Auditory brainstem response in infants and children with autism spectrum disorder: A meta-analysis of wave V

Oren Miron, Andrew L Beam, Isaac S Kohane, Oren Miron, Andrew L Beam, Isaac S Kohane

Abstract

Infants with autism spectrum disorder (ASD) were recently found to have prolonged auditory brainstem response (ABR); however, at older ages, findings are contradictory. We compared ABR differences between participants with ASD and controls with respect to age using a meta-analysis. Data sources included MEDLINE, EMBASE, Web of Science, Google Scholar, HOLLIS, and ScienceDirect from their inception to June 2016. The 25 studies that were included had a total of 1349 participants (727 participants with ASD and 622 controls) and an age range of 0-40 years. Prolongation of the absolute latency of wave V in ASD had a significant negative correlation with age (R2 = 0.23; P = 0.01). The 22 studies below age 18 years showed a significantly prolonged wave V in ASD (Standard Mean Difference = 0.6 [95% CI, 0.5-0.8]; P < 0.001). The 3 studies above 18 years of age showed a significantly shorter wave V in ASD (SMD = -0.6 [95% CI, -1.0 to -0.2]; P = 0.004). Prolonged ABR was consistent in infants and children with ASD, suggesting it can serve as an ASD biomarker at infancy. As the ABR is routinely used to screen infants for hearing impairment, the opportunity for replication studies is extensive. Autism Res 2018, 11: 355-363. © 2017 The Authors Autism Research published by International Society for Autism Research and Wiley Periodicals, Inc.

Lay summary: Our analysis of previous studies showed that infants and children with autism spectrum disorder (ASD) have a slower brain response to sound, while adults have a faster brain response to sound. This suggests that slower brain response in infants may predict ASD risk. Brain response to sound is routinely tested on newborns to screen hearing impairment, which has created large data sets to afford replication of these results.

Keywords: auditory; biomarker; children; event related potential; infants.

© 2017 The Authors Autism Research published by International Society for Autism Research and Wiley Periodicals, Inc.

Figures

Figure 1
Figure 1
Inclusion of studies in meta‐analysis.
Figure 2
Figure 2
Correlation of wave V ASD prolongation and age. Legend: Y = Wave V ASD prolongation in percentage. X = mean age at time of ABR in years. Blue line = Linear regression. Grey area = Linear regression confidence interval of 95%. White names indicate first author name and circle size corresponds to sample size. For example, Circle “Cohen” represents Cohen et al. [2013] and the size corresponds to a sample size of 70 participants.
Figure 3
Figure 3
Correlation of IPL I–V ASD prolongation and age. Legend: Y = IPL I–V ASD prolongation in percentage. X = mean age at time of ABR in years. Blue line = Linear regression. Grey area = Linear regression confidence interval of 95%. White names indicate first author name and circle size corresponds to sample size. For example, Circle “Cohen” represents Cohen et al. [2013] and the size corresponds to a sample size of 70 participants.
Figure 4
Figure 4
Forest plot of ASD prolongation. Legend: Study (first author), year (publication); Age (mean in years); Sample (combined for ASD and controls); V‐ Wave V latency; SD‐ Standard Deviation; Black square indicates SMD and error bars indicate confidence interval of 95%, which are indicated numerically under ASD Prolongation [95% CI]. Square size indicates the proportional weight of the study on the combined SMD.

