10 Normal Pediatric EEG

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10

Normal Pediatric EEG

Ann M. Bergin and Blaise F. D. Bourgeois

Summary

This chapter provides an overview of the developmental changes in the pediatric EEG from early prematurity through adolescence. The early development of recognizable sleep–wake cycles in the premature infant, the changes that occur around term and the maturation of the EEG in the awake, drowsy, and sleep states are described. Changes in response to routine activation procedures are also described. Figures are provided throughout the text. Discussion of common variant patterns observed in childhood is also provided.

Key Words: Child; development; EEG; normal variant; sleep–wake cycles.

1. INTRODUCTION

From the first detectable EEG tracings in the extremely premature infant, to the mature EEG of the 18-yr-old subject, the pediatric EEG undergoes enormous changes in parallel with the great increase in size and complexity of the brain and its connections. Characteristic pat- terns of activity are observed at various stages during normal development. These patterns emerge, wax, and wane during a broadly predictable time span. Their persistence beyond the expected period may be an indicator of dysmaturity or injury. Recognition of the normal developmental progression and deviation from normal patterns is essential for identifying, understanding, and predicting recovery from injury.

2. NEONATAL PERIOD

The patterns observed in the neonatal EEG and the significance attributed to them depends on the conceptional maturity of the infant. Therefore, to evaluate the neonatal EEG, the reader must know the conceptional age of the infant (duration in weeks since last menstrual period/beginning of pregnancy), in addition to the postnatal age. Patterns observed also depend on the infant’s state of arousal, and this should also be noted. The EEG patterns are evaluated in light of these conditions.

2.1. Premature Infants 2.1.1. Less Than 29 Wk

The most striking feature of the early premature EEG is the discontinuity of activity.

Bursts of high-voltage, predominantly delta activity, mixed with other frequencies and sharp

waves, are interspersed with periods of low-voltage quiescent recordings. Interburst intervals

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may be prolonged, up to 90 s or more, whereas active bursts are generally shorter, but may last up to 1 min. This pattern is described as trace discontinu (Fig. 1). At this early stage, there is virtually complete synchrony between the hemispheres. The EEG is invariant with clinical sleep or wakefulness, or with stimulation. The bursts of activity are predominant in the parasagittal and occipital areas, with relative inactivity in the temporal areas. Specific gesta- tional features observed at this stage may include monomorphic occipital theta or delta activity, occurring in bursts lasting up to 5 or 6 s, sharp theta in the occiput of premature infants (STOP) (Fig. 2), and delta brushes (beta–delta complexes) initially confined to the Rolandic and occipital areas.

2.1.2. Twenty-Nine to 32 Wk

At this age, the EEG remains for the most part discontinuous, although the average dura- tion of the interburst interval decreases (maximum ~60 s). Previously synchronous bursts of activity are now commonly asynchronous. This will persist, especially in quiet sleep (QS), until term and briefly beyond, during trace alterant. Brief periods of continuous activity cor- relate with active sleep (AS; rapid eye movement [REM] sleep) and irregular respirations, the earliest phase of differentiation of sleep–wake cycles. Specific gestational features include delta brushes that are more prominent in Rolandic, occipital, and parietal areas (Fig. 3).

Bursts of higher voltage, sharply contoured theta activity become more common in the mid- temporal regions (temporal theta bursts).

2.1.3. Thirty-Three to 36 Wk

At this stage, cyclic state changes between wakefulness, AS and QS become more easily defined, and the relationship between these electrical states and the attendant respiratory (irregular respiration in waking and AS; regular in QS) and musculoskeletal (clonic chin movements in QS; REM in AS) patterns become more consistent. The EEG background is a more continuous mix of theta and delta activity in waking and AS, with continuing cycling through periods of trace discontinu. The infant now responds to stimulation with diffuse attenuation of background activity (Fig. 4). Temporal theta bursts give way briefly (33–34 wk) to temporal alpha bursts before largely disappearing by 34 to 35 wk. Delta brushes persist and become more clearly associated with QS (Fig. 5). Sharp waves occur predominantly in central and temporal areas. Positive temporal sharp waves may occur singly or in runs, unilaterally or synchronously in both hemispheres. Toward 36 to 37 wk, frontal sharp waves (encoches frontales; Fig. 6), sometimes associated with rhythmic frontal delta activity (Fig. 7), become more prominent, and sharp waves in other areas wane in frequency.

