Study of the brainstem auditory evoked potential with speech stimulus in the pediatric population with and without oral language disorders: a systematic review

da Silva, Jéssica Dayane; Muniz, Lilian Ferreira; Gouveia, Mariana de Carvalho Leal; da Hora, Laís Cristine Delgado

doi:10.1016/j.bjorl.2020.05.025

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Review article • Braz. j. otorhinolaryngol. 86 (6) • Nov-Dec 2020 • https://doi.org/10.1016/j.bjorl.2020.05.025 copy

Study of the brainstem auditory evoked potential with speech stimulus in the pediatric population with and without oral language disorders: a systematic review^✰ ✰ Please cite this article as: Silva JD, Muniz LF, Gouveia MC, Hora LC. Study of the brainstem auditory evoked potential with speech stimulus in the pediatric population with and without oral language disorders: a systematic review. Braz J Otorhinolaryngol. 2020;86:793–811.

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Introduction:

The brainstem auditory evoked potential with speech stimulus, BAEP-speech, has been applied to observe how speech sounds are manifested in the brainstem. This tool can be used in children to assess central auditory processing, allowing preventive and early interventions.

Objective:

To assess the results found in the brainstem auditory evoked potential with speech stimulus in the pediatric population with and without oral language disorders, through a systematic literature review.

Methods:

The search was carried out in the scientific databases Portal BVS, Pubmed, Lilacs, Medline, Scielo and Web of Science, OpenGrey.eu, DissOnline, OpenDoar, OAIster and The New York Academy of Medicine. A systematic literature review was performed using the descriptors: auditory evoked potentials, children and their synonyms, combined by the Boolean operators AND and OR. The search filter “age: child” was used. The studies were independently read by peers and, in case of disagreement regarding the inclusion of studies, a third researcher was consulted. Original case-control articles that performed BAEP-speech without competitive noise, carried out in the pediatric population without and with oral language disorders, were included.

Result:

14 articles published between 2008 and 2019 were included in this review. Methodological variability was observed in the exam, with the syllable / da / being the most frequently used as the stimulus. When performing the average of the groups, it was observed that the population with specific language disorders showed greater latency delays in the sustained portion, lower amplitude values and VA complex slope. The group with phonological disorders had higher values in the transient portion of the responses.

Conclusion:

Children with language disorders of different etiologies have different patterns of BAEP-speech responses when compared to children with typical development.

KEYWORDS
Auditory evoked potentials; Speech perception; Child; Adolescents; Systematic review

