Gehoorverlies kan een negatief effect hebben op de ontwikkeling van kinderen. Hoorrevalidatie is een van de manieren om het risico op negatieve effecten en de mate waarin deze optreden te beperken. Om tot een adequate hoorrevalidatie te komen is het vroegtijdig en betrouwbaar bepalen van de gehoordrempels nodig. De gouden standaard voor het bepalen van de gehoordrempels is toonaudiometrie. Deze testmethode is echter niet haalbaar bij baby’s en jonge kinderen. Daarom wordt voor kinderen met een ontwikkelingsleeftijd tot 9 maanden van oudsher, naast impedantiemetrie en oto-akoestische emissies (OAE)meting, auditory brainstem response (ABR) onderzoek met een klikstimulus gebruikt (Drift 1988) om de aard en ernst van gehoorverlies te bepalen. Recenter zijn nieuwe elektrofysiologische meetmethoden mogelijk geworden, bijvoorbeeld de mogelijkheid om frequentie-specifiek te stimuleren. Tevens is er de auditory steady state response (ASSR) waarbij niet de reactie op de stimulus zelf gemeten wordt (zoals bij ABR) maar de detectie van de amplitudemodulatie- en/of de frequentiemodulatie van de stimulus. Binnen deze uitgangsvraag onderzoeken we de verschillen tussen ABR en ASSR. We onderzoeken of er tussen ABR en ASSR een verschil is in voorspellende waarde voor toonaudiometrische drempels op dezelfde/latere leeftijd.

De uitvoering van een OAE-meting en impedantiemetrie worden buiten beschouwing gelaten daar deze in een diagnostisch traject naar de gehoordrempels niet sensitief/specifiek genoeg zijn. Ook de ABR en ASSR via beengeleiding wordt buiten beschouwing gelaten. Het uitvoeren/toevoegen van deze metingen moet uiteraard wel overwogen worden om de aard van het gehoorverlies vast te kunnen stellen.

In het veld is er veel praktijkvariatie. Deze zoekvraag leidt tot aanbevelingen m.b.t. welke diagnostiek het best de aard en omvang van gehoorverlies kan bepalen bij kinderen met een ontwikkelingsleeftijd van 0-9 maanden.

1. ASSR vs audiometry

Pearson correlation coefficients

2. ABR vs audiometry

Pearson correlation coefficients

Intraclass correlation coefficients

3. ABR vs ASSR

Pearson correlation coefficients

Intraclass correlation coefficients

Abbreviations used in the summary of literature

(c)ABR:                (click) auditory brainstem responses

ASSR:                    auditory steady-state responses

AUC:                     area under the curve

BA                          behavioural audiometry

BERA:                   brainstem evoked auditory responses

BOA                      behavioural observation audiometry

ICC:                       intraclass correlation coefficient

MSSR:                  multiple auditory steady state responses

NPV:                     negative predictive value

PCHI                      permanent childhood hearing impairment

PPV:                      positive predictive value

PTA:                      pure tone audiometry

VRA:                     visual reinforcement audiometry

Description of studies

The used primary outcome measures per study are shown in the evidence table and summarized in Table 1. Of note, none of the studies reported diagnostic accuracy with PPV, NPV or AUC.

