Encoding of speech sounds with frequency-following response in infants with Congenital Zika Syndrome: A case-controlled study

Caroline Donadon; Milaine Dominici Sanfins; Natalia Ferrazoli; Tatiana Bordin Taglianetti; Silvana Maria Sobral Griz; Piotr Henryk Skarzynski; Lavínia Brandão; Adriana Melo

doi:10.1590/1982-0216/20242613223

Original Articles

Encoding of speech sounds with frequency-following response in infants with Congenital Zika Syndrome: A case-controlled study

Caroline Donadon; Milaine Dominici Sanfins; Natalia Ferrazoli; Tatiana Bordin Taglianetti; Silvana Maria Sobral Griz; Piotr Henryk Skarzynski; Lavínia Brandão; Adriana Melo

http://dx.doi.org/10.1590/1982-0216/20242613223 Revista CEFAC, vol.26, n1, e3223, 2024

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Abstract

Purpose: to investigate the frequency-following response (FFR) for sustained neural activity.

Methods: 39 individuals, aged between 20 to 47 months old were divided into 2 groups: (i) 20 individuals without prenatal exposure to the congenital Zika syndrome (CZS) or hydrocephaly, normal development, no risk factors for hearing loss or syndromic hearing impairment and (ii) 19 individuals diagnosed with CZS and microcephaly - based on imaging studies linked to the clinical presentation of the condition. All participants exhibited normal click-ABR tests. FFR waveforms were documented using the /da/ syllable employing the Navigator Pro. The statistical analysis used was ANOVA (p-value <0.05).

Results: no distinctions were observed concerning the variables of group, age, or gender with respect to FFR latency values, except for an interaction between gender and group for latency values associated with waves V and F. Children with CZS and microcephaly showed a difference for latency values in wave V for both males and females, when compared to the control group.

Conclusion: children presented with CZS and microcephaly showed higher average latencies for waves V, A, C, D and F (male) compared to the control group, whereas, in waves E, F (female) and O they showed higher values in the control group.

Keywords

Hearing, Zika Virus Infection, Microcephaly, Child, Speech Perception

Referencias

1. Joint Committee on Infant Hearing, Position Statement: principles and guidelines for early hearing detection and intervention programs. Pediatrics. 2007;120:898-921. https://doi.org/10.1542/peds.2007-2333 PMID: 17908777.

2. Joint Committee on Infant Hearing Year 2019 position statement: principles and guidelines for early hearing detection and intervention programs. J Early Hear Detect Interv. 2019;4(2):1-44. https://doi.org/10.15142/fptk-b748

3. Melo AS, Aguiar RS, Amorim MM, Arruda MB, Melo FO, Ribeiro STC et al. Congenital Zika virus infection: beyond neonatal microcephaly. JAMA Neurol. 2016;73(12):1407-16. https://doi.org/10.1001/jamaneurol.2016.3720 PMID: 27695855.

4. Mlakar J, Korva M, Tul N, Popovic M, Poljšak-Prijatelj M, Mraz J et al. Zika Virus associated with microcephaly. N Engl J Med. 2016;374(10):951-8. https://doi.org/10.1056/NEJMoa1600651 PMID: 26862926.

5. Ventura CV, Maia M, Bravo-Filho V, Góis AL, Belfort R. Zika virus in Brazil and macular atrophy in a child with microcephaly. Lancet. 2016;387(10015):228. https://doi.org/10.1016/S0140-6736(16)00006-4 PMID: 26775125.

6. Moore CA, Staples JE, Dobyns WB, Pessoa A, Ventura CV, Fonseca EB et al. Characterizing the pattern of anomalies in congenital Zika syndrome for pediatric clinicians. JAMA Pediatr. 2017;171(3):288-95. https://doi.org/10.1001/jamapediatrics.2016.3982 PMID: 27812690.

7. Center for disease control and prevention (CDC). Congenital Zika Syndrome & Other Birth Defects. Available at: https://www.cdc.gov/pregnancy/zika/testing-follow-up/zika-syndrome-birth-defects.html

8. Lage M, de Carvalho A, Ventura P, Taguchi T, Fernandes A, Pinho S et al. Clinical, Neuroimaging, and neurophysiological findings in children with microcephaly related to congenital Zika virus infection. Int J Environ Res Public Health. 2019;16(3):309. https://doi.org/10.3390/ijerph16030309 PMID: 30678125.

9. Satterfield-Nash A, Kotzky K, Allen J, Bertolli J, Moore CA, Pereira IO et al. Health and development at age 19-24 months of 19 children who were born with microcephaly and laboratory evidence of congenital Zika virus infection during the 2015 Zika virus outbreak - Brazil, 2017. MMWR Morb Mortal Wkly Rep. 2017;66(49):1347-51. https://doi.org/10.15585/mmwr.mm6649a2 PMID: 29240727.

