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Otoacoustic emissions and auditory assessment in infants at risk for early brain damage
International Journal of Pediatric Otorhinolaryngology 58 (2001) 139– 145 www.elsevier.com/locate/ijporl
Otoacoustic emissions and auditory assessment in infants at risk for early brain damage Jagoda Vatovec a,*, Milivoj Velickovic Perat b, Lojze S& mid a, Anton Gros a a
Uni6ersity Department of Otorhinolaryngology and Cer6icofacial Surgery, Clinical Center, 1525 Ljubljana Zalosˇka 2, Slo6enia b Uni6ersity Paediatric Hospital, Dept. of De6elopmental Neurology, 1525 Ljubljana Vrazo6 trg 1, Slo6enia Received 27 May 2000; received in revised form 8 December 2000; accepted 10 December 2000
Abstract The importance of early hearing screening has long been recognized, as the prognosis for the hearing impaired child is improved when the diagnosis is made as early as possible, and the intervention is begun immediately. For clinical screening of hearing impairment, the recording of otoacoustic emissions was recomended. As some risk factors for early brain damage are at the same time also risk factors for dysfunction of auditory system, we presumed that infants at risk for brain damage have hearing impairment more frequently than the rest of the population of the same age. We were interested in the role of otoacoustic emission testing during the assessment of auditory function in these infants. There were 110 infants at risk for brain damage included in the study. After thorough otorhinolaryngological examination, auditory function was estimated by recording of otoacoustic emissions, tympanometry, pure tone audiometry and, when necessary, auditory brainstem responses. Otoacoustic emissions were recorded by MadsenElectronics Celesta 503 in an acoustically treated sound room. We registered spontaneous as well as transient and distortion product otoacoustic emissions. The neurologist formed two groups with different degrees of neurological risk. The collected results of auditory function were compared with the degree of neurological risk. For the statistical analysis, the procedure 2 and Fischer test were used. Spontaneous otoacoustic emission was detected in 38.2% of examinees. Evoked otoacoustic emissions were registered in 87.3% of infants. The testing had to be repeated in 32.7% of infants. We observed evoked otoacoustic emissions to be present also in a child with sensorineural hearing impairment and no auditory brainstem responses. Up to 32.7% of infants at risk for brain damage were hard of hearing. Conductive hearing loss was discovered with 25.4% of infants, and eight (7.3%) had sensorineural hearing impairment. In the group of examinees with only risk factors 3.6% had sensorineural impairment and in a group with abnormal motor development, there were 18.5% with that kind of hearing loss. Fischer test confirmed a statistically significant difference between the groups. Infants at risk for brain damage have more frequently impaired auditory function than their peers. For this reason, it is especially important to focus attention on the hearing condition when dealing with this population. Recording of evoked otoacoustic emissions is very helpful in pediatric audiometry, but any interpretation of the results should consider the possibility of auditory neuropathy. © 2001 Elsevier Science Ireland Ltd. All rights reserved.
* Corresponding author. Tel.: + 386-61-1431315; fax: + 386-61-1431315. E-mail address: [email protected] (J. Vatovec). 0165-5876/01/$ - see front matter © 2001 Elsevier Science Ireland Ltd. All rights reserved. PII: S 0 1 6 5 - 5 8 7 6 ( 0 1 ) 0 0 4 1 9 - 0
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J. Vato6ec et al. / Int. J. Pediatr. Otorhinolaryngol. 58 (2001) 139–145
Keywords: Infants at risk; Deafness; Hearing screening; Labyrinth dysfunction
1. Introduction The integrity of the auditory system in early childhood is of utmost importance for the normal acquisition of language and speech. It is also essential for social and emotional development. For this reason, hearing loss in infancy has a special significance. The prognosis for the hearing-impaired child is improved when diagnosis is made as early as possible, and habilitation follows immediately [1–3]. Markides found that when habilitation with a hearing aid is begun in infancy, speech and language are better than when it is implemented at a later age [4]. This is supported by several studies [5 – 7]. Severe congenital hearing impairment is present in approximately one in every 1000 live births [1,8]. The prevalence of hearing impairment is higher among the population of neonatal intensive care units. Many of these infants have one or more high-risk factors for hearing loss [8 – 10]. Some risk factors for hearing impairment are at the same time also risk factors for a brain damage. The child with early brain damage frequently presents abnormal motor development. Other brain functions can also be affected, either due to the same cause as the motor dysfunction or, secondarily, due to other existing brain damage [11,12]. To detect children with developmental disorder early enough, a thorough and regular control of all would be necessary from the prenatal period onwards. However, such an extensive control is dependent on the sufficiently developed medical service. With a preliminary selection of children who have risk factors for a developmental disorder, the group can be narrowed down. In such narrowed groups, if the selection is carried out properly, the number of children who will actually develop a disturbance is higher than in the remaining majority. Screening tests as well are very helpful for an early identification of hearing disorders. Measurement of otoacoustic emissions (OAE) is clinically used as hearing screening method for the last decade. OAE were first described in humans by Kemp [13]. Spontaneous
otoacoustic emissions (SOAE) are recorded in the absence of the external sound stimuli, and evoked OAE are induced by sound stimuli in healthy ears [14]. The aim of our study was to assess the auditory function in infants at risk for early brain damage. Our presumption was that infants at risk for early brain damage have hearing loss more frequently than the rest of the population of the same age. We were also interested in the role of otoacoustic emission testing in identification of the site of lesion in the auditory pathway.
