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Aging process and central auditory pathway: a study based on auditory brainstem evoked potential and frequency-following response

ABSTRACT

Objective

To analyze age-related changes in the central auditory pathway in healthy elderly individuals.

Methods

A prospective, quantitative cross-sectional study. The caseload comprised 18 adults (mean age, 22.78 years) and 18 elderly individuals (mean age, 66.72 years) of both sexes, who met inclusion criteria. Subjects were submitted to basic audiological evaluation and related electrophysiologic tests: brainstem auditory evoked potential with click stimulus and frequency-following response.

Results

Elderly individuals had higher wave and interpeak latencies (waves I, III and V and interpeaks I-V and III-V) of brainstem auditory evoked potential. Latencies of frequency following response waves A, E, F and O were also higher in elderly individuals. Frequency following response amplitudes were better in A than in D, F and O waves in these subjects. Likewise, interpeak intervals (V-A and V-O) were larger in elderly relative to adult individuals. Lower slope values were observed in elderly individuals.

Conclusion

Brainstem auditory evoked potential and frequency-following response allowed appropriate assessment of age-related changes in the auditory pathway. Slower neural response to auditory stimuli suggests reduced synchrony between neural structures.

Hearing; Evoked potentials, auditory; Hearing loss; Electrophysiology; Adult; Aging

INTRODUCTION

Population aging has been extensively discussed in the last few years. According to the World Health Organization (WHO), 1.2 billion people will be aged over 60 years in 2025.( 11.Santos GL. Expressão de proteínas ligantes de cálcio e receptores de melatonina em centros encefálicos da via auditiva no envelhecimento [dissertação]. Marília: Universidade Estadual Paulista, Programa de Pós-Graduação em Fonoaudiologia da Faculdade de Filosofia e Ciências; 2019 [citado 2021 Jul 16]. Disponível em: https://repositorio.unesp.br/bitstream/handle/11449/182185/santos_gls_me_mar.pdf?sequence=3&isAllowed=y
https://repositorio.unesp.br/bitstream/h...
) The aging process is associated with several losses, including presbycusis,( 22.Barata VP. Presbiacusia: fator de risco para o declínio cognitivo? [dissertação]. Lisboa: Universidade de Lisboa, Faculdade de Medicina; 2019 [citado 2021 Jul 16]. Disponível em: https://repositorio.ul.pt/bitstream/10451/43654/1/VeraPBarata.pdf
https://repositorio.ul.pt/bitstream/1045...
, 33.Toledo WW, Vieira CA, Alcantara YB, Luiz AL, Lima KR, Pereira VS, et al. Avaliação da função auditiva em idosos presbiacúsicos com e sem transtorno cognitivo leve. In: Menezes PL, Andrade KC, Carnaúba AT, Frizzo AC, Anastasio AR, organizadores. Atualidades do I Congresso Internacional de Eletrofisiologia para Audiologia. Atena; 2020. Capítulo 37. p. 73-4. ) which reflects the functional decline of structures of the peripheral auditory system.( 11.Santos GL. Expressão de proteínas ligantes de cálcio e receptores de melatonina em centros encefálicos da via auditiva no envelhecimento [dissertação]. Marília: Universidade Estadual Paulista, Programa de Pós-Graduação em Fonoaudiologia da Faculdade de Filosofia e Ciências; 2019 [citado 2021 Jul 16]. Disponível em: https://repositorio.unesp.br/bitstream/handle/11449/182185/santos_gls_me_mar.pdf?sequence=3&isAllowed=y
https://repositorio.unesp.br/bitstream/h...
)

However, the most frequent complaint among the elderly is decline of speech understanding, particularly in noisy environments. This type of hearing impairment involves several central auditory structures and cannot be explained by increase in auditory thresholds alone.( 44.Profant O, Jilek M, Bures Z, Vencovsky V, Kucharova D, Svobodova V, et al. Functional age-related changes within the human auditory system studied by audiometric examination. Front Aging Neurosci. 2019;11:26. )

