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Magnetic resonance imaging-detected inner ear

hemorrhage as a potential cause of sudden


sensorineural hearing loss
Xuan Wu, PhD
a, 1
, Kaitian Chen, PhD
a, 1
, Liang Sun, MS
a
, Zhiyun Yang, PhD
b
,
Yuanping Zhu, MD
a
, Hongyan Jiang, MD, PhD
a,

a
Department of Otorhinolaryngology, The First Affiliated Hospital, Sun Yat-sen University and Institute of Otorhinolaryngology,
Sun Yat-sen University, Guangzhou, PR China
b
Department of Radiology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, PR China
A R T I C L E I N F O A B S T R A C T
Article history:
Received 25 November 2013
Purpose: The aim of this study is to assess the value of magnetic resonance imaging in
identifying the etiology of sudden sensorineural hearing loss, and to correlate the high signals
in the labyrinth with clinical features to identify if inner ear hemorrhage could be implicated.
Materials and methods: In this retrospective study, inner ear magnetic resonance imaging
was given to 112 patients with sudden sensorineural hearing loss in the First Affiliated
Hospital of Sun Yat-sen University from 2011 to 2012. The clinical features of patients with
high signals in the labyrinth on magnetic resonance imaging were analyzed.
Results: Abnormal magnetic resonance images were identified in 13 (11.6%) patients.
Retrocochlear pathology was found in six patients, including two cases of lacunar
infarction, one case of multiple ischemias in the brainstem and bilateral centrum
semiovale, two cases of acoustic neuroma, and one case of inner ear hemangioma. There
were seven cases showing high signals in the labyrinth on unenhanced T1-weighted and
fluid-attenuated inversion recovery images. Clinical features of these seven patients were
characterized by irreversible profound hearing impairment and vestibular dysfunction.
These findings were consistent with the hypothesis that their symptoms were caused by
an inner ear hemorrhage.
Conclusion: The results indicate the importance of magnetic resonance imaging in sudden
sensorineural hearing loss in patients. Moreover, patients with vestibular dysfunction and
sudden profound hearing loss may have an inner ear hemorrhage evident by interpreting
clinical and magnetic resonance imaging results.
2014 Elsevier Inc. All rights reserved.
1. Introduction
Sudden sensorineural hearing loss (SSNHL) is typically
defined as >30 dB sensorineural hearing loss in at least
three frequencies occurring over a span of less than
72 hours [1]. Despite efforts to clarify the pathophysiologic
characteristics of this condition, the exact cause of SSNHL
remains unclear. It is estimated that approximately 90% of
A M E R I C A N J O U R N A L O F O T O L A R Y N G O L O G Y H E A D A N D N E C K M E D I C I N E A N D S U R G E R Y 3 5 ( 2 0 1 4 ) 3 1 8 3 2 3
Corresponding author at: Department of Otorhinolaryngology, The First Affiliated Hospital, Sun Yat-sen University and Institute of
Otorhinolaryngology, Sun Yat-sen University, Guangzhou, 510080, PR China. Tel./fax: +86 20 87333733.
E-mail address: hyjiangwu@163.com (H. Jiang).
1
These authors contributed equally to the study.
0196-0709/$ see front matter 2014 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.amjoto.2014.02.004
Avai l abl e onl i ne at www. sci encedi r ect . com
ScienceDirect
www. el sevi er . com/ l ocat e/ amj ot o
SSNHL cases are idiopathic [1]. Possible causes include viral
infection, microcirculatory disturbance of the inner ear, and
immune factors. The unpredictability of idiopathic SSNHL
presents a challenge to preventive care and thus etiological
research investigating SSNHL is required.
Imaging studies are frequently utilized for the evaluation
of SSNHL in patients. Magnetic resonance imaging (MRI) has
the added advantage of identifying other causes of SSNHL (eg,
cochlear inflammation or multiple sclerosis) or findings that
imply an underlying etiology for the SSNHL (eg, small vessel
cerebral ischemia), compared to other imaging techniques.
