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Acta Oto-Laryngologica.

2014; 134: 34–40

ORIGINAL ARTICLE

Vestibular evoked myogenic potential according to middle ear condition


in chronic otitis media with tympanic membrane perforation

JUN SEOK LEE, SUN KYU LEE, IL HO SHIN, SEUNG GEUN YEO, MOON SUH PARK &
JAE YONG BYUN

Department of Otorhinolaryngology-Head and Neck Surgery, School of Medicine, Kyung Hee University, Seoul, Korea

Abstract
Conclusion: Vestibular evoked myogenic potential (VEMP) function results can vary between individuals with different middle
ear conditions. Therefore, by analyzing VEMP results after paper patching, we can predict the condition of the middle ear in
chronic otitis media (COM) patients. Objectives: VEMP responses decrease with impairment of sound transmission, such as in
conductive hearing loss (CHL). COM with tympanic membrane (TM) perforation is a common disorder that causes various
degrees of CHL. The aim of this study was to evaluate and clarify the VEMP responses in patients with COM with different
middle ear pathology. Methods: This study included 50 patients with unilateral COM with TM perforation. Initial pure-tone
audiometry (PTA) and VEMP responses were recorded. After paper patching, PTA and VEMP were re-performed. Each
VEMP response was compared with those of the healthy controls. Moreover, VEMP responses between pre- and post-paper
patching were compared. Results: There was a positive correlation between normalizing of VEMP parameters, such as p13 and
VEMP asymmetry ratio (VAR), and reduction of air–bone gap in patients with COM after paper patching. The VEMP
response in patients with COM with intact ossicle and clean mucosa was more normalized compared with those in patients with
COM with different middle ear conditions.

Keywords: Conductive hearing loss, paper patch, air–bone gap, VEMP asymmetry ratio

Introduction CHL or mixed hearing loss, depending on different


middle ear pathologic conditions. VEMP responses
Vestibular evoked myogenic potential (VEMP) is the are decreased although VEMP responses are elicited
reflex myogenic potential of neck muscles that is in patients with COM [2]. However, the VEMP
elicited by stimulating the vestibular system of the responses of patients with COM according to differ-
ear with a click or tone-burst sound. VEMPs have ent middle ear conditions such as ossicular status or
recently become a clinical tool for evaluating the the middle ear mucosal status remains unclear [3].
sacculo-collic reflex, and they have been broadly We hypothesize that VEMP responses may differ
studied in patients with cochleo-vestibular disorders according to different middle ear conditions that can
[1]. Because the VEMP is evoked by loud sound influence the air–bone gap (ABG) in CHL in patients
stimulation, impairment of sound transmission with COM with TM perforation. This ABG can be
through the middle ear may affect VEMP results. reduced promptly by the application of a paper patch
VEMP responses are decreased in cases of if not all before surgery. The aim of this study was to
impairment of sound transmission, such as conduc- detect the effects of middle ear conditions on VEMP
tive hearing loss (CHL). Chronic otitis media (COM) responses and to clarify the changes in VEMP para-
with tympanic membrane (TM) perforation is a com- meters after paper patching in each middle ear
mon middle ear disease that causes various degrees of condition.

Correspondence: Jae Yong Byun MD PhD, Department of Otorhinolaryngology-Head and Neck Surgery, Kyung Hee University Hospital at Gangdong,
#149 Sangil-dong, Gangdong-gu, Seoul 134-090, Korea. Tel: +82 2 440 6182. Fax: +82 2 440 7336. E-mail: otorhino512@naver.com

(Received 18 May 2013; accepted 7 August 2013)


ISSN 0001-6489 print/ISSN 1651-2251 online  2014 Informa Healthcare
DOI: 10.3109/00016489.2013.836756
VEMPs according to middle ear conditions in COM 35

