are normal hearing thresholds a sufficient condition for click-evoked otoacoustic emissions?

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Are normal hearing thresholds a sufficient conditionfor click-evoked otoacoustic emissions?

Sarosh Kapadiaa)

MRC Institute of Hearing Research, Ropewalk House, 113 The Ropewalk, Nottingham NG1 6HA,United Kingdom

Mark E. LutmanInstitute of Sound and Vibration Research, University of Southampton, Southampton SO17 1BJ,United Kingdom

~Received 6 June 1996; revised 3 February 1997; accepted 25 February 1997!

Transiently evoked otoacoustic emissions~TEOAE! have been reported in several studies as absentin a small minority of normal ears. Other studies have reported TEOAEs in all normal ears.Differences between studies may arise directly from criteria for TEOAE identification, criteria forselection of normals, or statistically due to limited sample sizes. In order to understand and modelcochlear processes involved in TEOAE generation, it needs to be known whether the presence ofnormal hearing leads automatically to generation of TEOAEs. The present study set out to establishin a large sample if any ears could be found that lacked TEOAEs despite normal hearing thresholdlevels ~HTL!. A total of 397 ears from highly cooperative adult subjects were examined underlaboratory conditions. Using cross correlation between replicate nonlinear waveforms as thecriterion, TEOAEs were present in 99.2% of the sample~lower CI 98.1%!. However, careful visualassessment of the recorded waveforms for the remaining ears did not unequivocally show absenceof TEOAE characteristics in any ear with normal HTLs. While TEOAE strength varies widelyamong ears, no clear evidence was found to show that TEOAEs can be absent when HTLs arenormal. © 1997 Acoustical Society of America.@S0001-4966~97!05906-7#

PACS numbers: 43.64.Jb, 43.64.Kc, 43.64.Bt@RDF#

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INTRODUCTION

Transiently evoked otoacoustic emissions~TEOAE! rep-resent the release of acoustic energy from the cochleathe ear canal~Kemp, 1978!. The existence of a TEOAE isheld to indicate normal or near-normal outer hair-cell funtion, and it is generally accepted that the presenceTEOAEs implies hearing threshold levels~HTL! are 30 dBor better at least at some frequencies in the range 0.5–4~Probstet al., 1991!, barring rare cases of purely retrocchlear disorder. However, it is unclear whether the conveis always true, as a number of studies have been unabdetect TEOAEs in a small minority of adult ears with normhearing~Rutten, 1980; Probstet al., 1986; van Dijk and Wit,1987; Stevens, 1988; Dolhenet al., 1991; Lutman and Saunders, 1992; Prieveet al., 1993!.1

Failure to record a TEOAE in a normally hearing emay be due to limitations of the measuring conditions~re-cording system, ambient conditions, scoring criteria!, or al-ternatively TEOAEs could be genuinely absent in some nmal ears. The latter would imply that normal cochlear~andmiddle-ear! function is not asufficientcondition for the gen-eration of TEOAEs. It is also well established that in manormal ears TEOAE energy may be measurable at somequencies of normal hearing, but not at adjacent frequenalso having normal hearing~Probstet al., 1991!. This againsuggests that factors other than those required for nor

a!Now at MRC Institute of Hearing Research, Southampton OutstatRoyal South Hants Hospital, Southampton SO14 0YG, UK.

3566 J. Acoust. Soc. Am. 101 (6), June 1997 0001-4966/97/101(

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hearing can influence the generation of TEOAEs, althoudestructive interference between TEOAE components moffer an alternative explanation. This paper representsfirst part of an investigation into the reasons why some nmal adult ears display absent or weak TEOAEs, theregathering insights into the generation and fundamental prerties of TEOAEs.

The literature is generally consistent in showing a prelence above 95% for TEOAEs in ears with normal hearin2

excluding studies where recording conditions were not wcontrolled. Some studies have obtained TEOAEs in all nmal ears tested; notably several studies by Bonfils andworkers, of which Bonfilset al. ~1988a! and Bonfilset al.~1988b! are representative, those of Vedantam and Mus~1991! and Reshefet al. ~1993!, being based on 131, 105100, and 61 normal ears, respectively. Other studies sucKemp ~1978! have also reported emissions in all normal etested, but in small samples. Four studies have repoprevalence figures of 96%–97%~Probst et al., 1986;Stevens, 1988; Dolhenet al., 1991; Lutman and Saunder1992!.

Part of this variation among studies may arise from stistical uncertainty in estimates obtained from small sampClearly, there is always the possibility that TEOAEs coube obtained in all ears in a random sample, even if the tpopulation prevalence is less than 100%. To minimize tpossibility, larger samples are required than those quoabove.3 However, if a genuine sample prevalence of anthing less than 100% is obtained, then the population prelence logicallycannotbe 100%~barring system limitations!.,

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Aside from statistical uncertainties, three further issuesimportant in considering studies of TEOAE prevalenamong normal ears, particularly those reporting 100% prelence. These concern the criteria for defining normal earsfor identifying TEOAEs.

First, most prevalence studies of normals have exclusubjects with ear-related irregularities, even if they have nmal HTLs. These exclusion criteria have included historyear disease, exposure to noise, exposure to ototoxic agupper respiratory tract infection at the time of testing, aminor otoscopic aberrations. Bonfilset al. ~1988b! also re-quired stapedius reflex thresholds to be normal. On the ohand, Vedantam and Musiek~1991! merely required thatsubjects ‘‘were without otologic or hearing complaints’’ anthat middle-ear compliance was 0.4 mmho or greater,Reshefet al. ~1993! only required that their subjects werfree of ‘‘middle-ear problems.’’ While it is not establishewhether these factors influence TEOAEswithout affectingthresholds, it is possible that prevalence figures are dedent on selection criteria additional to HTL.

