Precocious Auditory Evoked Potential Recording with Free-Field Stimulus

Abstract

The aim of this study is to determine the thresholds of normality in the recording of precocious auditory evoked potentials with free-field stimulation and to compare them with conventional stimulation with insertion headphones. For this purpose, we have carried out a case series study of children with normal hearing stimulated with insertion headphones, who underwent Auditory Brainstem Response (ABR) and Auditory Steady-State Response (ASSR) with free-field stimuli. Fifty-four ears with normal criteria of children between 6 months and 24 months of age were assessed. The latencies found with free-field stimulation in ABR were significantly longer than the latencies with insert earphone stimulation (p<0.05), and no differences were found in the inter-latencies. No significant differences were found in the thresholds of the ASSR response. We conclude that the ABR thresholds obtained in the free-field correspond to the delay due to the distance of the sound source to the eardrum and, therefore, are superimposable, being applicable to patients where it is not possible to stimulate with insert phones.

1. Introduction

The subjective hearing test, although fundamental in the study of hearing loss, depends on the active collaboration of the patient and is, therefore, subject to the patient, is very difficult to carry out in young children and impossible in babies. Current methods of objective hearing screening, known as “Electrical Response Audiometry,” are established by means of acoustic stimulation of the ear with insert earphones. This method does not exactly reproduce the natural stimulation of the ear that is carried out by sounds in our environment and which are usually transmitted through the air. With the new method we propose, using a loudspeaker, we transmit the stimulation of the ear in a natural way through the air and thus obtain results that more closely resemble natural hearing conditions [1].

1.1 Generalities

The Electrical Response Audiometry quantifies and qualifies the activity of the auditory central nervous system, in the brainstem, in response to sound stimulation without the need for the active participation of the subject and in a harmless manner. This response is called “Auditory Brainstem Response (ABR)” and is registered as voltage fluctuations generated by the nervous system in response to an appropriate acoustic stimulus. For this registered response, it is necessary to extract from the electroencephalographic tracing the electrical activity coming exclusively from the auditory system [2]. The acquisition and recording of this potential require the auditory nerve stimulus to be synchronized and significant. The synchronization of the electrical activity requires very brief stimuli, which is why clicks or filtered clicks are used. This mechanical stimulus is converted in the organ of Corti into an electrical stimulus that travels along with the acoustic pathway to the auditory cerebral cortex [3, 4].

The better-registered response is now being obtained thanks to modifications in pacing parameters and response processing, together with advances in software and hardware that facilitate and simplify the register. The reduction in hardware size has allowed for less bulky equipment, facilitating mobility with the ability to be easily transported to the operating room and neonatology wards [1].

1.2 The sound

In acoustics, sound (from the Latin sonitus) is a longitudinal wave created by the vibration of objects from a sound source (any object capable of disturbing the first particle of the medium) and propagating through a medium. The medium is understood as a set of interlocked and ordered particles interacting with each other. The sound wave propagates by the interaction of the particles of the medium (mechanical waves), so it is not transmitted through a vacuum, unlike electromagnetic waves [5].

Literally, sensation is defined as “the impression that a living being receives when one of its receptor organs is stimulated.” Therefore, we call the sensation produced in the organ of hearing by the vibratory movement of bodies (sound), transmitted by an elastic medium such as air, “hearing” [6].

The propagation in the air is determined as a function of temperature, humidity, and atmospheric pressure [7], this speed being 331.5 m/s at 0°C and 50% humidity at sea level [8]. Under these conditions, the speed of sound increases at a rate of 0.61 m/s for each degree of temperature. Therefore, in our environment, with a temperature of 22°C and a humidity of 50% at sea level, the speed of sound is 344.42 m/s [9].

1.2.1 Sound intensity assessment

The dB (decibel) is considered as a measure of intensity for the human ear. The scale that measures the dB has certain characteristics; it is logarithmic, non-linear, it is relative where 0 (zero) does not mean the absence of sound (sensation), and it is expressed with different reference levels.