Material and methods patch and post-patch groups were tested with
Student’s t test or the Mann–Whitney U test. Statis-
Fifty patients (28 males, 22 females) with unilateral tical significance was assumed at p < 0.05. The
TM perforation due to COM were included in this changes in VAR and latencies after paper patching
study. Eardrum perforation was diagnosed with an according to changes in ABG were tested with Pear-
otoscope and confirmed with tympanometry. We son correlation. The Statistical Package for the Social
excluded patients with a history of vertigo, neurolog- Sciences (SPSS) Windows Release 10.0.1 (SPSS Inc.,
ical disorders, external auditory canal lesions, any Chicago, IL, US) was used for statistical analyses.
inner ear anomaly, and cholesteatoma. We explained the process of PTA and VEMP and
The ages of participants ranged from 21 to 71 years; obtained informed consent from patients. The Insti-
the mean age was 48.3 years. The right side was tutional Review Boards (IFC/IRB) of the Kyung Hee
affected in 18 patients, while 32 were affected on University Hospital at Gangdong (Seoul, Korea)
the left side. The air conduction hearing threshold approved the protocol of this study.
levels were determined as the average of pure-tone
thresholds of 500 Hz, 1 kHz, and 2 kHz. All patients
Results
had CHL (mean ABG more than 15 dB in 500, 1000,
and 2000 Hz) on pure-tone audiometry (PTA). Fifty patients with COM exhibited CHL with a mean
After confirmation of the inclusion criteria, PTA hearing threshold of 47.7 ± 23.7 dB and a mean ABG
and VEMP tests were performed. Following the PTA of 26.8 ± 11.3 dB. The hearing threshold levels and
and VEMP tests, we applied a paper patch on the ABGs of the participants with COM improved sig-
perforation side. Repeat PTA and VEMP tests were nificantly after paper patching (Table I, p < 0.05).
performed after 1 h to allow for drying. Before patching, the VEMP response rate on ipsilat-
For the recording of VEMP, the patients were in a eral stimulation was 64% (32/50), and it increased to
sitting position. The sound stimuli (500 Hz, 90 dB 86% (43/50) after the paper patch was applied
nHL short tone burst) were conducted to the ears (p < 0.05, Chi-squared test), defining absent VEMP
monoaurally with an insertion-type earphone. The as less than 15 mV of p13-n23 interamplitude. Of the
electromyographic signals were amplified and col- seven participants with no VEMP after paper patch-
lected with a bandpass filter using a digital system ing, all had moderate to severe hearing loss. Figure 1
(model Navigator Pro Loader Ver. 5.1, Bio-Logic shows the VEMP responses of one study participant
System Corp., Mundelein, IL, USA). The analysis with right-sided COM. After paper patching, a 10 dB
time was 53.3 ms. The responses to 64 stimuli were improvement of average hearing threshold levels was
averaged for 1 trial, and 2 trials were acquired for noted in the frequency range of 250–8000 Hz. The
1 complete test. The initial positive/negative polarity p13 and n23 latencies were delayed and interampli-
of the waveform with peaks identified as p13 and tude was decreased in the right-sided (affected side)
n23 on the basis of their latency was used to identify stimulations before paper patching (Figure 1B) How-
the presence or absence of VEMPs. Then, the laten- ever, the VEMP responses on the affected side
cies of p13 and n23 and the amplitudes of showed a shortening of latency and an increase of
p13-n23 were measured. The VEMP asymmetry ratio interamplitude after paper patching (Figure 1D). Fol-
(VAR) was calculated as (Au–Aa)/(Aa+Au), where lowing the paper patch procedure, p13 latency and
Au is the amplitude of p13-n23 on the unaffected side VAR were significantly decreased in the COM group
and Aa is the p13-n23 amplitude on the affected side. (Table I).
The latencies of p13 and n23 of the two trials were We divided COM patients according to the status
averaged to represent the latencies of each test, and of the ossicular chain, middle ear mucosa status, and
the maximum of the p13-n23 amplitudes of the two the size of eardrum perforation, which can affect
trials was considered the amplitude of the test. The sound transmission. Then we analyzed the VEMP
p13 latency of the healthy control participants parameters of each condition after paper patch
(26 males and 19 females aged 43.2 ± 15.4 years) application.
at our laboratory was 18.4 ± 2.9 ms (mean ± SD). The
latency of n23 was 27.44 ± 3.92 ms and the VAR of
Effect of TM perforation size
the healthy controls was 19.30 ± 4.56%. During the
surgery (tympanomastoidectomy or tympanoplasty), We used microscopic examination of the entire TM to
we verified TM perforation size, ossicular mobility, determine the size of the perforations. We defined the
and middle ear mucosa status. small-to-moderate-sized group as those patients hav-
The differences in VEMP results after patch appli- ing a perforation size of less than 50% relative to the
cation according to middle ear condition in the pre- entire TM, and patients with greater than 50%
36 J. S. Lee et al.

