285
Views
0
CrossRef citations to date
0
Altmetric
Review

EEG in neonatal seizures: where to look and what to see

&
Pages 963-979 | Received 25 Jun 2022, Accepted 12 Jan 2023, Published online: 22 Jan 2023

References

  • Hellström-Westas L, Rosén I, Swenningsen NW. Silent seizures in sick infants in early life. Diagnosis by continuous cerebral function monitoring. Acta Paediatr Scand. 1985;74(5):741–748.
  • Boylan GB, Rennie JM, Chorley G, et al. Second-line anticonvulsant treatment of neonatal seizures: a video- EEG monitoring study. Neurology. 2004;62(3):486–488.
  • Rennie J, Boylan G. Treatment of neonatal seizures. Arch Dis Child Fetal Neonatal Ed. 2007;92(2):F148–50.
  • Rennie JM, de Vries LS, Blennow M, et al. Characterisation of neonatal seizures and their treatment using continuous EEG monitoring: a multicentre experience. Arch Dis Child Fetal Neonatal Ed. 2019;104(5):F493–501.
  • Pisani F, Facini C, Bianchi E, et al. Incidence of neonatal seizures, perinatal risk factors for epilepsy and mortality after neonatal seizures in the province of Parma, Italy. Epilepsia. 2018;59(9):1764–1773.
  • Pisani F, Cerminara C, Fusco C, et al. Neonatal status epilepticus vs recurrent neonatal seizures: clinical findings and outcome. Neurology. 2007;69(23):2177–2185.
  • Pisani F, Sisti L, Seri S. A scoring system for early prognostic assessment after neonatal seizures. Pediatrics. 2009;124(4):e580–7.
  • Pisani F, Copioli C, Di Gioia C, et al. Neonatal seizures: relation of ictal video-electroencephalography (EEG) findings with neurodevelopmental outcome. J Child Neurol. 2008;23(4):394–398.
  • Pisani F, Spagnoli C, Falsaperla R, et al. Seizures in the neonate: a review of etiologies and outcomes. Seizure. 2021;85:48–56.
  • Ronen GM, Buckley D, Penney S, et al. Long-term prognosis in children with neonatal seizures: a population-based study. Neurology. 2007;69(19):1816–1822.
  • Tekgul H, Gauvreau K, Soul J, et al. The current etiologic profile and neurodevelopmental outcome of seizures in term newborn infants. Pediatrics. 2006;117:1270–1280.
  • Holmes GL. The long-term effects of neonatal seizures. Clin Perinatol. 2009 Dec;36(4):901–14, vii–viii.
  • Dzhala VI, Kuchibhotla KV, Glykys JC, et al. Progressive NKCC1-dependent neuronal chloride accumulation during neonatal seizures. J Neurosci. 2010;30:11745–11761.
  • Nardou R, Ferrari DC, Ben-Ari Y. Mechanisms and effects of seizures in the immature brain. Semin Fetal Neonatal Med. 2013;18:175–184.
  • Pisani F, Prezioso G, Spagnoli C. Neonatal seizures in preterm infants: a systematic review of mortality risk and neurological outcomes from studies in the 2000’s. Seizure. 2020;75:7–17.
  • Garfinkle J, Shevell MI. Cerebral palsy, developmental delay, and epilepsy after neonatal seizures. Pediatr Neurol. 2011a;44:88–96.
  • Pisani F, Piccolo B, Cantalupo G, et al. Neonatal seizures and postneonatal epilepsy: a 7-y follow-up study. Pediatr Res. 2012;72(2):186–193.
  • Lee BL, Gano D, Rogers EE, et al. Long-term cognitive outcomes in term newborns with watershed injury caused by neonatal encephalopathy. Pediatr Res. 2022;92(2):505–512.
  • Pisani F, Spagnoli C. Outcome in preterm infants with seizures. Handb Clin Neurol. 2019;162:401–414.
  • Pisani F, Fusco C, Spagnoli C. Linking acute symptomatic neonatal seizures, brain injury and outcome in preterm infants. Epilepsy Behav. 2020 Nov;112:107406.
