Sleep Staging in Infants and Children

Chapter Points

• For infants younger than 2 months of age (48 wk CA—time since conception), sleep may be staged according to the rules of Anders, Emde, and Parmelee.

• Sleep staging in infants depends on behavioral observations because wake and sleep may have similar EEG patterns.

• In infants, AS corresponds to stage R and QS to NREM sleep.

• In term infants, entry to sleep via AS is the norm and AS composes about 50% of sleep.

• Timing of appearance of characteristic EEG patterns of sleep (age postterm):

Sleep spindles 2–3 mo

K complex 4–6 mo

Slow wave activity 4–5 mo

• By age 6 months, stages N1, N2, and N3 can usually be scored (sometimes younger).

• The DPR is the dominant rhythm over the occipital regions in relaxed wakefulness with eyes closed. DPR is attenuated by eye opening.

• The frequency of the DPR increases with age. The frequency of DPR increases from around 4 Hz at 4 months to 8 Hz by age 8 years in most individuals (adult range 8–13 Hz).

• Unique EEG patterns that are used to identify stage N1 in children include rhythmic anterior theta (5–7 Hz over frontal derivation) and hypnagogic hypersynchrony (high-voltage 3–4.5 Hz activity), maximal in frontal and central derivations.

The American Academy of Sleep Medicine (AASM) scoring manual 1,2 provides new scoring rules for infants older than 2 months and children. However, previously, the terminology for sleep staging for the newborn infant used different terminology, and sleep was staged according to the sleep scoring rules of Anders, Emde, and Parmelee.³ These have been widely used for infants in the past and can still be used for scoring sleep in infants younger than 2 months of age. The gestational age is the time from conception to birth (estimated from last menstrual period). The conceptional age (CA) is gestational age + time in weeks since birth. If one assumes term means 40 weeks, then the AASM rules would apply at 48 weeks’ CA. For an infant born at 36 weeks, the AASM rules would apply at age 3 months (CA 48 wk).

Bipolar Electroencephogram Recording

In some of the tracings to follow, bipolar electroencephalogram (EEG) montages are illustrated using frontal (F₃, F₄, F₇, and F₈), central (C₃ and C₄), parietal (P₃, P₄, P₇, and P₈), and occipital (O₁ and O₂) electrodes (Fig. 5–1). Some of these electrodes are used in standard sleep recording and others are not. Clinical EEG is discussed in detail in Chapter 27. However, for reference, EEG electrode positions are illustrated in Figure 5–1.

FIGURE 5–1 Electroencephalography (EEG) electrode positions. C = central; F = frontal; Fp = frontopolar; O = occipital; P = parietal; T = temporal.

Sleep in the Premature Infant and Infants Younger Than 48 Weeks CA

Sleep Stages in the Newborn

Infant sleep is divided into active sleep (AS; corresponding to rapid eye movement [REM] sleep), quiet sleep (QS; corresponding to non–rapid eye movement [NREM] sleep) and indeterminant sleep, which is often a transitional sleep stage. Unlike adults, infants transition from wake to sleep via AS. The characteristics of each stage are listed in Table 5–1: The EEG patterns associated with wake, QS, and AS are discussed later.¹–⁶ The sleep of premature infants differs from that of term infants (CA 38–40 wks). The timing of the appearance of different EEG patterns characteristic of different sleep stages is illustrated in Figure 5–2. Behavioral observations are essential for sleep staging because EEG patterns may be associated with more than one state.

TABLE 5–1

Characteristics of Sleep Stages in Term Infants³

	WAKE	ACTIVE SLEEP	QUIET SLEEP	INDETERMINANT
EEG	LVI or mixed	LVIM, HVS rarely	TA or HVSM rarelyPremature: TD	Not meeting criteria for QS or AS
EOG	Eyes open	Eyes closed, horizontal REMs	Eyes closedLittle or none
Chin	Phasic	Low tonic between movements	High tonic
Breathing	Irregular	Irregular, some postsigh pauses	RegularDeep and slow
Body movements	Calm or active with eyes open	Squirming, sucking, grimacing	Few, peaceful
Body movements	Calm or active with eyes open	Body: small digit or limb movements	Sucking can occur

AS = active sleep; EEG = electroencephalogram; EOG = electromyography; HVS = high-voltage slow; LVI = low-voltage irregular; M = mixed; QS = quiet sleep; REMs = rapid eye movements; TA = tracé alternant; TD = tracé discontinue.

EEG Patterns

The EEG patterns of sleep in the pre-term and term infant are ³

1. Tracé discontinue (TD): A discontinuous pattern consisting of high-voltage bursts with sharp features separated by long, dramatically flat EEG periods of 10 to 20 seconds (Fig. 5–3). TD is seen at or before 30 weeks CA (see Fig. 5–2) and is the EEG pattern of QS in that age group.