Language alteration	Author/Year	Country	Sample size (participants)	Age	Stimulation parameters	Slope values (mv/ms)	Amplitude values de (mv)	Latency value (ms)	Area values (mv × ms)	Main conclusions
PD	Ferreira, L. et. al., 2019	Brazil	60	5 - 8,11 years	Syllable / of /, 40 ms, right ear (RE), intensity of 80 dB nHL, impedance up to 3kΩ, presentation rate of 10.9 s, window of 80 - 100 ms, bandpass filter 100 - 2000 Hz, two scans of 3000 stimuli.	Group I: 0.55	x	Group 1:	Grupo I: 0,56 Grupo II: 0,77	Children with PD show disorganization in the neural coding of complex sounds, due to changes in the BAEP-speech responses. This could compromise the development of language skills, which can reflect on communication.
						Group II: 0.38		V: 6.79
								A: 7.84
								C: 17.43
								D: 23.07
								E: 32.07
								F: 39.96 O: 47.97
								Group 2:
								V: 7.18
								A: 8.66 C: 18.32
								D: 23.23
								E: 32.47
								F: 41.73
								O: 49.06
	Gonçalves, I. C., et. al., 2011	Brazil	36	7 - 11 years	Syllable [da], 40 ms, RE, intensity of 80 dBA, impedance of up to 5kΩ, presentation rate of 11.1 stimuli / s, band-pass filter 100 - 2000 Hz, 2000 stimuli.	VA complex: Group 1: 0.36 Group 2: 0.43	Group 1: V: 0,32 A: -0,31 C: -0,34 F: 0,33 VA Complex: 0.69 Group 2: V: 0.30 A: -0.35 C: -0.35 F: 0.37 VA Complex: 0.67	Group 1: V: 7,41 A: 9,39 C: 19,42 F: 40,10 VA Complex: 1.97 Group 2: V: 8.58 A: 10.32 C: 18.76 F: 40.00 VA Complex: 1.74	x	They indicate that the initial stages of processing an acoustic stimulus in the auditory pathway are not similar in children with typical development and with PD. They suggest that the abnormal encoding of speech sounds may be a biological marker of PD.
TEA	Chen, J., et al., 2019	China	35	3 - 6 years	Syllable [da], 40 ms, RE, intensity of 80 dB SPL, impedance of up to 5kΩ, presentation rate of 10.9 stimuli / s, three scans of 3000 stimuli.	x	Mean values in the first and second evaluations. respectively:	Mean values in the first and second evaluations. respectively:	x	Children with ASD show subcortical processing that is still immature when compared to those with DD.
							Group 1:	Group 1:
							V: 0.10/ 0.11; A: -0.20/-0.23 C: -0.14/	V: 6.66/6.54 A: 7.58/7.51
							-0.11	C: 18.37/ 18.20
							D: -0.14/	D: 22.58/ 22.39
							-0.18	E: 31.30/ 31.32
							E: -0.22/	F: 39.60/ 39.32 O: 48.04/48.07 Group 2:
							-0.23	V: 6.90/6.73 A: 7.83/7.86 C: 18.47/18.43
							F: -0.27/	D: 22.55/ 22.99
							-0.19	E: 31.13/ 31.08 F:39.74/39.58 O: 48.29/48.17
							O: -0.21/ -0.18 Group 2:
							V: 0.09/ 0.11 A: -0.18/-0.22 C: -0.04/
							-0.07
							D: -0.19/
							-0.21
							E: -0.16/ -0.18
							F: -0.18/
							-0.18
							O: -0.09/
							-0.14
	Ramezani, M., et. al., 2018	Iran	56	Mean ages: 14.36 - 14.99	Syllable [da], 40 ms, RE, 80 dB SPL intensity, impedance up to 5kΩ, intermittent polarity, presentation rate of 10.9 stimuli / s, band-pass filter 100-2000 Hz, two scans of 3000 stimuli.	x	x	Group 1: V: 6.32 A: 7.18 C: 18.03 D: 22.10 E: 30.74 F: 39.12 O: 47.68 Group 2: V: 6.89 A: 7.82 C: 20.01 D: 24.60 E: 33.35 F: 41.12 O: 49.58	x	There are losses in the synchronization of neural activity in individuals with ASD, indicating a dysfunction in the speech stimulus processing in the brainstem.