Table I. General characteristics and results of vestibular evoked myogenic potential testing and pure-tone audiometry.
Characteristic Normal controls COM patients COM patients p Value between
before patching after patching pre- and post-patch

No. of subjects 40 50
Age 43.2 ± 15.4 48.3 ± 14.6
Male:female 26:19 24:26
AC threshold average (dB) 6.1 ± 5.5 47.7 ± 23.7* 42.1 ± 24.2* 0.000†
AC threshold at 500 Hz (dB) 12 ± 14.2 50.8 ± 22.5* 44.2 ± 23.8* 0.000†
BC threshold average (dB) 2.3 ± 5.8 20.8 ± 18.1* 20.9 ± 17.4* 0.043†
BC threshold at 500 Hz (dB) 4.0 ± 9.7 16.0 ± 13.9* 17.0 ± 14.4* 0.286
ABG average (dB) 3.8 ± 2.3 26.8 ± 11.3* 21.2 ± 10.7* 0.000†
ABG at 500 Hz (dB) 8.0 ± 9.2 34.8 ± 16.8* 27.2 ± 15.4* 0.000†
VEMP
p13 latency (ms) 18.4 ± 2.9 21.9 ± 5.6* 19.6 ± 5.2 0.030†
n23 latency (ms) 27.44 ± 3.2 27.7 ± 5.8 27.4 ± 5.6 0.302
VAR (%) 19.30 ± 4.56 36.5 ± 17.8* 30.8 ± 17.2* 0.042†
ABG, air–bone gap; AC, air conduction; BC, bone conduction; COM, chronic otitis media; VAR, VEMP asymmetric ratio; VEMP, vestibular
evoked myogenic potential.
*Difference from normative data of normal controls with p < 0.05; †p < 0.05.

perforation were placed into the large-sized group. (10 tympanomastoidectomies). In the normal mucosa
The small-to-moderate-sized perforation group group, the interamplitude was 24.1 ± 5.9 mV, which
included 22 patients (16 tympanoplasties and 6 tym- significantly increased to 31.6 ± 6.7 mV after the paper
panomastoidectomies) and the large-sized group patching procedure; therefore, VAR significantly
included 28 patients (7 tympanoplasties and 21 tym- decreased from the values of 28.8 ± 4.6% to 19.1 ±
panomastoidectomies). No VEMP parameters showed 5.9% after paper patching (p < 0.05). In the moderate
any significant change after paper patching in the small- granulation or severe granulation group, no VEMP
to-moderate-sized perforation group. However, in the parameters changed significantly (Table III).
patients with large-sized perforations, the p13 latency
significantly decreased (Table II).

