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http://oto.sagepub.com/Otolaryngology -- Head and Neck Surgery
http://oto.sagepub.com/content/147/5/912The online version of this article can be found at:
DOI: 10.1177/0194599812452993
2012 147: 912 originally published online 29 June 2012Otolaryngology -- Head and Neck SurgeryMei-Chun Lin and Yi-Ho Young
The Use of Vestibular Test Battery to Identify the Stages of Delayed Endolymphatic Hydrops
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Original ResearchOtology and Neurotology
The Use of Vestibular Test Battery toIdentify the Stages of DelayedEndolymphatic Hydrops
Otolaryngology
Head and Neck Surgery
147(5) 912918
American Academy of
OtolaryngologyHead and Neck
Surgery Foundation 2012
Reprints and permission:
sagepub.com/journalsPermissions.nav
DOI: 10.1177/0194599812452993
http://otojournal.org
Mei-Chun Lin, MD1, and Yi-Ho Young, MD1
No sponsorships or competing interests have been disclosed for this article.
Abstract
Objective. Patients with delayed endolymphatic hydrops (DEH)underwent a vestibular test battery to evaluate the residualfunction, assess their clinical stage, and predict outcome.
Study Design. Case series with chart review.
Setting. University hospital.
Subjects and Methods. Twenty patients with DEH, 15 with
ipsilateral type and 5 with contralateral type, were enrolled.All patients underwent audiometry and caloric, ocularvestibular-evoked myogenic potential (oVEMP), and cervicalVEMP (cVEMP) tests. The DEH staging was based on vestib-ular test results. Stage 0 indicates that all 3 vestibular testsare normal, while stages I through III indicate abnormalresults in tests 1 through 3, respectively.
Results. Of the 20 DEH patients, 2 patients were stage 0, 12patients were stage I, 4 patients were stage II, and 2 patientswere stage III. The median frequency of vertigo in patientswith stages II and III was 4 episodes monthly, significantlyless than 15 episodes monthly in those with stages 0 and I.
Ipsilateral and contralateral types did not differ significantlyin the stage distribution. The percentages of abnormalcVEMP, oVEMP, and caloric test results for patients with ipsi-lateral type were 80%, 33%, and 13%, not significantly differ-
ent from those for contralateral type.
Conclusions. As a vertiginous attack may subside sponta-neously for patients with long-term DEH, one must identify
its clinical stage based on cVEMP, oVEMP, and caloric testresults. In early stage DEH, most vestibular function
remained relatively intact, leading to repeated vertiginousattacks. Conversely, subsidence of vertiginous episode canbe anticipated in patients with late stage DEH.
Keywords
delayed endolymphatic hydrops (DEH), vestibular-evokedmyogenic potential (VEMP), cervical VEMP (cVEMP), ocular
VEMP (oVEMP)
Received March 23, 2012; revised May 14, 2012; accepted June 6, 2012.
Ipsilateral delayed endolymphatic hydrops (DEH) refers
to one ear with profound hearing loss. After several
years or decades, episodic vertigo occurs, accompanied
by nausea and vomiting.1,2 Contralateral DEH exhibits the
same features as ipsilateral DEH and hearing loss in the
opposite (better) ear fluctuates. Via a long-term follow-up
study of cases with both ipsilateral and contralateral DEH,
Kamie3 reported that 65% to 90% of cases had episodic ver-
tigo that vanished within 5 to 10 years.