  • Shellhaas RA, Chang T, Tsuchida T, et al. The American clinical neurophysiology society’s guideline on continuous electroencephalography monitoring in neonates. J Clin Neurophysiol. 2011;28(6):611–617.
  • Clancy RR. Prolonged electroencephalogram monitoring for seizures and their treatment. Clin Perinatol. 2006 Sep;33(3):649–665.
  • Boylan GB, Rennie JM, Pressler RM, et al. Phenobarbitone, neonatal seizures, and video-EEG. Arch Dis Child Fetal Neonatal Ed. 2002;86:F165–70.
  • Murray DM, Ryan CA, Boylan GB, et al. Prediction of seizures in asphyxiated neonates: correlation with continuous video-electroencephalographic monitoring. Pediatrics. 2006;118(1):41–46.
  • Bye A, Flanagan D. Electroencephalograms, clinical observations and the monitoring of neonatal seizures. J Paediatr Child Health. 1995;31(6):503–507.
  • Murray DM, Boylan GB, Ali I, et al. Defining the gap between electrographic seizure burden, clinical expression and staff recognition of neonatal seizures. Arch Dis Child Fetal Neonatal Ed. 2008;93(3):F187–91.
  • Janackova S, Boyd S, Yozawitz E, et al. Electroencephalographic characteristics of epileptic seizures in preterm neonates. Clin Neurophysiol. 2016;127:2721–2727.
  • Pavlidis E, Spagnoli C, Pelosi A, et al. Neonatal status epilepticus: differences between preterm and term newborns. Eur J Paediatr Neurol. 2015;19:314–319.
  • Lombroso CT. Neonatal seizures: a clinician’s overview. Brain Dev. 2008;18:1–28.
  • McBride MC, Laroia N, Guillet R. Electrographic seizures in neonates correlate with poor neurodevelopmental outcome. Neurology. 2000;55:506–513.
  • Clancy RR, Legido A, Lewis D. Occult neonatal seizures. Epilepsia. 1988;29:256–261.
  • Goldberg RN, Goldman SL, Ramsay RE, et al. Detection of seizure activity in the paralyzed neonate using continuous monitoring. Pediatrics. 1982;69:583–586.
  • Nash KB, Bonifacio SL, Glass HC, et al. Video-EEG monitoring in newborns with hypoxic-ischemic encephalopathy treated with hypothermia. Neurology. 2011;76(6):556–562.
  • Murray DM, Boylan GB, Ali I, et al. Defining the gap between electrographic seizure burden, clinical expression and staff recognition of neonatal seizures. Arch Dis Child Fetal Neonat Ed. 2008;93:F187–91.
  • Naim MY, Gaynor JW, Chen J, et al. Subclinical seizures identified by postoperative electroencephalographic monitoring are common after neonatal cardiac surgery. J Thorac Cardiovasc Surg. 2015;150(1):169–178.
  • Clancy RR, McGaurn SA, Wernovsky G, et al. Risk of seizures in survivors of newborn heart surgery using deep hypothermic circulatory arrest. Pediatrics. 2003;111:592–601.
  • Helmers SL, Wypij D, Constantinou JE, et al. Perioperative electroencephalographic seizures in infants undergoing repair of complex congenital cardiac defects. Electroencephalogr Clin Neurophysiol. 1997;102:27–36.
  • Scher MS, Alvin J, Gaus L, et al. Uncoupling of EEG-clinical neonatal seizures after antiepileptic drug use. Pediatr Neurol. 2003;28(4):277–280.
  • Mizrahi E, Kellaway P. The response of electroclinical neonatal seizures to antiepileptic drug therapy. Epilepsia. 1992;33(suppl 3):114.
  • Pisani F, Facini C, Pelosi A, et al. Neonatal seizures in preterm newborns: a predictive model for outcome. Eur J Paediatr Neurol. 2016;20(2):243–251.
  • Pisani F, Pavlidis E, Cattani L, et al. Optimizing detection rate and characterization of subtle paroxysmal neonatal abnormal facial movements with multi-camera video-electroencephalogram recordings. Neuropediatrics. 2016;47:169–174.