References

    1. American‐Psychiatric‐Association . (2013). Diagnostic and statistical manual of mental disorders: DSM‐V (5th ed.). Washington, DC: American‐Psychiatric‐Association.
    1. Azouz, H.G. , Kozou, H. , Khalil, M. , Abdou, R.M. , & Sakr, M. (2014). The correlation between central auditory processing in autistic children and their language processing abilities. International Journal of Pediatric Otorhinolaryngology, 78, 2297–2300. doi:
    1. Bruneau, N. , Roux, S. , Adrien, J.L. , & Barthélémy, C. (1999). Auditory associative cortex dysfunction in children with autism: Evidence from late auditory evoked potentials (N1 wave–T complex). Clinical Neurophysiology, 110, 1927–1934. Retrieved from
    1. Cohen, I.L. , Gardner, J.M. , Karmel, B.Z. , Phan, H.T. , Kittler, P. , Gomez, T.R. , … Barone, A. (2013). Neonatal brainstem function and 4‐month arousal‐modulated attention are jointly associated with autism. Autism Research, 6, 11–22. doi:
    1. Courchesne, E. , Campbell, K. , & Solso, S. (2011). Brain growth across the life span in autism: age‐specific changes in anatomical pathology. Brain Research, 1380, 138–145. doi:
    1. Courchesne, E. , Carper, R. , & Akshoomoff, N. (2003). Evidence of brain overgrowth in the first year of life in autism. The Journal of the American Medical Association, 290, 337–344. doi:
    1. Courchesne, E. , Courchesne, R.Y. , Hicks, G. , & Lincoln, A.J. (1985). Functioning of the brain‐stem auditory pathway in non‐retarded autistic individuals. Electroencephalography and Clinical Neurophysiology, 61, 491–501.
    1. Courchesne, E. , Kilman, B.A. , Galambos, R. , & Lincoln, A.J. (1984). Autism: processing of novel auditory information assessed by event‐related brain potentials. Electroencephalography and Clinical Neurophysiology, 59, 238–248.
    1. Courchesne, E. , Mouton, P.R. , Calhoun, M.E. , Semendeferi, K. , Ahrens‐Barbeau, C. , Hallet, M.J. , … Pierce, K. (2011). Neuron number and size in prefrontal cortex of children with autism. The Journal of the American Medical Association, 306, 2001. (2010). doi:
    1. Coutinho, M.B. , Rocha, V. , & Santos, M.C. (2002). Auditory brainstem response in two children with autism. International Journal of Pediatric Otorhinolaryngology, 66, 81–85. doi:
    1. Dabbous, A.O. (2012). Characteristics of auditory brainstem response latencies in children with autism spectrum disorders. Audiological Medicine, 10, 122–131. doi:
    1. Dawson, G. , Rogers, S. , Munson, J. , Smith, M. , Winter, J. , Greenson, J. , … Varley, J. (2010). Randomized, controlled trial of an intervention for toddlers with autism: The Early Start Denver Model. Pediatrics, 125, 17–23.
    1. Demopoulos, C. , & Lewine, J.D. (2016). Audiometric profiles in autism spectrum disorders: Does subclinical hearing loss impact communication? Autism Research, 9, 107–120. doi:
    1. Demopoulos, C. , Yu, N. , Tripp, J. , Mota, N. , Brandes‐Aitken, A.N. , Desai, S.S. , … Marco, E.J. (2017). Magnetoencephalographic imaging of auditory and somatosensory cortical responses in children with autism and sensory processing dysfunction. Frontiers in Human Neuroscience, 11, 259. doi:
    1. DerSimonian, R. , & Laird, N. (1986). Meta‐analysis in clinical trials. Controlled Clinical Trials, 7, 177–188. doi:
    1. Developmental Disabilities Monitoring Network Surveillance Year 2010 Principal Investigators, & Centers for Disease Control and Prevention (CDC) . (2014). Prevalence of autism spectrum disorder among children aged 8 years ‐ autism and developmental disabilities monitoring network, 11 sites, United States, 2010. MMWR. Surveillance Summaries, 63, 1–21.
    1. Doshi‐Velez, F. , Ge, Y. , & Kohane, I. (2014). Comorbidity clusters in autism spectrum disorders: An electronic health record time‐series analysis. Pediatrics, 133, e54–e63. doi:
    1. Driscoll, C.J. , & McPherson, B. (2010). Newborn screening systems: The complete perspective (reprint.). San Diego: Plural Publishing.
    1. Edgar, J.C. , Khan, S.Y. , Blaskey, L. , Chow, V.Y. , Rey, M. , Gaetz, W. , … Roberts, T.P.L. (2015). Neuromagnetic oscillations predict evoked‐response latency delays and core language deficits in autism spectrum disorders. Journal of Autism and Developmental Disorders, 45, 395–405. doi:
    1. Edgar, J.C. , Lanza, M.R. , Daina, A.B. , Monroe, J.F. , Khan, S.Y. , Blaskey, L. , … Roberts, T.P.L. (2014). Missing and delayed auditory responses in young and older children with autism spectrum disorders. Frontiers in Human Neuroscience, 8, 417. doi:
    1. Fujikawa‐Brooks, S. , Isenberg, A.L. , Osann, K. , Spence, M.A. , & Gage, N.M. (2010). The effect of rate stress on the auditory brainstem response in autism: A preliminary report. International Journal of Audiology, 49, 129–140. doi:
    1. Gage, N.M. , Siegel, B. , Callen, M. , & Roberts, T.P.L. (2003). Cortical sound processing in children with autism disorder: An MEG investigation. Neuroreport, 14, 2047–2051. doi:
    1. Gage, N.M. , Siegel, B. , & Roberts, T.P.L. (2003). Cortical auditory system maturational abnormalities in children with autism disorder: An MEG investigation. Developmental Brain Research, 144, 201–209. Retrieved from
    1. Gai, X. , Xie, H.M. , Perin, J.C. , Takahashi, N. , Murphy, K. , Wenocur, A.S. , … White, P.S. (2012). Rare structural variation of synapse and neurotransmission genes in autism. Molecular Psychiatry, 17, 402–411. doi:
    1. Gillberg, C. , Rosenhall, U. , & Johansson, E. (1983). Auditory brainstem responses in childhood psychosis. Journal of Autism and Developmental Disorders, 13, 181–195.
    1. Grillon, C. , Courchesne, E. , & Akshoomoff, N. (1989). Brainstem and middle latency auditory evoked potentials in autism and developmental language disorder. Journal of Autism and Developmental Disorders, 19, 255–269. doi:
    1. Karmel, B.Z. , Gardner, J.M. , Meade, L.S. , Cohen, I.L. , London, E. , Flory, M.J. , … Harin, A. (2010). Early medical and behavioral characteristics of NICU infants later classified with ASD. Pediatrics, 126, 457–467. doi:
    1. Kwon, S. , Kim, J. , Choe, B.H. , Ko, C. , & Park, S. (2007). Electrophysiologic assessment of central auditory processing by auditory brainstem responses in children with autism spectrum disorders. Journal of Korean Medical Science, 22, 656–659. doi:
    1. Magliaro, F.C. , Scheuer, C.I. , Assumpção Júnior, F.B. , & Matas, C.G. (2010). Study of auditory evoked potentials in autism. Pro‐Fono: Revista De Atualizacao Cientifica, 22, 31–36.
    1. Maziade, M. , Mérette, C. , Cayer, M. , Roy, M.A. , Szatmari, P. , Côté, R. , & Thivierge, J. (2000). Prolongation of brainstem auditory‐evoked responses in autistic probands and their unaffected relatives. Archives of General Psychiatry, 57, 1077–1083.
    1. McClelland, R.J. , Eyre, D.G. , Watson, D. , Calvert, G.J. , & Sherrard, E. (1992). Central conduction time in childhood autism. The British Journal of Psychiatry, 160, 659–663.
    1. Miron, O. , Ari‐Even Roth, D. , Gabis, L.V. , Henkin, Y. , Shefer, S. , Dinstein, I. , & Geva, R. (2015). Prolonged auditory brainstem responses in infants with autism. Autism Research, 9, 689–695. doi:
    1. Mitchell, C. , Phillips, D.S. , & Trune, D.R. (1989). Variables affecting the auditory brainstem response: Audiogram, age, gender and head size. Hearing Research, 40, 75–85.
    1. Oram Cardy, J.E. , Flagg, E.J. , Roberts, W. , Brian, J. , & Roberts, T.P.L. (2005). Magnetoencephalography identifies rapid temporal processing deficit in autism and language impairment. Neuroreport, 16, 329–332.