According to the American Academy of Otolaryngology
Head and Neck Surgery,4 Menieres disease staging was based
on the arithmetic mean of pure tone thresholds at 0.5, 1, 2,
and 3 kHz using the worst audiogram at 6 months before treat-
ment. However, this staging system for Menieres disease
cannot be applied to cases with ipsilateral DEH, since the
latter manifests as profound sensorineural hearing loss on the
lesion ear. Alternatively, the interaural amplitude difference
(IAD) ratio (now termed asymmetry ratio) of the vestibular-
evoked myogenic potential (VEMP) test correlates with
Menieres disease stage and can be used as another tool forassessing the stage of Menieres disease.5
By stimulating the ear with loud sound or bone vibration
stimuli, VEMP can be recorded on contracted neck muscles,
now called cervical VEMP (cVEMP), and on the extraocular
muscles, termed ocular VEMP (oVEMP).6-8 These two
recently developed electrophysiological tests expand the test
battery for clinicians to assess utricular and saccular hydrops
in patients with Menieres disease.9-11 Based on the hypothesis
of efferent specificity proposed by Curthoys,12 cVEMP
arises from the saccular macula, whereas oVEMP predomi-
nantly originates from the utricular macula. Thus, when using
the inner ear monitoring system13
such as audiometry andcVEMP, oVEMP, and caloric tests to study the localization
and prevalence of hydrops formation, it reveals that the declin-
ing function in the cochlea, saccule, utricle, and semicircular
canals mimics the declining sequence of hydrops formation in
temporal bone studies.14,15 As the disease progresses, canal
1Department of Otolaryngology, National Taiwan University Hospital,
Taipei, Taiwan
Corresponding Author:
Yi-Ho Young, MD, Department of Otolaryngology, National Taiwan
University Hospital, 1 Chang-te St, Taipei, TaiwanEmail: [email protected]
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paresis is noted in 50% of Menieres patients after the first
decade.16,17 Restated, the fluctuation of endolymphatic hydrops
can be reflected by functional deterioration and recovery of
the cochlea, saccule, utricle, and semicircular canals. Thus, in
this study, DEH patients underwent a vestibular test battery to
evaluate residual vestibular function, assess their clinical stage,
and predict outcome.
Patients and Methods
Patients
From January 2009 to December 2010, consecutive 20
patients with DEH were encountered at the clinic (less than
180 patients with Menieres disease experienced during the
same period). The diagnosis of DEH was based on the liter-
ature.18 Briefly, one ear suffered from profound hearing loss
previously, with a pure tone average of 500, 1000, and 2000
Hz . 90 dB. Following several years or decades, episodic
vertigo accompanied by nausea/vomiting occurs (ipsilateral
type), or fluctuating hearing loss is noted on the opposite
ear (contralateral type). No central nervous system disorderwas observed.
Exclusion criteria consisted of concurrent middle or inner
ear infection or anomaly, previous ear surgery, systemic dis-
eases, neurological diseases (eg, acoustic neuroma and brain
tumor), and recent head trauma (within 6 months).
Eight patients were men and 12 patients were women,
with their ages ranging from 25 to 68 years (mean, 48 years).
Right side was affected in 7 ears and left side in 13 ears.
Fifteen patients were classified as ipsilateral type, while 5
patients belonged to contralateral type (Table 1). Neither
temporal bone CT scan nor MR imaging revealed abnormal-
ities in these patients. Prior to treatment, all patients underquiescent state received a battery of tests including otoscopy,
audiometry, and caloric, oVEMP, and cVEMP tests.
This study was approved by the institutional review
board of the College of Medicine, National Taiwan
University Hospital, and each subject signed the informed
consent to participate.
Caloric Test
Bithermal caloric test was conducted with electronystagmo-
graphic recorders (Sanei 1B21, Tokyo, Japan). Canal paresis
was defined when the mean slow phase velocity (SPV)\ 17o/s,
or as a greater than 25% difference between maximum slowphase velocity measurements for each ear, when compared with
the sum of SPVs from each ear. If no caloric response was eli-
cited, the subject underwent ice water (0oC, 10mL) caloric test-
ing to further confirm the caloric areflexia.
oVEMP Test
The subject was in a sitting position. Surface potentials, pre-
dominantly electromyographic (EMG) activities, were
recorded (Smart EP 3.90, Intelligent Hearing Systems,
Miami, Florida, USA). Two active electrodes were placed
around 1 cm below the center of the 2 lower eyelids. The
other 2 reference electrodes were positioned about 1 to 2
cm below the active ones, and 1 ground electrode was
placed on the sternum. During recording, the subject was
instructed to look upward at a small fixed target . 2 m
from the eyes, with a vertical visual angle of approximately
30o above horizontal. The EMG signals were amplified and
bandpass filtered between 1 and 1000 Hz. The stimulation
rate was 5 Hz. The duration of analysis of each response
was 50 ms, and 30 responses were averaged for each run.