The intensity level is determined by a reference. Zero dB indicates that the power intensity is equal to the reference [10].

The sound pressure level (SPL) indicates that the reference is the sound pressure.

The hearing level (HL) corresponds when the reference is the hearing level. It consists of a scale created to adapt dB SPL to dB HL because the human ear does not perceive different frequencies with the same intensity. In this way, the intensities and frequencies are adapted in an audiogram by weighting the intensity to obtain a linear graph that is easily readable visually. This scale considers differences at different frequencies so that 0 dB HL corresponds to the different frequencies in Table 1.

dB SPL	Frequency in Hz
47	125
26.5	250
13.5	500
7.5	1000
11	2000
10.5	4000
13	8000

Table 1.

Correlation between dB SPL and dB HL.

1.3 The human ear as a receiver of sound waves

Based on the principle of resonance, we hear sounds because the propagation of the wave in the air causes a displacement of the tympanic membrane. This displacement will result in mechanical transmission and amplification through the middle ear mechanisms and the displacement of the stapes plate. The stapes activates the basilar membrane that represents different elastic properties along with its length, being stiffer near the base and more elastic as it approaches the apex. Consequently, each segment of the basilar membrane is resonant at different frequencies, with high frequencies near the oval window and low frequencies at the opposite end. The organ of Corti sits on top of the basilar membrane, reproducing the movements of the basilar membrane and thus the movement of the stereocilia, resulting in electrical impulses that stimulate nerve fibers for central auditory processing. The combined action of the basilar membrane and the organ of Corti will create a spectral analysis, temporal identification, and intensity variation of the received sound wave which, transmitted through the acoustic pathway to the auditory areas of the cerebral cortex [11], will, in turn, create patterns of frequency, intensity and time, a fundamental process for decoding the communicative content of sound waves [5].

The human ear is an extraordinary receiver capable of receiving waves of very low intensity and can withstand, without being damaged, sounds a billion times more intense than its threshold of perception [1].

1.4 Electrophysiological basis of auditory examination

The auditory evoked potentials correspond to the recording, from surface electrodes, of the electrical activity of the acoustic pathway at the moment of an adapted sound stimulus. Therefore, to study this signal, it must be isolated from noise, that is unwanted electrical activities, such as electroencephalogram (EEG), electrocardiogram (ECG), and electromyogram (EMG), and the signal-to-noise ratio must be improved [12]. The electrical synchronization of these fibers requires very short stimuli, as in continuous noise, the unitary activity of the cochlear root is not synchronous [13].

From the generation of the stimulus to the activation of the cerebral cortex, approximately 300 ms elapse, a period we call “latency” [14]. However, each level of the acoustic pathway will generate a response with a different latency, which is why auditory evoked potentials will be classified according to the time segment in which we study this latency [13]. Thus:

• Cochlear microphonic: Corresponds to the electrical activity of the cochlea and its latency is zero.

• Electrocochleography: latency of 1–4 ms.

• Auditory Brainstem Response (ABR) and Auditory Steady-State Response (ASSR): These are early auditory potentials with a latency of 2–12 ms.

• Mid-latency auditory evoked potentials: With latencies of 20–50 ms.

• Long latency auditory evoked potentials: With latencies of 50–300 ms.

• We focus on auditory brainstem potentials, which are considered to be early auditory potentials.

• The Auditory Brainstem Response (ABR) corresponds to the recording of the evoked response in the first 12 ms of the acoustic pathway and, almost 50 years after their discovery, they constitute one of the pillars in the study of hearing and the diagnosis of infantile hearing loss. The response is formed by a curve with 5–7 waves, the first five of which are perfectly defined and practically constant and are denominated by Roman numerals, I, II, III, IV, and V, with I, III, and V standing out as the most evident and constant (Figure 1) [14].

Figure 1.

Auditory brainstem response (ABR) recording.