According to the guidelines by the American Academy of
Otolaryngology-Head and Neck Surgery (AAO-HNS) Founda-
tion, it is recommended that patients with SSNHL undergo
audiometry and MRI scans of the middle and inner ear [1].
In 1992, Weissman et al. described two patients with high
signals in the labyrinth on unenhanced T1-weighted MRI who
presented with SSNHL and vertigo [2]. They suggested the
possibility that the high signal was caused by hemorrhage.
Subsequently, a fewreports of high signals on the labyrinthon
unenhanced T1-weighted image (T1WI) have been presented
to support this hypothesis [35]; however, pathological
verification has not yet been obtained.
In this retrospective study, we evaluate the MRI findings of
112 patients with SSNHL in the First Affiliated Hospital of Sun
Yat-sen University from January 2011 to December 2012. The
goal of our study is to add our experience to the current body
of data regarding the importance of routine MRI for SSNHL and
the possibility of inner ear hemorrhage, not to provide a new
standard of examination for SSNHL. Nevertheless, the rela-
tively high positive rate of MRI findings and strong evidence of
inner ear hemorrhage by MRI and clinical features reiterate
the necessity for this examination. Therefore, the role of inner
ear hemorrhage in the etiology of SSNHL should be investi-
gated further.
2. Methods and patients
The study was approved by the institutional review board of
the First Affiliated Hospital, Sun Yat-sen University. We
retrospectively analyzed the MRI findings and relevant
audiometric results of 112 patients with SSNHL in the First
Affiliated Hospital of Sun Yat-sen University from January
2011 to December 2012. Patients underwent pure-tone audi-
ometry (PTA) or auditory brainstem response (ABR) and
auditory steady state response (ASSR). Patient inclusion was
contingent upon their fulfillment of the criteria, based on the
AAO-HNS guideline definition of sudden hearing loss [1].
MRI was conducted using a 3.0-Tesla superconducting
magnet system (Siemens Magnetom TrioTim, Munich, Ger-
many) with a phased-array head coil. The scanning encom-
passed the regionfromthe mastoidale to the upper edge of the
petrous bone. The protocol consisted of axial 23 mmthick T1
(repetition time [TR] 600 ms, echo time [TE] 14 ms) and T2 (TR
2500 ms, TE 80120 ms) weighted sequences. After a 0.5-mm
thick three-dimensional turbo spin echo (3D-TSE; TR 1000 ms,
TE 132 ms) survey, 1-mm thick reconstructions of axial,
coronal, and acoustic sagittal images were performed. Pa-
tients were additionally examined with a 2-mm thick T2-
weighted imaging (T2WI) three-dimensional fluid-attenuated
inversion recovery (FLAIR) sequence before contrast injection.
In addition, T1-weighted three-dimensional volumetric inter-
polated breath-hold examination (3D-VIBE) was repeated after
gadolinium-diethylenetriaminepentaacetate (Gd-DTPA) con-
trast enhancement in some patients.
PTA average thresholds in the conversational frequencies
(0.5, 1, 2, and 4 kHz) were calculated and used to define the
severity of deafness as mild (2650 dB), moderate (5070 dB),
severe (7090 dB), profound (90119 dB), or anacusis (>120 dB).
Response to therapy was categorized according to the Siegel
criteria as follows [6]:
(1) Healing: final threshold more than 25 dB.
(2) Partial improvement: gain of more than 15 dB, final
hearing threshold 2545 dB.
(3) Slight improvement: gain of more than 15 dB, final
hearing threshold more than 45 dB.
(4) No response: gain of less than 15 dB and final hearing
threshold more than 75 dB.
Both Healing and Partial improvement were considered
effective.
3. Results
In total, 112 patients (65 males and 47 females, mean age
47.6 years, ranging from 6 to 78 years) were eligible for
inclusion in the study. The history of hearing loss ranged
from 1 to 16 days, with a mean of 9.3 3.8 days. All patients
were subdivided into four categories on the basis of hearing
levels: five patients with mild hearing loss, 43 with moderate
loss, 30 withsevere loss, and34 withprofoundloss or anacusis.
