide clues to etiology (e.g., 3. Color vision interstitial keratitis in Cogan syndrome) Pearls Unilateral or bilateral optic neuropathy is common in patients with dizziness/ocular motor disorders related to multiple sclerosis; retinal abnormalities can be a feature of mitochondrial disorders, spinocerebellar ataxias (SCA 7), Susac syndrome, each of which can cause imbalance, dizziness, and/or ocular motor abnormalities Recognition of a homonymous hemianopia can assist in localization and etiology, especially with acute vertigo Dynamic visual acuity (DVA) Bilateral vestibulopathy Can be performed without glasses or contacts because A decrement of at least 4 lines of acuity is common the difference between static and dynamic acuity is Unilateral vestibulopathy being assessed When uncompensated, a decrement of 2-3 lines of acuity is 1. Record static binocular visual acuity common; horizontal DVA is often more impaired than 2. Oscillate the head horizontally and vertically (w2 Hz) vertical DVA while asking the patient to read the acuity chart Pearls An efferent abnormality (e.g., an abduction deficit from sixth nerve palsy) can affect DVA, even if the vestibular function is normal Abnormal DVA does not allow for lateralization of unilateral vestibular loss DVA improvement is seen with vestibular recovery, making it a useful bedside measure in rehabilitation Pupils and eyelids Horner syndrome (sympathetic) Pupils Anisocoria greater in dim lighting with a pupillary dilation lag; 1. Evaluate pupillary size in light and dark ipsilateral ptosis; anhidrosis-common in lateral medullary 2. Evaluate pupillary dilation and constriction syndrome (with associated skew, nystagmus, and ocular 3. If pupillary constriction is poor, evaluate the lateropulsion) response to a near target Third nerve palsy (parasympathetic) Eyelids Could see a complete or partial third nerve palsy with 1. Measurements of palpebral fissure, marginal reflex a vertebrobasilar vascular event distance, levator function, and lid creases (can differentiate mechanical ptosis from neurologic causes) Pearls Consider ophthalmic causes of anisocoria (e.g., uveitis, trauma, and surgery) and ptosis (e.g., trauma, surgery, and levator dehiscence) 2. Acute unilateral vestibular loss (UVL) a. A patient presenting with acute VN usually has an obvious (ipsilesional) abnormal HIT with catch-up (or "overt") saccades. https://collections.lib.utah.edu/ark:/87278/s62n91vq) (5). In these cases, HIT should have variable amplitude and be unpredictable-this can help to unmask overt saccades in patients who have developed effective coverts (6) (see example available at https://collections. lib.utah.edu/ark:/87278/s6r53kbq) (7). 3. Subacute to chronic UVL a. Patients with longer standing UVL may seem to have a normal HIT. Following a bout of VN, compensatory processes begin almost immediately. Neck proprioceptive afferents and/or efference copy signals converge on the vestibular nuclei to compensate for the deficient VOR, and "covert" saccades develop in response. As opposed to the overt saccades that are visible after the HIT, covert saccades are compensatory and occur during the HIT. Although covert saccades are not seen with HIT, covert and overt saccades can easily be seen with video HIT (vHIT, additional reading on vHIT- e50 4. Rarely, patients with VN only have involvement of the inferior division of the vestibular nerve, and as opposed to the mixed horizontal-torsional nystagmus seen in typical VN, patients will have downbeat-torsional SN and abnormal HIT in the plane of the ipsilesional posterior canal (PC). Given the proximity to and innervation of the cochlea, tinnitus and hearing loss may occur as well. In this situation, while the PC is involved, the HC is spared, so that the horizontal HIT is normal. Per HINTS+, the combination of normal (HC) HIT, vertical-torsional SN, and/or auditory symptoms are all suggestive of stroke and may lead to misdiagnosis. Shemesh and Gold: J Neuro-Ophthalmol 2020; 40: e49-e61 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Trainees' Corner TABLE 2. Assessing motility, ocular alignment, and subjective visual vertical (22) Test Test Rationale and/or Procedure Motility Can help differentiate restrictive or paralytic strabismus 1. Patient looks in the 9 cardinal positions of gaze with (e.g., sixth nerve palsy or internuclear ophthalmoplegia the eyes viewing together (versions) [INO]) from nonparalytic strabismus (e.g., infantile 2. With diplopia or when a motility deficit is suspected, esotropia or skew deviation) this is repeated with each eye individually viewing (ductions) Pearls A motility deficit, by itself, cannot distinguish paresis from restriction Versions and ductions can miss subtle motility deficits-both range of motion and ocular alignment must be assessed in patients with diplopia or strabismus Ocular alignment (objective) 1. Hirschberg (tropia) 1. Hirschberg Patient looks at a penlight, and the corneal light 2. Alternate cover reflections are compared to see whether there is 3. Cover-uncover decentration of the reflex on one pupil 4. Fundus torsion 2. Alternate cover test (phoria or tropia) What is the eye position? Patient fixates on a visual target while the examiner 1. Eso-eyes crossed (e.g., lateral rectus palsy) alternatively occludes each eye, while the examiner 2. Exo-eyes deviate outward (e.g., medial rectus looks for a refixation movement as each eye is palsy) uncovered 3. Hyper-the nonfixating eye is higher 3. Cover-uncover (tropia) 4. Hypo-the nonfixating eye is lower Patient fixates on a visual target, and as one eye is Is it a misalignment with one or both eyes