  • Orivoli S, Facini C, Pisani F. Paroxysmal nonepileptic motor phenomena in newborn. Brain Dev. 2015;37(9):833–839.
  • Facini C, Spagnoli C, Pisani F. Epileptic and non-epileptic paroxysmal motor phenomena in newborns. J Matern Fetal Neonatal Med. 2016;29(22):3652–3659.
  • Malone A, Ryan CA, Fitzgerald A, et al. Interobserver agreement in neonatal seizure identification. Epilepsia. 2009;50:2097–2101.
  • Clancy RR. The contribution of EEG to the understanding of neonatal seizures. Epilepsia. 1996;37(Suppl 1):S52–S59.
  • Nagarajan L, Ghosh S, Palumbo L. Classification of clinical semiology in epileptic seizures in neonates. Eur J Paediatr Neurol. 2012;16:118–125.
  • Volpe JJ. Neonatal seizures: current concepts and revised classification. Pediatrics. 1989;84:422–428.
  • Lombroso CT. Neonatal seizures: historic note and present controversies. Epilepsia. 1996;37(S3):5–13.
  • Mizrahi EM, Kellaway P. Characterization and classification of neonatal seizures. Neurology. 1987;37:1837–1844.
  • Watanabe K, Hara K, Miyazaki S, et al. Electroclinical studies of seizures in the newborn. Folia Psychiatr Neurol Jpn. 1977;31:383–392.
  • Pressler RM, Cilio MR, Mizrahi EM, et al. The ILAE classification of seizures and the epilepsies: modification for seizures in the neonate. Position paper by the ILAE task force on neonatal seizures. Epilepsia. 2021;62(3):615–628.
  • Fisher RS, Cross JH, D’Souza C, et al. Instruction manual for the ILAE 2017 operational classification of seizure types. Epilepsia. 2017;58(4):531–542.
  • Clancy RR, Legido A. The exact ictal and interictal duration of electroencephalographic neonatal seizures. Epilepsia. 1987;28:537–541.
  • Oliveira AJ, Nunes ML, Haertel LM, et al. Duration of rhythmic EEG patterns in neonates: new evidence for clinical and prognostic significance of brief rhythmic discharges. Clin Neurophysiol. 2000;111(9):1646–1653.
  • Nagarajan L, Ghosh S, Palumbo L. Ictal electroencephalogram in neonatal seizures: characteristics and associations. Pediatr Neurol. 2011;45:11–16.
  • Alix JJ, Ponnusamy A, Hart AR. Brief rhythmic discharges in neonates: a marker for seizures. Epileptic Disord. 2015;17(3):349.
  • Pisani F, Spagnoli C, Fusco C. EEG Monitoring of the Epileptic Newborn. Curr Neurol Neurosci Rep. 2020;20(4):6.
  • Pisani F, Percesepe A, Spagnoli C. Genetic diagnosis in neonatal-onset epilepsies: back to the future. Eur J Paediatr Neurol. 2018;22(3):354–357.
  • Cornet MC, Sands TT, Cilio MR. Neonatal epilepsies: clinical management. Semin fetal neonatal med. 2018;23(3):204–212.
  • Zuberi SM, Wirrell E, Yozawitz E, et al. ILAE classification and definition of epilepsy syndromes with onset in neonates and infants: position statement by the ILAE task force on nosology and definitions. Epilepsia. 2022;63(6):1349–1397.
  • Grieve PG, Emerson RG, Fifer WP, et al. Spatial correlation of the infant and adult electroencephalogram. Clin Neurophysiol. 2003;114(9):1594–1608.
  • Fifer WP, Grieve PG, Grose-Fifer J, et al. High-density electroencephalogram monitoring in the neonate. Clin Perinatol. 2006;33(3):679–691.
  • Vanhatalo S. Neonatal seizures in the EEG: to see or not to see? Clin Neurophysiol. 2007;118(10):2125–2127.
  • Patrizi S, Holmes GL, Orzalesi M, et al. Neonatal seizures: characteristics of EEG ictal activity in preterm and fullterm infants. Brain Dev. 2003;25:427–437.