FIGURE 5–3 Tracé discontinue. Bursts of high-voltage activity alternate with long periods of flat EEG activity. ECG = electrocardiogram; LUE = left under eye electrode; RAE = right above eye electrode. *From Libenson MH: Practical Approach to Electroencephalography. Philadelphia: Elsevier Saunders, 2010, p. 307.*

2. Tracé alternant (TA): A discontinuous pattern (Figs. 5–4 and 5–5) that characterizes the QS of newborns after about 30 weeks CA (see Fig. 5–2). Bursts of mixed activity of 2 to 8 seconds are interspersed with periods of flatter EEG. The bursts are composed of high-voltage slow waves superimposed with rapid low-voltage sharp waves. There is a continuum between TD and TA, but in general, in TA, the high and low periods have fairly equal durations and the bursts do not have full bilateral synchrony. In TD, the flat is very flat and the bursts are very high voltage and have synchrony.

FIGURE 5–4 EEG patterns of the newborn infant (30 sec tracings). HVS = high-voltage slow; LVI = low-voltage irregular; M = mixed. Reproduced with permission from Anders T, Emde R, Parmelee A: A Manual of Standardized Terminology, Techniques and Criteria for Scoring of Stages of Sleep and Wakefulness in Newborn Infants. Los Angeles: Brain Information Service, UCLA, 1971.

FIGURE 5–5 Tracé alternant (TA; quiet sleep in a 1-mo-old). Note that the quiet portions are not as flat or as long as in tracé discontinue (TD). Also, the higher-amplitude burst portions are longer and less synchronous. ECG = electrocardiogram. *From Libenson MH: Practical Approach to Electroencephalography. Philadelphia: Elsevier Saunders, 2010, p. 308.*

3. Low-voltage irregular (LVI): Continuous low-voltage mixed-frequency with prominent delta and theta rhythms and little variation. Voltage (14–35 µV), theta rhythm predominates (see Fig. 5–4).

4. High-voltage slow (HVS) pattern: Continuous, irregular mixed frequencies with higher voltages (50–100 µV) and more prominent delta frequencies (see Fig. 5–4).

5. Mixed pattern (M): Similar to LVI but with slightly higher voltages and more delta activity. Mixture of HVS and low-voltage polyrhythmic activity (see Fig. 5–4).

Premature Infants

In premature infants with a CA less than 30 weeks, QS usually shows a pattern of TD.3,4 The pattern of TD is characterized by electrical quiescence between bursts of high-voltage activity. In contrast, TA is characterized by a lesser reduction in amplitude between periods of higher-amplitude activity. Another difference between TA and TD is that delta brushes (fast waves of 10–20 Hz) are superimposed on the delta waves in TD. As the infant matures, delta brushes disappear and the TA pattern replaces TD. Finally, at term, the EEG of QS is characterized by an HVS pattern. The EEG of AS in premature infants younger than 30 weeks may also show TD but later is typically LVI or M. The EEG pattern of wake and sleep is similar and states are distinguished by sustained eye closure (sleep) and open eyes (wake).

Term Infants

Wakefulness is characterized by crying, open eyes, and feeding. Non-nutritive sucking commonly continues during sleep. Sleep is often defined by sustained eye closure. The epochs during the transition from definite AS to QS are often scored as indeterminant sleep.

AS is characterized by grimacing, sucking, an LVI EEG pattern, REMs, and low electromyogram (EMG) activity (Fig. 5–6; see also Table 5–1). Breathing is irregular in AS. QS (Fig. 5–7) is characterized by a peaceful infant with non-nutritive sucking and regular deep respiration. The EEG may show TA at early ages and HVS later. No or few eye movements are noted and the chin EMG is tonic and high.

FIGURE 5–6 Active sleep. The EEG shows an LVI pattern. The respiration channel shows irregular respiration with a respiratory pause. The eye movement channel shows rapid eye movements. ECG = electrocardiogram. *Adapted from Libenson MH: Practical Approach to Electroencephalography. Philadelphia: Elsevier Saunders, 2010, p. 310.*

FIGURE 5–7 Quiet sleep showing an HVS EEG pattern in a term infant. *From Libenson MH: Practical Approach to Electroencephalography. Philadelphia: Elsevier Saunders, 2010, p. 306.*

Sleep Architecture

Newborn infants typically have periods of sleep lasting 3 to 4 hours interrupted by feeding, and the total sleep duration in 24 hours is usually 16 to 18 hours. They have cycles of sleep with a 45- to 60-minute periodicity with about 50% AS. In newborns, the presence of REM (AS) at sleep onset is the norm. In contrast, the adult sleep cycle is 90 to 100 minutes, REM occupies about 20% of sleep, and NREM sleep is noted at sleep onset.

After about 3 months, the percentage of REM sleep starts to diminish and the intensity of body movements during AS (REM) begin to decrease. The pattern of NREM at sleep onset begins to emerge. However, the sleep cycle period does not reach the adult value of 90 to 100 minutes until adolescence.7–¹²

As children mature, more typical adult EEG patterns begin to appear. The time of appearance is somewhat variable, but the values in Table 5–2 are typical. Sleep architecture in children is discussed in more detail inChapter 6.

TABLE 5-2

Age of Onset of Electroencephalographic Patterns

WAVE FORM	DESCRIPTION	AGE FIRST SEEN
Sleep spindles	12–16 Hz	2–3 mo
K complexes	Biphasic initial neg (up)	4–6 mo
K complexes	Deflection	4–6 mo
Slow wave activity	>75 µV p-p in frontal derivation	4–5 mo postterm
Slow wave activity	Frequency 0.5–2 Hz	4–5 mo postterm