2. Patients and methods There were 110 infants, 66 boys and 44 girls at the age of 10–12 months, included in the study. Because of a suspected developmental disorder, they were examined by a developmental neurologist, who formed two groups with different degrees of risk for brain damage: Group A consisting of 83 infants with only a history of risk factors and a Group B consisting of 27 infants with motor disorders. All the infants were checked for their hearing ability after a thorough otorhinolaryngological examination, by registration of OAE, tympanometry, tone audiometry and, when necessary, auditory brainstem responses (ABR). During the measurements, the infants were held in their mother’s arms. OAE were recorded by MadsenElectronics Celesta 503. With SOAE testing, we detected narrow-band signals at one or more frequences in the range of 500 –5000 Hz of 15 dB SPL or more. Transient evoked otoacoustic emissions (TOAE) were recorded after performing an 80 dB SPL non-linear acoustic click for 80 ms. The response was 3000 time-averaged to enhance signal-to-noise ratio and analysed by a Fast Fourier Transform (FFT) to obtain a frequency spectrum in the range of 500 –4000 Hz. Distortion product otoacoustic emissions (DP) were measured after presenting two simultaneous pure tone signals with f2/f1 = 1.22 at a level of 70 dB SPL at 500,
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1000, 2000 and 4000 Hz. The responses were 300 time-averaged to produce an FFT response spectrum. The tympanometry was recorded by Interacoustics Impedancemeter AT 22. Sound-field audiometry for frequences of 500, 1000, 2000 and 4000 Hz was performed by the Interacoustics Peep show unit PS 2. Measurements of ABR were done under sedation with chloralhydrate using a Viking IV (Nicolet Biomedical Instruments) only in infants who had despite of tympanogram A unrecorded TOAE and DP and/or with sound field audiometry estimated thresholds for speech frequences above 30 dB. All the infants were also subjected to vestibular checks, both by assessment of spontaneous symptoms of dysfunction and by the evaluation of reactions evoked by caloric stimulation of the labyrinths. The direction, degree and duration of the evoked nystagmus were observed. The results of auditory and vestibular function were compared with the degree of neurological risk. 2 and Fischer test were used for statistical analysis of the collected data.
3. Results SOAE were detected only in 42 infants (38.2%) despite repeated attempts. TOAE were registered in the first examination in 74 infants (67.3%). In the check-up examination and after medical treatment of the remaining 36 children, TOAE were not recorded in 14 (12.7%), with two of them only in one ear. DP were evoked in 89 children (80.9%) in all tested frequences, but in 21 (19.1%), they
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were not recorded in spite of repeated measurements. With otoscopy and tympanometry, we confirmed middle-ear problems in 28 (25.4%) infants. After conservative treatment, the tympanogram remained type B in seven. No OAE were detected in either of them. Sound-field audiometry showed thresholds for speech frequences to be higher than 30 dB in 36 (32.7%) infants. Middle-ear problems were found in 28 of these. After medical treatment, there were still 15 infants whose thresholds were unreliable or higher than 30 dB. They underwent ABR testing. In seven infants, the threshold for waveform N5 could be detected on both ears with click of 30 dB HL. Two infants had on one side a threshold for click of 30 dB HL but on the other side a threshold for click of 80 dB HL. Two other infants had tresholds for click of 60 dB HL bilaterally. In one child, N5 could be detected only with a click of 100 dB HL on both ears that corresponded to behavioral testing. Three infants had no ABR waveform, even with a click of 105 dB HL. This was in agreement with behavioral testing in two of them. Despite an absence of waveforms on ABR testing present, the third infant had TOAE and DP in both ears as well as sound-field thresholds of 70 dB in speech frequences bilateraly. We concluded that 36 out of 110 infants, that is 32.7%, at risk for early brain damage had impaired hearing (Table 1). There were 24 (28.9%) infants with hearing impairment discovered in the Group A and 12 (44.4%) in the Group B. Despite the higher percentage of hearing impairment among infants with neurologically abnormal
Table 1 Results of auditory and vestibular assessment in infants Statoacoustic findings
Infants with risk factors only (n= 83)
Infants with motor disorder (n =27)
Total (n =110)
Normal hearing Conductive hearing impairment Sensorineural hearing impairment
59 (71.1%) 21 (25.3%) 3 (3.6%)
15 (55.6%) 7 (25.9%) 5 (18.5%)
74 (67.3%) 28 (25.5%) 8 (7.2%)
8 (9.6%)
8 (29.6%)
P =0.02 16 (14.5%) P =0.01
Vestibular disfunction
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symptoms, this figure was not found to be statistically significant ( 2 = 2.23). Eight (7.2%) of the examined infants had sensorineural hearing loss. Sensorineural hearing loss was discovered in three (3.6%) out of 83 infants with only risk factors and in five (18.5%) of 27 children with abnormal motor development. The Fischer test confirmed a statistically significant difference between these groups (P = 0.02). Three (2.7%) infants were deaf, and three others had a bilateral sensorineural impairment. In one child with a severe sensorineural hearing impairment, a neuropathy of the acoustic nerve was suspected as the ABRs were not detected, but EOAE were recorded, despite a 70 dB loss in speech frequencies. Two infants had severe unilateral sensorineural hearing loss. Conductive hearing loss was discovered in 28 (25.5%) of the examined infants. Causes of the latter were identified as: acute inflammation of the middle ear in six (5.5%) infants, otitis media with effusion in 20 (18.2%) and developmental anomaly, in the form of meatal stenosis, in two (1.8%) examinees . In 16 (14.5%) infants, the caloric test showed a disorder in their vestibular apparatus function. Unilateral hypoexcitability of the labyrinths was found in 13 (11.8%) children, while in three (2.7%), the labyrinths failed to respond to the stimulation bilaterally. In Group A, eight out of 83 (9.6%) were found to have vestibular apparatus damage, while in Group B, eight out of 27 (29.6%) had a vestibular disorder. A statistically significant correlation was established between the degree of neurological risk and vestibular dysfunction (P= 0.01). Out of 16 infants with vestibular disorder, three were deaf.
