sensorineural hearin

Xuan Wu, PhDa, 1, Kaitian ChYuanping Zhu, MDa, Hongyaa Department of Otorhinolaryngology, The FirSun Yat-sen University, Guangzhou, PR Chinab Department of Radiology, The First Affiliated

A R T I C L E I N F O

Article history:Received 25 November 2013

Results: Abnormal magnetic resonance images were identified in 13 (11.6%) patients.

infarction, one case of multiple ischemias in the brainstem and bilateral centrum

sensorineural hearing loss in patients. Moreover, patients with vestibular dysfunction andvident by interpreting

nc. All rights reserved.

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

Ava i l ab l e on l i ne a t www.sc i enced i r ec t . com

ScienceDirectom1. Introduction

Sudden sensorineural hearing loss (SSNHL) is typically

three frequencies occurring over a span of less than72 hours [1]. Despite efforts to clarify the pathophysiologiccharacteristics of this condition, the exact cause of SSNHLsudden profound hearing loss may have an inner ear hemorrhage eclinical and magnetic resonance imaging results.

2014 Elsevier Isemiovale, two cases of acoustic neuroma, and one case of inner ear hemangioma. Therewere seven cases showing high signals in the labyrinth on unenhanced T1-weighted andfluid-attenuated inversion recovery images. Clinical features of these seven patients werecharacterized by irreversible profound hearing impairment and vestibular dysfunction.These findings were consistent with the hypothesis that their symptoms were caused byan inner ear hemorrhage.Conclusion: The results indicate the importance of magnetic resonance imaging in suddendefined as >30 dB sensorineural hearin

Corresponding author at: Department of OOtorhinolaryngology, Sun Yat-sen University

E-mail address: hyjiangwu@163.com (H. J1 These authors contributed equally to the

0196-0709/$ see front matter 2014 Elsevhttp://dx.doi.org/10.1016/j.amjoto.2014.02.00Retrocochlear pathology was found in six patients, including two cases of lacunarential cause of suddeng loss

en, PhDa, 1, Liang Sun, MSa, Zhiyun Yang, PhDb,n Jiang, MD, PhDa,

st Affiliated Hospital, Sun Yat-sen University and Institute of Otorhinolaryngology,

Hospital, Sun Yat-sen University, Guangzhou, PR China

A B S T R A C T

Purpose: The aim of this study is to assess the value of magnetic resonance imaging inidentifying the etiology of sudden sensorineural hearing loss, and to correlate the high signalsin 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 imagingwas given to 112 patients with sudden sensorineural hearing loss in the First AffiliatedHospital of Sun Yat-sen University from 2011 to 2012. The clinical features of patients withhigh signals in the labyrinth on magnetic resonance imaging were analyzed.hemorrhage as a pot

Magnetic resonance imaging-detected inner earwww.e l sev i e r . cg loss in at least

torhinolaryngology, The, Guangzhou, 510080, PRiang).study.

ier Inc. All rights reserve4/ l oca te /amjo toremains unclear. It is estimated that approximately 90% of

First Affiliated Hospital, Sun Yat-sen University and Institute ofChina. Tel./fax: +86 20 87333733.

d.

to support this hypothesis [35]; however, pathological

eighted imaging (T2WI) three-dimensional fluid-attenuatedversion recovery (FLAIR) sequence before contrast injection.addition, T1-weighted three-dimensional volumetric inter-

olated breath-hold examination (3D-VIBE)was repeated afteradolinium-diethylenetriaminepentaacetate (Gd-DTPA) con-ast enhancement in some patients.PTA average thresholds in the conversational frequencies

.5, 1, 2, and 4 kHz) were calculated and used to define theeverity of deafness as mild (2650 dB), moderate (5070 dB),evere (7090 dB), profound (90119 dB), or anacusis (>120 dB).esponse to therapy was categorized according to the Siegelriteria as follows [6]:

(1) Healing: final threshold more than 25 dB.(2) Partial improvement: gain of more than 15 dB, final

levels: five patients with mild hearing loss, 43 with moderateloss, 30with severe loss, and34withprofound loss or anacusis.

