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Is behavioral audiometry achievable in infants younger than 6 months of age?
International Journal of Pediatric Otorhinolaryngology 75 (2011) 1502–1509
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International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Is behavioral audiometry achievable in infants younger than 6 months of age? Monique Delaroche a, Isabelle Gavilan-Cellie´ a, Sylvie Maurice-Tison b, Alphonse Kpozehouen b, Rene´ Dauman a,c,* a
Pediatric Audiology Unit, Department of ORL-HNS, University Hospital of Bordeaux, France Inserm, ISPED, University of Bordeaux Segalen, France c UMR-CNRS 5287, University of Bordeaux Segalen, France b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 23 May 2011 Received in revised form 16 August 2011 Accepted 19 August 2011 Available online 19 September 2011
Background and goal: When carried out in addition to objective tests, behavioral audiometry performed in children with the so-called ‘‘Delaroche protocol’’ [IJORL 68 (2004) 1233-1243] enables to determine hearing thresholds by air and bone conduction over the whole auditory frequency range. In the present report, seventy-three hearing-impaired infants with different levels of motor and cognitive development were tested behaviorally before 6 months of age. Reliability of these early determined behavioral thresholds was then after analyzed using: (a) cross-sectional study, and (b) longitudinal study. Methods: Cross-sectional study compared click-evoked ABR thresholds in the better ear with binaural high-frequency hearing thresholds. In longitudinal study, early measured binaural hearing thresholds from 500 through 4000 Hz were reassessed at 18 months. Results: In 13% of babies behavioral testing was not fully completed by 6 months of age. Nevertheless, both cross-sectional and longitudinal studies yielded intraclass correlation coefficients above 0.80, suggesting that behavioral testing is applicable to this very young population. Conclusions: Assessment of hearing after newborn screening should not be restricted to objective tests before 5 months. It should also include bone- and air-conduction behavioral tests adjusted to developmental stage and performed in presence of parents. ß 2011 Elsevier Ireland Ltd. All rights reserved.
Keywords: Auditory brainstem responses Behavioral audiometry Psychomotor development Bone and air-conducted sounds Cognitive status Reinforcement
1. Introduction Much evidence suggests that, early in life, auditory input and communication are essential for the normal development of language, cognition, and behavior [1]. Newborn hearing screening is aimed at identifying hearing-impaired children as early as possible. Powerfulness of objective tests in measuring auditory thresholds over the first months is well documented. Otoacoustic emissions (OAE) and auditory brainstem response (ABR) tests are extensively used at this age. When performed in addition to these objective tests, behavioral audiometry (BA) enables to determine hearing thresholds by air and bone conduction over the whole auditory frequency range [2]. This information is essential to know as far as speech development is concerned. Second, by assessing ‘‘the response of the entire auditory system from the outer ear through the cortex’’ [3,4] BA enables to analyze how babies react to acoustic stimuli and, consequently, provides further information on their cognitive and
* Corresponding author at: Pediatric Audiology Department of ORL-HNS, Unit, University hospital of Bordeaux, France. Tel.: +33 556795993; fax: +33 556795669. E-mail address: [email protected] (R. Dauman). 0165-5876/$ – see front matter ß 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ijporl.2011.08.016
relational aptitudes [5]. In the follow-up of infants who failed newborn screening test, a behavioral measure of hearing [6] should be the gold standard against which results of objective diagnostic tests are compared. Even though above-mentioned capacities of BA are recognized from 5 to 6 months onwards [4,7–10], this method of exploring hearing is often considered to be unfeasible or unreliable below this age [11–13]. In contradiction to these restrictive assertions, researchers have evidenced astonishing precocity of babies’ sensory and mnemonic capacities, starting already in utero [14]. Given these early skills, audiometric assessment procedure known as ‘‘the Delaroche Protocol’’ [2] has been adapted to infants of less than 6 months. This protocol differs from the Observer-based Psychoacoustic Procedure (OPP) described by Olsho et al. [15]. It also varies from the classic procedures of Behavioral Observation Audiometry (BOA) wherein robust unilateral head-turns towards lateral loudspeakers are reinforced by attractive visual stimuli in infants as young as 5 months [4,16–18]. Characteristically, in the present study, modalities of observation, stimulation and reinforcement are adapted to individual stage of development. Babies are turned into ‘‘active partners’’ with customized reinforcement.
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Behavioral assessment of pure-tone sensitivity in normalhearing infants aroused interest in providing reference values to findings in hearing-impaired babies. According to Olsho et al. [19] thresholds of 3 month-old infants are 15–30 dB higher than those of adults and thresholds of 6–12 month-old infants are 10–15 dB higher than those of adults, with the difference being greater at lower frequencies. In a follow-up of babies screened at birth, Widen et al. [6] reported that normal-hearing infants tested between 8 and 12 months corrected age demonstrate ‘‘minimum response level’’ of 20 dB HL at 1, 2 and 4 kHz, this value of 20 dB HL being thus a plausible fence to characterize normal hearing sensitivity by 12 months. The study here described was undertaken to determine whether subjective measurement of hearing is achievable below 6 months of age. We report on audiometric threshold findings in babies with sensorineural hearing loss (SNHL) whose age was less than 6 months at first audiometric tests, henceforth called early tests. We also analyze reliability of early test results by comparing them with more widely accepted test results around these ages: (a) ABR thresholds in the framework of a cross-sectional study performed by 6 months of age, and (b) hearing thresholds measured behaviorally at 18 months along a longitudinal assessment. 2. Methods 2.1. Procedures for auditory measurements 2.1.1. ABR tests Electrophysiological investigations were approved by Ethics Committee of our University and tests were conducted after parents gave informed consent. Babies were tested while asleep (natural sleep in most cases). Using a vertex-ipsilateral mastoid montage, ABR signals were amplified, band-filtered (100 Hz– 3 kHz) and averaged 2000 times. Alternated broad-band clicks (100 ms of duration) were delivered through a TDH39 headphone, at 21/s, from 80 to 90 dBnHL to threshold at 10 dB steps in a descending order. Contralateral ear was masked systematically. For the precise determination of ear-separated auditory thresholds, increments of 5 dB were used when signals were not any more identifiable and recordings were repeated three times. When no replicable response was observed at 90 dBnHL, two series of measurement were undertaken at 100 dBnHL (maximum output of equipment). Early audiometric data to which ABR thresholds were confronted in the cross-sectional study will be described in a section apart (see Section 2 for assessing validity). 2.1.2. Other objective tests Tympanometry was performed systematically at the end of each behavioral test. A single probe tone of 226 Hz was used, even though higher frequencies (660 Hz) are advocated in the first months [20]. OAE test results were not taken into account as not performed systematically. The same reasoning was applied to auditory steady-state response (ASSR) tests. 2.1.3. Behavioral audiometry (BA): the ‘‘Delaroche protocol’’ Adaptation of the protocol to the specific age category (less than 6 months) is described in the following sections addressing installation of the baby, nature of observable reactions, and stimulation strategy, successively (see also Appendix derived from Brunet-Le´zine’s scale) [21]. For a behavioral threshold to be considered as valid at a given frequency–intensity sound condition, the rule here is that two definite responses need to be substantiated. 2.1.3.1. Installation of the baby assessed behaviorally. The technical installation promoted in the protocol enables recourse to a single examiner, located in front of the audiometer and in the lateral field
Fig. 1. (A) Measurement of air conduction sensitivity in a 2-month-old baby who is about to sleep (see Section 2 for criteria of valid sound-related responses). The left part of the figure displays the audiometer and the hand of the examiner, both separated from baby’s visual field by a small screen. (B) Measurement of bone conduction sensitivity in a 4-month-old baby who is awake. The examiner is on the left, as in (A). (C) Bone vibrator adapted to less than 6-month-old babies.
