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3rd Congress of the European Academy of Neurology
Amsterdam, The Netherlands, June 24 – 27, 2017
Hands-on Course 3
Bedside examination of the vestibular and ocular motor system - Level 2
How to examine the vestibular system
Raymond van de Berg Maastricht, The Netherlands
Email: [email protected]
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Conflict of interest: The author has no conflict of interest in relation to this manuscript
Introduction
A complete and thorough neuro-otological and vestibular examination
is necessary to find any signs of vestibular hypofunction or any neuro-
logical diseases, particularly ataxia. Keep in mind that when testing the
vestibular system, each test has its own limitations in terms of sensitivity,
specificity, patient acceptance, costs and duration. During the neuro-
otological assessment, one should pay especially close attention to the
oculomotor examination, since abnormal oculomotor findings may be the
only or first presenting central signs that may explain the vestibular
symptoms [2]. The oculomotor examination is best performed before
inducing the substantial head movements that are typical for some major
components of the vestibular examination. The vestibular examination
includes the Dix-Hallpike and the lateral roll test, positional testing,
(V)HIT, the test for Dynamic Visual Acuity (DVA), the visually enhanced
vestibulo-ocular reflex test, fixation suppression, the Valsalva maneuver
(straining against the closed glottis and blowing out against pinched
nostrils), the head shake test, the vibration test, the hyperventilation test
and the Romberg test on foam rubber or in tandem [3, 4]. The Romberg,
(V)HIT, DVA and head shake test will be discussed more in detail in this
hands-on course.
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The Romberg test
The Romberg test mainly diagnoses ataxia and is not specific for a
vestibular loss, since it also detects cerebellar and proprioceptive impair-
ment [3, 5]. However, the sensitivity for detecting vestibular deficits
increases when the patient stands on foam rubber [6]. The Romberg test
on foam rubber has a sensitivity of up to 79% and a specificity of up to 80%
for detecting both patients with unilateral and those with bilateral
vestibular loss [3, 7].
Head impulse testing
A brief, high-acceleration head ‘impulse’ can test vestibular function of
all semicircular canals. Depending on the semicircular canal tested, the
head is rotated in a different direction [8, 9]. A corrective catch-up
saccade is made in case of vestibular hypofunction. HIT can be performed
with or without the use of a noninvasive video-oculography device (i.e.
Video Head Impulse Test: VHIT). This device consists of goggles that
contain a high-speed infrared video camera that tracks eye movements
and accelerometers that track head movements [10].
Although applying HIT may sound simple at first, some challenges are met
when performing it. The first challenge is to adequately deliver the
stimulus: it should be a high acceleration (1,000–6,000°/s2), rapid (100–
200°/s), low-amplitude (10–20°) head rotation. The horizontal as well as
the vertical canals can be tested. For the horizontal canals, the head is
moved in the horizontal plane. This is different for the vertical canals. For
this, it is important to know that the vertical canals form two pairs: The
left anterior and the right posterior canal (they are called LARP) and the
right anterior and left posterior canal (they are called RALP). They form
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pairs, since the anterior canal of one side, is oriented in the same plane as
the posterior canal of the other side. This can be seen in Figure 1 [11].
Figure 1. Orientation of the canals
This means that a head movement in the plane of for example LARP, has
effect on both canals. The anterior canal is sensitive for rotations going
down in its plane, and the posterior canal is sensitive for rotations going
up in its plane. Therefore, if you want to test the left anterior canal for
example, the following steps have to be taken: First bring the head in line
of the canal, so turn the head to the right. Secondly, have the patient
fixate on a target, for example your nose. Thirdly, make an impulse in line
of the canal and use the direction in which the canal is most sensitive.
Since the anterior canal is most sensitive for moving down, make a down-
wards movement. The same paradigm can be used for the other canals.
This is shown in Figure 2a and 2b [11].
Figure 2a. Testing LARP Figure 2b. Testing RALP
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For both horizontal and vertical impulses, the head movements can be
applied inward or outwards (figure 3). With the inward impulses, the head
is first displaced laterally and then rapidly rotated back to the center.
With the outward impulses, the head is put in neutral position and then
rapidly rotated toward either side. The inward impulses might be easier
to interpret in patients with acute unilateral peripheral vestibulopathy,
where spontaneous nystagmus will vary in intensity depending on orbital
position (figure 3). Also, less bounce artifacts are present. However,
outward impulses are less predictable, since the neck offers no clue as to
the direction of the next impulse. This might reduce the risk of covert
saccades (see below). Therefore, the risk of erroneously identifying a
normal HIT is higher using the inward technique [12].
Figure 3. Two head impulse techniques in a patients with left unilateral
vestibular deficit: inward HITs toward the deficient labyrinth with an
eccentric head and eye position before the HIT, and outward HITs to the
left, where the head and eye start moving from a centered position. The
final resting head and eye position, which is eccentric in outward HITs, is
important. Such an eccentric eye position would enhance an underlying
spontaneous nystagmus according to Alexander’s law and, thus,
potentially confound test interpretation [12].
