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

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.

Normal EEG of premature infants born between 24 and 30 weeks gestational age: terminology, definitions and maturation aspects.

This article presents normal EEG characteristics and their maturational pattern in premature infants of 24-30 weeks gestational age. Although the very premature infants with a normal outcome are not that numerous, their normal EEG pattern should be known, as EEG constitutes a basis for neurological prognosis. Background activity is first discontinuous but the discontinuity gradually decreases and the activity is completely continuous at 30 weeks of age, during active sleep. At the same time, interburst intervals become shorter so that the proportion of time without EEG activity decreases. Based on EEG activity and eyes movements, a rough sleep state differentiation appears as early as 25 weeks of gestational age and is complete at 30 weeks. The main EEG figures are high-voltage delta waves, whose frequency is slower and amplitude higher in younger infants. Temporal delta waves occur in sequences and are characteristic of the very premature infant; they progressively become smaller and less numerous and disappear around 27-28 weeks. In contrast, occipital delta waves remain numerous; they are of high voltage and usually bilaterally superimposed with fast rhythms. Both types of frontal delta waves that are seen in 24-27 weeks premature babies disappear with maturation. Bursts of synchronized delta waves, which are less numerous than localized delta waves, also disappear before 28 weeks of gestational age. Finally, diffuse theta bursts which are mainly recorded at 26-27 weeks, progressively focus on temporal areas with maturation. At 30 weeks, they are observed on temporal areas, mainly during slow-wave sleep.

Pathological features of neonatal EEG in preterm babies born before 30 weeks of gestationnal age.

Pathological features on very premature EEG concern background abnormalities and abnormal ictal and nonictal patterns. Positive rolandic sharp waves keep an important place regarding diagnosis and prognosis of white-matter lesions. Background abnormalities, that may be classified as acute-stage or chronic-stage abnormalities, give essential complementary information. These abnormal patterns remain precocious markers of cerebral lesions and are complementary to cerebral imaging. Analysis of these abnormalities has always to take into account medication received by the baby during the recording and that could modify the EEG.

[EEG of the very premature infant born at 24 to 30 weeks gestational age. Definitions and normal area]. / EEG normal du grand prématuré de 24 à 30 semaines d'âge gestationnel. Définitions et maturation.

This article aims at summarizing normal EEG criteria and their maturational pattern in premature infants of 24 to 30 weeks gestational age. Although very premature infants with a normal outcome are not numerous, their normal EEG patterns must be known, as EEG constitutes a basis for neurological prognosis. Background activity is first discontinuous. Discontinuity decreases thereafter with increasing age, so that some long periods of continuous activity may be observed in active sleep, around 30 weeks of age. Conversely, interburst intervals become shorter and the proportion of time without EEG activity is decreasing. Based on EEG activity and eye movements, a rough sleep-state differentiation was described as soon as 25 weeks of gestational age and is completely achieved at 30 weeks. The main EEG figures are high-voltage delta waves of higher amplitude and slower frequency in younger infants. Temporal delta waves occur in sequences, these are very characteristic of the very premature infant; thereafter, they become smaller, less numerous and eventually disappear around 27-28 weeks. In contrast, occipital delta waves remain numerous and of high voltage, are usually bilateral and superimposed with fast rhythms. The two types of frontal delta waves that are observed in 24-27 weeks prematures disappear with maturation. Bursts of synchronized delta waves are less numerous than localized delta waves and also disappear before 28 weeks of age. Finally, diffuse theta bursts are mainly recorded at 26-27 weeks GA and become more localized in temporal areas with maturation. At 30 weeks, they are observed on temporal areas, mainly during slow-wave sleep.

[Pathological patterns in neonatal EEG before 30 weeks of gestational age]. / Les aspects pathologiques de l'EEG du nouveau-né prématuré avant 30 semaines d'âge postmenstruel.

Pathological features on very premature EEG concern background abnormalities and abnormal patterns. Positive rolandic sharp waves keep an important place regarding diagnosis and prognosis. Background abnormalities give essential complementary informations. Unusual patterns (abnormal localisation or morphological aspect, high amplitude) remain early markers of cerebral lesions. Analysis of these pathological features must always take into account treatment given to the baby, which can by itself modify the EEG.