2.2. Term Infants

Sleep–wake cycles are now fully developed. The waking record is a continuous mixture of

frequencies. Infants at this stage move directly from waking into AS, characterized by two

patterns of activity (mixed-frequency AS [Fig. 8], and low-voltage irregular sleep [Fig. 9]),

both associated with irregular respiratory pattern and REM. QS is associated with two pat-

terns on EEG, trace alternant (Fig. 10), which persists to 46 wk conceptional age, and with

high-voltage slow pattern (Fig. 11), both of which are associated with regular respiratory pat-

tern and absence of eye movements. Frontal and temporal sharp transients persist, observed

predominantly in QS, but wane by 44 wk conceptional age. Interhemispheric synchrony is

complete in waking and virtually complete in sleep.

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Fig . 1. T wenty-six weeks gestation. T race discontinu. LE-RF , left e yelid to reference; RE-RF , right e yelid to reference; Chn-RF , chin to reference; LF , lo w frequenc y f ilter; HF , high frequenc y f ilter; Rsp, respiration.

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Fig . 2. T wenty-se v en weeks gestation. Sharp theta in the occiput of premature inf ants (ST OP).

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Fig . 3. Thirty weeks gestation. Delta brushes, prominent in the parietal areas. LUE, left under e ye; RAE, right abo v e e ye; RESP , respiration.

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Fig . 4. Thirty-four weeks gestation. Startle, producing arousal with dif fuse attenuation of background. LOC, left outer canthus; R OC, right outer canthus; Resp, respiration.

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Fig . 5. Thirty-four weeks gestation. Occipital delta and delta brushes. RESP , respiration; LUE, left under e ye; RAE, right abo v e e ye.

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Fig . 6. Thirty-six weeks gestation. Frontal sharp w av es (encoches frontales).

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Fig . 7. Thirty-six weeks gestation. Frontal sharp w av es and rhythmic frontal delta.

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Fig . 8. T erm. Acti v e sleep, mix ed-frequenc y pattern (note irre gular respirations). RESP , respiration; LUE, left under e ye; RAE, right abo v e e ye.

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Fig . 9. T erm. Acti v e sleep, lo w-v oltage irre gular pattern. RESP , respiration; LUE, left under e ye; RAE, right abo v e e ye.

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Fig . 10. T erm. Quiet sleep, trace alternant pattern. RESP , respiration; LUE, left under e y e; RAE, right abo v e e ye.

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Fig . 11. T erm. Quiet sleep, high-v oltage slo w pattern. Rsp, respiration; LF , lo w frequenc y f ilter; HF , high frequenc y filter; LE-RF , left e ye to reference; RE-RF , right e ye to reference; Chn-RF , chin to reference.

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2.2.1. Infancy (<1 Yr)

With the end of the neonatal period (after 6-8 wk of age), trace alternant and frontal sharp waves are no longer observed in the healthy infant. In the awake state, an early, often poorly sustained, poorly reactive posterior dominant rhythm of three per second is first observed at 3 mo of age, and often increases to four per second at 4 mo (Fig. 12). Reactivity to eye clo- sure emerges quickly. The posterior dominant rhythm may be up to 6 to 7 Hz by 12 mo of age (Fig. 13). The voltage of the dominant rhythm varies from 30 to 40 µV, up to 100 µV or higher in the first year. The waking background activity is dominated by delta frequencies throughout the first year, but there is a steady increase in the amount of theta activity present.

Central theta activity of 4 to 5 Hz may be observed as early as 3 mo (Fig. 14), is usual by 6 mo, and faster (?) rhythms up to 8 Hz are observed in the central/Rolandic areas by 12 mo.

