Acta Oto-Laryngologica. 2013; 133: 1173–1180

ORIGINAL ARTICLE

Risk factors for sensorineural hearing loss in chronic otitis media

MICHAL LUNTZ1, NOAM YEHUDAI1, MIKI HAIFLER1, GIL SIGAL1 & TOVA MOST2

1Cochlear Implant Program, Department of Otolaryngology–Head & Neck Surgery, Bnai-Zion Medical Center,Technion–Bruce Rappaport Faculty of Medicine, Haifa, Israel and 2School of Education, Department of CommunicationDisorders, Tel Aviv University, Tel Aviv, Israel

AbstractConclusions: Risk factors for sensorineural hearing loss (SNHL) development in patients with chronic otitis media (COM) arelonger duration of disease, older age and the presence of cholesteatoma. To prevent the expected development of SNHL, it isimperative to treat COM actively.Objectives:To assess the severity of SNHL in patients with unilateral COM and to define riskfactors for its development. Methods: The study included 317 patients with unilateral COM. Mean age was 28.7 ± 16.7 years(range 7–78 years) and mean duration of disease was 12.2 ± 11.3 years (range 0.25–60 years). In all patients, air conduction(AC) and bone conduction (BC) thresholds in both ears were measured at 500, 1000, 2000 and 4000 Hz. The parametersevaluated were demographics, duration of disease, presence and location of cholesteatoma and otologic history. Results:The difference in mean BC thresholds between the diseased ears and the healthy ears was statistically significant, ranging from4.55 ± 10.89 dB to 12.55 ± 19.09 dB across the measured frequency range (p < 0.0001). Multivariate regression analysisrevealed statistically significant correlations between advanced age, longer duration of disease and presence of cholesteatoma,and the BC threshold differences between the affected and healthy ears.

Keywords: Cholesteatoma, aging, air conduction, bone conduction

Introduction

Chronic otitis media (COM) with or without cho-lesteatoma is a significant public health problemaffecting 0.5–30% of any given population in devel-oping and developed countries [1]. It is characterizedby recurrent infections causing pain and purulentotorrhea, and can lead to serious complications.The resulting hearing loss, which can be conductive(CHL) or sensorineural (SNHL) or both, may haveserious long-term effects on language and educationalprogress [1]. CHL is considered to be a typical featureof COM, attributable to impairment in the middle earimpedance-matching mechanism as a result of perfo-ration of the tympanic membrane, fixation or loss ofcontinuity of the ossicular chain and accumulation offluids or semi-solid materials in the middle ear cavity,all of which comprise the essence of COM [2]. SNHL

is also considered a frequent sequela of COM, butthere is a lack of controlled data regarding its link withCOM, its clinical significance or practical recommen-dations for its prevention.Studies aimed at defining the clinical significance

of SNHL in COM have reached inconsistent conclu-sions. Several authors have reported a clinicallysignificant deterioration in bone conduction (BC)thresholds in COM ears relative to the contralateralnormal ears [3–7]. Others have found no such clinicallysignificant differences [8,9].Both direct and indirect mechanisms are implicated

when SNHL occurs as a sequela of middle ear disease.Direct damage to inner ear structures can be the resultof one or more of the following three mechanisms:Penetration of toxic agents (disease-related inflam-matory mediators, toxic ear drops) from the middleear via the round window membrane into the inner

Correspondence: Michal Luntz MD, Department of Otolaryngology–Head & Neck Surgery, Bnai-Zion Medical Center, Technion–Bruce Rappaport Faculty ofMedicine, 47 Golomb St, PO Box 4940, 31048 Haifa, Israel. Tel: +972 4 8359544. Fax: +972 4 8361069. E-mail: michal.luntz@b-zion.org.il

(Received 15 April 2013; accepted 3 June 2013)

ISSN 0001-6489 print/ISSN 1651-2251 online � 2013 Informa HealthcareDOI: 10.3109/00016489.2013.814154