Effect of the ossicular chain status


Effect of middle ear mucosa status
During ear surgery, we checked ossicular chain status
We divided our participants into three additional by assessing the mobility of the malleoincudal, incu-
groups according to their intraoperative middle ear dostapedial (MI, IS) joint with slight tapping pressure
mucosa status. We were concerned about the middle on the malleus handle. We defined intact MI, IS joint
ear mucosal status in the middle ear cavity after mobility as an intact ossicular chain, and the absence
tympanomeatal flap elevation, and therefore placed or destruction of the ossicle was defined as ossicular
patients with nearly absent normal middle ear mucosa discontinuity. The intact ossicular chain group com-
into the severe pathologic mucosal group. If patients prised 22 patients (17 tympanoplasties and 5 tympa-
had mucosa with edematous changes in some part of nomastoidectomies) and the ossicular discontinuity
the tympanic cavity (less than half of the total area of group comprised 28 patients (6 tympanoplasties and
cavity), those patients were divided into the moderate 22 tympanomastoidectomies). In the intact ossicular
pathologic changes mucosal group; patients with no chain group, the p13 latency was initially 21.3 ±
granulation tissue were classified as being in the clean 6.1 ms, and it significantly decreased to 17.3 ±
mucosa group. The normal mucosa group comprised 5.6 ms after the paper patch procedure. The
20 patients (16 tympanoplasties and 4 tympanomas- n23 latency and VAR represented a nonsignificant
toidectomies), the moderate pathologic changes difference from the values obtained after paper patch-
mucosal group comprised 20 patients (7 tympanoplas- ing (p > 0.05). However, in the ossicle discontinuity
ties and 13 tympanomastoidectomies), and the group, there was no significant change in any VEMP
severe granulation group comprised 10 patients parameter after paper patching (Table IV).
VEMPs according to middle ear conditions in COM 37

Figure 1. The pure-tone audiograms and vestibular evoked myogenic potentials (VEMPs) of a participant with right-sided tympanic
membrane perforation with, chronic otitis media (COM) before paper patching (A, B) and after paper patching (C, D). O, X, right, left,
air conduction level; D, right air conduction level with masking; [, right bone conduction level.

Discussion method in cases of sudden sensorineural hearing


loss was 100%, implying that an absence of VEMP
Many factors can affect the VEMP, including age, by the tone burst method was caused by CHL, but not
stimuli, laterality, middle ear status, and muscle ten- by sensorineural hearing loss [6]. A typical sound-
sion [4]. Halmagyi et al. reported that VEMP induced VEMP response requires good energy trans-
responses are typically absent in cases of CHL with fer to the inner ear, meaning that an intact middle ear
an ABG of greater than 20 dB [5]. Before paper is necessary. Many alternative methods of overcoming
patching, the mean ABG of 50 affected ears of our CHL, such as the tapping method or the use of bone-
patients with COM was 24.6 ± 10.9 dB. As the paper conduction stimuli, have been reported [2,7–10].
patch significantly attenuated the ABG, a VEMP Wang and Lee collected VEMP responses in patients
response was elicited in up to 86%, which was with middle ear effusion (MEE) and compared the
increased from 64%, assuming less than 15 mV of responses with those of both healthy controls and the
p13-n23 interlatency as absence of VEMP. The same participants after tympanic aspiration to clarify
VEMP response rate obtained by the tone burst the effects of MEE on VEMP responses [3]. They
38 J. S. Lee et al.

Table II. Difference in pure-tone audiometry and vestibular evoked myogenic potential testing by paper patching according to the size of the
tympanic membrane perforation.
Perforation size Characteristic COM patients COM patients p Value between
before patching after patching pre- and post-patch

< 50% (n = 22) ABG average (dB) 24.6 ± 11.5 21.9 ± 11.4 0.007*
ABG at 500 Hz (dB) 27.7 ± 15.8 25.0 ± 15.1 0.158
VEMP
p13 latency (ms) 21.2 ± 4.5 19.7 ± 5.9 0.641
n23 latency (ms) 27.8 ± 3.7 27.1 ± 6.6 0.351
VAR (%) 35.2 ± 25.5 31.5 ± 17.9 0.079
‡ 50% (n = 28) ABG average (dB) 28.5 ± 11.0 20.6 ± 10.3 0.000*
ABG at 500 Hz (dB) 40.4 ± 15.6 28.9 ± 15.7 0.000*
VEMP
p13 latency (ms) 22.9 ± 5.5 19.5 ± 4.6 0.071
n23 latency (ms) 27.6 ± 6.4 27.7 ± 4.8 0.371
VAR (%) 37.2 ± 18.9 31.7 ± 16.7 0.063
ABG, air–bone gap; AC, air conduction; BC, bone conduction; COM, chronic otitis media; VAR, VEMP asymmetric ratio; VEMP, vestibular
evoked myogenic potential.
*p < 0.05.