viewing? covered, the examiner looks for a movement in the 1. Tropia-misalignment with both eyes viewing opposite eye; needed to determine whether (e.g., paralytic disorders) a deviation seen with alternate cover is a tropia or 2. Phoria-misalignment with one eye viewing (e.g., phoria horizontal phorias are often normal) 4. Fundus torsion (pupillary dilation is often needed) Most helpful in skew deviation vs fourth nerve palsy Skew-hypertropic eye is incycloducted and hypotropic eye is excycloducted (referred to as ocular counterroll) Fourth nerve palsy-hypertropic eye is excycloducted Pearls Use Hirschberg test for uncooperative patients and patients with poor vision, although it is inexact (known as the Krimsky test when prism is used to quantify the deviation seen with Hirschberg) Cover-uncover and alternate cover tests do not work if the presented fixation target cannot be seen each eye individually Small horizontal phorias are common and usually normal while vertical deviations usually suggest pathology 1. Maddox rod test Ocular alignment (subjective) A lens composed of small parallel cylinders refracts 1. Maddox rod test-by convention a red lens is placed light, so that a pinpoint of light is seen in the right over the right eye, and a penlight is directed at the eye as a red line of light 90° to the orientation of the patient; the patient is asked if the white light is to cylinder, measures the total deviation (tropia plus the side, above, below, or is touching the red line phoria) 2. Double Maddox rod-by convention a red lens is 2. Double Maddox rod test placed over the right eye, a white lens over the left eye, and a penlight is directed at the patient, and If there is a vertical deviation, the red and white lines the red and white lines are compared will not be superimposed, and if cycloduction is present in either eye, the 2 lines will not be parallel (helpful to distinguish skew vs fourth nerve palsy) Pearl Maddox rod is particularly helpful in patients with nystagmus, small vertical deviations (e.g., due to skew), and in patients with mixed strabismus because horizontal and vertical deviations can be measured separately Shemesh and Gold: J Neuro-Ophthalmol 2020; 40: e49-e61 e51 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Trainees' Corner (Continued ) Test Test Rationale and/or Procedure Subjective visual vertical (SVV) Peripheral or central vestibulopathy A measurement of vertical perception or subjective The SVV will be tilted with unilateral or lesions affecting torsion the utriculo-ocular motor pathways, from labyrinth to Bucket test (can be performed binocular or monocular) vestibular cortex 1. Patient is upright, looking at a vertical bar inside The SVV can be believed of as the perceptual a bucket consequence of the ocular tilt reaction (OTR-skew 2. The opening of the bucket covers the patient's deviation, head tilt, and ocular counterroll) face (eliminates visual cues) and is held by the The head tilt, ocular counterroll, and SVV tilt will be in examiner (eliminates proprioceptive cues) the same direction: 3. The bucket is slowly rotated from an eccentric For example, right lateral medullary stroke causing position (starting from the right and from the left) ipsilesional (rightward) head tilt, ocular counterroll, to earth vertical SVV tilt-lesion involves the utriculo-ocular motor 4. When the patient thinks the line is perfectly vertical pathway caudal to its decussation (subjective vertical), this is recorded and compared For example, left INC stroke causing contralesional with the position of a weighted string and protractor (rightward) head tilt, ocular counterroll, SVV tilt- on the bottom outside the bucket (actual vertical) rostral to the decussating fibers Pearls Monocular SVV can help differentiate skew (SVV tilted in the same direction in both eyes) from fourth nerve palsy (SVV tilted in the affected hypertropic eye due to excycloduction) Lesions involving the thalamus or vestibular cortex can cause SVV tilts ipsilesionally or contralesionally However, this disorder is rare, so it is appropriate to first rule out a central etiology and retrospectively attribute the AVS to the inferior division variant of VN (8). With regard to the otoliths, the inferior division of the vestibular nerve only innervates the saccule while the superior division mainly innervates the utricle (minor innervation of the saccule as well). Therefore, cervical (a test of the saccule pathway) and ocular (a test of the utricle pathway) vestibular evoked myogenic potentials (VEMPs, additional reading on VEMPs-https://collections.lib. utah.edu/ark:/87278/s66d9smh) (9), along with knowledge of the affected semicircular canal(s), may be helpful to establish a superior or inferior division VN pattern. IT IS PERIPHERAL: JUST TELL ME WHAT I NEED TO KNOW! 1. A patient with acute VN should have a fairly obvious abnormal ipsilesional bedside HIT a. Exceptions and utility of vHIT (10): 1) inferior division VN sparing the HC-with vHIT, all 6 semicircular canals can be assessed; 2) a patient with effective covert saccades (invisible at the bedside)-with vHIT, covert saccades are clearly seen; and 3) a patient with mild VN-with vHIT, not only are covert and overt saccades seen, but the gain (eye movement velocity [output] to head movement velocity [input]) is also calculated. (a one-step test) in the AVS has a 90.3% sensitivity and 87% specificity to detect an acute stroke (compare to HINTS and HINTS+ above) (1,2). HEAD IMPULSE TEST: CENTRAL PEARLS 1. Per HINTS/HINTS+, a normal/negative HIT is highly suggestive of a central etiology (https://collections.lib. utah.edu/ark:/87278/s6g776f7) (11). 