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Neonatal hearing screening: A combined click evoked and tone burst otoacoustic emission approach
International Journal of Pediatric Otorhinolaryngology (2008) 72, 351—360
www.elsevier.com/locate/ijporl
Neonatal hearing screening: A combined click evoked and tone burst otoacoustic emission approach Vicky W. Zhang a,*, Bradley McPherson a, Bao-Xuan Shi b, Joyce L.F. Tang c, Buddy Y.K. Wong c a
Centre for Communication Disorders, The University of Hong Kong, Hong Kong SAR, China Department of Otolaryngology, Henan Provincial People’s Hospital, Zhengzhou, Henan, China c Department of ENT, Hong Kong Adventist Hospital, Hong Kong SAR, China b
Received 14 September 2007; received in revised form 20 November 2007; accepted 22 November 2007
KEYWORDS Click evoked otoacoustic emissions; Otoacoustic emissions; Tone burst otoacoustic emissions; Universal neonatal hearing screening
Summary Objective: This study evaluated an alternative transient evoked otoacoustic emissions method for screening hearing in newborn babies that may reduce the referral rate of initial screening. Methods: A total of 1033 neonates (2066 ears) from two hospitals were recruited. Subjects had their hearing screened in both ears using a combined approach–—both click evoked OAEs (CEOAEs) and 1 kHz tone burst evoked OAEs (TBOAEs). Results: 1 kHz TBOAEs were more robust than CEOAEs in terms of emission response level and signal-to-noise ratio (SNR) at both 1 and 1.5 kHz frequency bands. The prevalence rate for CEOAE and TBOAE responses in these two frequency bands was significantly different. The combined protocol significantly reduced the referral rate–—by almost 2 percentage points for first time screening. Conclusions: The implementation of a combined 1 kHz TBOAE/CEOAE screening protocol is a feasible and effective way to reduce referral rates, and hence false positive rates, in neonatal hearing screening programs. # 2007 Elsevier Ireland Ltd. All rights reserved.
1. Introduction * Corresponding author at: Division of Speech and Hearing Sciences, The University of Hong Kong, Room 544, 5F, Prince Philip Dental Hospital, 34 Hospital Road, Hong Kong. Tel.: +852 25890588; fax: +852 25590060. E-mail address: [email protected] (V.W. Zhang).
Click evoked otoacoustic emission (CEOAE) measures have gained widespread acceptance as a routine hearing screening procedure in many countries [1]. However, this technique still has limitations.
0165-5876/$ — see front matter # 2007 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ijporl.2007.11.010
352 Approximately 1—6% of newborns have bilateral or unilateral hearing loss [2—5]. However, neonatal CEOAE screening programmes generally show a referral rate of around 6% to more than 30% at the time of initial testing [3,6—9]. Hence the majority of positive cases are false positives. This is a drawback to any screening programme, as false positives may create unnecessary anxiety in parents, dampen enthusiasm for the screening program and give rise to burdens on the health care system [10—12]. In order to reduce the number of false positive cases, a multi-stage screening protocol has been recommended [6,13,14]. Infants who did not pass an initial otoacoustic emissions (OAEs) screening are retested for a second or third time. The retests may use the same OAE procedures or switch to auditory brain-stem evoked response (ABR)-based instrumentation. The ABR-based method provides information on the auditory pathway from the peripheral auditory system through to the brainstem auditory pathway, which is highly recommended for screening NICU infants. The combination of two screening methods may reduce the fail rate at discharge and the subsequent need for outpatient follow-up [8,15,16]. However, these protocols increase the economic burden on clinics, especially for those hospitals with high birth rates. In addition, ABRbased testing has a disadvantage of taking longer to perform and being more expensive than OAE screening [17,18]. Therefore, it is important for universal neonatal hearing screening (UNHS) programs to minimize initial false positive OAE results and to consider ways to improve OAE measurements. Among the factors leading to high referral rates in CEOAE screening, noise has been highlighted as the most intractable problem. Three key noise sources have been identified: instrumentation, environment and infant-related noises [19,20]. Among these three noise sources, infant noises produced by swallowing, snoring, heavy breathing, coughing and muscle movements are more difficult to exclude, and these phenomena can obscure CEOAE recordings, particularly in the 500—1500 Hz range [5,21,22]. Some UNHS programs recommend ignoring the low to mid frequency information collected from CEOAE screening, and determine pass/fail from a detectable OAE response in the mid to high frequency range only, typically at frequency bands centered from 2 to 4 kHz [23—26]. The rationale for this appears to be that most permanent sensorineural hearing loss will affect hearing acuity in the 2—4 kHz region. However certain hearing disorders, with low to mid frequency audiometric configurations, would be missed by these criteria [27—29].
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Fig. 1 CEOAE spectrums recorded by ILO V6 software from a normal hearing neonatal ear. Black depicts the evoked OAE response and grey color depicts the noise floor.
Therefore, it is preferable for neonatal hearing screening procedures to, at least, determine likely hearing deficit at 1 kHz in addition to examining higher frequency bands. However, a robust 1 kHz component of a CEOAE response is likely to be contaminated by low frequency noise in a normal hearing individual (e.g., Fig. 1) [30,31]. To resolve this, tone burst evoked OAEs (TBOAE) may be a promising supplement to the conventional CEOAE screening technique, since tone burst stimuli can elicit a more frequency-specific response [32,33]. In previous work, TBOAEs have been shown to provide a stronger response level with greater SNR than CEOAEs [34]. 1 kHz TBOAEs could be recorded clearly in healthy ears, and their test—retest reliability is comparable to that of CEOAEs [35,36]. Few studies have been carried out that use TBOAE techniques in newborn hearing screening. McPherson et al. [36] compared six passing criteria for transient evoked otoacoustic emissions (TEOAEs) screening, based on CEOAEs only, TBOAEs only, and four criteria using combined CEOAE results plus TBOAE data with different stimulus center frequencies. The 1 kHz TBOAE plus CEOAE procedure was the most effective screening tool in terms of a favorable pass/refer rate among the six pass/refer criteria sets. Compared with a CEOAE-only screening criterion, the CEOAE plus 1 kHz TBOAE procedure improved the pass rate from 79.2% to 86.3%. Similarly, the results of a related study [37] reported that a CEOAE plus 1 kHz TBOAE approach reduced the neonatal referral rate by 1.95% points compared to a conventional CEOAEonly protocol. A combined 1 kHz TBOAE/CEOAE
Neonatal hearing screening combined method protocol may better elicit a reliable OAE response in the lower frequency region, and assist in the reduction of high referral rates, and hence false positive rates, in neonatal hearing screening programs. The aims of this study were to evaluate the criteria of this combined protocol in a large group of neonates, and explore the feasibility of this combined method in a clinical universal hearing screening program.
2. Method 2.1. Participants A total of 1033 neonates (2066 ears) from well-baby nurseries were enrolled at the Henan Provincial People’s Hospital (HPPH; 559 neonates; 1118 ears) and the Hong Kong Adventist Hospital (HKAH; 474 neonates; 948 ears) between April 2006 and July 2007. Of these 53.4% were male and 46.6% were female. The babies were required to meet study inclusion criteria as follows: gestation between 37 and 42 weeks; older than 48 h and younger than 7 days; normal birth history and first 24 h after delivery; without apparent congenital defects; birth weight between 2.4 and 4.5 kg; APGAR scores between 8 and 10 and no history of high risk factors. High risk factors were family history of hearing loss; congenital perinatal infection; anatomical malformation of head or neck; hyperbilirubinaemia; bacterial meningitis; severe perinatal asphyxia; convulsions; prolonged aminoglycoside usage and intracranial hemorrhage. All the neonates were recruited into the research program after parents elected to participate on a voluntary basis.
2.2. Screening personnel A medical doctor with previous experience in newborn hearing screening and an audiologist conducted the TBOAE and CEOAE screening at HPPH and HKAH, respectively. The screenings took place at least twice a week at each hospital over an 18month period.
2.3. Procedures Any debris noted in the ear canal was removed using a cotton swab before inserting the OAE probe tip. The probe tip was checked for adequate fit and was refitted or changed as appropriate. Newborns were tested while in natural sleep or a quiet state. Both ears were tested and the ear, which was most easily accessible was tested first. CEOAE and 1 kHz TBOAE measurements were performed in a randomized
353 sequence in each ear. Parents were informed of the results based on the CEOAE-only screening outcomes and referred babies were rescreened within one month of initial screening.
2.4. Apparatus and parameters All the measures were recorded in a non-sound treated room in the obstetrics department at each hospital. The average ambient room noise level with OAE equipment in operation was under 50 dBA. Each hospital used similar OAE equipment, an Echoport ILO 292 USB system with V6 software (Otodynamics Ltd., UK) installed in a laptop computer. A standard ILO system clinical neonatal probe was used and calibrated before every test session. CEOAE measurement used the ‘‘QuickScreen’’ mode with a response window of 12.8 ms, and the analysis window for the TBOAE mode was 20.48 ms. The recorded stimulus level of 75—80 dB equivalent sound pressure level (peSPL) in the ear canal was considered acceptable for both CEOAE and TBOAE measures. A tone burst stimulus with a 1 kHz center frequency was used to elicit a TBOAE response for each neonate. Response stopping criteria for both CEOAE and TBOAE measurements required at least 70 OAE quiet responses. The noise rejection level was generally set lower than 8 mPa (52 dB SPL). The data were analyzed using half-octave bands in ILO V6 software.
