Characterization of spontaneous otoacoustic emissions in full-term newborns

International Journal of Pediatric Otorhinolaryngology 78 (2014) 2286–2291

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Characterization of spontaneous otoacoustic emissions in full-term newborns Beier Qi a,b, Xiaohua Cheng a,b, Hui En b, Lihui Huang a,b,1, Luo Zhang a,b,1,* a b

Department of Otolaryngology Head and Neck Surgery, Beijing TongRen Hospital, Capital Medical University, China Key Laboratory of Otolaryngology Head and Neck Surgery (Ministry of Education), Beijing Institute of Otolaryngology, China

A R T I C L E I N F O

A B S T R A C T

Article history: Received 1 August 2014 Received in revised form 25 October 2014 Accepted 29 October 2014 Available online 4 November 2014

Objective: To analyze the characteristics of spontaneous otoacoustic emissions (SOAEs) in full-term newborns. Methods: A total of 236 ears from 147 randomly selected full-term Chinese neonates (82 females and 65 males), who had passed the initial newborn hearing screening, were assessed for SOAEs using the Capella OAE equipment (Madsen, Denmark). The test was performed in a sound booth. Results: (1) The overall prevalence of SOAE was 56.77% of the ears. The prevalence of SOAEs was significantly higher in females (69.23%) than in males (41.51%, p < 0.01), as well as in the right ears (64.17%) than in the left ears (49.14%, p < 0.05). (2) The overall mean level of SOAE was 11.78  8.36 dB SPL, with no significant differences between males (11.73  8.25 dB SPL) and females (11.81  8.43 dB SPL) or between the left (11.97  8.56 dB SPL) and the right ears (11.65  8.22 dB SPL). (3) The 25th and 75th percentiles of SOAE frequencies were 2.31 and 4.36 kHz in females and 1.93 and 3.94 kHz in males, which were statistically significantly different (p < 0.01). In contrast, the SOAE frequency was not significantly different between ears (2.22–4.18 kHz in the left ears and 2.17–4.14 kHz in right ears). (4) The overall mean number of SOAEs was 3.70  2.75, with no significant differences in females (3.62  2.70) and males (3.86  2.87) or in right (3.70  2.55) and left ears (3.70  3.02). Conclusions: The prevalence rate of SOAE is significantly higher in females than in males and in the right ears than in the left ears in Chinese newborns. The frequencies of the SOAEs in newborns appeared to be higher than those reported in normal-hearing adults in the literature. ß 2014 Elsevier Ireland Ltd. All rights reserved.

Keywords: Newborn Spontaneous otoacoustic emission (SOAE) Ear laterality SOAE frequency SOAE level

1. Introduction Otoacoustic emissions (OAEs) are low-level sounds generated in the ear canal when the tympanum receives vibrations transmitted backwards through the middle ear from the cochlea. Spontaneous OAEs (SOAEs), are a type of sound signals, which emanate from the inner ear without any external stimulation, and are frequently detected in normal-hearing ears. Although the precise mechanism underlying the generation of SOAEs remains unclear, there is evidence that SOAEs originate from the outer hair cells of the organ of Corti and are an epiphenomena of micromechanical processes in

* Corresponding author at: Key Laboratory of Otolaryngology Head and Neck Surgery (Ministry of Education), Beijing Institute of Otolaryngology, No 17, HouGouHuTong, DongCheng District, Beijing 100005, China. Tel.: +86 10 65141136. E-mail addresses: [email protected] (B. Qi), [email protected] (X. Cheng), [email protected] (H. En), [email protected] (L. Huang), [email protected] (L. Zhang). 1 These authors contributed equally to the study. http://dx.doi.org/10.1016/j.ijporl.2014.10.035 0165-5876/ß 2014 Elsevier Ireland Ltd. All rights reserved.

the cochlea [1]. Evidence suggests that SOAEs may be influenced by factors not commonly involved in the occurrence of evoked (E)OAEs, which occur after presentation of brief acoustic stimuli such as clicks and tone bursts/pips [2] and may significantly be influenced by the presence of SOAEs [3]. Previous studies have indicated that the SOAE prevalence is age-related; with the prevalence of SOAEs being much higher and ranging from 64% to 78% in healthy newborns and infants younger than 18 months [4,5], to about 30% in adults [6,7] and between 26% and 31% in children aged between 6 and 12 years [8]. Studies have indicated that SOAE frequency distribution and number per ear are also age-dependent. Burns et al. [4] reported that both SOAE levels and predominant SOAE frequency range were higher in neonates (8.5 dB peak equivalent sound pressure level (peSPL) and 2.5 to 5.0 kHz, respectively) than in adults ( 2.6 dB peSPL and 1.0 to 2.0 kHz, respectively). More recently, Liu et al. [9] have demonstrated that over 85% of SOAEs in 2–4 days old neonates appeared at frequencies between 1.01 and 4.5 kHz. Furthermore, some studies have suggested that there is a difference in

