Skip to main content

Advertisement

SpringerLink
Log in

A practical approach toward interpretation of amplitude integrated electroencephalography in preterm infants

  • Review
  • Published:
European Journal of Pediatrics Aims and scope Submit manuscript

Abstract

The developing preterm brain is vulnerable to injury, especially during periods of clinical instability; therefore, monitoring the brain may provide important information on brain health. Over the last 2 decades, a growing body of literature has been reported on preterm amplitude integrated electroencephalography (aEEG) with regards to normative data and associations with adverse outcomes. Despite this, the use of aEEG for preterm infants remains mostly a research tool with limited clinical applicability. In this article, we review the literature on normal and abnormal aEEG patterns in preterm infants and propose a stepwise clinical algorithm for aEEG assessment at the bedside that takes into account assessment of maturation and identification of pathological patterns.

Conclusion: This algorithm may be used by clinicians at the bedside for interpretation to integrate it in clinical practice for neurological surveillance of preterm infants.

What is Known:

• Studies have reported normative data on aEEG in preterm infants for different gestational ages.

• Burst suppression pattern and absent sleep-wake cycling have been described to be associated with brain pathology and adverse outcomes in preterm infants.

What is New:

• We have synthesized aEEG characteristics in preterm infants across the spectrum of prematurity reported in the literature.

• We present a stepwise approach for clinically applicable interpretation of aEEG in preterm infants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

Not applicable.

Code availability

Not applicable.

Abbreviations

aEEG:

Amplitude integrated electroencephalography

AS:

Awake/active sleep

C:

Continuous

DC:

Discontinuous

GA:

Gestational age

HBV:

High base voltage

HIE:

Hypoxic ischemic encephalopathy

IBIs:

Interburst intervals

IVH:

Intraventricular hemorrhage

LBV:

Low base voltage

LMV:

Lower margin voltage

NICU:

Neonatal intensive care unit

PCA:

Post-conceptional age

PHVD:

Post-hemorrhagic ventricular dilatation

QS:

Quiet sleep

SWC:

Sleep-wake cycling

UMV:

Upper margin voltage

References

  1. al Naqeeb N, Edwards AD, Cowan FM, Azzopardi D (1999) Assessment of neonatal encephalopathy by amplitude-integrated electroencephalography. Pediatrics 103:1263–1271

    Article  Google Scholar 

  2. Shellhaas RA, Clancy RR (2007) Characterization of neonatal seizures by conventional EEG and single-channel EEG. Clin Neurophysiol : Official J Int Federation Clin Neurophysiol 118:2156–2161

    Article  Google Scholar 

  3. Toet MC, Hellstrom-Westas L, Groenendaal F, Eken P, de Vries LS (1999) Amplitude integrated EEG 3 and 6 hours after birth in full term neonates with hypoxic-ischaemic encephalopathy. Arch Dis Child Fetal Neonatal Ed 81:F19-23

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. ter Horst HJ, Sommer C, Bergman KA, Fock JM, van Weerden TW, Bos AF (2004) Prognostic significance of amplitude-integrated EEG during the first 72 hours after birth in severely asphyxiated neonates. Pediatr Res 55:1026–1033

    Article  PubMed  Google Scholar 

  5. van Laerhoven H, de Haan TR, Offringa M, Post B, van der Lee JH (2013) Prognostic tests in term neonates with hypoxic-ischemic encephalopathy: a systematic review. Pediatrics 131:88–98

    Article  PubMed  Google Scholar 

  6. Shah NA, Van Meurs KP, Davis AS (2015) Amplitude-integrated electroencephalography: a survey of practices in the United States. Am J Perinatol 32:755–760

    PubMed  Google Scholar 

  7. Grass B, Crosdale B, Keyzers M, Deshpande P, Hahn C, Ly LG, McNamara PJ (2019) Implementation of amplitude-integrated electroencephalography in tertiary Canadian Neonatal Intensive Care Units—a longitudinal study. Paediatr Child Health

  8. Thornberg E, Thiringer K (1990) Normal pattern of the cerebral function monitor trace in term and preterm neonates. Acta Paediatr Scand 79:20–25

