Electroencephalogram in premature infants: from normal to pathological activity
https://doi.org/10.17650/2073-8803-2019-14-1-26-35
Abstract
This study was aimed to assess electrophysiological brain activity in newborns of various gestational ages using electroencephalography (EEG). We summarized the data on the main EEG characteristics of premature infants and their dynamics and described the most common pathological EEG changes that can be identified at this age. We also discussed prognostic value of various neonatal EEG patterns (including their proportion and location), which allow verification of functional brain disorders at early stages.
About the Authors
D. A. ChegodaevRussian Federation
19 Mira St., Yekaterinburg 620002
N. V. Pavlova
Russian Federation
19 Mira St., Yekaterinburg 620002
O. A. Lvova
Russian Federation
19 Mira St., Yekaterinburg 620002; 3 Repina St., Yekaterinburg 620028
L. V. Shalkevich
Belarus
3/3 P. Brovki St., Minsk 220013, Republic of Belarus; 19 Mira St., Yekaterinburg 620002, Russia
References
1. Abalova V.V., Zavadenko A.N., Grebennikova O.V. et al. Amplitude-integrated electroencephalography for the assessment of the central nervous system in newborns of various gestational ages. Guidelines. Voprosy prakticheskoy pediatrii = Clinical Practice in Pediatrics 2013;8(2):41–53. (In Russ.).
2. Krivtsova L.A., Belskiy V.V. Significance of electroencephalography in the diagnosis and predicting outcomes in full-term newborns with hypoxic ischemic brain lesions. Belleten sibirskoy meditsiny = Bulletin of Siberian Medicine 2011;10(2):127–33. (In Russ.).
3. Shalkevich L.V., Tyrsin A.N., Ostroushko D.V., Shalkevich O.V. Mathematical model for the diagnosis of perinatal lesions of the central nervous system in neonates. Rossiyskiy vestnik perinatologii i pediatrii = Russian Bulletin of Perinatology and Pediatrics 2017;62(3):85–91. (In Russ.). DOI: 10.21508/10274065-2017-62-3-85-91.
4. Agut T., Leоn M., Rebollo M. et al. Early identification of brain injury in infants with hypoxic ischemic encephalopathy at high risk for severe impairments: accuracy of MRI performed in the first days of life. BMC Pediatr 2014;14:177. DOI: 10.1186/1471-2431-14-177. PMID: 25005267.
5. Andre M., Lamblin M.D., d’Allest A.M. et al. Electroencephalography in premature and full-term infants. Developmental features and glossary. Neurophysiol Clin 2010;40(2):59–124. DOI: 10.1016/j.neucli.2010.02.002. PMID: 20510792.
6. Baud О., d’Allest A.M., Lacaze-Masmonteil T. et al. Positive rolandic sharp waves are early electro-encephalographic markers of periventricular leukomalacia. Pediatric Research 1997;41:139. DOI: 10.1203/00006450-199704001-00840.
7. Biagioni E., Frisone M.F., Laroche S. et al. Occipital sawtooth: a physiological EEG pattern in very premature infants. Clin Neurophysiol 2000;111(12):2145–49. DOI: 10.1016/s1388-2457(00)00479-x. PMID: 11090764.
8. Castro Conde J.R., Martinez E.D., Campo C.G. et al. Positive temporal sharp waves in preterm infants with and without brain ultrasound lesions. Clin Neurophysiol 2004;115(11):2479–88. DOI: 10.1016/j.clinph.2004.05.028. PMID: 15465435.
9. Cherian P.J., Swarte R.M., Visser G.H. Technical standards for recording and interpretation of neonatal electroencephalogram in clinical practice. Ann Indian Acad Neurol 2009;12(1):58–70. DOI: 10.4103/0972-2327.33224. PMID: 20151016.
