Clin[ Otolaryn`ol[ 1999\ 25, 2Ð7

REVIEW

The influence of middle ear disorders on otoacousticemissions

F[ ZHAO\� H[ WADA\� T[ KOIKE� + D[ STEPHENS$�Department of Mechanical En`ineerin`\ Tohoku University\ Sendai\ Japan and $Welsh Hearin` Institute\ University Hospital ofWales\ Cardiff\ UK

Accepted for publication 20 August 0888

Otoacoustic emissions "OAEs# are low intensity sounds gen!erated within the normal cochlea and emitted from the exter!nal auditory meatus\ either spontaneously or in response toacoustic stimulation[ The _rst measurement of OAEs wasreported in 0867 by David Kemp[0 They are thought to re~ectactive biological mechanisms within the cochlea responsiblefor the exquisite sensitivity\ sharp frequency selectivity andwide dynamic range of the normal auditory system[ Moreover\this active cochlear process is presently thought to be basedin the outer hair cells[ Outer hair cell movement "mobility#generates mechanical energy within the cochlea that is believedto propagate outward through the middle ear system to theexternal auditory meatus[ Sounds produced in this mannerare termed OAEs and can be measured using a sensitive micro!phone[ When outer hair cells are structurally damaged ornonfunctional\ OAEs cannot be evoked by acoustic stimuli[1

Because the measurement of OAEs is simple\ fast\ objective\reproducible and noninvasive\ and because reduced OAEamplitudes are associated with certain types of hearing impair!ment\ over the past 19 years\ OAEs have been used in clinicalsettings to detect cochlear lesions resulting from factors suchas ototoxic drug administration\ noise overexposure\ Men!ie�re|s disorder\ sudden idiopathic hearing impairment\ pre!sbyacusis\ and hereditary hearing disorders[ In addition\OAEs have also been used as an indicator of the presence ofhearing impairment in neonates[1Ð3

However\ OAEs generated within the cochlea must passthrough the middle ear to their measurement site in the exter!nal auditory meatus\ and they are reduced when sound con!duction through the middle ear system is compromised[ There!fore\ great care must be taken to ensure normal middle earstatus if the OAEs are to be utilized as an index of cochlearfunction[

This paper reviews the e}ects of middle ear disorders onOAEs[ This would be valuable to provide some guidelines onthe limits of mild conductive hearing impairment which are

Correspondence] Professor Hiroshi Wada\ Department of Mech!anical Engineering\ Tohoku University\ Aoba!yama 90\ Sendai 879Ð7468\ Japan[

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associated with the presence of reliable OAEs\ and thus con!tribute to a clari_cation of the clinical application of OAEsand facilitate further research[

Relationship between middle ear dynamiccharacteristics and otoacoustic emissions

Studies of the acoustical characteristics of the middle ear haveshown that the sound energy coming into the external auditorymeatus is transmitted most e.ciently into the cochlea at themiddle ear resonance frequencies because the eardrumvibrates with the largest displacement amplitude[ However\the middle ear dynamic characteristics are not easily measuredby the conventional impedance meters[ Recently a new systemhas been developed to measure the middle ear dynamic charac!teristics under physiological conditions by means of a sweepfrequency impedance meter "SFI#\ which records sound pres!sure in dB SPL across a sweeping stimulus frequency insteadof immittance measures in the conventional impedance[4

The principles of the SFI technique are to provide a fre!quency sweep from 9[0 to 1 kHz instead of through a _xedstimulus frequency "usually at 199 or 115 Hz#[5 A three!dimen!sional output shows the sound pressure curves vs[ both fre!quency and external auditory meatus static pressure[ There!fore\ the SFI provides more information on middle eardynamic characteristics\ include the resonance frequencyregion and the sound pressure changes "DSPL#\ which re~ectsthe quantity of the tympanic membrane volume displacementat the resonance frequency and represents an index of themiddle ear mobility[ The resonance frequency region of themiddle ear in the normally hearing subjects is around 0[06 kHz"SD\ 9[16 kHz#[6