319N 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 3verification 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 SunYat-sen University from January 2011 to December 2012. Thegoal of our study is to add our experience to the current bodyof data regarding the importance of routineMRI for SSNHL andthe possibility of inner ear hemorrhage, not to provide a newstandard of examination for SSNHL. Nevertheless, the rela-tively high positive rate of MRI findings and strong evidence ofinner ear hemorrhage by MRI and clinical features reiteratethe necessity for this examination. Therefore, the role of innerear hemorrhage in the etiology of SSNHL should be investi-gated further.

2. Methods and patients

The study was approved by the institutional review board ofthe First Affiliated Hospital, Sun Yat-sen University. Weretrospectively analyzed the MRI findings and relevantaudiometric results of 112 patients with SSNHL in the FirstAffiliated Hospital of Sun Yat-sen University from January2011 to December 2012. Patients underwent pure-tone audi-ometry (PTA) or auditory brainstem response (ABR) andauditory steady state response (ASSR). Patient inclusion wascontingent upon their fulfillment of the criteria, based on theAAO-HNS guideline definition of sudden hearing loss [1].

MRI was conducted using a 3.0-Tesla superconductingmagnet system (Siemens Magnetom TrioTim, Munich, Ger-many) with a phased-array head coil. The scanning encom-passed the region from themastoidale to the upper edge of thepetrous bone. The protocol consisted of axial 23 mm thick T1(repetition time [TR] 600 ms, echo time [TE] 14 ms) and T2 (TR2500 ms, TE 80120 ms) weighted sequences. After a 0.5-mmthick three-dimensional turbo spin echo (3D-TSE; TR 1000 ms,TE 132 ms) survey, 1-mm thick reconstructions of axial,SSNHL cases are idiopathic [1]. Possible causes include viralinfection, microcirculatory disturbance of the inner ear, andimmune factors. The unpredictability of idiopathic SSNHLpresents a challenge to preventive care and thus etiologicalresearch investigating SSNHL is required.

Imaging studies are frequently utilized for the evaluationof SSNHL in patients. Magnetic resonance imaging (MRI) hasthe added advantage of identifying other causes of SSNHL (eg,cochlear inflammation or multiple sclerosis) or findings thatimply an underlying etiology for the SSNHL (eg, small vesselcerebral ischemia), compared to other imaging techniques.According to the guidelines by the American Academy ofOtolaryngology-Head and Neck Surgery (AAO-HNS) Founda-tion, it is recommended that patients with SSNHL undergoaudiometry and MRI scans of the middle and inner ear [1].

In 1992, Weissman et al. described two patients with highsignals in the labyrinth on unenhanced T1-weighted MRI whopresented with SSNHL and vertigo [2]. They suggested thepossibility that the high signal was caused by hemorrhage.Subsequently, a few reports of high signals on the labyrinth onunenhanced T1-weighted image (T1WI) have been presented

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 Acoronal, and acoustic sagittal images were performed. Pa-tients were additionally examined with a 2-mm thick T2-MRI identified auditory pathway pathology in 13 SSNHLpatients (11.6%, Table 1). The pathology was located in thebrain, internal auditory canal (IAC), and inner ear. Moreprecisely, three patients suffered from central nervous systemdiseases, such as temporal occipital junctional lacunarinfarction. Acoustic neuroma, rarely occurring in SSNHLpatients, was identified in two patients (1.79%, Fig. 1) andconfirmed to be the cause of SSNHL. Conservative treatment

Table 1 Summary of MRI findings in 112 patients withSSNHL.

Location Abnormality No. Percentage Responsiblefor SSNHL

Brain Lacunar infarction 2 1.79% PossibleMultiple ischemiasin the brainstemand centrumsemiovale

1 0.89% Possible

IAC Acoustic neuroma 2 1.79% YesIAC hemangioma 1 0.89% Yes

Inner ear Possibility of innerear hemorrhage

7 6.25% Probablyhearing 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 improvementwere consideredeffective.