of the baby (Fig. 1A). In this setting, the examiner is able to control in permanence a series of influential variables: (a) proper positioning of the baby and her parents; (b) state of vigilance of the baby, muscular relaxation, rhythm of sucking, breathing or gaze when awake; (c) adequate timing of stimulation, often performed in apnea to decrypt a minimal reaction; (d) shortness of delay in accordance to sound delivery, an important parameter to substantiate observed reactions; (e) synchronization of reinforcement to baby’s reaction; and (f) readjustment of installation or vigilance. The baby may be held in the arms of her parent or, alternatively, placed in a lounger or laid on a small mattress. Timing of examination is determined by baby’s rhythm of life, e.g. profound sleep or pangs of hunger are unsuitable circumstances to perform the test. 2.1.3.2. Nature of detectable reactions during BA test. Stimulusrelated reactions that can be detected with this protocol extend well beyond the changes in sucking reported e.g. by Madell [4]. They are described according to three distinguishable states of alertness: a) The baby is tested in drowsiness (Fig. 1A): eyelids are still fluttering between opening and closure, suggesting that brain is still susceptible to process auditory signals. The so-called ‘‘alert’’ phase is ideal to observe a wide range of most often combined reactions as described in literature [22,23]: generalized cochlear-muscular reflex, cochleo-palpebral reflex, Moro reflex,
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cephalic reflex towards sound source, subtle movements of head or limbs that are often combined to changes in nonnutritive sucking and respiratory rhythm. b) The baby is tested at the end of breast or bottle feeding. Start of feeding ought to be avoided when delivering the sound as the baby, swayed by hunger, noisily gulps the milk and is not receptive to sound stimulation. Reaction to sound perception can be stop of sucking when sound is delivered by the end of feeding or, on the contrary, reactivation of sucking when sound is presented to a fully fed or exhausted baby. Perception of sound may also take the form of a brief opening of eyelids or limb shudder. c) The baby is awake (Fig. 1B) but peaceful and reassured by the presence of her mother. In any of these test circumstances, no third person is allowed to distract the baby or catch her attention. Parents must refrain from any visual or tactile stimulation (kiss or caress) during sound presentation. Each reaction to sound is reinforced by the examiner, providing congratulations (see Appendix). Such a customized reinforcement renders sound perception meaningful and opens the field of multimodal communication to the hearing-impaired baby. 2.1.3.3. Stimulation strategy during BA test. The stimulation strategy depends on whether or not objective data is available. Consequently, two situations will be considered separately. 2.1.3.3.1. BA is performed before the ABR and OAE tests. Examination starts by observing the reactions to 2 or 3 sound-making toys of different frequency profile, including treble (little bell or maraca) and bass sounds (gong or small drum). Responses to these sounds are compared to those usually observed in normal-hearing babies of the same age and serve as landmarks for the frequency- and intensity-choices in next steps. The priority is to determine bone conduction hearing threshold curve with vibrator, reflecting the better functioning cochlea independently from any middle ear impairment. The headband of vibrator, adjusted to baby’s head size, is lined with foam for optimal comfort (Fig. 1C). When no reaction to sound-making toys of diverse frequencies is noticeable, suggesting the hypothesis of a severe to profound hearing loss across the whole frequency range, vibrator is also used first but with the purpose of verifying emergence of vibro-tactile reactions to low-frequency stimuli (i.e. 45 dB at 250 Hz and 65 dB at 500 Hz). Once vibro-tactile reactions to low-frequency stimuli are repeatedly observed, sensitivity to bone-conducted sounds of higher frequencies (1000 Hz and above) is explored up to vibrator maximum output (65–70 dB). 2.1.3.3.2. BA is performed after the ABR and OAE tests. In general, results of objective tests are taken into account to design sound stimulation strategy, as exemplified in Fig. 2. Whether BA is conducted before or after objective tests, bone conduction threshold curve is essential to establish for BC thresholds are used as landmarks in determining air conduction sensitivity. Thresholds to air-conducted sounds are measured with a headphone (such as TDH39 supra-aural device) rather than in sound field. This type of transducer is preferred to inserts which entail the risk of driving earwax more profoundly into the external canal or of coming up against a tiny auditory canal. Furthermore, adequate positioning of the transducer is easier to verify than with inserts. Finally, comparison between ABR and BA results is more direct with headphone since the same transducer is used in the two types of threshold measurement. In babies less than 6 months-old is there any advantage in determining air-conduction (AC) thresholds binaurally first? At this
age it is hard to predict how long the baby will remain receptive to sounds and able to produce reliable reactions. Binaural stimulation (air-conducted sound delivered simultaneously to both ears) enables determination of the better functioning ear and can thus be seen as a means to spare baby’s resources. Second, knowledge of binaural sensitivity at 500, 1000, 2000 and 4000 Hz enables early use of hearing aids adapted to speech development with minimal overamplification risk. Third, ear-specific AC thresholds are occasionally investigated immediately after binaural assessment; in this setting, changing baby’s installation is not required. Far more often, earspecific tests are performed subsequently, each frequency being then tested 10–15 dB above binaural threshold. By alternating, for a given frequency, the ear that is stimulated, a difference in reactions between the two ears readily identifies poorer sensitivity in one ear and thus the need for larger amplification in that ear. Using headphone to perform binaural stimulation yields much higher intensities (up to 120/130 dB HL) than with a sound field transducer, a difference that is not negligible in profoundly hearing-impaired children. 2.2. Procedure in cross-sectional study of BA validity Numerous studies have analyzed correlations between ABR and BA results and the predictive value of click- or tone-evoked ABR tests. In these comparative studies, ABR thresholds were most generally confronted to hearing thresholds determined behaviorally well beyond 6 months of age [6,24–27]. In the present study, we decided to compare click-evoked ABR thresholds to BA thresholds even though it is well known that click-evoked ABR thresholds correlate well with behavioral thresholds above 2 kHz, but are higher at lower frequencies. In an attempt to minimize this confounding factor, behavioral threshold values chosen for cross-sectional comparison were restricted to 2000 and 4000 Hz frequencies, and more precisely average of the two as suggested by Bauch and Olsen in adults [28]. As already discussed above, we took into consideration binaural AC thresholds. This appeared as a reasonable compromise to undertake valuable comparison with ABR threshold from the better ear. It was indeed expected that ear-specific behavioral thresholds would be difficult to measure in all babies at this early age. When no behavioral response at 2000 or 4000 Hz was evidenced, the frequency was given the value of 120 dB in accordance with the recommendation of BIAP [29] for calculating the degree of hearing impairment. However, to perform a valuable comparison with ABR measurements, any behavioral average threshold (2000 + 4000 Hz/2) above 100 dB HL was considered to be a non-response. All data were collected by EPIDATA and processed with the EXCEL and SAS software packages. Threshold differences were calculated by subtracting the pure-tone behavioral threshold (in dB HL) from the ABR threshold (in dBnHL). Agreement was calculated by the interclass correlation coefficient, the value ‘‘1’’ representing a perfect agreement. 2.3. Procedure in longitudinal study of BA validity The validity of thresholds measured at 500, 1000, 2000 and 4000 Hz in infants under 6 months of age (Thresholds 1, Th1) was also verified by comparing these early determined values with thresholds measured later. Time for this reference-measurement was fixed at 18 months (Thresholds 2, Th2) or, alternatively, 12 months in profoundly deaf infants who underwent cochlear implantation around this age. A linear mixed model, based on time-dependent reliability functions [30], was employed to estimate reliability of repeated measurements. Agreement was assessed by Intraclass correlation
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Fig. 2. Stimulation strategy according to objective tests results.
coefficient and by difference between the two series of measurement in each individual. The higher the Intraclass correlation coefficient, the better the agreement between the two types of measurements (a score above 0.75 being indicative of strong correspondence). Because measurement of hearing thresholds was occasionally limited to 120 dB, an extension of the statistical model was used to take account of this censoring effect [31]. In the crude analysis, we replaced values known to be above 120 dB by the 120 dB value. To study the impact of censoring, robustness analysis was also performed by calculating Intraclass correlation coefficient
when excluding censored values. Equality of hearing thresholds Th1 and Th2 was verified by testing the hypothesis of a zero difference using a nonparametric sign rank test. 3. Results 3.1. Study population All babies included in the report met the following criteria: (i) suffering from SNHL (as evidenced by elevated BC hearing
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Table 1 Feasibility of behavioral audiometry (BA) under 6 months.
Bilateral air conduction thresholds at 500, 1000, 2000 and 4000 Hz Partial air conduction thresholds (at 2 or 3 frequencies) Threshold impossible to determine
Table 3 Categorization of hearing impairment according to developmental stage group.