    Article  CAS  PubMed  Google Scholar 

  9. Sisman J, Campbell DE, Brion LP (2005) Amplitude-integrated EEG in preterm infants: maturation of background pattern and amplitude voltage with postmenstrual age and gestational age. J Perinatol: Official J California Perinatal Assoc 25:391–396

    Article  Google Scholar 

  10. Olischar M, Klebermass K, Kuhle S, Hulek M, Kohlhauser C, Rucklinger E, Pollak A, Weninger M (2003) Reference values for amplitude-integrated electroencephalographic activity in preterm infants younger than 30 weeks’ gestational age. Pediatrics 113:e61–e66

    Article  Google Scholar 

  11. Burdjalov VF, Baumgart S, Spitzer AR (2003) Cerebral function monitoring: a new scoring system for the evaluation of brain maturation in neonates. Pediatrics 112:855–861

    Article  PubMed  Google Scholar 

  12. Niemarkt HJ, Andriessen P, Peters CH, Pasman JW, Blanco CE, Zimmermann LJ, Bambang Oetomo S (2010) Quantitative analysis of amplitude-integrated electroencephalogram patterns in stable preterm infants, with normal neurological development at one year. Neonatology 97:175–182

    Article  CAS  PubMed  Google Scholar 

  13. Zhang D, Liu Y, Hou X, Zhou C, Luo Y, Ye D, Ding H (2011) Reference values for amplitude-integrated EEGs in infants from preterm to 3.5 months of age. Pediatrics 127:e1280-1287

    Article  PubMed  Google Scholar 

  14. Vesoulis ZA, Paul RA, Mitchell TJ, Wong C, Inder TE, Mathur AM (2015) Normative amplitude-integrated EEG measures in preterm infants. J Perinatol: Official J California Perinatal Assoc 35:428–433

    Article  CAS  Google Scholar 

  15. Kuint J, Turgeman A, Torjman A, Maayan-Metzger A (2007) Characteristics of amplitude-integrated electroencephalogram in premature infants. J Child Neurol 22:277–281

    Article  PubMed  Google Scholar 

  16. Griesmaier E, Enot DP, Bachmann M, Neubauer V, Hellstrom-Westas L, Kiechl-Kohlendorfer U, Keller M (2013) Systematic characterization of amplitude-integrated EEG signals for monitoring the preterm brain. Pediatr Res 73:226–235

    Article  PubMed  Google Scholar 

  17. Klebermass K, Kuhle S, Olischar M, Rucklinger E, Pollak A, Weninger M (2006) Intra- and extrauterine maturation of amplitude-integrated electroencephalographic activity in preterm infants younger than 30 weeks of gestation. Biol Neonate 89:120–125

    Article  PubMed  Google Scholar 

  18. Natalucci G, Rousson V, Bucher HU, Bernet V, Hagmann C, Latal B (2013) Delayed cyclic activity development on early amplitude-integrated EEG in the preterm infant with brain lesions. Neonatology 103:134–140

    Article  PubMed  Google Scholar 

  19. Benavente-Fernandez I, Lubian-Lopez SP, Jimenez-Gomez G, Lechuga-Sancho AM, Garcia-Alloza M (2014) Low-voltage pattern and absence of sleep-wake cycles are associated with severe hemorrhage and death in very preterm infants. Eur J Pediatr

  20. Sohn JA, Kim HS, Lee EH, Lee J, Lee JA, Choi CW, Kim EK, Kim BI, Choi JH (2013) Developmental change of amplitude-integrated electroencephalographic activity in preterm infants with intraventricular hemorrhage. Early Human Dev 89:961–966

    Article  Google Scholar 

  21. Hellstrom-Westas L, Klette H, Thorngren-Jerneck K, Rosen I (2001) Early prediction of outcome with aEEG in preterm infants with large intraventricular hemorrhages. Neuropediatrics 32:319–324

    Article  CAS  PubMed  Google Scholar 

  22. Soubasi V, Mitsakis K, Sarafidis K, Griva M, Nakas CT, Drossou V (2012) Early abnormal amplitude-integrated electroencephalography (aEEG) is associated with adverse short-term outcome in premature infants. Eur J Paediatr Neurol 16:625–630