The operator held the vibrator by hand so that the axis ofthe connected bakelite cap perpendicularly delivered a
repeatable tap on the subjects skull at Fz (midline of the
hairline). The initial peak driving voltage was about 8 V,
equivalent to 128 dB force level (FL). The input signal was
a half cycle 500 Hz sine wave, driven by a custom
amplifier.
The initial negative-positive biphasic waveform com-
prised peaks nI and pI. Consecutive runs were performed to
confirm the reproducibility of peaks nI and pI, and oVEMPs
were deemed to be present. Conversely, oVEMPs were
deemed to be absent when the biphasic waveform was not
reproducible. At our laboratory, the norm for the latency ofpeak nI was 11.4 6 0.8 (mean 6 SD) ms. Those with the nI
latency exceeding 13.0 ms were defined as delayed
response. The asymmetry ratio (%) was defined as the dif-
ference of the amplitude nI pI on each ear divided by the
sum of amplitude nI pI of both ears, that is, (larger ampli-
tude smaller amplitude / larger amplitude 1 smaller
amplitude) 3 100. Those with asymmetry ratio . 40%
were interpreted as reduced responses.19
cVEMP Test
Each subject was in a supine position. Two active electrodes
were placed on the upper half of the sternocleidomastoid(SCM) muscles; one reference electrode was positioned on
the suprasternal notch, and a ground electrode was situated
on the forehead. The other settings were the same as in the
oVEMP test, except that the vibrator delivered a repeatable
tap on the subjects head at inion.19 To measure background
muscle activity, subjects were given feedback of the level
of EMG activity in their SCM muscles during data collec-
tion and were required to keep a background muscle activity
of at least . 50 mV.20 The subjects elevated their heads
during testing. A total of 50 responses were averaged and
recorded bilaterally.
The first positive and second negative polarities of bipha-sic waveform were termed waves p13 and n23, respectively.
Consecutive runs were performed to confirm the reproduci-
bility of peaks p13 and n23, and cVEMP responses were
termed present. The latencies of p13, n23, and amplitude
p13 n23 were measured. At our laboratory, the norm for
the latency of p13 was 14.4 6 1.3 (mean 6 SD) ms, and
we defined when the latency of peak p13 exceeding 17.0 ms
as delayed cVEMPs. In addition, those with asymmetry
ratio . 33% were defined as reduced response.
Statistical Methods
Comparison of the abnormal test results between the 2 types
was analyzed by Fishers exact test. Comparison of the
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abnormal test results between the 2 sides was analyzed by
McNemar test. Frequency of vertigo between the stages was
compared by Mann-Whitney U test. A significant difference
indicates the P value\ .05.
Results
Clinical Manifestation
Clinical manifestation consisted of hearing loss in all 20
patients, vertigo in 15 (75%), nausea in 13 (65%), tinnitus
in 11 (55%), headache in 8 (40%), and aural fullness in 7
(35%). The median interval between initial deafness and
diagnosis of DEH was 10 years (range, 2-30 years).
Audiometry
All patients had profound hearing loss (. 90 dB) in at leastone ear. For the better hearing ear, the 4-tone average at
0.5, 1.0, 2.0, and 3.0 kHz was\ 26 dB in 12 ears, 26 to 40
dB in 5 ears, and 41 to 70 dB in 3 ears ( Table 1).