MRI identified auditory pathway pathology in 13 SSNHL
patients (11.6%, Table 1). The pathology was located in the
brain, internal auditory canal (IAC), and inner ear. More
precisely, three patients suffered fromcentral nervous system
diseases, such as temporal occipital junctional lacunar
infarction. Acoustic neuroma, rarely occurring in SSNHL
patients, was identified in two patients (1.79%, Fig. 1) and
confirmed to be the cause of SSNHL. Conservative treatment
Table 1 Summary of MRI findings in 112 patients with
SSNHL.
Location Abnormality No. Percentage Responsible
for SSNHL
Brain Lacunar infarction 2 1.79% Possible
Multiple ischemias
in the brainstem
and centrum
semiovale
1 0.89% Possible
IAC Acoustic neuroma 2 1.79% Yes
IAC hemangioma 1 0.89% Yes
Inner ear Possibility of inner
ear hemorrhage
7 6.25% Probably
Abbreviations: IAC, internal auditory canal; MRI, magnetic
resonance imaging; SSNHL, sudden sensorineural hearing loss.
319 A M E R I C A N J O U R N A L O F O T O L A R Y N G O L O G Y H E A D A N D N E C K M E D I C I N E A N D S U R G E R Y 3 5 ( 2 0 1 4 ) 3 1 8 3 2 3
and follow-up were prescribed to these two patients. Internal
auditory canal hemangioma was detected in one young
woman (Fig. 2). Therefore, retrocochlear pathology was
found in 5.4% SSNHL patients.
Seven cases (6.2%) showed high signal in the labyrinth in
unenhanced T1-weighted and 3DFLAIR images, indicating the
possibility of inner ear hemorrhage. The detailed MRI
characteristics were as follows:
(1) Abnormal signal intensity in the affected inner ear of
varying locations: the cochlea, semicircular canals, or
vestibule (Fig. 3, Table 2).
(2) High signal intensity observed on unenhanced T1WI in
the affected ear but not on the healthy side.
(3) Abnormal inner ear high signal could not be inhibited in
3D FLAIR images compared to the unaffected ear.
(4) All patients displayed high/medial signal on T2WI in
both the affected and unaffected ear.
(5) Gd-enhancement was negative in all cases. The pres-
ence of high intensity signal on T1WI and in 3D FLAIR
images was potentially consistent with intracochlear
hemorrhage [7].
These seven patients (5 males and 2 females) ranged from
11 to 60 years of age (mean: 27.3 years). Their history of
hearing loss was 3 to 10 days. One of these cases was caused
by anticoagulants (patient 3) while the others were idiopathic.
The period fromonset to MRI examination was between 8 and
18 days. Otoacoustic emission examinations and ABR were
abnormal in the affected ear. In summary, these patients were
characterized by severe labyrinthine symptoms including
profound to anacusis deafness and vestibular involvement
(vertigo, nausea, and/or vomiting). These clinical features
correlated with the MRI findings (Table 2), which strongly
supports the hypothesis that cochleovestibular dysfunction
was caused by the pathology in the affected inner ear, most
likely due to inner ear hemorrhage. Besides, the rate of
vestibular symptom (dizziness/vertigo) was 21.0% (22/105)
among 105 patients without MRI characteristics of
hemorrhage.
In the present study, all 112 patients received treatments
including oral corticosteroids (Methylprednisolone 48 mg/
day, full dose for 7 to 14 days, then taper over similar time
period) and/or hyperbaric oxygen therapy for two weeks [1],
Fig. 2 Unenhanced T1WI, T2WI, and enhanced T1WI
(arrow) demonstrate a low and high signal intensity mass in
the right IAC in one SSNHL patient. The mass was suspected
to be a hemangioma. IAC: internal auditory canal.
Fig. 3 High signal intensity was observed in the left cochlea
and vestibule on unenhanced T1WI (A) and 3D-FLAIR axial
images (B). Co: cochlea, Ve: vestibule.