2.5. Pass/fail criteria A valid, passing CEOAE-only measurement was one that fulfilled the following CEOAE criteria: stimulus stability 75%; whole reproducibility 70%; at least three of five test frequency bands centered at 1, 1.5, 2, 3 and 4 kHz with signal to noise ratio (SNR) 3 dB. These criteria were a modified form of that used in the study of Dort [17], where CEOAE pass criteria were set as SNR 3 in four bands centered at 1.5, 2, 3 and 4 kHz with 70% reproducibility. For 1 kHz TBOAE screening in this study, pass was defined as stimulus stability 75%; whole reproducibility 60%; and SNR 3 dB at 1 and/or 1.5 kHz frequency bands. For those ears, which failed CEOAE testing, the screening outcome was still considered as pass if the combined 1 kHz TBOAE/CEOAE protocol fulfilled the criteria listed in Table 1.
2.6. Statistical analysis The analyses for CEOAE and TBOAE measurement included overall mean response level, overall mean reproducibility, test duration and the mean response level, SNR and prevalence rate for 1, 1.5
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Table 1 Screening criteria for combined 1 kHz TBOAE/CEOAE approach Recorded parameters
Combined approach pass criteria
Stimulus stability Reproducibility SNR
CEOAE
TBOAE
75% 70% At least two of three test frequency bands centered at 2, 3 and 4 kHz with SNR 3 dB The total number of passed frequency bands for CEOAE plus 1 kHz TBOAE screening 3
75% 60% SNR 3 dB at 1 and/or 1.5 kHz frequency bands
and 2 kHz frequency components. TBOAE measures were also compared with CEOAE results using a paired-samples t-test. x2-test was used to compare the differences in referral rate between CEOAE-only and combined TBOAE/CEOAE protocols. The data set were extensively analyzed to determine whether the combined approach significantly reduced the number of referral cases. Statistical analyses were performed using SPSS for Windows version 12.0 software. The statistical significance was set at P < 0.05.
3. Results In total 1033 babies (2066 ears) without any risk factor for hearing disorder were included in this analysis. Response levels were averaged in dB SPL. A 1 kHz tone burst stimulus usually could evoke a TBOAE response in the 1—2 kHz frequency range, using a half-octave analysis. Therefore, the analyses of mean emission response, SNR and prevalence rate included results at 1, 1.5 and 2 kHz half-octave bands. The mean recorded stimulus levels for both CEOAE and TBOAE measurements were nearly identical in the present study–—78.77 dB peSPL (S.D. = 1.85) and 78.54 dB peSPL (S.D. = 1.96), respectively.
3.1. Analyses for CEOAEs and TBOAEs
other researchers [36,38—41] in neonatal and young infant hearing screening programs. The overall mean response level and the overall mean reproducibility for the recorded 1 kHz TBOAEs were 13.52 (S.D. = 19.64) and 66.0% (S.D. = 26.1), respectively. These two values were similar to previous findings for neonatal TBOAE recordings [36,37]. The mean response for CEOAEs and TBOAEs at different frequency bands is illustrated in Fig. 2. The statistical analysis indicated that TBOAE responses were significantly greater than in comparable frequency regions for CEOAE responses, at both the 1 kHz (t = 60.85, P < 0.05) and 1.5 kHz component regions (t = 91.49, P < 0.05). Comparative analysis of SNR also showed that 1 and 1.5 kHz components of CEOAE measurement were significantly lower than those of TBOAEs (at 1 kHz: t = 21.98, P < 0.05; at 1.5 kHz: t = 15.58, P < 0.05) (Fig. 3). At the 2 kHz frequency band, the mean response and SNR of CEOAEs were significantly higher than those for TBOAEs (for mean response: t = 15.42, P < 0.05; for mean SNR: t = 61.27, P < 0.05).
3.2. Prevalence rate for CEOAE and TBOAE at selected frequencies Based on the initial CEOAE-only screening outcomes, the total of 1033 neonates (2066 ears) were divided into pass (1872 ears) and refer groups (194
Some of the recorded variables for CEOAE and TBOAE measurements are listed in Table 2. The CEOAE results were similar to those obtained by Table 2 Recorded variables for CEOAE and TBOAE measurement (n = 2066 ears) Parameters
CEOAE
Test duration (s) Reproducibility (%) Stimulus stability (%) Response level (dB SPL)
43.05 29.81 51.76 30.91 83.21 19.88 66.07 26.10 97.40 7.48 95.55 9.87 17.00 12.25 13.52 19.64
Mean
TBOAE S.D.
Mean
S.D. Fig. 2 Comparison of mean response level for CEOAE and 1 kHz TBOAE at 1, 1.5 and 2 kHz frequency bands (n = 2066 ears). The solid line depicts the mean TBOAE response. The dashed line depicts the CEOAE response.
Neonatal hearing screening combined method
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Fig. 3 Comparison of SNR for CEOAE and 1 kHz TBOAE at 1, 1.5 and 2 kHz frequency bands (n = 2066 ears). The solid line depicts the SNR of TBOAE. The dashed line depicts the SNR of CEOAE.
ears). Fig. 4 illustrates the prevalence rates for CEOAEs and TBOAEs at 1, 1.5 and 2 kHz frequency bands among different groups. For the overall data, the prevalence rates for TBOAEs were significantly greater than those for CEOAE at both the 1 kHz (x2(1) = 218.74, P < 0.05) and 1.5 kHz (x2(1) = 5.46, P < 0.05) frequency bands. In the pass group, the 1 kHz tone burst elicited a response in 1167 ears (62.34%), but in only 694 ears (37.07%) did the CEOAE stimulus evoke a 1 kHz frequency band response. In the 1.5 kHz frequency band, the prevalence rate was 90.06% (1686 ears) for TBOAEs and 86.75% (1624 ears) for CEOAE measurement.
A x2-test also indicated that differences between these two measurements were significant in both the 1 kHz (x2(1) = 239.04, P < 0.05) and 1.5 kHz (x2(1) = 9.35, P < 0.05) frequency ranges. In the refer group, only 5 ears (2.58%) out of 194 failed ears gave an evoked response in the 1 kHz range of the CEOAE response, and 9.28% (18 ears) in the 1.5 kHz range. The prevalence rates for a 1 kHz TBOAE response were significantly greater than those for a CEOAE response at these two frequency bands, with x2(1) = 15.46, P < 0.05 at 1 kHz and x2(1) = 20.15, P < 0.05 at 1.5 kHz. The prevalence rate for TBOAEs in the 2 kHz frequency band was lower than that for CEOAEs in any of three groups (for overall data: x2(1) = 329.28, P < 0.05; for pass group: x2(1) = 465.97, P < 0.05; for refer group: x2(1) = 15.71, P < 0.05). Tables 3 and 4 indicate the relationship of individual screening outcomes for CEOAE and TBOAE measurements in the 1 and 1.5 kHz frequency bands. For the CEOAE pass group (Table 3), there was 61.7% (30.6% + 31.3%) and 90.9% (83.8% + 7.1%) agreement between the CEOAE and TBOAE results at 1 and 1.5 kHz, respectively. Table 3 also shows that 595 ears (31.8%) at 1 kHz and 117 ears (6.3%) at 1.5 kHz had a CEOAE fail result but the TBOAE measurement gave a pass result. For the CEOAE refer group (194 ears, Table 4), 12.9% (25 ears) at
Table 3 Relationship (numbers of ears and percentages) between the CEOAE and TBOAE screening outcomes at 1 and 1.5 kHz frequency bands in pass group (n = 1872 ears) Frequency bands (kHz)
CEOAE pass
CEOAE refer
Kappa value (k)
1
TBOAE pass TBOAE refer
572 (30.6%) 122 (6.5%)
595 (31.8%) 583 (31.1%)
0.28
1.5
TBOAE pass TBOAE refer
1569 (83.8%) 54 (2.9%)
117 (6.3%) 132 (7.1%)
0.56
Fig. 4 Prevalence rate of CEOAE and 1 kHz TBOAE at 1, 1.5 and 2 kHz frequency components in total ears (n = 2066 ears), CEOAE pass group (n = 1872 ears) and refer group (n = 194 ears).
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Table 4 Relationship (numbers of ears and percentages) between the CEOAE and TBOAE screening outcomes at 1 and 1.5 kHz frequency bands in refer group (n = 194 ears) Frequency bands (kHz)
CEOAE pass
CEOAE refer
Kappa value (k)
1
TBOAE pass TBOAE refer
1 (0.5%) 4 (2.1%)
25 (12.9%) 164 (84.5%)
0.02
1.5
TBOAE pass TBOAE refer
14 (7.2%) 4 (2.1%)
40 (20.6%) 137 (70.6%)
0.29
1 kHz and 20.6% (40 ears) at 1.5 kHz showed disagreement in the CEOAE and TBOAE outcomes. For both CEOAE pass and refer groups, Kappa values showed agreement between CEOAE and TBOAE was not good at both the 1 and 1.5 kHz frequency bands [42].
3.3. Analysis of overall pass rates for the two screening protocols For CEOAE-only screening, 1872 ears (90.61%) from 2066 neonatal ears fulfilled the pass criteria and 194 ears (9.39%) required referral. If screening were based on the combined criteria mentioned in Table 1, 40 additional ears from 194 CEOAE-only
Fig. 5
failed neonates would pass screening. The initial referral rate for screening using the combined criteria would reduce by 1.94 percentage points compared to the rate of the CEOAE-only criteria, a statistically significant difference (x2(1) = 5.021, P < 0.05).
3.4. Follow-up rescreening for positive cases Fig. 5 provides information on follow-up testing of the subject group. For the total 194 ears, which failed CEOAE screening, 109 ears (56.19%) were rescreened before discharge or within one month
Flowchart of the follow-up results of CEOAE failed group (n = 194 ears).
Neonatal hearing screening combined method post-discharge, including 2 ears that were retested in other hospitals. Of these, 86 ears passed at the second screening occasion. For those 154 ears which showed a refer screening outcome with both the CEOAE-only and combined approach at first time screening, there were 23 ears that still failed at the second screen, and 4 ears out of these 23 ears later failed diagnostic ABR at age 3 months. Further diagnostic test results have not become available. For the 40 ears that failed CEOAE-only screening but passed the combined protocol criteria, 33 ears have been retested. The outcomes showed that all of these ears finally passed the CEOAE rescreening (31 ears passed the rescreening at same hospital; 2 ears passed the rescreening at other hospitals). The remaining 7 ears could not be followed up.