Because OAE transmission is thought to be in~uenced bythe middle ear dynamic characteristics\ SFI consequentlyappears to be a useful apparatus to investigate relationshipsbetween EOAEs and the middle ear dynamic characteristics[7\8

Based on the results of their studies\ Wada et al[7\8 concludedthat transient evoked otoacoustic emissions "TEOAEs# aredetected most distinctly at the middle ear resonance frequency

3 F[ Zhao et al[

and that TEOAEs are most detectable in normal subjectswhose middle ear mobility is within normal limits[ Moreover\the relationship between the distortion product otoacousticemission "DPOAE# amplitude and middle ear frequencycharacteristics was investigated[ The results showed the meanresonance frequency of the middle ear to be ¼ 0077 Hz\ andthe DPOAE level was the largest at the primary f1 frequencyaround 0[1 kHz\ which nearly coincided with the resonancefrequency of the middle ear[8 Subsequent analysis showed thatthe frequency characteristics of the greatest measured DPOAElevel correlated well with the middle ear resonance frequencywhen the amplitude of the 1f0Ðf1 DPOAE was plotted againstfrequency f1 or the geometric mean frequency[

Animal experiments have also demonstrated that OAEs areextremely susceptible to changes in middle ear dynamic statusby manipulation of the tympanic bulla[ In a simpli_ed middleear model of the guinea!pig\ the in~uence of bulla perforationon DPOAEs was investigated to compare the DPOAEmeasurement results with those of the middle ear frequencycharacteristics recorded by SFI[8 The results showed that theresonance frequency of the middle ear was observed at 2[0 kHzbefore the tympanic bulla perforation[ When a hole 0 mm indiameter was made\ it decreased sharply to 9[4 kHz[ As thediameter of the hole increased\ the resonance frequencyincreased\ attaining 0[0 kHz when the bulla was fully opened[Moreover\ the sharp increase in the DPOAE level with theprimary f1 frequencies lower than 0 kHz after tympanic bullaperforation and the following upward primary f1 frequencyshift of the DPOAE peak level with an increase in the diameterof the hole were well coincident with the resonance frequencyshift of the middle ear due to the manipulation of the tympanicbulla[8

Effects of middle ear transmission on measure-ment of otoacoustic emissions

When evoked OAEs are recorded\ it is essential that theincoming acoustical signal is conducted through the tympanicmembrane and ossicular chain to cause a displacement of ovalwindow of the cochlea[ The tympanic membrane functions ina manner similar to the diaphragm of a loudspeakermembrane\ and the ossicular chain helps to transmit thevibration to the cochlea[ Ampli_ed basilar membranevibration achieved by an active electro!mechanical involve!ment of outer hair cells is transmitted to the external auditorymeatus through the middle ear in a retrograde fashion and isdetected by the probe microphone[09 Thus\ the level of theOAE is doubly dependent on the characteristics of both ante!rograde and retrograde middle ear transmission[

This double dependence of OAEs on the transmissioncharacteristics of the middle ear\ i[e[ the e}ects on the signalreceived by the cochlea and the cochlear response measuredin the external auditory meatus has been considered to have a

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large in~uence on the OAEs measured in the external auditorymeatus[09 Although the acoustic response of the middle earmay be partly eliminated from the recorded data by thederived nonlinear recording technique\ the stimulus and coch!lear response are nevertheless in~uenced by the anterogradeand retrograde transfer functions of the middle ear\ respec!tively[

Furthermore\ because of the anatomical arrangement ofthe middle ear\ the retrograde conduction is probably lesse.cient than the normal anterograde transmission of acous!tical stimuli[00Ð03 According to the middle ear transmissionmechanism\ many components are consist of the middle earanterograde resistance\ for example the eardrum\ the liga!ments and the muscles of the middle ear\ the ligaments holdingthe stapedial foot plate in the oval window\ and the elasticproperties of the round window membrane[ Of those\ the mainresistive component is contributed by the input impedanceof the cochlea[04 By contrast\ retrograde resistance is mainlydependent on the acoustic impedance at the external auditorymeatus[

