Am J Perinatol 2023; 40(08): 833-838
DOI: 10.1055/s-0041-1736593
Review Article

Mild Hypoxic–Ischemic Encephalopathy: Can Neurophysiological Monitoring Predict Unfavorable Neurological Outcome? A Systematic Review and Meta-analysis

Raffaele Falsaperla
1   Division of Pediatrics and Pediatric Emergency, University Hospital Policlinico “Rodolico-San Marco,” Catania, Italy
2   Division of Neonatal Intensive Care and Neonatology, University Hospital Policlinico “Rodolico-San Marco,” Catania, Italy
,
3   Division of Pediatrics and Child Neuropsychiatry, Department of Clinical and Experimental Medicine, Pediatrics Postgraduate Residency Program, University of Catania, Catania, Italy
,
Daniela Gioè
4   Division of Pediatrics, Hospital of Lentini, Lentini, Italy
,
Laura Sciuto
3   Division of Pediatrics and Child Neuropsychiatry, Department of Clinical and Experimental Medicine, Pediatrics Postgraduate Residency Program, University of Catania, Catania, Italy
,
Francesco Pisani
5   Division of Pediatrics, University Hospital of Children “Pietro Barilla,” Parma, Italy
,
Piero Pavone
6   Division of Rare Diseases of the Nervous System in Childhood, Department of Clinical and Experimental Medicine, Section of Pediatrics and Child Neuropsychiatry, University of Catania, Catania, Italy
,
Martino Ruggieri
6   Division of Rare Diseases of the Nervous System in Childhood, Department of Clinical and Experimental Medicine, Section of Pediatrics and Child Neuropsychiatry, University of Catania, Catania, Italy
› Author Affiliations

Abstract

Objective Hypoxic–ischemic encephalopathy (HIE) is the second cause of neonatal deaths and one of the main conditions responsible for long-term neurological disability. Contrary to past belief, children with mild HIE can also experience long-term neurological sequelae. The aim of this systematic review is to determine the predictive value of long-term neurological outcome of (electroencephalogram) EEG/amplitude-integrated electroencephalogram (aEEG) in children who complained mild HIE.

Study Design From a first search on PubMed, Google Scholar, and clinicalTrials.gov databases, only five articles were considered suitable for this study review. A statistical meta-analysis with the evaluation of odds ratio was performed on three of these studies.

Results No correlation was found between the characteristics of the electrical activity of the brain obtained through EEG/aEEG in infants with mild HIE and subsequent neurological involvement.

Conclusion EEG/aEEG monitoring in infants with mild HIE cannot be considered a useful tool in predicting their neurodevelopmental outcome, and its use for this purpose is reported as barely reliable.

Key Points

  • HIE is responsible for long-term neurological outcome, even in newborns with mild HIE.

  • No correlation was found between EEG/aEEG trace in infants with mild HIE and neurological sequelae.

  • Neurophysiological monitoring, in mild HIE, cannot predic neurodevelopmental outcome.

Financial Support and Sponsorship

None.