4. Discussion With any screening procedure, it is desirable to have a test that is as accurate as possible. Babies who screen positive for hearing loss should have a hearing disorder and babies who screen negative for hearing loss should indeed have normal hearing. In China, for example, it has been reported that 1.46—2.64% of newborns have permanent sensorineural hearing impairment. Yet published referral rates of first time CEOAE screening are about 15% [3,4]. Therefore, improving the current CEOAE measurement protocol and achieving a lower referral rate are very important. The present study aimed to develop an improved 1 kHz TBOAE/CEOAE approach, and determine if this combined method could significantly reduce the referral rate during first time neonatal hearing screening.
4.1. OAE responses In the present study, the 1 kHz frequency component of the CEOAE response had a lower average response than other frequency components (Fig. 2). This trend was also found for CEOAE SNR analysis (Fig. 3). 1 kHz TBOAEs were more robust than CEOAEs in terms of emission response level and SNR at comparable frequency components, for both 1 and 1.5 kHz. This finding was consistent with other reports comparing TBOAEs and CEOAEs in both adult and newborn populations [5,31,35—37,43]. The values can be used as normative data for screening and diagnostic purposes in the neonatal population.
4.2. Screening outcomes In present study, SNR 3 dB was used as a criterion defining a detectable OAE response at each
357 frequency band. As shown in Fig. 4, only 33.83% and 79.48% of ears reached the SNR pass criteria for 1 and 1.5 kHz frequency components of the CEOAE assessment, compared with 57.74% and 84.12% of ears in TBOAE testing. The overall prevalence rates for CEOAE and TBOAE responses at these two frequency ranges were significantly different. The results also indicated that even in the CEOAE pass group (1872 ears), there were still 62.93% and 13.25% of ears that could not evoke a clear CEOAE response at 1 and 1.5 kHz, respectively. In the refer group, when using 1 kHz TBOAE data the number of passed ears was nearly 5 times that when 1 kHz CEOAE data was utilized. The percentage of ears passed by TBOAE testing was about three times higher than that when CEOAE test results at 1.5 kHz were used. In the 2 kHz frequency range, the prevalence rate elicited by a 1 kHz TBOAE was lower than that for the CEOAE stimulus. The mean response and SNR of CEOAEs were higher than those for TBOAE results in the 2 kHz frequency range. Therefore, a 1 kHz tone burst stimulus is more suitable than a broadband click stimulus when seeking restricted lower frequency information (lower than 2 kHz) in neonatal hearing screening. For individual outcomes in the refer group (Table 4), 25 ears (12.9%) at 1 kHz and 40 ears (20.6%) at 1.5 kHz were found that failed CEOAE but could pass TBOAE screening. After the follow-up rescreening, 33 out of 40 ears (82.5%) that failed CEOAE criteria but passed using the combined approach were confirmed with negative CEOAE results. A combined 1 kHz TBOAE/CEOAE test protocol may be a promising approach to reducing false positive rates in TBOAE screening, and hence contribute to more accurate and efficient UNHS programs. The overall pass percentage by ears for the CEOAE-only criteria in the present study was 90.61%, which is similar to the reports from other UNHS programs in their initial stages [44,45]. If the pass/refer determination had included 1 kHz TBOAE results, and set the criteria of this alternative combined approach as Table 1 mentioned, an additional 40 ears (20.6% of refer group) could have been detected with a clear OAE within the 1 k to 1.5 kHz bandwidth, improving the pass percentage for screened ears to 92.55%. The pass rate for the total number of screened ears would therefore have increased by 1.94 percentage points, a significantly lower referral rate than for the conventional CEOAE-only criteria. This may be an important benefit to a hearing health care system. For example, there are an estimated 20 million
358 children born in 31 cities/provinces of China each year1. About 1.87 million newborns may fail first time CEOAE screening (calculated using a 9.39% referral rate). Therefore, reducing the referral rate by 1.94 percentage points using combined approach would result in nearly 320,000 additional babies passing initial screening. This would greatly reduce the heavy follow-up burden on the health care system and also decrease parental anxiety.
4.3. Test duration In this study, the mean test duration for CEOAE measurement was 43 s per ear, and for 1 kHz TBOAE measurement it was 51.7 s. Hence, the combined screening approach takes about 2 min per ear. Including the additional preparation time in the test duration, the combined approach in the present study took about 6—8 min for both ears, which is less time-consuming than performing distortion product otoacoustic emission (DPOAE; 11:04 min) or automated ABR screening (18:50 min) [17]. With the development of an automatic, computerized technique time constraints could be further reduced for a combined CEOAE and TBOAE procedure. In addition, protocols could be developed that allow 1 kHz TBOAE testing to be considered with CEOAE screening only when clear lower frequency CEOAE responses could not be evoked. This may provide more information on lower frequency components of OAEs and improve pass rates (for CEOAE refer group), and thus reduce the overall refer outcomes from screening.
4.4. Cost In China, a routine clinical CEOAE or DPOAE screening test costs 40—80 Yuan2 according to region and equipment used. If ABR-based testing is included in a screening procedure, an additional 70—100 Yuan needs to be paid, often placing great financial pressure on parents. Also, OAE administration is comparatively straightforward and little extra screener training is needed. Therefore, the combined 1 kHz TBOAE/CEOAE approach may improve the accuracy and efficiency for first time screening by reducing the burdens on both the medical system and the family. For those ears which failed a combined CEOAE/TBOAE protocol diagnostic procedures could then be conducted.
1
http://www.moh.gov.cn/open/statistics/digest01/Tyf3156.htm. 2 1 USD 7.5 Yuan (August 2007).
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4.5. Limitations Some limitations of this study should be noted. Firstly, only 55.15% (107 ears) out of 194 failed ears participated in the follow-up rescreening procedures provided by HPPH and HKAH. An additional 2 ears from 2 neonates were retested at other hospitals. The proportion of retested ears was similar to a North American report [15], but was relatively lower than noted in other Chinese reports [3,4]. The high frequency of cases lost to follow-up is an important challenge for UNHS. Although they would improve the quality of UNHS screening programs, well integrated tracking systems and followup services are always not easy to conduct. For HPPH, the low follow-up rate may be due to it being a government hospital providing services to both urban and rural patients. Rural parents often have lower income and education levels, and may have lower awareness of the importance of hearing tests for their babies. Although the screener explained the value of neonatal hearing screening to parents, and all rescreening tests were free of charge, rural families may still not attend since transport and lost income costs still need to be borne by parents. Hong Kong is an important center for international finance and trade, with a large expatriate population. HKAH is a private hospital and has a patient population with middle to high income and education levels. Most patients have their own private health insurance and may choose to consult a clinic in a wide range of areas. This also makes follow-up retests difficult to monitor. Among the 40 ears, which failed the CEOAE criteria but passed the combined approach, there were still 7 ears from 7 neonates that had lost touch with us. Therefore, the actual overall false positive rate for all 40 failed neonatal ears could not be determined. In addition, due to the constraints in our ability to monitor diagnostic test results, the sensitivity and specificity of the combined CEOAE/TBOAE approach could not be evaluated in this study. The false negative rate for the combined approach could not been determined. A second limitation is that the current CEOAE measures used the ‘‘QuickScreen’’ mode with a response window of 12.8 ms, and the analysis window for TBOAE mode was 20.48 ms. These two parameters cannot be adjusted in V6 software. ‘‘QuickScreen’’ mode was used in the present study because this mode has been widely used in UNHS in China and internationally, and it was of benefit to compare the overall pass/refer outcomes for current CEOAE-only screening with results obtained in other studies. However, the shortened time window of the ‘‘QuickScreen’’ mode may also reduce the
Neonatal hearing screening combined method OAE response at 1 kHz, although the main purpose of this mode is to reduce noise contamination at lower frequencies.
5. Conclusion An evaluation of the 1 kHz TBOAE/CEOAE combined approach was conducted in this study. By providing supplementary information in the lower frequency region, fewer neonates required referral because neonatal ears, which failed CEOAE screening often, had a clear TBOAE response at the 1 and/or 1.5 kHz frequency band and were reassigned to the pass category. When compared with conventional CEOAE-only screening, the combined approach reduced the overall referral rate by 1.94 percentage points, and this was shown to be a significant improvement on the pass rate for CEOAE-only screening. Available follow-up rescreening results also confirmed that all tested ears, which failed CEOAE screening but passed the combined approach, were false positive cases. In addition, the ease of administration of an additional TBOAE test may reduce the need for major retraining for screening personnel. A combined 1 kHz TBOAE/ CEOAE measurement approach is a feasible way of reducing referral rates, improving the accuracy and efficiency for first time neonatal hearing screening, and may assist in furthering the long-term goal of universal, cost-effective screening for all infants.
Acknowledgements The authors wish to thank all the medical and nursing staff of the Obstetrics Departments at both Hong Kong Adventist Hospital and Henan Provincial People’s Hospital for their generous assistance during data collection. The work was fully supported by a grant from the Research Grants Council of the Hong Kong Special Administrative Region, China (HKU7434/04M).
References [1] B.O. Olusanya, W. Swanepoel de, M.J. Chapchap, S. Castillo, H. Habib, S.Z. Mukari, et al., Progress towards early detection services for infants with hearing loss in developing countries, BMC Health Serv. Res. 7 (2007) 14. [2] A. Erenberg, J. Lemons, C. Sia, D. Trunkel, P. Ziring, Newborn and infant hearing loss: detection and intervention. American academy of pediatrics. Task force on newborn and infant hearing, 1998—1999, Pediatrics 103 (1999) 527—530.