4. Discussion SOAE were successfully recorded in 42 infants (38.2%). Strickland and his team also reported successful measurements in only 40 – 60% when testing healthy ears [15]. The incidence is higher with females, and this fact was also confirmed in our research. SOAE were namely recorded in 30 girls and 12 boys. The amplitudes are somewhat
higher in children than in adults, probably because of the difference in size of the outer ear canal [16]. TOAE provide, for their simplicity, quick results and responsiveness with practically every healthy ear recommended as screening test with new-borns and small children [17,18]. We successfully evoked TOAE in 96 infants (87.3%), in 14 infants (12.7%), but the emissions were not recorded in spite of frequent attempts. Seven infants in the latter group had a middle-ear disorder and consequently conductive hearing impairment. Many agree that TOAE can be an indicator of conductive, as well as sensorineural, hearing impairment [19]. In the remaining seven infants, in whom there were no OAE registered, sensorineural hearing impairment was confirmed with other diagnostic procedures. The interpretation of positive test results should be cautious as we observed TOAE and DP also in one infant with a moderate hearing impairment. It was concluded that the functioning of outer hair cells is preserved and that the defect is situated behind the cochlea. Doyle and coworkers emphasize the importance of TOAE in diagnostics of central auditory pathways, especially in those who do not co-operate well in subjective diagnostic procedures [20]. Suckful and his team reported that they managed to record DP, even in cases of hearing impairment with 50–70 dB loss [21]. Kon reported DP to be more prominent at high frequences, which may reflect different functions of outer hair cells [22]. In our research, DP were evoked in 89 infants (80.9%). DP measuring takes more time than TOAE, and its feasibility is also more lacking because of the restlessness of small children. The procedure was disturbed by external noises as well as an incorrectly inserted measuring probe. In our study, we found that up to 32.7% of examined at risk infants referred for neurological examination did not have normal hearing. No child had visited the physician previously through problems with auditory function or ear disease. Hearing impairment is not readily apparent, and infants with sound deprivation have the same prespeech vocal production (babbling, crying) as normal hearing peers, so parents can easily overlook it. Sensorineural hearing loss was detected in 7.3% of infants at risk for brain damage. This is a
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substantially higher percentage than 0.2 – 0.5% found in the entire population of the same age [18,19]. In four of the infants with bilateral sensorineural impairment, rehabilitation with hearing aids was commenced. Three infants out of 110 (2.7%) were deaf. This high percentage indicates a more frequent hearing handicap within the group of infants at risk for early brain damage than within the general population of the same age in our country, where the percentage with a profound hearing loss is 0.09% [23]. Krageloh-Mann and coworkers found a similar percentage of 3% deafness in their study of children with cerebral palsy [24]. In the two deaf infants, surgery for cochlear implantation is planned. Deaf children commonly benefit from early intervention, and a cochlear implant can be a critical turning point for their future life [25]. Auditory neuropathy was suspected in one child with a severe hearing loss for pure tones, absent ABR and recordable evoked OAE. This followed the opinion of Ferber-Viart and coworkers, who studied OAE and ABR in children with neurological afflictions: when no wave is identifiable by ABR, the presence of evoked OAE indicates retrocochlear damage [26]. Doyle and coworkers point out the therapeutic challenge in childhood auditory neuropathy where the implementation of hearing aids seems to be of little benefit [20]. Two infants had unilateral sensorineural hearing loss. Vartiainen and Karjalainen reported the prevalence of this kind of hearing impairment to be 1.7 per 1000 livebirths [27]. The potential impact of unilateral sensorineural hearing loss is frequently underestimated. Bovo and coworkers demonstrated its serious negative consequences in areas of auditory, psycholinguistic skills and educational progress [28]. In Group A, 3.6% had sensorineural hearing loss, and in Group B, there were 18.5% with a similar hearing impairment. A statistically significant difference between the groups was confirmed by the Fischer test (P = 0.02). We conclude that it is necessary to be highly attentive to auditory function, especially when dealing with infants who have motor dysfunction. Conductive hearing loss was discovered in 25.4% of the examined infants, in line with earlier studies [19,29]. It is known that otitis media has a