Second, authors have differed in their criteria for normHTL, and group thresholds may have varied substantiamong studies. Stevens~1988! specified an upper limit baseon mean HTL~0.5, 1, 2, and 4 kHz! of 20 dB, whereasBonfils et al. ~1988b! required HTLs for all frequencies~0.25, 0.5, 1, 2, 4, and 8 kHz! to be 10 dB or better. Thisstrict criterion also applied to 70% of the normal earsBonfils et al. ~1988a!, representing subjects below the age40 years.~For subjects between 40 and 50 years and betw50 and 60 years, who also all had emissions, thresholdsreported as being normal relative to the subject’s age, buonly reported as means for the two groups.!

Third, the criteria for deciding whether an emissionpresent or absent may vary between studies. Most ofabove studies appear to have made this decision primarilthe basis of subjective rating by experienced scorers. Sscorers presumably take a combination of factors intocount, and can more readily allow for contaminating noand discount subtle artifacts that can influence most obtive scoring schemes~Stevens, 1988; Lutman, 1993Salomonet al., 1993a!. Even when objective measures suas cross correlation between a pair of replicate TEOwaveforms are used, lack of standardization between difent probes, recording equipment, and methods of calculamakes direct comparisons among studies questionable.situation is further complicated by differences between~a!those measurement techniques that allowonly the derived‘‘nonlinear’’ component of the TEOAE to be recorded ananalyzed, and~b! those that record and store a set of ra~often termed ‘‘linear’’! emission waveforms from whichnonlinear component can be derived in addition to the lincomponents.4

In reviewing the available literature, and notwithstaning the reports of failure to measure TEOAEs in some nmal ears, Probstet al. ~1991! state ‘‘it is likely that all nor-mal ears have transiently evoked otoacoustic emissions wtested carefully with specialized laboratory equipment.5

They suggest that TEOAEs are a general property ofnormal human peripheral auditory system and point to te

3567 J. Acoust. Soc. Am., Vol. 101, No. 6, June 1997 S. Kapadia an


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nical reasons as being responsible for reports of ‘‘abseTEOAEs in normal ears. This proposition is scientificaparsimonious and accounts for~a! the weight of evidencethat prevalence in normal ears is very close to 100%, and~b!the theoretical understanding of the commonality of the bmechanical processes which underlie normal cochlear setivity and the generation of TEOAEs. Given the statisticimpossibility of establishing that all normal ears haTEOAEs, it is reasonable to adopt this proposition, in tabsence of clear evidence to the contrary. However, if it wshown convincingly that TEOAEs can be absent in soears under good recording conditions, despite normal HTthe proposition would fail. Such a finding would be impotant to the understanding and modeling of cochlear acand mechanical processes. If normal cochlear sensitivityoccur without TEOAE generation, then there must be at lea partial dissociation of the processes leading to normal ssitivity and to the generation of TEOAEs.

The aim of the present work was to search for ears wnormal HTLs but no evidence of a TEOAE. To increase tprobability of finding such ears, a large sample was tesunder well-specified laboratory conditions. In so doing, tstudy would also establish a reliable estimate for the prelence of TEOAEs, which would have value for setting tupper limit of specificity that could be achieved by heariscreening programs based on TEOAEs. As a by-prodsubjects without TEOAEs, but with normal HTLs, would bidentified for further detailed study into the reasons for thabsent TEOAEs. If no such subjects were identified, ewith weak TEOAE would be identified for similar purpose

I. METHODS

A. Subjects

Potential subjects were drawn from two main sourcesone group from research, clinical and support staff workat the authors’ institute and associated clinical departmeand the second from students at the attached university. Sjects in the second group were paid for participating instudy. This approach avoided the potentially biased samthat would occur by testing patients attending an audioloclinic, but found to have normal HTLs. Written informeconsent was obtained from all subjects in the study.

As the main aim of the study was to search for ears wboth normal HTLs and absent TEOAEs, ears could becluded from the search as soon as it was discovered thathad either TEOAEs or abnormal hearing. In view of the larnumbers to be tested, the following strategy was adoptedthe sake of efficiency. Ears were excluded from the searcany of three stages, arranged in order of ease of implemtation: self-reported hearing difficulty, then TEOAE screeing, and finally follow-up test sessions which included dtailed TEOAE testing and audiometry.

Self-reported hearing status was ascertained initiallyan interview where subjects were asked if they had any hing difficulties, such as in using the telephone or in othday-to-day activities. All ears for which no such difficultiewere reported were classed as ‘‘presumed normals’’went on to be screened for TEOAEs. Any ears that ga

3567d M. E. Lutman: Otoacoustic emissions and normal thresholds


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weak or absent emissions were then tested by audiomand those with HTLs outside the criteria given below weeliminated from the search. In addition, a subgroup of ewith normal emissions also underwent audiometry for ctrol purposes~see Sec. III!. This contingent approach obvated audiometry in most presumed normals and affordednificant economies of test time. However, it meant it wuncertain whether all subjects with TEOAEs had normHTLs. This was of no consequence to the main propositexamined by the study, but entails that our prevalence emate based on ‘‘presumed normals’’ rather than verified nmals contains a degree of uncertainty. Section III addresthis issue and demonstrates that the degree of uncertainnegligible, as was obvious from the outset.

In all, 203 subjects attended the initial interviews. Twsubjects reported unilateral hearing loss verified by priordiological testing and these two ears were excluded. T404 ‘‘presumed normal’’ ears from 203 subjects wescreened for TEOAEs. Of these, 7 ears of 5 subjects wfound at audiometry to have HTLs outside the study criteand were hence eliminated from the analysis, leavingears from 201 subjects. These 397 ears will be referred tthe basic test group of the study. Of the basic test group,ears~58%! were from female subjects. Subject age rangfrom 18.2 to 59.6 years. Table I shows the age distributiof the 201 subjects, for males and females separately.