Vestibular Test Battery
Of the 20 affected ears (Table 2), the cVEMP test identi-
fied normal responses for 6 ears and abnormal responses for
14 ears (70%), including absent cVEMPs in 13 ears and
delayed cVEMPs in 1 ear. The oVEMP test revealed normal
responses for 11 ears and abnormal responses for 9 ears
(45%), consisting of absent oVEMPs in 8 and reduced
oVEMPs in 1. With the caloric test, normal responses were
shown in 17 ears and canal paresis was observed in 3 ears
(15%).
For the opposite unaffected ears, the cVEMP, oVEMP,
and caloric tests identified abnormal responses in 55%,30%, and 30% of the ears, respectively (Table 2). There
were no significant differences in the abnormal percentage
of the 3 tests between the affected and unaffected ears (P .
.05, McNemar test).
DEH Staging
The DEH staging was based on cVEMP, oVEMP, and calo-
ric test results. Stage 0 indicates that all 3 test results of the
affected ear are normal; stage I indicates that 1 of 3 test
results are abnormal (Figure 1); stage II indicates that 2
test results are abnormal (Figure 2); and stage III indicates
that no test result is normal. Of the 20 DEH patients, 2patients were classified as stage 0, 12 patients were stage I,
4 patients were stage II, and 2 patients were stage III
(Table 2).
Frequency of Vertigo versus DEH Stage
Frequency of vertigo is defined as the total vertiginous epi-
sodes within 1 month before treatment. Of the 15 DEH
patients with vertigo, the median frequency of vertigo for
patients with stages II and III was 6 episodes (range, 1-10)
monthly, significantly less than 15 episodes (range, 6-30)
monthly in those with stages 0 and I (P \ .05, Mann-
Whitney U test).
Table 1. Clinical Information of 20 Patients with Delayed Endolymphatic Hydrops
Four-Tone Average(dB)
Case No. Age, y Sex Side Type Right Left
1 68 F R I so 28
2 68 M R I so 38
3 57 F R I so 194 42 F R I so 26
5 25 F R I 93 12
6 61 M R I so 28
7 45 M R I so 13
8 57 F L I 24 so
9 42 F L I 4 so
10 52 F L I 18 so
11 34 M L I 11 94
12 58 M L I 36 so
13 68 F L I 23 90
14 48 F L I 6 so
15 32 F L I 12 so16 34 M L C so 53
17 55 F L C so 64
18 40 F L C so 19
19 29 M L C 103 51
20 55 M L C so 17
Abbreviations: I, ipsilateral type; C, contralateral type; so, scale out.
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Ipsilateral versus Contralateral Types
The percentages of abnormal cVEMP, oVEMP, and calorictest results were 80%, 33%, and 13% for ipsilateral type
and 40%, 80%, and 20% for contralateral type, respectively.
Both types did not differ significantly, regardless of whether
cVEMP, oVEMP, or caloric test results were analyzed (P .
.05, Fishers exact test). One, 10, 3, and 1 patients of ipsilat-
eral type and 1, 2, 1, and 1 patients of contralateral type
were classified as having stage 0, I, II, and III, respectively.
The staging distribution did not significantly differ for both
types (P . .05).
Discussion
The mechanism of DEH is a sufficiently major labyrinthineinsult that causes total deafness while vestibular function is
preserved, producing delayed atrophy or fibrous obliteration
of the endolymph resorption system.2 Thus, clinical expres-
sions of DEH vary with involvement severity. The most
severe involvement results in immediate total loss of auditory
and vestibular function, whereas the mildest involvement
causes delayed malfunction of endolymph resorption, result-
ing in episodic vertigo (ie, ipsilateral type) and/or fluctuating
hearing loss (ie, contralateral type). Clinically, it is usually
difficult to determine the ear causing vertigo when ipsilateral
DEH occurs in patients with bilateral profound hearing loss
unless it is accompanied by tinnitus or aural fullness during
episodic vertigo. When the vestibular involvement occurs in
both ears, termed bilateral DEH, the time of onset could be
different for each ear. In other words, 2 situations are sup-
posed in bilateral DEH; namely, both ears are affected by the
ipsilateral type, or 1 ear is affected by the ipsilateral type
while the other ear is affected by the contralateral type.3
Nevertheless, such a case has rarely been observed.