359 [3] W.Y. Nie, L.X. Gong, Y.J. Liu, L.L. Xiang, Q. Lin, Y.S. Qi, et al., Hearing screening of 10,501 newborns, Chin. Med. J. 83 (2003) 274—277. [4] Y.J. Nie, Y.S. Qi, X.T. Zhao, Z.H. Cai, Y.L. Yang, D. Tao, et al., Value of otoacoustic emission (OAE) technique in perinatal audiology, Chin. Arch. Otolaryngol. Head Neck Surg. 6 (1999) 207—211. [5] S.J. Norton, M.P. Gorga, J.E. Widen, B.R. Vohr, R.C. Folsom, Y.S. Sininger, et al., Identification of neonatal hearing impairment: transient evoked otoacoustic emissions during the perinatal period, Ear Hearing 21 (2000) 425—442. [6] P. Clarke, M. Iqbal, S. Mitchell, A comparison of transientevoked otoacoustic emissions and automated auditory brainstem responses for pre-discharge neonatal hearing screening, Int. J. Audiol. 42 (2003) 443—447. [7] A.B. Maxon, B.R. Vohr, K.R. White, Newborn hearing screening: comparison of a simplified otoacoustic emissions device (ILO1088) with the ILO88, Early Hum. Dev. 45 (1996) 171— 178. [8] B.R. Vohr, W. Oh, E.J. Stewart, J.D. Bentkover, S. Gabbard, J. Lemons, et al., Comparison of costs and referral rates of 3 universal newborn hearing screening protocols, J. Pediatr. 139 (2001) 238—244. [9] A. Ciorba, S. Hatzopoulos, L. Camurri, L. Negossi, M. Rossi, D. Cosso, et al., Neonatal newborn hearing screening: four years’ experience at Ferrara University Hospital (CHEAP project). Part 1, Acta Otorhinolaryngol. Ital. 27 (2007) 10—16. [10] M.J. Johnsen, A.B. Maxon, K.R. White, B.R. Vohr, Operating a hospital-based universal newborn hearing screening: program using transient evoked otoacoustic emissions, Semin. Hearing 14 (1993) 46—55. [11] G.T. Mencher, S.J. DeVoe, Universal newborn screening: a dream realized or a nightmare in the making? Scand. Audiol. 30 (2001) 15—21. [12] K.R. White, B.R. Vohr, T.R. Behrens, Universal newborn screening using transient evoked otoacoustic emissions: results of the Rhode Island hearing assessment project, Semin. Hearing 14 (1993) 18—29. [13] S. Iwasaki, Y. Hayashi, A. Seki, M. Nagura, Y. Hashimoto, G. Oshima, et al., A model of two-stage newborn hearing screening with automated auditory brainstem response, Int. J. Pediatr. Otorhinolaryngol. 67 (2003) 1099—1104. [14] K.R. White, B.R. Vohr, S. Meyer, J.E. Widen, J.L. Johnson, J.S. Gravel, et al., A multisite study to examine the efficacy of the otoacoustic emission/automated auditory brainstem response newborn hearing screening protocol: research design and results of the study, Am. J. Audiol. 14 (2005) 186—199. [15] Joint Committee on Infant Hearing, Year 2007 position statement: principles and guidelines for early hearing detection and intervention programs, Pediatrics 120 (2007) 898— 921. [16] J. Gravel, A. Berg, M. Bradley, A. Cacace, D. Campbell, L. Dalzell, et al., New York State universal newborn hearing screening demonstration project: effects of screening protocol on inpatient outcome measures, Ear Hearing 21 (2000) 131—140. [17] J.C. Dort, C. Tobolski, D. Brown, Screening strategies for neonatal hearing loss: which test is best? J. Otolaryngol. 29 (2000) 206—210. [18] S. Meier, O. Narabayashi, R. Probst, N. Schmuziger, Comparison of currently available devices designed for newborn hearing screening using automated auditory brainstem and/ or otoacoustic emission measurements, Int. J. Pediatr. Otorhinolaryngol. 68 (2004) 927—934.
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[19] P. Muller, M. Kompis, Evaluation of a noise reduction system for the assessment of click-evoked otoacoustic emissions, J. Acoust. Soc. Am. 112 (2002) 164—171. [20] G.R. Popelka, R.K. Karzon, R.A. Clary, Identification of noise sources that influence distortion product otoacoustic emission measurements in human neonates, Ear Hearing 19 (1998) 319—328. [21] K. Rhoades, B. McPherson, V. Smyth, J. Kei, A. Baglioni, Effects of background noise on click-evoked otoacoustic emissions, Ear Hearing 19 (1998) 450—462. [22] G. Tognola, P. Ravazzani, F. Grandori, An optimal filtering technique to reduce the influence of low-frequency noise on click-evoked otoacoustic emissions, Br. J. Audiol. 29 (1995) 153—160. [23] M.T. Huynh, R.A. Pollack, R.A. Cunningham, Universal newborn hearing screening: feasibility in a community hospital, J. Fam. Pract. 42 (1996) 487—490. [24] B.R. Vohr, L.M. Carty, P.E. Moore, K. Letourneau, The Rhode Island Hearing Assessment Program: experience with statewide hearing screening (1993—1996), J. Pediatr. 133 (1998) 353—357. [25] S. Hatzopoulos, G. Pelosi, J. Petruccelli, M. Rossi, V. Vigi, R. Chierici, et al., Efficient otoacoustic emission protocols employed in a hospital-based neonatal screening program, Acta Otolaryngol. 121 (2001) 269—273. [26] L. Spivak, L. Dalzell, A. Berg, M. Bradley, A. Cacace, D. Campbell, et al., New York State universal newborn hearing screening demonstration project: inpatient outcome measures, Ear Hearing 21 (2000) 92—103. [27] N. Gurtler, Y. Kim, A. Mhatre, C. Schlegel, A. Mathis, A.K. Lalwani, DFNA54, a third locus for low-frequency hearing loss, J. Mol. Med. 82 (2004) 775—780. [28] A.M. King, S.C. Purdy, H. Dillon, M. Sharma, W. Perce, Australian hearing protocols for the audiological management of infants who have auditory neuropathy, Aust. N. Z. J. Audiol. 27 (2005) 69—77. [29] R.J. Pennings, S.J. Bom, K. Cryns, K. Flothmann, P.L. Huygen, H. Kremer, et al., Progression of low-frequency sensorineural hearing loss (DFNA6/14-WFS1), Arch. Otolaryngol. Head Neck Surg. 129 (2003) 421—426. [30] S.J. Norton, M.P. Gorga, J.E. Widen, R.C. Folsom, Y. Sininger, B. Cone-Wesson, et al., Identification of neonatal hearing impairment: evaluation of transient evoked otoacoustic emission, distortion product otoacoustic emission, and auditory brain stem response test performance, Ear Hearing 21 (2000) 508—528. [31] D. Welch, K.A. Greville, P.R. Thorne, S.C. Purdy, Influence of acquisition parameters on the measurement of click evoked
[32] [33] [34]
[35]
[36]
[37]
[38]
[39]
[40]
[41]
[42] [43]
[44]
[45]
otoacoustic emissions in neonates in a hospital environment, Audiology 35 (1996) 143—157. J.W. Hall, Handbook of Otoacoustic Emissions, Singular, San Diego, Calif., 2000. D.T. Kemp, S. Ryan, P. Bray, A guide to the effective use of otoacoustic emissions, Ear Hearing 11 (1990) 93—105. R. Probst, B.L. Lonsbury-Martin, G.K. Martin, A review of otoacoustic emissions, J. Acoust. Soc. Am. 89 (1991) 2027— 2067. R.H. Chan, B. McPherson, Test—retest reliability of toneburst-evoked otoacoustic emissions, Acta Otolaryngol. 120 (2000) 825—834. B. McPherson, S.F. Li, B.X. Shi, J.L. Tang, B.Y. Wong, Neonatal hearing screening: evaluation of tone-burst and clickevoked otoacoustic emission test criteria, Ear Hearing 27 (2006) 256—262. V.W. Zhang, B. McPherson, B.X. Shi, J.L.F. Tang, An alternative method in neonatal hearing screening: click otoacoustic emissions plus tone-burst otoacoustic emissions, in: Paper presented at: XXVIIIth International Congress of Audiology, September 3—7, Innsbruck, Austria, 2006. J. Kei, B. McPherson, V. Smyth, S. Latham, J. Loscher, Transient evoked otoacoustic emissions in infants: effects of gender, ear asymmetry and activity status, Audiology 36 (1997) 61—71. A. Salamy, L. Eldredge, R. Sweetow, Transient evoked otoacoustic emissions: feasibility in the nursery, Ear Hearing 17 (1996) 42—48. Y.L. Yang, H.H. Sun, X.Q. Tang, Y.S. Qi, Y.J. Nie, L.S. Guo, et al., Transient evoked otoacoustic emissions and auditory brain stem response in full-term neonates, Chin. Arch. Otolaryngol. Head Neck Surg. 8 (2001) 131—134. Y.S. Chi, Y.J. Nie, Z.H. Cai, Y.L. Yang, D. Tao, The features of transient evoked otoacoustic emissions (TEOAEs) in full-term newborns, Acta Biophys. Sinica (Chin) 16 (2000) 66—72. B. Everitt, Statistical Methods in Medical Investigations, 2nd. ed., Edward Arnold, London, 1994. B.A. Prieve, M.P. Gorga, S.T. Neely, Click- and tone-burstevoked otoacoustic emissions in normal-hearing and hearing-impaired ears, J. Acoust. Soc. Am. 99 (1996) 3077—3086. D. Aidan, P. Avan, P. Bonfils, Auditory screening in neonates by means of transient evoked otoacoustic emissions: a report of 2842 recordings, Ann. Otol. Rhinol. Laryngol. 108 (1999) 525—531. H.S. Habib, H. Abdelgaffar, Neonatal hearing screening with transient evoked otoacoustic emissions in Western Saudi Arabia, Int. J. Pediatr. Otorhinolaryngol. 69 (2005) 839—842.