B. Audiometric criteria

Audiometric thresholds were determined at 0.25, 0.52, 3, 4, 6, and 8 kHz. Normal hearing was defined by aconduction HTLs no greater than 20 dB at any test frequebetween 0.25 and 4 kHz. These frequencies were chobecause TEOAEs do not tend to have frequency componabove about 5 kHz~Probstet al., 1991!—indeed most re-cording systems, including the one used here, have bwidths limited to about 5 kHz.

C. Equipment

TEOAEs were measured using the Programmable Ocoustic Emission Measurement System~POEMS! describedby Cope and Lutman~1988!, which was run in its ‘‘auto-matic’’ mode. This equipment comprises a probe containa miniature earphone and microphone, a click generasystem, preamplification, and signal conditioning circuit

TABLE I. Age distributions for female and male subjects in the basic tgroup.

Age band~years!

Male Female

N % N %

10–20 19 22 21 18

20–30 45 53 59 51

30–40 13 15 25 22

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all controlled by a personal computer with time-domain aeraging software. It has been widely used in researchclinical practice in the U.K.

Unipolar ~condensation! clicks, obtained by applyingrectangular pulses with a duration of 100ms to the probeearphone, were presented at a rate of 40/s. Click levels ufor each test were 70, 60, and 50 dB peak-equivalent~pe!SPL, as measured at the reference microphone in a ‘‘2-coupler conforming to IEC 126. The measurement systincorporates an overload rejection facility, which eliminatraw time records that contain any sound-pressure amplituwhich exceed preset limits, as can occur due to submovement or breathing noises. The remaining ‘‘good’’ timrecords are then averaged. The overload rejection limits wset for each individual test, at a level which would rejeabout 5% of all raw time records. This statistical schemean effective way to improve signal-noise ratio for a givnumber of averages, and was preferred to an arbitrary ficriterion equal for all subjects.

One thousand ‘‘good’’ time records were interleavinto two separate averaging buffers at each click level. Ttime records corresponded to the period from 4 to 20following the click. The click waveform generated in eacear was also recorded by separately averaging two reptions of 100 time records each, starting at electrical clonset, for a click level of 50 dB pe SPL.

Where audiometry was performed, a clinical audiome~Grason-Stadler GSI 16 fitted with TDH-50 earphones! cali-brated according to ISO 389 was used.

D. Procedure

All TEOAE measurements were performed by the fiauthor, who is experienced in the measurement of emissiSoft plastic eartips were used to secure the measuremprobe in the ear canal. Close attention was paid to the setion of tip size, the placement of the probe, and the routingthe probe lead such that it was not in contact with the sject’s body or chair. Subjects were seated comfortably insa sound-isolated booth, with the tester and the main partthe emission recording system outside the booth. Subjwere asked to avoid swallowing and to remain as still arelaxed as possible while measurements were made. Atconclusion of the recording in each ear, the position ofprobe in the subject’s ear canal was checked. In the evenany probe slippage apparent to the tester or reported bysubject, or if any significant subject movement during tmeasurement had occurred, a repeat recording wasformed after refitting the probe and reinstructing the subjeIn all such instances both sets of recordings were analyand the clearer recorded emission was taken as the resuthat ear for that test session.

II. RESULTS

A. Preliminary analysis

The nonlinear or saturating component of the TEOAwas computed by extracting a pair of ‘‘nonlinear’’ waveforms from the pairs of replicate ‘‘linear’’ waveforms measured at 70 dB and 60 dB pe SPL. The original linear

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sponses at 70, 60, and 50 dB pe SPL were preservedavailable for further analysis.6 This contrasts with the morecommon practice of only preserving the nonlinear comnent.

Cross correlation coefficients between replicate linwaveforms measured at 70, 60, and 50 dB pe SPL, andbetween the derived nonlinear pair, were computed for thto 16-ms segments. This time window avoids potenstimulus artifacts that can occur at the start of the wavefoand potentially poor signal-noise ratio at the end.

Historically, the identification of TEOAEs has relieheavily on expert visual evaluation of the measured waforms. Although such approaches may be less prone tovious errors than are simple objective means of identifica~Stevens, 1988; Lutman, 1993; Salomonet al., 1993a!, vi-sual scorers may differ where marginal judgements are tomade. Thus objective means of identification are importfor comparisons between different studies. We have baour prevalence estimate on the cross correlation betweenlicate nonlinear waveforms (r nl). Nonetheless, we recognizits potential shortcomings and have also utilized expertsual rating.

The cross correlation measurer nl has been widely usedin the analysis of TEOAEs~e.g., Kempet al., 1986; Stevens1988; Harris and Probst, 1991; Prieveet al., 1993!. Its use isalso supported by our previous work that attempted to demine reliable objective scoring methods to be used insteavisual rating~Lutman, 1993!. Of several measures used sigly and in combination, none was a more reliable predicof visual scoring thanr nl ~using the 6–16 ms time segmen!.In the present study the calculation of the correlation coecient was preceded by off-line high-pass filtering of the msured waveforms, in order to reduce the influence of lofrequency noise. Tognolaet al. ~1995! have confirmed thevalue of post hochigh-pass filtering as an aid to TEOAidentification. Waveforms yielding values ofr nl below 0.5were classified as ‘‘fails’’~emissions absent or questionab!and those withr nl greater than or equal to 0.5 as ‘‘passe~emissions present!. A criterion value of approximately 0.5has been reported by others~e.g., Kemp et al., 1986;Stevens, 1988!, and is currently widely used in many cente~Dirckx et al., 1996!, although differences between test sytems and choice of waveform time segments mean that eequivalence is not assured. We did not attempt to discrinate between ‘‘absent’’ and ‘‘questionable’’ TEOAEs bason an arbitrary value ofr nl , none having received generacceptance in the literature.