<3 months (N = 29)
<6 months (N = 73)
<12 months (N = 73)
82.75%
87.67%
98.63%
13.80%
5.47%
0
3.44%
6.85%
1.36%
Table 2 Feasibility of behavioral audiometry (BA) under 6 months according to developmental stage group. Binaural air conduction thresholds at 500, 1000, 2000 and 4000 Hz <6 months Normal development (N = 56) Delayed development (N = 11) Multihandicap (N = 6)
91.10% 81.81% 66.66%
thresholds and no air-bone gap) or mixed hearing loss (SNHL associated to a mild middle ear alteration); (ii) followed up in our department; and (iii) aged less than 6 months at first behavioral testing. Two types of cohort of comparable size were included in this retrospective study: (1) babies screened at birth (N = 39) over a period of three years (2005–2007) using the Automated Auditory Brainstem Responses ALGO3i hearing screener (Natus1 Medical, San Carlos, CA, USA) [32], and (2) babies identified independently from newborn screening over a wide period extending from 1985 to 2007 (N = 34), amounting to a total of 73 hearing-impaired babies. Based on medical records (weight at birth, Apgar score, clinical examinations in Departments of Pediatrics, Neonatology or Neurology) and also observations made during BA test, the 73 babies (37 boys) were subdivided into 3 groups: - Babies who evidenced normal development (see left column in Appendix) (N = 56, 76.71%). - Babies with delayed development (N = 11, 15.06%). - Babies presenting with hearing impairment associated to retarded development, visual impairment, multi-malformation syndrome, or relationship disorder (N = 6, 8.21%). For premature babies, corrected age1 was determined before assignment to developmental group. Etiologies included nonsyndromic family hearing loss (N = 34, 46.6%), prematurity (N = 7, 9.6%), genetic syndrome (N = 6, 8.2%), pathology during pregnancy (N = 6, 8.2%), other causes (such as consanguinity, N = 4) and no risk factor (N = 16, 21.9%).
Normal Delayed Multihandicap Overall % development development Moderate (40–69 dB HL) 18 Severe (70–89 dB HL) 9 Profound (90 dB HL) 29
3 2 6
1 2 3
30.13% 17.80% 52.05%
12 months) do not belong to the feasibility study (limited by definition to 6 months) but are shown to illustrate the development of auditory behaviors in these hearing-impaired children. Results as a function of development attained at 6 months are displayed in Table 2. As degree of hearing impairment was determined on the basis of BA results (bilateral air conduction hearing thresholds averaged in dB HL over the four frequencies), categorization of hearing loss as a function of developmental stage is depicted only now (Table 3). 3.3. Cross-sectional study of validity As complete binaural air-conduction threshold curves were documented by 6 months of age in less than 90% of the whole hearing-impaired population (Table 1), ABR and behavioral thresholds could be compared in only 63 children. The delay between the two types of auditory measurements was inferior to 3 months in 99%. Comparison of test results is displayed according to whether or not ABR thresholds were evidenced at maximum output of the transducer (100 dBnHL) (see Table 4). In the subgroup where both types of measurements gave numerical data (N = 32) interclass correlation coefficient amounted 80.28%. 3.4. Longitudinal study of validity Number of infants in whom early- and later-determined behavioral thresholds were compared varied across frequencies: 67 at 1000 Hz, 66 at 500 H, 63 at 4000 Hz and 62 at 2000 Hz. Incomplete threshold determination over the whole frequency range (see Table 1) or unrealizable testing before 6 months of age were mostly accountable for unequal comparability through frequencies. Results are first described in Tables 5a and 5b. Additional results, applicable to severe and profound hearing impairment are provided in Table 6. As seen in Table 5b, Intraclass correlation coefficient between the two types of measurements (Th1 and Th2) reached or exceeded
Table 4 Results of cross-sectional study in 63 hearing-impaired infants (displayed according to whether or not ABR thresholds were evidenced at maximum output of the transducer).
3.2. Feasibility study
ABR test results
Behavioral audiometry (BA) test results under 6 months
The study of feasibility was based on the percentage of babies in whom bilateral air conduction (AC) threshold curve was obtained for the first time, consecutively to bone conduction (BC) determination. As indicated in Table 1, full achievement of bilateral air conduction thresholds at 500, 1000, 2000 and 4000 Hz was obtained in 64 babies (i.e. 87.70%) before the age of 6 months (95%CI = 77.9–94.2). Data in the right column (test performance at
No response at 100 dBnHL (N = 31)
No response at 100 dB HL Response at 100 dB HL Thresholds between 70 and 90 dB HL ABR – BA threshold difference 10 dB ABR – BA threshold difference 15 dB ABR – BA threshold difference 20 dB ABR – BA threshold difference 30 dB
1
Corrected age was established as from the number of weeks of amenorrhea.
Measurable ABR thresholds (N = 32)
61.29% (N = 19) 19.35% (N = 6) 19.35% (N = 6) 53.10% (N = 17) 81.30% (N = 26) 90.60% (N = 29) 100% (N = 32)
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Table 5a Results of longitudinal study, 1st part (Th1: early determined measures, Th2: late-determined measures).
Difference Difference Difference Difference
Th2-Th1 Th2-Th1 Th2-Th1 Th2-Th1
equal to 0 dB HL 10 dB HL 15 dB HL 20 dB HL
500 Hz
1000 Hz
2000 Hz
4000 Hz
(N = 66)
(N = 67)
(N = 62)
(N = 63)
23% 64% 75% 93%
27% 69% 73% 91%
42% 79% 82% 95%
41% 76% 78% 91%
(N = 15) (N = 42) (N = 49) (N = 61)
(N = 18) (N = 46) (N = 49) (N = 61)
(N = 26) (N = 49) (N = 51) (N = 58)
(N = 26) (N = 48) (N = 49) (N = 57)
Table 5b Results of longitudinal study: 2nd part. Intraclass correlation coefficient
500 Hz 1000 Hz 2000 Hz 4000 Hz *
Mean of difference (standard error)
Crude
Accounting for 120 censoring
0.80825 0.79975 0.82787 0.85288
0.9137 0.9090 0.9092 0.9384
4.6 2.4 3.0 2.6
(1.7) (1.75) (1.62) (1.57)
500 Hz 1000 Hz 2000 Hz 4000 Hz b
Sign rank test*
63.63 68.66 79.03 76.19
0.05 N.S. N.S. N.S.
Non-significant test, i.e. p > 0.05, means no statistical difference between Th1 and Th2.
Table 6 Results of longitudinal study: 3rd part, sensitivity of early measurements in severe to profound hearing impairment, and in profound hearing impairment.
a
Percentage difference 10 dB
Severe to profound hearing lossa
Profound hearing lossb
91.43 90.24 92.68 96.92
66.67 75.00 88.89 88.86
[76.94–98.20] [76.87–97.28] [80.08–99.46] [90.97–100.0]
[43.03–85.41] [53.29–90.23] [70.84–97.65] [69.85–97.65]
Defined as 70 dB HL. Defined as 90 dB HL.