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high prevalence among the neonatal intensive care unit population. With immunological immaturity, an indwelling nasotracheal tube can be an important factor in the development of middle-ear problems. Residual mesenchyme in the middle ear of premature infants is also likely to play a role in the etiology of otitis media in these infants [30]. Another possible factor can be the lack of breastfeeding and sucking, which can have an influence on the development of the visceral part of the cranium [31]. In our study, adequate responses to caloric stimulation of labyrinths were achieved in 85.5% of infants, which is consistent with the report by Eviatar and Eviatar [32]. A vestibular disorder was established in 14.5% of infants at risk for early brain damage. Those with abnormal neurological signs presented with vestibular dysfunction more frequently than those with risk factors only. The association between vestibular disorder and the degree of neurological risk was statistically significant, which is probably attributable to a disorder along the vestibulo-ocular reflex arch rather than a disorder in the labyrinth alone. Three (18.7%) out of 16 (14.5%) infants with a vestibular apparatus dysfunction were deaf. Eviatar and Eviatar believe that the delay in posture development in infants with congenital hearing disorder can be attributed to vestibular apparatus damage [33]. Selz and coworkers found greater changes in electronystagmography of deaf children than in their normal-hearing peers [34]. According to Kaga, the vestibular apparatus dysfunction in infants is well compensated for, owing to numerous connections within the central nervous system [35]. Therefore, damage that occurs in childhood can be detected incidentally at a later systematic physical examination [36]. The process of vestibular compensation can be accelerated by daily physical exercises [37]. 5. Conclusion TOAE testing is highly suitable as a screening test because it can be carried out very easily, and it does not take much time. Caution, however, is advised when interpreting results, as a defect in the central auditory pathway can be overlooked.
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Infants at risk of early brain damage have more frequently impaired hearing than their peers. In infants with abnormal motor development in particular, it is also necessary to be attentive to vestibular dysfunction and to assure assistance with motor skills. The prompt recognition of hearing impairment and disturbances in vestibular functioning in infants will prevent secondary consequences of hearing and/or vestibular impairments, which can influence significantly the quality of an infant’s future life.
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[13] D.T. Kemp, Stimulated acoustic emissions from within the human auditory system, J. Acoust. Soc. Am. 64 (1978) 1386– 1391. [14] B. Lonsbury-Martin, M. Witehead, G. Martin, Clinical applications of otoacoustic emissions, Hear. Res. 34 (1991) 964– 979. [15] A.E. Strickland, E.M. Burns, A. Tubis, Incidence of spontaneous otoacoustic emissions in children and infants, J. Acoust. Soc. Am. 78 (1985) 931– 935. [16] B.A. Stach, Clinical Audiology, Singular Publishing Group, San Diego, CA, 1998, pp. 193– 256. [17] J.C. Stevens, H.D. Webb, J. Hutchinson, J. Connell, M.F. Smith, J.T. Buffin, Click evoked otoacoustic emissions in neonatal screening, Ear Hear. 11 (1990) 128– 133. [18] A. Mehl, V. Thomson, Newborn hearing screening: the great omission, Pediatrics 101 (1998) 1 – 6. [19] K. White, B. Vohr, T. Behrens, Universal newborn hearing screening using transient evoked otoacoustic emissions: results of the Rhode island hearing assessment project, Semin. Hear. 14 (1993) 18 – 29. [20] K.J. Doyle, Y. Sininger, A. Starr, Auditory neuropathy in childhood, Laryngoscope 108 (9) (1998) 1374– 1377. [21] M. Suckfull, S. Schneeweiss, A. Dreher, K. Schorn, Evaluation of TEOAE and DPOAE measurements for the assessment of auditory thresholds in sensorineural hearing loss, Acta Otolaryngol. (Stockh.) 116 (1996) 528– 533. [22] K. Kon, M. Inagaki, M. Kaga, Developmental changes of distortion product and transient evoked otoacoustic emissions in different age groups, Brain Dev. 22 (2000) 41 – 46. [23] J. Vatovec, S. Cernelc, Prispevek k epidemiologiji naglusˇnosti, in: N. Ribnikar-Kastelic (Ed.), Usposabljanje slusˇno prizadetih na Slovenskem, Zavod za usposabljanje slusˇno in govorno prizadetih, Ljubljana, 1989, pp. 67 – 73. [24] I. Krageloh-Mann, G. Hagberg, C. Meisner, B. Schelp, G. Haas, K. Eeg-Olofsson, H. Selbmann, B. Hagberg, R. Michaelis, Bilateral spastic cerebral palsy — a comparative study between south.west Germany and western Sweden. I: clinical patterns and disabilities, Dev. Med. Child Neurol. 35 (1993) 1037– 1047. [25] M. Somers, Effects of cochlear implants in children: implications for rehabilitation, in: H. Cooper (Ed.), Cochlear Implants, Whurr Publishers, London, 1991, pp. 322– 345. [26] C. Ferber-Viart, R. Duclaux, C. Dubreuil, F. Sevin, L. Collet, J.C. Berthier, Otoacoustic emissions and brainstem auditory evoked potentials in children with neurological afflictions, Brain Dev. 16 (1994) 213– 218. [27] E. Vartiainen, S. Karjalainen, Prevalence and etiology of unilateral sensorineural hearing impairment in a Finnish childhood population, Int. J. Pediatr. Otorhinolaryngol. 43 (1998) 253– 259. [28] R. Bovo, A. Martini, M. Agnoletto, Auditory and academic performance of children with unilateral hearing loss, Scand. Audiol. Suppl. 30 (1988) 71 – 74. [29] B. Arnold, K. Schorn, M. Stecker, Screening program for selection of hearing loss in newborn infants instituted by the European Community, Laryngorhinootologie 74 (1995) 172– 178.