Table 1: Overview of study characteristics included in this analysis

1. ASSR vs audiometry

Chou (2012) conducted a retrospective chart review to investigate whether multi-stimulus ASSR were capable of estimating hearing thresholds in high-risk infants. Three tertiary care centers in Taiwan participated. Infants born between January 2004 and December 2006 and aged <13 months were enrolled in the study if they met the inclusion criteria, which included risk factors for congenital hearing loss. Subjects with mental retardation and otitis media were excluded by pediatric psychiatrists and otolaryngologists. Subjects received multi-stimulus ASSR measurements at infancy and audiometry at a later age. The maximum stimulation level for ASSR was 120 dB HL, and the volume was increased in steps of 10 dB. The inter-electrode impedance was less than 10 kOhm at 260 Hz. The multi-stimulus stimuli consisted of four carrier frequencies (0.5, 1, 2 and 4 kHz) with amplitude modulation at a rate of 77, 85, 93 and 101 Hz for the left ear stimuli and 79, 87, 95, and 103 for the right ear stimuli. Play audiometry was performed to obtain tone thresholds. A pure tone threshold measurement was obtained at age 23-48 months for each ear in all subjects using a clinical audiometer (GSI, Grason-Stadler, G1 clinical audiometer, Madison, WI, USA). Pure tone thresholds were obtained at 0.5, 1, 2 and 4 kHz via insertion-phones or headphones and the employment of a standard threshold searching procedure using a 5 dB up and 10 dB down technique. The maximum stimulation intensity was 120 dB HL with intensity steps of 5 dB. In total, 249 high-risk infants were enrolled, of which 33 were lost to follow-up. Pearson’s correlation linear correlation was reported as outcome measure.

Rodrigues (2010b) performed a prospective study to compare ASSRs to tone-evoked ABR and to behavioral thresholds obtained on follow-up audiometry at 0.5, 1, 2 and 4 kHz in infants and young children. The study included 17 infants and young children ages between 2 months and 3 years old (average 11 months), with sensorineural hearing loss. The ASSRs thresholds were compared with the tone-evoked ABR thresholds, and with the behavioral thresholds obtained on follow-up audiometry. Pearson correlation coefficients were reported as outcome measure.

Savio (2006) conducted a diagnostic study to determine the test accuracy and prognostic validity of Multiple Auditory Steady State Responses (MSSR) and click Auditory Brainstem Responses (cABR) when compared within the context of a targeted screening protocol. A sample of 508 high-risk babies were selected. All babies included in the study were born between February 1999 and January 2001. At the corrected age of 3 months, babies received MSSR and cABR tests. All babies screened were called back between three and four years of age for behavioral audiometric testing and psychological assessment. At the first test, children received cABR and MSSR and pass/fail criteria were set at 40 dB nHL for both methods (equivalent to 75 dB pSPL for the click and 62 dB SPL RMS for the multiple frequency stimuli). At the first follow up, children again received cABR and MSSR (0.5, 1, 2 and 4 kHz). Pearson correlation and diagnostic accuracy were reported as outcome measure.

Rance (2002a) studied the evoked potential and behavioral hearing test findings for 200 infants and young children 1 to 8 months in whom permanent, moderate to profound hearing loss was diagnosed with the auditory steady-state response (ASSR) procedure. Findings at the time of the ASSR evaluation (mean age 3 months) are presented in this study. The subjects were all referred for ASSR testing after failure on a click-evoked ABR screening assessment (ABR threshold of >40 dB nHL in both ears). Inclusion criteria were "elevated" ASSR thresholds (>60 dB HL) at any test frequency, and no evidence of middle ear disease. All children had at least one of the following risk factors: prematurity with hypoxia, a family history of hearing loss, jaundice, maternal infection, meningitis, malformation, other. 184 of the 200 children appeared to have sensorineural hearing loss. The most common risk factor in this group was prematurity with hypoxia and a family history of hearing loss. The remaining 16 children suffered from a neural transmission disorder, and their most common risk factor was jaundice. These two groups of children were analyzed separately in this study. For this document, the group of children with a neural transmission disorder was not included. ASSR testing was performed in a sound-treated room with the child in natural sleep. The test stimuli were 500-Hz, I-kHz, 2-kHz, and 4-kHz tones that were amplitude and frequency modulated at a rate of 90 Hz. ASSR thresholds were obtained by increasing the presentation level in IO-dB steps from a starting point around 60 dB HL until a statistically significant, phase-locked response could be obtained. The stimulus level was then decreased in 5-dB steps until the distribution of phase angles became random. Behavioral audiograms were obtained for each ear (monaural stimulation) under headphones or insert earphones for all subjects by means of conditioned audiometric techniques (visual response audiometry). Threshold levels were determined by a 10-dB-down, 5-dB-up search procedure. The test stimuli were warble tones at octave frequencies from 500 Hz to 4 kHz. Pearson correlation coefficients were reported as outcome measure.

