Electronystagmography (ENG) is the fundamental test and the first step in a vestibular testing battery to evaluate the vestibuloocular reflex in patients with a balance disorder. It is based on recording and measuring eye movements or eye positions in response to visual or vestibular stimuli.
Standard ENG equipment consists of the following components: (1) an amplifier for amplification of the corneal-retinal potential that occurs following eye movement, (2) band-pass and notch filters, (3) a signal recorder, (4) a light array, and (5) water and air caloric stimulators. The techniques available to record eye movements are electrooculography (EOG), infrared recording, magnetic search coil, and video-recording systems.
An ENG analysis consists mainly of three tests: (1) oculomotor tests, (2) positional tests, and (3) caloric tests. Before each test, the system needs to be calibrated to maintain accuracy. The calibration is performed via a saccade test that is discussed in the section on oculomotor tests.
Utility of Electronystagmography
ENG is very useful in diagnosing vestibular pathology. No other test provides information on the site of the lesion. The data obtained from an ENG test battery support the diagnoses of horizontal BPPV, vestibular neuronitis, Meniere disease, labyrinthitis, and ototoxicity. With acoustic neuromas, it may be helpful to predict the nerve from which the tumor originates; caloric weakness may be associated with a tumor that originates from the superior vestibular nerve. ENG may also predict whether the patient will experience vertigo after acoustic tumor removal. However, relying on ENG alone to identify lesions in the CNS would not be appropriate.
Abnormal findings in ENG testing do not necessarily indicate a definite CNS lesion. One study investigated the ratio of patients with abnormal results as reported by magnetic resonance imaging (MRI) to patients with abnormal ENG findings in different age groups and found a better correlation between MRI and ENG findings in a group of elderly patients. Overall, MRI confirmed a central lesion in 52% of patients with abnormal ENG findings. In contrast, ENG findings were abnormal in 15 of 21 patients (71%) with an abnormal MRI. In two recent studies, only 30–37% of the patients with abnormal ENG findings had abnormal MRI scans.
Oculomotor tests measure the accuracy, latency, and velocity of eye movements for a given stimulus. The standard oculomotor test battery includes saccade tests, smooth pursuit tests, optokinetic nystagmus testing, gaze tests, and fixation suppression testing. All oculomotor tests are performed with the patient seated upright, with the head stabilized. For oculomotor tests, the ENG device should have a light array on which LED (light-emitting diodes) are given as a stimulus. The light array may be rotated vertically for calibration purposes as well as for testing vertical saccades. The center of the light arrays should be at the same level as the patient's eyes.
Saccades are rapid eye movements that bring objects in the periphery of the visual field onto the fovea. The latency of saccades is very brief. Because peak velocity can be as high as 700°/s, vision is not clear during saccadic movement. Saccades are controlled by the occipitoparietal cortex, the frontal lobe, the basal ganglia, the superior colliculus, the cerebellum, and the brainstem.
To test saccadic eye movement, the patient is asked to follow the LED with as much accuracy as possible. The LED flashes sequentially in two positions: at the center of the array and then 15–20° to the right or left from the center. The interval between flashes is usually a few seconds. The test is repeated vertically.
Three parameters are of clinical significance in evaluating saccades: latency, peak eye velocity, and accuracy of the saccades.
Latency is the time difference between the presentation of a target and the beginning of a saccade. The mean latency is 192 ± 32 ms in normal subjects. Abnormalities in latency include prolonged latency, shortened latency, and differences in the latency between the right eye and the left eye. These abnormalities are observed in the presence of neurodegenerative disease.
The peak velocity is the maximum velocity that eyes reach during a saccadic movement. It ranges from 283°/s to 581°/s for 20° of amplitude in normal subjects. Abnormalities in the saccadic velocity are slow saccades, fast saccades, or a difference in the velocity between the right eye and the left eye. Reasons for saccadic slowing include the use of sedative drugs, drowsiness, cerebellar disorders, basal ganglia disorders, and brainstem lesions. Fast saccades can be observed in calibration errors and eye muscle restrictions. The asymmetry of velocity is observed in internuclear ophthalmoplegia, eye muscle restrictions, ocular muscle palsies, and palsy of cranial nerves III and VI (the oculomotor and abducens nerves, respectively).