The origin of these different waves is not clearly defined considering the complexity of the auditory pathway and the number of synaptic steps involved in its functioning [15]. However, the location of generation of each of the responses that give rise to each of the waves has been widely agreed since the 1996 studies by Melcher et al. in the cat [16]. These are as follows [5, 17, 18, 19, 20, 21]:

• Wave I: very close to the cochlea, at the level of the spiral ganglion and cochlear nerve (VIII cranial nerve).

• Wave II: Proximal part of the VIII cranial nerve and cochlear nucleus.

• Wave III: Superior olivary complex.

• Wave IV: Lateral lemniscus and part of the superior olivary complex.

• Wave V: Lateral lemniscus, inferior coniculum, and quadrigeminal tubercle.

1.4.1 Characteristics of auditory brainstem response (ABR)

Presence of response: Obviously we have to obtain the described curve with the presence of the five fundamental waves or, at least, of the three most frequent (I, III, and V) [21].

Latency: Each wave has a latency defined under normal conditions and corresponds to the time elapsed between the production of the stimulus and the appearance of the wave. Waves III and V are the most stable waves and wave I appears only at medium and high intensities [12]. The last wave in disappearing is the V-wave considering the psychoacoustic threshold at the last intensity at which its presence is observed. This threshold corresponds to frequencies between 2000 and 5000 Hz with the use of filtered clicks [22]. The interlatencies correspond to values between waves, the most important being the I-III interlatency, the III-V interlatency, and, above all, the I-V interlatency [14].

The auditory evoked potentials can already be performed at birth. From the first studies, an increased latency of wave V and a different morphology of the birth response curve have already been observed. The interlatency I-III and III-V are also increased, but to a lesser extent than I-V [23]. These changes recover progressively with age, with amplitudes at 3 months and latencies at 1 year equaling those of adults [24].

Some authors have described the latencies of neonates [17, 20], expressed in ms (Table 2).

Pediatric ABR normative values [17, 20]
Age	Latency MSEC
	I	III	V	I-V
33 weeks preterm	2.57–0.54	5.68–0.75	8.21–0.79	5.64–0.70
36 weeks preterm	2.41–0.38	5.35–0.49	7.83–0.59	5.43–0.55
40 weeks term	2.00–0.31	4.82–0.44	7.14–0.43 (8)	5.14–0.40 (5.94)
40 weeks preterm	2.34–0.44	5.07–0.60	7.54–0.62	5.20–0.60
3 weeks term	1.80–0.24	4.50–0.46	6.93–0.37	5.13–0.36
3 weeks preterm	2.01–0.24	4.70–0.37	7.07–0.23	5.07–0.33
6 weeks	1.80–0.20	4.40–0.30	6.60–0.30	4.90–0.30
12 weeks (3 m)	1.70–0.20(2.1)	4.30–0.30(4.9)	6.40–0.30(7)	4.70–0.30(5.7)
26 weeks (6 m)	1.70–0.20	4.10–0.30(4.7)	6.20–0.30(6.8)	4.60(0.30)5.2
52 weeks (1 year)	1.70–0.20	4.00–0.30(4.6)	6.00–0.30(6.6)	4.30–0.20(4.7)
2 years	1.70–0.20	3.80–0.20	5.70,0.20	4.00–0.20

Table 2.

Normal values in pediatrics. Auditory brainstem response with 70 dB stimulus, with stimulation by insert earphones.

Increased wave I latency is interpreted as incomplete maturation of the basal cochlear zone and/or transmission of hair cells and auditory nerve fibers. An increase in the interval of interlatency, and especially I-V, is considered to be incomplete myelination of axons and increased synaptogenesis [10].

Amplitude: The height of each wave manifests the amplitude measured in microV, although their values are very unstable.