All visual rating was performed independently by thsecond author~who has similarly rated several thousand suwaveforms in various studies!. Sets of waveforms from the‘‘screening’’ test sessions were classified simply‘‘passes’’ ~i.e., TEOAEs present! or ‘‘fails’’ ~TEOAEs ab-sentor questionable!, taking all original and derived nonlinear replicate pairs into account. Waveforms recorded inrepeat test sessions were rated in more detail using a sligmodified version of the five-point subjective rating systedescribed previously by Lutman~1989!. For the presentstudy, only three rating categories were used: ‘‘absen‘‘questionable,’’ and ‘‘present.’’ These correspond to the r



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To illustrate the above analyses and to provide a framwork for discussions to follow, Fig. 1 shows a typical setclear TEOAEs measured in the present study. The figshows the measured replicate responses to clicks at 70and 50 dB pe SPL and the replicate nonlinear responses@la-beled NL# derived from the responses to the clicks at 70 a60 dB pe SPL. The nonlinear waveforms are calculated sthat linearly scaling components~in the corresponding measured responses! cancel, while the amplitudes of fully saturated components are exactly preserved. Partially saturcomponents are reduced in amplitude, but do not cancel

Many of the features commonly exhibited by TEOAEare seen in the waveform set of Fig. 1.

~i! The replicate waveforms are highly correlated.~ii ! A recognizably similar waveform pattern occurs in a

four replicate pairs.~iii ! A degree of frequency dispersion occurs, such th

higher-frequency components tend to occur earland lower-frequency components later.

~iv! Comparing traces labeled 70 and 60 dB, the wavform amplitudes are almost equal from the middthrough to the end of the time records; that is, temission is largely saturated. This is reflected by tamplitude in this part of the waveform being much th

FIG. 1. TEOAE waveform pairs from an ear exhibiting clear emissioFour pairs of superimposed waveforms are shown; replicate waveform pfor click levels of 70, 60, and 50 dB pe SPL, and the nonlinear wavefopair derived from the waveform pairs for click levels of 70 and 60 dB. Thorizontal axis indicates elapsed time following delivery of the click. Twaveforms exhibit several features commonly seen in TEOAEs, whichdescribed in the text. The cross correlation coefficient between the nonliwaveforms, calculated for the time segment 6 to 16 ms (r nl) is 0.98.



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same in the nonlinear response. On the other handamplitude at the start of the waveform is clearsmaller in the 60-dB trace than in the 70-dB trace,is reflected in the substantially reduced amplitudethe corresponding part of the nonlinear waveform.

Our experience of conducting these measurementsgests that the period comprising the first 1–2 ms showneach waveform is often dominated by the tail of the clistimulus, rather than representing a true TEOAE. Howevin the example of Fig. 1, notice that total cancellation of tearliest part of the waveform does not occur in NL. Tresidual high-frequency component is possibly a shlatency TEOAE, but may be a small artifact arising frosystem nonlinearities. This component is well correlatedtween the replicate waveforms, and its existence illustrawhy excluding the first 6 ms of the time record is helpfwhen calculatingr nl . The r nl value obtained here is 0.98.

Figure 2 shows the waveforms obtained exactlyabove, but with the probe inserted into a hard-walled cavwith a volume of 0.5 ml. The waveforms show little evdence of correlated signals, other than a small, very-lofrequency component in the early part of the top trace, uwhich is superimposed a high-frequency signal similar toartifact referred to in Fig. 1. The waveforms would be rat‘‘absent’’ for TEOAEs; ther nl value obtained is 0.07. Similar recordings are obtained in ears with severe hearingpairment, albeit with greater noise having physiological ogin.

FIG. 2. TEOAE waveform pairs from a hard-walled 0.5 ml cavity. Tfigure layout is as for Fig. 1. The cross correlation coefficient betwnonlinear waveforms (r nl) is 0.07.



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B. Cross correlation coefficients between nonlinearwaveforms

Examination of the 397 ears of the basic test group aapplication of the cross correlation criterion to the initi‘‘screening’’ test measurements resulted in 11 ears classas ‘‘fails’’ ( r nl , 0.5). Of these 11 ears, 10 were tested insecond test session and the waveforms obtained againsified on the basis ofr nl . Of the ten sets of waveforms fromrepeat test sessions, three yieldedr nl values less than 0.5, anwere thus finally classified as ‘‘fails.’’ The remaining seveears passed at the second test session, which was condunder less time pressure and in a different test booth, whprovided better isolation at low frequencies. Prevalenbased onr nl is therefore 393 out of 396 ears, or 99.2%. Tcalculate this prevalence figure we have excluded the onethat gave anr nl value less than 0.5 upon initial testing, bdid not undergo a repeat test session and did not have Hchecked.

C. Results of visual rating

Of the 397 ears in the basic test group, 9 were rated‘‘fails’’ ~TEOAEs absent or questionable!, based on visualrating of the initial screening measurements. Eight of thnine were in the group similarly classified on the basisr nl above.~The remaining 388 that were rated as passescluded the ear that failed initially onr nl but was not retested.!All nine ‘‘fails’’ were tested in a second test session and twaveforms rated again. Of the nine second sets of waforms, nonereceived a rating of ‘‘absent,’’ and only tworating of ‘‘questionable.’’ Emissions in the remaining sevears were rated as ‘‘present.’’ Hence, the overall outcomeour evaluation of the 397 ears based on visual rating of blinear and nonlinear TEOAE waveforms is: TEOAE‘‘present’’ in 395 ears, ‘‘questionable’’ in two ears, and ‘‘absent’’ in zero ears. We were thus unable to identify a sinear in our sample in which the TEOAE waveform sshowed no evidence of an emission, having excluded ewith abnormal HTLs.