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ear [10,11]; disease-related destruction of the innerear bony framework, mostly a lateral semicircularcanal fistula exposing the inner ear to the environmentof the diseased middle ear, resulting in labyrinthitis[12] and mechanical and acoustic trauma to inner earstructures as a result of intraoperative drilling andmanipulation of the ossicular chain for diseaseremoval [13].An increase in the functional mass of the ossicular

chain can indirectly increase the BC threshold as aresult of ossicular chain fixation or the accumulationof fluids and semi-solid material in the middle earcavity, replacing normal gas [14]. This might lead tochanges in the resonant frequency of the ossicularchain, thereby limiting the mobility of oval windowand inner ear fluids, similar to the Carhart effect inotosclerosis [7].The aims of this study were to assess the severity of

SNHL in patients with unilateral COM, using thecontralateral healthy ear as a control, and to definerisk factors for the development of SNHL in COM.Identifying these risk factors is likely to be helpful indefining additional treatment indications for COM,thereby reducing the incidence of SNHL.

Material and methods

Subjects

Between December 1997 and June 2011, 650 conse-cutive patients were admitted to a tertiary-referralotologic centre for surgical management of COM.Patients with bilateral disease, congenital cholestea-toma, additional otologic pathology or a congenitalinner ear malformation were excluded. In all, 317patients with unilateral COM were included in thestudy. Mean age at admission was 28.7 ± 16.7 years(range 7–78 years) and the mean duration of diseasebefore admission was 12.2 ± 11.3 years (range 0.25–60 years). The contralateral healthy ear was used as acontrol, thus eliminating possible environmental,occupational or age-related effects on hearing status.The study was approved by the Institutional Review

Board of the Bnai-Zion Medical Center, Haifa, Israel.

Audiometry

Audiometric evaluation was performed according tothe recommendations of the American Academy ofOtolaryngology–Head and Neck Surgery Committeefor reporting hearing thresholds in CHL (in accor-dance with the guidelines, recorded data at 4000 Hzreplace non-existing data at 3000 Hz) [15]. Thecollected data included air conduction (AC) andBC thresholds at frequencies of 500, 1000, 2000

and 4000 Hz in both ears. BC pure-tone average(BC-PTA) in both ears was calculated as the averageof BC thresholds at 500, 1000, 2000 and 4000 Hz.The difference between BC thresholds in the ear withCOM and the healthy ear (DBC) was calculated. Theair–bone gap (ABG) in the affected ear was calculatedas the difference between AC and BC thresholds at500, 1000, 2000 and 4000 Hz.

Other parameters

The parameters assessed were age, duration of dis-ease, gender, side of disease, presence and location ofcholesteatoma, location of the tympanic membraneperforation, otologic history, and the types and num-bers of previous ear surgeries.

Statistical analysis

Data were analyzed using SPSS 18.0 (SPSS, Chicago,IL, USA). A paired t test was used to examine thedifferences in AC and BC thresholds at each fre-quency between the healthy and the affected ear.A t test and ANOVA were used to determine therelationship between the DBC at each frequency andthe categorical variables (gender, side, disease type,type and number of previous ear surgeries, type ofdisease, site of perforation and otologic history).Pearson’s correlation coefficient analysis was used todetermine the relationship between the DBC at eachfrequency and the disease duration and the patient’sage, and between the BC at each frequency and theABG. Stepwise multiple linear regression analysis wasused to predict the relationships between DBC andseveral predictor (independent) variables. A p value of0.05 was considered statistically significant.

Results

Pure-tone AC and BC thresholds at 500, 1000,2000 and 4000 Hz in the affected ear and the normalear are presented in Figure 1. A statistically significantdifference in AC and BC thresholds between the twoears, ranging from 27.21 ± 10.27 dB to 31.48 ± 9.57 dBand from 4.55 ± 10.89 dB to 12.55 ± 19.09 dB, respec-tively, was found across the range of frequencies(p < 0.0001, Table I).We found that DBC betweenthe two earswas 20dBormore in 11–25.2%of patients,andDBCwasmore than 25dB in 6.3–17.6%of patientsacross the range of frequencies (Figure 2).Table II records ABG values in the affected ear at

each frequency. No correlation was found betweenthe BC threshold and the ABG at any of the testedfrequencies. Table III presents the DBC values foreach of the categorical parameters evaluated.