In ABRs, a transient potential is elicited in response to a click, which returns to its initial resting state because each stimulus is followed by a sufficiently long interval before the next stimulus. But if we perform the stimulus with a sufficiently fast stimulation frequency so that the response to one stimulus is not extinguished before the emission of the next stimulus, we obtain a succession of overlapping responses. The sum of these potentials results in a sinusoidal response that will have exactly the same frequency as the modulation frequency of the stimulus. These are called Auditory Steady-State Response (ASSR). Unlike transient potentials, this response will be maintained over time, as will the stimulus that provokes it [25]. Therefore, a repetitive sound at frequencies between 3 and 300 Hz evokes a steady-state response and can be said to be quasi-sinusoidal periodic responses whose amplitude and phase are maintained over time [26].

With a fast stimulation frequency range of 70–110 Hz, the overlapping transient responses are of shorter latency and generated in the brainstem similar to those of the ABR [27]. This is why they are not affected by sleep or sedation, being optimal in the study of auditory function in infants and young children [7], being this range the one used in the stimulus of our exploration.

To shorten scanning times without appreciable loss of diagnostic accuracy [25], we use multifrequency as a method of stimulating ASSRs that allows simultaneous stimulation of several frequencies, and even binaurally, requires that each tone is modulated at an identifying frequency different from the stimulation frequencies of the rest of the tones so that it can be identified later in the frequency analysis of the response [8]. We can separate in each ear the response for each frequency by evaluating the spectral component for each stimulus. In this way, we simultaneously stimulate four frequencies (500, 1000, 2000, and 4000 Hz) and both ears (ASSR-MF) [28].

To establish hearing thresholds in infants and young children, we use ABR and ASSR-MF recordings together using either insertion headphone or bone conduction stimulation, however, we are not aware of normality criteria using the free field as the sound stimulus in ABR and ASSR, that is using a loudspeaker close to the patient, a stimulus more similar to natural hearing stimulation.

The aim of this study is to determine criteria for normality in ABR and ASSR recordings with free-field stimulus and to be able to apply these neurophysiological tests in patients where they cannot be performed conventionally.

2. Material and method

We conducted a descriptive observational study of a set of cases of children aged 6–24 months from our ENT clinic at the University Hospital Santa Lucía, Cartagena (Murcia, Spain) in the period between April 2016 and January 2017 who underwent ABR and ASSR-MF using insertion earphones and ABR and ASSR-MF using free-field stimulation.

The selected patients fulfilled the criteria of normality with insertion earphones, that is with latencies and amplitudes within normality in ABR with V-wave threshold at 20 dB HL and with stabilization of responses in ASSR before 6 minutes and threshold of 20 dB HL at the four frequencies of 500, 1000, 2000, and 4000 Hz. These patients, after testing with insertion headphones, were tested again with a free-field stimulus. Children outside the age range and children with some degree of hearing impairment were excluded.

Following these criteria, the children were selected and the ABR and ASSR-MF with free-field stimulus were recorded after the conventional tests with insertion headphones, in the same exploratory act, under the same conditions, using the same sound stimulus, unilateral clicks for the ABR and amplitude-modulated tones in ASSR-MF, and taking advantage of the child’s sedation. All cases were performed and recorded in the same environmental conditions, same acoustic booth, same equipment, and same explorer.

To carry out free-field stimulation, new software and hardware had to be incorporated. These modifications were carried out by the company Audiología, S.L. (Gijón, Spain), Interacoustic’s technical service and distributors, and with the brand’s permission. The modification of the software consisted of the possibility of choosing the use of loudspeakers in the stimulation menu, in this case using Phonestra © preamplified free-field loudspeakers whose potentiometer was mechanically fixed to avoid changing the gain of the tests.

