EEG of Premature and Full-Term Infants
Thoru Yamada
Elizabeth Meng
Michael Ciliberto
The EEG of premature and neonatal infants must be viewed from a different perspective than the EEG of adults or children because of the wide variation of “normal” EEG patterns in the neonate, especially in premature infants. The rapid progression of EEG maturation and a number of EEG patterns of uncertain clinical significance impose further difficulty in determining normality. Accurate interpretation of neonatal EEG has become increasingly important since many neonatal seizures occur without definite evidence of clinical seizures and also, even experienced clinical observers may have a difficulty in recognizing seizures in neonates.1 This has led to an era of expanding use of EEG in the neonatal periods. The aim of this chapter is not to discuss the variations of premature EEG patterns in detail; only essential and well-established concepts will be described here. For further details, the reader should refer to several excellent review papers.2,3,4
Recording Techniques
Because of the smaller head size in children, fewer electrodes are generally used than in adult patients with whom the 10-20 system is typically used. American Clinical Neurophysiologic Society (ACNS) guidelines5 recommend the following placement: Fp1 and Fp2 [or Fp3 and Fp4 (Fp3 is halfway between Fp1 and F3 and Fp4 is halfway between Fp2 and F4)], C3 and C4, T3 and T4, O1 and O2, A1 and A2, and Cz. A recording utilizing at least 12 channels should be used. For EEG recording, the use of low-frequency filter of 0.3 to 0.6 Hz or time constant of 0.27 to 0.33 second is recommended. The sensitivity is usually 7 µv/mm but might need to be adjusted either higher or lower depending on the case.
In order to assess waking and sleeping states (quiet and active sleep), respiratory movements and airflow, EKG, EOG, and submental EMG are routinely recorded. This has been facilitated by the ability of some software packages to interface with typical neonatal monitoring systems allowing the accurate acquisition of respiratory, pulse oximetry, and heart rate data. Besides recording EEG, additional channels are dedicated to respiratory movements by abdominal and/or thoracic strain gauges or impedance pneumogram and airflow by thermistors/thermocouples, EKG, EOG, and submental EMG. For EOG recording, low-frequency filter of 0.3 to 0.6 Hz would be adequate. For EMG recording, low-filter setting of 5 Hz and high filter of 70 Hz, and sensitivity of 3 µv/mm are used.
Commonly used montages (as recommended by ACNS) are shown in Table 16-1.5 Recording montages should routinely include the vertex (Cz) electrode because significant EEG patterns characteristic for this age group (positive vertex sharp waves, negative vertex sharp waves, and electrographic seizures) may be detected only from this region. Unlike in older children and adults, multiple reviewing montages are typically not used with readers typically relying on a comprehensive bipolar montage with the addition of the aforementioned other leads.
The Role of Technologists
Besides gathering routine information for EEG recording (history, reason for referral, medication, state of consciousness, etc.),
it is imperative to note the gestational age (GA) (the time elapsed between the first day of the last menstrual period and the day of delivery) and chronological age (the time elapsed since birth). The term “conceptional age (CA)” has been used based on the day of conception. The American Academy of Pediatrics now recommends using postmenstrual age, not the day of conception for determining GA. For example, a baby whose EEG is recorded at 4 weeks after birth with a GA of 30 weeks at the time of birth is 34 weeks CA. A baby born at 38 to 40 weeks GA is a full-term baby. A baby born at or before 38 weeks GA is considered to be premature. And, a baby born after 40 weeks GA is postmature. The survival of infants born before 34 or 35 weeks GA was not common 30 years ago, but today, it is not uncommon for a 24- to 26-week-GA baby to survive.
it is imperative to note the gestational age (GA) (the time elapsed between the first day of the last menstrual period and the day of delivery) and chronological age (the time elapsed since birth). The term “conceptional age (CA)” has been used based on the day of conception. The American Academy of Pediatrics now recommends using postmenstrual age, not the day of conception for determining GA. For example, a baby whose EEG is recorded at 4 weeks after birth with a GA of 30 weeks at the time of birth is 34 weeks CA. A baby born at 38 to 40 weeks GA is a full-term baby. A baby born at or before 38 weeks GA is considered to be premature. And, a baby born after 40 weeks GA is postmature. The survival of infants born before 34 or 35 weeks GA was not common 30 years ago, but today, it is not uncommon for a 24- to 26-week-GA baby to survive.
TABLE 16-1 Neonatal Montages | ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
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Other relevant clinical information includes blood gas, body temperature, serum electrolyte, and current medications. Also, technologists should consult nursing staff concerning the patient’s condition or any limitation in handing the baby.
The recording is preferably scheduled right after feeding time, since babies tend to sleep after feeding although an hourlong recording of most neonates should capture all stages of sleep and sleep-wake transitions. The technologist must observe the patient carefully throughout the recording and annotate the baby’s movement or behavioral changes. The notation may include eye opening and closing, head position, hiccups, sucking, breathing patterns, etc. The technologist should also note any unusual behaviors such as tonic posturing, clonic movement, eye deviation, skin color change, and other vital signs including SaO2 saturation, blood pressure, and respiratory changes (Video 16-1). It is also important for the technologist to observe and note the baby’s state of consciousness. Routine use of video recording with EEG would be extremely helpful to correlate EEG findings with babies’ various behaviors.