0.80 on all frequencies when crude values were considered. Intraclass correlation coefficient exceeded even 0.90 when 120 dB censoring was taken into account. Furthermore, using sign rank test, the two groups of measurements (Th1 and Th2) did not differ significantly except at 500 Hz. Sensitivity was defined as the probability to identify correctly level of hearing before 6 months of age, the golden standard being hearing level determined at 18 months (or 12 months in implanted children). Sensitivity was calculated separately in infants with severe-to-profound hearing loss (evidenced by average threshold at or above 70 dB HL with binaural air-conducted stimulation) and in profound hearing loss (90 dB HL). As depicted in Table 6, the probability to identify correctly severe-to-profound hearing loss exceeded 90% on all frequencies, whereas it was somewhat lower when analysis was restricted to profound hearing loss. 4. Discussion Originality of this report is to describe behavioral hearing measurement based on developmental stage in infants aged of less than 6 months. With the widespread use of newborn screening, pediatric otolaryngologists and audiologists are faced with the need to identify correctly hearing-impaired children who failed screening at birth. Cross-sectional study (comparing behavioral thresholds with click-evoked ABR test results by 6 months of age) and longitudinal study (comparing early- to later-determined behavioral thresholds) both suggest that behavioral testing is applicable to this very young population. Three basic principles need to be respected to enable successful testing of hearing at this age. First, behavioral tests are not aimed at replacing objective tests which remain the tests to perform in priority after newborn screening. Conversely, evaluation of hearing should not be limited to objective tests before 5 months, age at which robust head-turns towards sound source are more and more
considered as obtainable. Indeed, knowledge of air- and boneconduction hearing thresholds over the whole frequency range is appreciable when amplification with hearing aids is to be implemented by 6 months of age or earlier. Second, motor skills and cognitive development are essential to estimate before starting behavioral test of hearing. Far from being readily predicted from chronologic age, these developmental achievements directly influence the way infants are testable. Third, infant-related variables need to be permanently controlled by the examiner. Unquestionably, mastery of behavioral test technique at this age requires sustained training and not all infants can be tested thoroughly (i.e. over all frequencies) by 6 months of age. Skepticism on performing behavioral tests in infants with delayed development or, even more, multihandicap is understandable. However, by adapting both sound stimulation and search of reactions to the effective developmental stage, the examiner is able to significantly increase the rate of success. For instance, in premature babies the optimal period of vigilance is often shorter and the need to spare sound stimulations is consequently greater. In infants with multihandicap, behavioral responses with longer latency are to be expected. Paradoxically, infants with multihandicap appear in fact easier to test behaviorally when they are less than 6 months old than later, when disharmonious development and relationship disorder are well-established. As a rule, in difficult-to-test babies, confrontation of repeated objective and behavioral test results is of special interest. In profoundly hearing-impaired babies (52% of our population), usefulness of assessing bone-conduction sensitivity should not be overlooked even though level of cochlear functioning is generally beyond output limits of the transducer. When no reaction to airconducted sound stimulation is noticeable, it is indeed helpful to verify responsiveness to vibro-tactile stimulations (45 dB at 250 Hz and 65 dB at 500 Hz). Responsiveness to vibro-tactile stimulations while the infant is not responding to air-conducted sounds strengthens likelihood of profound hearing impairment. In confirmation to a former study performed on older hearingimpaired children [9], early behavioral testing at 500 Hz seems less effective than at 1000 Hz and above (see right column in Table 5b). Clear explanation to this phenomenon is not available yet. The so far suggested hypotheses of frequency-dependent maturation process [15] or, alternatively, differential sensitivity to airconducted sounds through the space between headphone membrane and eardrum [33] need complementary investigations. As evidenced by Widen et al. [6] normal-hearing infants tested between 8 and 12 months corrected age demonstrate minimum
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response level of 20 dB HL at 1, 2 and 4 kHz. In our population of hearing-impaired infants, the difference between early- and laterdetermined thresholds seldom exceeds 10 dB HL (see Table 5a). This suggests that thresholds measured behaviorally in hearingimpaired infants are closer to ‘‘reality’’ than in normal-hearing infants. As already discussed in a previous paper [9], auditory recruitment is likely to play a role in this greater ‘‘responsiveness’’ of hearing-impaired infants. Behavioral audiometry has the advantage of being performed in presence of parents. These are thus closely involved in the diagnostic process and first services to their hearing-impaired child.
In the context of newborn hearing screening, it is worthwhile to recall that behavioral tests and objective tests need to be controlled beyond 6 months of age in children who apparently present with profound hearing impairment, whenever the context (great prematurity and severe hyperbilirubinemia) suggest the risk of delayed maturation of auditory pathway [32,34,35]. Acknowledgments The authors wish to thank Marie de Pommerol (PhD) and Rodolphe Thie´baut (PhD) for their advices, as well as the reviewers of this report.
Appendix A. Delaroche behavioral audiometry protocol adapted to developmental stage as defined by Brunet-Le´zine’s scale [21] Motor skills and cognitive development
2 months Baby capable of fixed gaze: start of preverbal dialogue, follows an object in horizontal plane Smiles to environmental stimulations Grasping reflex
3 months Baby holds the head, explores environment, follows movement in any plane Begins eye-hand coordination Discovers objects Plays with voice 4 months Start of deliberate grasping and two-hand coordination Plays with hands and puts them in mouth Observes at length an object in hands, learns concentrating 5 months Baby sits up with support Grasps deliberately Transfers object from one hand to the other Diversifies vocal expressions 6 months Sitting position is acquired Two hands are coordinated Hearing control on voice is starting
Installation of baby during the test
Observable reactions (need of two definite responses with a given sound stimulation)
Reinforcement procedure
Baby about to fall asleep at the end of feeding, or awake Held in the arms of her parent or placed in a lounger or laid on a small mattress Attention must be paid to lightening and shadows No visual or tactile stimulation at the time of sound stimulation
Various reflex reactions Modification in sucking, breathing or gaze if baby awake
If baby awake, upon each reaction the examiner enters baby’s field of vision and congratulates her with smiles, signs, caresses, speech = Multimodal communication = Reinforcement by personalized relationship
If awake in the arms of her parent or in a lounger, place a motionless object in line of eyes (to focus gaze) No third person intervenes to distract baby
As at previous age Smile Vocal production
As above
Baby sits partially on knees of parent One small toy is put in her hands to focus gaze and stabilize activity As above no third person intervenes
As at previous age + Modification in manual activity and/or direction of gaze
As above
Baby is sitting on knees of parent, in front of a table where 2 or 3 toys are laid No third person intervenes to distract her
Same reactions than in previous month Beginning of orientation reflex
Examiners establishes multimodal communication (speech, signs, gestures) to render sound stimulation meaningful
Baby, sitting on knees of parent, plays alone: manual activity monitored by eyes No third person intervenes to distract her
Orientation reflex (head-turn towards examiner)
Examiner expresses rhythmically sound stimulation (into sways, head movements, hand movements, etc.)
References [7] [1] A.L. Quittner, P. Leibach, K. Marciel, The Impact of cochlear implants on young deaf children: new methods to assess cognitive and behavioral development, Arch. Otolaryngol. Head Neck Surg. 130 (2004) 547–554. [2] M. Delaroche, R. Thie´baut, R. Dauman, Behavioral audiometry: protocols for measuring hearing thresholds in babies aged 4–18 months suffering from bilateral sensorineural hearing loss, Int. J. Pediatric Otorhinolaryngol. 68 (2004) 1233–1243. [3] J.F.C. van der Drift, M.P. Brocaar, G.A. van Zanten, The relation between the puretone audiogram and the click auditory brainstem response threshold in cochlear hearing loss, Audiology 26 (1987) 1–10. [4] J.R. Madell, Using behavioral observation audiometry to evaluate hearing in infants from birth to 6 months, in: J.R. Madell, C. Flexer (Eds.), Pediatric Audiology: Diagnosis, Technology and Management, Thieme, New York, 2008, pp. 54–64. [5] M. Delaroche, Audiome´trie Comportementale du Tre`s Jeune Enfant: Enjeux et Modalite´s, de Boeck Universite´, Bruxelles, 2000. [6] J.E. Widen, R.C. Folsom, B. Cone-Wesson, L. Carty, J.J. Dunell, K. Koebsell, et al., Identification of neonatal hearing impairment: hearing status at 8 to 12 months
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corrected age using a visual reinforcement audiometry protocol, Ear Hear. 21 (2000) 471–487. J.E. Widen, S.K. Keener, Diagnostic testing for hearing loss in infants and young children, Ment. Retard. Dev. Disabil. Res. Rev. 9 (2003) 220–224. J. Jacobson, C. Jacobson, Evaluation of hearing loss in infants and young children, Pediatr. Ann. 33 (2004) 811–821. M. Delaroche, R. Thie´baut, R. Dauman, Behavioral audiometry: validity of audiometric measurements obtained using the Delaroche Protocol in babies aged 4–18 months suffering from bilateral sensorineural hearing loss, Int. J. Pediatric Otorhinolaryngol. 70 (2006) 993–1002. L. Gaylord, Normal hearing misdiagnosed as hearing loss (case 1), in: J.R. Madell, C. Flexer (Eds.), Pediatric Audiology Casebook, Thieme, New York, 2011, pp. 3–5. C.B. Hicks, A.M. Tharpe, D.U. Ashmead, Auditory assessment of young infants: methodological limitations or natural lack of auditory responsiveness? Am. J. Audiol. 9 (2000) 124–130. American Speech-Language-Hearing Association (ASHA), Guidelines for the Audiologic Assessment of Children from Birth to 5 Years of Age, 2004. B. Pham, B. Clem, Cochlear implant: Sensory integration disorder (case 21), in: J.R. Madell, C. Flexer (Eds.), Pediatric Audiology Casebook, Thieme, New York, 2011, pp. 77–82.