Two noninvasive objective potentials can be used to assess central auditory function: the brainstem auditory evoked potential (BAEP) with click stimulus, and frequency-following response (FFR). The BAEP is generated by structures located between the auditory portion of the vestibulocochlear nerve (cranial nerve VIII) and the brainstem and is therefore a short-latency potential.( 55.Casali RL, Santos MF. Auditory brainstem evoked response: response patterns of full-term and premature infants. Braz J Otorhinolaryngol. 2010;76(6):729-38. )

The FFR reflects the encoding of speech sounds along the central auditory nervous system,( 66.Bueno CD. Aplicabilidade do potencial evocado auditivo frequency following response em crianças e adolescentes: uma revisão sistemática com metanálise [dissertação]: Porto Alegre: Universidade Federal do Rio Grande do Sul; 2020 [citado 2021 Jul 16]. Disponível em: https://www.lume.ufrgs.br/bitstream/handle/10183/211295/001115077.pdf?sequence=1
https://www.lume.ufrgs.br/bitstream/hand...
) with subcortical responses( 77.Anderson S, Parbery-Clark A, White-Schwoch T, Kraus N. Auditory brainstem response to complex sounds predicts self-reported speech-in-noise performance. J Speech Lang Hear Res. 2013;56(1):31-43. ) and potential cortical contributions.( 88.Coffey EB, Herholz SC, Chepesiuk AM, Baillet S, Zatorre RJ. Cortical contributions to the auditory frequency-following response revealed by MEG. Nat Commun. 2016;7:11070. )

The reliability of measures which involve behavioral assessment must be verified and validated. Difficulties to resolve and track dynamic sounds impair speech processing in elderly individuals.( 99.Ng CW, Recanzone GH. Age-related changes in temporal processing of rapidly-presented sound sequences in the macaque auditory cortex. Cereb Cortex. 2018;28(11):3775-96. ) This study was designed to understand age-related FFR changes in this population.

Decreasing amplitudes and increasing latencies of BAEP and FFR waves are thought to be valid markers to assess the aging of the auditory system.

OBJECTIVE

To analyze age-related changes in the central auditory pathway in healthy elderly individuals.

METHODS

This prospective, quantitative cross-sectional study was examined and approved by the Research Ethics Committee of Universidade Federal de Santa Maria (UFSM), # 2.456.418, CAAE: 78740117.3.0000.5346. Procedures were carried out in the Speech Pathology and Auditory Electrophysiology Outpatient Service of a teaching hospital.

Individuals who agreed to participate signed an Informed Consent Form and a Confidentiality Form. Research procedures and related risks and benefits were detailed in the Informed Consent Form, in compliance with ethical standards of Resolution # 655/21 of the National Health Council.( 1010.Brasil. Ministério da Saúde. Conselho Nacional de Saúde (CNS). Resolução Nº 655, de 13 de abril de 2021. Dispõe sobre as diretrizes referentes à definição de prioridades para as ações e serviços públicos de saúde que integrarão a Programação Anual de Saúde e o Projeto de Lei de Diretrizes Orçamentárias da União para 2022. Ministério da Saúde; 2021 [citado 2021 Abr 28]. Disponível em: http://conselho.saude.gov.br/images/Resolucoes/2021/Reso655.pdf
http://conselho.saude.gov.br/images/Reso...
)

Eligibility criteria

Subjects were recruited at the aforementioned Speech Pathology service. The following inclusion criteria were adopted: healthy individuals aged 19 to 76 years with normal auditory thresholds in both ears,( 1111.Conselho Federal de Fonoaudiologia (CFF). Sistema de Conselhos de Fonoaudiologia. Sociedade Brasileira de Fonoaudiologia. Guia de orientações na avaliação audiológica básica. Brasília (DF): CFF; 2017 [citado 2021 Abr 28]. Disponível em: https://www.fonoaudiologia.org.br/wp-content/uploads/2019/09/Manual-de-Audiologia-1.pdf
https://www.fonoaudiologia.org.br/wp-con...
) no auditory complaints, bilateral type A tympanogram and right-handed according to the Edinburgh Handedness Inventory. Only elderly individuals with normal scores in the Mini Mental State Examination (MMSE) cognitive screening test were included.