reported that the VEMP asymmetry ratio was signif- variable conditions, such as ossicle chain status, mid-
icantly decreased, and the latencies of p13 and dle ear mucosa condition, and the size of the eardrum
n23 returned to the range of control participants perforation intraoperatively, which could affect sound
immediately after tympanic aspiration. We suspect energy transmission. In cases with an intact ossicular
that the paper patch helps sound energy transfer to chain, the p13 latency of 21.3 ± 6.1 ms was signifi-
the inner ear. In the present study, the latency of cantly decreased to 17.3 ± 5.6 ms after paper patch-
p13 and n23 had a tendency of mild delay, which was ing, whereas no significant change was observed in
not seen in other studies. We thought that the reason ossicular chain discontinuity. According to the con-
for this discrepancy was probably due to differences in dition of the middle ear mucosa, the p13 latency and
sound stimuli. We used a 90 dB, 500 Hz short tone the VAR showed significant changes only in patients
burst sound instead of the 95 dB sound used in other with clean mucosa by paper patching. There were no
studies. Commonly, VEMP stimulation is by a significant changes in p13, n23 latency or the VAR in
500 Hz, 90 dB nHL, or 95 dB nHL short tone burst. patients with any degree of middle ear granulation.
Our laboratory data were relatively stable and consis- There were also no significant changes of latency or
tent when the stimulus was 90 dB nHL. The VAR by paper patching regardless of the TM perfo-
p13 latency and p13-n23 interamplitude of the ration size. Therefore, we can assume that the influ-
COM group were significantly different from those ence of the ossicle and middle ear mucosa status on
of the control group. After paper patching, the sound transmission might be important for eliciting
p13 latency delay was significantly decreased and VEMP response. Because any degree of ossicular
the p13-n23 interamplitude significantly increased. chain discontinuity in patients with COM may
The ABG also decreased after paper patching. Based directly interfere with air conduction, less acoustic
on the significant shortening of p13 latency after paper energy is transmitted into the inner ear when using air
patching, a decrease in energy transfer to the middle conduction acoustic stimulation. The p13 latency was
ear seemed to be the major cause of the delay in significantly shortened in the intact ossicular chain
VEMP latencies in patients with COM. However, group after paper patching; based upon this result, we
the n23 latency showed no difference between con- assumed that it was mainly affected by the velocity of
trols and patients with COM, and the reason for this acoustic energy transmission rather than the ampli-
was unclear. Based on these results, we can partially tude. There were no changes in VEMP parameters in
predict the presence or absence of the VEMP patients with ossicular discontinuity after paper patch-
response on an audiogram according to the ABG. ing. In COM patients with middle ear granulation, no
We subdivided the patient groups according to parameters changed. This finding indicates that
VEMPs according to middle ear conditions in COM 39

Table III. Difference in pure tone audiometry and vestibular evoked myogenic potential by patching according to the middle ear mucosal
status.
Middle ear mucosa status Characteristic COM patients COM patients p Value between
before patching after patching pre- and post-patch