10. Ching S., Purdon P.L., Vijayan S. et al. A neurophysiological-metabolic model for burst suppression. Proc Natl Acad Sci USA 2012;109(8):3095–100. DOI: 10.1073/pnas.1121461109. PMID: 22323592.
11. Chipaux M., Colonnese M.T., Mauguen A. et al. Auditory stimuli mimicking ambient sounds drive temporal “delta-brushes” in premature infants. PLoS One 2013;8(11):e79028. DOI: 10.1371/journal.pone.0079028. PMID: 24244408.
12. Conde J.R., de Hoyos A.L., Martínez E.D. et al. Extrauterine life duration and ontogenic EEG parameters in preterm newborns with and without major ultrasound brain lesions. Clin Neurophysiol 2005;116(12):2796–809. DOI: 10.1016/j.clinph.2005.08.020. PMID: 16253552.
13. Crippa A.C., Silvado C.E., de Paola L. et al. Analysis of frontal sharp transients in 32 neonatal polysomnography in healthy fullterm newborns. Arq Neuropsiquiatr 2007;65(2A):222–7. DOI: 10.1590/s0004-282x2007000200007. PMID: 17607418.
14. Douglass L.M., Wu J.Y., Rosman N.P. et al. Burst suppression electroencephalogram pattern in the newborn: predicting the outcome. J Child Neurol 2002;17(6):403–8. DOI: 10.1177/088307380201700601. PMID: 12174958.
15. Hanganu I.L., Ben-Ari Y., Khazipov R. Retinal waves trigger spindle bursts in the neonatal rat visual cortex. J Neurosci 2006;26(25):6728–36. DOI: 10.1523/jneurosci.0752-06.2006. PMID: 16793880.
16. Hayakawa M., Okumura A., Hayakawa F. et al. 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 2001;84(3):F163–7. DOI: 10.1136/fn.84.3.f163. PMID: 11320041.
17. Holmes G.L., Lombroso C.T. Prognostic value of background patterns in the neonatal EEG. J Clin Neurophysiol 1993;10(3): 323–52. DOI: 10.1097/00004691199307000-00008. PMID: 8408599.
18. Hughes J.R., Miller J.K., Fino J.J. et al. The sharp theta rhythm on the occipital areas of prematures (STOP): a newly described waveform. Clin Electroencephalogr 1990;21(2):77–87. DOI: 10.1177/155005949002100207. PMID: 2335042.
19. Husain A.M. Review of neonatal EEG. Am J Electroneurodiagnostic Technol 2005;45(1):12–35. PMID: 15832672.
20. Khazipov R., Luhmann H.J. Early patterns of electrical activity in the developing cerebral cortex of humans and rodents. Trends Neurosci 2006;29(7):414–8. DOI: 10.1016/j.tins.2006.05.007. PMID: 16713634.
21. Kheder A., Bianchi M.T., Westover M.B. Burst suppression in sleep in a routine outpatient EEG. Epilepsy Behav Case Rep 2014;2:71–4. DOI: 10.1016/j.ebcr.2014.01.003. PMID: 25667874.
22. Klebermass K., Olischar M., Waldhoer T. et al. Amplitude-integrated EEG pattern predicts further outcome in preterm infants. Pediatr Res 2011;70(1):102–8. DOI: 10.1203/pdr.0b013e31821ba200. PMID: 21436758.
23. Lombroso C.T. Neonatal polygraphy in full-term and premature infants: a review of normal and abnormal findings. J Clin Neurophysiol 1985;2(2):105–55. DOI: 10.1097/00004691-19850400000002. PMID: 3916839.
24. Milh M., Kaminska A., Huon C. et al. Rapid cortical oscillations and early motor activity in premature human neonate. Cereb Cortex 2007;17(7):1582–94. DOI: 10.1093/ cercor/bhl069. PMID: 16950867.