Subjects with auditory complaints or obvious neurologic or psychiatric impairment were excluded.

Caseload

This caseload comprised 36 healthy subjects: 18 adults aged 19 to 30 years (mean age, 22.78 years) and 18 elderly individuals aged 60 to 76 years (mean age, 66.72 years). Groups ( i.e. , adults and elderly individuals) were paired and comprised four males and 14 females each. The level of education was not examined.

Sampling procedures

Subjects were submitted to hearing history-taking, meatoscopy, pure-tone threshold audiometry, speech audiometry, acoustic immitance testing, Edinburgh Handedness Inventory and MMSE.

Research procedures

The BAEP test with click stimulus and the FFR test were carried out using Smart-EP equipment (Intelligent Hearing Systems, IHS). Tests were performed in a single day and lasted approximately 1 hour 30 minutes in both groups.

Individuals were accommodated in a reclining chair prior to skin cleaning with an abrasive paste. To ensure test reliability, tests were carried out with impedance values equal to or lower than 3kOhms and the number of artifacts did not exceed 10% of number of stimuli. Surface electrodes were attached using electrolyte paste and micropre tape. The active (Fz) and ground (Fpz) electrodes were placed on the central aspect of the front (upper and lower portion, respectively). Reference electrodes M1 and M2 were placed on the mastoid process of the temporal bone (left and right side). Stimulii were delivered using insert earphones.

Click-evoked BAEP was recorded using the following settings: 80 dB nHL intensity, 12ms recording window, 2.048 sweeps, 27.7/s rate, 100Hz to 3.000Hz filter (high and low pass, respectively), 100.0K repetition rate, 100μs duration and rarefaction polarity. Waves I, III and V were marked in wave tracings ( Figure 1 ).

Figure 1
Brainstem auditory evoked potential with click stimulus - tracing recorded in one of research subjects

Click-evoked BAEP absolute latency was analyzed using Webster values.( 1212.Webster R. The Auditory Brainstem Response (ABR): a normative study using the intelligent hearing system’s smart evoked potential system[dissertations]. Maryland: Towson University, Department of Audiology, Speech Language Pathology and Deaf Studies; 2017 [cited 2021 Apr 28]. Available from: https://mdsoar.org/bitstream/handle/11603/3281/TSP2016Webster.pdf?sequence=1&isAllowed=y
https://mdsoar.org/bitstream/handle/1160...
)Normality standards for a stimulation intensity of 80 dB nHL were as follows: wave I, 1.66 (Standard deviation, SD 0.10); wave III, 3.87 (SD 0.14); wave V, 5.68 (SD 0.11); interpeak I-III, 2.21 (SD 0.14); interpeak III-V, 1.81 (SD 0.10); interpeak I-V, 4.02 (SD 0.13).

In the FFR test (right ear only, as per guidelines), responses were elicited using the 40ms /da/ syllable provided by the manufacturer, with intensity of 80 dB nHL. Other settings were as follows: 60ms recording window, 40ms pre-stimulation, 100Hz to 3.000Hz filter (high and low pass, respectively), 125μs duration, 10.9/s rate and alterned polarity. A total of 3.000 sweeps were averaged and the resultant wave used in the analysis.( 1313.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(5):217-26. )

Whenever detected, waves V, A, C, D, E, F and O were marked in tracings ( Figure 2 ). The slope (amplitude V - amplitude A/latency A - latency V) was measured manually from baseline. Amplitudes were marked placing the cursor on the tip of each peak and troughs.

Figure 2
Frequency-following response - tracing recorded in one of research subjects

Absolute latency was estimated according to the following values Filippini et al:( 1313.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(5):217-26. ) wave V, 6.46ms; wave A, 7.37ms; wave C, 18.32ms; wave D, 22.47ms; wave E, 30.64ms; wave F, 39.19ms; wave O, 48.01ms. Frequency analysis (pitch and harmonics) could not be carried out since the module required was not available at the organization.