Accuracy is the final parameter in the evaluation of saccades. Saccadic accuracy is determined by saccadic movement by comparing the patient's eye position relative to the target position. Figure 46–3 provides a record of normal saccadic movement with accurate square tracing. If the saccadic eye movement goes farther than the target position, it is referred to as a hypermetric saccade (or overshoot dysmetria). If the saccadic movement is shorter than the target position, it is referred to as hypometric saccade (or undershoot dysmetria). Undershooting by 10% of the amplitude of the saccade may be observed in healthy subjects, whereas hypermetric saccades rarely occur in healthy subjects. Inaccurate saccades suggest the presence of a pathologic condition in the cerebellum, brainstem, or basal ganglia.
An EOG recording of normal saccadic eye movement. (A) Horizontal record. (B) Vertical record.
Smooth pursuit is the term used to describe eye movement that is created when the eyes track moving objects. Similar central pathways to those of saccadic movement produce smooth pursuit movement. The neural pathways serving the “pursuit system” are distributed in the cortical and subcortical areas of the brain. Smooth pursuit function also involves the fovea.
In a commonly used stimulus paradigm of the smooth pursuit test, the LED moves back and forth between two points on a light bar at a constant frequency and velocity. The patient is asked to follow this moving target. The frequency of the test stimulus should be between 0.2 and 0.8 Hz/s. A typical pursuit velocity is between 20°/s and 40°/s. Performance declines with higher velocities and increasing patient age.
The primary parameters for evaluation are gain, phase, and trace morphology. Gain is the ratio of peak eye velocity to the target velocity. For a stimulus of 0.5 Hz with a sweeping amplitude of 40°, a gain >0.8 is considered normal. A low gain is suggestive of a CNS disorder. Phase is the difference in time between eye movement and target movement. Under optimal conditions, healthy subjects can track a target with a phase angle of 0°. The level of attention and drugs affecting the CNS can destroy pursuit performance.
A morphologic assessment of the trace is also important. Figure 46–4 shows a record of normal tracking eye movement. A morphologic abnormality is referred to as a staircase of saccades, in which the trace shows staircase-like eye movement while the target is followed. Pursuit traces can be impaired symmetrically or asymmetrically. An asymmetrically impaired pursuit is more suggestive of a CNS lesion than is a symmetrically impaired pursuit. Acute peripheral vestibular lesions can also impair smooth pursuit contralateral to the affected side when the eyes are moving against the slow phase of a spontaneous nystagmus.
EOG recording of normal tracking eye movement. (A) and (B) are horizontal and vertical records of the tracking movement, respectively.
Optokinetic Nystagmus & Optokinetic Afternystagmus
Optokinetic nystagmus (OKN) is an involuntary oculomotor response to a moving target that fills at least 90% of the visual field.
The best optokinetic stimulator is a 360° turning cloth drum with black and white stripes. Because this drum can be unwieldy, it is preferable to use an optokinetic projector.
The normal response to an optokinetic stimulator is a smooth eye movement that follows the direction of the visual stimulus both clockwise and counterclockwise. OKN aims to stabilize the visual field onto the retina. OKN is produced by cortical and brainstem structures, which is the same as the pursuit. Optokinetic afternystagmus (OKAN) is a form of nystagmus that is produced by the brainstem after a 10-second, constant-velocity optokinetic stimulus. It lasts about 30 seconds.
OKN can be stimulated with a constant target speed between 20°/s and 60°/s or a sinusoidal target speed of up to 100°/s. Each target speed needs to be repeated in both clockwise and counterclockwise directions. The patient is asked to gaze straight ahead, while the target is moved in front of his or her field of vision. The type of stimulus chosen is presented for 1 minute. When a constant-velocity optokinetic stimulus is used, the patient's eyes reach a constant velocity after 10 seconds of stimulation in one direction. Once this stimulus is discontinued, the room light is turned off and the recording is continued for OKAN until the OKAN is decayed. The same stimulus is then applied in the opposite direction. It should be noted that a sinusoidal stimulus cannot be used to test OKAN.
Parameters of Optokinetic Nystagmus
In testing of OKN, the most useful parameters are gain and phase.
The normal value of gain is ≥0.5, as well as symmetry on both sides (ie, in both eyes) for a stimulus of 60°/s. A gain in OKN may be reduced symmetrically or asymmetrically. A symmetrically reduced gain is observed in visual disorders, fast-phase disorders, and congenital nystagmus. Unilateral parietal-occipital lesions cause an asymmetrically reduced gain.