Rance (2002b) conducted another study (in the same case series reported by Rance 2002a) to examine the relationship between ASSR thresholds determined in infancy and subsequently obtained behavioral hearing levels in children with normal hearing or varying degrees of sensorineural hearing loss. In total, 211 infants were included (age 1-8 months, mean age 3.2 months). ASSR procedures were similar to Rance (2002a). Pearson correlation coefficients were reported as outcome measure.

2. ABR vs audiometry

Baldwin (2013) performed a study to investigate the accuracy of the cABR when undertaken below the age of 6 months (from expected date of delivery) in predicting the pure-tone thresholds subsequently found to be present in children with a congenital permanent childhood hearing impairment. Subjects were selected if they had a bilateral PCHI of mild or worse degree and had received both a cABR undertaken below the age of 6 months (from the expected date of delivery), and subsequent reliable ear-specific PTA. Those with a temporary external or middle ear blockage present at either test were excluded. During the 14-year period there were 92 (44 female and 48 male) participants who fulfilled these criteria. Subjects received cABR before the age of 6 months and received PTA at 2.6 to 12.8 years, with a mean age of 5.2 years (SD = 2.2). Pearson correlation coefficients (r) were reported as outcome measure.

Delaroche (2006) performed a study to investigate the validity of a specific audiometric protocol (the Delaroche protocol) for assessing hearing in infants with bilateral sensorineural hearing loss. The study involved infants aged 4 to 18 months who had been diagnosed with bilateral sensorineural hearing loss. A total of 105 infants were included in the study (of which 51 boys and 54 girls). In the cross-sectional study, 78 babies were included (36 boys, 42 girls; median age 11 months at ABR and 12 months at BA). 50 infants were included in the longitudinal study. For all these children age at first behavioral audiometric test ranged between 4 and 18 months (median = 12 months, mean = 10 months, standard deviation = 3.27 months) and follow-up demonstrated a stable hearing loss until the age of 3 or 4 years (median age at last examination for this report = 39 months, mean = 40 months, standard deviation = 6.46 months) Delaroche Protocol: The Delaroche protocol involves a series of auditory tests designed to assess various aspects of hearing, such as sound localization, discrimination, and threshold detection. Behavioral Responses: During the audiometric assessment, the infants' behavioral responses to auditory stimuli were observed, including head-turning and attention to sound sources. ABR was compared to behavioral audiometry. Interclass correlation (ICC) and sensitivity were reported as outcome measure.

Lu (2017) conducted a study to examine whether behavioral pure-tone audiometry (PTA) thresholds in children can be accurately estimated from the corresponding infants' click-evoked auditory brainstem response (ABR). 104 children (82, both ears; 22, one ear; total, 186 ears) received regular follow-up and were recruited as subjects. The PTA machine, GSI 61, was used for behavioral hearing assessment. BOA or VRA was performed in babies were aged 6-36 months and PTA (to determine thresholds at frequencies of 0.5, 1, 2, and 4 KHz) in those older than 3 years. Click ABR was performed using the following parameters: stimulus sound type, click; transducer, earphone; stimulus sound duration, 100 ms; repetition rate (RR), 27.7/s; and number of sweeps, 1500 times/s; additional settings were click-stimulus with rarefaction polarity, 16-ms time window of analysis, and filter settings of 100-1500 Hz. Pearson correlation coefficients (r) were reported as outcome measure.

Rodrigues (2010b) also reported on ABR vs audiometry. For a summary of the article, see above.

Savio (2006) also reported on ABR vs audiometry. For a summary of the article, see above.