The calibration of hearing thresholds with the correction coefficients of insert earphones is governed by IEC-60645-7 “Instruments for the measurement of auditory brainstem responses” [29]. We are not aware of any specific standards and correction coefficients for the realization of ABR and ASSR tests in the free field. For the calculation of correction coefficients, we based ourselves on the ISO-389 standard for the “zero” reference calculation in the calibration of audiometric equipment. Free-field pure-tone control audiometry was performed on 25 healthy individuals aged 14–38 years. An ASSR measurement was made in each subject, stimulating in a free field, with 0 dB correction. New correction coefficients for ASSR in the free field were obtained by the difference of the values recorded with the free-field tonal tests and the ASSR without correction, calculating a correction coefficient of 5 dB HL (±1.5 dB HL) in the four frequencies with respect to the correction rates with insertion headphones. The theoretical calculation was made following the “law of spherical divergence” by means of the behavior of sound in the free field which allows us to define the attenuation or variation of level between two previously defined points, r1 and r2 (RE: 1, 2). With these modifications and with the sound source (loudspeaker) 70 cm away from the ear to be tested, we performed the ABR and ASSR with free-field stimulus in the same environmental conditions, same booth, same equipment, and same explorer as with insertion headphones to control non-differential errors.

The tests were carried out in the rather quiet outpatient room, inside a booth with an acoustic attenuation of 38 dB SPL on average, which also houses the laptop and the explorer who operates the equipment.

The patient should be relaxed to reduce electrical noise as much as possible [30], with physiological sleep or, as in most of our cases, with mild sedation which we achieve with the oral administration of Chloral Hydrate at a dose of 75 mg/kg/weight which allows 2–3 hours of sedation. Chloral hydrate has very few adverse reactions and although it has a bad taste, it is well tolerated by children. The maximum dose of 2 g should not be exceeded and it cannot be used to maintain prolonged sedation due to the sedative effect of its metabolites [31].

After careful cleaning of the skin with alcohol, we use an abrasive cream to peel off light desquamation to reduce the resistance of the skin in the location of the electrodes that are placed once the child is asleep, placing the active electrode in the vertex, the reference electrode in the mastoid (right and left) and zygomatic region. After placing the electrodes, the ABR3A type earphones are inserted into the external auditory canal, held in place by a silicone cushion to hold them in place and to stagnate them in the size best suited to the canal orifice.

2.1 Recording the ABR with insert earphones

We stimulated with alternating clicks at a rate of 44/s with contralateral white noise masking with −30 dB HL of the stimulus intensity, using a 100 Hz high-pass filter and a 1500 Hz low-pass filter, a maximum of 4000 stimuli, a 12 ms screen window, admitting a curve quality response of 99% and a residual noise of 40 nV. The procedure is programmed using 70, 60, 40, and 20 dB HL in descending order, and the intensity can be changed manually. When it ends in one ear, it automatically starts the stimulus in the contralateral ear and we can stop the test when we consider it convenient when we have reached the threshold of wave V. In case of absence of response or poor quality of the response at 70 dB HL, we will continue with stimuli at 80, 90 or 100 dB HL until we find a graph of sufficient quality to observe amplitudes and latencies.

Once the graphs are obtained, latencies and interlatencies are measured and the results are stored for later evaluation.

2.2 Recording ASSR with insert earphones

We performed multi-frequency stimuli allowing us to stimulate both ears simultaneously at frequencies of 500, 1000, 2000, and 4000 with CE-Chirp© [17], the stimulation rate at 90 Hz, and a rejection level of 40 nV. The maximum stabilization time of the response was set at 6 minutes. We also stored the results.

2.3 Recording of the ABR with free-field stimulus

The procedure is similar to the ABR recording with insertion earphones and is carried out after performing the tests with insertion earphones and without modifying the conditions, in the same clinical act and with the patient being selected following the inclusion and exclusion criteria, as described above. Using a stimulus through a loudspeaker, selecting in the transducer menu, placed 70 cm from the ear to be tested, with masking of contralateral white noise and storing results.

2.4 Recording of ASSR with free field stimulus

Following a similar procedure to the ASSR with insertion earphones and with the modifications described for the free field, we record the ASSR with free-field stimulus after the ABR in the free field and store the results.

3. Results

Applying the inclusion and exclusion criteria, 54 ears of 27 selected children were studied, with a mean age of 16.7 months (SD = 5.7) and age range between 6 and 24 months, corresponding to 19 males (70.4%) and 8 females (29.6%).