M. Delaroche et al. / International Journal of Pediatric Otorhinolaryngology 75 (2011) 1502–1509 [14] J.P. Lecanuet, C. Granier-Deferre, A.J. de Casper, Are we expecting too much from prenatal sensory experiences? in: B. Hopkins, S. Johnson (Eds.), Prenatal Development of Postnatal Functions, Advances in Infancy Research, 2005 , pp. 31–49. [15] L.W. Olsho, E.G. Koch, C.F. Halpin, E.A. Carter, An observed-based psychoacoustic procedure for use with young infants, Dev. Psychol. 23 (1987) 627–640. [16] G. Thomson, B.A. Weber, Responses of infants and young children to behavior observation audiometry (BOA), J. Speech Hear. Dis. 39 (1974) 140–147. [17] R.J. Nozza, W.R. Wilson, Masked and unmasked pure-tone thresholds of infants and adults: development of auditory frequency selectivity and sensitivity, J. Speech Hear. Res. 27 (1984) 613–622. [18] D.P. Gans, Improving behavior observation audiometry testing and scoring procedures, Ear Hear. 8 (1987) 92–100. [19] L.W. Olsho, E.G. Koch, E.A. Carter, C.F. Halpin, N.B. Spetner, Pure-tone sensitivity of human infants, J. Acoust. Soc. Am. 84 (1988) 1316–1324. [20] L.L. Hunter, R.H. Margolis, Multifrequency tympanometry: current clinical application, Am. J. Audiol. 1 (1992) 33–43. [21] Brunet-Le´zine re´vise´ par Denise Josse (BLR-C), Brunet-Le´zine Re´vise´: Echelle de de´veloppement psychomoteur de la premie`re enfance, EAP (1997). [22] J. Bench, Y. Collyer, L. Mentz, I. Wilson, Studies in infants’ behavioral audiometry: (I) Neonates, Audiology 15 (1976) 85–105; J. Bench, Y. Collyer, L. Mentz, I. Wilson, Studies in infants’ behavioral audiometry: (II) Six-week-old infants, Audiology 15 (1976) 302–314. [23] J.L. Northern, M.P. Downs, Clinical Audiologic testing of children, In: Hearing in Children, Baltimore: Williams & Wilkins, 1st (1978) and 5th (2002) Ed. [24] P.R. Kileny, M.G. Magathan, Predictive value of ABR in infants and children with moderate to profound hearing impairment, Ear Hear. 8 (1987) 217–221.
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[25] O. Fjermedal, E. Laukli, Paediatric auditory brainstem response and pure-tone audiometry: threshold comparisons, Scand. Audiol. 18 (1989) 105–111. [26] P.E. Brookhouser, M.P. Gorga, W.J. Kelly, Auditory brainstem response results as predictors of behavioral auditory thresholds in severe and profound hearing impairment, Laryngoscope 100 (1990) 803–810. [27] D.R. Stappels, J.S. Gravel, B.A. Martin, Thresholds for auditory brainstem responses to tone in notched noise from infants and young children with normal hearing or SNHL, Ear Hear. 16 (1995) 361–371. [28] C.D. Bauch, W. Olsen, The effect of 2000–4000 Hz hearing sensitivity on ABR results, Ear Hear. 7 (31) (1986) 4–317. [29] Audiometric classification of hearing impairments, Bureau International d’AudioPhonologie (BIAP), Technical Commission 02 (1996) [30] T. Vangeneugden, A. Laenen, H. Geys, D. Renard, D.G. Molenberghs, Applying linear mixed models to estimate reliability in clinical trial data with reABRted measurements, Control. Clin. Trials 25 (2004) 13–30. [31] R. Thie´baut, H. Jacqmin-Gadda, Mixed models for longitudinal left-censored reABRted measures, Comput. Methods Programs Biomed. 74 (2004) 255–260. [32] R. Dauman, M. Roussey, V. Be´lot, F. Denoyelle, S. Roman, I. Gavilan-Cellie´, et al., Screening to detect permanent childhood hearing impairment in neonates transferred from the newborn nursery, Int. J. Pediatric Otorhinolaryngol. 73 (2009) 457–465. [33] D.H. Keffe, J.C. Bulen, K.H. Arehart, E.M. Burns, Ear-canal impedance and reflection coefficient in human infants and adults, J. Acoust. Soc. Am. 94 (1993) 2617–2638. [34] M.L. Hyde, Newborn hearing screening programs: overview, J. Otolaryngol. 34 (Suppl. 2) (2005) S70–S78. [35] J. Attias, E. Raveh, Transient deafness in young candidates for cochlear implants, Audiol. Neurotol. 12 (2007) 325–333.
Contents lists available at SciVerse ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Is behavioral audiometry achievable in infants younger than 6 months of age? Monique Delaroche a, Isabelle Gavilan-Cellie´ a, Sylvie Maurice-Tison b, Alphonse Kpozehouen b, Rene´ Dauman a,c,* a
Pediatric Audiology Unit, Department of ORL-HNS, University Hospital of Bordeaux, France Inserm, ISPED, University of Bordeaux Segalen, France c UMR-CNRS 5287, University of Bordeaux Segalen, France b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 23 May 2011 Received in revised form 16 August 2011 Accepted 19 August 2011 Available online 19 September 2011
Background and goal: When carried out in addition to objective tests, behavioral audiometry performed in children with the so-called ‘‘Delaroche protocol’’ [IJORL 68 (2004) 1233-1243] enables to determine hearing thresholds by air and bone conduction over the whole auditory frequency range. In the present report, seventy-three hearing-impaired infants with different levels of motor and cognitive development were tested behaviorally before 6 months of age. Reliability of these early determined behavioral thresholds was then after analyzed using: (a) cross-sectional study, and (b) longitudinal study. Methods: Cross-sectional study compared click-evoked ABR thresholds in the better ear with binaural high-frequency hearing thresholds. In longitudinal study, early measured binaural hearing thresholds from 500 through 4000 Hz were reassessed at 18 months. Results: In 13% of babies behavioral testing was not fully completed by 6 months of age. Nevertheless, both cross-sectional and longitudinal studies yielded intraclass correlation coefficients above 0.80, suggesting that behavioral testing is applicable to this very young population. Conclusions: Assessment of hearing after newborn screening should not be restricted to objective tests before 5 months. It should also include bone- and air-conduction behavioral tests adjusted to developmental stage and performed in presence of parents. ß 2011 Elsevier Ireland Ltd. All rights reserved.
Keywords: Auditory brainstem responses Behavioral audiometry Psychomotor development Bone and air-conducted sounds Cognitive status Reinforcement
1. Introduction Much evidence suggests that, early in life, auditory input and communication are essential for the normal development of language, cognition, and behavior [1]. Newborn hearing screening is aimed at identifying hearing-impaired children as early as possible. Powerfulness of objective tests in measuring auditory thresholds over the first months is well documented. Otoacoustic emissions (OAE) and auditory brainstem response (ABR) tests are extensively used at this age. When performed in addition to these objective tests, behavioral audiometry (BA) enables to determine hearing thresholds by air and bone conduction over the whole auditory frequency range [2]. This information is essential to know as far as speech development is concerned. Second, by assessing ‘‘the response of the entire auditory system from the outer ear through the cortex’’ [3,4] BA enables to analyze how babies react to acoustic stimuli and, consequently, provides further information on their cognitive and
* Corresponding author at: Pediatric Audiology Department of ORL-HNS, Unit, University hospital of Bordeaux, France. Tel.: +33 556795993; fax: +33 556795669. E-mail address: [email protected] (R. Dauman). 0165-5876/$ – see front matter ß 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ijporl.2011.08.016
relational aptitudes [5]. In the follow-up of infants who failed newborn screening test, a behavioral measure of hearing [6] should be the gold standard against which results of objective diagnostic tests are compared. Even though above-mentioned capacities of BA are recognized from 5 to 6 months onwards [4,7–10], this method of exploring hearing is often considered to be unfeasible or unreliable below this age [11–13]. In contradiction to these restrictive assertions, researchers have evidenced astonishing precocity of babies’ sensory and mnemonic capacities, starting already in utero [14]. Given these early skills, audiometric assessment procedure known as ‘‘the Delaroche Protocol’’ [2] has been adapted to infants of less than 6 months. This protocol differs from the Observer-based Psychoacoustic Procedure (OPP) described by Olsho et al. [15]. It also varies from the classic procedures of Behavioral Observation Audiometry (BOA) wherein robust unilateral head-turns towards lateral loudspeakers are reinforced by attractive visual stimuli in infants as young as 5 months [4,16–18]. Characteristically, in the present study, modalities of observation, stimulation and reinforcement are adapted to individual stage of development. Babies are turned into ‘‘active partners’’ with customized reinforcement.