Available online at www.sciencedirect.com
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Neonatal hearing screening: A combined click evoked and tone burst otoacoustic emission approach Vicky W. Zhang a,*, Bradley McPherson a, Bao-Xuan Shi b, Joyce L.F. Tang c, Buddy Y.K. Wong c a
Centre for Communication Disorders, The University of Hong Kong, Hong Kong SAR, China Department of Otolaryngology, Henan Provincial People’s Hospital, Zhengzhou, Henan, China c Department of ENT, Hong Kong Adventist Hospital, Hong Kong SAR, China b
Received 14 September 2007; received in revised form 20 November 2007; accepted 22 November 2007
KEYWORDS Click evoked otoacoustic emissions; Otoacoustic emissions; Tone burst otoacoustic emissions; Universal neonatal hearing screening
Summary Objective: This study evaluated an alternative transient evoked otoacoustic emissions method for screening hearing in newborn babies that may reduce the referral rate of initial screening. Methods: A total of 1033 neonates (2066 ears) from two hospitals were recruited. Subjects had their hearing screened in both ears using a combined approach–—both click evoked OAEs (CEOAEs) and 1 kHz tone burst evoked OAEs (TBOAEs). Results: 1 kHz TBOAEs were more robust than CEOAEs in terms of emission response level and signal-to-noise ratio (SNR) at both 1 and 1.5 kHz frequency bands. The prevalence rate for CEOAE and TBOAE responses in these two frequency bands was significantly different. The combined protocol significantly reduced the referral rate–—by almost 2 percentage points for first time screening. Conclusions: The implementation of a combined 1 kHz TBOAE/CEOAE screening protocol is a feasible and effective way to reduce referral rates, and hence false positive rates, in neonatal hearing screening programs. # 2007 Elsevier Ireland Ltd. All rights reserved.
1. Introduction * Corresponding author at: Division of Speech and Hearing Sciences, The University of Hong Kong, Room 544, 5F, Prince Philip Dental Hospital, 34 Hospital Road, Hong Kong. Tel.: +852 25890588; fax: +852 25590060. E-mail address: [email protected] (V.W. Zhang).
Click evoked otoacoustic emission (CEOAE) measures have gained widespread acceptance as a routine hearing screening procedure in many countries [1]. However, this technique still has limitations.
0165-5876/$ — see front matter # 2007 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ijporl.2007.11.010
352 Approximately 1—6% of newborns have bilateral or unilateral hearing loss [2—5]. However, neonatal CEOAE screening programmes generally show a referral rate of around 6% to more than 30% at the time of initial testing [3,6—9]. Hence the majority of positive cases are false positives. This is a drawback to any screening programme, as false positives may create unnecessary anxiety in parents, dampen enthusiasm for the screening program and give rise to burdens on the health care system [10—12]. In order to reduce the number of false positive cases, a multi-stage screening protocol has been recommended [6,13,14]. Infants who did not pass an initial otoacoustic emissions (OAEs) screening are retested for a second or third time. The retests may use the same OAE procedures or switch to auditory brain-stem evoked response (ABR)-based instrumentation. The ABR-based method provides information on the auditory pathway from the peripheral auditory system through to the brainstem auditory pathway, which is highly recommended for screening NICU infants. The combination of two screening methods may reduce the fail rate at discharge and the subsequent need for outpatient follow-up [8,15,16]. However, these protocols increase the economic burden on clinics, especially for those hospitals with high birth rates. In addition, ABRbased testing has a disadvantage of taking longer to perform and being more expensive than OAE screening [17,18]. Therefore, it is important for universal neonatal hearing screening (UNHS) programs to minimize initial false positive OAE results and to consider ways to improve OAE measurements. Among the factors leading to high referral rates in CEOAE screening, noise has been highlighted as the most intractable problem. Three key noise sources have been identified: instrumentation, environment and infant-related noises [19,20]. Among these three noise sources, infant noises produced by swallowing, snoring, heavy breathing, coughing and muscle movements are more difficult to exclude, and these phenomena can obscure CEOAE recordings, particularly in the 500—1500 Hz range [5,21,22]. Some UNHS programs recommend ignoring the low to mid frequency information collected from CEOAE screening, and determine pass/fail from a detectable OAE response in the mid to high frequency range only, typically at frequency bands centered from 2 to 4 kHz [23—26]. The rationale for this appears to be that most permanent sensorineural hearing loss will affect hearing acuity in the 2—4 kHz region. However certain hearing disorders, with low to mid frequency audiometric configurations, would be missed by these criteria [27—29].
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Fig. 1 CEOAE spectrums recorded by ILO V6 software from a normal hearing neonatal ear. Black depicts the evoked OAE response and grey color depicts the noise floor.
Therefore, it is preferable for neonatal hearing screening procedures to, at least, determine likely hearing deficit at 1 kHz in addition to examining higher frequency bands. However, a robust 1 kHz component of a CEOAE response is likely to be contaminated by low frequency noise in a normal hearing individual (e.g., Fig. 1) [30,31]. To resolve this, tone burst evoked OAEs (TBOAE) may be a promising supplement to the conventional CEOAE screening technique, since tone burst stimuli can elicit a more frequency-specific response [32,33]. In previous work, TBOAEs have been shown to provide a stronger response level with greater SNR than CEOAEs [34]. 1 kHz TBOAEs could be recorded clearly in healthy ears, and their test—retest reliability is comparable to that of CEOAEs [35,36]. Few studies have been carried out that use TBOAE techniques in newborn hearing screening. McPherson et al. [36] compared six passing criteria for transient evoked otoacoustic emissions (TEOAEs) screening, based on CEOAEs only, TBOAEs only, and four criteria using combined CEOAE results plus TBOAE data with different stimulus center frequencies. The 1 kHz TBOAE plus CEOAE procedure was the most effective screening tool in terms of a favorable pass/refer rate among the six pass/refer criteria sets. Compared with a CEOAE-only screening criterion, the CEOAE plus 1 kHz TBOAE procedure improved the pass rate from 79.2% to 86.3%. Similarly, the results of a related study [37] reported that a CEOAE plus 1 kHz TBOAE approach reduced the neonatal referral rate by 1.95% points compared to a conventional CEOAEonly protocol. A combined 1 kHz TBOAE/CEOAE
Neonatal hearing screening combined method protocol may better elicit a reliable OAE response in the lower frequency region, and assist in the reduction of high referral rates, and hence false positive rates, in neonatal hearing screening programs. The aims of this study were to evaluate the criteria of this combined protocol in a large group of neonates, and explore the feasibility of this combined method in a clinical universal hearing screening program.
2. Method 2.1. Participants A total of 1033 neonates (2066 ears) from well-baby nurseries were enrolled at the Henan Provincial People’s Hospital (HPPH; 559 neonates; 1118 ears) and the Hong Kong Adventist Hospital (HKAH; 474 neonates; 948 ears) between April 2006 and July 2007. Of these 53.4% were male and 46.6% were female. The babies were required to meet study inclusion criteria as follows: gestation between 37 and 42 weeks; older than 48 h and younger than 7 days; normal birth history and first 24 h after delivery; without apparent congenital defects; birth weight between 2.4 and 4.5 kg; APGAR scores between 8 and 10 and no history of high risk factors. High risk factors were family history of hearing loss; congenital perinatal infection; anatomical malformation of head or neck; hyperbilirubinaemia; bacterial meningitis; severe perinatal asphyxia; convulsions; prolonged aminoglycoside usage and intracranial hemorrhage. All the neonates were recruited into the research program after parents elected to participate on a voluntary basis.
2.2. Screening personnel A medical doctor with previous experience in newborn hearing screening and an audiologist conducted the TBOAE and CEOAE screening at HPPH and HKAH, respectively. The screenings took place at least twice a week at each hospital over an 18month period.
2.3. Procedures Any debris noted in the ear canal was removed using a cotton swab before inserting the OAE probe tip. The probe tip was checked for adequate fit and was refitted or changed as appropriate. Newborns were tested while in natural sleep or a quiet state. Both ears were tested and the ear, which was most easily accessible was tested first. CEOAE and 1 kHz TBOAE measurements were performed in a randomized
353 sequence in each ear. Parents were informed of the results based on the CEOAE-only screening outcomes and referred babies were rescreened within one month of initial screening.
2.4. Apparatus and parameters All the measures were recorded in a non-sound treated room in the obstetrics department at each hospital. The average ambient room noise level with OAE equipment in operation was under 50 dBA. Each hospital used similar OAE equipment, an Echoport ILO 292 USB system with V6 software (Otodynamics Ltd., UK) installed in a laptop computer. A standard ILO system clinical neonatal probe was used and calibrated before every test session. CEOAE measurement used the ‘‘QuickScreen’’ mode with a response window of 12.8 ms, and the analysis window for the TBOAE mode was 20.48 ms. The recorded stimulus level of 75—80 dB equivalent sound pressure level (peSPL) in the ear canal was considered acceptable for both CEOAE and TBOAE measures. A tone burst stimulus with a 1 kHz center frequency was used to elicit a TBOAE response for each neonate. Response stopping criteria for both CEOAE and TBOAE measurements required at least 70 OAE quiet responses. The noise rejection level was generally set lower than 8 mPa (52 dB SPL). The data were analyzed using half-octave bands in ILO V6 software.
2.5. Pass/fail criteria A valid, passing CEOAE-only measurement was one that fulfilled the following CEOAE criteria: stimulus stability 75%; whole reproducibility 70%; at least three of five test frequency bands centered at 1, 1.5, 2, 3 and 4 kHz with signal to noise ratio (SNR) 3 dB. These criteria were a modified form of that used in the study of Dort [17], where CEOAE pass criteria were set as SNR 3 in four bands centered at 1.5, 2, 3 and 4 kHz with 70% reproducibility. For 1 kHz TBOAE screening in this study, pass was defined as stimulus stability 75%; whole reproducibility 60%; and SNR 3 dB at 1 and/or 1.5 kHz frequency bands. For those ears, which failed CEOAE testing, the screening outcome was still considered as pass if the combined 1 kHz TBOAE/CEOAE protocol fulfilled the criteria listed in Table 1.