Table II lists the values ofr nl and the visual ratings fromboth TEOAE test sessions, for each of the 11 ears thatderwent a repeat test session as a result of ‘‘fail’’ classifitions from either scheme. The table demonstrates a satistorily high degree of correspondence between the tindependent assessment schemes. The repeat sessionare of main interest here, as they represent the finalcomes. It can be seen that the three ears finally classe‘‘fails’’ on r nl ~ears A, C, and D,r nl , 0.5! include one of thetwo results visually rated as questionable~ear A!, but not theother~ear B!. The waveforms from ears C and D are visuarated as having TEOAEs present, despite havingr nl valuesless than 0.5.

D. TEOAE waveforms for marginal results

Figures 3 and 4 respectively, show the two TEOAwaveform sets that were visually rated as ‘‘questionab~ears A and B!. Neither exhibits the extent of repeatabilitbetween replicate waveforms seen in the example of FigTo the extent that repeatable TEOAE-type waveforms

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present in Figs. 3 and 4, these are predominantly in the eparts of the ‘‘linear’’ waveforms recorded in response to thighest click levels and show a more or less uniform defrom the very start of the time records. A cautious interptation could be that these components represent unuslong-lasting ringing of the clicks rather than an emission, a

TABLE II. Visual ratings of waveform sets and cross correlation coecients between replicate nonlinear waveforms (r nl), for initial and repeatTEOAE measurements. Results are shown for each of the 11 ears thaderwent a repeat test session as a result of ‘‘fail’’ classification from eischeme.

Ear

Initial session Repeat session

Visual rating r nl Visual rating r nl

A absent/questionable 0.12 questionable 0.2

B absent/questionable 0.57 questionable 0.7

C absent/questionable 0.16 present 0.40

D absent/questionable 0.08 present 0.49

E absent/questionable 0.20 present 0.51

F absent/questionable 0.09 present 0.53

G absent/questionable 0.26 present 0.54

H absent/questionable 0.37 present 0.59

I absent/questionable 0.28 present 0.68

J present 0.49 present 0.81

K present 0.12 present 0.86

FIG. 3. TEOAE waveform pairs from repeat test session of ear A. Tfigure layout is as for Fig. 1. The cross correlation coefficient betwnonlinear waveforms (r nl) is 0.25.



rlyey-llydTEOAEs were therefore rated as ‘‘questionable’’ rather th‘‘present.’’ In the case of Fig. 4, although this early compnent is not completely cancelled in the nonlinear wavefo~thus accounting for the high value ofr nl!, it is also at alower frequency than is typical for a genuine TEOAE. Fnally, it should be stressed that the ‘‘questionable’’ ratinhere were not associated with poor test conditions, suchexcessive ambient or subject-generated noise. Neither owaveform sets which were rated ‘‘questionable’’ demostrated an unusually high level of noise compared withnorm for TEOAE waveforms recorded in this study.~Com-pare, e.g., Fig. 1 with Figs. 3 and 4.!

Figures 5 and 6, respectively, show the two TEOAwaveform sets from the repeat test sessions that yieldedr nlvalues less than 0.5, but which were visually rated as havemissions present~ears C and D!. Although the emissions inthese two ears are not as clear and repeatable as in thample of Fig. 1, in both cases a clear TEOAE, distinct frothe tail of the stimulus, can be seen.

Figures 3–6 represent TEOAE waveforms which arethe margins of detectability and serve to contrast the resof visual rating and classification onr nl . The reasons for thediscrepant results arising from these two approaches arecussed further in the next section.

Table III gives the HTLs for ears A–D, obtained on thsame days as the TEOAE waveforms shown in Figs. 3They confirm that the four ears met our normal audiomecriterion. Furthermore, barring ear D~in which the failure onr nl is most clearly erroneous!, thresholds were also withinnormal limits at 6 and 8 kHz.

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FIG. 4. TEOAE waveform pairs from repeat test session of ear B. Tfigure layout is as for Fig. 1. The cross correlation coefficient betwenonlinear waveforms (r nl) is 0.78.



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FIG. 5. TEOAE waveform pairs from repeat test session of ear C. Tfigure layout is as for Fig. 1. The cross correlation coefficient between nlinear waveforms (r nl) is 0.40.

FIG. 6. TEOAE waveform pairs from repeat test session of ear D. Tfigure layout is as for Fig. 1. The cross correlation coefficient betwenonlinear waveforms (r nl) is 0.49.



III. DISCUSSION

A. Prevalence of TEOAEs in normals

One aim of the study was to estimate the prevalenceTEOAEs in adult ears with normal hearing. Using the objetive parameterr nl to identify TEOAEs yields a prevalencestimate of 99.2%. The use of a cut-offr nl value of 0.5reflects a historical context of hearing screening, where this a deliberate bias toward failing~i.e., regarding TEOAEsabsent in! marginal cases. Further, being a relatively simpmeasure,r nl is also prone to recognizable errors~some ofwhich are discussed in Sec. III B below! in both sensitivityand specificity. Nonetheless it is a widely used basisidentifying TEOAEs, and we have adopted it for our prevlence estimates to facilitate comparisons across studHowever, ther nl criterion of 0.5 is inherently conservativewhich suggests we should also regard our prevalencemate as conservative, possibly underestimating theprevalence of TEOAEs in normal ears.

All ‘‘presumed normal’’ ears that were classified a‘‘fails’’ on r nl ~as well as those rated ‘‘questionable’’ ovisual rating! underwent audiometry. Therefore, such clasfications in our study could not be explained by undetechearing impairment. However, we did not perform audioetry on all ears that passed. It is a simple matter to demstrate by sensitivity analysis that even gross violations ofpresumption of normal hearing have only a minimal inflence on the prevalence estimate. For that purpose we pthat 20% of the presumed normal ears that passed onr nlclassification would not have met our audiometric criterio7

This would reduce the audiometrically normal sample to 3ears. Three of these gaver nl values below our TEOAE cri-terion, and hence the prevalence in the sample would315/318 instead of 393/396~99.1% rather than 99.2%!.Hence, the prevalence estimate is insensitive to our presution of normal hearing in ears not tested audiometrically.