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prevalence of SOAEs among different races. While Whitehead et al. [10] have reported a greater prevalence of SOAEs in the African American group compared to Asian and the Caucasian groups, Chan and McPherson [11] have reported significantly more SOAEs at higher frequencies in Chinese subjects than in Caucasian subjects. Thus, in view of these findings the purpose of this study was to characterize the effects of gender and ear side on SOAE prevalence, peak number per ear, frequency, and amplitude in a large sample of full-term Chinese newborns.

2. Materials and methods 2.1. Participants

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(2) TEOAE test: Non-linear clicks at 75 dB peSPL were employed for this test. The non-linear method employed the use of three stimuli of a single intensity and a fourth stimulus three times greater and with opposite polarity. The overall analysis time was 20 ms, of which the first 3 ms were eliminated by a data processing treatment to suppress muscular and respiratory artifacts. Each recording was made as the mean result of 2080 sweeps; with minimal pass criteria being 50% reproducibility, 10 dB SPL at emission response, and 3 dB signal-to noise ratio at any three analysis frequencies (1, 1.5, 2, 3, and 4 kHz). (3) DPOAE test: Two pure-tone stimuli at 65/50 dB SPL (f2:f1 = 1.22) were presented to the ear simultaneously. Each recording was made as the mean result of 2080 sweeps; with minimal pass criteria being 3 dB signal-to noise ratio at any three analysis frequencies (1, 1.5, 2, 4, and 6 kHz). (4) SOAE test: Five hundred epochs of 80 ms after a synchronizing click stimulus (duration 1–1.5 ms, intensity of 70–80 dB peSPL) were acquired (sampling frequency 25 kHz). For each SOAE recording, all peaks were noted when the level was at least 3 dB above the related noise floor.

Overall, 147 randomly selected full-term neonates were enrolled into the study from Beijing Tongren Hospital, Capital Medical University, including 82 females and 65 males, from September, 2012 to May, 2013. In order to be included in the study, all subjects were required to have passed the initial newborn hearing screening test; including tympanometry, transient otoacoustic emission, (TEOAE) and distortion product otoacoustic emission (DPOAE); prior to further evaluations of SOAEs. There was no history of auditory pathology in the family of any of the subjects and the parent/guardian of each child provided written informed consent prior to entry of their child into the study. The study protocol was approved by the Ethics Committee of Beijing Institute of Otolaryngology and performed in accordance with the guidelines of the World Medical Association’s Declaration of Helsinki.

2.3. Statistical methods

2.2. Design and procedures

3. Results

2.2.1. Procedure for auditory testing After cleaning the external ear canal with a disinfectant swab, all auditory tests were performed in a sound booth (<50 dB(A)) at least 2 days after birth during the baby’s natural sleep and after being fed. Any recording that was interrupted, particularly by movement of the neonate leading to disturbance of the probe and breakage of the seal obtained at the beginning of the recording, was repeated after the probe had been refitted in the outer ear canal. The middle ear function was tested firstly by tympanometry using the Interacoustics AA220 (Assens, Denmark), followed by TEOAE and DPOAE and SOAE tests, according to the method proposed by Bray [12]. Stimulus presentation, data recording, averaging, and spectrum analysis (Fast Fourier Transform, 0.5– 6 kHz) were carried out using the Capella OAE (Madsen, Denmark). The probe consisted of a Knowles 1843 microphone, a BP 1712 transmitter, and a 20 dB attenuator embedded in a plastic ear plug, and adapted to the neonate external auditory canal with a foam rubber tip. Bilateral SOAE tests were performed in each newborn, but only one ear was tested when the guardian refused the test to continue.

Overall, a total of 130/164 ears in the 82 female newborns and 106/130 ears in the 65 male newborns were tested for SOAEs. Bilateral SOAE testing was not possible in all babies because at the time of testing, some newborns began to cry or needed to be fed. In such instances, the nursing mother or the baby’s guardian did not allow the test to be continued and thus the data were analyzed by each ear.