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Behavioral assessment of pure-tone sensitivity in normalhearing infants aroused interest in providing reference values to findings in hearing-impaired babies. According to Olsho et al. [19] thresholds of 3 month-old infants are 15–30 dB higher than those of adults and thresholds of 6–12 month-old infants are 10–15 dB higher than those of adults, with the difference being greater at lower frequencies. In a follow-up of babies screened at birth, Widen et al. [6] reported that normal-hearing infants tested between 8 and 12 months corrected age demonstrate ‘‘minimum response level’’ of 20 dB HL at 1, 2 and 4 kHz, this value of 20 dB HL being thus a plausible fence to characterize normal hearing sensitivity by 12 months. The study here described was undertaken to determine whether subjective measurement of hearing is achievable below 6 months of age. We report on audiometric threshold findings in babies with sensorineural hearing loss (SNHL) whose age was less than 6 months at first audiometric tests, henceforth called early tests. We also analyze reliability of early test results by comparing them with more widely accepted test results around these ages: (a) ABR thresholds in the framework of a cross-sectional study performed by 6 months of age, and (b) hearing thresholds measured behaviorally at 18 months along a longitudinal assessment. 2. Methods 2.1. Procedures for auditory measurements 2.1.1. ABR tests Electrophysiological investigations were approved by Ethics Committee of our University and tests were conducted after parents gave informed consent. Babies were tested while asleep (natural sleep in most cases). Using a vertex-ipsilateral mastoid montage, ABR signals were amplified, band-filtered (100 Hz– 3 kHz) and averaged 2000 times. Alternated broad-band clicks (100 ms of duration) were delivered through a TDH39 headphone, at 21/s, from 80 to 90 dBnHL to threshold at 10 dB steps in a descending order. Contralateral ear was masked systematically. For the precise determination of ear-separated auditory thresholds, increments of 5 dB were used when signals were not any more identifiable and recordings were repeated three times. When no replicable response was observed at 90 dBnHL, two series of measurement were undertaken at 100 dBnHL (maximum output of equipment). Early audiometric data to which ABR thresholds were confronted in the cross-sectional study will be described in a section apart (see Section 2 for assessing validity). 2.1.2. Other objective tests Tympanometry was performed systematically at the end of each behavioral test. A single probe tone of 226 Hz was used, even though higher frequencies (660 Hz) are advocated in the first months [20]. OAE test results were not taken into account as not performed systematically. The same reasoning was applied to auditory steady-state response (ASSR) tests. 2.1.3. Behavioral audiometry (BA): the ‘‘Delaroche protocol’’ Adaptation of the protocol to the specific age category (less than 6 months) is described in the following sections addressing installation of the baby, nature of observable reactions, and stimulation strategy, successively (see also Appendix derived from Brunet-Le´zine’s scale) [21]. For a behavioral threshold to be considered as valid at a given frequency–intensity sound condition, the rule here is that two definite responses need to be substantiated. 2.1.3.1. Installation of the baby assessed behaviorally. The technical installation promoted in the protocol enables recourse to a single examiner, located in front of the audiometer and in the lateral field
Fig. 1. (A) Measurement of air conduction sensitivity in a 2-month-old baby who is about to sleep (see Section 2 for criteria of valid sound-related responses). The left part of the figure displays the audiometer and the hand of the examiner, both separated from baby’s visual field by a small screen. (B) Measurement of bone conduction sensitivity in a 4-month-old baby who is awake. The examiner is on the left, as in (A). (C) Bone vibrator adapted to less than 6-month-old babies.
of the baby (Fig. 1A). In this setting, the examiner is able to control in permanence a series of influential variables: (a) proper positioning of the baby and her parents; (b) state of vigilance of the baby, muscular relaxation, rhythm of sucking, breathing or gaze when awake; (c) adequate timing of stimulation, often performed in apnea to decrypt a minimal reaction; (d) shortness of delay in accordance to sound delivery, an important parameter to substantiate observed reactions; (e) synchronization of reinforcement to baby’s reaction; and (f) readjustment of installation or vigilance. The baby may be held in the arms of her parent or, alternatively, placed in a lounger or laid on a small mattress. Timing of examination is determined by baby’s rhythm of life, e.g. profound sleep or pangs of hunger are unsuitable circumstances to perform the test. 2.1.3.2. Nature of detectable reactions during BA test. Stimulusrelated reactions that can be detected with this protocol extend well beyond the changes in sucking reported e.g. by Madell [4]. They are described according to three distinguishable states of alertness: a) The baby is tested in drowsiness (Fig. 1A): eyelids are still fluttering between opening and closure, suggesting that brain is still susceptible to process auditory signals. The so-called ‘‘alert’’ phase is ideal to observe a wide range of most often combined reactions as described in literature [22,23]: generalized cochlear-muscular reflex, cochleo-palpebral reflex, Moro reflex,
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cephalic reflex towards sound source, subtle movements of head or limbs that are often combined to changes in nonnutritive sucking and respiratory rhythm. b) The baby is tested at the end of breast or bottle feeding. Start of feeding ought to be avoided when delivering the sound as the baby, swayed by hunger, noisily gulps the milk and is not receptive to sound stimulation. Reaction to sound perception can be stop of sucking when sound is delivered by the end of feeding or, on the contrary, reactivation of sucking when sound is presented to a fully fed or exhausted baby. Perception of sound may also take the form of a brief opening of eyelids or limb shudder. c) The baby is awake (Fig. 1B) but peaceful and reassured by the presence of her mother. In any of these test circumstances, no third person is allowed to distract the baby or catch her attention. Parents must refrain from any visual or tactile stimulation (kiss or caress) during sound presentation. Each reaction to sound is reinforced by the examiner, providing congratulations (see Appendix). Such a customized reinforcement renders sound perception meaningful and opens the field of multimodal communication to the hearing-impaired baby. 2.1.3.3. Stimulation strategy during BA test. The stimulation strategy depends on whether or not objective data is available. Consequently, two situations will be considered separately. 2.1.3.3.1. BA is performed before the ABR and OAE tests. Examination starts by observing the reactions to 2 or 3 sound-making toys of different frequency profile, including treble (little bell or maraca) and bass sounds (gong or small drum). Responses to these sounds are compared to those usually observed in normal-hearing babies of the same age and serve as landmarks for the frequency- and intensity-choices in next steps. The priority is to determine bone conduction hearing threshold curve with vibrator, reflecting the better functioning cochlea independently from any middle ear impairment. The headband of vibrator, adjusted to baby’s head size, is lined with foam for optimal comfort (Fig. 1C). When no reaction to sound-making toys of diverse frequencies is noticeable, suggesting the hypothesis of a severe to profound hearing loss across the whole frequency range, vibrator is also used first but with the purpose of verifying emergence of vibro-tactile reactions to low-frequency stimuli (i.e. 45 dB at 250 Hz and 65 dB at 500 Hz). Once vibro-tactile reactions to low-frequency stimuli are repeatedly observed, sensitivity to bone-conducted sounds of higher frequencies (1000 Hz and above) is explored up to vibrator maximum output (65–70 dB). 2.1.3.3.2. BA is performed after the ABR and OAE tests. In general, results of objective tests are taken into account to design sound stimulation strategy, as exemplified in Fig. 2. Whether BA is conducted before or after objective tests, bone conduction threshold curve is essential to establish for BC thresholds are used as landmarks in determining air conduction sensitivity. Thresholds to air-conducted sounds are measured with a headphone (such as TDH39 supra-aural device) rather than in sound field. This type of transducer is preferred to inserts which entail the risk of driving earwax more profoundly into the external canal or of coming up against a tiny auditory canal. Furthermore, adequate positioning of the transducer is easier to verify than with inserts. Finally, comparison between ABR and BA results is more direct with headphone since the same transducer is used in the two types of threshold measurement. In babies less than 6 months-old is there any advantage in determining air-conduction (AC) thresholds binaurally first? At this
age it is hard to predict how long the baby will remain receptive to sounds and able to produce reliable reactions. Binaural stimulation (air-conducted sound delivered simultaneously to both ears) enables determination of the better functioning ear and can thus be seen as a means to spare baby’s resources. Second, knowledge of binaural sensitivity at 500, 1000, 2000 and 4000 Hz enables early use of hearing aids adapted to speech development with minimal overamplification risk. Third, ear-specific AC thresholds are occasionally investigated immediately after binaural assessment; in this setting, changing baby’s installation is not required. Far more often, earspecific tests are performed subsequently, each frequency being then tested 10–15 dB above binaural threshold. By alternating, for a given frequency, the ear that is stimulated, a difference in reactions between the two ears readily identifies poorer sensitivity in one ear and thus the need for larger amplification in that ear. Using headphone to perform binaural stimulation yields much higher intensities (up to 120/130 dB HL) than with a sound field transducer, a difference that is not negligible in profoundly hearing-impaired children. 2.2. Procedure in cross-sectional study of BA validity Numerous studies have analyzed correlations between ABR and BA results and the predictive value of click- or tone-evoked ABR tests. In these comparative studies, ABR thresholds were most generally confronted to hearing thresholds determined behaviorally well beyond 6 months of age [6,24–27]. In the present study, we decided to compare click-evoked ABR thresholds to BA thresholds even though it is well known that click-evoked ABR thresholds correlate well with behavioral thresholds above 2 kHz, but are higher at lower frequencies. In an attempt to minimize this confounding factor, behavioral threshold values chosen for cross-sectional comparison were restricted to 2000 and 4000 Hz frequencies, and more precisely average of the two as suggested by Bauch and Olsen in adults [28]. As already discussed above, we took into consideration binaural AC thresholds. This appeared as a reasonable compromise to undertake valuable comparison with ABR threshold from the better ear. It was indeed expected that ear-specific behavioral thresholds would be difficult to measure in all babies at this early age. When no behavioral response at 2000 or 4000 Hz was evidenced, the frequency was given the value of 120 dB in accordance with the recommendation of BIAP [29] for calculating the degree of hearing impairment. However, to perform a valuable comparison with ABR measurements, any behavioral average threshold (2000 + 4000 Hz/2) above 100 dB HL was considered to be a non-response. All data were collected by EPIDATA and processed with the EXCEL and SAS software packages. Threshold differences were calculated by subtracting the pure-tone behavioral threshold (in dB HL) from the ABR threshold (in dBnHL). Agreement was calculated by the interclass correlation coefficient, the value ‘‘1’’ representing a perfect agreement. 2.3. Procedure in longitudinal study of BA validity The validity of thresholds measured at 500, 1000, 2000 and 4000 Hz in infants under 6 months of age (Thresholds 1, Th1) was also verified by comparing these early determined values with thresholds measured later. Time for this reference-measurement was fixed at 18 months (Thresholds 2, Th2) or, alternatively, 12 months in profoundly deaf infants who underwent cochlear implantation around this age. A linear mixed model, based on time-dependent reliability functions [30], was employed to estimate reliability of repeated measurements. Agreement was assessed by Intraclass correlation
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Fig. 2. Stimulation strategy according to objective tests results.