Publication History

Received: 11 April 2021

Accepted: 23 September 2021

Article published online:
19 October 2021

© 2021. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 
  • References

  • 1 WHO, Maternal and Child Epidemiology Estimation Group. Child causes of death 2000–2017. 2018. https://www.who.int/ healthinfo/global_burden_disease/estimates/en/index2.htmMCEE-WHO methods and data sources for child causes of death 2000-2017. Accessed December 20, 2018 at: https://www.who.int/healthinfo/global_burden_disease/childcod_methods_2000_2017.pdf
  • 2 Chalak L, Latremouille S, Mir I, Sánchez PJ, Sant'Anna G. A review of the conundrum of mild hypoxic-ischemic encephalopathy: Current challenges and moving forward. Early Hum Dev 2018; 120: 88-94
  • 3 Sarnat HB, Sarnat MS. Neonatal encephalopathy following fetal distress. A clinical and electroencephalographic study. Arch Neurol 1976; 33 (10) 696-705
  • 4 Conway JM, Walsh BH, Boylan GB, Murray DM. Mild hypoxic ischaemic encephalopathy and long term neurodevelopmental outcome - A systematic review. Early Hum Dev 2018; 120: 80-87
  • 5 Zanelli SA, Stanley DP. Hypoxic-ischemic encephalopathy. Accessed October 6, 2021 at: https://emedicine.medscape.com/article/973501-overview#a7
  • 6 Ahearne CE, Boylan GB, Murray DM. Short and long term prognosis in perinatal asphyxia: An update. World J Clin Pediatr 2016; 5 (01) 67-74
  • 7 Azzopardi D, Strohm B, Marlow N. et al; TOBY Study Group. Effects of hypothermia for perinatal asphyxia on childhood outcomes. N Engl J Med 2014; 371 (02) 140-149
  • 8 Jacobs SE, Berg M, Hunt R, Tarnow-Mordi WO, Inder TE, Davis PG. Cooling for newborns with hypoxic ischaemic encephalopathy. Cochrane Database Syst Rev 2013; 1 (01) CD003311
  • 9 Murray DM, O'Connor CM, Ryan CA, Korotchikova I, Boylan GB. Early EEG grade and outcome at 5 years after mild neonatal hypoxic ischemic encephalopathy. Pediatrics 2016; 138 (04) e20160659
  • 10 van Kooij BJ, van Handel M, Nievelstein RA, Groenendaal F, Jongmans MJ, de Vries LS. Serial MRI and neurodevelopmental outcome in 9- to 10-year-old children with neonatal encephalopathy. J Pediatr 2010; 157 (02) 221-227.e2
  • 11 Finder M, Boylan GB, Twomey D, Ahearne C, Murray DM, Hallberg B. Two-year neurodevelopmental outcomes after mild hypoxic ischemic encephalopathy in the era of therapeutic hypothermia. JAMA Pediatr 2020; 174 (01) 48-55
  • 12 Robertson CM, Finer NN. Long-term follow-up of term neonates with perinatal asphyxia. Clin Perinatol 1993; 20 (02) 483-500
  • 13 van Handel M, de Sonneville L, de Vries LS, Jongmans MJ, Swaab H. Specific memory impairment following neonatal encephalopathy in term-born children. Dev Neuropsychol 2012; 37 (01) 30-50
  • 14 Prempunpong C, Chalak LF, Garfinkle J. et al. Prospective research on infants with mild encephalopathy: the PRIME study. J Perinatol 2018; 38 (01) 80-85
  • 15 DuPont TL, Chalak LF, Morriss MC, Burchfield PJ, Christie L, Sánchez PJ. Short-term outcomes of newborns with perinatal acidemia who are not eligible for systemic hypothermia therapy. J Pediatr 2013; 162 (01) 35-41
  • 16 Walsh MC, Bell EF, Kandefer S. et al. Neonatal outcomes of moderately preterm infants compared to extremely preterm infants. Pediatr Res 2017; 82 (02) 297-304
  • 17 Massaro AN, Murthy K, Zaniletti I. et al. Short-term outcomes after perinatal hypoxic ischemic encephalopathy: a report from the Children's Hospitals Neonatal Consortium HIE focus group. J Perinatol 2015; 35 (04) 290-296
  • 18 Patel J, Edwards AD. Prediction of outcome after perinatal asphyxia. Curr Opin Pediatr 1997; 9 (02) 128-132