As a testing parameter, phase is applied only for the sinusoidal stimulus of OKN. The testing of OKN is less sensitive than a pursuit test. The sensitivity and specificity of OKN elicited by stimulation of the full visual field are 46% and 92%, respectively, which is superior to the sensitivity and specificity of OKN elicited by stimulation of the partial visual field.
Parameters of Optokinetic Afternystagmus
The testing of OKAN is evaluated by three parameters: the initial velocity, the time constant, and the slow-cumulative eye position. The initial velocity is calculated from the OKAN at the 2nd second. This initial velocity is approximately 10°/s for a stimulus of 60°/s. The time constant is the length of time required for the slow-phase velocity to decline to 37% of the initial velocity. The slow cumulative eye position is a function of both the initial velocity and the time constant. Because it shows less intersubject variability compared with the other two, it is the most useful parameter. The normative value of the slow cumulative eye position varies among the vestibular laboratories. Abnormalities in OKAN present as symmetrically reduced OKAN, which is bilateral; asymmetrically reduced OKAN; and hyperactive OKAN. A complete bilateral loss of OKAN is observed in a bilateral vestibular loss, which may be either peripheral or central. Asymmetry in OKAN is indicative of a unilateral vestibular loss. Hyperactive OKAN may be seen in mal de debarquement syndrome.
The gaze test is performed by recording eye movements, while the patient fixes his vision on the center of a target; the patient then fixes his gaze 30–40° to the right, to the left, and then above and below the center of the target. The patient's gaze, as well as a recording of that gaze, is sustained for at least 30 seconds. A gaze test may reveal peripheral or CNS lesions that are either vestibular or nonvestibular in origin. It may also reveal either congenital or spontaneous nystagmus. Patients with gaze nystagmus cannot maintain stable conjugate eye deviation away from the primary position; therefore, the focus of the patient's vision is brought back to the center by resetting the corrective saccades. Vestibular spontaneous nystagmus is seen during and after unilateral vestibular dysfunction and beats away from the afflicted side. It is seen as a horizontal nystagmus in an ENG recording, but it is actually both horizontal and torsional in nature. The intensity of vestibular spontaneous nystagmus increases when the patient's gaze is directed toward the direction of the nystagmus.
A typical gaze-evoked nystagmus that is peripheral in origin is unidirectional on a horizontal plane; it is both horizontal and torsional. Its intensity increases when gaze is directed toward the direction of the nystagmus. A gazeevoked nystagmus with a CNS origin may change direction with the patient's gaze. A nystagmus that results from a vertical gaze is always suggestive of CNS lesions.
Gaze nystagmus may be classified as symmetric, asymmetric, rebound, or disassociated. In symmetric gaze nystagmus, the eyes move in equal amplitude in both directions. The ingestion of drugs that affect the CNS, as well as multiple sclerosis, myasthenia gravis, and cerebellar atrophy, may all cause symmetric gaze nystagmus. Asymmetric gaze nystagmus is indicative of a lesion within the brainstem or the cerebellum. Rebound nystagmus begins in lateral gaze positions and reverses its direction to the primary position, even though there is no evidence of nystagmus in the primary position at the beginning of testing. It is also a strong indicator of cerebellar or brainstem lesions. Dissociated (disconjugate) nystagmus is the difference in eye movements during the gaze. It results from lesions of the medial longitudinal fasciculus.
Fixation Suppression Testing
Spontaneous nystagmus is determined by placing the patient, with eyes closed, in a totally darkened room without any visual or positional stimuli. If spontaneous nystagmus is found, its slow-phase velocity is recorded. The patient is then asked to fixate on the center of a visual target (central gaze). The ratio of the slow-phase velocity with fixation to the slow-phase velocity without fixation is then calculated. This calculation provides a fixation suppression index. This index should be <50%. Nystagmus that results from a peripheral origin decays to more than 50% with fixation. Figure 46–5 shows the effect of fixation on a spontaneous nystagmus that is peripheral in origin.
(A) A right-beating spontaneous nystagmus with a slow-phase velocity of 4°/s. (B) Note that the nystagmus disappears with fixation. (Reprinted, with permission of Hussam K. El-Kashlan, MD; University of Michigan, Ann Arbor, Department of Otolaryngology–Head & Neck Surgery.)