2. Although an abnormal HIT can occasionally be seen in stroke or other conditions, in those cases, one or more of the other HINTS+ examination features will be in a central or dangerous pattern. Abnormalities in saccades (e.g., ipsilesional hypermetria and contralesional hypometria in a lateral medullary stroke) and smooth pursuit (e.g., low gain will cause a saccadic or choppy appearance since the impaired pursuit system will not be able to maintain fixation on the visual target, the eyes lag behind, and saccades supplement the deficient pursuit system) often help with localization as well. The following are examples of central or dangerous causes of an abnormal HIT: a. Stroke involving nucleus prepositus hypoglossi (NPH) or flocculus. b. An abnormal HIT in the AVS is not always peripheral (see below Central Pearls)-using the HIT by itself i. Abnormal HIT contralesionally, and associated ipsilesional SN, gaze-evoked nystagmus (GEN -greater ipsilesionally), and impaired horizontal smooth pursuit (SP, ipsilesionally) (12-14). e52 Shemesh and Gold: J Neuro-Ophthalmol 2020; 40: e49-e61 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Trainees' Corner TABLE 3. Assessing ocular motor function (22) Test Gaze holding 1. Straight ahead fixation 2. Eccentric fixation (horizontal and vertical) Why? To look for spontaneous or gaze-evoked movements Nystagmus-the slow phase is the culprit and initiates the movement Saccadic intrusions/oscillations-a saccade is the culprit and initiates the movement (e.g., square wave jerks, flutter and opsoclonus) Pearl Mild right-beating nystagmus in right gaze and left-beating nystagmus in left gaze that fatigue are usually physiologic endpoint nystagmus; resolve when the target is moved back, so both eyes can foveate the target (small target is best) Convergence When vertical nystagmus is present, convergence can Examiner moves a small fixation target toward the increase, suppress, or change direction of nystagmus patient's nose When binocular horizontal diplopia at near is experienced, convergence insufficiency is a common cause, especially with head trauma or parkinsonism Pearls The conversion of upbeat to downbeat nystagmus is common in Wernicke encephalopathy Infantile nystagmus is typically suppressed by convergence Downbeat nystagmus is typically accentuated with convergence Saccades Saccades can help with localization-hypermetric The patient is presented with 2 targets (e.g., ipsilesional and hypometric contralesional in lateral examiner's nose and a fingertip held eccentrically) medullary syndrome and instructed to redirect gaze on command Saccades can help with etiology-slow saccades (and between horizontal and vertical (occasionally whether they are slow vertically and/or horizontally) can diagonal) targets narrow the differential when a neurodegenerative The examiner evaluates the following: disorder is suspected (e.g., slow downward saccades 1. Latency (prolonged?) are often seen first in progressive supranuclear palsy, 2. Accuracy (dysmetric?) PSP) 3. Velocity (too slow?) 4. Conjugacy (e.g., adduction lag in INO?) Pearls Saccades that are only slow vertically-think rostral interstitial medial longitudinal fasciculus (riMLF-usually down worse than up) Saccades that are only slow horizontally-think paramedian pontine reticular formation (PPRF) Patients with acquired increased latency of saccades (so-called ocular motor apraxia) can lose voluntary saccades but retain quick phases of optokinetic and vestibular nystagmus Smooth Pursuit Smooth pursuit and localization The patient is asked to follow a slowly moving target in Unilateral horizontal pursuit impairment indicates horizontal and vertical planes ipsilesional localization (frontal/parietal cortex, pons) Corrective "catch-up" movements (saccades) are seen Vertical pursuit ("up-down") asymmetry can be seen in cerebellar disease, and downbeat nystagmus is when smooth pursuit is impaired (gain is too low), hypothesized to be one consequence which gives a "saccadic" or "choppy" appearance Pearls Inattention, aging, and medications can all impair smooth pursuit Severe smooth pursuit impairment in all directions is seen in patients with diffuse cerebellar disease Spontaneous or gaze-evoked nystagmus can confound evaluation of smooth pursuit Vestibulo-ocular reflex suppression (VORS) During combined eye-head tracking of moving objects, the A combined eye-head movement that can be assessed pursuit system will keep the eyes on the target while in several ways-for example, the patient is asked the normal VOR would move the eyes away from the to fixate on their thumb with the arm outstretched as fixation target; therefore, the VOR must be suppressed the head and body are passively rotated (e.g. in or cancelled at times to maintain fixation (foveation) a rotating chair) Pearls VORS and smooth pursuit are usually both normal or both abnormal (saccadic/choppy), unless there is cerebellar disease (impaired pursuit) and bilateral vestibular loss (pursuit will be impaired while VORS will look normal or less saccadic)-this is because there is no VOR to suppress (e.g., cerebellar ataxia, neuropathy, vestibular areflexia syndrome, called CANVAS) Shemesh and Gold: J Neuro-Ophthalmol 2020; 40: e49-e61 e53 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Trainees' Corner (Continued ) Test Why? Optokinetic nystagmus (OKN) The patient is asked to follow moving stripes on a banded cloth (optokinetic flag or tape) or on an optokinetic drum 1. Slow phases-combined response of 2 tracking mechanisms (smooth pursuit and optokinetic system) 2. Fast phases-these are saccades An optokinetic