Activation by photic stimulation is most likely to produce a driving response in the lower theta frequencies.

After the first to second month, infants move from wakefulness into QS (Fig. 15), instead of directly into AS. The drowsy pattern is characterized by nonspecific slowing and increase in amplitude in the first 6 mo. Thereafter, drowsiness is manifest by an increase in diffuse, highly synchronous and rhythmic, theta activity (hypnagogic hyper- synchrony). Sleep spindles develop by 3 mo of age, although fragmentary forms may be observed shortly after term (Fig. 16). Spindles in infancy are typically comb-like, with rounded positive and a sharper negative component. They increase to a maximum dura- tion (up to 10 s) at approx 6 mo of age, and are maximal in the central and parietal areas, rather than at the midline, at this age. They are commonly asynchronous. Vertex waves appear between 3 and 5 mo. They are broader, and less sharply contoured than later in childhood.

2.2.2. Early Childhood (>1 to 3 Yr)

The posterior dominant rhythm increases in frequency from 6 to 7 Hz in the second year to 7 to 8 Hz in the third year, and the blocking response to eye opening is now robust (Fig. 17).

As in adults, the dominant rhythm may be of greater amplitude in the nondominant hemi- sphere. The difference should not be greater than 50%. In the waking background, delta activity remains prominent and may be observed diffusely or shifting in position throughout the record. There is a relative increase in the amount of theta activity, and this is visually the most striking frequency at this age. Throughout childhood, waking theta activity is prominent, often shifting in prominence from side to side. Children of this age are usually unable to cooperate with hyperventilation, but occasionally sobbing may induce diffuse slowing caused by a hyperventilation effect (Fig. 18). Occipital driving response to photic stimulation is still more likely at slower stimulation rates.

With drowsiness, diffuse, high-voltage, rhythmic theta (3–5 Hz) appears, mainly in the parasagittal areas. It is typically continuous, but may appear as discrete bursts in some chil- dren. It is often also present at arousal (hypnagogic and hypnopompic hypersynchrony) (Fig. 19). As the child progresses into sleep, diffuse irregular slow activity (1–3 Hz) develops, mixed with medium voltage theta activity. Slow activity has a maximal amplitude in the occipital leads (Fig. 20). Vertex sharp waves appear, which are now of higher voltage and more sharply contoured than previously. Runs of vertex sharp waves may occur (Fig. 21).

Spindles, usually 12 to 14 Hz, may have a wider field, and are mostly synchronous by 2 yr of age.

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Fig . 12. F our months. F our per second posterior rhythm; LF , lo w frequenc y f ilter; HF , high frequenc y f ilter .

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Fig . 13. T w elv e months. Six per second reacti v e posterior dominant rhythm; LUE, left under e ye; RAE, right abo v e e ye.

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Fig . 14. F our and a half months. Fi v e per second central acti vity , four per second posterior rhythm; LF , lo w frequenc y filter; HF , high frequenc y f ilter .

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Fig . 15. One month. Quiet sleep. RESP , respiration; LUE, left under e ye; RAE, right abo v e e ye.

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Fig . 16. Three months. Asynchronous sleep spindles; LF , lo w frequenc y f ilter; HF , high frequenc y f ilter .

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Fig . 17. Three years. Reacti v e posterior dominant rhythm in the alpha range (8/s); LUE, left under e ye; RAE, right abo v e e ye.

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Fig . 18. Three years. Sobbing produces hyperv entilation ef fect; LUE, left under e ye; RAE, right abo v e e ye.

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Fig . 19. Three years. Hypnagogic hypersynchron y with dro wsiness; LUE, left under e ye; RAE, right abo v e e ye.

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Fig . 20. Three years. Sleep— spindles with frontal maximum, delta with posterior maximum; LUE, left under e ye; RAE, right ab ove ey e.