coefficient and by difference between the two series of measurement in each individual. The higher the Intraclass correlation coefficient, the better the agreement between the two types of measurements (a score above 0.75 being indicative of strong correspondence). Because measurement of hearing thresholds was occasionally limited to 120 dB, an extension of the statistical model was used to take account of this censoring effect [31]. In the crude analysis, we replaced values known to be above 120 dB by the 120 dB value. To study the impact of censoring, robustness analysis was also performed by calculating Intraclass correlation coefficient
when excluding censored values. Equality of hearing thresholds Th1 and Th2 was verified by testing the hypothesis of a zero difference using a nonparametric sign rank test. 3. Results 3.1. Study population All babies included in the report met the following criteria: (i) suffering from SNHL (as evidenced by elevated BC hearing
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Table 1 Feasibility of behavioral audiometry (BA) under 6 months.
Bilateral air conduction thresholds at 500, 1000, 2000 and 4000 Hz Partial air conduction thresholds (at 2 or 3 frequencies) Threshold impossible to determine
Table 3 Categorization of hearing impairment according to developmental stage group.
<3 months (N = 29)
<6 months (N = 73)
<12 months (N = 73)
82.75%
87.67%
98.63%
13.80%
5.47%
0
3.44%
6.85%
1.36%
Table 2 Feasibility of behavioral audiometry (BA) under 6 months according to developmental stage group. Binaural air conduction thresholds at 500, 1000, 2000 and 4000 Hz <6 months Normal development (N = 56) Delayed development (N = 11) Multihandicap (N = 6)
91.10% 81.81% 66.66%
thresholds and no air-bone gap) or mixed hearing loss (SNHL associated to a mild middle ear alteration); (ii) followed up in our department; and (iii) aged less than 6 months at first behavioral testing. Two types of cohort of comparable size were included in this retrospective study: (1) babies screened at birth (N = 39) over a period of three years (2005–2007) using the Automated Auditory Brainstem Responses ALGO3i hearing screener (Natus1 Medical, San Carlos, CA, USA) [32], and (2) babies identified independently from newborn screening over a wide period extending from 1985 to 2007 (N = 34), amounting to a total of 73 hearing-impaired babies. Based on medical records (weight at birth, Apgar score, clinical examinations in Departments of Pediatrics, Neonatology or Neurology) and also observations made during BA test, the 73 babies (37 boys) were subdivided into 3 groups: - Babies who evidenced normal development (see left column in Appendix) (N = 56, 76.71%). - Babies with delayed development (N = 11, 15.06%). - Babies presenting with hearing impairment associated to retarded development, visual impairment, multi-malformation syndrome, or relationship disorder (N = 6, 8.21%). For premature babies, corrected age1 was determined before assignment to developmental group. Etiologies included nonsyndromic family hearing loss (N = 34, 46.6%), prematurity (N = 7, 9.6%), genetic syndrome (N = 6, 8.2%), pathology during pregnancy (N = 6, 8.2%), other causes (such as consanguinity, N = 4) and no risk factor (N = 16, 21.9%).
Normal Delayed Multihandicap Overall % development development Moderate (40–69 dB HL) 18 Severe (70–89 dB HL) 9 Profound (90 dB HL) 29
3 2 6
1 2 3
30.13% 17.80% 52.05%
12 months) do not belong to the feasibility study (limited by definition to 6 months) but are shown to illustrate the development of auditory behaviors in these hearing-impaired children. Results as a function of development attained at 6 months are displayed in Table 2. As degree of hearing impairment was determined on the basis of BA results (bilateral air conduction hearing thresholds averaged in dB HL over the four frequencies), categorization of hearing loss as a function of developmental stage is depicted only now (Table 3). 3.3. Cross-sectional study of validity As complete binaural air-conduction threshold curves were documented by 6 months of age in less than 90% of the whole hearing-impaired population (Table 1), ABR and behavioral thresholds could be compared in only 63 children. The delay between the two types of auditory measurements was inferior to 3 months in 99%. Comparison of test results is displayed according to whether or not ABR thresholds were evidenced at maximum output of the transducer (100 dBnHL) (see Table 4). In the subgroup where both types of measurements gave numerical data (N = 32) interclass correlation coefficient amounted 80.28%. 3.4. Longitudinal study of validity Number of infants in whom early- and later-determined behavioral thresholds were compared varied across frequencies: 67 at 1000 Hz, 66 at 500 H, 63 at 4000 Hz and 62 at 2000 Hz. Incomplete threshold determination over the whole frequency range (see Table 1) or unrealizable testing before 6 months of age were mostly accountable for unequal comparability through frequencies. Results are first described in Tables 5a and 5b. Additional results, applicable to severe and profound hearing impairment are provided in Table 6. As seen in Table 5b, Intraclass correlation coefficient between the two types of measurements (Th1 and Th2) reached or exceeded
Table 4 Results of cross-sectional study in 63 hearing-impaired infants (displayed according to whether or not ABR thresholds were evidenced at maximum output of the transducer).
3.2. Feasibility study
ABR test results
Behavioral audiometry (BA) test results under 6 months
The study of feasibility was based on the percentage of babies in whom bilateral air conduction (AC) threshold curve was obtained for the first time, consecutively to bone conduction (BC) determination. As indicated in Table 1, full achievement of bilateral air conduction thresholds at 500, 1000, 2000 and 4000 Hz was obtained in 64 babies (i.e. 87.70%) before the age of 6 months (95%CI = 77.9–94.2). Data in the right column (test performance at
No response at 100 dBnHL (N = 31)
No response at 100 dB HL Response at 100 dB HL Thresholds between 70 and 90 dB HL ABR – BA threshold difference 10 dB ABR – BA threshold difference 15 dB ABR – BA threshold difference 20 dB ABR – BA threshold difference 30 dB
1
Corrected age was established as from the number of weeks of amenorrhea.
Measurable ABR thresholds (N = 32)
61.29% (N = 19) 19.35% (N = 6) 19.35% (N = 6) 53.10% (N = 17) 81.30% (N = 26) 90.60% (N = 29) 100% (N = 32)
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Table 5a Results of longitudinal study, 1st part (Th1: early determined measures, Th2: late-determined measures).