  • 19 Cawley P, Chakkarapani E. Fifteen-minute consultation: therapeutic hypothermia for infants with hypoxic ischaemic encephalopathy-translating jargon, prognosis and uncertainty for parents. Arch Dis Child Educ Pract Ed 2020; 105 (02) 75-83
  • 20 Toet MC, Hellström-Westas L, Groenendaal F, Eken P, de Vries LS. Amplitude integrated EEG 3 and 6 hours after birth in full term neonates with hypoxic-ischaemic encephalopathy. Arch Dis Child Fetal Neonatal Ed 1999; 81 (01) F19-F23
  • 21 Awal MA, Lai MM, Azemi G, Boashash B, Colditz PB. EEG background features that predict outcome in term neonates with hypoxic ischaemic encephalopathy: A structured review. Clin Neurophysiol 2016; 127 (01) 285-296
  • 22 Hellström-Westas L, Rosén I. Continuous brain-function monitoring: state of the art in clinical practice. Semin Fetal Neonatal Med 2006; 11 (06) 503-511
  • 23 Holmes GL, Rowe J, Hafford J. Significance of reactive burst suppression following asphyxia in full term infants. Clin Electroencephalogr 1983; 14 (03) 138-141
  • 24 Moher D, Liberati A, Tetzlaff J. et al. Linee guida per il reporting di revisioni sistematiche e meta-analisi: PRISMA Statement. Evidence 2015; 7 (06) e1000114
  • 25 Ballot DE, Ramdin T, Rakotsoane D. et al. Use of the Bayley Scales of Infant and Toddler Development, Third Edition, to assess developmental outcome in infants and young children in an urban setting in South Africa. Int Sch Res Notices 2017; 2017: 1631760
  • 26 Roid GH, Miller LJ. Leiter International Performance Scale-Revised. Wood Dale, Illinois: Stoelting Co.; 1997
  • 27 Griffiths R. The Abilities of Babies. London, United Kingdom: University of London Press; 1954
  • 28 World Health Organization. International classification of impairments, disabilities and handicaps. A manual of classification relating to the consequences of disease. Accessed October 6, 2021 at: https://apps.who.int/iris/bitstream/handle/10665/41003/9241541261_eng.pdf?sequence=1&isAllowed=y
  • 29 Warschausky S. Wechsler preschool and primary scale of intelligence. In: Kreutzer JS, DeLuca J, Caplan B. eds. Encyclopedia of Clinical Neuropsychology. New York, NY: Springer; 2011
  • 30 Hellstrom-Westas L, Rosén I, de Vries LS, Greisen G. Amplitude-integrated EEG classification and interpretation in preterm and term infants. Neoreviews 2006; 7 (02) e76-e87
  • 31 Lombroso CT. Neonatal polygraphy in full-term and premature infants: a review of normal and abnormal findings. J Clin Neurophysiol 1985; 2 (02) 105-155
  • 32 Rowe JC, Holmes GL, Hafford J. et al. Prognostic value of the electroencephalogram in term and preterm infants following neonatal seizures. Electroencephalogr Clin Neurophysiol 1985; 60 (03) 183-196
  • 33 Watanabe K, Miyazaki S, Hara K, Hakamada S. Behavioral state cycles, background EEGs and prognosis of newborns with perinatal hypoxia. Electroencephalogr Clin Neurophysiol 1980; 49 (5,6): 618-625
  • 34 Shany E, Goldstein E, Khvatskin S. et al. Predictive value of amplitude-integrated electroencephalography pattern and voltage in asphyxiated term infants. Pediatr Neurol 2006; 35 (05) 335-342
  • 35 Murray DM, Boylan GB, Ryan CA, Connolly S. Early EEG findings in hypoxic-ischemic encephalopathy predict outcomes at 2 years. Pediatrics 2009; 124 (03) e459-e467
  • 36 Biagioni E, Mercuri E, Rutherford M. et al. Combined use of electroencephalogram and magnetic resonance imaging in full-term neonates with acute encephalopathy. Pediatrics 2001; 107 (03) 461-468
  • 37 Van Lieshout HB, Jacobs JW, Rotteveel JJ, Geven W, Hof Mv't. The prognostic value of the EEG in asphyxiated newborns. Acta Neurol Scand 1995; 91 (03) 203-207