    Article  PubMed  Google Scholar 

  23. Inder TE, Buckland L, Williams CE, Spencer C, Gunning MI, Darlow BA, Volpe JJ, Gluckman PD (2003) Lowered electroencephalographic spectral edge frequency predicts the presence of cerebral white matter injury in premature infants. Pediatrics 111:27–33

    Article  PubMed  Google Scholar 

  24. Song J, Xu F, Wang L, Gao L, Guo J, Xia L, Zhang Y, Zhou W, Wang X, Zhu C (2015) Early amplitude-integrated electroencephalography predicts brain injury and neurological outcome in very preterm infants. Sci Rep 5:13810

    Article  PubMed  PubMed Central  Google Scholar 

  25. Olischar M, Klebermass K, Kuhle S, Hulek M, Messerschmidt A, Weninger M (2004) Progressive posthemorrhagic hydrocephalus leads to changes of amplitude-integrated EEG activity in preterm infants. Childs Nerv Syst 20:41–45

    Article  CAS  PubMed  Google Scholar 

  26. Olischar M, Klebermass K, Hengl B, Hunt RW, Waldhoer T, Pollak A, Weninger M (2009) Cerebrospinal fluid drainage in posthaemorrhagic ventricular dilatation leads to improvement in amplitude-integrated electroencephalographic activity. Acta Paediatr 98:1002–1009

    Article  PubMed  Google Scholar 

  27. Klebermass-Schrehof K, Rona Z, Waldhor T, Czaba C, Beke A, Weninger M, Olischar M (2013) Can neurophysiological assessment improve timing of intervention in posthaemorrhagic ventricular dilatation? Arch Dis Child Fetal Neonatal Ed 98:F291-297

    Article  PubMed  Google Scholar 

  28. Wikstrom S, Pupp IH, Rosen I, Norman E, Fellman V, Ley D, Hellstrom-Westas L (2012) Early single-channel aEEG/EEG predicts outcome in very preterm infants. Acta Paediatr 101:719–726

    Article  PubMed  PubMed Central  Google Scholar 

  29. Hellstrom-Westas L, Rosen I, Svenningsen NW (1995) Predictive value of early continuous amplitude integrated EEG recordings on outcome after severe birth asphyxia in full term infants. Arch Dis Child Fetal Neonatal Ed 72:F34-38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Middel RG, Brandenbarg N, Van Braeckel K, Bos AF, Ter Horst HJ (2018) The predictive value of amplitude-integrated electroencephalography in preterm infants for IQ and other neuropsychological outcomes at early school age. Neonatology 113:287–295

    Article  PubMed  Google Scholar 

  31. El Ters NM, Vesoulis ZA, Liao SM, Smyser CD, Mathur AM (2018) Term-equivalent functional brain maturational measures predict neurodevelopmental outcomes in premature infants. Early Human Dev 119:68–72

    Article  Google Scholar 

  32. El Ters NM, Vesoulis ZA, Liao SM, Smyser CD, Mathur AM (2017) Impact of brain injury on functional measures of amplitude-integrated EEG at term equivalent age in premature infants. J Perinatol: Official J California Perinatal Assoc 37:947–952

    Article  Google Scholar 

  33. Bruns N, Dransfeld F, Huning B, Hobrecht J, Storbeck T, Weiss C, Felderhoff-Muser U, Muller H (2017) Comparison of two common aEEG classifications for the prediction of neurodevelopmental outcome in preterm infants. Eur J Pediatr 176:163–171

    Article  CAS  PubMed  Google Scholar 

  34. Vesoulis ZA, Inder TE, Woodward LJ, Buse B, Vavasseur C, Mathur AM (2014) Early electrographic seizures, brain injury, and neurodevelopmental risk in the very preterm infant. Pediatr Res 75:564–569

    Article  PubMed  Google Scholar 

  35. Pisani F, Spagnoli C (2018) Acute symptomatic neonatal seizures in preterm neonates: etiologies and treatments. Semin Fetal Neonatal Med 23:191–196

    Article  PubMed  Google Scholar 

  36. Pisani F, Facini C, Pelosi A, Mazzotta S, Spagnoli C, Pavlidis E (2016) Neonatal seizures in preterm newborns: a predictive model for outcome. Eur J Paediatr Neurol 20:243–251