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Vestibular deficits in deaf children, Otolaryng. Head Neck 115 (1996) 70 – 77. [35] K. Kaga, H. Maeda, J. Suzuki, Development of righting reflexes, gross motor functions and balance in infants with labyrinth hypoactivity with or without mental retardation, Adv. Oto-Rhyno-Laryng. 41 (1988) 152– 161. [36] J. Vatovec, S. Cernelc, J. Primozic, M. Zargi, Children with vestibular dysfunction, in: C.F. Claussen, M.V. Kirtane, D. Schneider (Eds.), Proceedings of the XXth Scientific Meeting of Neurootological and Equilibriometric Society Linkoping 1993, Hamburg, medicin + pharmacie dr werner rudat & co, 1995, pp. 357– 360. [37] S. Telian, N. Shepard, M. Smith-Wheelock, J. Kemink, Habituation therapy for chronic vestibular dysfunction, Otolaryng. Head Neck 103 (1990) 89 – 96.
[30] L. Proctor, D. Kennedy, High risk newborns who fail hearing screening: implications of otological problems, Semin. Hear. 11 (1990) 167–176. [31] A. S& ercer, Embriologija. Otorinolaringologija I, Jugoslavenski leksikografski zavod, Zagreb, 1966, pp. 159– 190. [32] L. Eviatar, A. Eviatar, The neurovestibular testing of infants and children, in: C. Bluestone, S. Stool (Eds.), Pediatric Otolaryngology, vol. 1, W.B. Saunders Company, Philadelphia, PA, 1983, pp. 199–212. [33] L. Eviatar, A. Eviatar, Neurovestibular examination of infants and children, Adv. Oto-Rhino-Laryng. 23 (1978) 169– 191. [34] P.A. Selz, M. Girardi, H.R. Konrad, L.F. Hughes,
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Otoacoustic emissions and auditory assessment in infants at risk for early brain damage Jagoda Vatovec a,*, Milivoj Velickovic Perat b, Lojze S& mid a, Anton Gros a a
Uni6ersity Department of Otorhinolaryngology and Cer6icofacial Surgery, Clinical Center, 1525 Ljubljana Zalosˇka 2, Slo6enia b Uni6ersity Paediatric Hospital, Dept. of De6elopmental Neurology, 1525 Ljubljana Vrazo6 trg 1, Slo6enia Received 27 May 2000; received in revised form 8 December 2000; accepted 10 December 2000
Abstract The importance of early hearing screening has long been recognized, as the prognosis for the hearing impaired child is improved when the diagnosis is made as early as possible, and the intervention is begun immediately. For clinical screening of hearing impairment, the recording of otoacoustic emissions was recomended. As some risk factors for early brain damage are at the same time also risk factors for dysfunction of auditory system, we presumed that infants at risk for brain damage have hearing impairment more frequently than the rest of the population of the same age. We were interested in the role of otoacoustic emission testing during the assessment of auditory function in these infants. There were 110 infants at risk for brain damage included in the study. After thorough otorhinolaryngological examination, auditory function was estimated by recording of otoacoustic emissions, tympanometry, pure tone audiometry and, when necessary, auditory brainstem responses. Otoacoustic emissions were recorded by MadsenElectronics Celesta 503 in an acoustically treated sound room. We registered spontaneous as well as transient and distortion product otoacoustic emissions. The neurologist formed two groups with different degrees of neurological risk. The collected results of auditory function were compared with the degree of neurological risk. For the statistical analysis, the procedure 2 and Fischer test were used. Spontaneous otoacoustic emission was detected in 38.2% of examinees. Evoked otoacoustic emissions were registered in 87.3% of infants. The testing had to be repeated in 32.7% of infants. We observed evoked otoacoustic emissions to be present also in a child with sensorineural hearing impairment and no auditory brainstem responses. Up to 32.7% of infants at risk for brain damage were hard of hearing. Conductive hearing loss was discovered with 25.4% of infants, and eight (7.3%) had sensorineural hearing impairment. In the group of examinees with only risk factors 3.6% had sensorineural impairment and in a group with abnormal motor development, there were 18.5% with that kind of hearing loss. Fischer test confirmed a statistically significant difference between the groups. Infants at risk for brain damage have more frequently impaired auditory function than their peers. For this reason, it is especially important to focus attention on the hearing condition when dealing with this population. Recording of evoked otoacoustic emissions is very helpful in pediatric audiometry, but any interpretation of the results should consider the possibility of auditory neuropathy. © 2001 Elsevier Science Ireland Ltd. All rights reserved.