    1. Oram Cardy, J.E. , Flagg, E.J. , Roberts, W. , & Roberts, T.P.L. (2005). Delayed mismatch field for speech and non‐speech sounds in children with autism. Neuroreport, 16, 521–525.
    1. Ornitz, E.M. , Mo, A. , Olson, S.T. , & Walter, D.O. (1980). Influence of click sound pressure direction on brainstem responses in children. Audiology, 19, 245–254.
    1. Ornitz, E.M. , & Walter, D.O. (1975). The effect of sound pressure waveform on human brain stem auditory evoked responses. Brain Research, 92, 490–498.
    1. Redcay, E. , & Courchesne, E. (2005). When is the brain enlarged in autism? A meta‐analysis of all brain size reports. Biological Psychiatry, 58, 1–9. doi:
    1. Roberts, T.P. , Lanza, M.R. , Dell, J. , Qasmieh, S. , Hines, K. , Blaskey, L. , … Berman, J.I. (2013). Maturational differences in thalamocortical white matter microstructure and auditory evoked response latencies in autism spectrum disorders. Brain Research, 1537, 79–85. doi:
    1. Roberts, T.P.L. , Cannon, K.M. , Tavabi, K. , Blaskey, L. , Khan, S.Y. , Monroe, J.F. , … Edgar, J.C. (2011). Auditory magnetic mismatch field latency: A biomarker for language impairment in autism. Biological Psychiatry, 70, 263–269. doi:
    1. Roberts, T.P.L. , Khan, S.Y. , Blaskey, L. , Dell, J. , Levy, S.E. , Zarnow, D.M. , & Edgar, J.C. (2009). Developmental correlation of diffusion anisotropy with auditory‐evoked response. Neuroreport, 20, 1586–1591. doi:
    1. Roberts, T.P.L. , Khan, S.Y. , Rey, M. , Monroe, J.F. , Cannon, K. , Blaskey, L. , … Edgar, J.C. (2010). MEG detection of delayed auditory evoked responses in autism spectrum disorders: Towards an imaging biomarker for autism. Autism Research, 3, 8–18. doi:
    1. Rosenblum, S.M. , Arick, J.R. , Krug, D.A. , Stubbs, E.G. , Young, N.B. , & Pelson, R.O. (1980). Auditory brainstem evoked responses in autistic children. Journal of Autism and Developmental Disorders, 10, 215–225.
    1. Rosenhall, U. , Nordin, V. , Brantberg, K. , & Gillberg, C. (2003). Autism and auditory brain stem responses. Ear and Hearing, 24, 206–214. doi:
    1. Rosenhall, U. , Nordin, V. , Sandström, M. , Ahlsen, G. , & Gillberg, C. (1999). Autism and hearing loss. Journal of Autism and Developmental Disorders, 29, 349–357.
    1. Roth, D.A. , Muchnik, C. , Shabtai, E. , Hildesheimer, M. , & Henkin, Y. (2012). Evidence for atypical auditory brainstem responses in young children with suspected autism spectrum disorders. Developmental Medicine and Child Neurology, 54, 23–29. doi:
    1. Rumsey, J.M. , Grimes, A.M. , Pikus, A.M. , Duara, R. , & Ismond, D.R. (1984). Auditory brainstem responses in pervasive developmental disorders. Biological Psychiatry, 19, 1403–1418.
    1. Russo, N. , Nicol, T. , Trommer, B. , Zecker, S. , & Kraus, N. (2009). Brainstem transcription of speech is disrupted in children with autism spectrum disorders. Developmental Science, 12, 557–567. doi:
    1. Santos, M. , Marques, C. , Nóbrega Pinto, A. , Fernandes, R. , Coutinho, M.B. , Almeida, E. , & Sousa, C. (2017). Autism spectrum disorders and the amplitude of auditory brainstem response wave I. Autism Research, 10, 1300–1305. doi:
    1. Sersen, E.A. , Heaney, G. , Clausen, J. , Belser, R. , & Rainbow, S. (1990). Brainstem auditory‐evoked responses with and without sedation in autism and Down's syndrome. Biological Psychiatry, 27, 834–840.
    1. Silverstein, M. , & Radesky, J. (2016). Embrace the complexity. The Journal of the American Medical Association, 315, 661. doi:
    1. Siu, A.L. , U.S., Preventive Services Task Force, (Uspstf,) , Bibbins‐Domingo, K. , Grossman, D.C. , Baumann, L.C. , Davidson, K.W. , … Pignone, M.P. (2016). Screening for autism spectrum disorder in young children: US preventive services task force recommendation statement. The Journal of the American Medical Association, 315, 691–696. doi:
    1. Skoff, B.F. , Mirsky, A.F. , & Turner, D. (1980). Prolonged brainstem transmission time in autism. Psychiatry Research, 2, 157–166.
    1. Sohmer, H. , & Student, M. (1978). Auditory nerve and brain‐stem evoked responses in normal, autistic, minimal brain dysfunction and psychomotor retarded children. Electroencephalography and Clinical Neurophysiology, 44, 380–388.
    1. Starr, A. (1976). Correlation between confirmed sites of neurological lesions and abnormalities of far‐field auditory brainstem responses. Electroencephalography and Clinical Neurophysiology, 41, 595–608. doi:
    1. Stevenson, R.A. , Segers, M. , Ferber, S. , Barense, M.D. , Camarata, S. , & Wallace, M.T. (2016). Keeping time in the brain: Autism spectrum disorder and audiovisual temporal processing. Autism Research, 9, 720–738. doi:
    1. Stevenson, R.A. , Siemann, J.K. , Schneider, B.C. , Eberly, H.E. , Woynaroski, T.G. , Camarata, S.M. , & Wallace, M.T. (2014). Multisensory temporal integration in autism spectrum disorders. The Journal of Neuroscience, 34, 691–697. doi:
    1. Student, M. , & Sohmer, H. (1978). Evidence from auditory nerve and brainstem evoked responses for an organic brain lesion in children with autistic traits. Journal of Autism and Childhood Schizophrenia, 8, 13–20.
    1. Talkowski, M.E. , Maussion, G. , Crapper, L. , Rosenfeld, J.A. , Blumenthal, I. , Hanscom, C. , … Ernst, C. (2012). Disruption of a large intergenic noncoding RNA in subjects with neurodevelopmental disabilities. American Journal of Human Genetics, 91, 1128–1134. doi:
    1. Tanguay, P.E. , Edwards, R.M. , Buchwald, J. , Schwafel, J. , & Allen, V. (1982). Auditory brainstem evoked responses in autistic children. Archives of General Psychiatry, 39, 174–180.
    1. Tas, A. , Yagiz, R. , Tas, M. , Esme, M. , Uzun, C. , & Karasalihoglu, A.R. (2007). Evaluation of hearing in children with autism by using TEOAE and ABR. Autism, 11, 73–79. doi:
    1. Taylor, M.J. , Rosenblatt, B. , & Linschoten, L. (1982). Auditory brainstem response abnormalities in autistic children. The Canadian Journal of Neurological Sciences. Le Journal Canadien Des Sciences Neurologiques, 9, 429–433.
    1. Tharpe, A.M. , Bess, F.H. , Sladen, D.P. , Schissel, H. , Couch, S. , & Schery, T. (2006). Auditory characteristics of children with autism. Ear and Hearing, 27, 430–441. doi:
    1. Thivierge, J. , Bédard, C. , Côté, R. , & Maziade, M. (1990). Brainstem auditory evoked response and subcortical abnormalities in autism. The American Journal of Psychiatry, 147, 1609–1613. doi:
    1. Toma, C. , Torrico, B. , Hervás, A. , Valdés‐Mas, R. , Tristán‐Noguero, A. , Padillo, V. , … Cormand, B. (2014). Exome sequencing in multiplex autism families suggests a major role for heterozygous truncating mutations. Molecular Psychiatry, 19, 784–790. doi:
    1. Ververi, A. , Vargiami, E. , Papadopoulou, V. , Tryfonas, D. , & Zafeiriou, D. (2015). Brainstem auditory evoked potentials in boys with autism: Still searching for the hidden truth. Iranian Journal of Child Neurology, 9, 21–28.
    1. White, K.R. (2003). The current status of EHDI programs in the United States. Developmental Disabilities Research Reviews, Retrieved from
    1. Wolff, J.J. , Gu, H. , Gerig, G. , Elison, J.T. , Styner, M. , Gouttard, S. … Ibis Network , (2012). Differences in white matter fiber tract development present from 6 to 24 months in infants with autism. The American Journal of Psychiatry, 169, 589–600. doi:
    1. Wong, V. , & Wong, S.N. (1991). Brainstem auditory evoked potential study in children with autistic disorder. Journal of Autism and Developmental Disorders, 21, 329–340.

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