stimulus can reveal pursuit or saccade impairments or asymmetries, such as an adducting lag in an internuclear ophthalmoplegia. One of the earliest ocular motor signs in PSP may be the loss of downward fast phases with an optokinetic stimulus. Allows the examiner to quickly assess for impairment and symmetry in pursuit and saccadic systems, even in uncooperative patients. Pearl OKN will not be generated when vision in both eyes is poor (worse than w20/400). However, a patient who is fixating on a stationary object across the room (instead of the optokinetic stimulus) may seem to have an absent optokinetic response-this can be a clue to a functional disorder. Vestibulo-ocular reflex (VOR) vVOR The head is rotated horizontally and vertically while the Corrective saccades ("choppy" appearance) opposite patient fixates on a target (e.g., examiner's nose) to the head rotation indicate deficits in smooth 1. Slow rotational or visually enhanced (vVOR) pursuit and VOR (characteristic clinical sign in 2. Fast rotational (head impulse test or HIT)-the head CANVAS) is quickly rotated from the center to 15° to right or HIT left, or by turning the head 15° right or left and then The examiner looks for a catch-up movement after the rotating the head back to center HIT, which indicates impairment of the VOR Helpful to diagnose unilateral or bilateral vestibular loss; differentiate peripheral (e.g., vestibular neuritis- abnormal HIT) from central (e.g., stroke-normal HIT) Pearls In patients with alternating fixation strabismus, the clinician should patch or occlude one eye Rotating the head from an eccentric position back to center is favored in patients with robust eccentric nystagmus, limited passive cervical range of motion, or known cervical disease Ocular motor dysfunction (e.g., sixth nerve palsy) will affect the appearance of the HIT, even when vestibular function is normal b. Stroke involving vestibular nucleus i. Abnormal HIT ipsilesionally, and associated contralesional SN, GEN (greater contralesionally), and impaired horizontal SP (contralesionally) (15). c. Wernickes encephalopathy i. This is due to thiamine deficiency and the classic triad of findings includes ophthalmoparesis (e.g., sixth nerve palsy [NP]), ataxia, and altered mental status. However, the classic triad occurs in less than 20% of patients. When suspected, IV thiamine should be given immediately. The medial vestibular nuclei (MVN) are susceptible to thiamine deficiency, which can cause bilateral horizontal vestibulo-ocular reflex (VOR) impairment and bilaterally abnormal HIT. Given the role of the MVN in neural integration, GEN is also common. Involvement of nearby dorsal medullary nuclei (nucleus intercalatus and nucleus of Roller) may explain spontaneous upbeat nystagmus (16) (see example-https://collections.lib. utah.edu/ark:/87278/s6h74j6d) (17). e54 d. AICA territory ischemia i. The AICA perfuses the labyrinth, vestibulocochlear nerve, and its root entry zone, cerebellum, and dorsolateral pons (including cochlear nucleus and vestibular nuclei). Therefore, in the AVS, AICA territory strokes can cause cochlear ischemia (peripheral) and/or vestibulopathy (which can be peripheral and/or central). Because the AICA supplies the cerebellar flocculus, central patterns of head-shaking nystagmus (HSN) should be sought. Central patterns of HSN (after horizontal shaking) include perverted HSN (also known as crosscoupled, see example-https://collections.lib. utah.edu/ark:/87278/s6m08nrv) (18), HSN in the opposite direction of SN, or when strong HSN is elicited in the absence of UVL (see example-https://collections.lib.utah.edu/ark:/87278/ s61c5vkg) (19). Because a peripheral pattern of AVS that is indistinguishable from vestibular neuritis can be seen with AICA strokes, the presence of cochlear ischemia and hearing loss will enable stroke detection using HINTS+ (20). Shemesh and Gold: J Neuro-Ophthalmol 2020; 40: e49-e61 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Trainees' Corner TABLE 4. Assessing the vestibular system with provocative maneuvers (ideally performed with visual fixation removed) (22) Test Relevant Disorder(s) Occlusive Ophthalmoscopy With vestibular neuritis (or any cause of peripheral vestibular One eye is covered while the fundus of the fellow eye is nystagmus), the nystagmus will be brought out or observed with the ophthalmoscope-this removes accentuated by removing fixation fixation Pearls For vertical and horizontal movements, the optic nerve is posterior to the axis of rotation, so the true nystagmus vector is opposite to what is seen-e.g., if there is right-beating nystagmus with the direct ophthalmoscope, this is actually leftbeating nystagmus Because the axis of rotation for torsional movements is anterior-posterior, the observed nystagmus vector with direct ophthalmoscopy is correct Valsalva Closed glottis 1. Closed glottis-the patient takes a deep breath and Superior canal dehiscence syndrome (SCDS) bears down to increase intrathoracic pressure, which Perilymphatic fistula increases systemic arterial pressure while decreasing In craniocervical junction anomalies (e.g., Arnold-Chiari venous return, leading to increased intracranial malformation), increase in ICP due to Valsalva can pressure (ICP) cause or increase downbeat nystagmus 2. Pinched nose-the patient pinches the nose, takes Pinched nose a deep breath, and is asked to try to pop the ears. This SCDS increases middle ear pressure (through the Eustachian Perilymphatic fistula tubes), displacing the stapes inward Pearls Closed glottis: in SCDS, the inner ear fluid is displaced into the labyrinth, causing inhibitory nystagmus (upbeat torsional toward the unaffected ear) Pinched nose: in SCDS, the fluid is displaced out of the labyrinth, causing excitatory nystagmus (downbeat torsional toward the affected ear) Tragal compression (Hennebert sign) or pneumatic otoscope SCDS Application of positive pressure in the external auditory Perilymphatic fistula canal (EAC, inserting a wet finger or by pneumatic otoscope) or negative pressure in the external auditory canals (pulling out a wet finger or by pneumatic otoscope) changes middle ear pressure Pearls In SCDS-negative pressure in the EAC displaces fluid into the labyrinth, causing inhibitory nystagmus, and positive pressure in the EAC, fluid displaced out of the labyrinth, causing excitatory nystagmus In perilymphatic fistula-excitatory or inhibitory nystagmus in the plane of the semicircular canal with the fistula Head-shaking nystagmus (HSN) Unilateral vestibulopathy: The head is oscillated in the horizontal (or vertical) plane Horizontal HSN-ipsilesional slow phase and at 2-3 Hz for 10-15 seconds-the examiner observes contralesional nystagmus Bilateral vestibulopathy: for nystagmus The normal response to circular HS (patient is asked to Uses velocity storage to create transient asymmetry in trace an imaginary circle with the chin while, clockwise vestibular inputs when vestibular imbalance is present and counterclockwise) is torsional nystagmus at baseline (e.g., unilateral vestibulopathy), even when The absence of circular HSN suggests bilateral compensation has occurred vestibulopathy Central vestibulopathy: HSN may be in the wrong plane-e.g., horizontal HS results in vertical nystagmus ("perverted HSN") If spontaneous nystagmus is present, HSN may be in the opposite direction Shemesh and Gold: J Neuro-Ophthalmol 2020; 40: e49-e61 e55 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Trainees' Corner (Continued ) Test Relevant Disorder(s) Pearls In acute vestibular neuritis, there may be a downregulation of the velocity storage mechanism to minimize asymmetric vestibular afferents-this may result in little or no HSN HSN in Meniere's can be ipsilesional or contralesional In peripheral vestibulopathy, there can be a mild reversal in HSN (e.g., initial contralesional followed by weak ipsilesional nystagmus); in central vestibulopathy, the reversal can occur early and be more intense Vibration Vibration-induced nystagmus indicates high-frequency Application of a vibrator (w100 Hz) over the mastoids and vestibular asymmetry, which should be contralesional in vertex for 5-10 seconds may induce stimulus-locked unilateral vestibulopathy nystagmus (without reversal) Vibration is an excitatory stimulus that is transmitted from the vertex and each mastoid to both labyrinths The vibrator should not applied to the mastoid tip because this will stimulate posterior cervical muscles and can create nystagmus due to secondary proprioceptive inputs instead of vestibular afferents (41) Pearls In SCDS, the induced nystagmus is usually ipsilesional Some patients with unilateral vestibulopathy have ipsilesional vibration-induced nystagmus (central adaptation) In acute vestibular neuritis, typical contralesional nystagmus may increase more with vibration than with HS Hyperventilation Peripheral vestibulopathy: The patient hyperventilates for 40-60 seconds resulting in: Neurovascular compression of CN 8 (vestibular Decrease in CSF pCO2, arterial vasoconstriction, and paroxysmia) or vestibular schwannoma-excitatory decrease in ICP (ipsilesional) nystagmus is common Increase in pH and change in extracellular calcium Vestibular neuritis-nystagmus is typically contralesional concentration (42,43) acutely and subacutely but may become ipsilesional as compensation occurs Central vestibulopathy: Demyelinating lesion-spontaneous nystagmus may lessen due to an increase in conduction velocity Cerebellopathy-can increase spontaneous downbeat nystagmus (decompensation of Purkinje cells) Pearls Patients with panic attacks may experience worsening symptoms with hyperventilation; there is no nystagmus Changes in ICP in patients with craniocervical lesions (e.g., Chiari) or third window syndromes (perilymphatic fistula and SCDS) may induce symptoms and nystagmus Positional maneuvers Posterior canal (PC) BPPV: 1. Dix-Hallpike (DH) test-for example, right DH-the In the right DH, after a latency of a few seconds, upbeatpatient's head is turned 45° to the right, and then the torsional (top poles beating toward affected, right ear) patient is brought from a seated to supine position with nystagmus the head 20° extended Horizontal canal (HC) BPPV: 2. Supine roll test-for example, right roll test-the In the right roll test, after a latency of a few seconds, rightpatient is supine and the head is flexed 20-30° and beating nystagmus (RBN) will be seen in the geotropic then rotated 90° to the right (if cervical range of motion variant while left-beating nystagmus (LBN) will be seen is poor, the patient's head and body are rolled to the in the apogeotropic variant, while the direction will right) change in left roll-for example, LBN in geotropic and RBN in apogeotropic Anterior canal (AC) BPPV: In the rare AC variant, downbeat (DB) or downbeat-torsional (top poles beating toward affected ear) nystagmus Pearls The most common central BPPV mimics include positional downbeat followed by apogeotropic nystagmus A central etiology should be considered (especially with DB or apogeotropic) if the ocular motor or neurologic examination is abnormal; there is no latency; nystagmus persists; there is no response in positional nystagmus to repeatedly and properly performed repositioning maneuvers; the