Numerical variables were analyzed using descriptive statistics (mean and SD). Auditory potential data were compared using non-parametric tests (U or Mann-Whitney). The level of significance was set at 5% (<0.05).

RESULTS

Results shown in figures 3 and 4 represent absolute and interpeak latencies of waves I, III and V recorded in right and left ears. Different numbers (n) of adult and elderly subjects reflect absence of waves in testing.

Figure 3
Comparison of latencies and interpeaks of brainstem auditory evoked potential with click stimulus (right ear)

Figure 4
Comparison of latencies and interpeaks of brainstem auditory evoked potential with click stimulus (left ear)

Figures 5 to 7 show the analysis of FFR test results (absolute latencies of waves, slopes, and amplitudes and interpeaks).

Figure 5
Comparison of latencies and slope of frequency-following response with speech stimulus between adult and elderly individuals

Figure 6
Comparison of amplitudes of frequency-following response with speech stimulus between adult and elderly individuals

Figure 7
Comparison of interpeaks of frequency-following response with speech stimulus between adult and elderly individuals

DISCUSSION

This study provides insights into the aging of the auditory system in healthy subjects from the analysis of brainstem, subcortical and cortical auditory evoked potentials. Age-stratified investigation is vital for interpretation of diagnostic audiologic evaluation findings to support appropriate speech and hearing rehabilitation.

As hypothesized in this study, aging is associated with higher absolute latency of BAEP waves I, III and V, and with interpeak changes. These data show longer time is required for auditory stimuli to travel along the auditory pathway to the brainstem in elderly individuals and are consistent with prior studies( 1414.Samelli AG, Matas CG, Rabelo CM, Magliaro FC, Luiz NP, Silva LD. Peripheral and central auditory assessment in among the elderly. Rev Bras Geriatr Gerontol. 2016;19(5):839-49. , 1515.Gupta S, Gupta G. Brainstem auditory evoked potentials in the older population. Natl J Physiol Pharm Pharmacol. 2017;7(3):290-6. ) addressing the impact of age on absolute BAEP latencies and interpeaks. According to Gupta et al.,( 1515.Gupta S, Gupta G. Brainstem auditory evoked potentials in the older population. Natl J Physiol Pharm Pharmacol. 2017;7(3):290-6. ) central conduction involving the superior olivary complex and the inferior colliculus is compromised with increasing age.

Wave I was absent in the left ear in four out of 18 elderly individuals in this sample. These findings are in keeping with data reported by Matas et al.( 1616.Matas CG, Filha VA, Okada MM, Resque JR. Auditory evoked potentials in individuals over 50 years. ProFono. 2006;18(3):277-84. ) In that study, absence of BAEP waves was the most common change detected in subjects aged 70 to 79 years, indicating impaired neural synchrony.

As to FFR, most studies have reported on pediatric rather than elderly populations. Significant increase in latency and decrease in amplitude and slope values were observed in elderly individuals. Likewise, in a study( 1717.Clinard CG, Tremblay KL. Aging degrades the neural encoding of simple and complex sounds in the human brainstem. J Am Acad Audiol. 2013;24(7):590-9; quiz 643-4. ) with 34 subjects aged 22 to 77 years, aging was associated with longer wave latency and less robust responses with lower amplitudes.