[Indications of electroencephalogram in the newborn]. / Indications de l'électroencéphalogramme en période néonatale. Recommandations du groupe de neurophysiologie clinique de l'enfant.

The electroencephalogram (EEG), an easy-to-use and non invasive cerebral investigation, is a useful tool for diagnosis and early prognosis in newborn babies. In newborn full term babies manifesting abnormal clinical signs, EEG can point focal lesions or specific aetiology. EEG background activity and sleep organization have a high prognostic value. Tracings recorded over long period can detect seizures, with or without clinical manifestations, and differentiate them from paroxysmal non epileptic movements. The EEG should therefore be recorded at the beginning of the first symptoms, and if possible before any seizure treatment. When used as a neonatal prognostic tool, EEG background activity is classified as normal, abnormal (type A and type B discontinuous and hyperactive rapid tracing) or highly abnormal (inactive, paroxysmal, low voltage plus theta tracing). In such cases, the initial recording must be made between 12 and 48 h after birth, and then between 4 and 8 days of life. Severe EEG abnormalities before 12 h of life have no reliable prognostic value but may help in the choice of early neuroprotective treatment of acute cerebral hypoxia-ischemia. During presumed hypoxic-ischemic encephalopathy, unusual EEG patterns may indicate another diagnosis. In premature newborn babies (29-32 w GA) with neurological abnormalities, EEG use is the same as in term newborns. Without any neurological abnormal sign, EEG requirements depend on GA and the mother's or child's risk factors. Before 28 w GA, when looking for positive rolandic sharp waves (PRSW), EEG records are to be acquired systematically at D2-D3, D7-D8, 31-32 and 36 w GA. It is well known that numerous and persistent PRSW are related to periventricular leukomalacia (PVL) and indicate a bad prognosis. In babies born after 32 GA with clinically severe symptoms, an EEG should be performed before D7. Background activity, organization and maturation of the tracing are valuable diagnosis and prognosis indicators. These recommendations are designed (1) to get a maximum of precise informations from a limited number of tracings and (2) to standardize practices and thus facilitate comparisons and multicenter studies.

Late-onset cystic periventricular leukomalacia in premature infants: a threat until term.

The purposes of this study are (1) to describe a "late-onset" form of cystic periventricular leukomalacia eventually appearing in premature infants whose neurological assessments were normal in the first month of life; (2) to retrospectively evaluate its incidence among a large population of premature infants; (3) to suggest that a few unexpected complications of prematurity may trigger the development of white matter damage, even several weeks after birth. Retrospective study in a population of 1452 surviving infants after 5 days born before 33 weeks. We identified 10 cases of late-onset cystic periventricular leukomalacia appearing beyond the first 5 weeks of life. In 8 cases, an intercurrent event associated with a systemic inflammatory response preceded the appearance of cysts: necrotizing enterocolitis (n = 5), septicemia (n = 2 cases), strangulated inguinal hernia in one infant. Neurological surveillance should be repeated until discharge in very preterm infants, especially after the occurrence of an intercurrent complication coming along with a systemic inflammatory response.

[Electroencephalography of the premature and term newborn. Maturational aspects and glossary]. / Electroencéphalographie du nouveau-né prématuré et à terme. Aspects maturatifs et glossaire.

From the first publication of C. Dreyfus-Brisac and N. Monod, a strong tradition combined with tremendous development of neonatal EEG has taken place in France. After 3 years of collaborative work, 12 clinical neurophysiologists trained at the Port-Royal medical school in Paris detail in this paper the currently available neonatal EEG recording techniques. They have synthesized the criteria of maturational state analysis and have defined the normal and pathological neonatal EEG patterns, including descriptions already present in the French as well as the English literature. In this review one may find a complete description of neonatal EEG patterns according to the states of vigilance and to gestational age. Furthermore, definitions of all normal and pathological patterns are provided in a glossary. Both chapters are illustrated by numerous figures. This detailed terminology in neonatal EEG should allow a better homogeneity in EEG reports, and could lead to multicentric studies on normal, unusual or pathological patterns, according to etiology. Although based on analogic EEG data, this work can equally be applied to digitized EEG tracings.