Except for extremely premature infants (23 to 24 weeks GA), wakefulness is simply determined by eye opening and sleep is determined by eye closure. It may be possible to determine clinically if a baby is in active or quiet sleep, because of corresponding rapid eye movement (REM) or non-REM sleep, respectively, by observing the baby’s behavior. In active sleep, a baby may show a variety of facial, eyelid, arm, and leg twitches or body movements, sucking, or even crying. Under closed eyelids, REMs (rapid eye movements), predominantly in the horizontal direction, can be observed. Respiration becomes irregular, occasionally associated with apnea. The EEG during active sleep essentially consists of a low-voltage and continuous pattern, resembling quiet wakefulness (Fig. 16-1). In newborn infants, 50% of sleep time is active sleep, and sleep may start with active sleep directly from wakefulness. This pattern of active sleep onset may continue until about 4 months postterm, when quiet sleep becomes a prerequisite to entering active sleep. Also, the percentage of active sleep decreases rapidly to 20% to 25% of sleep time. In contrast to active sleep, quiet
sleep is characterized by few movements or twitches of face, head, limb, or trunk. Respirations are quiet and regular, without apnea. The EEG of quiet sleep consists of a variety of slow waves or bursts interrupted by a relatively low-voltage pattern representing trace discontinue (TD) (Fig. 16-2) or trace alternant (TA) (Fig. 16-3). It is important to capture quiet sleep because this may be the only state in which some EEG abnormalities become evident. The recording should include waking and all cycles of sleep including active and quiet sleep. Since active sleep occupies more than 50% of the sleep time in the neonate, a 1-hour recording will generally capture all states. After a satisfactory sleep record, the baby may be aroused while the recording continues. In order to capture all sleep stages and awake record, recording time for neonates should be at least 1 hour.
sleep is characterized by few movements or twitches of face, head, limb, or trunk. Respirations are quiet and regular, without apnea. The EEG of quiet sleep consists of a variety of slow waves or bursts interrupted by a relatively low-voltage pattern representing trace discontinue (TD) (Fig. 16-2) or trace alternant (TA) (Fig. 16-3). It is important to capture quiet sleep because this may be the only state in which some EEG abnormalities become evident. The recording should include waking and all cycles of sleep including active and quiet sleep. Since active sleep occupies more than 50% of the sleep time in the neonate, a 1-hour recording will generally capture all states. After a satisfactory sleep record, the baby may be aroused while the recording continues. In order to capture all sleep stages and awake record, recording time for neonates should be at least 1 hour.
General Characteristics of Normal Neonatal EEG
The first step of neonatal EEG analysis is to examine the degree of continuity of EEG activity. The second step is to examine the synchrony of EEG activity between homologous cortical areas. The third step is to evaluate the various EEG patterns characteristic for neonates and, lastly, to determine whether these features are appropriate for the stated CA.
CONTINUITY VERSUS DISCONTINUITY
The EEG in a neonate less than 27 to 30 weeks CA is characterized by a discontinuous pattern, consisting of intermittent irregularly mixed bursts of theta-delta with sharp and fast activities interrupted by relative voltage suppression periods. There are two types of discontinuous patterns: one is TD (Fig. 16-2) and the other is TA (Fig. 16-3). Both patterns occur during all stages of sleep.6 The TD pattern consists of very slow (0.3 to 1 Hz) delta bursts, which may be intermixed with 4- to 5-Hz theta activity, alternating with quiescent periods.7,8 The length of this “flat” or inactive EEG may carry important diagnostic value; a flat period greater than 30 seconds carries a greater risk of nonsurvival, whereas a shorter inactive period tends to correlate with a favorable outcome.9 However, some data suggest that longer periods of relative voltage suppression may be acceptable in CAs less than 28 weeks.10 TD continues until 35 weeks CA and evolves to TA thereafter (Fig. 16-3, see also Fig. 16-14). TA consists of a variety of theta-delta waves mixed with fast and “spiky” or sharply contoured activities lasting 3 to 10 seconds followed by a relative suppression period of 5 to 10 seconds. Unlike TD, the inactive period of TA is not truly “flat” but consists of low-voltage activities of mixed frequency. The TA pattern is gradually replaced by slow-wave sleep toward full term and is completely replaced by 44 to 45 weeks CA (Fig. 16-4, see also Fig. 16-14).11
SYNCHRONY VERSUS ASYNCHRONY
Degrees of interhemispheric synchrony of the above described bursts differ depending on the CA. About 70% of the bursts during quiet sleep are synchronous at 31 to 32 weeks CA. Thereafter, synchronization increases to 80% at 33 to 34 weeks
CA, 85% at 35 to 36 weeks CA, and 100% after 37 weeks CA.5,8,12 Paradoxically, infants younger than 30 weeks CA may show more synchronized bursts with infants less than 26 weeks CA being mostly synchronous.13 Persistent asynchrony after 37 weeks CA is considered to be abnormal.12 Despite the presence of interhemisphere and intrahemisphere asynchrony, overall EEG activities between the two hemispheres should be symmetric. An abnormality is suspected if an amplitude asymmetry is consistently greater than 50%; the depressed side is abnormal in most cases.