1174 M. Luntz et al.

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Univariate analysis disclosed significant correlationsbetween DBC and advanced age (Figure 3), longerduration of disease (Figure 4), the presence of cho-lesteatoma (Figure 5) and more than one previoussurgery (Figure 6).Multivariate stepwise linear regression analysis

revealed that the parameters with the greatest influ-ence on DBC were duration of disease, patient’s ageand the presence of cholesteatoma. The resultingpredictive equations for DBC at each frequency are:

Δ =− + × + ×

= = <

BC Hz age duration

r F p

500 2 884 0 194 0 013

0 39 26 788

. . .

. , . , 00 0001.( )

ð1Þ

Δ = + × − × +

× =

BC Hz age type

duration r

1000 0 593 0 178 5 056 0 016

0 432

. . . .

. ,, . , .F p= <( )22 799 0 0001

ð2Þ

Δ = + × − × +

× =

BC Hz age type

duration r

2000 5 693 0 189 8 601 0 021

0 445

. . . .

. ,, . , .F p= <( )24 569 0 0001

ð3Þ

Δ = + × − ×

= =

BC Hz duration

type r F

4000 12 814 0 027 7 881

0 289 13 666

. . .

. . ,pp<( )0 0001.

ð4ÞDiscussion

The widely accepted treatment for COM is surgical,with the aim of making the ear safe (thus avoidingcomplications) and dry, and achieving the best

possible restoration of hearing. Clinicians should per-form the minimum number of surgical proceduresconsistent with achieving these goals [16].SNHL is a documented but unpredictable sequela

of COM. In the present study, statistically significantdifferences in both AC and BC thresholds were foundbetween healthy and COM ears (Table I). In 11–25.2% of our patients, BC thresholds in the healthyand the COM ear differed by at least 20 dB at all of themeasured frequencies (Figure 2). These results are inaccordance with the findings of several studies. In amulticentre study, Paparella et al. found that 58% of874 patients with unilateral COM presented with aSNHL of more than 15 dB in the affected ear [6]. El-Sayed showed in 218 patients that BC thresholds over

AC-COM

Frequency (Hz)

500 1000 2000 4000

Hea

rin

g t

hre

sho

ld (

dB

SP

L)

AC-normal BC-normalBC-COM

605550454035302520151050

Figure 1. Mean group air conduction and bone conduction thresh-olds at 500, 1000, 2000 and 4000 Hz. SPL, sound pressure level.

Table 1. Mean group differences in air conduction thresholds(DAC) and bone conduction thresholds (DBC) between the affectedear and healthy ear at 500, 1000, 2000 and 4000 Hz.

Frequency

500(Hz) 1000(Hz) 2000(Hz) 4000(Hz)

Mean SD Mean SD Mean SD Mean SD

DAC(dB)

31.14 10.33 28.49 10.2 27.21 10.27 31.48 9.57

DBC(dB)

4.55 10.89 5.27 11.73 9.49 15.15 12.55 19.09

p 0.0001 0.0001 0.0001 0.0001

Frequency (Hz)

11.0%

0%10%20%30%40%50%60%

8.5%15.1%

≥20 dB

≥25 dB

25.2%

500 1000 2000 4000

Frequency (Hz)

A

B

500 1000 2000 4000

6.3% 6.3%

0%10%20%30%40%50%60%

8.8%17.6%

Figure 2. Percentages of patients with bone conduction thresholddifferences of more than 20 dB (A) and more than 25 dB (B)between the ear with chronic otitis media and the healthy ear.