Lower slope values in elderly individuals suggest deficient temporal synchrony in generators. Importantly, studies( 1818.Pereira LD, Dias TL, Andrade AN. Escuta dicótica, ordenação temporal e o processo de envelhecimento saudável. Estud Interdiscipl Envelhec. 2016;21(3):145-59. , 1919.Deperon TM, Silva IM, Caldas FF, Mendes BC, Novaes BC. Processamento temporal auditivo em idosos. Distúrbios Comun. 2016;28(3):530-8. ) have shown that aging has a significant impact on temporal processing, interfering with the ability to track rapid changes in sound stimuli. Profant et al.( 44.Profant O, Jilek M, Bures Z, Vencovsky V, Kucharova D, Svobodova V, et al. Functional age-related changes within the human auditory system studied by audiometric examination. Front Aging Neurosci. 2019;11:26. ) also alluded to the significance of temporal processing for speech understanding in complex listening environments, as did other authors Skoe et al.,( 2020.Skoe E, Krizman J, Anderson S, Kraus N. Stability and plasticity of auditory brainstem function across the lifespan. Cereb Cortex. 2015;25(6):1415-26. )who investigated 24 elderly individuals with normal auditory thresholds and reported stable FFR responses among adults and higher FFR latencies in elderly populations.

The auditory pathway is a sensory system that can be stimulated by environmental stimuli and communication. Hence, speech pathologists should submit patients to subjective and objective qualitative assessment. In this study, FFR was an effective tool for objective monitoring of auditory pathway aging. Different variables with potential impacts on the central auditory pathway of elderly individuals must be accounted for. These factors are also implicated in diagnosis and rehabilitation processes.

CONCLUSION

Brainstem auditory evoked potential and frequency-following response allowed appropriate assessment of the aging of the auditory pathway in healthy elderly individuals. Slower neural response to auditory stimuli suggested reduced synchrony between neural structures.