2.6. Statistical analysis The analyses for CEOAE and TBOAE measurement included overall mean response level, overall mean reproducibility, test duration and the mean response level, SNR and prevalence rate for 1, 1.5
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Table 1 Screening criteria for combined 1 kHz TBOAE/CEOAE approach Recorded parameters
Combined approach pass criteria
Stimulus stability Reproducibility SNR
CEOAE
TBOAE
75% 70% At least two of three test frequency bands centered at 2, 3 and 4 kHz with SNR 3 dB The total number of passed frequency bands for CEOAE plus 1 kHz TBOAE screening 3
75% 60% SNR 3 dB at 1 and/or 1.5 kHz frequency bands
and 2 kHz frequency components. TBOAE measures were also compared with CEOAE results using a paired-samples t-test. x2-test was used to compare the differences in referral rate between CEOAE-only and combined TBOAE/CEOAE protocols. The data set were extensively analyzed to determine whether the combined approach significantly reduced the number of referral cases. Statistical analyses were performed using SPSS for Windows version 12.0 software. The statistical significance was set at P < 0.05.
3. Results In total 1033 babies (2066 ears) without any risk factor for hearing disorder were included in this analysis. Response levels were averaged in dB SPL. A 1 kHz tone burst stimulus usually could evoke a TBOAE response in the 1—2 kHz frequency range, using a half-octave analysis. Therefore, the analyses of mean emission response, SNR and prevalence rate included results at 1, 1.5 and 2 kHz half-octave bands. The mean recorded stimulus levels for both CEOAE and TBOAE measurements were nearly identical in the present study–—78.77 dB peSPL (S.D. = 1.85) and 78.54 dB peSPL (S.D. = 1.96), respectively.
3.1. Analyses for CEOAEs and TBOAEs
other researchers [36,38—41] in neonatal and young infant hearing screening programs. The overall mean response level and the overall mean reproducibility for the recorded 1 kHz TBOAEs were 13.52 (S.D. = 19.64) and 66.0% (S.D. = 26.1), respectively. These two values were similar to previous findings for neonatal TBOAE recordings [36,37]. The mean response for CEOAEs and TBOAEs at different frequency bands is illustrated in Fig. 2. The statistical analysis indicated that TBOAE responses were significantly greater than in comparable frequency regions for CEOAE responses, at both the 1 kHz (t = 60.85, P < 0.05) and 1.5 kHz component regions (t = 91.49, P < 0.05). Comparative analysis of SNR also showed that 1 and 1.5 kHz components of CEOAE measurement were significantly lower than those of TBOAEs (at 1 kHz: t = 21.98, P < 0.05; at 1.5 kHz: t = 15.58, P < 0.05) (Fig. 3). At the 2 kHz frequency band, the mean response and SNR of CEOAEs were significantly higher than those for TBOAEs (for mean response: t = 15.42, P < 0.05; for mean SNR: t = 61.27, P < 0.05).
3.2. Prevalence rate for CEOAE and TBOAE at selected frequencies Based on the initial CEOAE-only screening outcomes, the total of 1033 neonates (2066 ears) were divided into pass (1872 ears) and refer groups (194
Some of the recorded variables for CEOAE and TBOAE measurements are listed in Table 2. The CEOAE results were similar to those obtained by Table 2 Recorded variables for CEOAE and TBOAE measurement (n = 2066 ears) Parameters
CEOAE
Test duration (s) Reproducibility (%) Stimulus stability (%) Response level (dB SPL)
43.05 29.81 51.76 30.91 83.21 19.88 66.07 26.10 97.40 7.48 95.55 9.87 17.00 12.25 13.52 19.64
Mean
TBOAE S.D.
Mean
S.D. Fig. 2 Comparison of mean response level for CEOAE and 1 kHz TBOAE at 1, 1.5 and 2 kHz frequency bands (n = 2066 ears). The solid line depicts the mean TBOAE response. The dashed line depicts the CEOAE response.
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Fig. 3 Comparison of SNR for CEOAE and 1 kHz TBOAE at 1, 1.5 and 2 kHz frequency bands (n = 2066 ears). The solid line depicts the SNR of TBOAE. The dashed line depicts the SNR of CEOAE.
ears). Fig. 4 illustrates the prevalence rates for CEOAEs and TBOAEs at 1, 1.5 and 2 kHz frequency bands among different groups. For the overall data, the prevalence rates for TBOAEs were significantly greater than those for CEOAE at both the 1 kHz (x2(1) = 218.74, P < 0.05) and 1.5 kHz (x2(1) = 5.46, P < 0.05) frequency bands. In the pass group, the 1 kHz tone burst elicited a response in 1167 ears (62.34%), but in only 694 ears (37.07%) did the CEOAE stimulus evoke a 1 kHz frequency band response. In the 1.5 kHz frequency band, the prevalence rate was 90.06% (1686 ears) for TBOAEs and 86.75% (1624 ears) for CEOAE measurement.
A x2-test also indicated that differences between these two measurements were significant in both the 1 kHz (x2(1) = 239.04, P < 0.05) and 1.5 kHz (x2(1) = 9.35, P < 0.05) frequency ranges. In the refer group, only 5 ears (2.58%) out of 194 failed ears gave an evoked response in the 1 kHz range of the CEOAE response, and 9.28% (18 ears) in the 1.5 kHz range. The prevalence rates for a 1 kHz TBOAE response were significantly greater than those for a CEOAE response at these two frequency bands, with x2(1) = 15.46, P < 0.05 at 1 kHz and x2(1) = 20.15, P < 0.05 at 1.5 kHz. The prevalence rate for TBOAEs in the 2 kHz frequency band was lower than that for CEOAEs in any of three groups (for overall data: x2(1) = 329.28, P < 0.05; for pass group: x2(1) = 465.97, P < 0.05; for refer group: x2(1) = 15.71, P < 0.05). Tables 3 and 4 indicate the relationship of individual screening outcomes for CEOAE and TBOAE measurements in the 1 and 1.5 kHz frequency bands. For the CEOAE pass group (Table 3), there was 61.7% (30.6% + 31.3%) and 90.9% (83.8% + 7.1%) agreement between the CEOAE and TBOAE results at 1 and 1.5 kHz, respectively. Table 3 also shows that 595 ears (31.8%) at 1 kHz and 117 ears (6.3%) at 1.5 kHz had a CEOAE fail result but the TBOAE measurement gave a pass result. For the CEOAE refer group (194 ears, Table 4), 12.9% (25 ears) at
Table 3 Relationship (numbers of ears and percentages) between the CEOAE and TBOAE screening outcomes at 1 and 1.5 kHz frequency bands in pass group (n = 1872 ears) Frequency bands (kHz)
CEOAE pass
CEOAE refer
Kappa value (k)
1
TBOAE pass TBOAE refer
572 (30.6%) 122 (6.5%)
595 (31.8%) 583 (31.1%)
0.28
1.5
TBOAE pass TBOAE refer
1569 (83.8%) 54 (2.9%)
117 (6.3%) 132 (7.1%)
0.56
Fig. 4 Prevalence rate of CEOAE and 1 kHz TBOAE at 1, 1.5 and 2 kHz frequency components in total ears (n = 2066 ears), CEOAE pass group (n = 1872 ears) and refer group (n = 194 ears).
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Table 4 Relationship (numbers of ears and percentages) between the CEOAE and TBOAE screening outcomes at 1 and 1.5 kHz frequency bands in refer group (n = 194 ears) Frequency bands (kHz)
CEOAE pass
CEOAE refer
Kappa value (k)
1
TBOAE pass TBOAE refer
1 (0.5%) 4 (2.1%)
25 (12.9%) 164 (84.5%)
0.02
1.5
TBOAE pass TBOAE refer
14 (7.2%) 4 (2.1%)
40 (20.6%) 137 (70.6%)
0.29
1 kHz and 20.6% (40 ears) at 1.5 kHz showed disagreement in the CEOAE and TBOAE outcomes. For both CEOAE pass and refer groups, Kappa values showed agreement between CEOAE and TBOAE was not good at both the 1 and 1.5 kHz frequency bands [42].
3.3. Analysis of overall pass rates for the two screening protocols For CEOAE-only screening, 1872 ears (90.61%) from 2066 neonatal ears fulfilled the pass criteria and 194 ears (9.39%) required referral. If screening were based on the combined criteria mentioned in Table 1, 40 additional ears from 194 CEOAE-only
Fig. 5
failed neonates would pass screening. The initial referral rate for screening using the combined criteria would reduce by 1.94 percentage points compared to the rate of the CEOAE-only criteria, a statistically significant difference (x2(1) = 5.021, P < 0.05).
3.4. Follow-up rescreening for positive cases Fig. 5 provides information on follow-up testing of the subject group. For the total 194 ears, which failed CEOAE screening, 109 ears (56.19%) were rescreened before discharge or within one month
Flowchart of the follow-up results of CEOAE failed group (n = 194 ears).
Neonatal hearing screening combined method post-discharge, including 2 ears that were retested in other hospitals. Of these, 86 ears passed at the second screening occasion. For those 154 ears which showed a refer screening outcome with both the CEOAE-only and combined approach at first time screening, there were 23 ears that still failed at the second screen, and 4 ears out of these 23 ears later failed diagnostic ABR at age 3 months. Further diagnostic test results have not become available. For the 40 ears that failed CEOAE-only screening but passed the combined protocol criteria, 33 ears have been retested. The outcomes showed that all of these ears finally passed the CEOAE rescreening (31 ears passed the rescreening at same hospital; 2 ears passed the rescreening at other hospitals). The remaining 7 ears could not be followed up.