Table 3 presents the latencies of waves I, III, and V (the most constant) and I-V interlatencies obtained with insertion headphone and free-field stimuli, as well as the differences between them. No significant differences were observed in the interlatency values.

Waves	Wave I	Wave III	Wave V	Interval I-V
Insertion earphones	1.56 (SD = 0.22)	4.09 (SD = 0.29)	6.27 (SD = 0.19)	4.68 (SD = 0.46)
Free field	3.47 (SD = 0.59)	5.97 (SD = 0.61)	8.22 (SD = 0.51)	4.75 (SD = 0.36)
Difference	1.91	1.88	1.95	0.07
p	<0.001	<0.001	<0.001
Rho	0.78	0.49	0.63

Table 3.

Latencies of waves I, III and V and I-V interlatencies obtained with a stimulus with insertion headphones and free field, at 70 dB HL, as well as the differences between them, p-value and rho value in between them, p-value and rho value in Spearmen’s contrast test.

SD: standard deviation; p: significance level; Spearman’s Rho: Spearman’s Rho.

We found statistically significant differences in the latency values of waves I, III, and V, p < 0.001, and Rho values of 0.78, 0.49, and 0.63, respectively. In the assessment of agreement or concordance in the distribution of mean latencies, a significant difference (p < 0.001) was observed in the Wilcoxon test for the three main waves of the ABR.

The V-wave threshold was obtained at 20 dB HL in all ears studied.

Table 4 represents the results of the thresholds obtained in the ASSR-MF recording with insertion headphone stimulus and in free field.

Frequencies	500	1000	2000	4000
Insertion earphones	10	14	14	15
Free field	22	24	25	25
Difference	12	10	11	10

Table 4.

Results of the thresholds obtained in the ASSR-MF recording with insert earphone stimulus and in free field and the differences between the two limits (dB HL).

In the recordings with insert earphones, the 500 Hz recording was achieved in 50 of the 54 ears studied (7.41%), with responses obtained at all other frequencies. The average response stabilization time was 2.12 minutes.

In the recordings with free-field stimulus, the absence of response at 500 Hz was 22.22%, at 1000 Hz 12.96%, at 2000 Hz 5.55%, and at 4000 Hz 1.85%. The mean response stabilization time was 3.68 minutes which is an increase of 1.56 minutes over the insert phones.

4. Discussion

The children in our study are aged between 6 and 24 months, some of them premature, so latency values may be variable. This is why we decided to apply this age range to minimize variations in latencies due to the immaturity and hypomyelination of the acoustic pathway, which maturity does not end until 12 months [18, 29].

The ABR and ASSR are usually recorded by means of earphones inserted inside the external auditory canal and using surface electrodes placed as described above. The recordings of both tests taken together will give us the hearing thresholds in intensity and frequency, which are necessary for a correct objective diagnosis of hearing loss in children.

The ABR recording is composed of a 5 to 7-wave trace, with the first five waves being the most important, called I, II, III, IV, and V and I, III, and V being the most constant [15, 16] waves that present fundamental characteristics of amplitude and latency [12, 15, 23]. The latencies generate interlatencies, time intervals between waves, the most important being interlatency I-III, III-V, and above all I-V [19, 23].

These waves disappear as the intensity of the stimulus decreases, with the V wave remaining constant, the last recording of which in intensity does not mark the threshold of the response. The average values that we have obtained in the children with normal criteria studied, using acoustic stimuli through insertion headphones, are similar to those observed in the literature [17, 20, 21, 29, 32].

Likewise, the ABR study was carried out in a similar way to that employed by other authors, using the same type of stimulus (click) [33], with a cadence of 44 stimuli/sec, lower than the critical rate of 50 st/sec [34], 2000 stimuli in monaural stimulation and with contralateral masking [35].

After stimulation and stable ASSR response, the software of the device applies the Fast Fourier Transform (FFT) algorithm, which is the recording of the electroencephalographic trace corresponding to the modulated frequency of the presented tone, and calculates the estimated audiometry at frequencies of 500, 1000, 2000, and 4000 Hz, so the normality criteria do not require detailed interpretation [10, 36] and therefore do not require the patient’s cooperation or the explorer’s intervention [37].