Stevens (2013) conducted a study to investigate the predictive value of hearing assessment by the ABR following universal newborn hearing screening. All babies (N=94) born between January 2002 and September 2007 referred from the Sheffield, UK universal newborn hearing screen who, following assessment, were considered to have significant hearing impairment in at least one ear were included in the study. Click-ABR was performed on all 160 ears and a tone-pip-ABR was recorded at 4 kHz in 34 left and 37 right ears, and for 1 kHz in 19 left and 18 right ears. For the 160 ears included, with an ABR threshold, good ear and frequency specific thresholds from follow up were available in 94 ears. All available hearing tests carried out following the ABR hearing assessment were examined and used to determine the true hearing level in each ear of the infants. The age at which a satisfactory ear and frequency specific threshold could be obtained varied, depending in part of the child ’ s ability to perform the test. The mean age for the follow up test results used was 3.86 years, with a SD of 1.55 years. Two thirds of the tests were PTA or play audiometry, and one third insert VRA. A linear regression analysis was carried out between the ABR thresholds, and the behavioral thresholds found on follow up as well as calculating the correlation between the two thresholds.

Xu (2014) conducted a study to investigate the clinical usefulness of the LS-chirp auditory brainstem response for estimation of behavioral thresholds in young children aged 6–12 months with mild to severe hearing losses. 68 infants (mean age = 9.2 months) with bilateral mild to severe hearing losses were included. In all cases, the children were referred for chirp-ABR and VRA measurements following failure on a click-evoked ABR screen assessment. All ABR thresholds were >40 dB nHL and ≤ 90 dB nHL in both ears. The VRA thresholds were measured at 0.25, 0.5, 1, 2, and 4 kHz in 136 ears of 68 infants, whereas the LS-chirp ABR thresholds were also performed in 136 ears of 68 infants at the LFchirp (0.1–0.85 kHz) and the HF-chirp (1–10 kHz). Pearson correlation coefficients were reported as outcome measure.

3. ABR vs ASSR

Nunez-Batalla (2016) conducted a cohort study to assess auditory-steady-state response reliability in the audiological diagnosis after neonatal hearing screening. Inclusion criteria were a) that auditory brainstem and auditory steady-state response had been performed with no methodological problems, with clear results (b) that behavioral audiometry had been carried out until results considered definitive had been obtained. No exclusion criteria were mentioned. In total, 35 infants were included. ABR and ASSR were performed at a mean age of 4 months. Impedance remained below 6 kOhm and inter-electrode impedance higher than 4 kOhm. The auditory evoked potential recordings were obtained after they were amplified using an external preamplifier. The adjustments made to the equipment were as recommended by the Nottingham group to optimize ABR recording in neonates and lactating infants: click-type stimuli repeated 49.1 times per second with alternate polarity and low pass filters of 1500 Hz and high pass filters of 50 Hz. The minimum intensity at which the stimuli were presented was 30 dB through insert earphones. Recording of steady-state evoked auditory potentials enabled the 2 ears to be assessed at the same time and up to 4 frequencies to be used per ear. The filters used are high pass between 40 Hz and 90 Hz and low pass between 320 Hz and 720 Hz, with slopes of 6 dB per octave and a gain of 10000. The infant audiometry was performed at the age of 6-12 months and was undertaken in the regional program’s hearing aid office in accordance with the current protocol. Pearson regression coefficients were reported as outcome measures.

Rodrigues (2010a) conducted a cross-sectional cohort study to investigate the agreement level between results obtained from ASSR and click-ABR in a group of children aged between 2 and 36 months with sensorineural hearing loss, to study the clinical applicability of this technique to evaluate the hearing status in young children. 15 children with a diagnosis of sensorineural hearing loss were included. The outcome measure was correlation between the responses of the two tests and was evaluated by intraclass correlation coefficient and McNemar test comparing the probability of responses in both tests.

Rodrigues (2010b) also reported on ABR vs ASSR. For a summary of the article, see above.