2.2.2. Parameters and pass criteria of auditory test battery

Statistical analysis was carried out with the use of the SPSS software (V.17.0; SPSS Inc., USA). Chi-square test was used to detect significant differences in prevalence rate between gender and ear side; Rank-sum test was used to analyze significant differences in frequency, level and peak between gender and ear side. The selected level of significance was p < 0.05.

3.1. SOAE prevalence in full-term neonate Table 1 shows the overall prevalence of SOAE in present study. A total of 134 out of 236 ears tested (56.77%) displayed SOAEs, 69.23% in female and 41.51% males, as well as 64.17% in right ears and 49.14% in left ears. There was significantly difference both in gender (p < 0.01) and in ear side (p < 0.05) (Table 1a). Assessment of SOAE prevalence in each ear by gender further demonstrated significantly higher prevalence in females than in males in both the left ear (63.64% vs 30.0%; p < 0.01) and the right ear (75% vs 51.79%; p < 0.01) (Table 1b).

Table 1a SOAE prevalence in full-term neonates. Group

(1) Tympanometry test: This was performed by presenting a typical 226 Hz probe tone into the ear canal while altering the air pressure of the canal from +200 to 400 daPa. Type A curve (Jerger classification system) suggested normal middle ear function, including the compliance peak occurring between 100 and +100 daPa, and the value of compliance ranging between 0.3 and 1.6 ml.

Number of testing ears

Number of SOAE ears

Prevalence rate (%)

Chi-square test

x2

p

Male Female

106 130

44 90

41.51 69.23

18.285

0.000

Left ear Right ear

116 120

57 77

49.14 64.17

5.429

0.025

Total

236

134

56.77

–

–

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Table 1b Ear side of SOAE prevalence in full-term neonates. Group

Male

4. Discussion Female

4.1. SOAE prevalence in full-term neonates

Chi-square test

x2

p

Left ear

Number of testing ears Number of SOAE ears Prevalence rate (%)

50 15 30.00

66 42 63.64

12.878

0.000

Right ear

Number of testing ears Number of SOAE ears Prevalence rate (%)

56 29 51.79

64 48 75.00

7.000

0.008

3.2. SOAE Level in full-term neonates The overall mean level of SOAE was 11.78  8.36 dB SPL, ranged from 6.4 dB SPL to 39.6 dB SPL, with no significant differences between males (11.73  8.25 dB SPL) and females (11.81  8.43 dB SPL) or between the left (11.97  8.56 dB SPL) and the right ears (11.65  8.22 dB SPL) (Table 2a). Assessment of SOAE level in each ear by gender further demonstrated no significant difference (Table 2b). 3.3. SOAE Frequency in full-term neonates The overall 25th and 75th percentiles of SOAE frequencies were 2.18 and 4.16 kHz. There were statistically significantly different between the 25th and 75th percentiles of SOAE frequencies were 2.31 and 4.36 kHz in females and 1.93 and 3.94 kHz in males (p < 0.01). In contrast, the SOAE frequency was not significantly different between ears (2.22–4.18 kHz in the left ears and 2.17– 4.14 kHz in right ears) (Figs. 1 and 2). 3.4. SOAE number in full-term neonates In present study, 104 ears showed multiple SOAE. The overall mean number of SOAEs was 3.70  2.75, with no significant differences in females (3.62  2.70) and males (3.86  2.87) or in right (3.70  2.55) and left ears (3.70  3.02).