REFERENCES

  • 1
    Santos GL. Expressão de proteínas ligantes de cálcio e receptores de melatonina em centros encefálicos da via auditiva no envelhecimento [dissertação]. Marília: Universidade Estadual Paulista, Programa de Pós-Graduação em Fonoaudiologia da Faculdade de Filosofia e Ciências; 2019 [citado 2021 Jul 16]. Disponível em: https://repositorio.unesp.br/bitstream/handle/11449/182185/santos_gls_me_mar.pdf?sequence=3&isAllowed=y
    » https://repositorio.unesp.br/bitstream/handle/11449/182185/santos_gls_me_mar.pdf?sequence=3&isAllowed=y
  • 2
    Barata VP. Presbiacusia: fator de risco para o declínio cognitivo? [dissertação]. Lisboa: Universidade de Lisboa, Faculdade de Medicina; 2019 [citado 2021 Jul 16]. Disponível em: https://repositorio.ul.pt/bitstream/10451/43654/1/VeraPBarata.pdf
    » https://repositorio.ul.pt/bitstream/10451/43654/1/VeraPBarata.pdf
  • 3
    Toledo WW, Vieira CA, Alcantara YB, Luiz AL, Lima KR, Pereira VS, et al. Avaliação da função auditiva em idosos presbiacúsicos com e sem transtorno cognitivo leve. In: Menezes PL, Andrade KC, Carnaúba AT, Frizzo AC, Anastasio AR, organizadores. Atualidades do I Congresso Internacional de Eletrofisiologia para Audiologia. Atena; 2020. Capítulo 37. p. 73-4.
  • 4
    Profant O, Jilek M, Bures Z, Vencovsky V, Kucharova D, Svobodova V, et al. Functional age-related changes within the human auditory system studied by audiometric examination. Front Aging Neurosci. 2019;11:26.
  • 5
    Casali RL, Santos MF. Auditory brainstem evoked response: response patterns of full-term and premature infants. Braz J Otorhinolaryngol. 2010;76(6):729-38.
  • 6
    Bueno CD. Aplicabilidade do potencial evocado auditivo frequency following response em crianças e adolescentes: uma revisão sistemática com metanálise [dissertação]: Porto Alegre: Universidade Federal do Rio Grande do Sul; 2020 [citado 2021 Jul 16]. Disponível em: https://www.lume.ufrgs.br/bitstream/handle/10183/211295/001115077.pdf?sequence=1
    » https://www.lume.ufrgs.br/bitstream/handle/10183/211295/001115077.pdf?sequence=1
  • 7
    Anderson S, Parbery-Clark A, White-Schwoch T, Kraus N. Auditory brainstem response to complex sounds predicts self-reported speech-in-noise performance. J Speech Lang Hear Res. 2013;56(1):31-43.
  • 8
    Coffey EB, Herholz SC, Chepesiuk AM, Baillet S, Zatorre RJ. Cortical contributions to the auditory frequency-following response revealed by MEG. Nat Commun. 2016;7:11070.
  • 9
    Ng CW, Recanzone GH. Age-related changes in temporal processing of rapidly-presented sound sequences in the macaque auditory cortex. Cereb Cortex. 2018;28(11):3775-96.
  • 10
    Brasil. Ministério da Saúde. Conselho Nacional de Saúde (CNS). Resolução Nº 655, de 13 de abril de 2021. Dispõe sobre as diretrizes referentes à definição de prioridades para as ações e serviços públicos de saúde que integrarão a Programação Anual de Saúde e o Projeto de Lei de Diretrizes Orçamentárias da União para 2022. Ministério da Saúde; 2021 [citado 2021 Abr 28]. Disponível em: http://conselho.saude.gov.br/images/Resolucoes/2021/Reso655.pdf
    » http://conselho.saude.gov.br/images/Resolucoes/2021/Reso655.pdf
  • 11
    Conselho Federal de Fonoaudiologia (CFF). Sistema de Conselhos de Fonoaudiologia. Sociedade Brasileira de Fonoaudiologia. Guia de orientações na avaliação audiológica básica. Brasília (DF): CFF; 2017 [citado 2021 Abr 28]. Disponível em: https://www.fonoaudiologia.org.br/wp-content/uploads/2019/09/Manual-de-Audiologia-1.pdf
    » https://www.fonoaudiologia.org.br/wp-content/uploads/2019/09/Manual-de-Audiologia-1.pdf
  • 12
    Webster R. The Auditory Brainstem Response (ABR): a normative study using the intelligent hearing system’s smart evoked potential system[dissertations]. Maryland: Towson University, Department of Audiology, Speech Language Pathology and Deaf Studies; 2017 [cited 2021 Apr 28]. Available from: https://mdsoar.org/bitstream/handle/11603/3281/TSP2016Webster.pdf?sequence=1&isAllowed=y
    » https://mdsoar.org/bitstream/handle/11603/3281/TSP2016Webster.pdf?sequence=1&isAllowed=y
  • 13
    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(5):217-26.
  • 14
    Samelli AG, Matas CG, Rabelo CM, Magliaro FC, Luiz NP, Silva LD. Peripheral and central auditory assessment in among the elderly. Rev Bras Geriatr Gerontol. 2016;19(5):839-49.
  • 15
    Gupta S, Gupta G. Brainstem auditory evoked potentials in the older population. Natl J Physiol Pharm Pharmacol. 2017;7(3):290-6.
  • 16
    Matas CG, Filha VA, Okada MM, Resque JR. Auditory evoked potentials in individuals over 50 years. ProFono. 2006;18(3):277-84.
  • 17
    Clinard CG, Tremblay KL. Aging degrades the neural encoding of simple and complex sounds in the human brainstem. J Am Acad Audiol. 2013;24(7):590-9; quiz 643-4.
  • 18
    Pereira LD, Dias TL, Andrade AN. Escuta dicótica, ordenação temporal e o processo de envelhecimento saudável. Estud Interdiscipl Envelhec. 2016;21(3):145-59.
  • 19
    Deperon TM, Silva IM, Caldas FF, Mendes BC, Novaes BC. Processamento temporal auditivo em idosos. Distúrbios Comun. 2016;28(3):530-8.
  • 20
    Skoe E, Krizman J, Anderson S, Kraus N. Stability and plasticity of auditory brainstem function across the lifespan. Cereb Cortex. 2015;25(6):1415-26.

Publication Dates

  • Publication in this collection
    27 May 2022
  • Date of issue
    2022

History

  • Received
    15 June 2021
  • Accepted
    30 Sept 2021
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