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When using VHIT, one should pay attention by avoiding a loose strap,
wrong calibration, pupil tracking loss, (mini-)blinks, touching the goggles,
patient inattention and investigator induced bounce; if these are not
avoided, they will result in artifacts [13].
The second challenge is not to be fooled by preprogrammed compensatory
saccades (‘covert saccades’) that can be invisible to the naked eye of the
examiner and can occur (not only) in bilateral vestibulopathy patients.
Consequently, vestibulopathy may be missed [14]. A recent study by
Strupp et al. indicated that HIT observed by the naked eye of experts is
false negative for about 50% of the patients when compared to VHIT [15].
This clearly supports the use of the VHIT device, which is able to track
these saccades. Examples of normal and abnormal VHIT recordings with
overt and covert saccades are presented in Figure 4.1a–c.
The third challenge is to correctly interpret the traces. VHIT traces can
have many artifacts, leading up to 42% of uninterpretable traces [13].
Besides these artifacts, eye movements in patients with a vestibular
hypofunction can show patterns that challenge interpretations. Ideally,
vestibulo-ocular reflex gain is calculated by peak eye velocity divided by
peak head velocity [16]. However, artifacts and abnormal patterns distort
the process of correct gain calculation, and commercially available soft-
ware is not yet able to adequately compensate for it. An example of an
eye movement pattern that interferes with gain calculation is presented
in Figure 4.2. In order not to miss a bilateral vestibulopathy, a physician
should not yet solely rely on software processing for gain calculation, but
should be trained in assessing the raw data and should be aware of the im-
pact of deviant eye movement patterns and measurement artefacts [13].
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Figure 4.1 Raw VHIT recordings of different subjects, recorded with the
EyeSeeCam system (EyeSeeCam VOG; EyeSeeCam, Munich, Germany).
Head velocity traces are shown in gray, eye velocity traces in black. a VHIT recordings of head impulses to the right in a healthy subject. The
eye movements compensate for the passive head movements. b VHIT
recordings of head impulses to the left in a patient with a peripheral
vestibular deficit, resulting in overt saccades (peaks in eye velocity after
head movements). The eye movements do not compensate for the passive
head movements. c VHIT recordings of head impulses to the right in a
patient with a peripheral vestibular deficit, mainly resulting in covert
saccades (peaks in eye velocity during head movements).
300Rightn= 3
200EyeHead
100
0 –100 –200
–3000 100 200 300
c Time(ms)
Velocity (°/s)
300Leftn= 4
200EyeHead
100
0 –100 –200
–3000 100 200 300
b Time(ms)
Velocity (°/s)
300Rightn= 4
200EyeHead
100
0 –100 –200
–3000 100 200 300
a Time(ms)
Velocity (°/s)
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Figure 4.2 Example of an eye movement pattern that interferes with gain
calculation. Raw VHIT recordings of head impulses to the left in a patient
with bilateral vestibulopathy are presented. Head velocity traces are
shown in gray, eye velocity traces in black. Normally, gain is calculated by
peak eye velocity divided by peak head velocity. In this case, gain
calculation is challenged, since at the moment the peak head velocities
are reached, the eyes are actually moving along with the head in the same
direction. The passive head movements are not compensated by the eye
movements. Although this is clearly an abnormal HIT, there is not yet any
consensus about how to determine (or whether it is even possible to
determine) the real peak eye velocity which is necessary for gain
calculation.
The fourth challenge is to correctly interpret the end result. HIT provides
a stimulus for measuring gain of the vestibulo-ocular reflex which is
different from those used in other vestibular tests such as the rotatory
chair tests or the caloric test; it includes many more high frequency
components than the rotatory chair tests and the caloric test. Differences
in response to the caloric test versus the rotation tests versus HIT are
especially pointing to this difference in frequency content. It has been
shown that a bilateral vestibular loss can be measured with the caloric
test, while the responses as measured with HIT are relatively preserved
[17, 18]. In other words, it is necessary to understand that the presence of
a normal vestibulo-ocular reflex as measured with HIT does not rule out a
vestibular deficiency.
300Leftn= 3
200EyeHead
100
0 –100 –200
–3000 100 200 300
Time(ms)
Velocity (°/s)
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Dynamic visual acuity
During head movements, efficient stabilization of the image on the retina
is necessary to preserve visual acuity [19]. In (bilateral) vestibulopathy
patients, gaze stabilization fails and can lead to significant deterioration
in visual acuity during head movements [20, 21]. Visual acuity in dynamic
conditions can be assessed by testing for DVA. DVA testing can be
performed in many ways: the patient has to read letters from a visual
acuity chart or a computer screen during active or passive, vertical or
horizontal head movements, or while walking on a treadmill at different
velocities [19, 22]. Passive high-angular-velocity movements (150°/s) have
been shown to be most useful for discrimination between healthy subjects
and patients with a unilateral or bilateral vestibular loss. However, that
study did not include DVA testing by walking on a treadmill [23]. A decline
of more than 2 lines on the optotype chart is considered abnormal [24],
although a loss of 2 lines (0.2 logMAR) is not unusual for healthy subjects.