25. Murray D.M., Boylan G.B., Ryan C.A. et al. Early EEG findings in hypoxic-ischemic encephalopathy predict outcomes at 2 years. Pediatrics 2009;124(3):e459–67. DOI: 10.1542/peds.2008-2190. PMID: 19706569.
26. Myers M.M., Fifer W.P., Grose-Fifer J. et al. A novel quantitative measure of Tracé-alternant EEG activity and its association with sleep states of preterm infants. Dev Psychobiol 1997;31(3):167–74. DOI: 10.1002/(sici)10982302(199711)31:3<167::aiddev1>3.0.co;2-q. PMID: 9386918.
27. Nosralla Mde O., Silva D.F., Botelho R.V. Significance of background activity and positive sharp waves in neonatal electroencephalogram as prognostic of cerebral palsy. Arq Neuropsiquiatr 2009;67(3A):609–15. DOI: 10.1590/s0004-282x2009000400007. PMID: 19722036.
28. Novotny E.J., Tharp B.R., Coen R.W. et al. Positive rolandic sharp waves in the EEG of the premature infant. Neurology 1987;37(9):1481–6. DOI: 10.1212/wnl.37.9.1481. PMID: 3306454.
29. Nunes M.L., Gameleira F.T., Oliveira A.J. et al. Developmental characteristics of temporal sharp transients in the EEG of normal preterm and term newborns. Arq Neuropsiquiatr 2003;61(3A):574–9. DOI: 10.1590/s0004-282x2003000400009. PMID: 14513160.
30. Ohtsuka Y., Ohno S., Oka E. Electroclinical characteristics of hemimegalencephaly. Pediatr Neurol 1999;20(5):390–3. DOI: 10.1016/s0887-8994(98)00165-9. PMID: 10371388.
31. Okumura A., Hayakawa F., Kato T. et al. Developmental outcome and types of chronic-stage EEG abnormalities in preterm infants. Dev Med Child Neurol 2002;44(11):729–34. DOI: 10.1111/j.1469-8749.2002.tb00278.x. PMID: 12418612.
32. Okumura A., Hayakawa F., Kato T. et al. Positive rolandic sharp waves in preterm infants with periventricular leukomalacia: their relation to background electroencephalographic abnormalities. Neuropediatrics 1999;30(6):278–82. DOI: 10.1055/s-2007-973505. PMID: 10706020.
33. Pezzani C., Radvanyi-Bouvet M.F., Relier J.P. et al. Neonatal electroencephalography during the first twenty-four hours of life in full-term newborn infants. Neuropediatrics 1986;17(1):11–8. DOI: 10.1055/s-2008-1052492. PMID: 3960278.
34. Scher M.S. Ontogeny of EEG-sleep from neonatal through infancy periods. Sleep Med 2008;9(6):615–36. DOI: 10.1002/0471751723.ch63. PMID: 18024172.
35. Scher M.S., Painter M.J., Bergman I. et al. EEG diagnoses of neonatal seizures: clinical correlations and outcome. Pediatr Neurol 1989;5(1):17–24. DOI: 10.1016/0887-8994(89)90004-0. PMID: 2712934.
36. Selton D., Andre M. Prognosis of hypoxic-ischaemic encephalopathy in full-term newborns value of neonatal electroencephalography. Neuropediatrics 1997;28(5):276–80. DOI: 10.1055/s-2007-973714. PMID: 9413008.
37. Teplan M. Fundamentals of EEG measurement. Measurement Science Review 2002;2:1–11.
38. Tich S.N., d’Allest A.M., Villepin A.T. et al. Pathological features of neonatal EEG in preterm babies born before 30 weeks of gestational age. Neurophysiol Clin 2007; 37(5):325–70. DOI: 10.1016/j.neucli.2007.10.001. PMID: 18063234.
39. Torres F., Anderson C. The normal EEG of the human newborn. J Clin Neurophysiol 1985;2(2):89–103. DOI: 10.1097/00004691-19850400000001. PMID: 3916842.