The purpose of positional testing is to determine the effect of different stationary head positions (and not head movements) on eye movements. The assumption of these tests is that the patient's nystagmus is generated as a result of the orientation of the patient's head to gravity. The patient is asked to wear Frenzel glasses (or the test can be performed while the patient's eyes are closed), and the patient is brought slowly into the following positions: the patient's head (1) is turned right and then left while sitting, (2) is turned right and then left in the supine position, (3) is turned right and then left in a decubitus position, and (4) hangs straight down. Each position is maintained for at least 20 seconds. Positional nystagmus may be intermittent or persistent, and the direction may be fixed or changing.
The identification of positional nystagmus is not a localizing finding since it may be observed in patients with both peripheral and CNS lesions. Two features may help to distinguish the positional nystagmus that results from a peripheral lesion from one that results from a central lesion: (1) positional nystagmus caused by a peripheral lesion is suppressed by fixation; (2) the direction changing nystagmus may be indicative of a CNS lesion. The clinician must be careful about the contamination of spontaneous nystagmus with positional changes. If persistent nystagmus is noted, it should be observed for at least 2 minutes. This observation is especially important with periodic alternating nystagmus, in which the nystagmus reverses direction every 2 minutes. It is found that this type of nystagmus is caused by CNS lesions.
Caloric tests are based on comparing magnitude of the induced nystagmus on the right and left sides. Since the outer ear canal is close to the horizontal SCC, most of the response origins come from the horizontal SCC. Therefore, the nystagmus is horizontal. The temperature gradient produced by a cold stimulus causes the cupula to move away from the utricle, thereby creating a nystagmus that beats toward the opposite side. A warm stimulus causes the endolymph to rise, resulting in a nystagmus that beats toward the stimulus side.
Caloric testing is an important tool in assessing the vestibular system. It allows for the separate stimulation of each ear. Therefore, it provides data about the site of the lesion. However, there are some disadvantages of this test. Heat transfer from the ear canal to the horizontal SCC may vary among individuals, depending on the differences in the temporal bone pneumatization among patients. Another disadvantage is the fact that a caloric stimulus can provide a means of evaluating the vestibular response, but at only one frequency. The last disadvantage is that the caloric test allows only for the evaluation of the horizontal SCC.
The caloric test uses a caloric stimulator, either a water or air irrigator, in addition to the EOG recording equipment. Two types of water stimulators are available: open loop and closed loop. The difference between the two stimulators is where the water circulates. An open-loop stimulator delivers water directly into the outer ear canal. In closed-loop systems, the water circulates in an expandable rubber medium to preserve its temperature. Open-loop systems are thought to provide more reliable and reproducible results than closed-loop systems. Caloric testing with either air or a closed-loop water stimulus should be reserved for patients who have a tympanic membrane perforation.
The patient should be in the supine position, with his head tilted 30° upward to bring the horizontal SCC into the earth vertical position—this position makes the horizontal SCC more sensitive. The test can be performed with either a bithermal or a monothermal caloric stimulus. The bithermal caloric test provides the most useful data on the vestibular system, which is stimulated by warm and cold water or air. To enhance the nystagmus response, mental tasks are given to the patient during the test. The recording can be performed with the patient's eyes opened in total darkness, with his eyes opened and wearing Frenzel glasses, or with his eyes closed.
In performing caloric testing, temperatures 7 C below and above body temperature (30°C and 44°C) are used as cold- and warm-water stimuli. A total volume of 250 mL of water is given to the outer ear canal over a period of 30–40 seconds. As an alternative to the water stimulus, two air stimuli that are 24°C and 50°C, respectively, are used with a flow rate of 8 L/min for 60 seconds. Four caloric stimuli are given with an interval of no less than 5 minutes to prevent superimposition or conflicting responses. The following order of stimuli is preferred: (1) right–warm, (2) left–warm, (3) right–cold, and (4) left–cold. In response to the caloric stimulus, the nystagmus begins just before the end of the caloric stimulus and reaches a peak at approximately 60 seconds of stimulation; it then slowly decays over the next minute. When it reaches its peak, patients are asked to fixate their eyes on a central point to check the fixation suppression index.
The most reliable and consistent parameter is the peak slow-phase velocity of the induced nystagmus. The peak slow-phase velocity is averaged over a 10-second period and is calculated for each side.