In a recent study\ the retrograde and anterograde trans!mission factors of the middle ear have been investigated usinga computer model[03 The middle ear anterograde transmissionfactor "TA# was de_ned as the ratio of the intracochlear pres!sure in the scala vestibuli "PC# to the external auditory meatuspressure in front of the tympanic membrane "PT#[ The retro!grade transmission factor "TR# was the ratio of the externalauditory meatus pressure in front of the tympanic membrane"POAE# to the corresponding intraocochlear pressure "PAMP#[Figure 0 shows the anterograde and retrograde transmissionfactors in the middle ear[

The numerical transmission factors were obtained andshowed that the maximum value of the TA was ¼07 dB SPLand that of the TR was around Ð 21 dB SPL at 0[9 kHz\ whichindicated the middle ear resonance frequency "Fig[ 1#[ Theseresults are in keeping with the _ndings by Puria andRosowski[02 Thus\ the TR was estimated far more lower thanthe TA because of the large di}erence between the impedanceof the cochlea and that of the external auditory meatus[

Based on the middle ear model of Zwislocki\04 Kemp05

calculated a 01 dB loss for retrograde transmission of a signalwithin the best frequency range of 0[9Ð0[4 kHz[ This loss

Figure 0[ Schematic of middle ear transmission factors[

In~uence of middle ear disorders on OAEs 4

Figure 1[ Comparison of the anterograde and retrograde transmissionfactors[

increased at a rate of about 01 dB:oct for both lower andhigher frequencies[ A similar frequency dependence of theretrograde transfer function for OAEs was measured bySchloth[06 This can explain why spontaneous OAEs "SOAEs#and evoked OAEs "EOAEs# are most readily demonstratedin the frequency range between 0[9 kHz and 1[9 kHz\ as theretrograde transfer function of the middle ear is most e.cientwithin this frequency range[01 According to the study of themiddle ear dynamic characteristics by Wada et al[7 such afrequency region represents the middle ear resonance fre!quencies in normally hearing subjects[ Therefore\ OAEs aredetected most distinctly at the middle ear resonance frequencyin normally hearing subjects[7

Influence of middle ear disorders on otoac-oustic emissions

Dysfunction of the middle ear ossicular system has beenshown to be associated with reduced TEOAEs in many middleear disorders\ e[g[ children with otitis media\07\08 patients withotosclerosis\19 etc[ Although these case reports suggested thatTEOAEs and DPOAEs were not necessarily obliterated bythe presence of patent ventilation tubes or mild middle eardisorders\ any changes in the transmission e.ciency of themiddle ear would be expected to have a considerable in~uenceon the cochlear emission measured in the external auditorymeatus[ Therefore\ various studies have investigated thein~uence of middle ear disorders on the OAE levels\ theirspectra and reproducibility[

Influence of static middle ear pressure on OAEs

Most early investigations speci_cally addressing the e}ect ofmiddle ear status on OAEs used experimental manipulationof middle ear status in normally hearing subjectsÐe[g[ by vary!

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ing air pressure in the external auditory meatus[10Ð13 Thesearti_cially induced changes in middle ear function dem!onstrated that middle ear sti}ness could be increased by chan!ges of static air pressure in the external auditory meatus[

In ears with normal middle ear pressure\ altering the staticpressure in the ear canal by 2 199 daPa caused a meanreduction of ¼ 6 dB for TEOAE frequencies below 0[4 kHz\with little e}ect at frequencies over 2[4 kHz[14 Moreover\ equa!lization of the middle ear pressure increased TEOAE ampli!tudes\ especially at low frequencies[15 In ears with abnormalnegative middle ear pressure caused by eustachian tube dys!function\ the amplitude of TEOAEs in the low frequencyband "³ 1[9 kHz# was signi_cantly attenuated[16 Individualadaptations of static ear canal pressure eliminated these alter!ations of the TEOAEs[ Thus\ it is clear that changes in themiddle ear impedance can have an e}ect on the measurementof TEOAEs[