10. Leal MC, Muniz LF, Caldas Neto SD, van der Linden V, Ramos RC. Sensorineural hearing loss in a case of congenital Zika virus. Braz J Otorhinolaryngol. 2020;86(4):513-5. https://doi.org/10.1016/j.bjorl.2016.06.001 PMID: 27444419.

11. Van der Linden V, Pessoa A, Dobyns W, Barkovich AJ, van der Linden Júnior H, Rolim Filho EL et al. Description of 13 infants born during october 2015-january 2016 with congenital Zika virus infection without microcephaly at birth - Brazil. MMWR Morb Mortal Wkly Rep. 2016;65(47):1343-8. https://doi.org/10.15585/mmwr.mm6547e2 PMID: 27906905.

12. Muniz LF, Maciel RJF, Ramos DS, Albuquerque KMG, Leão ÂC, Van Der Linden V et al. Audiological follow-up of children with congenital Zika syndrome. Heliyon. 2022;8(1):e08720. https://doi.org/10.1016/j.heliyon.2022.e08720 PMID: 35059518.

13. Sanfins MD, Brandão L, Skarzynski PH, Griz S, Melo A. Auditory evaluation in a case of hearing loss in an infant with congenital Zika syndrome (CZS). J Hear Sci. 2021;11(1):65-71. https://doi.org/10.17430/JHS.2021.11.1.7

14. Ferreira L, Skarzynski PH, Skarzynska MB, Sanfins MD, Biaggio EPV. Effect of auditory maturation on the encoding of a speech syllable in the first days of life. Brain Sci. 2021;11(7):844. https://doi.org/10.3390/brainsci11070844 PMID: 34202020.

15. Hornickel J, Kraus N. Unstable representation of sound: a biological marker of dyslexia. J Neurosci. 2013;33(8):3500-4. https://doi.org/10.1523/JNEUROSCI.4205-12.2013 PMID: 23426677.

16. Hora LCD, Muniz LF, Griz SMS, Silva JD, Britto DBLA, Venâncio LGA et al. Frequency-Following Response and auditory behavior in children with prenatal exposure to the Zika virus. Int Arch Otorhinolryngol. 2022;26(3):380-9. https://doi.org/10.1055/s-0041-1726048 PMID: 35846828.

17. Ferreira L, Valadão MCDS, Skarzynski PH, Sanfins MD, Biaggio EPV. Effect of congenital toxoplasmosis on the encoding of speech in infants. Int J Pediatr Otorhinolaryngol. 2020;129:109767. https://doi.org/10.1016/j.ijporl.2019.109767 PMID: 31726372.

18. White-Schwoch T, Anderson S, Krizman J, Bonacina S, Nicol T, Bradlow AR et al. Multiple cases of auditory neuropathy illuminate the importance of subcortical neural synchrony for speech-in-noise recognition and the frequency-following response. Ear Hear. 2022;43(2):605-19. https://doi.org/10.1097/AUD.0000000000001122 PMID: 34619687.

19. Picton TW, Durieux-Smith A, Moran LM. Recording auditory brainstem responses from infants. Int J Pediatr Otorhinolaryngol. 1994;28(2-3):93-110. https://doi.org/10.1016/0165-5876(94)90001-9 PMID: 8157427.

20. Gorina-Careta N, Ribas-Prats T, Arenillas-Alcón S, Puertollano M, Gómez-Roig MD, Escera C. Neonatal Frequency-Following Responses: a methodological framework for clinical applications. Semin Hear. 2022;43(3):162-76. https://doi.org/10.1055/s-0042-1756162 PMID: 36313048.

21. Jeng FC, Lin CD, Chou MS, Hollister GR, Sabol JT, Mayhugh GN et al. Development of subcortical pitch representation in three-month-old chinese infants. Percept Mot Skills. 2016;122(1):123-35. https://doi.org/10.1177/0031512516631054 PMID: 27420311.

22. Anderson S, Parbery-Clark A, White-Schwoch T, Kraus N. Development of subcortical speech representation in human infants. J Acoust Soc Am. 2015;137(6):3346-55. https://doi.org/10.1121/1.4921032 PMID: 26093424.

23. Kraus N, Anderson S, White-Schwoch T. The Frequency-Following Response: a window into human communication. Vol 61. Cham, Switzerland: Springer International Publishing; 2017.

24. Jerger J. Clinical experience with impedance audiometry. Arch Otolaryngol. 1970;92(4):311-24. https://doi.org/10.1001/archotol.1970.04310040005002 PMID: 5455571.