Fig. 1 MRI identified acoustic neuroma in one patient on the
ipsilateral side. T1WI (A) and T2WI (B) show an isointensity
mass in the left IAC (arrow). Gd-Enhancement was seen
postcontrast (C). IAC: internal auditory canal.
320 A M E R I C A N J O U R N A L O F O T O L A R Y N G O L O G Y H E A D A N D N E C K M E D I C I N E A N D S U R G E R Y 3 5 ( 2 0 1 4 ) 3 1 8 3 2 3
with an average effective rate of 46%. The prognoses of these
seven patients with possible inner ear hemorrhage were
poorer than expected, as none showed any response to
therapy. Among the other 27 patients with profound deafness
or anacusis, 37% (10/27) had effective results. In the seven
patients with suspected inner ear hemorrhage effective
results were not obtained (Fig. 4); however, the accompanying
symptoms, such as vertigo and tinnitus in these patients with
inner ear hemorrhage, were alleviated. Patient 5 with bilateral
deafness attained satisfactory hearing 6 months later follow-
ing cochlear implantation in the left ear.
4. Discussion
The present study evaluated the value for MRI to diagnose
SSNHL and addressed the importance of this examination for
elucidating SSNHL etiology. Routine MRI may identify 11.2%of
the pathologic changes in the audiovestibular tract, a result
that is consistent with previous reports (from 7% to 13.75%)
[5,811]. Moreover, patients with SSNHL loss may have a 6.25%
chance of inner ear hemorrhage detectable by interpreting
clinical and MRI results.
Many findings indicate the importance of complete MRI
screenings of the audiovestibular tract in SSNHL patients. For
example, intracranial abnormalities believed to be responsible
for sensorineural hearing loss were found in 19.2% patients
[12]. The two case series' by Aarnisalo and Cadoni found MRI
abnormalities in 44%of SSNHL cases [11,13]. Furthermore, MRI
of the temporal bone, cerebellopontine angle, and brain
showed abnormal results in 24 of 78 patients (31%) with
SSNHL [10]. Ina smaller series of 16 patients withSSNHL, three
patients (18.8%) had a significant pathologic condition iden-
tified on MRI [14]. Our series of 13 abnormalities (11.6%) in 112
patients supports the hypothesis that a significant number of
pathologic conditions can be detected by MRI.
Additionally, failure to identify lesions, such as acoustic
neuroma, could have detrimental consequences for patients.
For instance, Chaimoff's study reported a far higher rate of
acoustic neuroma in SSNHL patients (48%) [15] than the 14%to
19% rate previously documented in a retrospective series of
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Fig. 4 Poor therapy results in SSNHL patients with profound
deafness to anacusis. Patients with possible inner ear
hemorrhage showed no response to therapy.
321 A M E R I C A N J O U R N A L O F O T O L A R Y N G O L O G Y H E A D A N D N E C K M E D I C I N E A N D S U R G E R Y 3 5 ( 2 0 1 4 ) 3 1 8 3 2 3
acoustic neuroma patients [16]. The present study identified a
lower rate of acoustic neuroma (1.79%); however, we validated
the significance of MRI for diagnosing the cause of SSNHL.
Thus, we recommend the use of MRI for the diagnostic
evaluation of SSNHL patients.
We identified seven patients showing a high signal in the
labyrinth on unenhanced T1-weighted and FLAIR images. The
possibility of false-positive results may be ruled out since our
results and those from a previous study [7] never identified a
contralateral alteration and/or a hyper-signal in the control
group. Weissman et al. stated that the presence of fat,
decreased blood flow, high protein concentration, or prior
hemorrhage generates hyperintense T1 images [2]. Fat is not
found in the labyrinth and is an extremely unlikely cause of
high signal in this location. The high signal was not replaced
in FLAIR images in our seven patients, confirming an increase
in inner ear proteins or prior hemorrhage, rather than
lymphatic fluid.
3D FLAIR hyperintensity indicates the modification of the
inner ear protein composition that can be ascribed to a minor
hemorrhage or to an acute inflammatory process [11]. In this
cohort, the delay from onset to MRI exam is between 8 and
18 days (average 15.3 days). This time period does not support
acute inflammation as a potential cause of this characteristic.