CA, 85% at 35 to 36 weeks CA, and 100% after 37 weeks CA.5,8,12 Paradoxically, infants younger than 30 weeks CA may show more synchronized bursts with infants less than 26 weeks CA being mostly synchronous.13 Persistent asynchrony after 37 weeks CA is considered to be abnormal.12 Despite the presence of interhemisphere and intrahemisphere asynchrony, overall EEG activities between the two hemispheres should be symmetric. An abnormality is suspected if an amplitude asymmetry is consistently greater than 50%; the depressed side is abnormal in most cases.
FIGURE 16-3 | EEG of trace alternant (TA) in a 38- to 40-week-CA infant. There are intermittent generalized bursts consisting of various frequency activities lasting several seconds followed by relative quiescent period during quiet (non-REM) sleep. Note the quiescent period is not as “flat” as in TD (see Fig. 16-2). (From Hrachovy RA. Development of the normal electroencephalogram. In: Levin KH, Luders HO, eds. Comprehensive Clinical Neurophysiology. Philadelphia, PA: WB Saunders, 2000, with permission.) |
FIGURE 16-4 | EEG of continuous slow-wave sleep (CSWS) during quiet sleep in a 38- to 40-week-CA infant. EEG is dominated by relatively high amplitude continuous delta mixed with some theta and fast activities. Note the difference from TA (see Fig. 16-3), wherein slow waves are interrupted by relatively quiescent periods. (From Hrachovy RA. Development of the normal electroencephalogram. In: Levin KH, Luders HO, eds. Comprehensive Clinical Neurophysiology. Philadelphia, PA: WB Saunders, 2000, with permission.) |
ACTIVE VERSUS QUIET SLEEP AND WAKE EEG PATTERN
In early prematurity (before 30 weeks CA), no sleep stage distinction can be made; newborns show an atypical pattern with mixed characteristics of active and quiet sleep. EEG of active sleep consists of more or less continuous, relatively low amplitude (<100 µV), theta activity mixed with delta and some alpha and fast frequency activities (see Fig. 16-1B). After 30 weeks CA, continuity occurs only in active (REM) sleep. Active sleep is predominant until 34 weeks CA14 (see Fig. 16-14). The wake EEG pattern closely resembles active sleep, consisting mostly of low amplitude (15 to 60 µV), mixed theta and delta rhythms, with intermingled or superimposed low-voltage alpha and beta activities. The high tonic EMG activity and eye opening help to distinguish awake from active sleep. Active sleep is characterized by (i) REMs; (ii) irregular respiration, often associated with apnea; and (iii) decreased muscle tone. Despite decreased muscle tone, phasic motor activities such as random muscle twitches, smiling, or grimacing increase in this state.
Quiet sleep emerges after 34 to 36 weeks CA, and at full term (40 weeks CA), active sleep and quiet sleep share an equal percentage of sleep15 (see Fig. 16-14). During quiet sleep, the infant (i) lies quietly with only occasional startle-like movements, (ii) shows no eye movements, (iii) has regular respiration, and (iv) shows continuous tonic muscle activity in the EMG channel. The EEG of quiet sleep is characterized by two types of activity; one is high-voltage slow (HVS) or continuous slow waves (CSW) and the other is TA.
The EEG pattern of TA consists of bursts of 3- to 10-Hz waves mixed with sharp, spike-like discharges lasting 3 to 10 seconds, separated by periods (5 to 10 seconds) of low voltage (see Fig. 16-3). HVS is characterized by 0.5- to 4-Hz delta-theta waves with amplitude reaching 200 V, mixed with low-voltage faster activity (see Fig. 16-4). After full term, quiet sleep progressively increases with concomitant decrease of active sleep, and by 8 months of age, active sleep occupies only 25% of total sleep time, which approximates the amount of REM sleep in an adult.
Specific Pattern Characteristic for a Premature Baby
DELTA BRUSH
The delta brush has also been called “spindle-like fast,”11 “brushes,”12 “rapid bursts,”15 or “ripple of prematurity.”16 This pattern consists of a slow wave of 0.5 to 1.5 Hz with amplitude ranging from 100 to 250 µV with a superimposed, rhythmic 8- to 22-Hz activity of 40 to 70 µV amplitude17,18 (Fig. 16-5). Delta brush appears as early as 27 weeks CA, mainly in the central areas and becomes most abundant at 32 to 34 weeks CA, appearing maximally in occipital and/or temporal, central areas (see Fig. 16-11). They are rare at full term and should not be present after 44 weeks CA. They are more common in quiet than in active sleep.