Risk factors for SNHL in chronic otitis media 1175

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a range of frequencies were increased by 9.2 to14.1 dB in COM ears, with an average differencebetween COM and normal ears of more than 10 dB in39% of patients and of 20 dB or more in 12% ofpatients [5]. Eisenman and Parisier found greaterdifferences at 4000 Hz (5 dB) than at 500, 1000 or

2000 Hz (3 dB) in 145 patients with unilateral COM[4]. Redaelli de Zinis et al. observed significant dif-ferences in BC between COM and normal ears in344 patients, ranging from 0.6 dB at 500 Hz to 3.7 dBat 4000 Hz for all frequencies [7]. Da Costa et al.reported on 150 patients, a BC difference of 5 dBbetween COM and normal ears at 1000 and 2000 Hz,increasing to 10 dB at 3000 and 4000 Hz [3].Whereas the conductive component of the hearing

loss can be surgically resolved in many patients suf-fering from COM, the sensorineural componentreflected by the deterioration in BC threshold isirreversible and often clinically significant evenwhen unilateral.If the assumption that deleterious substances can

pass through the round window membrane is correct,it is reasonable to assume that SNHL will be moresevere in patients suffering from COM with choles-teatoma than in those with COM without

Table 3. Correlations between DBC at 500, 1000, 2000 and 4000 Hz and patients’ gender, side, type of COM, site of perforation, otologichistory, and number of previous surgeries.

DBC† (dB) according to frequency500 (Hz) 1000 (Hz) 2000 (Hz) 4000 (Hz)

n % Mean SD Mean SD Mean SD Mean SD

Gender Male 172 54.1 3.87 9.88 4.16 9.97 9.39 14.28 12.27 17.81

Female 145 45.9 5.38 11.96 6.59 13.46 9.62 16.19 12.9 20.57

p ns* ns ns ns

Side Right 156 49.1 4.36 10.3 5.29 11.09 8.62 13.64 12.24 19.42

Left 161 50.1 4.75 11.47 5.25 12.32 10.34 16.5 12.86 18.83

p ns ns ns ns

Type of COM§ Simple 129 40.9 3.74 9.18 3.03 9.13 5.66 11.85 8.74 14.76

Cholest 188 59.1 5.73 13.01 8.346 14.3 14.65 17.7 17.27 22.87

p ns 0.0001 0.0001 0.0001

Site of perforation Central 74 39.3 3.65 9.94 3.72 9.18 6.35 14.77 8.18 18.18

Anterior 36 19.1 5.28 11.83 4.38 12.86 5.42 10.45 10.97 10.48

Subtotal 29 15.9 3.45 7.69 0.34 5.97 4.31 7.04 5.52 9.29

Others 40 25.7 3.38 8.35 4.13 7.84 7.38 11.82 11.13 13.02

p ns ns ns ns

Recurrent AOM‡ Yes 206 64.8 4.19 14.56 4.77 15.11 8.76 17.43 11.36 21.10

No 111 35.2 5.09 10.09 5.93 11.50 10.14 15.20 14.86 19.16

VT** 57 17.9 2.98 12.81 4.39 15.18 8.77 17.69 12.72 22.20

p ns ns ns ns

Previous Surgeries 0 157 50.3 4.36 10.36 3.98 10.57 6.85 13.39 9.27 15.08

1 104 33.0 3.51 11.04 4.52 10.60 9.95 13.21 11.88 16.96

>1 53 16.7 6.89 11.9 10 15.06 15.47 20.13 22.74 28.31

p, 0 vs.>1 ns 0.005 0.001 0.0001

p, 1 vs.>1 0.019 ns 0.003

*Not significant; †DBC; ‡Acute otitis media; §Chronic otitis media cholesteatoma; **Ventilating tube.

Table 2. Mean air-bone gap values in the affected ear at 500, 1000,2000 and 4000 Hz.