vector of nystagmus cannot be explained given the canal(s) stimulated (e.g., vertical nystagmus is seen in roll test) e56 Shemesh and Gold: J Neuro-Ophthalmol 2020; 40: e49-e61 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Trainees' Corner e. The following are examples of an abnormally appearing HIT, although actual VOR function may be normal: https://collections.lib.utah.edu/ark:/87278/s6f80x5q (25); vibration example-https://collections.lib.utah. edu/ark:/87278/s66t541n) (26). i. Stroke involving dorsal ocular motor vermis 1. Can cause ipsilesional saccade hypometria, which may mimic catch-up saccades during contralesional HIT (21). Likewise, in a lateral medullary (Wallenberg) syndrome, contralesional hypometria is a common feature, which may mimic catch-up saccades during ipsilesional HIT. ii. Some patients with cerebellar disease will demonstrate cross-coupling during HIT, where instead of a horizontal catch-up saccade that occurs with UVL, a downward or diagonally oriented refixation saccade is triggered by a horizontal HIT (22). iii. Some patients with cerebellar disease will demonstrate a hyperactive VOR, where instead of a catch-up saccade that occurs with UVL, a back-up saccade is required as the VOR brings the eyes past the visual target (22). IT IS CENTRAL: JUST TELL ME WHAT I NEED TO KNOW! 1. A normal HIT in the AVS is highly suggestive of a central etiology. 2. Although the HIT should be performed in patients even after vertigo has subsided to assess the VOR, the HINTS examination (including the HIT) cannot be applied in patients who do not have spontaneous nystagmus and ongoing vertigo. For example, a normal HIT in the AVS will lead to an accurate "central" classification-a proper application of HIT/HINTS. However, a normal HIT in a patient with benign paroxysmal positional vertigo may lead to an inaccurate "central" classification by the novice examiner-an improper application of HIT/HINTS. NYSTAGMUS: PERIPHERAL PEARLS 1. Alexander law-the intensity of the nystagmus increases in the direction of the quick phase (21) (see example-https:// collections.lib.utah.edu/ark:/87278/s64205qx) (23). 2. Due to fixation suppression, the intensity of the nystagmus increases by removing fixation. This can be performed at the bedside with Frenzel goggles, occlusive ophthalmoscopy, or penlight-cover test (24). 3. Involvement of all 3 unilateral semicircular canals will result in a characteristic mixed horizontal-torsional nystagmus. 4. With peripheral UVL, head shaking or application of mastoid/vertex vibration will either intensify or provoke contralesional nystagmus (vibration example- Shemesh and Gold: J Neuro-Ophthalmol 2020; 40: e49-e61 IT IS PERIPHERAL: JUST TELL ME WHAT I NEED TO KNOW! Acute VN almost always causes spontaneous unidirectional, mixed horizontal-torsional contralesional nystagmus that intensifies with removal of fixation. Anything other than this should be assumed to be central until proven otherwise. NYSTAGMUS: CENTRAL PEARLS 1. Nystagmus that changes direction on eccentric gaze (e.g., right-beating nystagmus [RBN] in right gaze and left-beating nystagmus [LBN] in left gaze) implies impairment in gaze-holding networks (the neural integrator), and GEN is the result. By contrast, physiological end-point nystagmus should fatigue over seconds, resolves when the eyes are brought back toward primary position enough that both eyes can see the visual target, and rebound nystagmus (e.g., RBN when looking to the right and then LBN when the patient looks back to center) is absent (22) (see examples of GEN and rebound-https://collections.lib.utah.edu/ark:/87278/ s6089dz6) (27). 2. Pure torsional or pure vertical (downbeat or upbeat) is almost always central. It is important to know that there exists a poor torsional visual fixation mechanism, so that in peripheral conditions such as VN or BPPV, the horizontal or vertical (respectively) vector may be suppressed with fixation, but the torsional component will not. This can give peripheral conditions a predominantly torsional appearance, which might give the false impression of a central disorder (see example of fixation suppression of upbeat, but not torsional, nystagmus in BPPV-https://collections. lib.utah.edu/ark:/87278/s67m3hm9) (28). 3. Vestibular nystagmus that does not suppress with visual fixation suggests a central localization. However, in one study, it was shown that horizontal SN in AICA/posterior inferior cerebellar artery territory cerebellar strokes suppressed with fixation in 60% of patients (29). In another study, all patients with superior cerebellar artery cerebellar strokes who had predominantly horizontal SN demonstrated fixation suppression (30). 4. Central vestibular nystagmus may or may not obey Alexander law (22). 5. Convergence may change direction of vertical nystagmus (e.g., in acute Wernicke encephalopathy, spontaneous upbeat may transition to downbeat (16); see example in encephalitis-https://collections.lib.utah.edu/ark:/ 87278/s6bg75c3) (31). e57 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Trainees' Corner IT IS CENTRAL: JUST TELL ME WHAT I NEED TO KNOW! 1. Direction changing or GEN is a central sign in the AVS. 2. Central vestibular nystagmus can be unidirectional, obey Alexander's law, and suppressed with fixation, thereby making it look peripheral. This is why the complete HINTS+ examination should be performed in addition to looking for central patterns of HSN. TEST OF SKEW: PERIPHERAL PEARLS 1. Acute peripheral vestibulopathy as a complication of stapedectomy, surgical labyrinthectomy, or vestibular neurectomy has been reported to cause a skew deviation, although these recover over days to weeks (32). The superior division of the vestibular nerve innervates the utricle, and although vestibular neuritis almost always involves this division, vertical diplopia due to a skew deviation is rarely seen. However, when a "peripheral" skew is present, the magnitude of the vertical ocular misalignment is relatively small and may only be appreciated with Maddox rod testing (see example of a peripheral skew deviation in vestibular neuritis-https://collections.lib.utah.edu/ark:/ 87278/s6ht70fx) (33). 