Table 2a SOAE level in full-term neonates (dB SPL). Group

Mean SOAE level

Range of level

Rank sum test

Male Female

11.73  8.25 11.81  8.43

Lower 4.9 6.4

35.1 39.6

Z 0.37

0.712

Left ear Right ear

11.97  8.56 11.65  8.22

4.9 6.4

35.5 39.6

0.346

0.729

Total

11.78  8.36

6.4

39.6

Upper

p

–

–

Table 2b Ear side of SOAE level in full-term neonates (dB SPL). Group

Male

Female

Rank sum test Z

Left ear

Right ear

Mean SOAE level Lower Upper

11.53  8.21

12.22  8.72

4.9 30.1

4.7 35.5

Mean SOAE level Lower Upper

11.87  8.29

11.46  8.19

4.0 35.1

6.4 39.6

p 0.430

0.667

0.511

0.610

The prevalence of SOAEs in the present study was found to be 56.8% in 236 ears of 147 full-term newborns older than 48 h. Comparing these values with the previously reported SOAE prevalence of about 30% in adults [6,7], this study suggests that in accordance with the findings for infants and children, the prevalence of SOAE in healthy newborns is also higher than in adults. Moreover, our study demonstrated that the prevalence of SOAEs was significantly gender- (69.23% in females and 41.51% in males, p < 0.01) and ear side-dependent (64.17% in right ears and 49.14% in left ears, p < 0.05). Both gender- and ear-side-related differences demonstrated in full-term neonates in the present study are in accordance with the findings of other studies [13–16]. The gender dimorphism in SOAE production may result from differential prenatal exposure to androgens. It can be caused by either of two major classes of mechanisms: direct effect of genes carried on the X or Y chromosome or by the organizational actions of testosterone or its metabolites on a neutral physiological substrate [17]. Additionally, evidence from human and non-human populations also provides support for a hormonal effect [18,19]. Sexual differentiation of the brain and soma was thought to occur between weeks 8 and 24 of gestation, a temporal window that overlapped the development and maturation of the auditory system [20]. The prenatal hypothesis proposed that exposure of the male fetus to elevated testosterone during the critical window dampens the cochlear amplifiers (i.e., outer hair cells) responsible for OAE production, thereby decreasing the prevalence, frequency, and amplitude of OAEs in males compared to females [18]. The physiological differences between males and females may be the other main reason for the gender-dependent differences. In particular, the structural differences including a shorter cochlea and a higher count of outer hair cells in female subjects have a strong influence on SOAE prevalence [21]. As lowlevel SOAE has been shown to be amplified by the smaller volume of the outer auditory canal in female subjects, it is likely that SOAEs can be detected more easily in females than in males [21]. The right-ear advantage in SOAE production has been observed not only in adults but also in children [4,13]. In preterm neonates, Morlet et al. [5] found a SOAE prevalence of 79% for the right ear and 72% for the left ear, whereas Khalfa et al. [22] showed a significantly higher prevalence in right ears. The findings of the present study are also in accordance with these previous findings, as demonstrated by significantly higher SOAE prevalence of 64.17% in right ears, compared with 49.14% SOAE prevalence in left ears. One possibility of the ear effect in SOAE production maybe the ear asymmetry of middle-ear functioning. Previc [23] has hypothesized that a right-ear advantage in monaural sensitivity results from a smaller right craniofacial region during embryonic development, resulting in enhanced middle-ear conduction of sound. Keefe et al. [24], found that the energy reflectance were larger in left ears below 1.4 kHz, whereas energy reflectance was larger in right ears between 2 and 5.7 kHz based on acoustic reflectance and admittance measurements in the ear canal. Any ear asymmetries in middle-ear function might act as a confounding factor on measurements of ear asymmetries at all levels of the auditory pathway, including the cochlea. An alternative explanation for the observed ear asymmetries in OAEs could be the difference in the strength of the efferent influence by the medial olivocochlear system on the outer hair cells of the cochlea [25]. Specifically, OAEs may be greater in the right ear than the left because of less inhibition by the medial olivocochlear efferent system in the right ear [26]. The different prevalence in ear-side might also depend on the asymmetries of the efferent

[(Fig._1)TD$IG]

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Fig. 1. Distribution of SOAE frequency in different ears in full-term neonates. Panels (a) and (b) display the SOAE frequceny distribution in different ears. The x axis displays the SOAE frequency (Hz), the y axis displays the case (number). Panel (c) displays the stastic value of SOAE frequceny distribution in different ears. In panel (c), the means of difference ears are displayed by the solid lines across each box,respectively. The upper and lower bounds of each box bounds represent the quartiles. The whisker away from the box bounds showed the 1.25 SD of the mean, and the filled circles represent the data are outside the end of whisker. The p value is indicated on panel (c).

auditory system also caused the asymmetries of hearing sensitivity [25] and of auditory brainstem response [27].

adults and newborns may in part be due to the smaller ear canal volume in newborns.