[Indications for emergency EEG in perinatal pain]. / Indications urgentes de l'EEG dans la souffrance périnatale.

EEG is a basic tool in neurological evaluation of fullterm or premature newborn. An emergency recording (in hours following birth) is required in two circumstances: a suspicion of seizure (especially before starting specific therapy), and a major behavioral disorder. The main cause is, in fullterm newborn, hypoxic-ischemic encephalopathy. More precise informations are provided by recording between 10 and 48 hours after birth. In premature, emergency EEG may be recorded between 24 and 48 hours after birth. Some particular EEG features suggest specific causes such as metabolic or infectious diseases and focal lesions. In some cases, especially during seizures, conventional EEG can be completed by continuous monitoring.

The early diagnosis of periventricular leukomalacia in premature infants with positive rolandic sharp waves on serial electroencephalography.

OBJECTIVE: The objective of this study was to determine the specificity and the sensitivity of electroencephalography's positive rolandic sharp waves (PRSW) for the diagnosis of cystic and noncystic periventricular leukomalacia (PVL). METHODS: A retrospective study was performed on a population of 765 premature infants alive after 5 days who were divided into two groups; 166 infants born before 28 weeks (group 1) and 599 born between 28 and 32 completed weeks' gestation (group 2). Each infants underwent repeated ultrasound scanning and electroencephalography recordings during the first weeks of life. Magnetic resonance imaging was performed in infants with persisting hyperechoic periventricular densities on ultrasonography. RESULTS: A total of 83 (10.8%) newborns had PVL; 65 (8.5%) had cystic PVL PRSW, observed in 55 (7.2%) infants, always preceded the ultrasonic detection of cysts. PRSW were very specific markers of PVL in both groups (100% in group 1, 99.8% in group 2). PRSW sensitivity was found dependent on gestational age: 32.4% in group 1 in contrast to 87.8% in group 2. CONCLUSION: PRSW are an early and very specific marker of PVL in premature infants.

Quantitative analysis of discontinuous EEG in premature and full-term newborns during quiet sleep.

To assess the spatio-temporal structure of discontinuous EEG tracing in mature and immature newborns, we analysed mean spectral power in frequency bands between 0.8 and 16.8 Hz in 6 full-term newborns and 7 premature newborns < 32 weeks of conceptional age. The most striking results showed a significantly higher mean spectral power for the first half of bursts than for the second half recorded in > 2.8-14.8 Hz frequency bands. This pattern was more pronounced in premature than in full-term newborns. No clear differences were observed in comparisons between the first and the second half of the interburst periods. In addition, as far as mid and high frequency band spectra were considered, the mean spectral power of burst was, in both groups, higher in the right as compared to the left occipital regions.

[Intraventricular hemorrhage and parenchymatous ischemia in the newborn at term. Report of five cases]. / Hémorragie intraventriculaire et ischémie parenchymateuse chez le nouveau-né à terme à propos de cinq cas.

Although intraventricular hemorrhage associated with cerebral ischemia without severe perinatal asphyxia is rare in full-term newborns, it can be severe, have early or late onset depending on the etiology and be of poor prognosis. Five full-term neonates (37 to 41 weeks of gestational age) without criteria of severe perinatal asphyxia were admitted to the intensive care unit for seizures: four were between seven and 11 days of age and one was only 12 h old. Clinical or electroclinical seizures recorded by continuous EEG monitoring were numerous, leading to status epilepticus in three babies. They were unilateral (at the level of the left hemisphere) in one infant and have not been recorded in the fourth case. Past-ictal EEG abnormalities were numerous rolandic or temporal slow or fast sharp waves of variable polarity. Cranial CT scans showed uni- or bilateral intraventricular hemorrhage with dilatation and subcortical or periventricular ischemic lesions with hemorrhage. Four out of the five infants died during the neonatal period.

Periventricular leukomalacia: risk factors revisited.