  • Shelhaas RA, Clancy RR. Characterization of neonatal seizures by conventional EEG and single-channel EEG. Clin Neurophysiol. 2007;118(10):2156–2161.
  • Pisani F, Barilli AL, Sisti L, et al. Preterm infants with video-EEG confirmed seizures: outcome at 30 months of age. Brain Dev. 2008;30(1):20–30.
  • Boylan GB, Kharoshankaya L, Mathieson SR. Diagnosis of seizures and encephalopathy using conventional EEG and amplitude integrated EEG. Handb Clin Neurol. 2019;162:363–400.
  • Okumura A, Hayakawa F, Kato T, et al. Ictal electroencephalographic findings of neonatal seizures in preterm infants. Brain Dev. 2008;30(4):261–268.
  • Stockard-Pope JE, Werner SS, Bickford RG. Atlas of neonatal electroencephalography. 2nd ed. New York NY: Raven Press; 1992.
  • Tsuchida TN, Wusthoff CJ, Shellhaas RA, et al. American clinical neurophysiology society critical care monitoring committee. American clinical neurophysiology society standardized EEG terminology and categorization for the description of continuous EEG monitoring in neonates: report of the American clinical neurophysiology society critical care monitoring committee. J Clin Neurophysiol. 2013;30(2):161–173.
  • Wusthoff CJ. Diagnosing neonatal seizures and status epilepticus. J Clin Neurophysiol. 2013;30(2):115–121.
  • Watanabe K. Neurophysiological aspects of neonatal seizures. Brain Dev. 2014;36(5):363–371.
  • Dreyfus-Brisac C, Monod N. Electroclinical studies of status epilepticus and convulsions in the newborn. In: Kellaway P, Petersen I, editors. Neurological and electroencephalographic correlative studies in infancy. New York NY: Grune and Stratton; 1964. p. 250–272.
  • Dreyfus-Brisac C, Monod N. Neonatal status epilepticus. In: Rémond A, editor. Handbook of electroencephalography and clinical neurophysiology. 1972. Vol. 15. Amsterdam: Elsevier. p. 38–52.
  • Bazhenov M, Timofeev I, Fröhlich F, et al. Cellular and network mechanisms of electrographic seizures. Drug Discov Today Dis Models. 2008;5(1):45–57.
  • Krishnan GP, Bazhenov M. Ionic dynamics mediate spontaneous termination of seizures and postictal depression state. J Neurosci. 2011;31(24):8870–8882.
  • Kitayama M, Otsubo H, Parvez S, et al. Wavelet analysis for neonatal electroencephalographic seizures. Pediatr Neurol. 2003;29(4):326–333.
  • Scher MS, Sun M, Steppe DA, et al. Comparisons of EEG spectral and correlation measures between healthy term and preterm infants. Pediatr Neurol. 1994;10(2):104–108.
  • Aziz SS, Wallace SJ, Murphy JF, et al. Cotside EEG monitoring using computerised spectral analysis. Arch Dis Child. 1986;61(3):242–246.
  • Mathieson SR, Livingstone V, Low E, et al. Phenobarbital reduces EEG amplitude and propagation of neonatal seizures but does not alter performance of automated seizure detection. Clin Neurophysiol. 2016;127(10):3343–3350.
  • Lloyd RO, O’Toole JM, Pavlidis E, et al. Electrographic seizures during the early postnatal period in preterm infants. J Pediatr. 2017;187:18–25.e2.
  • Radvanyi-Bouvet MF, Vallecalle MH, Morel-Kahn F, et al. Seizures and electrical discharges in premature infants. Neuropediatrics. 1985;16(3):143–148.
  • Low E, Boylan GB, Mathieson SR, et al. Cooling and seizure burden in term neonates: an observational study. Archs Dis Child Fetal Neonat Ed. 2012;97:F267e72.
  • Bennet L, Dean JM, Wassink G, et al. Differential effects of hypothermia on early and late epileptiform events after severe hypoxia in preterm fetal sheep. J Neurophysiol. 2007;97(1):572–578.
  • Lynch NE, Stevenson NJ, Livingstone V, et al. The temporal evolution of electrographic seizure burden in neonatal hypoxic ischemic encephalopathy. Epilepsia. 2012 Mar;53(3):549–557.