Therefore, the presence of a high intensity signal on T1WI,
owing to the presence of intracellular and extracellular
methemoglobin, and in 3D FLAIR images, owing to the
increased protein content in the membranous fluid secondary
to the presence of methemoglobin, implicates intracochlear
hemorrhage [7].
In the work Pathology of the ear, Schuknecht states that
inner ear hemorrhage can cause sudden hearing loss and
vertigo [17]. He also states that spontaneous hemorrhage into
the inner ear mainly occurs as a complication of bleeding
disorders, the most common being leukemia. Schuknecht
confirmed this from histological studies of the temporal bone
in patients who died just after the onset of ear symptoms [17].
In our cohort, patient 3 (Table 2) continued to take warfarin
since undergoing an aortic valve replacement 2 years before-
hand. The clotting test in this patient showed an obvious
hemorrhagic tendency: a prothrombin time of 43.6 seconds
and activated partial thromboplastin time of 46.7 seconds.
The hypothesis regarding the cause of inner ear hemorrhage
in the rest six patients may be presumed to be angiopsathyro-
sis, vascular malformation or stress response etc.
An inner ear hemorrhage diagnosis may be made using the
interpretation of clinical features combined with MRI in this
study based on the following observations: first, one of our
patients had anticoagulant prescription history before SSNHL,
while the other six patients were free of any other etiology.
Second, the labyrinthine symptoms were well correlated with
the MRI results (cochlea, semicircular canals, or vestibule
involvement). Third, abnormally high MRI signals were only
seen in the affected side compared to the contralateral side.
Furthermore, high intensity on unenhanced T1WI and 3D
FLAIR without postcontrast enhancement might help exclude
patterns consistent with an inflammatory process or break-
down of the blood labyrinth barrier [7].
The prognosis of patients with high signals onunenhanced
T1WI and 3D FLAIR in this study and other reports is
consistently poor. None of the seven of our patients showed
any response to therapy except for alleviation of vertigo or
tinnitus. Yoshida et al. showed that high signals in the cochlea
onprecontrast 3DFLAIRare relatedtoa poor hearing prognosis
[18]. Ryuet al. evaluatedtwelve patients whose initial andfinal
hearing levels were 98.0 31.1 dB and 87.7 33.1 dB, respec-
tively. They statedthat highsignals inthe affectedinner ear on
3D FLAIR closely correlate with vestibular dysfunction and
poor hearing recovery in patients with SSNHL [19]. Lee et al.
concluded that the absence of high-intensity signal on 3D
FLAIR MRI can possibly imply a relative good prognosis [20]. In
fact, simple hemorrhage into the perilymphatic space in small
amounts is reportedly well tolerated; massive hemorrhage,
however, has not been followed up long enough in reported
cases and series. In principle, hemorrhage by itself may have a
different outcome from hemorrhagic transformation of an
ischemic process. Although left inner ear hyperintensity
disappeared in patient 4 (Table 2) during a second MRI exam
3 months later, none of these seven patients recovered
hearing at a 6-month follow-up.
This study has certain limitations. Since biopsies are
completed forbidden in a study of this nature, the definitive
diagnosis of an inner ear hemorrhage could not be made.
Perhaps more advanced technology or post-mortem patho-
logic findings may facilitate further research. Long term
follow-up and a larger number of patients in a clinical trial
would also favor the hypothesis presented in this study.
5. Conclusion
The results of this study emphasize the importance of MRI
in SSNHL patients. Moreover, patients with vestibular
dysfunction and sudden profound hearing loss may have
an inner ear hemorrhage detectable by interpretation of
clinical and MRI results.
Conflict of interests
None.
Acknowledgments
The authors thank all participants in this study. The authors
also thank Wenting Zou for her great technical assistance in
radiology. The study was supported by grants from the
National Basic Research Program of China (2011CB504502),
the National Natural Science Fund of China (30973306) and the
key nature fund of Guangdong Province (8251008901000016).
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