As the TEOAE prevalence figure based onr nl is inher-ently conservative, and the value obtained is close to 10it is inappropriate to ascribe an upper confidence limit. Thwe have calculated a one-sided 95% confidence interval~CI!,extending from 100% down to a prevalence of 98.1%8

Given the large size of our sample and the resulting narconfidence interval on our prevalence estimate, it is likthat previous studies that obtained significantly lowTEOAE prevalence figures were conducted using systeprotocols, or analyses that result in poorer TEOAE sensiity. It is of course possible that future studies using mosensitive systems than ours might detect unambigu

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TABLE III. Hearing threshold levels for ears A–D.

Ear

Frequency~kHz!

0.25 0.5 1 2 3 4 6 8

A 5 5 5 15 0 0 10 5

B 0 0 5 15 5 210 10 20

C 0 25 25 0 10 0 10 10

D 25 5 20 15 5 20 30 35



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TEOAEs in 100% of a comparable number of ears. Tpresent study simply indicates the lower bound of populatprevalence of TEOAEs in normal adult human ears.

The two-stage testing protocol, with all ears that failon r nl classification from the initial screening sessions betested a second time, afforded a degree of security in assing marginal cases. In the majority of cases where measments were repeated, there was a reduction in the noise iwaveforms recorded in the repeat sessions, leading direto increased measures ofr nl . Subjects may have been bettable to remain physically still during the second test ssions, the need for this having again been reinforced.repeat tests were also conducted at a more leisurelyover extended sessions. This emphasizes the need for calaboratory measurement~coupled with the use of clearly defined criteria! in studies that seek to estimate the prevaleof TEOAEs.

B. Absence of TEOAEs

Cross correlation,r nl , is a somewhat arbitrary measufor the identification of TEOAEs, but compares well wivisual rating in most cases. However, in marginal casestwo methods can give discrepant results~Table II!. There-fore, when attempting to establish the absence of a recable TEOAE with certainty in exceptional cases, it is necsary to examine the limitations of both methods andcompare discrepancies. Part of the reason for discrepancthe superior ability of an experienced scorer to reject cerkinds of artifact, and also to identify an emission in a nowaveform. These two factors are illustrated in the TEOAwaveforms from ears B and D~Figs. 4 and 6! and are prob-ably largely responsible for the discrepant outcomes in thtwo ears. A further important difference between the visrating and the objective classification, as performed in tstudy, is the fact that the former makes use of all four waform pairs, while the latter uses only the derived nonlinewaveform pair. For this reason it is instructive to considwhat visual ratings may be given to the nonlinear wavefopairs alone in Figs. 5 and 6. These two waveform sets wvisually rated as having TEOAEs present, but yieldedr nlvalues less than 0.5. Arguably, TEOAEs would be ra‘‘absent’’ in both ears if based on the nonlinear waveforonly. Thus at least some of the discrepancy between thesual rating and the objective classification outcomes instudy is explicable in terms of the different information owhich these two assessment methods were based, ratheon the greater sensitivity of expert visual ratingper se. Thisreinforces our contention that the availability of lineTEOAE waveform data is important for the assessmenthe emission, regardless of the choice of assessment meThe same point has been made by other workers~e.g.,Salomonet al., 1993b!, in particular relation to measuremeof TEOAEs in neonates.

A fundamental reason for a poorer rating~visualor ob-jective! arising from evaluation of the nonlinear trace paalone in general is that TEOAEs in some subjects are sstantially nonsaturated at the stimulus levels used to dethe nonlinear waveform. The less saturated a waveform cponent, the greater its degree of cancellation in the deriva



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of the nonlinear waveform. Examination of Fig. 5 in particlar supports this explanation in the case of ear C. Pooratings may also arise from the reduction in signal-noise rainherent in the derivation of the nonlinear waveform~Kempet al., 1990!.

The preceding discussions raise the philosophical isof what exactly should be construed as representingTEOAE. Ideally, this would be according to the definitioused in the Introduction, the release or return of acouenergy from the cochlea into the ear canal, in response tacoustic transient. In practice~and particularly in measurements in human ears!, it is seldom possible to substantiathat a particular recorded signal is of cochlear origin.9 Inevaluating recorded waveforms, therefore, an operatiodefinition is required: for example, a repeatable signal thadistinguishable from the ringing of the stimulus click. Addtional features of the response, such as amplitude saturaand frequency-latency relationships, provide secondary gance, as discussed above. In our experience of thus evaing TEOAE recordings, however, a gray area in betweTEOAE ‘‘presence’’ and ‘‘absence’’ is inescapable, and whave been forced to admit a ‘‘questionable’’ category insual rating of waveforms.

On this basis, accepting that TEOAEs are present inrecordings from ears C and D~Figs. 5 and 6! seems justified,despite the lowr nl values. In the case of ears A and B, threpeatable components evident in the waveforms~Figs. 3 and4! cannot be dismissed unequivocally as stimulus artifactsummary, we are therefore unable to identify unequivocaany ears in our sample with normal HTLs but no evidenceTEOAE.

C. Theoretical implications

It has been suggested that the generation of TEOArequires an inherent, perhaps anatomical, irregularity althe basilar membrane~e.g., Wilson, 1980; Sutton and Wilson, 1983; Kemp, 1986; Furst and Lapid, 1988; Witet al.,1994!. This hypothesis implicitly allows for occasional findings of absent TEOAEs in normal ears, as rare occurrenof anatomically perfect cochleae might exist. Hypothesthat do not incorporate such irregularities require alternameans to allow for ‘‘anomalous’’ absences of TEOAEsthey exist.10 Such hypotheses may be simplified and mamore tenable by the removal of this requirement, if all nomal ears generate TEOAEs.