40. Tsuchida T.N., Wusthoff C.J., Shellhaas R.A. et al. 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):161–73. DOI: 10.1097/wnp.0b013e3182872b24. PMID: 23545767.
41. Turnbull J.P., Loparo K.A., Johnson M.W. et al. Automated detection of tracé alternant during sleep in healthy full-term neonates using discrete wavelet transform. Clin Neurophysiol 2001;112(10):1893–900. DOI: 10.1016/s1388-2457(01)00641-1. PMID: 11595149.
42. Urrego J.A., Greene S.A., Rojas M.J. Brain burst suppression activity. Psychol Neurosci 2014;7(4):531–43. DOI: 10.3922/j.psns.2014.4.12.
43. Van Lieshout H.B., Jacobs J.W., Rotteveel J.J. et al. The prognostic value of the EEG in asphyxiated newborns. Acta Neurol Scand 1995;91(3):203–7. DOI: 10.1111/j.1600-0404.1995.tb00435.x. PMID: 7793237.
44. Vanhatalo S., Kaila K. Development of neonatal EEG activity: from phenomenology to physiology. Semin Fetal Neonatal Med 2006;11(6):471–18. DOI: 10.1016/j.siny.2006.07.008. PMID: 17018268.
45. Vanhatalo S., Palva J.M., Andersson S. et al. Slow endogenous activity transients and developmental expression of K+-Cl–cotransporter 2 in the immature human cortex. Eur J Neurosci 2005;22(11):2799–804. DOI: 10.1111/j.1460-9568.2005.04459.x. PMID: 16324114.
46. Vecchierini M.F., Andre M., d’Allest A.M. Normal EEG of premature infants born between 24 and 30 weeks gestational age: terminology, definitions and maturation aspects. Neurophysiol Clin 2007;37(5):311–23. DOI: 10.1016/j.neucli.2007.10.008. PMID: 18063233.
47. Vecchierini M.F., d’Allest A.M., Verpillat P. EEG patterns in 10 extreme premature neonates with normal neurological outcome: qualitative and quantitative data. Brain Dev 2003;25(5):330–7. DOI: 10.1016/s0387-7604(03)00007-x. PMID: 12850512.
48. Vermeulen R.J., Sie L.T., Jonkman E.J. et al. Predictive value of EEG in neonates with periventricular leukomalacia. Dev Med Child Neurol 2003;45(9):586–90. DOI: 10.1111/j.1469-8749.2003.tb00962.x. PMID: 12948325.
49. Watanabe K., Hakamada S., Kuroyanagi M. et al. Electroencephalographic study of intraventricular hemorrhage in the preterm newborn. Neuropediatrics 1983;14(4): 225–30. DOI: 10.1055/s-2008-1059583. PMID: 6657009.
50. Watanabe K., Hayakawa F., Okumura A. Neonatal EEG: a powerful tool in the assessment of brain damage in preterm infants. Brain Dev 1999;21(6):361–72. DOI: 10.1016/s0387-7604(99)00034-0. PMID: 10487468.
51. Whitehead K., Pressler R., Fabrizi L. Characteristics and clinical significance of delta brushes in the EEG of premature infants. Clini Neurophysiol Pract 2017;(2):12–8. DOI: 10.1016/j.cnp.2016.11.002.
52. Zeinstra E., Fock J.M., Begeer J.H. et al. The prognostic value of serial EEG recordings following acute neonatal asphyxia in full-term infants. Eur J Paediatr Neurol 2001;5(4):155–60. DOI: 10.1053/ejpn.2001.0496. PMID: 11587379.
Review
For citations:
Chegodaev D.A., Pavlova N.V., Lvova O.A., Shalkevich L.V. Electroencephalogram in premature infants: from normal to pathological activity. Russian Journal of Child Neurology. 2019;14(1):26-35. (In Russ.) https://doi.org/10.17650/2073-8803-2019-14-1-26-35