Although it is generally accepted that a stable ASSR response should not occur beyond 8–10 minutes, in our daily practice, and depending on the individual patient, we have come to accept response stabilization times of 12–14 minutes. However, in our study, we have selected cases with response stabilization of not more than 6 minutes.

We agree with the various authors that the most difficult response to record in the ASSR is the frequency of 500 Hz, with all other frequencies being fairly constant and with no differences between the two ears [10, 36, 38].

In the ASSR test, the child is in the same environment, with the same electrodes and their location on the skin as in the ABR test and with stimulation through insert earphones, the only difference being acoustic stimulation with clicks in the case of ABR and CE-Chirp in the case of ASSR. This difference does not affect the attainment of hearing thresholds, although the CE-Chirp follows a response with higher amplitude and curve quality [39].

The threshold of ASSR responses compared to hearing screening methods, such as tone audiometry or behavioral audiometry, in children has been studied by numerous authors, indicating, with minor adjustments for correction, the similarity of hearing thresholds [37, 38, 40, 41]. In our daily practice, we have found this similarity between threshold levels in older children undergoing tonal audiometry and ABR/ASSR-MF under sedation [42].

As we have already mentioned, to avoid bias, the ABR/ASSR-MF tests of the selected children, in free field (loudspeaker 70 cm away from the ear to be tested), were carried out in the same clinical act, in the same environment (cabin with acoustic attenuation), by the same explorer as in the tests with insertion earphones, first performing the stimulus with insertion earphones and then, if the child was selected, the stimulus in free field.

The performance of the tests with stimulus in the free field required the modification of the software and hardware of the equipment and its calibration, and we are not aware of any standard or correction coefficient for the performance of these tests in the free field, adjusting ourselves to the calibration performed by the company Audiología, S.L. [43].

The differences in the mean evoked latency of the ABR recording in the tests performed with insertion earphones and those in free field with 70 dB HL stimulation are presented in Table 3. We can see that the mean difference in the latency of the main waves (I, III, and V) corresponds to the delay caused by the distance at which the sound source is located (70 cm) in the free-field stimulation. In the conditions in which the test was performed, with an ambient temperature of 22°C, a humidity of 50%, and the cabin being located at sea level (Cartagena, Spain), the speed at which sound is transmitted in the air is 244.4 m/sec [9]. At this distance of 70 cm, the average delay of the arrival of the stimulus at the eardrum (receiver) from the loudspeaker (transmitter) is 2.032 ms, a delay that resembles the average difference of the latencies of the three waves I, III, and V of the ABR response tracing, taking into account possible variations of a few centimeters when placing the loudspeaker in each of the tests or due to the movements of the child’s head during the exploration.

Likewise, the interlatencies were similar in both tests, with no significant differences between them, especially in the most important interlatency I-V, interlatencies not affected by the distance of the sound source and which shows the response of the different levels of neural generators at the level of the brainstem.

The ASSR-MF thresholds obtained with a stimulus with insert earphones in our daily practice and the selected cases are similar to those found in the literature [44, 45, 46, 47], accepting normal values close to 30 dB HL, although there is a slight decrease in those obtained in free field in relation to those obtained with insert earphones, representing a difference of 10.37 dB HL. In our study, the mean response stabilization time was less than 6 minutes, with the most inconsistent response at 500 Hz, in both different stimulations, and the most constant responses at 1000, 2000, and 4000 Hz.

In the literature, we have found very few studies in which free-field stimulation has been used to obtain ABR and ASSR.