	Otto-Meyer, S., et. al., 2018	USA	24	7 - 13 years	Stimulus / d /, 40 ms, RE, 80 dB SPL intensity, impedance up to 5kΩ, alternating polarity, 10.9 ms presentation rate, 75 ms window, 100 Hz high-pass filter and 2000 Hz low-pass filter, two scans of 2000 stimuli. Syllable [ya] going up and [ya] going down, 230 ms, RE, 60 dB SPL intensity, alternating polarity, 80 - 1000 Hz band-pass filter, 4800 stimuli.	x	x	x	x	Children with high-performance ASD have less stable BAEP-speech than children with typical development, persisting through multiple stimuli. The effects can go beyond the auditory system, given the integrated nature of the BAEP-speech generators.
	Russo, N., et. al., 2009	USA	39	7 - 13 years	Syllable [da], 40 ms, RE, 80 dB SPL intensity, alternating polarity, impedance up to 5kΩ, presentation rate of 10.9 stimuli/s, 75 ms window, 100 - 2000HZ band-pass filter, three scans of 2000 stimuli.	x	x	Group 1: V: 6.54 A: 7.48 D: 22.38 F: 39.25 Group 2: V: 6.73 A: 7.85 D: 22.77 F: 39.54	x	There is a reduction in neural synchrony and phase block in speech stimulation.
	Russo, N. M., et. al., 2008	USA	42	7 - 13 years	Syllable [ya], 230 ms, RE, 60 dB SPL intensity, impedance up to 5kΩ, 50 ms window, alternating polarity, 80 - 1000 Hz band-pass filter, two scans of 1200 stimuli per polarity.	x	x	X	x	Some children with ASD show marked deficiencies in pitch tracking. In addition, they indicate a reduction in the phase block.
Stuttering	Mozaffarilegha, M.; Adeli, H., 2018.	Iran	29	15 - 33 years	Syllable [da], 40 ms, RE, 80 dB SPL intensity, alternating polarity, 85.33 ms window, 6000 stimuli.	x	x	X	x	Promising capacity of the graphic index complexity (GIC) to assess abnormal activation of the brainstem level in the study group. They associate the visibility of BAEP graphs with mechanisms associated with long-term memory of the auditory system dynamics at the brainstem level.
DEL	Gabr, T. A.; Darwish, M. E., 2015	Egypt	40	3 - 7 years	Syllable [da], 206 ms, both ears, 70 dB nHL intensity, alternating polarity, presentation rate of 11.1 stimuli / s, 75 ms window, band-pass filter 50 - 1000HZ, three scans of 1024 stimuli.	VA Complex: Group 1: 0.426 Group 2: 0.195	Group 1:	Group 1:	Group 1: 1.65 Group 2: 2.05	Children with SLD have abnormal coding for specific acoustic characteristics, reduced neural synchrony for transient changes in speech and impaired neural coding for the duration of the stimulus. Manifesting as abnormal BAEP-speech.
							V: 0.468	V: 6.60
							A: 0.319	A: 8.73 C: 14.04
							C: 0.446	D: 21.0
							D: 0.513	E: 29.1
							E: 0.818	F: 37.9
							F: 0.95	O: 47.00 Group 2:
							O: 0.765 VA Complex: 0.787 Group 2:	V: 7.95
							V: 0.13	A: 12.1
							A: 0.86	C: 21.0
							C: 0.159	D: 29.7
							D: 0.111	E: 38.6
							E: 0.199	F: 47.3
							F: 0.188	O: 55.8
							O: 0.31 VA Complex: 0.334
	Rocha-Muniz, C. N., Befi-Lopes, D. M., & Schochat, E., 2014	Brazil	75	6 - 12 years	Syllable [da], 40 ms, RE, impedance up to 5kΩ, alternating polarity, 74.67 ms window, band-pass filter 100 - 2000 Hz, three scans of 1000 stimuli.	x	x	Group 1: V: 6.32 A: 7.87 C: 17.57 D: 22.83 E: 30.64 F: 39.37 O:48.01 Group 2: V: 6.78 A: 8.61 C: 18.76 D: 23.72 E: 31.79 F: 41.14 O: 49.27	x	BAEP-speech can be used to diagnose language impairments, considering other factors and the presence of risks. Suggested use of the Brazilian procedure in English speakers, since the results obtained for the syllable [da] are similar for speakers of both languages.