The dramatic improvement in neonatal care during the last decade did not succeed in reducing the incidence of periventricular leukomalacia (PVL), suggesting that prenatal events may be the main target for PVL prevention. The studied cohort included 753 very preterm infants born between 24 and 32 weeks of gestational age, admitted to the intensive care unit and surviving at least 7 days; 69 (9.2%) of these infants had a diagnosis of cystic PVL. The highest PVL frequency was observed among the infants born at 28 weeks of gestation (16%). Inflammatory prenatal events occurring during the last days or weeks before delivery and PVL occurrence are strongly correlated. Indeed, the combination of intra-uterine infection and premature rupture of membranes is associated with a very high risk (22%). Prolongation of pregnancy with tocolysis for more than 24 hours also carries a significant 8% risk of PVL. In contrast, chronic fetal distress of long duration, such as severe intra-uterine growth retardation and pre-eclampsia, is seldom followed by PVL (< 2% risk). Similarly, rapid unexpected deliveries entail a minimal PVL risk (4%). Experimental and epidemiological confirmations of these data would have an influence on the management of both the preterm onset of labour and the premature rupture of membranes.

Segmental myoclonus in a child with spinal cord tumour.

Segmental spinal myoclonus (SSM) involving a child's lower limb revealed the presence of a spinal cord tumour from T8 to T12. The clinical and electrophysiological features of SSM-during the child's development were studied. The presence of this disorder at two months of age did not disturb the development of walking, but did lead to orthopaedic complications. Four electromyographic recordings performed between 23 months and 7 years 10 months of age revealed the topographical extension of the SSM, its passage to rhythmicity, variable frequency and change in the sequence of activation of the muscles. These electroclinical features enable discussion of the pathophysiology of SSM by reference to neonatal motor automatisms and spinal generators.

Sleep state organization in premature infants of less than 35 weeks' gestational age.

To assess sleep organization in premature infants of < 35 wk gestational age (w GA), we performed polygraphic recordings in 24 neurologically normal neonates (eight per group): artificially ventilated 27-30 and 31-34 w GA infants and nonventilated 31-34 w GA infants. Sleep states were defined by concordance of EEG and rapid eye movement criteria. Uninterrupted active sleep periods of > 13 min and quiet sleep periods of > 5 min were observed in all babies, except in one 33 w GA ventilated infant. Intervals from the beginning of recording to the 1st quiet sleep period varied from 0 to 63 min and intervals to the beginning of the longest sleep cycle varied from 5 to 84 min. Nonventilated 31-34 w GA infants had longer sleep cycles (p < 0.02), principally because of longer active sleep periods. However, percentages of different states in the cycles were similar in all groups. When body movements were required for state definition, amounts of active and quiet sleep diminished and the percentage of indeterminate sleep was augmented significantly. In conclusion, our study demonstrated that 1) sleep state differentiation is present as soon as 27 w GA; and 2) artificial ventilation, performed in a highly specialized neonatal intensive care unit, does not modify sleep organization of neurologically normal premature infants. We hypothesize that this "earlier" sleep state differentiation, compared with previous data, may be related to improvements in neonatal intensive care over recent years.

[Periventricular leukomalacia of late onset in a premature infant]. / Leucomalacie périventriculaire d'apparition tardive chez un prématuré.

BACKGROUND: Periventricular leukomalacia in preterm neonates is usually due to abnormal cerebral blood flow before and/or during delivery. It is diagnosed during the first month of life. This study describes a case of late-developing periventricular leukomalacia. CASE REPORT: A girl was delivered by cesarean section at the 23rd week of gestation that was complicated by placenta previa. She weighted 880 g and immediately required resuscitation. She did not develop respiratory distress syndrome. She was intubated and ventilated for the first two weeks of life and developed bronchopulmonary dysplasia requiring corticosteroid treatment. Extubation was possible on day 43. The neonate had been given antibiotics for the first 10 days of life and indomethacin on day 8 because of a patent ductus arteriosus. Repeated craniosonography showed moderate bilateral intraventricular hemorrhage and occipital areas of hyperechogenicity that disappeared at the end of the first month of life. Repeated electroencephalograms revealed no positive rolandic sharp waves until the infant was 42 days old. Craniosonography on day 48 showed areas of heterogeneous hyperechogenicity and NMR imaging showed bilateral frontoparietal leukomalacia with loss of white matter. The baby died on day 71. CONCLUSIONS: Late periventricular leukomalacia is exceptional and usually seen after postnatal abnormalities in cerebral blood flow and/or prolonged hypoxemia. Both these risk factors were absent in this patient.