3. Results

In total, 112 patients (65 males and 47 females, mean age47.6 years, ranging from 6 to 78 years) were eligible forinclusion in the study. The history of hearing loss rangedfrom 1 to 16 days, with a mean of 9.3 3.8 days. All patientswere subdivided into four categories on the basis of hearingwinInpgtr

(0ssRcAbbreviations: IAC, internal auditory canal; MRI, magneticresonance imaging; SSNHL, sudden sensorineural hearing loss.

possibility of inner ear hemorrhage. The detailed MRIcharacteristics were as follows:

(1) Abnormal signal intensity in the affected inner ear ofvarying locations: the cochlea, semicircular canals, orvestibule (Fig. 3, Table 2).

(2) High signal intensity observed on unenhanced T1WI inthe affected ear but not on the healthy side.

(3) Abnormal inner ear high signal could not be inhibited in3D FLAIR images compared to the unaffected ear.

(4) All patients displayed high/medial signal on T2WI inboth 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 FLAIRimages was potentially consistent with intracochlearhemorrhage [7].

These seven patients (5 males and 2 females) ranged from11 to 60 years of age (mean: 27.3 years). Their history of

Fig. 1 MRI identified acoustic neuroma in one patient on theipsilateral side. T1WI (A) and T2WI (B) show an isointensitymass in the left IAC (arrow). Gd-Enhancement was seen

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 3and follow-up were prescribed to these two patients. Internalauditory canal hemangioma was detected in one youngwoman (Fig. 2). Therefore, retrocochlear pathology wasfound in 5.4% SSNHL patients.

postcontrast (C). IAC: internal auditory canal.Seven cases (6.2%) showed high signal in the labyrinth inunenhanced T1-weighted and 3D FLAIR images, indicating the

Fig. 2 Unenhanced T1WI, T2WI, and enhanced T1WI(arrow) demonstrate a low and high signal intensity mass inthe right IAC in one SSNHL patient. The mass was suspectedto be a hemangioma. IAC: internal auditory canal.hearing loss was 3 to 10 days. One of these cases was causedby anticoagulants (patient 3) while the others were idiopathic.The period from onset to MRI examination was between 8 and18 days. Otoacoustic emission examinations and ABR wereabnormal in the affected ear. In summary, these patients werecharacterized by severe labyrinthine symptoms includingprofound to anacusis deafness and vestibular involvement(vertigo, nausea, and/or vomiting). These clinical featurescorrelated with the MRI findings (Table 2), which stronglysupports the hypothesis that cochleovestibular dysfunctionwas caused by the pathology in the affected inner ear, mostlikely due to inner ear hemorrhage. Besides, the rate ofvestibular symptom (dizziness/vertigo) was 21.0% (22/105)among 105 patients without MRI characteristics ofhemorrhage.

In the present study, all 112 patients received treatmentsincluding oral corticosteroids (Methylprednisolone 48 mg/day, full dose for 7 to 14 days, then taper over similar timeperiod) and/or hyperbaric oxygen therapy for two weeks [1],

Fig. 3 High signal intensity was observed in the left cochlea

and vestibule on unenhanced T1WI (A) and 3D-FLAIR axialimages (B). Co: cochlea, Ve: vestibule.

with an average effective rate of 46%. The prognoses of theseseven patients with possible inner ear hemorrhage werepoorer than expected, as none showed any response totherapy. Among the other 27 patients with profound deafnessor anacusis, 37% (10/27) had effective results. In the sevenpatients with suspected inner ear hemorrhage effectiveresults were not obtained (Fig. 4); however, the accompanyingsymptoms, such as vertigo and tinnitus in these patients withinner ear hemorrhage, were alleviated. Patient 5 with bilateraldeafness 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

Table2Clin

ical

featuresof

SSNHLpa

tien

tswhoweresu

spectedof

sufferingfrom

aninner

earhem

orrhage.

Patien

tsno.