* Corresponding author. Tel.: + 386-61-1431315; fax: + 386-61-1431315. E-mail address: [email protected] (J. Vatovec). 0165-5876/01/$ - see front matter © 2001 Elsevier Science Ireland Ltd. All rights reserved. PII: S 0 1 6 5 - 5 8 7 6 ( 0 1 ) 0 0 4 1 9 - 0
140
J. Vato6ec et al. / Int. J. Pediatr. Otorhinolaryngol. 58 (2001) 139–145
Keywords: Infants at risk; Deafness; Hearing screening; Labyrinth dysfunction
1. Introduction The integrity of the auditory system in early childhood is of utmost importance for the normal acquisition of language and speech. It is also essential for social and emotional development. For this reason, hearing loss in infancy has a special significance. The prognosis for the hearing-impaired child is improved when diagnosis is made as early as possible, and habilitation follows immediately [1–3]. Markides found that when habilitation with a hearing aid is begun in infancy, speech and language are better than when it is implemented at a later age [4]. This is supported by several studies [5 – 7]. Severe congenital hearing impairment is present in approximately one in every 1000 live births [1,8]. The prevalence of hearing impairment is higher among the population of neonatal intensive care units. Many of these infants have one or more high-risk factors for hearing loss [8 – 10]. Some risk factors for hearing impairment are at the same time also risk factors for a brain damage. The child with early brain damage frequently presents abnormal motor development. Other brain functions can also be affected, either due to the same cause as the motor dysfunction or, secondarily, due to other existing brain damage [11,12]. To detect children with developmental disorder early enough, a thorough and regular control of all would be necessary from the prenatal period onwards. However, such an extensive control is dependent on the sufficiently developed medical service. With a preliminary selection of children who have risk factors for a developmental disorder, the group can be narrowed down. In such narrowed groups, if the selection is carried out properly, the number of children who will actually develop a disturbance is higher than in the remaining majority. Screening tests as well are very helpful for an early identification of hearing disorders. Measurement of otoacoustic emissions (OAE) is clinically used as hearing screening method for the last decade. OAE were first described in humans by Kemp [13]. Spontaneous
otoacoustic emissions (SOAE) are recorded in the absence of the external sound stimuli, and evoked OAE are induced by sound stimuli in healthy ears [14]. The aim of our study was to assess the auditory function in infants at risk for early brain damage. Our presumption was that infants at risk for early brain damage have hearing loss more frequently than the rest of the population of the same age. We were also interested in the role of otoacoustic emission testing in identification of the site of lesion in the auditory pathway.
2. Patients and methods There were 110 infants, 66 boys and 44 girls at the age of 10–12 months, included in the study. Because of a suspected developmental disorder, they were examined by a developmental neurologist, who formed two groups with different degrees of risk for brain damage: Group A consisting of 83 infants with only a history of risk factors and a Group B consisting of 27 infants with motor disorders. All the infants were checked for their hearing ability after a thorough otorhinolaryngological examination, by registration of OAE, tympanometry, tone audiometry and, when necessary, auditory brainstem responses (ABR). During the measurements, the infants were held in their mother’s arms. OAE were recorded by MadsenElectronics Celesta 503. With SOAE testing, we detected narrow-band signals at one or more frequences in the range of 500 –5000 Hz of 15 dB SPL or more. Transient evoked otoacoustic emissions (TOAE) were recorded after performing an 80 dB SPL non-linear acoustic click for 80 ms. The response was 3000 time-averaged to enhance signal-to-noise ratio and analysed by a Fast Fourier Transform (FFT) to obtain a frequency spectrum in the range of 500 –4000 Hz. Distortion product otoacoustic emissions (DP) were measured after presenting two simultaneous pure tone signals with f2/f1 = 1.22 at a level of 70 dB SPL at 500,
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1000, 2000 and 4000 Hz. The responses were 300 time-averaged to produce an FFT response spectrum. The tympanometry was recorded by Interacoustics Impedancemeter AT 22. Sound-field audiometry for frequences of 500, 1000, 2000 and 4000 Hz was performed by the Interacoustics Peep show unit PS 2. Measurements of ABR were done under sedation with chloralhydrate using a Viking IV (Nicolet Biomedical Instruments) only in infants who had despite of tympanogram A unrecorded TOAE and DP and/or with sound field audiometry estimated thresholds for speech frequences above 30 dB. All the infants were also subjected to vestibular checks, both by assessment of spontaneous symptoms of dysfunction and by the evaluation of reactions evoked by caloric stimulation of the labyrinths. The direction, degree and duration of the evoked nystagmus were observed. The results of auditory and vestibular function were compared with the degree of neurological risk. 2 and Fischer test were used for statistical analysis of the collected data.