Frequency (Hz) ABG (dB)

Mean SD

500 29.92 9.82

1000 26.25 7.64

2000 20.65 8.74

4000 22.14 6.46

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cholesteatoma. The severity can be expected toworsen the longer the disease lasts, because of theprolonged exposure of the round window membraneto such substances and to the further growth andspreading of the cholesteatoma. Advanced age isanother risk factor for SNHL, owing to age-related structural changes in the inner ear. To neu-tralize its effect, and assuming that age affects bothears similarly, we selected patients with unilateralCOM and compared the BC threshold in the COMear to that in the healthy non-COM ear of eachpatient.Several demographic and clinical parameters have

been implicated in the development of SNHL inpatients with COM, but in most studies only oneor two factors have been shown to be significantlyinfluential. Eisenman and Parisier found that inpatients with COM, SNHL develops in the thirddecade of life and worsens with age, reaching maxi-mum severity in the sixth decade in the presence ofdisease [4]. El-Sayed reported a significant relation-ship between threshold elevation and the type andduration of disease [5]. Levine et al. surveyed thecharts of 161 unilateral COM patients, and found a

significant relationship between SNHL and the pres-ence of acquired cholesteatoma in the middle ear [9].In the present study, using a multivariate stepwise

linear regression model, we established several vari-ables that affect SNHL in COM, making it possible topredict its severity. The DBC was found to be signif-icantly correlated with duration of disease at 500,1000, 2000 and 4000 Hz, with patient’s age at 500,1000 and 2000 Hz, and with the presence of choles-teatoma at 1000, 2000 and 4000 Hz. By using thesuggested formulas for predicting hearing thresholdsamong COM patients, clinicians can improve man-agement counselling.It is questionable whether BC threshold levels in

COM actually represent thresholds of sensorineuralhearing, or as with otosclerosis, it is merely an arti-ficial BC threshold elevation around 2.0 kHz (theCarhart effect), which resolves after resumption ofnormal ossicular chain mobility. Five factors contrib-ute to the BC thresholds recorded by the introductionof a bone vibrator on the skull: the spreading of soundwaves to the external auditory canal and adjacenttissues; inertial movement of the ossicular chain;inertial movement of cochlear fluids; mechanical

Years

DBC 500

y = 0.3604x + 6.8771R2 = 0.2393

0 10 20 30 40 50 60 70 80 90

dB

0

10

20

30

40

50

60

70

80

Years

DBC 2000

0 10 20 30 40 50 60 70 80 90

dB

0

20

40

60

80

100

120

Years

DBC 1000

y = 0.3854x + 4.9925R2 = 0.2096

0 10 20 30 40 50 60 70 80 90

dB

0

10

20

30

40

50

60

70

80

y = 0.5188x + 6.221R2 = 0.2362

Years

DBC 4000

0 10 20 30 40 50 60 70 80 90

dB

0

20

40

60

80

100

120

y = 0.5188x + 6.221R2 = 0.238

Figure 3. Correlation between age and bone conduction threshold differences at 500, 1000, 2000 and 4000 Hz.

Risk factors for SNHL in chronic otitis media 1177

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compression of the cochlear wall; and transmission ofpressure through the cerebrospinal fluid [17]. Themost important of these is the inertial movement ofcochlear fluids between the oval and round windows

as a result of the pressure gradient produced by thevibrating bone transducer. Under pathological con-ditions, other factors become more important. Inotosclerosis, BC thresholds are elevated at middlefrequencies and are maximal at 2000 Hz, as describedby Carhart [18]. This shift in BC can be explained byfixation of the stapes to the oval window, resulting in achange in the resonant frequency of the ossicularchain, which is manifested in BC elevations at fre-quencies representing the normal resonant frequencyof the ossicular chain (1000–3000 Hz). It is possiblethat a similar effect on the resonant frequency mightoccur in COM, which is associated with interruptionof the ossicular chain and mechanical occlusion of theoval window by granulations, exudates or cholestea-toma. These pathological processes can reduce themovements of the round window membrane, therebyartificially elevating measurements of BC thresholdswithout representing a true SNHL. Several studiessupport this hypothesis. Papastavros and Varlejidesfound significant improvement in BC thresholds as aresult of medical treatment of purulent COM [19].Linstrom et al. observed that in 71% of patients whounderwent ossicular reconstruction the BC thresholdswere improved by at least 10 dB at two or more

Frequency (Hz)

Simple COM COM with cholesteatoma

500

3.7 5.7 5.73.0

8.3

14.717.3

8.75.3

11.5

1000 2000 4000 PTA

D B

on

e co

nd

uct

ion

(d

B)

0

5

10

15

20

25

30

35

Figure 5. Correlation between presence of cholesteatoma and boneconduction threshold differences at 500, 1000, 2000 and 4000 Hz.