Age

(years)

Indu

cemen

tCochlear

symptom

sVestibu

lar

Delay

ofMRI

exam

ination

MRIfindings

Side

Deafness

Tinnitus

Vertigo

Location

T1W

IT2W

IFLAIR

Gd-en

han

cemen

t

117

Fatigu

eRight

>120dB

Yes

Yes

18da

ysRightVe,Sc

High

High

High

No

223

Unkn

own

Right

92dB

Yes

Yes

14da

ysRightCo,

ScHigh

High

High

No

360

Anticoagulant

Left

93.75dB

Yes

Yes

17da

ysLeftCo,

ScHigh

High

High

No

423

Unkn

own

Left

93dB

Yes

Yes

15da

ysLeftCo,

ScHigh

High

High

No

511

URI

Bilateral

>120/>120dB

Yes

Yes

17da

ysBilateralC

o,Ve

High

Med

ium

High

No

634

URI

Left

>120dB

Yes

Yes

8da

ysLeftCo,

Sc,V

eHigh

Med

ium

High

No

723

Unkn

own

Right

102dB

Yes

Yes

18da

ysRightSc

High

High

High

No

Abb

reviations:Co,

coch

lear;S

C,sem

icircu

larcanal;S

SNHL,su

dden

sensorineu

ralh

earingloss;U

RI,upp

errespiratorytractinfection;V

e,vestibule.

321A 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 3Fig. 4 Poor therapy results in SSNHL patients with profoundSSNHL and addressed the importance of this examination forelucidating SSNHL etiology. RoutineMRImay identify 11.2% ofthe pathologic changes in the audiovestibular tract, a resultthat is consistent with previous reports (from 7% to 13.75%)[5,811]. Moreover, patients with SSNHL lossmay have a 6.25%chance of inner ear hemorrhage detectable by interpretingclinical and MRI results.

Many findings indicate the importance of complete MRIscreenings of the audiovestibular tract in SSNHL patients. Forexample, intracranial abnormalities believed to be responsiblefor sensorineural hearing loss were found in 19.2% patients[12]. The two case series' by Aarnisalo and Cadoni found MRIabnormalities in 44% of SSNHL cases [11,13]. Furthermore, MRIof the temporal bone, cerebellopontine angle, and brainshowed abnormal results in 24 of 78 patients (31%) withSSNHL [10]. In a smaller series of 16 patientswith SSNHL, threepatients (18.8%) had a significant pathologic condition iden-tified on MRI [14]. Our series of 13 abnormalities (11.6%) in 112patients supports the hypothesis that a significant number ofpathologic conditions can be detected by MRI.

Additionally, failure to identify lesions, such as acousticneuroma, could have detrimental consequences for patients.For instance, Chaimoff's study reported a far higher rate ofacoustic neuroma in SSNHL patients (48%) [15] than the 14% to19% rate previously documented in a retrospective series ofdeafness to anacusis. Patients with possible inner earhemorrhage showed no response to therapy.

onprecontrast 3DFLAIRare related to apoorhearingprognosis[18]. Ryu et al. evaluated twelve patientswhose initial and final

cases and series. In principle, hemorrhage by itselfmay have a

hearing at a 6-month follow-up.This study has certain limitations. Since biopsies are

5. Conclusion

N Dacoustic neuroma patients [16]. The present study identified alower rate of acoustic neuroma (1.79%); however, we validatedthe significance of MRI for diagnosing the cause of SSNHL.Thus, we recommend the use of MRI for the diagnosticevaluation of SSNHL patients.

We identified seven patients showing a high signal in thelabyrinth on unenhanced T1-weighted and FLAIR images. Thepossibility of false-positive results may be ruled out since ourresults and those from a previous study [7] never identified acontralateral alteration and/or a hyper-signal in the controlgroup. Weissman et al. stated that the presence of fat,decreased blood flow, high protein concentration, or priorhemorrhage generates hyperintense T1 images [2]. Fat is notfound in the labyrinth and is an extremely unlikely cause ofhigh signal in this location. The high signal was not replacedin FLAIR images in our seven patients, confirming an increasein inner ear proteins or prior hemorrhage, rather thanlymphatic fluid.

