After the discovery of electroencephalogram (EEG) waves in dogs by the English physician Caton1 in 1875 and of the alpha waves from scalp EEG by the German physician Hans Berger2 in 1929, researchers began to obtain recordings of brain electrical activity from fetuses and infants. Lindsley3 recorded fetal cardiac and cerebral electrical activity, and Hughes4 performed EEG studies in premature infants. Following the discovery of rapid eye movements (REM) sleep by Aserinsky and Kleitman5 in 1953, it was also noted that REM and nonrapid eye movements (NREM) sleep could be differentiated by 30 weeks conceptional age (CA).6 CA is the sum of the gestational age (from the first day of the last recorded menstrual period through birth) plus chronologic age since delivery. Infants are considered full term at 38 weeks and beyond and <38 weeks are considered preterm. With improved ventilation and neonatal intensive care, healthy 23-30 weeks CA infants are more likely to survive without hypoxic ischemic injury, and EEG recordings showed evidence of state differentiation as early as 27 weeks CA. Sleep and wakefulness patterns develop rapidly during the prenatal and newborn period and continue to change during the first years of life. Sleep and wake EEG patterns then remain stable and without significant changes until late adulthood. The waking background frequency continues to evolve through the early teens.
NEONATAL EEG RECORDING
EEG provides a way to investigate the functional properties of the developing CNS. This may be necessary to understand the effects of a variety of insults to the brain including hypoxic encephalopathy, intracerebral hemorrhage, neonatal seizures, hypotonia, or behavior disturbances such as abnormal tone or movements or altered mental status. There are no specific contraindications in performing EEG on neonates, though scalp edema and cranial molding during delivery can complicate electrode placement. The smaller heads of babies make the full 10-20 system of electrode placement impractical, and the standard neonatal montage includes Fp1, Fp2, C3, C4, T3, T4, O2, and O4 and sometimes the midline electrodes Fz, Cz, and Pz. Canthal electrodes for eye movements, EKG electrodes, and an EMG electrode are also helpful. A reduced anteroposterior bipolar (“double banana”) montage with an additional transverse chain is often used. Recording should last at least an hour and endeavor to record a full sleep-wake cycle (see below).
When reading a neonatal or pediatric EEG study, it is essential to know the patient’s CA (for neonates) or chronologic age in months/years, as the normal and abnormal EEG features are age-dependent. The approach to visual analysis is similar to that in adults, with the addition of several steps that take into account the specific features of the activity in the developing brain. In neonates, the first consideration is the continuity of the background. Is there continuous activity or are there periods of voltage suppression? How is the activity organized, and how synchronous and symmetric is it between the hemispheres? Are there waveforms appropriate to a specific CA that can indicate the level of brain maturity or is there an abnormal absence of expected waveforms at the patient’s reported CA? Lastly, are there abnormal features present that suggest brain injury or dysfunction? Following this roadmap, particularly with the guidance of an expert in neonatal/pediatric EEG, can help you develop your reading skills for the youngest patients.
REVIEW
7.1: What are some of the common indications for neonatal EEG recording?
7.1: An EEG may be required to assess hypoxic encephalopathy, intracerebral hemorrhage, neonatal seizures, hypotonia, abnormal tone or movements, or altered mental status.
7.2: What electrodes are used for standard neonatal electrode placement?
7.2: Standard neonatal electrode placement includes Fp1, Fp2, C3, C4, T3, T4, O2, and O4; the midline electrodes Fz, Cz, and Pz; epicanthal electrodes; EKG electrodes; and an EMG electrode.
7.3: What single item of demographic information is needed for neonatal EEG interpretation?
7.3: It is essential to know the patient’s CA (for neonates) or chronologic age in months/years for children, in order to interpret the EEG correctly.
DIFFERENTIATION OF SLEEP AND WAKEFULNESS STATES
As in adults, brain electrical activity, body and eye movements, and respiratory patterns are used to differentiate sleep and wake states in neonates (see Table 7.1).
Full-term newborns have a polyphasic sleep pattern fragmented into multiple 1- to 4-hour periods over the course of the day and spend about two-thirds of their time sleeping during the first weeks of life. This polyphasic sleep pattern gradually changes into the monophasic adult pattern.7 On falling asleep, a normal newborn enters into REM sleep, also referred to as active sleep. Random spontaneous movements of arms, legs, and facial muscles accompany active sleep. These movements can make it difficult to distinguish REM from wakefulness, particularly in premature infants (<37 weeks CA). In wake, the baby’s eyes are often open, movements are more frequent, and the REMs are due to volitional saccades rather than the spontaneous and often alternating REMs of active sleep. Despite the brief spontaneous extremity and facial muscle movements seen in active sleep, the general EMG tone in active sleep is low, whereas it can be high or variable in wake. The breathing pattern in both wake and active sleep is irregular. The EEG activity during different sleep stages can be helpful in sleep staging (see Table 7.2).
