Electroencephalography in premature and full-term infants. Developmental features and glossary

doi:10.1016/j.neucli.2010.02.002

Neurophysiologie Clinique/Clinical Neurophysiology

Volume 40, Issue 2, May 2010, Pages 59-124

https://doi.org/10.1016/j.neucli.2010.02.002 Get rights and content

Summary

Following the pioneering work of C. Dreyfus-Brisac and N. Monod, research into neonatal electroencephalography (EEG) has developed tremendously in France. French neurophysiologists who had been trained in Paris (France) collaborated on a joint project on the introduction, development, and currently available neonatal EEG recording techniques. They assessed the analytical criteria for the different maturational stages and standardized neonatal EEG terminology on the basis of the large amount of data available in the French and the English literature. The results of their work were presented in 1999. Since the first edition, technology has moved towards the widespread use of digitized recordings. Although the data obtained with analog recordings can be applied to digitized EEG tracings, the present edition, including new published data, is illustrated with digitized recordings. Herein, the reader can find a comprehensive description of EEG features and neonatal behavioural states at different gestational ages, and also a definition of the main aspects and patterns of both pathological and normal EEGs, presented in glossary form. In both sections, numerous illustrations have been provided. This precise neonatal EEG terminology should improve homogeneity in the analysis of neonatal EEG recordings, and facilitate the setting up of multicentric studies on certain aspects of normal EEG recordings and various pathological patterns.

Résumé

À la suite des travaux pionniers de C. Dreyfus-Brisac et N. Monod, une école d’EEG néonatal s’est développée en France. Des neurophysiologistes français issus de cette formation ont collaboré à la rédaction d’une mise au point, publiée en 1999, sur la naissance et l’évolution de la technique d’enregistrement de l’électroencéphalogramme en néonatalogie. Ils ont aussi fait la synthèse des critères d’analyse des différents stades maturatifs et précisé la terminologie de l’EEG néonatal à partir des nombreuses données de la littérature francophone et anglophone. Depuis la première édition, la technologie a évolué et la numérisation des enregistrements est très largement utilisée. Bien que les données obtenues à l’aide des enregistrements analogiques puissent être appliquées aux enregistrements numérisés, cette nouvelle édition, qui rapporte aussi les données publiées récemment, est illustrée à l’aide d’enregistrements numérisés. Le lecteur pourra trouver dans cet ouvrage la description des aspects électroencéphalographiques et des états de vigilance du nouveau-né selon l’âge gestationnel, mais aussi la définition des principaux aspects et figures EEG normaux et pathologiques rassemblés sous la forme d’un glossaire. Ces deux chapitres sont étayés d’une abondante iconographie. Une terminologie EEG précise en néonatalogie devrait aussi améliorer l’harmonisation dans l’analyse des tracés et faciliter la réalisation d’études multicentriques sur certains aspects de l’EEG normal ou lors de différentes pathologies.

Section snippets

Historical background

By D. Samson-Dollfus, 1999 [41]

In 1933, Berger [9] claimed that no cerebral electrical activity was apparent before the age of 35 days. Five years later, however, Smith [83], [84], [85] showed that the tracings recorded in full-term neonates displayed 4 to 7 Hz frequencies, mixed with slow waves (2 or 3 Hz) and 12–14 Hz rhythms. In 1942, Lindsley [42] published the tracing recorded in a fetus of gestational age 7 months, recorded through the mother's abdominal wall. Between 1948 and 1953, Hugues

Definitions

Gestational age (GA): number of weeks from the first day of the woman's last menstrual cycle to the birth date.

Conceptional or corrected age (CA): GA at birth plus week number postpartum.

Full-term neonate: neonate born after 38 weeks of amenorrhea.

Premature infant: infant born before 37 weeks of amenorrhea.

The infants born at 37 and 38 weeks are usually considered as having the same clinical and neurological characteristics as the completely full-term newborns, but their EEG show some

Recording methods

Neonatal EEG recording should disturb the infant's behaviour and standard care as little as possible. The EEG equipment must be carefully prepared in advance to minimize the time required for electrode positioning and to avoid interference during recording (for example, opening the incubator). The EEG/polysomnography recorder should be positioned close to the infant, allowing the technician to report behavioural observations and/or to make video recordings.

Interpretation requires knowledge of

Recognition of sleep and wakefulness

Prechtl [74] reported that “behavioural states are constellations of physiological and behavioural variables, which are repeated and remain stable over time not only in a given child, but also in different infants”.