3D FLAIR hyperintensity indicates the modification of theinner ear protein composition that can be ascribed to a minorhemorrhage or to an acute inflammatory process [11]. In thiscohort, the delay from onset to MRI exam is between 8 and18 days (average 15.3 days). This time period does not supportacute 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 extracellularmethemoglobin, and in 3D FLAIR images, owing to theincreased protein content in themembranous fluid secondaryto the presence of methemoglobin, implicates intracochlearhemorrhage [7].

In the work Pathology of the ear, Schuknecht states thatinner ear hemorrhage can cause sudden hearing loss andvertigo [17]. He also states that spontaneous hemorrhage intothe inner ear mainly occurs as a complication of bleedingdisorders, the most common being leukemia. Schuknechtconfirmed this from histological studies of the temporal bonein patients who died just after the onset of ear symptoms [17].In our cohort, patient 3 (Table 2) continued to take warfarinsince undergoing an aortic valve replacement 2 years before-hand. The clotting test in this patient showed an obvioushemorrhagic tendency: a prothrombin time of 43.6 secondsand activated partial thromboplastin time of 46.7 seconds.The hypothesis regarding the cause of inner ear hemorrhagein the rest six patients may be presumed to be angiopsathyro-sis, vascular malformation or stress response etc.

An inner ear hemorrhage diagnosismay bemade using theinterpretation of clinical features combined with MRI in thisstudy based on the following observations: first, one of ourpatients had anticoagulant prescription history before SSNHL,while the other six patients were free of any other etiology.Second, the labyrinthine symptoms were well correlated withthe MRI results (cochlea, semicircular canals, or vestibuleinvolvement). Third, abnormally high MRI signals were onlyseen in the affected side compared to the contralateral side.Furthermore, high intensity on unenhanced T1WI and 3DFLAIR without postcontrast enhancement might help excludepatterns consistent with an inflammatory process or break-down of the blood labyrinth barrier [7].

322 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 AThe prognosis of patientswith high signals on unenhancedT1WI and 3D FLAIR in this study and other reports isThe results of this study emphasize the importance of MRIin SSNHL patients. Moreover, patients with vestibulardysfunction and sudden profound hearing loss may havean inner ear hemorrhage detectable by interpretation ofclinical and MRI results.

Conflict of interests

None.

Acknowledgments

The authors thank all participants in this study. The authorsalso thank Wenting Zou for her great technical assistance inradiology. The study was supported by grants from theNational Basic Research Program of China (2011CB504502),the National Natural Science Fund of China (30973306) and thekey nature fund of Guangdong Province (8251008901000016).

R E F E R E N C E S

[1] Stachler RJ, Chandrasekhar SS, Archer SM, et al. Clinicalcompleted forbidden in a study of this nature, the definitivediagnosis of an inner ear hemorrhage could not be made.Perhaps more advanced technology or post-mortem patho-logic findings may facilitate further research. Long termfollow-up and a larger number of patients in a clinical trialwould also favor the hypothesis presented in this study.different outcome from hemorrhagic transformation of anischemic process. Although left inner ear hyperintensitydisappeared in patient 4 (Table 2) during a second MRI exam3 months later, none of these seven patients recoveredhearing levels were 98.0 31.1 dB and 87.7 33.1 dB, respec-tively. They stated that high signals in the affected inner ear on3D FLAIR closely correlate with vestibular dysfunction andpoor hearing recovery in patients with SSNHL [19]. Lee et al.concluded that the absence of high-intensity signal on 3DFLAIR MRI can possibly imply a relative good prognosis [20]. Infact, simple hemorrhage into the perilymphatic space in smallamounts is reportedly well tolerated; massive hemorrhage,however, has not been followed up long enough in reportedconsistently poor. None of the seven of our patients showedany response to therapy except for alleviation of vertigo ortinnitus. Yoshida et al. showed that high signals in the cochlea

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323A 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

Magnetic resonance imaging-detected inner ear hemorrhage as a potential cause of sudden sensorineural hearing loss1. Introduction2. Methods and patients3. Results4. Discussion5. ConclusionConflict of interestsAcknowledgmentsReferences