Various studies have con_rmed that DPOAE amplitudesare also attenuated signi_cantly by changes of the static earcanal pressure\ with greater changes at low frequencies thanat high frequencies[16Ð18 A marked reduction in DPOAE ampli!tude was observed especially at 0 and 0[4 kHz[16 Such an e}ectat low frequencies has been hypothesized to be related to thesti}ness of the middle ear apparatus "i[e[ tympanic membranesti}ness and ossicular chain angular sti}ness#[ The changes inthe emission spectra resembled the characteristics of a high!pass _lter[ Similar relationships between pure tone audiogramand sti}ness have been described by Johansen[29

Moreover\ the alterations of OAE amplitude may be depen!dent on the polarity of the pressure[20 In an animal model\DPOAEs were measured in order to analyse the polaritye}ects of the middle ear pressure[ When positive pressure of099 and 199 mm H1O was applied to the middle ear\ there wasa greater e}ect at low frequencies than at high frequencies[ Itcould be explained by the fact that the tympanic membranewas pushed toward the external ear and its sti}ness wasincreased when positive pressure was applied[ Since the middleear is mainly dominated by sti}ness at low frequencies\ it isexpected that low frequencies would be more a}ected thanhigh frequencies[13\14 By contrast\ negative middle ear pressureof Ð 149 to Ð 099 H1O a}ected transmission across allfrequencies[ In addition\ negative middle ear pressures have agreater e}ect on both anterograde and retrograde trans!mission than positive pressures for almost all frequencies from9[14 to 5 kHz[13\20 The mechanism underlying the e}ect ofnegative pressure at low frequency appears to be related totympanic membrane sti}ness\ whereas the e}ect of negativepressure at high frequency may be related to changes in theincudostapedial joint[20

The in~uence of the static middle ear pressure on spon!taneous otoacoustic emissions "SOAEs# has also been inves!tigated[01 Because SOAEs represent a steady transfer retro!grade transmission condition without interference by externalstimuli\ pathological changes in the middle ear transfer func!

5 F[ Zhao et al[

tion may interfere with the release of energy from the cochleaand alter the frequency of SOAEs[ Several studies have sug!gested that these changes may also modify the perception ofSOAEs so that a special form of tinnitus associated withmiddle ear disorders\ is induced[01

Animal experiments have shown that changes in middle earpressure of 2 49 mm H1O decreased SOAE amplitude by 19dB in guinea!pigs\ while having little e}ect on the amplitudeof the electrical correlate SOAEs recorded at the roundwindow[21 This _nding suggests that\ whereas the SOAEs werereduced in the external auditory meatus due to a sti}ening ofthe middle ear transmission system\ the amplitude of theSOAEs within the cochlea remained unchanged[

In the study by Ohyama et al[22 the e}ect of external audi!tory meatus pressure on frequency shifts of the electrical cor!relate of SOAE was investigated[ The SOAE frequencyaround 0 kHz increased by ¼ 29 Hz when positive pressureof 099 mm H1O was applied to the sealed external auditorymeatus[ The level change was not signi_cant[ When the incu!dostapedial joint was disrupted\ a slight decrease in frequencywas observed[ Such e}ect of pressure on the frequency ofSOAEs can be explained as follows] "0# the applied pressureincreases the middle ear sti}ness^ and "1# it directly modi_essome undetermined tuning components within the cochlea[22

Influence of otitis media with effusion on OAEs

It is well documented that childrenÐparticularly between theages of about 1 and 5 yearsÐhave a high prevalence and inci!dence of middle ear disorders\ particularly eustachian tubedysfunction and otitis media with e}usion[23 Measures ofOAEs in children with middle ear disease are severely limitedwith respect to investigating inner ear function[ It is thereforenecessary to investigate the feasibility of such an applicationin young patient populations[

In the study by Amedee\24 the presence or absence of emis!sions in ears with chronic e}usions was primarily a functionof the type of ~uid in the middle ear space\ with mucoide}usions resulting in less likelihood of recording OAEs[ Thus\the type of e}usion found within the middle ear appears to bethe controlling factor a}ecting the presence or absence ofemissions[24 It seems logical to suppose that thicker e}usionswould increase the resistant loading e}ect on the middle earsystem and account for the absence of OAEs[