4.2. SOAE Level in full-term neonates

4.3. SOAE frequency in full-term neonates

In literature, the SOAE level in adults was reported to amount – 10 to 20 dB SPL. In this study, the SOAE level in the newborns ranged from 6.4 to 39.6 dB SPL and in accordance with form studies [28]. It is possible that the difference in SOAE level between

In this study, SOAE in full-term neonates were recorded at higher frequencies (3.2–3.7 kHz). This was in accordance with findings of other studies in infants (3–4 kHz [4]), but higher than those seen in adults (1–2 kHz [29]). Although the precise cause for

[(Fig._2)TD$IG]

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Fig. 2. Distribution of SOAE frequency by gender in full-term neonates. Panels (a) and (b) display the SOAE frequceny distribution by gender. The x axis displays the SOAE frequency (Hz), the y axis displays the case (number). Panel (c) displays the stastic value of SOAE frequceny distribution by gender. In panel (c), the means of difference ears are displayed by the solid lines across each box, respectively. The upper and lower bounds of each box bounds represent the quartiles. The whisker away from the box bounds showed the 1.25 SD of the mean, and the filled circles represent the data are outside the end of whisker. The p value is indicated on panel (c).

the higher SOAE frequencies in newborns compared to adults is not clear, it is highly likely that differences in the general growth/ developmental characteristics of the middle and/or the external ear in newborns and adults play a role. Westwood and Bamford [29] compared the mean resonance frequency in un-sedated infants and adults using a probe-tube microphone and demonstrated that mean infant resonance frequency (4.2 kHz) was significantly higher than the mean adult resonance frequency (2.95 kHz; p < 0.05). Moreover, the size of the resonance peak was

found to vary positively with the ear canal volume. The high resonance frequency resulted in easier transmission and subsequently better detection of the high frequency SOAEs in infants than in adults. 4.4. SOAE number in full-term neonates The current study has shown that the SOAE peak number was greater, and ears with multiple SOAEs more frequent, similar to that

B. Qi et al. / International Journal of Pediatric Otorhinolaryngology 78 (2014) 2286–2291

shown in adults (3.0 at 20–29years, 3.3 at 30–39years, 2.6 at 40–49 years [28]). However, these findings were not in accordance with the findings from other studies [13]. Also, the current study did not show any significant differences in SOAE numbers with respect to either gender or ear-side. Whilst, it was possible that this was a true reflection of the status with regard to SOAE number in newborns, the possibility that the lack of any significant difference in SOAE numbers in either gender or ear-side observed in the present study may be due to the relatively small size of the study cohort employed cannot be discounted. Thus, further studies with larger cohorts are clearly needed to both confirm the present findings. In the future studies, it would also be of interest to clarify whether the investigated characteristics of SOAE are dependent on genetic determination or functional maturation of the peripheral auditory system and its controlling efferents. Acknowledgments The authors thank Prof. Yisheng Qi and Liansheng Guo from the Beijing Institute of Otolaryngology for their helpful comments on this manuscript. This study was supported by Ministry of Health Foundation (201202005), Capital Clinic and Applied research Foundation (Z131107002213123) and Capital Medical R&D Program (No.20091049). References [1] W.E. Brownell, Outer hair cell electromotility and otoacoustic emissions, Ear Hear. 11 (2) (1990) 82–92. [2] W.A. Harrison, S.J. Norton, Characteristics of transient evoked otoacoustic emissions in normal-hearing and hearing-impaired children, Ear Hear. 20 (1) (1999) 75–86. [3] W.W. Jedrzejczak, S. Hatzopoulos, L. Sliwa, E. Pilka, K. Kochanek, H. Skarzynski, Otoacoustic emissions in neonates measured with different acquisition protocols, Int. J. Pediatr. Otorhinolaryngol. 76 (3) (2012) 382–387. [4] E.M. Burns, K.H. Arehart, S.L. Campbell, Prevalence of spontaneous otoacoustic emissions in neonates, J. Acoust. Soc. Am. 91 (1992) 1571–1575. [5] T. Morlet, L. Collet, R. Duclaux, A. Lapillonne, B. Salle, G. Putet, et al., Spontaneous and evoked otoacoustic emissions in pre-term and full-term neonates: is there a clinical application? Int. J. Peidatr. Otorhinolaryngol. 33 (3) (1995) 207–211. [6] D.T. Kemp, P. Bray, L. Alexander, A.M. Brown, Acoustic emission cochleography – practical aspects, Scand. Audiol. Suppl. 25 (1986) 71–95. [7] G. Cianfrone, M. Mattia, Spontaneous otoacoustic emissions from normal ears. Preliminary report, Scand. Audiol. Suppl. 25 (1986) 121–127.

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