As the recently developed inner ear test battery including
audiometry and cVEMP, oVEMP, and caloric tests investi-
gates the inner ear function completely,13 it may assist clini-
cians in evaluating inner ear involvements in DEH patients
with various inner ear insults.
Inner Ear Test Battery
The presence of normal cVEMPs implies that the sacculo-collic reflex has retained normal conduction velocity; an
intact saccular macula accounts for normal cVEMPs.
Histopathological study of DEH demonstrated that the sac-
cule was markedly dilated with the saccular macula either
severe degenerated or apparently normal, accompanied by
partial cellular encapsulation of the otolithic membrane, and
a granular basophilic plaque overlying the supporting net-
work of the macular epithelium.2 These findings correlate
with the high rate (70%) of abnormal cVEMPs for DEH
patients (Table 2) and are compatible with those in previ-
ous reports.21,22
However, DEH ears with absent cVEMPs also provoke
episodic vertigo, indicating that factors other than saccule
Table 2. Vestibular Test Results in 20 Patients with Delayed Endolymphatic Hydrops
Case No.
(ears)
cVEMP Test
(affected/opposite)
oVEMP Test
(affected/opposite)
Caloric Test
(affected/opposite) Stage
1 absent/absent n/absent n/n I
2 absent/n n/absent cp/n II
3 absent/n n/n n/n I
4 absent/n n/n n/n I
5 absent/n n/n n/n I
6 absent/n absent/absent cp/absent III
7 absent/absent n/n n/n I
8 n/n absent/n n/n I
9 n/n n/n n/n 0
10 absent/delayed n/n n/n I
11 n/absent reduced/n n/n I
12 delayed/absent absent/n n/n II
13 absent/n absent/n n/n II
14 absent/absent n/n n/n I
15 absent/absent n/n n/n I
16 n/n absent/n n/absent I
17 absent/absent absent/absent cp/absent III
18 absent/absent absent/absent n/absent II
19 n/absent absent/absent n/absent I
20 n/absent n/n n/cp 0
Abnormal rate 70%/55%a 45%/30%a 15%/30%a
Abbreviations: cp, canal paresis; n, normal.aP. .05, McNemar test.
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Figure 1. Case No. 5, female, 25 years, delayed endolymphatic hydrops, right, stage I, ipsilateral type. Caloric test results are normal. The
oVEMP test shows normal (nI pI) responses, bilaterally. The cVEMP test shows absent responses on the right ear, but normal (p13 n23)
responses on the left ear.
Figure 2. Case No. 13, female, 68 years, delayed endolymphatic hydrops, left, stage II, ipsilateral type. Caloric test results are normal. Both
oVEMP and cVEMP tests show normal responses on the right ear, but absent responses on the left ear.
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prevail. Thus, function of the utricle and semicircular canals
warrants further investigation.
As it stimulates the semicircular canals, the caloric test
has been utilized to analyze the rotational vestibulo-ocular
reflex (VOR) system in individual ears for over 100 years.
In contrast, the recently developed oVEMP test assesses the
translational VOR by activating the otolithic maculae. As
saccular neurons have a strong projection to neck musclesand a weak projection to the oculomotor system, neural con-
nections in the sacculo-ocular system are relatively weak
compared with neural connections in the utriculo-ocular and
sacculo-collic reflexes.23 Thus, the oVEMP test may reflect
utricular macula activity. Unlike the substantial damage to
the pars inferior (cochlea and saccule) in DEH patients, the
pars superior (utricle and canals) was relatively intact, as
evidenced in a temporal bone study by the normal appear-
ance of the utricular macula, crista ampullaris, and semicir-
cular ducts except for dilatation of the utricle.2 These
findings may explain why abnormal percentages of oVEMP
(45%) and caloric (15%) tests are less than that of thecVEMP (70%) test. Even in the opposite unaffected ears,
similar deteriorated results are also observed (Table 2),
indicating that primary labyrinthine insult may cause poten-
tial defects in both ears. Once both ears showed deteriorated
functions in vestibular test battery, which ear having tinnitus
or aural fullness during vertiginous episode was considered
to be the cause of vertigo.