Difference Difference Difference Difference
Th2-Th1 Th2-Th1 Th2-Th1 Th2-Th1
equal to 0 dB HL 10 dB HL 15 dB HL 20 dB HL
500 Hz
1000 Hz
2000 Hz
4000 Hz
(N = 66)
(N = 67)
(N = 62)
(N = 63)
23% 64% 75% 93%
27% 69% 73% 91%
42% 79% 82% 95%
41% 76% 78% 91%
(N = 15) (N = 42) (N = 49) (N = 61)
(N = 18) (N = 46) (N = 49) (N = 61)
(N = 26) (N = 49) (N = 51) (N = 58)
(N = 26) (N = 48) (N = 49) (N = 57)
Table 5b Results of longitudinal study: 2nd part. Intraclass correlation coefficient
500 Hz 1000 Hz 2000 Hz 4000 Hz *
Mean of difference (standard error)
Crude
Accounting for 120 censoring
0.80825 0.79975 0.82787 0.85288
0.9137 0.9090 0.9092 0.9384
4.6 2.4 3.0 2.6
(1.7) (1.75) (1.62) (1.57)
500 Hz 1000 Hz 2000 Hz 4000 Hz b
Sign rank test*
63.63 68.66 79.03 76.19
0.05 N.S. N.S. N.S.
Non-significant test, i.e. p > 0.05, means no statistical difference between Th1 and Th2.
Table 6 Results of longitudinal study: 3rd part, sensitivity of early measurements in severe to profound hearing impairment, and in profound hearing impairment.
a
Percentage difference 10 dB
Severe to profound hearing lossa
Profound hearing lossb
91.43 90.24 92.68 96.92
66.67 75.00 88.89 88.86
[76.94–98.20] [76.87–97.28] [80.08–99.46] [90.97–100.0]
[43.03–85.41] [53.29–90.23] [70.84–97.65] [69.85–97.65]
Defined as 70 dB HL. Defined as 90 dB HL.
0.80 on all frequencies when crude values were considered. Intraclass correlation coefficient exceeded even 0.90 when 120 dB censoring was taken into account. Furthermore, using sign rank test, the two groups of measurements (Th1 and Th2) did not differ significantly except at 500 Hz. Sensitivity was defined as the probability to identify correctly level of hearing before 6 months of age, the golden standard being hearing level determined at 18 months (or 12 months in implanted children). Sensitivity was calculated separately in infants with severe-to-profound hearing loss (evidenced by average threshold at or above 70 dB HL with binaural air-conducted stimulation) and in profound hearing loss (90 dB HL). As depicted in Table 6, the probability to identify correctly severe-to-profound hearing loss exceeded 90% on all frequencies, whereas it was somewhat lower when analysis was restricted to profound hearing loss. 4. Discussion Originality of this report is to describe behavioral hearing measurement based on developmental stage in infants aged of less than 6 months. With the widespread use of newborn screening, pediatric otolaryngologists and audiologists are faced with the need to identify correctly hearing-impaired children who failed screening at birth. Cross-sectional study (comparing behavioral thresholds with click-evoked ABR test results by 6 months of age) and longitudinal study (comparing early- to later-determined behavioral thresholds) both suggest that behavioral testing is applicable to this very young population. Three basic principles need to be respected to enable successful testing of hearing at this age. First, behavioral tests are not aimed at replacing objective tests which remain the tests to perform in priority after newborn screening. Conversely, evaluation of hearing should not be limited to objective tests before 5 months, age at which robust head-turns towards sound source are more and more
considered as obtainable. Indeed, knowledge of air- and boneconduction hearing thresholds over the whole frequency range is appreciable when amplification with hearing aids is to be implemented by 6 months of age or earlier. Second, motor skills and cognitive development are essential to estimate before starting behavioral test of hearing. Far from being readily predicted from chronologic age, these developmental achievements directly influence the way infants are testable. Third, infant-related variables need to be permanently controlled by the examiner. Unquestionably, mastery of behavioral test technique at this age requires sustained training and not all infants can be tested thoroughly (i.e. over all frequencies) by 6 months of age. Skepticism on performing behavioral tests in infants with delayed development or, even more, multihandicap is understandable. However, by adapting both sound stimulation and search of reactions to the effective developmental stage, the examiner is able to significantly increase the rate of success. For instance, in premature babies the optimal period of vigilance is often shorter and the need to spare sound stimulations is consequently greater. In infants with multihandicap, behavioral responses with longer latency are to be expected. Paradoxically, infants with multihandicap appear in fact easier to test behaviorally when they are less than 6 months old than later, when disharmonious development and relationship disorder are well-established. As a rule, in difficult-to-test babies, confrontation of repeated objective and behavioral test results is of special interest. In profoundly hearing-impaired babies (52% of our population), usefulness of assessing bone-conduction sensitivity should not be overlooked even though level of cochlear functioning is generally beyond output limits of the transducer. When no reaction to airconducted sound stimulation is noticeable, it is indeed helpful to verify responsiveness to vibro-tactile stimulations (45 dB at 250 Hz and 65 dB at 500 Hz). Responsiveness to vibro-tactile stimulations while the infant is not responding to air-conducted sounds strengthens likelihood of profound hearing impairment. In confirmation to a former study performed on older hearingimpaired children [9], early behavioral testing at 500 Hz seems less effective than at 1000 Hz and above (see right column in Table 5b). Clear explanation to this phenomenon is not available yet. The so far suggested hypotheses of frequency-dependent maturation process [15] or, alternatively, differential sensitivity to airconducted sounds through the space between headphone membrane and eardrum [33] need complementary investigations. As evidenced by Widen et al. [6] normal-hearing infants tested between 8 and 12 months corrected age demonstrate minimum
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response level of 20 dB HL at 1, 2 and 4 kHz. In our population of hearing-impaired infants, the difference between early- and laterdetermined thresholds seldom exceeds 10 dB HL (see Table 5a). This suggests that thresholds measured behaviorally in hearingimpaired infants are closer to ‘‘reality’’ than in normal-hearing infants. As already discussed in a previous paper [9], auditory recruitment is likely to play a role in this greater ‘‘responsiveness’’ of hearing-impaired infants. Behavioral audiometry has the advantage of being performed in presence of parents. These are thus closely involved in the diagnostic process and first services to their hearing-impaired child.
In the context of newborn hearing screening, it is worthwhile to recall that behavioral tests and objective tests need to be controlled beyond 6 months of age in children who apparently present with profound hearing impairment, whenever the context (great prematurity and severe hyperbilirubinemia) suggest the risk of delayed maturation of auditory pathway [32,34,35]. Acknowledgments The authors wish to thank Marie de Pommerol (PhD) and Rodolphe Thie´baut (PhD) for their advices, as well as the reviewers of this report.
Appendix A. Delaroche behavioral audiometry protocol adapted to developmental stage as defined by Brunet-Le´zine’s scale [21] Motor skills and cognitive development
2 months Baby capable of fixed gaze: start of preverbal dialogue, follows an object in horizontal plane Smiles to environmental stimulations Grasping reflex
3 months Baby holds the head, explores environment, follows movement in any plane Begins eye-hand coordination Discovers objects Plays with voice 4 months Start of deliberate grasping and two-hand coordination Plays with hands and puts them in mouth Observes at length an object in hands, learns concentrating 5 months Baby sits up with support Grasps deliberately Transfers object from one hand to the other Diversifies vocal expressions 6 months Sitting position is acquired Two hands are coordinated Hearing control on voice is starting
Installation of baby during the test
Observable reactions (need of two definite responses with a given sound stimulation)
Reinforcement procedure
Baby about to fall asleep at the end of feeding, or awake Held in the arms of her parent or placed in a lounger or laid on a small mattress Attention must be paid to lightening and shadows No visual or tactile stimulation at the time of sound stimulation
Various reflex reactions Modification in sucking, breathing or gaze if baby awake
If baby awake, upon each reaction the examiner enters baby’s field of vision and congratulates her with smiles, signs, caresses, speech = Multimodal communication = Reinforcement by personalized relationship
If awake in the arms of her parent or in a lounger, place a motionless object in line of eyes (to focus gaze) No third person intervenes to distract baby
As at previous age Smile Vocal production
As above
Baby sits partially on knees of parent One small toy is put in her hands to focus gaze and stabilize activity As above no third person intervenes
As at previous age + Modification in manual activity and/or direction of gaze
As above
Baby is sitting on knees of parent, in front of a table where 2 or 3 toys are laid No third person intervenes to distract her
Same reactions than in previous month Beginning of orientation reflex
Examiners establishes multimodal communication (speech, signs, gestures) to render sound stimulation meaningful
Baby, sitting on knees of parent, plays alone: manual activity monitored by eyes No third person intervenes to distract her
Orientation reflex (head-turn towards examiner)
Examiner expresses rhythmically sound stimulation (into sways, head movements, hand movements, etc.)
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