In the study by Owens et al[07 ears with either type B or typeC tympanogram patterns showed absent or markedly reducedOAE amplitudes\ when compared with emissions measuredin their control counterparts[ Further frequency analysis ofDPOAE audiograms "DP!grams# showed that DPOAEs weree}ectively absent for the acutely infected ear except for arestricted frequency range between about 1[9 and 3[9 kHz[

However\ the presence or absence of emissions seems notalways dependent on tympanogram types[ Based on the results

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of a study by Amedee\24 tympanogram type does not seem tobe a signi_cant contributor to the presence or absence ofemissions in all subjects with type B or type C tympanograms[Therefore\ neither the presence of abnormal tympanogramsnor otoscopic evidence of middle ear e}usion is su.cient toexpect emissions to be absent in a given individual[

Influence of ventilating tube insertion andrelated surgery

In the study by Owens et al[07 ears with ventilation tubes hadexhibited OAE amplitudes smaller than those from healthyears\ but larger than those of the untreated diseased ears[Moreover\ at 6 weeks following the procedure\ OAE levels forthe both TEOAEs and the DPOAEs were improved to normalor near!normal amplitude[ Thus\ OAEs can also be used asa means to monitoring the e.cacy of medical or surgicalintervention on the transmission properties of the middle earin conditions involving otitis media[

Although the presence of ventilation tubes does not resultin a total loss of previously measurable TEOAEs in ears withemissions present prior to myringotomy and ventilation tubeinsertion\ the presence of ventilation tubes appears to modifythe properties of the TEOAEs\ resulting in lower amplitudesin the mid to high frequencies "³ 3 kHz#[24 Based on theseresults\ a ventilation tube may be expected to function in asimilar manner as a small\ dry perforation of the tympanicmembrane and allow for measurable OAEs[

Conclusions

This review has examined the current knowledge regardingthe relationship between middle ear disorders and otoacousticemissions[ Although OAEs are expected to be particularlyvulnerable to the e}ects of middle ear disorders in general\the presence of middle ear disorders does not necessarily causeemissions to be absent in an individual\ particularly in patientswith deviations of middle ear pressure from normal can resultin substantial reductions of OAE amplitude\ with greaterchanges at low frequencies that at high frequencies[

OAEs can be recorded in middle ear disease when hearingthreshold levels are − 29 dB\ if patients with middle ear dis!orders have normal cochlear function[ However\ middle eardisorders associated with mild sensorineural hearing impair!ment will have a disproportionate impact on expression ofOAEs[ Thus\ middle ear disease compromises the validity ofOAEs aimed at evaluating the status of the biomechanicalfunction of outer hair cells[

At present\ there are no guidelines on the limits of negativemiddle ear pressure\ types of tympanogram\ amount or qual!ity of the middle ear e}usion and so forth that are associatedwith the presence of reliable OAEs[ In future research\ detaileddescriptions of TEOAE and DPOAE _ndings in large num!

In~uence of middle ear disorders on OAEs 6

bers of subgroups of patients with well de_ned middle eardisorders "e[g[ serous otitis media\ acute otitis media withe}usion\ tympanic membrane perforation\ otosclerosis\ cho!lesteatoma\ discontinuity of the ossicular chain# and infor!mation on the relationships between OAE _ndings and otheraudiometric _ndings could make an important contributionto the clinical application of OAEs[

Finally\ computer models may enable to overcome the com!plicated\ irregular geometries of the biological structures ofthe middle ear\ and thus further eliminate dynamic behaviourin detail[ Moreover\ pathological changes can also be simu!lated using computer models\ which would be useful forinvestigating the in~uence of middle ear disorders on OAEs[

Acknowledgements

Dr Fei Zhao is supported by Postdoctoral Fellowship of JapanSociety for the Promotion of Science "JSPS#[

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