3. Results SOAE were detected only in 42 infants (38.2%) despite repeated attempts. TOAE were registered in the first examination in 74 infants (67.3%). In the check-up examination and after medical treatment of the remaining 36 children, TOAE were not recorded in 14 (12.7%), with two of them only in one ear. DP were evoked in 89 children (80.9%) in all tested frequences, but in 21 (19.1%), they
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were not recorded in spite of repeated measurements. With otoscopy and tympanometry, we confirmed middle-ear problems in 28 (25.4%) infants. After conservative treatment, the tympanogram remained type B in seven. No OAE were detected in either of them. Sound-field audiometry showed thresholds for speech frequences to be higher than 30 dB in 36 (32.7%) infants. Middle-ear problems were found in 28 of these. After medical treatment, there were still 15 infants whose thresholds were unreliable or higher than 30 dB. They underwent ABR testing. In seven infants, the threshold for waveform N5 could be detected on both ears with click of 30 dB HL. Two infants had on one side a threshold for click of 30 dB HL but on the other side a threshold for click of 80 dB HL. Two other infants had tresholds for click of 60 dB HL bilaterally. In one child, N5 could be detected only with a click of 100 dB HL on both ears that corresponded to behavioral testing. Three infants had no ABR waveform, even with a click of 105 dB HL. This was in agreement with behavioral testing in two of them. Despite an absence of waveforms on ABR testing present, the third infant had TOAE and DP in both ears as well as sound-field thresholds of 70 dB in speech frequences bilateraly. We concluded that 36 out of 110 infants, that is 32.7%, at risk for early brain damage had impaired hearing (Table 1). There were 24 (28.9%) infants with hearing impairment discovered in the Group A and 12 (44.4%) in the Group B. Despite the higher percentage of hearing impairment among infants with neurologically abnormal
Table 1 Results of auditory and vestibular assessment in infants Statoacoustic findings
Infants with risk factors only (n= 83)
Infants with motor disorder (n =27)
Total (n =110)
Normal hearing Conductive hearing impairment Sensorineural hearing impairment
59 (71.1%) 21 (25.3%) 3 (3.6%)
15 (55.6%) 7 (25.9%) 5 (18.5%)
74 (67.3%) 28 (25.5%) 8 (7.2%)
8 (9.6%)
8 (29.6%)
P =0.02 16 (14.5%) P =0.01
Vestibular disfunction
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symptoms, this figure was not found to be statistically significant ( 2 = 2.23). Eight (7.2%) of the examined infants had sensorineural hearing loss. Sensorineural hearing loss was discovered in three (3.6%) out of 83 infants with only risk factors and in five (18.5%) of 27 children with abnormal motor development. The Fischer test confirmed a statistically significant difference between these groups (P = 0.02). Three (2.7%) infants were deaf, and three others had a bilateral sensorineural impairment. In one child with a severe sensorineural hearing impairment, a neuropathy of the acoustic nerve was suspected as the ABRs were not detected, but EOAE were recorded, despite a 70 dB loss in speech frequencies. Two infants had severe unilateral sensorineural hearing loss. Conductive hearing loss was discovered in 28 (25.5%) of the examined infants. Causes of the latter were identified as: acute inflammation of the middle ear in six (5.5%) infants, otitis media with effusion in 20 (18.2%) and developmental anomaly, in the form of meatal stenosis, in two (1.8%) examinees . In 16 (14.5%) infants, the caloric test showed a disorder in their vestibular apparatus function. Unilateral hypoexcitability of the labyrinths was found in 13 (11.8%) children, while in three (2.7%), the labyrinths failed to respond to the stimulation bilaterally. In Group A, eight out of 83 (9.6%) were found to have vestibular apparatus damage, while in Group B, eight out of 27 (29.6%) had a vestibular disorder. A statistically significant correlation was established between the degree of neurological risk and vestibular dysfunction (P= 0.01). Out of 16 infants with vestibular disorder, three were deaf.