In order to trade sensitivity for specificity, 4 lines may be required [25].
Moreover, DVA may show false negative results due to mechanisms that
at least partially compensate for the retinal instability during head
movements [3, 23]. However, in subjects with unilateral and bilateral
vestibular loss, computerized DVA testing reached a sensitivity of 94.5%
and a specificity of 95.2% [26]. In another group of bilateral vestibulo-
pathy patients, DVA was impaired in 96% of the cases [27]. To conclude,
DVA can help establishing the diagnosis of (bilateral) vestibulopathy, but a
normal DVA does not definitely rule out bilateral vestibulopathy, and an
impaired DVA does not imply vestibulopathy per se. It is still not under-
stood by which specific vestibular deficits (which semicircular canals,
which otolith organs and which frequencies) DVA decreases.
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Head shake test [4]
The head shake test is performed by shaking the head of the patient when
the patient is wearing Frenzel or video goggles. The head is rotated at a
comfortable range at a frequency of about 2 to 3 Hertz for 10- to 15
seconds. After shaking, the head remains in the center and the eyes of the
patient are observed for nystagmus. The head shake test is used to look
for signs of dynamic imbalance of vestibular function by evaluating the
post-shaking nystagmus. This test is part of the whole diagnostic test
battery and will not give enough information on its own.
Different types of nystagmus can be found when applying the head shake
test. First a schematic representation of the process of head shaking will
be used to explain the physiology: By shaking the head, the velocity
storage within the vestibular nuclei is charged. So when the head is turned
to the right a VOR is produced moving the eyes in the opposite direction.
At the same time the velocity storage is charged with each head turn to
the right. For schematic purposes, we will call this “the velocity storage
on the right”. When the head is turned to the left, the velocity storage on
the left is charged. However, in case of a vestibular hypofunction or
imbalance, the velocity storage on the affected side cannot be charged as
much as the velocity storage on the other side due to the hypofunction.
This will become apparent when suddenly the head is stopped at the end
of the shaking. At that moment, both velocity storages discharge. If one
velocity storage was better charged than the other one, this will discharge
more strongly. At that moment it gives the same result as if the head was
turning to the side of the strongest velocity storage. This results in a
nystagmus away from the affected side. Therefore, in for example an
recent vestibular loss, a post-head shaking nystagmus might be found
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pointing towards the healthy side. In some cases, the nystagmus may
reverse direction after the initial phase. This probably reflects an adapta-
tion mechanism. However, it is not always this easy, since nystagmus does
not always point to the affected side. In some cases, the brain already
compensated to the hypofunction. This means, from a schematic point of
view, that the velocity storage on the side of the hypofunction, is equally
charged compared to the healthy side when the head is rotated. That is
why, after a longer standing vestibular loss, the head shake test does
often not show any post shaking nystagmus. However, if in the meantime
the vestibular function on the paretic side was restored, the new level of
velocity storage on the paretic side velocity storage becomes excessive
relative to the compensation. During head shaking, the velocity storage on
the paretic side becomes more charged than on the healthy side. At the
end of head shaking, the velocity storage of the paretic side will therefore
discharge stronger than the healthy side. Since nystagmus points to the
strongest side, the post shaking nystagmus will point to the paretic or
former paretic side. This is called a “recovery” nystagmus.
In some central cases, mainly of the cerebellum and brainstem, head
shaking induced nystagmus can also be found. The nystagmus may beat
ipsilaterally, but also a cross-coupled “perverted” nystagmus can be
present. This means that horizontal head shaking induces a vertical post
head shaking nystagmus. From a schematic point of view: horizontal
vestibular input is calculated wrongly by the central system and this
results in a vertical nystagmus. So when a vertical nystagmus results after
the head shaking test, always take a central vestibular disorder into
account.
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Keypoints
Each vestibular test has its own sensitivity, specificity and challenges
when applying it in clinical practice:
- The Romberg test is not a sensitive test for vestibular hypofunction.
The Romberg test on foam rubber can increase sensitivity and
specificity.
- An abnormal clinical head impulse test is a sign of vestibular hypo-
function, but a normal clinical head impulse test does not rule out
vestibular hypofunction, mainly due to adaptation mechanisms. A
video head impulse test can help detecting these adaptive
mechanisms.
- The Dynamic Visual Acuity test can help establishing the diagnosis of
(bilateral) vestibulopathy, but a normal DVA does not definitely rule
out bilateral vestibulopathy, and an impaired DVA does not imply
vestibulopathy per se.
- The head shake test is used to look for signs of dynamic imbalance of
vestibular function by evaluating the post-shaking nystagmus (slow
phases directed toward affected ear, or recovery nystagmus, or
perverted nystagmus). This test is part of the whole diagnostic test
battery and will not give enough information on its own.
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