4. Discussion With any screening procedure, it is desirable to have a test that is as accurate as possible. Babies who screen positive for hearing loss should have a hearing disorder and babies who screen negative for hearing loss should indeed have normal hearing. In China, for example, it has been reported that 1.46—2.64% of newborns have permanent sensorineural hearing impairment. Yet published referral rates of first time CEOAE screening are about 15% [3,4]. Therefore, improving the current CEOAE measurement protocol and achieving a lower referral rate are very important. The present study aimed to develop an improved 1 kHz TBOAE/CEOAE approach, and determine if this combined method could significantly reduce the referral rate during first time neonatal hearing screening.
4.1. OAE responses In the present study, the 1 kHz frequency component of the CEOAE response had a lower average response than other frequency components (Fig. 2). This trend was also found for CEOAE SNR analysis (Fig. 3). 1 kHz TBOAEs were more robust than CEOAEs in terms of emission response level and SNR at comparable frequency components, for both 1 and 1.5 kHz. This finding was consistent with other reports comparing TBOAEs and CEOAEs in both adult and newborn populations [5,31,35—37,43]. The values can be used as normative data for screening and diagnostic purposes in the neonatal population.
4.2. Screening outcomes In present study, SNR 3 dB was used as a criterion defining a detectable OAE response at each
357 frequency band. As shown in Fig. 4, only 33.83% and 79.48% of ears reached the SNR pass criteria for 1 and 1.5 kHz frequency components of the CEOAE assessment, compared with 57.74% and 84.12% of ears in TBOAE testing. The overall prevalence rates for CEOAE and TBOAE responses at these two frequency ranges were significantly different. The results also indicated that even in the CEOAE pass group (1872 ears), there were still 62.93% and 13.25% of ears that could not evoke a clear CEOAE response at 1 and 1.5 kHz, respectively. In the refer group, when using 1 kHz TBOAE data the number of passed ears was nearly 5 times that when 1 kHz CEOAE data was utilized. The percentage of ears passed by TBOAE testing was about three times higher than that when CEOAE test results at 1.5 kHz were used. In the 2 kHz frequency range, the prevalence rate elicited by a 1 kHz TBOAE was lower than that for the CEOAE stimulus. The mean response and SNR of CEOAEs were higher than those for TBOAE results in the 2 kHz frequency range. Therefore, a 1 kHz tone burst stimulus is more suitable than a broadband click stimulus when seeking restricted lower frequency information (lower than 2 kHz) in neonatal hearing screening. For individual outcomes in the refer group (Table 4), 25 ears (12.9%) at 1 kHz and 40 ears (20.6%) at 1.5 kHz were found that failed CEOAE but could pass TBOAE screening. After the follow-up rescreening, 33 out of 40 ears (82.5%) that failed CEOAE criteria but passed using the combined approach were confirmed with negative CEOAE results. A combined 1 kHz TBOAE/CEOAE test protocol may be a promising approach to reducing false positive rates in TBOAE screening, and hence contribute to more accurate and efficient UNHS programs. The overall pass percentage by ears for the CEOAE-only criteria in the present study was 90.61%, which is similar to the reports from other UNHS programs in their initial stages [44,45]. If the pass/refer determination had included 1 kHz TBOAE results, and set the criteria of this alternative combined approach as Table 1 mentioned, an additional 40 ears (20.6% of refer group) could have been detected with a clear OAE within the 1 k to 1.5 kHz bandwidth, improving the pass percentage for screened ears to 92.55%. The pass rate for the total number of screened ears would therefore have increased by 1.94 percentage points, a significantly lower referral rate than for the conventional CEOAE-only criteria. This may be an important benefit to a hearing health care system. For example, there are an estimated 20 million
358 children born in 31 cities/provinces of China each year1. About 1.87 million newborns may fail first time CEOAE screening (calculated using a 9.39% referral rate). Therefore, reducing the referral rate by 1.94 percentage points using combined approach would result in nearly 320,000 additional babies passing initial screening. This would greatly reduce the heavy follow-up burden on the health care system and also decrease parental anxiety.
4.3. Test duration In this study, the mean test duration for CEOAE measurement was 43 s per ear, and for 1 kHz TBOAE measurement it was 51.7 s. Hence, the combined screening approach takes about 2 min per ear. Including the additional preparation time in the test duration, the combined approach in the present study took about 6—8 min for both ears, which is less time-consuming than performing distortion product otoacoustic emission (DPOAE; 11:04 min) or automated ABR screening (18:50 min) [17]. With the development of an automatic, computerized technique time constraints could be further reduced for a combined CEOAE and TBOAE procedure. In addition, protocols could be developed that allow 1 kHz TBOAE testing to be considered with CEOAE screening only when clear lower frequency CEOAE responses could not be evoked. This may provide more information on lower frequency components of OAEs and improve pass rates (for CEOAE refer group), and thus reduce the overall refer outcomes from screening.
4.4. Cost In China, a routine clinical CEOAE or DPOAE screening test costs 40—80 Yuan2 according to region and equipment used. If ABR-based testing is included in a screening procedure, an additional 70—100 Yuan needs to be paid, often placing great financial pressure on parents. Also, OAE administration is comparatively straightforward and little extra screener training is needed. Therefore, the combined 1 kHz TBOAE/CEOAE approach may improve the accuracy and efficiency for first time screening by reducing the burdens on both the medical system and the family. For those ears which failed a combined CEOAE/TBOAE protocol diagnostic procedures could then be conducted.
1
http://www.moh.gov.cn/open/statistics/digest01/Tyf3156.htm. 2 1 USD 7.5 Yuan (August 2007).
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4.5. Limitations Some limitations of this study should be noted. Firstly, only 55.15% (107 ears) out of 194 failed ears participated in the follow-up rescreening procedures provided by HPPH and HKAH. An additional 2 ears from 2 neonates were retested at other hospitals. The proportion of retested ears was similar to a North American report [15], but was relatively lower than noted in other Chinese reports [3,4]. The high frequency of cases lost to follow-up is an important challenge for UNHS. Although they would improve the quality of UNHS screening programs, well integrated tracking systems and followup services are always not easy to conduct. For HPPH, the low follow-up rate may be due to it being a government hospital providing services to both urban and rural patients. Rural parents often have lower income and education levels, and may have lower awareness of the importance of hearing tests for their babies. Although the screener explained the value of neonatal hearing screening to parents, and all rescreening tests were free of charge, rural families may still not attend since transport and lost income costs still need to be borne by parents. Hong Kong is an important center for international finance and trade, with a large expatriate population. HKAH is a private hospital and has a patient population with middle to high income and education levels. Most patients have their own private health insurance and may choose to consult a clinic in a wide range of areas. This also makes follow-up retests difficult to monitor. Among the 40 ears, which failed the CEOAE criteria but passed the combined approach, there were still 7 ears from 7 neonates that had lost touch with us. Therefore, the actual overall false positive rate for all 40 failed neonatal ears could not be determined. In addition, due to the constraints in our ability to monitor diagnostic test results, the sensitivity and specificity of the combined CEOAE/TBOAE approach could not be evaluated in this study. The false negative rate for the combined approach could not been determined. A second limitation is that the current CEOAE measures used the ‘‘QuickScreen’’ mode with a response window of 12.8 ms, and the analysis window for TBOAE mode was 20.48 ms. These two parameters cannot be adjusted in V6 software. ‘‘QuickScreen’’ mode was used in the present study because this mode has been widely used in UNHS in China and internationally, and it was of benefit to compare the overall pass/refer outcomes for current CEOAE-only screening with results obtained in other studies. However, the shortened time window of the ‘‘QuickScreen’’ mode may also reduce the
Neonatal hearing screening combined method OAE response at 1 kHz, although the main purpose of this mode is to reduce noise contamination at lower frequencies.
5. Conclusion An evaluation of the 1 kHz TBOAE/CEOAE combined approach was conducted in this study. By providing supplementary information in the lower frequency region, fewer neonates required referral because neonatal ears, which failed CEOAE screening often, had a clear TBOAE response at the 1 and/or 1.5 kHz frequency band and were reassigned to the pass category. When compared with conventional CEOAE-only screening, the combined approach reduced the overall referral rate by 1.94 percentage points, and this was shown to be a significant improvement on the pass rate for CEOAE-only screening. Available follow-up rescreening results also confirmed that all tested ears, which failed CEOAE screening but passed the combined approach, were false positive cases. In addition, the ease of administration of an additional TBOAE test may reduce the need for major retraining for screening personnel. A combined 1 kHz TBOAE/ CEOAE measurement approach is a feasible way of reducing referral rates, improving the accuracy and efficiency for first time neonatal hearing screening, and may assist in furthering the long-term goal of universal, cost-effective screening for all infants.
Acknowledgements The authors wish to thank all the medical and nursing staff of the Obstetrics Departments at both Hong Kong Adventist Hospital and Henan Provincial People’s Hospital for their generous assistance during data collection. The work was fully supported by a grant from the Research Grants Council of the Hong Kong Special Administrative Region, China (HKU7434/04M).
References [1] B.O. Olusanya, W. Swanepoel de, M.J. Chapchap, S. Castillo, H. Habib, S.Z. Mukari, et al., Progress towards early detection services for infants with hearing loss in developing countries, BMC Health Serv. Res. 7 (2007) 14. [2] A. Erenberg, J. Lemons, C. Sia, D. Trunkel, P. Ziring, Newborn and infant hearing loss: detection and intervention. American academy of pediatrics. Task force on newborn and infant hearing, 1998—1999, Pediatrics 103 (1999) 527—530.