Therefore, the analysis of behavioural states should never be based on a single variable.

In full-term infants, wakefulness is characterized either by agitation (active wakefulness [AW]), or by bright, wide-open eyes, without agitation (quiet wakefulness [QW]).

In daily practice,

Developmental features

The evolution of EEG and of behavioural features according to gestational age is presented in the following pages.

As EEG aspects are almost identical for the same GA and CA, no distinction is made in clinical practice.

The description of some aspects during maturation depends of the thresholds chosen for definitions, in particular for amplitude. They vary from study to study; so the values given for the durations of the activity and inactivity periods may be different [89] ; the main recent

Organization of behavioural states

•
Alternate periods of activity and rest.
•
Variations of EEG activity are inconsistently associated with behaviour.

Background activity

•
Very discontinuous tracing; lability is present which leads to a variable discontinuity.
•
Sequences of amplitude higher than 50 μV lasting less than 60 s.
•
Sequences of 15 to 50 μV lasting around 20–25 s.

EEG features

•
Mono- or diphasic delta waves. They are smooth, with very sparse superimposed theta or alpha rhythms. They are mainly of high amplitude (> 300 μV) and very low frequency (0.3–1 Hz).
•
Theta

Organization of behavioural states

•
Alternate periods with eye movements (less discontinuous EEG and higher amplitude) and periods without eye movements (discontinuous EEG and lower amplitude).
•
Variations of EEG activity are inconsistently associated with behaviour.

Background activity

•
Very discontinuous tracing; lability is present which leads to a variable discontinuity. In studies published after 1988, the longest interburst intervals last 29 to 46 s.
•
Brief periods of semi-continuous tracing. The bursts of amplitude higher than 50 μV can last around

Organization of behavioural states

•
Active wakefulness (AW).
•
Active sleep (AS) with rapid eye movements.
•
Quiet sleep (QS).

These are now well discernible.

Differentiation between AS and QS on EEG can be made from the discontinuous (QS) or continuous (AS) aspect, but not yet from EEG features.

Background activity

•
Discontinuous tracing. Lability is present. The duration of the “hypoactive periods” (interburst intervals, IBI) is very variable (up to 30 s).
•
Periods of continuity are longer (up to 160 s) and more numerous than before 28 weeks GA. They are more

Organization of behavioural states

•
Active wakefulness (AW).
•
Active sleep (AS).
•
Quiet sleep (QS).

A good concordance is established between EEG activity and behavioural criteria.

Background activity

•
AW: mainly artefacts are registered.
•
AS: continuous or semi-continuous tracing.
•
QS: discontinuous tracing; bursts of activity ≥ 3 s, periods of hypoactivity (IBI) ≤ 20 s.

EEG features

•
Delta waves (0.7–2 Hz) have an amplitude of 100 to 200 μV. Smooth delta waves are no longer observed. Theta rhythms superimposed on delta waves persist.
•
Delta waves with superimposed alpha or beta

Organization of behavioural states

AW, AS and QS are easily differentiated, but periods of quiet wakefulness (QW) are still rare.

Background activity

•
AW: continuous activity with frequent artefacts.
•
QW: continuous tracing.
•
AS: continuous tracing identical to that for QW; the two states may be differentiated in terms of polygraphic patterns, or by visual observation.
•
QS: discontinuous tracing: the burst duration lengthens between 32 and 34 weeks GA, with a concomitant decrease in the interburst interval. Despite lower values of interburst intervals

Organization of behavioural states

•
AW, AS and QS.
•
QW is clearly differentiated.
•
Differentiation of two states of AS as of 36 weeks GA: AS 1 precedes QS, AS 2 follows QS.

Background activity

•
AW and QW: continuous activity, activité moyenne (“polyfrequency activity”) appears at 36 weeks GA.
•
AS 1: high-amplitude continuous tracing.
•
AS 2: continuous tracing with more rapid activity and amplitude lower than that during AS 1.
•
QS: still discontinuous or semi-discontinuous. The duration of periods of hypoactivity is < 10 s.

EEG features

•
Delta waves with superimposed fast

Organization of behavioural states

•
AS 1 and AS 2.
•
QS.
•
AW and QW are clearly differentiated.

Background activity

•
AW, QW, AS 2: activité moyenne (“polyfrequency activity”).
•
AS 1: continuous activity, mixed frequencies. The amplitude is higher, the activity is less rapid than during AS 2.
•
QS: semi-discontinuous or sometimes tracé alternant.