25. Hornickel J, Skoe E, Kraus N. Subcortical laterality of speech encoding. Audiol Neurootol. 2009;14(3):198-207. https://doi.org/10.1159/000188533 PMID: 19122453.

26. Krizman J, Skoe E, Kraus N. Sex differences in auditory subcortical function. Clin Neurophysiol. 2012;123(3):590-7. https://doi.org/10.1016/j.clinph.2011.07.037 PMID: 21855407.

27. Don M, Ponton CW, Eggermont JJ, Masuda A. Gender differences in cochlear response time: an explanation for gender amplitude differences in the unmasked auditory brain-stem response. J Acoust Soc Am. 1993;94(4):2135-48. https://doi.org/10.1121/1.407485 PMID: 8227753.

28. Bowman DM, Brown DK, Kimberley BP. An examination of gender differences in DPOAE phase delay measurements in normal-hearing human adults. Hear Res. 2000;142(1-2):1-11. https://doi.org/10.1016/s0378-5955(99)00212-9 PMID:10748323.

29. Friel-Patti S, Finitzo T. Language learning in a prospective study of otitis media with effusion in the first two years of life. J Speech Hear Res. 1990;33(1):188-94. https://doi.org/10.1044/jshr.3301.188 PMID: 2314079.

30. Banai K, Hornickel J, Skoe E, Nicol T, Zecker S, Kraus N. Reading and subcortical auditory function. Cereb Cortex. 2009;19(11):2699-707. https://doi.org/10.1093/cercor/bhp024 PMID: 19293398.

31. Basu M, Krishnan A, Weber-Fox C. Brainstem correlates of temporal auditory processing in children with specific language impairment. Developmental Science. 2010;13(1):77-91. https://doi.org/10.1111/j.1467-7687.2009.00849.x PMID: 20121865.

32. Hornickel J, Chandrasekaran B, Zecker S, Kraus N. Auditory brainstem measures predict reading and speech-in-noise perception in school-aged children. Behav Brain Res. 2011;216(2):597-605. https://doi.org/10.1016/j.bbr.2010.08.051 PMID: 20826187.

33. 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(4):557-67. https://doi.org/10.1111/j.1467-7687.2008.00790.x PMID: 19635083.

34. Santiago JM, Luiz CBL, Garcia M, Gil D. Masking Level difference and electrophysiological evaluation in adults with normal hearing. Int Arch Otor. 2020;24(4):e399-e406. https://doi.org/10.1055/s-0040-1701266 PMID: 33101502.

35. Chandrasekaran B, Kraus N. The scalp-recorded brainstem response to speech: neural origins and plasticity. Psychophysiology. 2010;47(2):236-46. https://doi.org/10.1111/j.1469-8986.2009.00928.x PMID: 19824950.

36. Sanfins MD, Borges LR, Donadon C, Hatzopoulos S, Skarzynski PH, Colella-Santos MF. Electrophysiological responses to speech stimuli in children with otitis media. J Hear Sci. 2017;7(4):9-19. https://doi.org/10.17430/1002726

37. Colella-Santos MF, Donadon C, Sanfins MD, Borges LR. Otitis Media: long-term effect on central auditory nervous system. Biomed Res Int. 2019;2019:8930904. https://doi.org/10.1155/2019/8930904 PMID: 31032365.

38. Elmahallawi TH, Gabr TA, Darwish ME, Seleem FM. Children with developmental language disorder: a frequency following response in the noise study. Braz J Otorhinolaryngol. 2022;88(6):954-61. https://doi.org/ 10.1016/j.bjorlp.2022.09.019

39. Skoe E, Krizman J, Spitzer E, Kraus N. The auditory brainstem is a barometer of rapid auditory learning. Neuroscience. 2013;243:104-14. https://doi.org/10.1016/j.neuroscience.2013.03.009 PMID: 23518221.

40. Barman A, Prabhu P, Mekhala VG, Vijayan K, Swapna N. Auditory processing in children with specific language impairment: a FFR based study. Indian J Otolaryngol Head Neck Surg. 2022;74(Suppl 1):368-73. https://doi.org/10.1007/s12070-020-02127-x PMID: 36032839.

Submitted date:
17/04/2023

Accepted date:
16/10/2023

Encoding of speech sounds with frequency-following response in infants with Congenital Zika Syndrome: A case-controlled study

Caroline Donadon; Milaine Dominici Sanfins; Natalia Ferrazoli; Tatiana Bordin Taglianetti; Silvana Maria Sobral Griz; Piotr Henryk Skarzynski; Lavínia Brandão; Adriana Melo

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