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Fig . 21. Three years. Sleep— V w av e and run of V w av es (transv erse montage). F ourteen per second spindle with v erte x maximum; LUE, left under e ye; RAE, right abo v e e ye.

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Normal Pediatric EEG 165

2.2.3. Preschool Age (>3 to 6 Yr)

At this age, the posterior basic rhythm consistently reaches alpha frequency. It is still of high amplitude, often greater than 100 µV. Throughout early childhood, low voltage background (<30 µV) is abnormal. Posterior slow waves of youth emerge at this age (Fig. 22). These are 1.5- to 3-Hz waves, maximal in the occipital region. They are intermixed with posterior alpha, and, at times, fused slow waves can resemble occipital sharp waves, although lacking typi- cal morphology and after-coming slow wave. Posterior slow waves, in common with the pos- terior dominant rhythm, block with eye opening. This pattern persists throughout childhood and adolescence, disappearing in young adulthood. Rolandic mu rhythm may be apparent at this stage, often shifting from side to side. Children can now cooperate with hyperventilation.

Hyperventilation produces prominent diffuse slowing to 3 to 5 Hz, which may be more apparent on the left initially, although becoming symmetrical (Fig. 23). This response is enhanced by fasting. It may persist beyond apparent cessation of hyperventilation if the child continues to breathe deeply. Intermittent photic stimulation is still associated with a driving response at stimulation rates less than 8 Hz.

Drowsiness is often still associated with hypersynchrony, as described in Section 2.2.2.

Vertex waves are increasingly sharply contoured. Spindles are now maximal in the midline, at 14 Hz, decreasing to 10 Hz with deeper sleep. Sleep-related slowing is still maximum in amplitude posteriorly. Positive occipital sharp transients of sleep (POSTS) are not yet expected, and, if present, are poorly formed. Frontal arousal rhythm in the theta range may be observed, but is more common later.

2.2.4. Late Childhood (>6 to 12 Yr)

Posterior dominant rhythm reaches 10 Hz by 10 yr of age, and reaches its maximum amplitude before that age. Posterior slow waves are prominent, and may be asymmetric, with higher amplitude on the right, as with the posterior dominant rhythm. Medium volt- age semi-rhythmic frontal theta activity may be observed in healthy children at this age, and may persist into young adulthood (Fig. 24). There is increasing prominence of the mu rhythm (up to 15–16 yr) (Fig. 25). Lambda waves may be observed posteriorly with saccadic eye movements in response to patterned visual stimulus. Hyperventilation still produces high-voltage slowing (1.5–4 Hz). Intermittent photic stimulation now stimulates driving at 6 to 16 Hz.

Hypnagogic hypersynchrony is disappearing, and is rare after the age of 6 yr. The drowsy pattern at this age is gradual alpha dropout, with increasing amounts of theta and delta activity.

Vertex sharp waves are still prominent, with large amplitude, and may have asymmetric field over the midline. Spindles are now disposed anteriorly over the frontal midline, and typically last less than 1 s. Fully developed POSTS are observed for the first time (Fig. 26), and other sleep patterns, such as 14- and/or 6-Hz positive sharp waves are more common.

2.2.5. Adolescence (>12 to 18 Yr)

At this age, the EEG begins to resemble the adult EEG more closely, as the amount of

underlying delta activity wanes completely (Fig. 27). The amplitude of the posterior domi-

nant rhythm also declines gradually, although it remains higher than in adults throughout this

period in many children. The mu rhythm reaches its maximum prominence at 15 to 16 yr,

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Fig . 22. Six years. Posterior slo w w av es of youth; LUE, left under e ye; RAE, right abo v e e ye.

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Fig . 23. Six years. Hyperv entilation— dif fuse slo wing; LUE, left under e ye; RAE, right abo v e e ye.

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Fig . 24. Nine years. Frontal theta. PHO-STM, photic stimulation; LUE, left under e ye; RAE, right abo v e e ye.

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Fig . 25. T w elv e years. Mu rhythm on right, responds to mo v ement of left hand; LUE, left under e ye; RAE, right abo v e e ye.