The frequency spectra of TEOAEs commonly exhiunexplained gaps, in that little emission energy is measuraat some frequencies of normal hearing, despite demonstion of stimulus energy at the same frequencies. Two brexplanations could be postulated for this observation:~a!Some areas of a normal cochlea are unable to geneTEOAEs; or~b! All areas of a normal cochlea can~and per-haps do! generate TEOAEs, but interactions or other inflences suppress emissions of some frequencies.11 Alternative~a! is more consistent with the notion of TEOAEs beingenerated by anatomical irregularities and would also sgest that normal cochleae which do not generate TEOAmight exist. To the extent that we were unable to dem



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strate clear examples of such ears, our findings would tensupport alternative~b!.

We chose at the outset of the study not to apply asubject exclusions other than those based on air-conducthresholds. This contrasts with some earlier studies, as npreviously, in which subjects were excluded due to factsuch as past ear disease, exposure to noise or ototoxic agelevated stapedius reflex thresholds, presence of otoscaberrations, or upper respiratory tract infection at the timetesting. We indeed wanted such conditions to be admissin our subject sample, for the very purpose of investigattheir influence on TEOAE prevalence. The finding that vtually all of the 397 ears in our basic test group demonstraTEOAEs shows that any such minor auditory factors halittle effect on TEOAE prevalence, insofar as they may habeen present.

We also ignored HTLs at and above 6 kHz in applyiexclusions, in accordance with the broad consensusTEOAEs provide no information on HTLs at frequenciother than those present in the emission spectrum. THTLs at 6 kHz and above are not expected to have any diassociation with TEOAE prevalence. Indeed, some auth~Rutten, 1980; Johnsenet al., 1993! have concluded thaHTLs up to only 2 kHz are of primary importance to TEOAgeneration. Somewhat contrary to this view, Avan andworkers ~Avan et al., 1991; Avanet al., 1993; Avanet al.,1995! have suggested that damage to the basal region onthe cochlea~as evidenced by increased high-frequency putone thresholds! can reduce the amplitudes and alter twaveform patterns of TEOAEs in both guinea pigs ahumans.12 Additionally, Hauser et al. ~1991! comparedTEOAEs in ears with high-frequency sensorineural hearloss with those from normal ears, by analyzing amplitudesthe TEOAEs across emission frequency. They found lowTEOAE amplitudes in the ears with hearing loss, even atfrequencies of normal hearing. Were mild-to-moderate hifrequency hearing loss~corresponding to basal cochlear pthology! to influence TEOAE presence in humans, we mhave expected some absent emissions from the appmately 10% of our subject pool aged 40 to 60 years~TableI!. Our failure to detect such ears suggests that hearing lohigh frequencies alone~to the degree that may be expectedsubjects aged 40–60! does not materially affect TEOAEprevalence in humans. Not only did we fail to detect any ewith ‘‘absent’’ emissions that passed our restricted audmetric criterion, but the only two ears with ‘‘questionableratings had HTLs no greater than 20 dB at 6 and 8 k~Table III!.

In summary, we have found no clear evidence for a dsociation between the cochlear processes leading to noHTLs and to the generation of TEOAEs in responseclicks. It therefore seems likely that the condition of normHTLs is indeed sufficient to ensure TEOAE generation. Tquestion remains as to whether the low amplitudesTEOAEs occurring in some normal ears representsanomaly, or whether this can be explained on the basiother measures of auditory function or status. Further invtigation of the ears identified as having relatively weTEOAEs and suitable controls will attempt to answer th



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question, by gathering detailed measurements of other tyof otoacoustic emissions in the same ears, and by conduca range of other detailed measurements of auditory functThis should shed some further light on the general variatof otoacoustic emissions across ears and any associationother properties of hearing. Those studies may ultimathelp to answer the question why markedly different emisslevels can be recorded in ears with similar hearing threshlevels.

IV. CONCLUSIONS

~1! The prevalence of TEOAEs in normal adult eaidentified on the basis of the cross correlation between rlicate nonlinear waveforms, is estimated to be 99.2%, witone-sided 95% lower confidence limit of 98.1%. Within thrange of HTL accepted into the present study, up to 20 dBfrequencies between 0.25 and 4 kHz, any minor auditfactors that may have been present can have little effecTEOAE prevalence.

~2! This prevalence estimate is inherently conservatiCareful visual evaluation of the waveforms could not ruout TEOAEs in any ears.

~3! The amplitudes of TEOAEs, and hence the signnoise ratios of recordings, vary considerably across earsnormal hearing. Less sensitive measurement systems,ideal test conditions, or less cooperative subjects may yprevalence figures somewhat lower than that reported hThe variation of TEOAE amplitude across audiometricanormal ears may arise from aspects of auditory function tare not evident in pure-tone air-conduction thresholds. Fther research is required to explore this possibility.

~4! We were unable to identify any ear in our normsample that unequivocally lacked TEOAEs, and are thereunable to reject the scientifically parsimonious propositthat normal HTLs are a sufficient condition for TEOAE geeration.

ACKNOWLEDGMENTS

We thank Pauline Smith and Melanie Ferguson for thadvice and help over the duration of this study, and our sjects for their cooperation and patience. The manuscriptmuch improved by the comments of Mark Haggard and APalmer, and the statistical advice of David Marshall aAdrian Davis. This work was supported in part by DefeatiDeafness~formerly Hearing Research Trust!, 330/332 Gray’sInn Road, London WC1X 8EE.