	Rocha-Muniz, N. C.; Befi-Lopes, M. D.; Schochat, E., 2012	Brazil	57	6 - 12 years	Syllable [da], 40 ms, RE, impedance up to 5kΩ, alternating polarity, 74.67 ms window, band-pass filter 100 - 2000 Hz, three scans of 1000 stimuli.	x	x	Group 1: V: 6.31 A: 7.35 C: 17.54 D: 22.83 E: 30.79 F: 39.17 O: 48.13 Group 2: V: 6.78 A: 8.75 C: 18.89 D: 23.80 E: 32.01 F: 41.48 O: 49.39	x	The group with SLD showed alterations for temporal measures and frequency coding measures. Abnormal BAEP-s should manifest as difficulties in speech perception. The group with SLD showed worse responses than the others.
	Filippini, R.; Befi-Lopes, M. D.; Schochat E., 2012	Brazil	Three groups: 1: DD 2: SLD (formal auditory training and speech therapy) 3: SLD (speech therapy only)	7 - 13 years	Syllable [da], 40 ms, RE, 80 dB nHL, alternating polarity, presentation rate of 10.9 stimuli / s, 74.67 ms window, band-pass filter of 100 - 2000 Hz, three scans of 1000 stimuli.	VA complex, before and after auditory training, respectively: Group 1: 0.45 / 0.37 Group 2: 0.33 / 0.32 Group 3: 0.35 / 0.38	VA complex, before and after auditory training, respectively: Group 1: 0.41 / 0.34 Group 2: 0.29 / 0.29 Group 3: 0.35 / 0.35	Means before and after auditory training, respectively. Group 1: V: 6.53/6.63 A: 7.45/7.60 C: 18.43/18.21 D: 22.22/22.45 E: 31.04/31.16 F: 39.41/39.33 O:48.10/47.94 VA Complex: 0.92/0.92 Group 2: V: 6.64/6.67 A: 7.51/7.58 C: 18.74/18.56 D: 22.51/22.22 E: 31.45/30.72 F: 39.59/39.23 O: 47.88/47.93 VA Complex: 0.88/0.91 Group 3: V: 6.59/6.59 A: 7.63/7.48 C: 18.89/18.58 D: 22.39/22.14 E: 30.80/31.02 F: 39.27/39.37 O: 48.13/47.95 VA Complex: 1.02/0.90		Deficits in auditory processing in behavioral and electrophysiological assessments in the SLD groups, similar to those observed in participants with auditory processing disorder. Additionally, the benefits of formal auditory training and formal auditory training associated with speech therapy were observed in behavioral and electrophysiological responses.
	Basu, M.; Krishnan, A.; Weber-Fox, C., 2009	USA	20 participants. Two groups: I: SLD II: DD	4 - 11 years	Syllables [ba] and [de], 150 ms, RE, intensity of 50 dB nHL, impedance up to 3kΩ, band-pass filter 100 - 3000 Hz.	x	x	X	x	Children with SLD have a temporal deficit at the brainstem level, sounds with rapid presentations or changes are not adequately coded. The assessed population showed a marked interruption in the neural phase block.
TDAH	Jafari, Z.; Malayeri, S.; Rostami, R., 2015	Iran	84	8 - 12 years	Syllable [da], 40 ms, RE, intensity of 80 dB SPL, impedance up to 5kΩ, presentation rate of 10.9 stimuli / s, band-pass filter 100 - 2000 Hz, two scans of 2000 stimuli.	x	x	Group 1: V: 5.920 A: 6.749 C: 17.366 D: 21.178 E: 30.047 F: 38.690 O: 46.788 Group 2: V: 5.935 A: 7.065 C: 17.565 D: 21.716 E: 30.466 F: 39.04 O: 47.08	x	BAEP-speech indicating delay in temporal coding in children of the study group. Children with ADHD have dysfunction in processing speech stimuli and no speech at the brainstem level.