359 [3] W.Y. Nie, L.X. Gong, Y.J. Liu, L.L. Xiang, Q. Lin, Y.S. Qi, et al., Hearing screening of 10,501 newborns, Chin. Med. J. 83 (2003) 274—277. [4] Y.J. Nie, Y.S. Qi, X.T. Zhao, Z.H. Cai, Y.L. Yang, D. Tao, et al., Value of otoacoustic emission (OAE) technique in perinatal audiology, Chin. Arch. Otolaryngol. Head Neck Surg. 6 (1999) 207—211. [5] S.J. Norton, M.P. Gorga, J.E. Widen, B.R. Vohr, R.C. Folsom, Y.S. Sininger, et al., Identification of neonatal hearing impairment: transient evoked otoacoustic emissions during the perinatal period, Ear Hearing 21 (2000) 425—442. [6] P. Clarke, M. Iqbal, S. Mitchell, A comparison of transientevoked otoacoustic emissions and automated auditory brainstem responses for pre-discharge neonatal hearing screening, Int. J. Audiol. 42 (2003) 443—447. [7] A.B. Maxon, B.R. Vohr, K.R. White, Newborn hearing screening: comparison of a simplified otoacoustic emissions device (ILO1088) with the ILO88, Early Hum. Dev. 45 (1996) 171— 178. [8] B.R. Vohr, W. Oh, E.J. Stewart, J.D. Bentkover, S. Gabbard, J. Lemons, et al., Comparison of costs and referral rates of 3 universal newborn hearing screening protocols, J. Pediatr. 139 (2001) 238—244. [9] A. Ciorba, S. Hatzopoulos, L. Camurri, L. Negossi, M. Rossi, D. Cosso, et al., Neonatal newborn hearing screening: four years’ experience at Ferrara University Hospital (CHEAP project). Part 1, Acta Otorhinolaryngol. Ital. 27 (2007) 10—16. [10] M.J. Johnsen, A.B. Maxon, K.R. White, B.R. Vohr, Operating a hospital-based universal newborn hearing screening: program using transient evoked otoacoustic emissions, Semin. Hearing 14 (1993) 46—55. [11] G.T. Mencher, S.J. DeVoe, Universal newborn screening: a dream realized or a nightmare in the making? Scand. Audiol. 30 (2001) 15—21. [12] K.R. White, B.R. Vohr, T.R. Behrens, Universal newborn screening using transient evoked otoacoustic emissions: results of the Rhode Island hearing assessment project, Semin. Hearing 14 (1993) 18—29. [13] S. Iwasaki, Y. Hayashi, A. Seki, M. Nagura, Y. Hashimoto, G. Oshima, et al., A model of two-stage newborn hearing screening with automated auditory brainstem response, Int. J. Pediatr. Otorhinolaryngol. 67 (2003) 1099—1104. [14] K.R. White, B.R. Vohr, S. Meyer, J.E. Widen, J.L. Johnson, J.S. Gravel, et al., A multisite study to examine the efficacy of the otoacoustic emission/automated auditory brainstem response newborn hearing screening protocol: research design and results of the study, Am. J. Audiol. 14 (2005) 186—199. [15] Joint Committee on Infant Hearing, Year 2007 position statement: principles and guidelines for early hearing detection and intervention programs, Pediatrics 120 (2007) 898— 921. [16] J. Gravel, A. Berg, M. Bradley, A. Cacace, D. Campbell, L. Dalzell, et al., New York State universal newborn hearing screening demonstration project: effects of screening protocol on inpatient outcome measures, Ear Hearing 21 (2000) 131—140. [17] J.C. Dort, C. Tobolski, D. Brown, Screening strategies for neonatal hearing loss: which test is best? J. Otolaryngol. 29 (2000) 206—210. [18] S. Meier, O. Narabayashi, R. Probst, N. Schmuziger, Comparison of currently available devices designed for newborn hearing screening using automated auditory brainstem and/ or otoacoustic emission measurements, Int. J. Pediatr. Otorhinolaryngol. 68 (2004) 927—934.
360
V.W. Zhang et al.
[19] P. Muller, M. Kompis, Evaluation of a noise reduction system for the assessment of click-evoked otoacoustic emissions, J. Acoust. Soc. Am. 112 (2002) 164—171. [20] G.R. Popelka, R.K. Karzon, R.A. Clary, Identification of noise sources that influence distortion product otoacoustic emission measurements in human neonates, Ear Hearing 19 (1998) 319—328. [21] K. Rhoades, B. McPherson, V. Smyth, J. Kei, A. Baglioni, Effects of background noise on click-evoked otoacoustic emissions, Ear Hearing 19 (1998) 450—462. [22] G. Tognola, P. Ravazzani, F. Grandori, An optimal filtering technique to reduce the influence of low-frequency noise on click-evoked otoacoustic emissions, Br. J. Audiol. 29 (1995) 153—160. [23] M.T. Huynh, R.A. Pollack, R.A. Cunningham, Universal newborn hearing screening: feasibility in a community hospital, J. Fam. Pract. 42 (1996) 487—490. [24] B.R. Vohr, L.M. Carty, P.E. Moore, K. Letourneau, The Rhode Island Hearing Assessment Program: experience with statewide hearing screening (1993—1996), J. Pediatr. 133 (1998) 353—357. [25] S. Hatzopoulos, G. Pelosi, J. Petruccelli, M. Rossi, V. Vigi, R. Chierici, et al., Efficient otoacoustic emission protocols employed in a hospital-based neonatal screening program, Acta Otolaryngol. 121 (2001) 269—273. [26] L. Spivak, L. Dalzell, A. Berg, M. Bradley, A. Cacace, D. Campbell, et al., New York State universal newborn hearing screening demonstration project: inpatient outcome measures, Ear Hearing 21 (2000) 92—103. [27] N. Gurtler, Y. Kim, A. Mhatre, C. Schlegel, A. Mathis, A.K. Lalwani, DFNA54, a third locus for low-frequency hearing loss, J. Mol. Med. 82 (2004) 775—780. [28] A.M. King, S.C. Purdy, H. Dillon, M. Sharma, W. Perce, Australian hearing protocols for the audiological management of infants who have auditory neuropathy, Aust. N. Z. J. Audiol. 27 (2005) 69—77. [29] R.J. Pennings, S.J. Bom, K. Cryns, K. Flothmann, P.L. Huygen, H. Kremer, et al., Progression of low-frequency sensorineural hearing loss (DFNA6/14-WFS1), Arch. Otolaryngol. Head Neck Surg. 129 (2003) 421—426. [30] S.J. Norton, M.P. Gorga, J.E. Widen, R.C. Folsom, Y. Sininger, B. Cone-Wesson, et al., Identification of neonatal hearing impairment: evaluation of transient evoked otoacoustic emission, distortion product otoacoustic emission, and auditory brain stem response test performance, Ear Hearing 21 (2000) 508—528. [31] D. Welch, K.A. Greville, P.R. Thorne, S.C. Purdy, Influence of acquisition parameters on the measurement of click evoked
[32] [33] [34]
[35]
[36]
[37]
[38]
[39]
[40]
[41]
[42] [43]
[44]
[45]
otoacoustic emissions in neonates in a hospital environment, Audiology 35 (1996) 143—157. J.W. Hall, Handbook of Otoacoustic Emissions, Singular, San Diego, Calif., 2000. D.T. Kemp, S. Ryan, P. Bray, A guide to the effective use of otoacoustic emissions, Ear Hearing 11 (1990) 93—105. R. Probst, B.L. Lonsbury-Martin, G.K. Martin, A review of otoacoustic emissions, J. Acoust. Soc. Am. 89 (1991) 2027— 2067. R.H. Chan, B. McPherson, Test—retest reliability of toneburst-evoked otoacoustic emissions, Acta Otolaryngol. 120 (2000) 825—834. B. McPherson, S.F. Li, B.X. Shi, J.L. Tang, B.Y. Wong, Neonatal hearing screening: evaluation of tone-burst and clickevoked otoacoustic emission test criteria, Ear Hearing 27 (2006) 256—262. V.W. Zhang, B. McPherson, B.X. Shi, J.L.F. Tang, An alternative method in neonatal hearing screening: click otoacoustic emissions plus tone-burst otoacoustic emissions, in: Paper presented at: XXVIIIth International Congress of Audiology, September 3—7, Innsbruck, Austria, 2006. J. Kei, B. McPherson, V. Smyth, S. Latham, J. Loscher, Transient evoked otoacoustic emissions in infants: effects of gender, ear asymmetry and activity status, Audiology 36 (1997) 61—71. A. Salamy, L. Eldredge, R. Sweetow, Transient evoked otoacoustic emissions: feasibility in the nursery, Ear Hearing 17 (1996) 42—48. Y.L. Yang, H.H. Sun, X.Q. Tang, Y.S. Qi, Y.J. Nie, L.S. Guo, et al., Transient evoked otoacoustic emissions and auditory brain stem response in full-term neonates, Chin. Arch. Otolaryngol. Head Neck Surg. 8 (2001) 131—134. Y.S. Chi, Y.J. Nie, Z.H. Cai, Y.L. Yang, D. Tao, The features of transient evoked otoacoustic emissions (TEOAEs) in full-term newborns, Acta Biophys. Sinica (Chin) 16 (2000) 66—72. B. Everitt, Statistical Methods in Medical Investigations, 2nd. ed., Edward Arnold, London, 1994. B.A. Prieve, M.P. Gorga, S.T. Neely, Click- and tone-burstevoked otoacoustic emissions in normal-hearing and hearing-impaired ears, J. Acoust. Soc. Am. 99 (1996) 3077—3086. D. Aidan, P. Avan, P. Bonfils, Auditory screening in neonates by means of transient evoked otoacoustic emissions: a report of 2842 recordings, Ann. Otol. Rhinol. Laryngol. 108 (1999) 525—531. H.S. Habib, H. Abdelgaffar, Neonatal hearing screening with transient evoked otoacoustic emissions in Western Saudi Arabia, Int. J. Pediatr. Otorhinolaryngol. 69 (2005) 839—842.
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