Results

1. ASSR vs audiometry

Pearson correlation coefficients

Chou (2012) reported that the Pearson correlation coefficients (r) between the ASSR levels and pure tone thresholds were 0.88, 0.94, 0.94 and 0.97 at 0.5, 1, 2 and 4 kHz, respectively.

Rodrigues (2010b) reported that the Pearson correlation coefficients (r) between the ASSR levels and pure tone thresholds were 0.94, 0.97, 0.96, and 0.94 at 0.5, 1, 2 and 4 kHz, respectively.

Savio (2006) reported that the Pearson correlation coefficient between ASSR and audiometry were 0.88, 0.93, 0.98, and 0.95 at 0.5, 1, 2 and 4 kHz respectively.

Rance (2002a) reported that the Pearson correlation coefficients (r) between the ASSR levels and behavioral audiometry were 0.86, 0.81, 0.93, and 0.89 for 0.5, 1, 2 and 4 kHz, respectively.

Rance (2002b) reported that the Pearson correlation coefficients (r) between the ASSR levels and behavioral audiometry were 0.96, 0.97, 0.98, and 0.97 for 0.5, 1, 2 and 4 kHz, respectively. See Table 2 for a summary of results.

Table 2: Overview of results studies comparing ASSR and audiometry

2. ABR vs audiometry

Pearson correlation coefficients

Baldwin (2013) reported that the Pearson correlation coefficients between ABR and PTA were 0.81, 0.85, 0.87, and 0.89 at 0.5, 1, 2 and 4 kHz respectively.

Lu (2017) reported that the Pearson correlation coefficients between ABR and PTA were 0.69, 0.69, 0.73, and 0.76 at 0.5, 1, 2 and 4 kHz respectively.

Rodrigues (2010b) reported that the Pearson correlation coefficients between ABR and PTA were 0.94, 0.81, 0.90, and 0.87 at 0.5, 1, 2 and 4 kHz respectively.

Savio (2006) reported that the Pearson correlation coefficient between ABR and behavioral audiometry was 0.88 (ABR was performed using non-frequency specific click stimuli).

Stevens (2013) reported that the Pearson correlation coefficients between ABR and PTA were 0.74, 0.74, 0.74, and 0.73 at 0.5, 1, 2 and 4 kHz respectively.

Xu (2014) reported that the best correlations between LS-chirp ABR thresholds and VRA thresholds were obtained at VRA frequency of 0.25 kHz/LF-chirp-ABR (r = 0.98) and VRA frequency of 1 kHz/HFchirp-ABR (r = 0.98). See Table 3 for a summary of results.

Table 3: Overview of results studies comparing ABR and audiometry

Intraclass correlation coefficients

Delaroche (2006) reported intraclass correlation coefficients of 0.92, 0.95, 0.96 and 0.96 at 0.5, 1, 2 and 4 kHz respectively (ABR measured at 4-18 months and audiometry measured at 3-4 years). Delaroche (2006) reported that when thresholds were obtained with ABR and BA, the agreement between both methods measured by an intraclass correlation coefficient was good (0.74).

3. ABR vs ASSR

Nunez-Batalla (2016) reported the following:

• Correlation between the ASSR threshold in the right ear at 0.5 kHz and audiometric threshold of the right ear at 0.5 kHz. Mean difference 9.5 ± 12. Pearson’s correlation: 0.80 (significance=0.000).
• Correlation between the ASSR threshold in the right ear at 1 kHz and audiometric threshold of the right ear at 1 kHz. Mean difference 9.8 ± 12. Pearson’s correlation: 0.84 (significance=0.000).
• Correlation between the ASSR threshold in the right ear at 2 kHz and audiometric threshold of the right ear at 2 kHz. Mean difference 19.4 ± 24. Pearson’s correlation: 0.85 (significance=0.000).
• Correlation between the ASSR threshold in the right ear at 4 kHz and audiometric threshold of the right ear at 4 kHz. Mean difference 10.9 ± 11. Pearson’s correlation: 0.83 (significance=0.000).
• Correlation between the ASSR threshold in the left ear at 0.5 kHz and audiometric threshold of the right (left) ear at 0.5kHz. Mean difference 7.2 ± 8. Pearson’s correlation: 0.91 (significance=0.000).
• Correlation between the ASSR threshold in the left ear at 1 kHz and audiometric threshold of the left ear at 1 kHz. Mean difference 11.4 ± 12. Pearson’s correlation: 0.82 (significance=0.000).
• Correlation between the ASSR threshold in the left ear at 2 kHz and audiometric threshold of the left ear at 2 kHz. Mean difference 9.1 ± 12. Pearson’s correlation: 0.84 (significance=0.000).
• Correlation between the ASSR threshold in the left ear at 4 kHz and audiometric threshold of the left ear at 4 kHz. Mean difference 10.1 ± 11. Pearson’s correlation: 0.82 (significance=0.000)

Rodrigues (2010b) reported that the correlation of tone-evoked ABR and ASSRs thresholds at 0.5, 1, 2 and 4 kHz was 0.91, 0.76, 0.81, 0.89, respectively. See Table 4 for an overview of the results.

Table 4: Overview of results studies comparing ASSR and ABR

Intraclass correlation coefficients

Rodrigues (2010a) reported that the intraclass correlation coefficients between click-BERA and ASSR were 0.70, 0.64, 0.49, 0.69, 0.63 and 0.68 for 1, 2, 4, 1-2, 2-4, and 1-2-4 kHz, respectively.

Level of evidence of the literature

Summary

Most observational studies do suggest a similar effect in diagnostic accuracy for the various tests used. The level of evidence (GRADE method) is determined per comparison and outcome measure and is based on results from 12 observational studies and starts at level “HIGH” (diagnostic studies). Subsequently, the level of evidence was downgraded if there were relevant shortcomings in one of the several GRADE domains: risk of bias, inconsistency, indirectness, imprecision, and publication bias. The level of evidence was downgraded by two levels because of risk of bias (-1) due to heterogeneity in study population, and indirectness (-1) due to the outcome measure not being diagnostic accuracy but correlation coefficients (Pearson’s or intraclass). Furthermore, due to heterogeneity in study population, pooling of data was not feasible.

Welke type ABR-onderzoek kan het best gebruikt worden om de gehoordrempels vast te stellen bij kinderen van 0-9 maanden?

A systematic review of the literature was performed to answer the following question: Which stimulus is best to use with ABR to determine the hearing thresholds in children aged 0-9 months?

Relevant outcome measures

The guideline development group considered diagnostic accuracy a critical outcome measure for decision making.

A priori, the working group did not define the outcome measures listed above but used the definitions used in the studies.

Search and select (Methods)

The databases Medline (via OVID) and Embase (via Embase.com) were searched with relevant search terms from 2007 until April 5^th, 2023. The detailed search strategy is depicted under the tab Methods. The systematic literature search resulted in 1562 hits. Studies were selected based on the following criteria:

• Systematic review (detailed search strategy, risk of bias assessment, and results of individual comparative studies available), randomized control trial or observational comparative study;
• Research question includes all elements of the PICO;
• Full text available;
• Full text written in English or Dutch.

58 studies were initially selected based on title and abstract screening. After reading the full text, 46 studies were excluded (see the table with reasons for exclusion under the tab Methods), and 12 studies were included. None of the included studies were randomized or pseudorandomized studies.

Results

Twelve observational studies were included in the analysis of the literature. Important study characteristics and results are summarized in the evidence tables. The assessment of the risk of bias is summarized in the risk of bias tables. Studies were divided into three comparisons: ASSR vs audiometry, ABR vs audiometry and ABR vs ASSR. Due to heterogeneity between study design, exposures and outcome definitions, it was decided to not pool the results.