4. Discussion SOAE were successfully recorded in 42 infants (38.2%). Strickland and his team also reported successful measurements in only 40 – 60% when testing healthy ears [15]. The incidence is higher with females, and this fact was also confirmed in our research. SOAE were namely recorded in 30 girls and 12 boys. The amplitudes are somewhat
higher in children than in adults, probably because of the difference in size of the outer ear canal [16]. TOAE provide, for their simplicity, quick results and responsiveness with practically every healthy ear recommended as screening test with new-borns and small children [17,18]. We successfully evoked TOAE in 96 infants (87.3%), in 14 infants (12.7%), but the emissions were not recorded in spite of frequent attempts. Seven infants in the latter group had a middle-ear disorder and consequently conductive hearing impairment. Many agree that TOAE can be an indicator of conductive, as well as sensorineural, hearing impairment [19]. In the remaining seven infants, in whom there were no OAE registered, sensorineural hearing impairment was confirmed with other diagnostic procedures. The interpretation of positive test results should be cautious as we observed TOAE and DP also in one infant with a moderate hearing impairment. It was concluded that the functioning of outer hair cells is preserved and that the defect is situated behind the cochlea. Doyle and coworkers emphasize the importance of TOAE in diagnostics of central auditory pathways, especially in those who do not co-operate well in subjective diagnostic procedures [20]. Suckful and his team reported that they managed to record DP, even in cases of hearing impairment with 50–70 dB loss [21]. Kon reported DP to be more prominent at high frequences, which may reflect different functions of outer hair cells [22]. In our research, DP were evoked in 89 infants (80.9%). DP measuring takes more time than TOAE, and its feasibility is also more lacking because of the restlessness of small children. The procedure was disturbed by external noises as well as an incorrectly inserted measuring probe. In our study, we found that up to 32.7% of examined at risk infants referred for neurological examination did not have normal hearing. No child had visited the physician previously through problems with auditory function or ear disease. Hearing impairment is not readily apparent, and infants with sound deprivation have the same prespeech vocal production (babbling, crying) as normal hearing peers, so parents can easily overlook it. Sensorineural hearing loss was detected in 7.3% of infants at risk for brain damage. This is a
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substantially higher percentage than 0.2 – 0.5% found in the entire population of the same age [18,19]. In four of the infants with bilateral sensorineural impairment, rehabilitation with hearing aids was commenced. Three infants out of 110 (2.7%) were deaf. This high percentage indicates a more frequent hearing handicap within the group of infants at risk for early brain damage than within the general population of the same age in our country, where the percentage with a profound hearing loss is 0.09% [23]. Krageloh-Mann and coworkers found a similar percentage of 3% deafness in their study of children with cerebral palsy [24]. In the two deaf infants, surgery for cochlear implantation is planned. Deaf children commonly benefit from early intervention, and a cochlear implant can be a critical turning point for their future life [25]. Auditory neuropathy was suspected in one child with a severe hearing loss for pure tones, absent ABR and recordable evoked OAE. This followed the opinion of Ferber-Viart and coworkers, who studied OAE and ABR in children with neurological afflictions: when no wave is identifiable by ABR, the presence of evoked OAE indicates retrocochlear damage [26]. Doyle and coworkers point out the therapeutic challenge in childhood auditory neuropathy where the implementation of hearing aids seems to be of little benefit [20]. Two infants had unilateral sensorineural hearing loss. Vartiainen and Karjalainen reported the prevalence of this kind of hearing impairment to be 1.7 per 1000 livebirths [27]. The potential impact of unilateral sensorineural hearing loss is frequently underestimated. Bovo and coworkers demonstrated its serious negative consequences in areas of auditory, psycholinguistic skills and educational progress [28]. In Group A, 3.6% had sensorineural hearing loss, and in Group B, there were 18.5% with a similar hearing impairment. A statistically significant difference between the groups was confirmed by the Fischer test (P = 0.02). We conclude that it is necessary to be highly attentive to auditory function, especially when dealing with infants who have motor dysfunction. Conductive hearing loss was discovered in 25.4% of the examined infants, in line with earlier studies [19,29]. It is known that otitis media has a
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high prevalence among the neonatal intensive care unit population. With immunological immaturity, an indwelling nasotracheal tube can be an important factor in the development of middle-ear problems. Residual mesenchyme in the middle ear of premature infants is also likely to play a role in the etiology of otitis media in these infants [30]. Another possible factor can be the lack of breastfeeding and sucking, which can have an influence on the development of the visceral part of the cranium [31]. In our study, adequate responses to caloric stimulation of labyrinths were achieved in 85.5% of infants, which is consistent with the report by Eviatar and Eviatar [32]. A vestibular disorder was established in 14.5% of infants at risk for early brain damage. Those with abnormal neurological signs presented with vestibular dysfunction more frequently than those with risk factors only. The association between vestibular disorder and the degree of neurological risk was statistically significant, which is probably attributable to a disorder along the vestibulo-ocular reflex arch rather than a disorder in the labyrinth alone. Three (18.7%) out of 16 (14.5%) infants with a vestibular apparatus dysfunction were deaf. Eviatar and Eviatar believe that the delay in posture development in infants with congenital hearing disorder can be attributed to vestibular apparatus damage [33]. Selz and coworkers found greater changes in electronystagmography of deaf children than in their normal-hearing peers [34]. According to Kaga, the vestibular apparatus dysfunction in infants is well compensated for, owing to numerous connections within the central nervous system [35]. Therefore, damage that occurs in childhood can be detected incidentally at a later systematic physical examination [36]. The process of vestibular compensation can be accelerated by daily physical exercises [37]. 5. Conclusion TOAE testing is highly suitable as a screening test because it can be carried out very easily, and it does not take much time. Caution, however, is advised when interpreting results, as a defect in the central auditory pathway can be overlooked.
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Infants at risk of early brain damage have more frequently impaired hearing than their peers. In infants with abnormal motor development in particular, it is also necessary to be attentive to vestibular dysfunction and to assure assistance with motor skills. The prompt recognition of hearing impairment and disturbances in vestibular functioning in infants will prevent secondary consequences of hearing and/or vestibular impairments, which can influence significantly the quality of an infant’s future life.
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