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Fig . 26. T w elv e years. Sleep— positi v e occipital sharp transients of sleep; LUE, left under e ye; RAE, right abo v e e ye.

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Fig . 27. Sixteen years. A w ak e EEG, little delta acti vity remains; LUE, left under e ye; RAE, right abo v e e ye.

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The drowsy pattern is now mature, with alpha dropout, and replacement with a low- voltage mixture of slow and fast activity. Prominent V waves remain, still sharper in con- tour than in adulthood, but less so than earlier in childhood. Spindles are mature. POSTS are abundant and mature. They may occur in semiregular runs and resemble an occipital rhythm. Fourteen- and/or 6-Hz positive sharp waves are not uncommon in sleep.

3. NORMAL VARIANT PATTERNS

3.1. Phantom Spike Wave (Six Per Second Spike Wave Complex)

This pattern looks like a miniature version of the typical three per second spike wave of typical absence. The spike component is often unimpressive (hence, the “phantom spike”

designation). Although it may be diffuse, at times the distribution of this phenomenon and the state in which it occurs allow discrimination of two forms. It occurs in waking, at rel- atively higher amplitude and the anterior head regions in male subjects (Fig. 28), and, in female subjects, is typically occipital, of lower amplitude, and occurs in drowsiness. The discharge usually lasts 1 to 2 s, but may persist longer. It is usually symmetrical, but may have a lateral predominance. This pattern is present in adolescence and adulthood. Unlike more pathological spike wave patterns, it tends to disappear as sleep deepens. Although here described as a normal variant, the status of phantom spike wave as denoting increased risk of seizure has been controversial, particularly the anterior/frontal form, which some authors consider more likely to be associated with other epileptiform findings and with epileptic seizures.

3.2. Fourteen- and 6-Hz Positive Spikes (Fig. 29)

This benign pattern is first observed in early childhood, achieves maximum frequency in the adolescent age group, and wanes thereafter. It is observed in drowsiness and sleep, has a broad field, but is usually maximum in the posterior temporal area. At times, the 14-Hz or the 6-Hz component may predominate. The 14-Hz component may be observed more frequently in middle childhood or adolescence, the 6-Hz pattern in younger children and young adults.

The discharge may last 1 to 2 s. It often occurs independently on both sides. Because the amplitude is low, it is best observed with referential montages, which, in general, use longer interelectrode distances.

3.3. Rhythmic Temporal Theta Bursts of Drowsiness (Psychomotor Variant) (Fig. 30) This is a rare pattern. It is observed in adolescents and adults. It occurs in drowsiness, and, similar to other benign patterns, disappears as sleep supervenes. It may occur bilaterally or independently. It begins with rhythmic sharply contoured, often notched or flat-topped theta waves in the mid-temporal area. The amplitude and field increase, but there is no evolution in frequency or of waveform. These last features help distinguish this pattern from true seizure. This pattern is no longer thought to denote increased risk of seizure or epilepsy.

3.4. Alpha Variant Patterns 3.4.1. Slow Alpha Variant

This is most likely the result of the superimposition of two alpha rhythms producing the sudden appearance of a notched posterior rhythm at half the previous frequency. Similar to the individual’s usual alpha frequency, it is blocked by eye opening. This change may occur in trains during normal alpha activity. It may be more likely to occur in drowsiness.

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Fig . 28. F ourteen years. Phantom spik e w av e, “w aking, at relati v ely higher amplitude and the anterior head re gions in males” v ari- ant ( see te xt). Note Fp1 and F3 electrodes (a v erage referential montage).

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Fig . 29. Thirteen years. F ourteen- and 6-Hz positi v e spik es. Note P7 and P8 electrodes (a v erage referential montage).

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Fig . 30. Se v enteen years. Rhythmic temporal theta b ursts of dro wsiness (“psychomotor v ariant”); LUE, left under e ye; RAE, right abo v e e ye.