Months

DBC 500

y = 0.0294x + 12.866R2 = 0.1045

0 100 200 300 400 500 600 700 800

dB

0

10

20

30

40

50

60

70

80

Months

DBC 2000

0 100 200 300 400 500 600 700 800

dB

0

20

40

60

80

100

120

Months

DBC 1000

y = 0.0352x + 10.849R2 = 0.1145

0 100 200 300 400 500 600 700 800

dB

0

10

20

30

40

50

60

70

80

y = 0.046x + 14.297R2 = 0.122

Months

DBC 4000

0 100 200 300 400 500 600 700 800

dB

0

20

40

60

80

100

120 y = 0.0459x + 21.344R2 = 0.0815

Figure 4. Correlation between duration of disease and bone conduction threshold differences at 500, 1000, 2000 and 4000 Hz.

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frequencies, while no such improvement was seen in acontrol group without ossicular reconstruction [20]. Ifthis is indeed the mechanism underlying the BCthreshold elevations in COM, its effect should bemaximal at frequencies that represent the resonantfrequency of the ossicular chain (1000–3000 Hz). Inaddition, if the reason for BC threshold elevations is animpairment of one or more middle ear components, itwill be reasonable to expect a correlation between theseverity of the CHL and the severity of the SNHL.However, in the present study no correlation was foundbetween the ABG (representing CHL) and BC thresh-olds (representing SNHL) in the affected ear. Further-more, the difference in BC thresholds between the earsincreased along the frequency range, reaching a max-imum at 4000 Hz, not at 1000–3000 Hz as would havebeen expected. These findings exclude the Carharteffect as a possible explanation for the BC thresholdelevations observed in patients with COM, and ratherlead to the conclusion that this is a true SNHL. This isin agreement with Stenfelt and Goode, who concludedthat no major alterations could be expected in BCthresholds at the high (‡4000 Hz) or low frequencies(£500 Hz) that result from middle ear disease [17].The factors found to have a significant influence on

the severity of SNHL in COM in the present studycan and should be controlled. This can be achieved byearly surgical control of the disease, thus preventingits prolonged duration and avoiding the problem ofreaching an older age while still suffering from activeinflammatory middle ear disease.In conclusion, the clinical importance of SNHL in

COM should not be overlooked. To prevent theexpected development of SNHL, it is imperative

to treat COM patients actively, also when dealingwith a unilateral disease since even a mild degree ofunilateral SNHL might lead to compromised social,academic and functional accomplishments. Anaggressive approach in the case of older patients,those presenting with longer duration of COM orwith cholesteatoma is mandatory because they areprone to developing a more severe form of SNHL. IfSNHL has already developed in an ear with COM, itshould be properly rehabilitated.

Acknowledgments

The authors thank Ronit Leiba MSc for the statisticalanalysis and Shirley Smith for the scientific editing.

Declaration of interest: The authors report noconflicts of interest. The authors alone are responsiblefor the content and writing of the paper.

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6.910.0

15.5

22.7

13.8

Frequency (Hz)

No surgery One surgery > One surgery

4.4 3.5 4.0 4.56.8

p = 0.019

10.0 9.311.9

6.1 7.5

500 1000 2000 4000 PTA

D B

on

e co

nd

uct

ion

(d

B)

0.000

5.000

10.000

15.000

20.000

25.000

30.000

35.000

p = 0.003

Figure 6. Correlation between number of previous surgeries and bone conduction threshold differences at 500, 1000, 2000 and 4000 Hz.

Risk factors for SNHL in chronic otitis media 1179

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