In our previous report,14 abnormal percentages of cVEMP,
oVEMP, and caloric tests in Menieres ears were 45%, 25%,
and 20%, respectively. In this study, those in DEH cases
were 70%, 45%, and 15%, respectively. Notably, the declin-
ing sequence of abnormal percentages of cVEMP, oVEMP,and caloric tests in DEH cases mimics that in Menieres
cases, and this further supports that DEH and Menieres dis-
ease may, at least in part, share the same pathophysiology.
In late stage Menieres disease, severe dilatation or col-
lapsed ampullary walls may interfere with cupular move-
ment, resulting in a poor caloric response.17 The vestibular
sense organs may also undergo severe atrophic change.
After repeated ruptures of the labyrinthine membrane, par-
tial or total collapse of the membranous labyrinth ensues.
This condition is coined as vestibular atelectasis.24 These
histopathological findings explain why caloric areflexia was
observed in late stage Menieres disease, leading to sponta-neous relief of vertigo. As only 15% of DEH ears in this
study showed canal paresis, one may expect that most
patients had preserved canal function, leading to frequent
vertiginous attacks. Conversely, most vestibular function
deteriorates in late stage DEH patients, which may cause
relief of vertiginous episode. Hence, investigating residual
vestibular function to identify the clinical stage of DEH is
necessary.
However, one may question whether a physician can
base the decision on whether someone is at a late stage of
DEH according to the number of episodes of vertigo he or
she has. As some DEH patients with episodic vertigo may
visit other hospitals for help, the true numbers of episodic
vertigo may be higher than estimation. Nevertheless, this dis-
advantage can be overcome with the aid of caloric, oVEMP,
and cVEMP tests, which may help evaluate the residual ves-
tibular function in deaf ears. It takes a short time (approxi-
mately 20 minutes) for both oVEMP and cVEMP tests, and
the fee for the vestibular test battery (including ENG,
oVEMP test, and cVEMP test) at our hospital costs US$70,
which is significantly less than a routine MR imaging(US$700). Thus, it would be practical to make the inner ear
test battery a routine examination in DEH patients.
Clinical Relevance
As episodic vertigo disappeared in 90% of DEH patients
within 10 years,3 vertiginous attacks may subside sponta-
neously. For those with intractable vertigo, surgical labyr-
inthectomy or intratympanic gentamicin injections may be
an alternative treatment for abolition of the vestibular func-
tion.18 Our study is useful because when a surgeon can
identify the DEH stage, surgical intervention may be
reserved in late stage DEH patients. For patients with pro-found deafness and recalcitrant vertigo, surgical labyr-
inthectomy or gentamicin injection should be mentioned as
a treatment option, and this may be reasonable early in the
disease process since many DEH patients ultimately lose
significant vestibular function.
Conclusion
As a vertiginous attack may subside spontaneously for
patients with long-term DEH, one must identify its clinical
stage based on cVEMP, oVEMP, and caloric test results. In
early stage DEH, most vestibular function remained rela-
tively intact, leading to repeated vertiginous attacks.Conversely, subsidence of vertiginous episode can be antici-
pated in patients with late stage DEH, and surgical interven-
tion may be set aside.
Author Contributions
Mei-Chun Lin, performed VEMP and wrote paper; Yi-Ho Young,
supervised study.
Disclosures
Competing interests: None.
Sponsorships: None.
Funding source: None.
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