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3.4.2. Fast Alpha Variant

This typically occurs on first eye closure, when a beta-range activity occurs in the posterior regions, which attenuates with eye opening. This is usually replaced within a second or two by the individual’s usual alpha frequency. This fast occipital activity has been described as the “squeak” phenomenon. Both the slow and fast alpha variants are normal physiological phenomena.

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Daly DD, Pedley TA. Current Practice of Clinical Electroencephalography. 2nd ed. Lippincott-Raven, Philadelphia, PA, 1997.

Neidermeyer E. Maturation of the EEG: development of waking and sleep patterns. In:

Electroencephalography. Basic Principles, Clinical Applications and Related Fields, 4th ed.

(Neidermeyer E, Lopes da Silva F, eds). Williams & Wilkins, Baltimore, MD, 1999.

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REVIEW QUESTIONS

1. To accurately assess the preterm EEG, all of the following facts must be known except:

A. Chronological age.

B. Conceptional age.

C. Physiological data (EKG, respirations, etc.).

D. State of infant (awake, asleep).

E. Time of last feed.

2. Which of the following statements is true regarding the EEG in premature infants?

A. EEG response to stimulation is typically observed as early as 26 wk.

B. The EEG of the 30-wk premature infant is mostly synchronous.

C. Cyclic state changes begin to correlate with changes in respiratory rate, heart rate, and eye movements at 34 to 35 wk.

D. Frontal sharp waves are always abnormal at 36 wk.

E. At 36 wk the infant responds to stimulation with high voltage synchronous activity.

3. At term:

A. Reactive posterior dominant activity is observed with eye closure.

B. Discontinuity of EEG is no longer present in any state.

C. Asynchrony of EEG is no longer present in any state.

D. Frontal sharp waves are normal in the first month.

E. Infants fall directly from waking into QS.

4. The posterior dominant rhythm in childhood:

A. Is poorly reactive to eye closure throughout early childhood.

B. Rarely reaches alpha frequency before 8 yr.

C. May exhibit voltage of greater than 100 µV in the first year.

D. Should never by asymmetrical.

E. Is commonly of low voltage (<30 µV).

5. As the EEG matures through childhood:

A. Theta activity is unusual in the first year.

B. Delta activity predominates in the first year.

C. Frontal theta activity is never normal.

D. Theta activity is synchronous throughout childhood.

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6. The following are true of sleep spindles except:

A. They are first observed at 3 mo of age.

B. They may be prolonged up to 10 s in the first year of life.

C. They are synchronous at 2 yr.

D. They remain comb-shaped until adolescence.

E. They are central and parietal in infancy and frontal midline by late childhood.

7. In childhood, during sleep:

A. Vertex waves are first observed at 1 mo of age.

B. Slow activity in sleep is maximal in the frontal area.

C. Vertex sharp waves may be asymmetrical.

D. POSTs are normally observed early childhood.

E. Hypnagogic and hypnopompic hypersynchrony remain common in adolescence.

8. Activation procedures:

A. There is no response to photic stimulation before 2 yr of age.

B. Younger children demonstrate a driving response at higher flash frequencies than older age groups.

C. Slowing associated with hyperventilation may be initially asymmetrical.

D. High-voltage slowing with hyperventilation is exacerbated by hyperglycemia.

9. Normal variants:

A. The slow alpha variant is more likely to be associated with pathology than the fast alpha variant.

B. Alpha variant patterns are alpha patterns observed in posterior head regions in sleep.

C. Phantom spike wave pattern occurring in the occipital areas is more likely to be abnormal than that occurring in the frontal areas.

D. Fourteen- and/or 6-Hz positive sharp waves are high-amplitude phenomena, usually in the posterior temporal area.

E. Rhythmic temporal theta bursts are distinguished from seizure by the absence of change in frequency and waveform.

10. In pediatric EEG:

A. Lambda waves are occipital sleep phenomena related to REM movements.

B. Mu activity is blocked by movement of the contralateral hand.

C. Posterior slow waves of youth, unlike posterior dominant activity, do not block with eye opening.