  • Nunes ML, Yozawitz EG, Zuberi S, et al. Task force on neonatal seizures, ILAE commission on classification & terminology. neonatal seizures: is there a relationship between ictal electroclinical features and etiology? A critical appraisal based on a systematic literature review. Epilepsia Open. 2019;4(1):10–29.
  • Santarone ME, Pietrafusa N, Fusco L. Neonatal seizures: when semiology points to etiology. Seizure. 2020;80:161–165.
  • Low E, Mathieson SR, Stevenson NJ, et al. Early postnatal EEG features of perinatal arterial ischaemic stroke with seizures. PLoS One. 2014 Jul 22;9(7):e100973.
  • Lynch NE, Stevenson NJ, Livingstone V, et al. The temporal characteristics of seizures in neonatal hypoxic ischemic encephalopathy treated with hypothermia. Seizure. 2015;33:60–65.
  • Aso K, Scher MS, Barmada MA. Neonatal electroencephalography and neuropathology. J Clin Neurophysiol. 1989 Apr;6(2):103–123.
  • Legido A, Clancy RR, Berman PH. Neurologic outcome after electroencephalographically proven neonatal seizures. Pediatrics. 1991;88:583–596.
  • 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(3):183–196.
  • Watanabe K, Hayakawa F, Neonatal OA. EEG: a powerful tool in the assessment of brain damage in preterm infants. Brain Dev. 1999 Sep;21(6):361–372.
  • Doménech-Martínez E, Castro-Conde JR, Herraiz-Culebras T, et al. Neonatal convulsions: influence of the electroencephalographic pattern and the response to treatment on the outcome. Rev Neurol. 2003;37(5):413–420.
  • Bye AM, Cunningham CA, Chee KY, et al. Outcome of neonates with electrographically identified seizures, or at risk of seizures. Pediatr Neurol. 1997;16(3):225–231.
  • Pisani F, Spagnoli C. Determining outcome from neonatal seizures.. In: Moshé SL, Cross JH, de Bellescize J, et al., editors. Seizure and syndromes of onset in the two first years of life. John Libbey Eurotext. Paris; 2015. p. 123–138.
  • Lamblin MD, André M. Électroencéphalogramme du nouveau-né à terme. Aspects normaux et encéphalopathie hypoxo-ischémique [Electroencephalogram of the full-term newborn. Normal features and hypoxic-ischemic encephalopathy]. Neurophysiol Clin. 2011;41(1):1–18.
  • Malfilâtre G, Mony L, Hasaerts D, et al. Technical recommendations and interpretation guidelines for electroencephalography for premature and full-term newborns. Neurophysiol Clin. 2021;51(1):35–60.
  • Pitkänen A, Ekolle Ndode-Ekane X, Lapinlampi N, et al. Epilepsy biomarkers - Toward etiology and pathology specificity. Neurobiol Dis. 2019;123:42–58.
  • Costa A-M, Lo Barco T, Spezia E, et al. Prospective evaluation of ghrelin and des-acyl ghrelin plasma levels in children with newly diagnosed epilepsy: evidence for reduced ghrelin-to-des-acyl ghrelin ratio in generalized epilepsies. J Pers Med. 2022;12(4):527.
  • Milikovsky DZ, Weissberg I, Kamintsky L, et al. Electrocorticographic dynamics as a novel biomarker in five models of epileptogenesis. J Neurosci. 2017;37(17):4450–4461.
  • Costa AM, Lucchi C, Malkoç A, et al. Relationship between delta rhythm, seizure occurrence and allopregnanolone hippocampal levels in epileptic rats exposed to the rebound effect. Pharmaceuticals (Basel). 2021;14(2):127.
  • Noorlag L, van ‘t Klooster MA, van Huffelen AC, et al. High-frequency oscillations recorded with surface EEG in neonates with seizures. Clin Neurophysiol. 2021;132(7):1452–1461.
  • Major P, Lortie A, Dehaes M, et al. Periictal activity in cooled asphyxiated neonates with seizures. Seizure. 2017;47:13–16.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.