Normal (n = 20) ABG average (dB) 26.1 ± 10.8 17.0 ± 10.2 0.001*
ABG at 500 Hz (dB) 31.0 ± 14.5 27.5 ± 16.7 0.045*
VEMP
p13 latency (ms) 21.3 ± 3.5 18.7 ± 7.1 0.043*
n23 latency (ms) 26.7 ± 6.3 27.8 ± 6.6 0.948
VAR (%) 28.8 ± 4.6 19.1 ± 5.9 0.012*
Moderate pathologic ABG average (dB) 24.1 ± 11.4 21.8 ± 11.0 0.012*
state (n = 20) ABG at 500 Hz (dB) 31.5 ± 16.7 22.5 ± 14.4 0.001*
VEMP
p13 latency (ms) 21.9 ± 5.3 19.9 ± 3.2 0.307
n23 latency (ms) 27.9 ± 6.4 25.5 ± 5.1 0.479
VAR (%) 35.8 ± 38.3 32.9 ± 22.5 0.061
Severe pathologic AB gap average (dB) 33.3 ± 10.4 28.3 ± 7.5 0.111
state (n = 10)
ABG at 500 Hz (dB) 49.0 ± 14.7 36.0 ± 11.3 0.111
VEMP
p13 latency (ms) 23.3 ± 4.1 22.5 ± 3.0 0.101
n23 latency (ms) 29.2 ± 4.1 28.4 ± 4.1 0.331
VAR (%) 45.7 ± 28.8 45.1 ± 34.3 0.274
ABG, air–bone gap; AC, air conduction; BC, bone conduction; COM, chronic otitis media; VAR, VEMP asymmetric ratio; VEMP, vestibular
evoked myogenic potential.
*p < 0.05.

Table IV. Difference in pure tone audiometry and vestibular evoked myogenic potential by patching according to the state of the ossicular
chain.
Ossicle state Characteristic COM patients COM patients p Value between
before patching after patching pre and post-patch

Intact ossicular ABG average (dB) 24.6 ± 12.8 18.1 ± 14.5 0.001†
chain (n = 22)
ABG at 500 Hz (dB) 27.1 ± 6.4 18.3 ± 8.1 0.001†
VEMP
p13 latency (ms) 21.3 ± 6.1 17.3 ± 5.6 0.028†
n23 latency (ms) 27.7 ± 6.4 25.4 ± 6.2 0.157
VAR (%) 35.4 ± 27.8 29.3 ± 24.8* 0.068
Ossicular ABG average (dB) 28.3 ± 22.1 24.1 ± 20.02 0.102
discontinuity (n = 28) ABG at 500 Hz (dB) 36.9 ± 21.8 34.1 ± 17.9 0.381
VEMP
p13 latency (ms) 22.2 ± 3.6 21.6 ± 3.3 0.116
n23 latency (ms) 29.1 ± 2.8 28.1 ± 4.8 0.307
VAR (%) 36.9 ± 22.1 33.9 ± 20.1 0.179
ABG, air–bone gap; AC, air conduction; BC, bone conduction; COM, chronic otitis media; VAR, VEMP asymmetric ratio; VEMP, vestibular
evoked myogenic potential.
*Difference from normative data of normal controls with p < 0.05; †p < 0.05.
40 J. S. Lee et al.

granulation tissue may absorb some sound energy, we suggest that VEMP reflects middle ear conditions,
and in the presence of granulation tissue, the para- and thus VEMP could be an informative tool to
meters of VEMP were not changed following paper identify middle ear conditions preoperatively.
patching. Acoustic energy impinged on a perforated
TM, and the reduced transforming action attenuated
the stimulated sound, leading to absent VEMPs. The Acknowledgment
rates of p13 and n23 latency and VAR of COM
patients were in normal ranges (average ± 2 SD): This research was supported by the Kyung Hee
16%, 24%, and 8%, respectively. After paper patch- University Research Fund in 2010 (KHU-20100740).
ing, however, these rates increased to 27%, 43%, and
16% when the ipsilateral COM side was compared Declaration of interest: The authors report no
with same side in the control group. conflicts of interest. The authors alone are responsible
These findings indicate that paper patching rein- for the content and writing of the paper.
forced some portion of the attenuated acoustic
energy. Therefore, we should be aware that the effects
of middle ear conditions, such as the status of the References
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