    Article  PubMed  Google Scholar 

  37. Boylan G, Burgoyne L, Moore C, O’Flaherty B, Rennie J (2010) An international survey of EEG use in the neonatal intensive care unit. Acta Paediatr 99:1150–1155

    Article  PubMed  Google Scholar 

  38. Hellstrom-Westas L, Rosen I, de Vries LS, Greisen G (2006) Amplitude-integrated EEG classification and interpretation in preterm and term infants. NeoReviews 7:e76–e87

    Article  Google Scholar 

  39. Andre M, Lamblin MD, d’Allest AM, Curzi-Dascalova L, Moussalli-Salefranque FTSNT, Vecchierini-Blineau MF, Wallois F, Walls-Esquivel E, Plouin P (2010) Electroencephalography in premature and full-term infants. Developmental Features Glossary Neurophysiol Clin 40:59–124

    CAS  PubMed  Google Scholar 

  40. Vanhatalo S, Tallgren P, Andersson S, Sainio K, Voipio J, Kaila K (2002) DC-EEG discloses prominent, very slow activity patterns during sleep in preterm infants. Clin Neurophysiol : Official J Int Federation Clin Neurophysiol 113:1822–1825

    Article  Google Scholar 

  41. Hayakawa M (2001) Background electroencephalographic (EEG) activities of very preterm infants born at less than 27 weeks gestation: a study on the degree of continuity. Arch Dis Child Fetal Neonatal Ed 84:163F – 167

    Article  Google Scholar 

  42. Curzi-Dascalova L, Figueroa JM, Eiselt M, Christova E, Virassamy A, d’Allest AM, Guimaraes H, Gaultier C, Dehan M (1993) Sleep state organization in premature infants of less than 35 weeks’ gestational age. Pediatr Res 34:624–628

    Article  CAS  PubMed  Google Scholar 

  43. Kuhle S, Klebermass K, Olischar M, Hulek M, Prusa AR, Kohlhauser C, Birnbacher R, Weninger M (2001) Sleep-wake cycles in preterm infants below 30 weeks of gestational age. Preliminary results of a prospective amplitude-integrated EEG study. Wien Klin Wochenschr 113:219–223

    CAS  PubMed  Google Scholar 

  44. Olischar M, Klebermass K, Waldhoer T, Pollak A, Weninger M (2007) Background patterns and sleep-wake cycles on amplitude-integrated electroencephalography in preterms younger than 30 weeks gestational age with peri-/intraventricular haemorrhage. Acta Paediatr 96:1743–1750

    Article  PubMed  Google Scholar 

  45. Steriade M, Gloor P, Llinas RR, Lopes de Silva FH, Mesulam MM (1990) Report of IFCN Committee on Basic Mechanisms. Basic mechanisms of cerebral rhythmic activities. Electroencephalogr Clin Neurophysiol 76:481–508

    Article  CAS  PubMed  Google Scholar 

  46. El-Dib M, Massaro AN, Glass P, Aly H (2014) Sleep wake cycling and neurodevelopmental outcome in very low birth weight infants. The journal of maternal-fetal & neonatal medicine : the official journal of the European Association of Perinatal Medicine, the Federation of Asia and Oceania Perinatal Societies, the International Society of Perinatal Obstet 27:892–897

    Article  Google Scholar 

  47. Selton D, Andre M, Hascoet JM (2000) Normal EEG in very premature infants: reference criteria. Clin Neurophysiol : Official J Int Federation Clin Neurophysiol 111:2116–2124

    Article  CAS  Google Scholar 

  48. Li XF, Zhou YX, Zhang L (2016) Newborns’ sleep-wake cycle development on amplitude integrated electroencephalography. World J Pediatr 12:327–334

    Article  PubMed  Google Scholar 

  49. Benavente-Fernandez I, Lubian-Lopez SP, Jimenez-Gomez G, Lechuga-Sancho AM, Garcia-Alloza M (2015) Low-voltage pattern and absence of sleep-wake cycles are associated with severe hemorrhage and death in very preterm infants. Eur J Pediatr 174:85–90

    Article  PubMed  Google Scholar 

  50. Vecchierini MF, Andre M, d’Allest AM (2007) Normal EEG of premature infants born between 24 and 30 weeks gestational age: terminology, definitions and maturation aspects. Neurophysiol Clin 37:311–323