2. Differentiating a skew deviation from a fourth NP can be a diagnostic conundrum. With a fourth NP, the paretic eye is hypertropic, and there is a contralateral head tilt. The head tilt seen in a fourth NP is compensatory and uses the (normal or physiologic) utriculoocular motor reflex (which is induced by the head tilt) to minimize vertical misalignment and diplopia. Although a contralateral head tilt is compensatory, an ipsilateral head tilt will worsen the hypertropia (see example-https://collections.lib.utah.edu/ark:/87278/ s6hf1tbf) (34). The head tilt that is often seen with a skew deviation is a feature of the ocular tilt reaction (skew deviation, head tilt, ocular counterroll, and tilted subjective visual vertical [SVV]). A fourth NP will be incomitant (e.g., the size of the hypertropia is larger in contralateral gaze), whereas a skew deviation is usually comitant (same in all directions of gaze). However, in a fourth NP, the vertical deviation may become more comitant with time (spread of comitance), whereas the deviation in skew may be incomitant or alternating (right hypertropia in right gaze and left hypertropia in left gaze (35)-see example of alternating hypertropias in bilateral fourth NP and skew deviation-https:// collections.lib.utah.edu/ark:/87278/s6d83n91) (36). To distinguish the two, ocular torsion should be assessed objec- e58 tively with fundus photography or indirect ophthalmoscopy, or subjectively with monocular SVV measurements (using the bucket test (37)) or double Maddox rod. Excycloduction of the hypertropic eye is seen with fourth NP (due to the paretic superior oblique muscle, whose primary action is incycloduction), while incycloduction of the hypertropic eye is seen with skew. The "Bielschowsky 3 step test" is used to diagnose fourth NP and, while in an upright position, consists of 1) identifying the hypertropic eye (ipsilesional in a fourth), 2) hypertropia increases in contralateral gaze, and 3) hypertropia increases in ipsilateral head tilt. Knowledge of how to differentiate skew from fourth can be particularly valuable in the AVS, when a patient may rarely have a vertical deviation from a longstanding or congenital fourth NP, not a skew deviation (35). However, when diagnostic uncertainty remains, the etiology should be assumed central (skew) until proven otherwise. IT IS PERIPHERAL: JUST TELL ME WHAT I NEED TO KNOW! 1. In the AVS, when either vertical binocular diplopia is experienced or a vertical refixation is seen with ocular alignment testing, a central localization should be assumed until proven otherwise, although skew can rarely be "peripheral." 2. Horizontal deviations seen in the AVS are often normal and unrelated and do not suggest a skew deviation (see example of a patient with VN who has a small [normal] exophoria available at https://collections.lib.utah.edu/ ark:/87278/s6tn1htv) (38). TEST OF SKEW: CENTRAL PEARLS 1. When a skew deviation is due to a brainstem lesion, the hypotropic (lower) eye will be ipsilesional when the lesion is caudal to the decussating utriculo-ocular motor fibers in the pontomedullary junction (e.g., left hypotropia in left lateral medullary stroke), or the hypertropic (higher) eye will be ipsilesional when the lesion is rostral to the decussating fibers (e.g., right hypertropia in right medial longitudinal fasciculus [MLF] stroke). a. The afferents that begin in the left utricle (peripherally in the labyrinth) enter the brainstem in the left lateral medulla, synapse in the vestibular nucleus, then decussate and ascend through the right MLF to end in the right interstitial nucleus of Cajal; therefore, a left lateral medullary or right MLF stroke will affect the same utriculo-ocular motor pathway, just at different levels of the brainstem and on opposite sides. Shemesh and Gold: J Neuro-Ophthalmol 2020; 40: e49-e61 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Trainees' Corner TABLE 5. The most common vestibular conditions categorized by timing and triggers, with specific ocular motor and vestibular features that should be sought for each (adapted from https://collections.lib.utah.edu/ark:/ 87278/s6tr0d0h) Vestibular Conditions to Consider Acute vestibular syndrome (.24 hours) 1) Vestibular neuritis 2) Stroke (demyelination and other central etiologies less common) 3) Wernicke's Episodic spontaneous vestibular syndrome* 1) TIA 2) Vestibular migraine 3) Meniere's 4) Vestibular paroxysmia Episodic triggered vestibular syndrome 1) BPPV 2) SCDS Chronic vestibular syndrome 1) BVL 2) PPPD Shemesh and Gold: J Neuro-Ophthalmol 2020; 40: e49-e61 Targeted Ocular Motor and Vestibular Examination 1) HINTS+: HIT abnormal (see example-https:// collections.lib.utah.edu/ark:/87278/s6x398q2) AND unidirectional nystagmus that obeys Alexander law (see example-https://collections.lib.utah.edu/ark:/ 87278/s64205qx) AND skew deviation absent (see alternate cover testing at 1 and 3 minutes-https:// collections.lib.utah.edu/ark:/87278/s6tn1htv) AND no acute hearing loss; peripheral pattern of HSN 2) HINTS+: HIT normal (see demonstration in a normal patient-https://collections.lib.utah.edu/ark:/ 