The EEG activities in wake and active sleep are similar. Beginning at ˜35 weeks CA, activité moyenne, a continuous, low- to moderate-amplitude (25-50 µV), mixed-frequency (predominantly 4-7 Hz) background becomes the primary activity during wakefulness and active sleep. This activity is similar to the low-voltage irregular (LVI) pattern seen at earlier CA (see below) but slightly higher in amplitude. Mixed activity consisting of both high-voltage slow (HVS) and low-voltage polyrhythmic activity can also be seen in both wake and active sleep.
TABLE 7.1 Characteristics of wakefulness, active sleep, and quiet sleep
Wake
Active Sleep
Quiet Sleep
Indeterminant
Behavior
Eyes open
Frequent movement of the limbs, face, and body
Eyes closed
Face: smiles, grimaces, frowns, burst of sucking; Body: small digit or limb movements
Eyes closed
No body movements except startles, phasic jerks, sucking
Not meeting the criteria for active or quiet sleep
EEG
LVI, M
LVI, M, HVS (rarely)
HVS, TA, M
EOG
Saccades, pursuits
REMs
A few SEMs and a few dysconjugate movements may occur
No REMs
EMG, body movements
High, variable
Low
High
Respiration
Irregular
Irregular
Regular
Post-sigh pauses may occur
After an initial period of active sleep, babies generally then cycle into quiet sleep, though the order of state transitions can be variable early in life. In quiet sleep, the eyes are closed and no body movement is seen, except occasional startle responses and phasic jerks. Sucking behavior can occur. Breathing is regular with occasional pauses after longer exhalations (post-sigh pauses). The EMG tone is relatively high but lacks the facial and limb movements of REM/active sleep. Unlike wake and active sleep, no REMs occur. EEG during quiet sleep in full-term infants consists primarily of continuous 50-150 µV delta frequency activity (0.5-4 Hz) known as HVS.
The EEG patterns in wake, active sleep and quiet sleep depend on the CA. In infants who have developmental abnormalities or brain injuries, the EEG pattern may suggest an earlier CA than the patient’s chronologic age, and EEG is an important tool for evaluating the location and severity of such problems as well as the prognosis. It is thus critically important to know the CA, whether from the mother’s records or ultrasound dating of fetal age. Likewise, as the child grows and develops, EEG patterns change with brain development, and the EEG can only be interpreted correctly by knowing the age of the patient and how the observed patterns compare to norms at that specific developmental stage. To evaluate the EEG activity in neonates and young children, it is essential that all stages of wake and sleep be recorded (if possible) and technicians will typically record at least 1 hour to ensure that the study shows examples of each state.
TABLE 7.2 EEG patterns used in infant sleep staging
EEG Pattern
Activity
Low-voltage irregular (LVI)
Low voltage (14-35 µV), little variation
Theta (5-8 Hz) predominates
Slow activity (1-5 Hz) is also present
Tracé alternate (TA)
Bursts of high-voltage slow waves (1-3 Hz) with superimposed rapid low-voltage sharp waves (2-4 Hz) alternating with low-voltage mixedfrequency activity lasting 4-8 seconds
7.5: Active sleep is marked by rapid eye movements (REM) and random spontaneous movements of arms, legs, and facial muscles. The EEG shows a moderate-amplitude mixed-frequency pattern known as activité moyenne, which is similar to that seen in wake. EMG tone is low, and breathing is irregular. Quiet sleep has no eye moments and only sporadic limb jerks, though sucking can occur. Breathing is more regular, and EMG tone is higher than in active sleep. EEG shows continuous high-voltage delta activity.
ONTOGENY OF THE NORMAL EEG
Body movements and brainstem electrical activity are present at ˜10 weeks CA, and cerebral cortical activity can be identified at 17 weeks CA. Rhythmic cycling body movements begin at 20-24 weeks CA.6 Bursts of mixed HVS waves and low-voltage 8-14 Hz activity are separated by 20- to 30-second intervals of low-voltage, nearly isoelectric background. This EEG activity occurs in an asynchronous fashion over the two hemispheres and is usually accompanied by irregular respiration and irregular eye movements. This discontinuous EEG pattern is often referred to as tracé discontinu (Fig. 7.1). Since sleep associated with tracé discontinu and other premature patterns cannot be classified as either quiet or active sleep at this CA, the terms indeterminate sleep and transitional sleep are sometimes used.
Between 27 and 30 weeks CA, the EEG is usually discontinuous, and background activity is asynchronous. With increasing age, the periods between bursts become shorter. Central and temporal sharp wave transients (see Figs. 7.2 and 7.3) are common features and not considered abnormal at this CA. Posterior predominant delta waves with superimposed 14-24 Hz activity called delta brushes appear (Fig. 7.2). During quiet sleep, the EEG is discontinuous and eye movements are rare. During active sleep, continuous delta or theta-delta activity predominates. Cardiac and respiratory rhythms are more regular and apparent during quiet sleep than during active sleep.
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