The values obtained for each caloric stimulus are placed into equations, with each used for specific conditions that define vestibular function. Unilateral weakness (ie, canal paresis) indicates a significantly weak response on one side relative to the other. It is formulated as follows:
(R 30Â°C + R 44Â°C) â (L 30Â°C + L 44Â°C) × 100% ÷ (R 30Â°C + R 44Â°C + L 30Â°C + L 44Â°C)
The difference between the sides ≥20–25% indicates the presence of a unilateral weakness. However, normative data for this critical percentage should be determined for each laboratory. Unilateral weakness is not a localizing finding and may be caused by lesions from the labyrinth to the root entry zone of the eighth cranial nerve (ie, the vestibulocochlear nerve) in the brainstem, such as Meniere disease, labyrinthitis, vestibular neuronitis, acoustic neuromas (and other tumors pressing on the eighth nerve), and multiple sclerosis.
Directional preponderance (ie, unidirectional weakness) refers to a condition in which the mean-peak, slow-phase velocity of the nystagmus beating toward one side is significantly greater than the mean-peak, slow-phase velocity of the nystagmus beating toward the opposite side. It is determined by the following equation:
(R 30Â°C + L 44Â°C) â (R 44Â°C + L 30Â°C) × 100% ÷ (R 30Â°C + R 44Â°C + L 30Â°C + L 44Â°C)
A difference >20–30% assumes the existence of a directional preponderance. This critical percentage should be determined by a testing laboratory. The directional preponderance is often associated with a spontaneous nystagmus because a spontaneous nystagmus enhances the nystagmus beating toward its direction and eliminates the nystagmus beating toward the opposite direction. The directional preponderance simply shows the existence of bias in the tonic activity of the vestibular system. However, the directional preponderance is considered to reflect an asymmetry in the dynamic sensitivity between the left and the right medial vestibular neurons, as opposed to the reason behind the spontaneous nystagmus, which is reflected in asymmetry in the resting activity. The directional preponderance is a poor localizing finding. It may be observed in lesions from the labyrinth to the cortex. The directional preponderance is toward the lesion site for labyrinth and eighth nerve lesions, and toward the uninvolved site for lesions of the brainstem and cortex. It is controversial that a directional preponderance without a spontaneous nystagmus is suggestive of a CNS disorder. One retrospective study showed that 5% of patients with an isolated directional preponderance had a CNS lesion. Other patient groups had peripheral lesions or no definite diagnosis. Directional preponderance and unilateral weakness may be observed together, which is suggestive of acute unilateral peripheral lesions.
Caloric weakness may be found in both sides, which is referred to as bilateral weakness. The level of response that is considered a bilateral weakness varies based on the normative data. However, several physicians give their own normative measurements. For both sides, the total response to a warm stimulus (<11°/s) and the total response to a cold stimulus (<6°/s) are considered bilateral weakness. Patients with bilateral weakness often present with oscillopsia. A bilateral weakness is often associated with vestibulotoxic antibiotherapy or bilateral Meniere disease. However, it is also observed in patients with lesions of the vestibular nuclei, Lyme disease, Cogan syndrome, pseudotumor cerebri, and neurodegenerative diseases of the brainstem and cerebellum.
Hyperactive caloric responses may also be observed. The numeric criteria for these responses varies among laboratories from 40°/s to 80°/s. Hyperactive caloric responses are associated with a cerebellar lesion or atrophy due to removal of the cerebellar inhibitory effect on the vestibular nuclei.
Failure (ie, an abnormal finding) of the fixation suppression test may be found in the caloric test. The patient is asked to fixate on a central point during the peak caloric response. Vestibular nystagmus is normally suppressed by visual fixation. The fixation index expresses this attenuation quantitatively, which is the difference between the slow-phase velocity in the dark and in the light divided by the slow-phase velocity in the dark. The normal value for the visual suppression of the caloric response is >50%. If it fails—that is, <50%—impaired fixation suppression results. Cerebellar lesions affecting the flocculus cause impaired fixation suppression.
The inversion of caloric nystagmus is observed in patients with a tympanic membrane perforation. It occurs because of the cooling effect of the evaporation of moisture in the middle ear mucosa when warm air is used as a caloric stimulus.
Premature caloric reversal is the finding that can be observed in patients with Friedreich ataxia and brainstem lesions. The normal caloric response starts to decay at 90 seconds of the stimulation and disappears after 200 seconds, with a nystagmus beating toward the opposite side. In premature caloric reversal, nystagmus reversal occurs earlier than 140–150 seconds. It is worth noting that one should not refer to a preexisting spontaneous nystagmus as a premature caloric response.
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