87278/s63b97tz) OR gaze-evoked nystagmus (see example-https://collections.lib.utah.edu/ark:/ 87278/s6kh4n5k) OR skew deviation present (see example-https://collections.lib.utah.edu/ark:/ 87278/s6c0045t) OR acute hearing loss; look for central patterns of HSN (see example-https:// collections.lib.utah.edu/ark:/87278/s61c5vkg) 3) Bilaterally abnormal HIT, spontaneous vertical (see example-https://collections.lib.utah.edu/ark:/ 87278/s6h74j6d) and gaze-evoked nystagmus are common, also sixth NP, ataxia 1) Usually symptoms have resolved, and eye movement examination is normal, otherwise may use HINTS† 2) Can see peripheral or central patterns of nystagmus (spontaneous, gaze-evoked, head-shaking-induced, positional) during the attack, often normal interictally, often spontaneous, but typical migraine triggers are common too 3) Nystagmus can be in excitatory or inhibitory patterns during the attack, often normal interictally 4) Hyperventilation-induced nystagmus (see demonstration in a normal patient-https:// collections.lib.utah.edu/ark:/87278/s6pz98ht) 1) Dix-Hallpike test (see example-https://collections. lib.utah.edu/ark:/87278/s6s79d1w) and supine roll test (with bow and lean to localize, see example- https://collections.lib.utah.edu/ark:/87278/ s68h2wk9) 2) Valsalva and pinched-nose Valsalva (see example- https://collections.lib.utah.edu/details? id=1213443), tragal compression, and loud sounds 1) Bilaterally abnormal HIT (see example-https:// collections.lib.utah.edu/ark:/87278/s62z4z8g), additional cerebellar signs can narrow differential 2) No typical ocular motor/vestibular findings e59 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Trainees' Corner (Continued ) Vestibular Conditions to Consider 3) Cerebellar disease 4) Acoustic neuroma 5) Oculopalatal tremor Targeted Ocular Motor and Vestibular Examination 3) Flocculus/paraflocculus: Gaze-evoked nystagmus, spontaneous downbeat nystagmus, saccadic pursuit and VORS (when VOR is present), saccadic dysmetria (see example-https://collections.lib.utah.edu/ark:/ 87278/s6dj8q9h), alternating skew deviation (see example-https://collections.lib.utah.edu/ark:/ 87278/s6d83n91) while additional vestibular loss can narrow differential (e.g., CANVAS, see example- https://collections.lib.utah.edu/ark:/87278/ s6s50fth) Nodulus/uvula: periodic alternating nystagmus (see example-https://collections.lib.utah.edu/ark:/ 87278/s62k013r) 4) Hyperventilation-induced nystagmus (see example- https://collections.lib.utah.edu/ark:/87278/ s63f8cgs) and Bruns nystagmus (see example- https://collections.lib.utah.edu/ark:/87278/ s60p4p3j) 5) Vertical or vertical-torsional pendular nystagmus with palatal tremor (see example-https://collections.lib. utah.edu/ark:/87278/s6mh1mnm) *If first attack of TIA, vestibular migraine or Meniere's may be better described as the acute transient vestibular syndrome (,24 hours). † HINTS has been studied in the acute vestibular syndrome and should not be relied on in the episodic or acute transient vestibular syndrome. BPPV, benign paroxysmal positional vertigo; BVL, bilateral vestibular loss; CANVAS, cerebellar ataxia, neuropathy, vestibular areflexia syndrome; HINTS+, head impulse, nystagmus, test of skew, "plus" bedside assessment of auditory function; HIT, head impulse test; NP, nerve palsy; PPPD, persistent postural perceptual dizziness; SCDS, superior canal dehiscence syndrome. IT IS CENTRAL: JUST TELL ME WHAT I NEED TO KNOW! 1. A skew deviation (especially one causing diplopia) is almost always central in origin and reflects imbalance in utricle-ocular motor pathway tone due to lesions in the brainstem or cerebellum (39) (see example available at https://collections.lib.utah.edu/ark:/87278/s6c0045t (40)). CONCLUSION Accurate localization and management of dizzy patients are based on knowledge of the neuroanatomy and interactions between visual, vestibular and ocular motor systems. Understanding, what should be evaluated and why, allows the clinician to select and interpret the most appropriate bedside tests for a dizzy patient. By applying a methodical approach to examination, the clinician can easily probe hypotheses at the bedside, such that audiovestibular laboratory testing and/or neuroimaging often simply confirm what was suspected. This often results in elucidating the underlying diagnosis of dizziness/vertigo (Table 5) and appropriate course of therapy, which can be satisfying for patient and clinician alike. e60 REFERENCES 1. Newman-Toker DE, Kerber KA, Hsieh YH, Pula JH, Omron R, Saber Tehrani AS. HINTS outperforms ABCD2 to screen for stroke in acute continuous vertigo and dizziness. Acad Emerg Med. 2013;20:986-996. 2. Kattah JC. Use of HINTS in the acute vestibular syndrome. An overview. Stroke Vasc Neurol. 2018;3:190-196. 3. Choi KD, Lee H, Kim JS. Ischemic syndromes causing dizziness and vertigo. Handb Clin Neurol. 2016;137:317-340. 4. Gold DR. 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Date | 2020-09 |
Language | eng |
Format | application/pdf |
Type | Text |
Publication Type | Journal Article |
Source | Journal of Neuro-Ophthalmology, September 2020, Volume 40, Issue 3 |
Collection | Neuro-Ophthalmology Virtual Education Library - Journal of Neuro-Ophthalmology Archives: https://novel.utah.edu/jno/ |
Publisher | Lippincott, Williams & Wilkins |
Holding Institution | Spencer S. Eccles Health Sciences Library, University of Utah, 10 N 1900 E SLC, UT 84112-5890 |
Rights Management | © North American Neuro-Ophthalmology Society |
ARK | ark:/87278/s67714qj |
Setname | ehsl_novel_jno |
ID | 1592956 |
Reference URL | https://collections.lib.utah.edu/ark:/87278/s67714qj |