Shemesh et al. carried out a study with 20 patients aged between 24 and 60 years, 10 of whom underwent ASSR recording with insertion headphones, and another 10 patients with hearing aids underwent ASSR recording with free-field stimulus, comparing the thresholds. In this work, there are hardly any indications of the calibration of the equipment, although it uses a booth with acoustic attenuation according to the ISO392-2, 1994 standard. He also recorded the ASSR with and without hearing aids, finding, logically, significant differences in the thresholds with and without hearing aids, but not, on the other hand, between the thresholds with audiometry and ASSR without hearing aids. A control group of 21–24-year-olds with normal hearing recorded audiometric thresholds below 20 dB HL at frequencies between 250 and 8000 Hz and thresholds below 20 dB in ASSR at frequencies of 500, 1000, 2000, and 4000 Hz. They conclude the benefits of ASSR testing on hearing thresholds for objective assessment of the benefit of hearing aids and that it may be determinant in young uncooperative individuals [48].

Arias et al. conducted a study with 14 patients aged 2–14 years with cochlear implants to obtain ASSR-MF thresholds and behavioral audiometry. They used an Audix V, model NDOO1A USB from Neuronic, S, A., calibrated with a sound level meter model 2260 and a microphone type 4144 (Brüel & Kjaer) ensuring that the acoustic energy measured in dB SPL corresponded to its value in dB HL, but no further details are given. They did not record ABR and compared the results of ASSR thresholds with free-field stimuli with behavioral audiometry. However, the study does not give data on distance from the sound source and does not show normality thresholds as these are patients with cochlear implants and therefore profound hearing loss. They conclude that ASSR-MF recording with the free-field stimulus is useful for assessing free-field hearing thresholds in cochlear implant patients [49].

Though clinically useful, the results obtained in these studies are not comparable with those obtained in our studies since none of them examines thresholds of normality in children.

Given that there are no standards or correction coefficients for the ABR and ASSR-MF tests with free-air stimuli and the absence of sufficient literature on studies with free-field stimuli for recording early auditory evoked potentials, we consider our results as a new possibility as a determination of criteria for normality in children in whom stimulation through earphone insertion in the external auditory canal is impossible, such as children with hearing aids or implants and in those who do not cooperate in liminal or behavioral audiometry tests, such as children with down syndrome and autistic spectrum disorders.

5. Conclusions

The results obtained in this study support the usefulness of free-field stimulation as an objective method for acquiring normality criteria in ABR and ASSR tests, allowing these tests to be performed in patients who cannot be stimulated through the external auditory canal with insertion earphones, such as children with hearing aids or implantable hearing aids.

The modification of the software and hardware of the equipment currently on the market is necessary to obtain ABR and ASSR-MF recordings with free-field stimulation. The thresholds of the recordings obtained with free-field stimulation are superimposable to the thresholds obtained with current conventional insert earphones.

6. Limitations and future lines of research

The method used for the collection of auditory pathway information as a measurement instrument is widely validated worldwide.

Among possible random errors, we must take into account the variability of the measurements. We cannot control the child’s head movements, even when asleep, by varying the exact distance to the loudspeaker. To minimize sampling variability, we assess the effect of chance by conducting hypothesis test.

To avoid selection bias errors, patients with perfect normal conditions with insertion earphones were selected in order to know which children without pathology could be tested with free-field stimulus.

When comparing tests performed with insert earphones and in the free field, an information bias may occur during the measurement. To avoid this bias as much as possible, we have performed the tests with the same explorer, in the same environmental conditions, with the same equipment, the same data collection, and the same processing.

Finally, there is no confounding bias as we do not want to know a cause-effect relationship in our research.

Future research should be directed toward its application in daily clinical practice with hearing-impaired children, assessing that the responses obtained with free-field stimuli are similar to the ABR/ASSR-MF values in cases of hearing pathology.

We consider the need for free-field stimulus studies in the fitting and follow-up of assistive listening devices, both conventional hearing aids and implantable devices.

Conflict of interest

The authors declare the absence of interests between the manufacturer of the equipment used (Interacoustics), the staff of the company that carried out the calibration of the equipment, and the working environment (Audiología, S.L.), or any other natural or legal person. Likewise, this work has been financed exclusively by its authors.