	Latencies							Amplitude	Slope
	V	A	C	D	E	F	O	VA Complex	VA Complex
Phonological disorder ⁹9 Chen J, Liang C, Wei Z, Cui Z, Kong X, Dong C, et al. Atypical longitudinal development of speech-evoked auditory brainstem response in preschool children with autism spectrum disorders. Autism Research. 2019;12:1022-31. ^, ¹⁶16 Filippini R, Befi-Lopes DM, Schochat E. Efficacy of auditory training using the auditory brainstem response to complex sounds: auditory processing disorder and specific language impairment. Folia Phoniatr Logop. 2012;64:217-26.
Mean	7.88	9.49	18.54	x	x	40.86	x	x	0.37
Minimum	7.18	8.66	18.32	x	x	40	x	x	0.36
Maximum	8.58	10.32	18.76	x	x	41.73	x	x	0.38
Standard deviation	0.989	1.173	0.311	x	x	1.223		x	0.014
SLD ¹¹11 Ramezani M, Lotfi Y, Moossavi A, Bakhshi E. Auditory brainstem response to speech in children with high functional autism spectrum disorder. Neurol Sci. 2018;40:121-5. ^, ¹³13 Jafari Z, Malayeri S, Rostami R. Subcortical encoding of speech cues in children with attention deficit hyperactivity disorder. ClinNeurophysiol. 2015;126:325-32. ^, ¹⁴14 Rocha-Muniz CN, Befi-Lopes DM, Schochat E. Sensitivity, specificity and efficiency of speech-evoked ABR. Hear Res. 2014;317:15-22.
Mean	7.02	9.27	19.38	24.9	33.3	42.29	50.64	0.342	0.322
Minimum	6.59	7.63	18.76	22.39	30.8	39.27	48.13	0.334	0.195
Maximum	7.95	12.1	21	29.7	38.6	47.3	55.8	0.35	0.45
Standard deviation	0.623	1.949	1.078	3.263	3.572	3.473	3.481	0.011	0.18
TEA ⁹9 Chen J, Liang C, Wei Z, Cui Z, Kong X, Dong C, et al. Atypical longitudinal development of speech-evoked auditory brainstem response in preschool children with autism spectrum disorders. Autism Research. 2019;12:1022-31. ^, ¹⁰10 Ferreira L, Gubiani MB, Keske-Soares M, Skarzynski PH, Sanfins MD, Biaggio EPV. Analysis of the components of Frequency-Following Response in phonological disorders. Int J Pediatr Otorhinolaryngol. 2019;122:47-51. ^, ¹⁷17 Goncalves IC, Wertzner HF, Samelli AG, Matas CG. Speech and non-speech processing in children with phonological disorders: an electrophysiological study. Clinics. 2011;66:293-8.
Mean	6.78	7.85	19.22	23.45	32.21	40.08	48.87	x	X
Minimum	6.73	7.82	18.43	22.77	31.08	39.54	48.17	x	X
Maximum	6.89	7.88	20.01	24.6	33.35	41.12	49.58	x	X
Standard deviation	0.092	0.03	1.117	0.999	1.605	0.900	0.997	x	X
Typical development ⁹9 Chen J, Liang C, Wei Z, Cui Z, Kong X, Dong C, et al. Atypical longitudinal development of speech-evoked auditory brainstem response in preschool children with autism spectrum disorders. Autism Research. 2019;12:1022-31. 10 Ferreira L, Gubiani MB, Keske-Soares M, Skarzynski PH, Sanfins MD, Biaggio EPV. Analysis of the components of Frequency-Following Response in phonological disorders. Int J Pediatr Otorhinolaryngol. 2019;122:47-51. ^- ¹¹11 Ramezani M, Lotfi Y, Moossavi A, Bakhshi E. Auditory brainstem response to speech in children with high functional autism spectrum disorder. Neurol Sci. 2018;40:121-5. ^, ¹³13 Jafari Z, Malayeri S, Rostami R. Subcortical encoding of speech cues in children with attention deficit hyperactivity disorder. ClinNeurophysiol. 2015;126:325-32. 14 Rocha-Muniz CN, Befi-Lopes DM, Schochat E. Sensitivity, specificity and efficiency of speech-evoked ABR. Hear Res. 2014;317:15-22. 15 Rocha-Muniz CN, Befi-Lopes DM, Schochat E. Investigation of auditory processing disorder and language impairment using the speech-evoked auditory brainstem response. Hear Res. 2012;294:143-52. 16 Filippini R, Befi-Lopes DM, Schochat E. Efficacy of auditory training using the auditory brainstem response to complex sounds: auditory processing disorder and specific language impairment. Folia Phoniatr Logop. 2012;64:217-26. 17 Goncalves IC, Wertzner HF, Samelli AG, Matas CG. Speech and non-speech processing in children with phonological disorders: an electrophysiological study. Clinics. 2011;66:293-8. 18 Russo N, Nicol T, Trommer B, Zecker S, Kraus N. Brainstem transcription of speech is disrupted in children with autism spectrum disorders. Dev Sci. 2009;12:557-67. ^- ¹⁹19 Mozaffarilegha M, Adeli H. Visibility graph analysis of speech evoked auditory brainstem response in persistent developmental stuttering. Neurosci Lett. 2018;696:28-32.
Mean	6.52	7.75	17.55	22.17	30.71	39.28	46.13	0.59	0.43
Minimum	5.92	6.74	14.04	21	29.1	37.9	40.68	0.41	0.35
Maximum	7.41	9.39	19.42	23.07	32.07	40.1	48.1	0.78	0.55
Standard deviation	0.388	0.773	1.470	0.683	0.876	0.622	3.00	0.266	0.082

	Specific language disorder	Autism spectrum disorder	Phonological disorder	Persistent developmental stuttering	Attention deficit hyperactivity disorder
BAEP-speech alterations	Increased wave latency;	Increased wave latency;	Increased wave latency; VA complex slope reduction;	Greater complexity of the graphic index;	Increased wave latency;
	Amplitude reduction;	Reduction of the VA complex slope;			Longer duration of the VA complex;
	Reduction of frequency encoding phase block;	Speech pitch encoding impairment;			Reduction of amplitude and slope of the VA complex;
	Reduction of frequency encoding phase block;	Phase block reduction;			Extension of the initial phase of the response;
	Changes in wave morphology	Lower representation of early speech;			Lower signal-to-noise ratio;

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[1] ⁎ Corresponding author. jessica_aa@live.com