EEG features

•
Delta waves with superimposed fast rhythms (delta brushes) in all behavioural states, with a higher amplitude during QS.
•
Clearly differentiated frontal transients during AS 1 and at the onset of QS.
•
Slow anterior dysrythmia

Organization of behavioural states

AS 1, QS, AS 2, AW and QW are clearly differentiated.

Background activity

•
AW, QW, AS 2: activité moyenne (“polyfrequency activity”)
•
AS 1: continuous tracing, with decreased amplitude compared to the activity at 37–38 weeks GA (mixed frequencies).
•
QS: tracé alternant and/or slow continuous tracing.

EEG features

•
Delta brushes persist, but they are rare and only observed during QS.
•
Frontal transients: identical to those observed at 37–38 weeks GA.
•
Slow anterior dysrythmia: identical to that observed at 37–38 weeks GA.
•
Appearance of

Glossary

Definitions of the main normal and pathological neonatal EEG aspects.

Normal EEG tracings

Figures from the previous sections illustrate some of these definitions.

Pathological EEG tracings

The diagnostic and prognostic value of the EEG in neonates is the result of detailed morphological analysis performed over many years, which has formed the basis for the following descriptions.

Some tracings and patterns frequently observed in neonatal pathology are highly suggestive of certain etiologies. However, the aim of this paper is not to report the correlations between EEG patterns and diseases. Should you so wish, please refer to the references for such correlations.

It should also be

Conflict of interest statement

None.

Acknowledgements

The authors are very grateful to Mickaël Walls for the revision of the English language.

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Review/Mise au pointElectroencephalography in premature and full-term infants. Developmental features and glossaryÉlectroencéphalographie du nouveau-né prématuré et à terme. Aspects maturatifs et glossaire

Summary

Résumé

Section snippets

Historical background

Definitions

Recording methods

Recognition of sleep and wakefulness

Developmental features

Organization of behavioural states

Background activity

EEG features

Organization of behavioural states

Background activity

Organization of behavioural states

Background activity

Organization of behavioural states

Background activity

EEG features

Organization of behavioural states

Background activity

Organization of behavioural states

Background activity

EEG features

Organization of behavioural states

Background activity

EEG features

Organization of behavioural states

Background activity

EEG features

Glossary

Normal EEG tracings

Pathological EEG tracings

Conflict of interest statement

Acknowledgements

Rev Electroencephalogr Neurophysiol Clin

Electroencephalogr Clin Neurophysiol

Rev Electroencephalogr Neurophysiol Clin

J Pediatr

Electroencephalogr Clin Neurophysiol

Electroencephalogr Clin Neurophysiol

Rev Electroencephalogr Neurophysiol Clin

Rev Electroencephalogr Neurophysiol Clin

Rev Electroencephalogr Neurophysiol Clin

Neurophysiol Clin

Rev Electroencephalogr Neurophysiol Clin

Rev Electroencephalogr Neurophysiol Clin

Clin Neurophysiol

Electroencephalogr Clin Neurophysiol

Neurophysiol Clin

J Epilepsy

Electroencephalogr Clin Neurophysiol

Rev Electroencephalogr Neurophysiol Clin

Rev Electroencephalogr Neurophysiol Clin

Rev Electroencephalogr Neurophysiol Clin

Rev Electroencephalogr Neurophysiol Clin

Electroencephalogr Clin Neurophysiol

Rev Electroencephalogr Neurophysiol Clin

Electroencephalogr Clin Neurophysiol

Brain Dev

Electroencephalogr Clin Neurophysiol

Rev Electroencephalogr Neurophysiol Clin

Brain Res

Rev EEG Neurophysiol Clin

Rev Electroencephalogr Neurophysiol Clin

Electroencephalogr Clin Neurophysiol

Clin Neurophysiol

Neurophysiol Clin

Neurophysiol Clin

Neurophysiol Clin

Neurophysiol Clin

Neurophysiol Clin

Neurophysiol Clin

Electroencephalogr Clin Neurophysiol

A manual of standardized terminology, techniques and criteria for scoring of states of sleep and wakefulness in newborn infants

Neonatal seizures--recent aspects

Neuropediatrics

Neonatal electroencephalography and neuropathology

J Clin Neurophysiol

Uber das Elektrenkephalogram des Menschen

Review/Mise au point
Electroencephalography in premature and full-term infants. Developmental features and glossaryÉlectroencéphalographie du nouveau-né prématuré et à terme. Aspects maturatifs et glossaire