    Article  PubMed  Google Scholar 

  51. Verma UL, Archbald F, Tejani NA, Handwerker SM (1984) Cerebral function monitor in the neonate. I: Normal patterns. Dev Med Child Neurol 26:154–161

    Article  CAS  PubMed  Google Scholar 

  52. Chalak LF, Sikes NC, Mason MJ, Kaiser JR (2011) Low-voltage aEEG as predictor of intracranial hemorrhage in preterm infants. Pediatr Neurol 44:364–369

    Article  PubMed  PubMed Central  Google Scholar 

  53. Bowen JR, Paradisis M, Shah D (2010) Decreased aEEG continuity and baseline variability in the first 48 hours of life associated with poor short-term outcome in neonates born before 29 weeks gestation. Pediatr Res 67:538–544

    Article  PubMed  Google Scholar 

  54. Bruns N, Metze B, Buhrer C, Felderhoff-Muser U, Huseman D (2015) Electrocortical activity at 7 days of life is affected in extremely premature infants with patent ductus arteriosus. Klin Padiatr 227:264–268

    Article  CAS  PubMed  Google Scholar 

  55. Shah D, Paradisis M, Bowen JR (2013) Relationship between systemic blood flow, blood pressure, inotropes, and aEEG in the first 48 h of life in extremely preterm infants. Pediatr Res 74:314–320

    Article  PubMed  Google Scholar 

  56. Klebermass K, Olischar M, Waldhoer T, Fuiko R, Pollak A, Weninger M (2011) Amplitude-integrated EEG pattern predicts further outcome in preterm infants. Pediatr Res 70:102–108

    Article  PubMed  Google Scholar 

  57. Stevenson NJ, Tataranno ML, Kaminska A, Pavlidis E, Clancy RR, Griesmaier E, Roberts JA, Klebermass-Schrehof K, Vanhatalo S (2020) Reliability and accuracy of EEG interpretation for estimating age in preterm infants. Ann Clin Transl Neurol 7:1564–1573

    Article  PubMed  PubMed Central  Google Scholar 

  58. Stevenson NJ, Oberdorfer L, Tataranno ML, Breakspear M, Colditz PB, de Vries LS, Benders M, Klebermass-Schrehof K, Vanhatalo S, Roberts JA (2020) Automated cot-side tracking of functional brain age in preterm infants. Ann Clin Transl Neurol 7:891–902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Olischar M, Klebermass K, Kuhle S, Hulek M, Kohlhauser C, Rucklinger E, Pollak A, Weninger M (2004) Reference values for amplitude-integrated electroencephalographic activity in preterm infants younger than 30 weeks’ gestational age. Pediatrics 113:e61-66

    Article  PubMed  Google Scholar 

Download references

Funding

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Author information

Authors and Affiliations

  1. Department of Paediatrics, Mount Sinai Hospital, 600 University Ave, Toronto, ON, M5G 1X5, Canada

    Poorva Deshpande & Prakesh S. Shah

  2. Hospital for Sick Children, Toronto, Canada

    Patrick J. McNamara, Cecil Hahn & Anne-Marie Guerguerian

  3. Division of Neonatology, University of Toronto, Toronto, Canada

    Poorva Deshpande & Prakesh S. Shah

  4. Division of Neonatology, Departments of Pediatrics and Internal Medicine, Neurosciences and Mental Health Program, University of Iowa, Iowa, USA

    Patrick J. McNamara, Cecil Hahn & Anne-Marie Guerguerian

Authors
  1. Poorva Deshpande
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Patrick J. McNamara
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cecil Hahn
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Prakesh S. Shah
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anne-Marie Guerguerian
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. Deshpande and Guerguerian devised the concept. Deshpande performed the literature search and Guerguerian verified the literature. The first draft of the manuscript was written by Deshpande and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Poorva Deshpande.

Ethics declarations

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Conflict of interest

The authors declare no conflict of interest.

Additional information

Communicated by Daniele De Luca

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Deshpande, P., McNamara, P.J., Hahn, C. et al. A practical approach toward interpretation of amplitude integrated electroencephalography in preterm infants. Eur J Pediatr 181, 2187–2200 (2022). https://doi.org/10.1007/s00431-022-04428-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00431-022-04428-5

Keywords

Search

Navigation