1There have also been many reports of TEOAE prevalence in healthynates~e.g., Stevenset al., 1987; Bonfilset al., 1988c; Johnsenet al., 1988;Kok et al., 1993; Whiteet al., 1994!, that have reported prevalences of thorder of 95%–97%. However the major difficulties in ensuring goodcording conditions and in accurately ascertaining HTLs mean prevalereports of less than 100% are difficult to interpret.2A notable exception is the study by van Dijk and Wit~1987! who reportedthe markedly low figure of 40%. It has been suggested by Probstet al.~1991! that this low figure was largely due to technical limitations of thequipment used in that study.~Relevant technical limitations include poosensitivity of the recording apparatus to low-level TEOAEs, and inadequrejection or reduction of extraneous noise.! Other studies that showedprevalence figures substantially less than 100% may have been simlimited. Furthermore, some recent studies~e.g., Prieveet al., 1993! have



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involved testing under ‘‘typical clinical conditions,’’ rather than ideal labratory situations, and lower apparent prevalence figures in those stumight be expected due to contamination of weak emissions by extrannoise.3Small sample size results in greater uncertainty attached to a concluthat all normal ears demonstrate TEOAEs, than to a conclusion that snormal ears lack TEOAEs. For example, if the true population prevaleis 97%, the probability of finding emissions inall ~100%! of a randomsample of 50 ears is 0.22~0.97 raised to the power of 50!. Hence, about onein five studies of that size would be expected to show 100% prevalepurely on statistical grounds. For the probability of obtaining a samprevalence of 100% to be, 0.05, when the true population prevalence~say! 99%, it is necessary to test a random sample of at least 300 ear4One approach to comparing the performance of different systems of recing and rating is by examination of what is analogous to the sensitivspecificity trade-off for screening tests. Thus in evaluating the prevalefigures in normals yielded by different systems, one could also compercentage prevalence of TEOAEs found inhearing-impaired subjects.@Prieveet al. ~1993! address this point in some detail, in a study aimedoptimally separating normal and hearing-impaired subjects under clinconditions.# To illustrate, Reshefet al. ~1993! found a 100% prevalence oTEOAEs in their normal ears at click levels of 70 dB SPL and also repoas many as 80% of ears with noise-induced hearing loss registering esions at this click level. Emissions were identified by subjective ratingtheir study: More conservative rating could possibly have yielded loprevalence figures in both subject groups. In contrast, Stevens~1988! foundprevalences of 97% in his normals and only 7% in a group of hearimpaired ears. Although hearing losses were probably more severe ingroup than in the hearing-impaired group of Reshefet al. ~1993!, the largedifference in prevalence of emissions in impaired ears reported in thesestudies may also be a reflection of differences in the subjective racriteria. ~Neither author presents examples of poor emission wavefofrom normal ears, which may help address this issue.!5Probstet al. ~1991! also suggest that in some ears TEOAEs evokedclicks may be difficult to detect, whereas the use of tone-burst stimuli mresult in clearer emissions.6Although a measured TEOAE response may be regarded as contalinear and nonlinear components~Kempet al., 1986! a convention amongmany authors~e.g., Grandoriet al., 1993; Salomonet al., 1993a! is todenote the responses actually measured~at various stimulus levels! as ‘‘lin-ear’’ responses. The ‘‘nonlinear’’ response is then derived from the ‘‘lear’’ responses at two different stimulus levels.7In fact, a total of 49 of the presumed normal ears that passed on TEOclassification viar nl also underwent audiometry, and only 3~6%! of thesedid not meet the study’s audiometric criterion.~These 3 were, of courseexcluded in the figure of 397 for our basic test group.!8One qualification on the interpretation of this CI arises because nearly aour sample ears came from subjects from whom both ears were teMany properties of TEOAEs are significantly similar between left and riears of the same subject~Probstet al., 1986; Bonfilset al., 1988a; Jonhsenet al., 1988!. However, measures from one ear are not completely depdent on those from the other, and it is difficult to specify the degreecovariation between the two ears. Most studies~including the three citedabove and Bonfilset al., 1988b! have pooled the data from the two earstheir subjects. In the case of our sample, only three ears~from three differ-ent subjects! failed onr nl classification. Hence, we can make no inferencfrom these data, concerning associations between TEOAE presence iears and in right ears of the same normal subjects. Nevertheless, were-estimate our CI to examine the extreme possibility of complete dedence between the two ears by considering results from only left orright ears. As all three ears which failed onr nl happened to be left, differen95% confidence limits are obtained, namely 96.2% for left and 97.5%right ears.9Tests of physiological vulnerability of a recorded signal, for example,exposure of subjects to noise or low doses of aspirin, were beyondscope of this study. Cochlear origin could also be indicated if the sigcould be suppressed by additional acoustic stimulation. However, althowe did not attempt such procedures in this study, our experience from oongoing work is that ipsilateral acoustic stimulation effects little supprsion of TEOAEs that are of low level to begin with.10Indeed, the original hypothesis of Kemp~1978! was that ‘‘impedancediscontinuities’’ arose due to the response of the basilar membrane. S~1989, p. 44! and Shera and Zweig~1993, footnote 2! also speculate onTEOAE generation without mechanical irregularities.



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11A localized TEOAE generation process~with place-frequency mapping! isimplicit under alternative~a!. In the case of alternative~b!, the generationprocess for a given TEOAE frequency component may be either locadistributed.

12Avan et al. ~1995! allow for two possible explanations for their data:~a!that TEOAEs are sensitive to damage to basal parts of the cochlea~whichcorrespond to higher characteristic frequencies!; or ~b! that TEOAEs mayindeed be sensitive to damage to those partsonly of the cochlea which aretuned to their frequencies, but that TEOAEs may be more sensitive tolocal damage than are the corresponding auditory thresholds. Our dission here applies equally to either hypothesis.

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are normal hearing thresholds a sufficient condition for click-evoked otoacoustic emissions?

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