ACNS Standardized EEG Terminology and Categorization for the Description of

Continuous EEG Monitoring in Neonates

Report of the American Clinical Neurophysiology Society

Critical Care Monitoring Committee

Tammy N. Tsuchida*, Courtney J. Wusthoff*, Renée A. Shellhaas, Nicholas S. Abend,

Cecil D. Hahn, Joseph E. Sullivan, Sylvie Nguyen, Steven Weinstein, Mark S. Scher,
James J. Riviello, Robert R. Clancy

Tammy N. Tsuchida, MD, PhD

Assistant Clinical Professor of Neurology and Pediatrics
Children's National Medical Center
George Washington University School of Medicine

Courtney J. Wusthoff, MD
Assistant Professor of Child Neurology
Stanford University School of Medicine
Lucile Packard Children's Hospital

Renée A. Shellhaas, MD, MS

Clinical Assistant Professor
Pediatrics & Communicable Diseases
University of Michigan, Ann Arbor, MI

Nicholas S. Abend, MD
Assistant Professor of Neurology and Pediatrics
Division of Neurology, The Children's Hospital of Philadelphia
Departments of Neurology and Pediatrics, The University of Pennsylvania School of
Medicine

Cecil D. Hahn, MD, MPH

Division of Neurology, The Hospital for Sick Children
Assistant Professor of Paediatrics (Neurology), University of Toronto
Associate Scientist, The Hospital for Sick Children Research Institute
Joseph E. Sullivan, MD
Assistant Professor of Neurology & Pediatrics
Director, UC San Francisco Pediatric Epilepsy Center
University of California San Francisco

Sylvie Nguyen The Tich, MD, PhD

Professor of Pediatrics
Child Neurology Unit
Laboratoire Ingenierie Systeme Automatises EA4094, LUNAM University Hospital
ANGERS

Steven Weinstein, MD
Professor of Neurology and PediatricsChildren's National Medical Center
George Washington University School of Medicine

Mark S. Scher, MD
Professor of Pediatrics and Neurology
Department of Pediatrics
Division Chief, Pediatric Neurology
Director, Rainbow Neurological Center, Neurological Institute of University Hospitals
Director, Pediatric Neurointensive Care Program/Fetal Neurology Program Rainbow
Babies and Children's Hospital University Hospitals Case Medical Center

James J. Riviello, MD
NYU Comprehensive Epilepsy Center
NYU Langone Medical Center
Director, Division of Pediatric Neurology
Professor of Neurology
Department of Neurology
New York University School of Medicine

Robert R. Clancy, MD
Professor of Neurology and Pediatrics
The University of Pennsylvania School of Medicine
The Children’s Hospital of Philadelphia

*These authors contributed equally to this manuscript.

Background:
Critically ill neonates are at high risk for adverse neurologic sequelae but the
bedside evaluation of a neonate’s neurologic status, especially cortical functioning, is
extremely limited. In such circumstances, continuous video EEG provides particularly
useful information about brain function and can identify electroencephalographic seizures
without clinical correlate.1, 2 For these reasons, continuous video EEG monitoring is a
useful tool in the intensive care nursery (ICN). The American Clinical Neurophysiology
Society (ACNS) has recently produced guidelines regarding methods and indications for
continuous EEG monitoring in neonates.3
A challenge in EEG monitoring of neonates is to understand the clinical
significance of various EEG patterns. In the adult ICU population, there has been
extensive debate, for example, regarding the importance of fluctuating rhythmic
patterns.4-7 The ACNS Critical Care Monitoring Committee has generated standardized
terminology of rhythmic EEG patterns in the critically ill in order to facilitate multicenter
collaborations to determine whether these patterns have clinical significance.8 Neonates
have distinctive EEG patterns that necessitate separate terminology.
This document is the consensus of experts to establish standardized neonatal EEG
nomenclature aimed at improving consistency and facilitating collaborative research.
Where evidence exists to support a particular definition, it is noted. For terms with
historically variable definitions, alternative nomenclature is referenced but a single
definition is proposed. We anticipate that future revisions will incorporate feedback and
emerging research building upon this initial effort. Many of the studies upon which these
criteria are based utilized routine-length EEG recordings and in this limited context,
values such as acceptable duration of interburst intervals have been offered. However,
greater variability may be expected in recordings of longer duration. Our hope is that this
document provides groundwork for collaboration to determine the clinical significance of
various EEG patterns in continuous monitoring of the critically ill neonate.

DETAILS TO BE REPORTED

Characterization of a 24 hour period of continuous video EEG recording should include:

(Box 1)
1. Documentation of patient’s postmenstrual age (PMA= gestational age, measured from
the time of the last menstrual period + chronological age) at the time of recording.9a
a) Term = 37 up to 44 weeks PMA
b) Preterm = less than 37 weeks PMA
c) Post term = 44 to 48 weeks PMA
2. Documentation of neuroactive medications at the time of recording. This includes
sedatives, hypnotics, anxiolytics, general anesthesia, and anti-epileptic drugs. An

a
We use the term PMA here in accordance with the American Academy of Pediatrics policy statement on
age terminology in the perinatal period. However, we recognize that historically, many seminal
investigations of EEG ontogeny calculated gestational age from the time of conception rather than the last
menstrual period. This has been traditionally termed conceptional age (CA).The LMP occurs about 2 weeks
before conception.
 ideal report would also document when these medications are administered during the
recording.
3. Documentation of the depth and duration of hypothermia during the recording, and
whether it is spontaneous or induced.
4. An ideal report would also document clinical changes that have the potential to
impact cerebral function. These would include sudden hemodynamic instability, rapid
changes in respiratory function or cardiorespiratory failure.
5. Documentation of the number of hours of recording that cannot be interpreted due to
technical problems.
6. Detailed characterization of the background EEG features during the first hour of
recording. Presence or absence of state changes must be included.
7. Characterization of one hour of background recording within each 24 hour period of
EEG monitoring.
8. Characterization of additional epochs of background when there are relevant changes.
Relevant changes include not only evidence for increasing encephalopathy but also
the new development of episodic state changes.
9. Documentation of seizure onset, seizure burden, and seizure resolution. When
present, specific note should also be made of the beginning and end of status
epilepticus.

The normal neonatal EEG evolves as the brain matures, reflecting both antenatal and
postnatal experiences. All else being equal, two healthy infants with the same PMA
should have very similar appearing EEG recordings. There should be no visible
differences between an EEG recorded from a 5 weeks chronological age infant born at 35
weeks EGA (PMA = 40 weeks) compared to a 1 week chronological age baby born at 39
weeks EGA (PMA is also 40 weeks). However, in contrast to the older child or adult, a
few weeks’ age difference can cause visible changes in normal EEG features. The
following text proposes nomenclature to describe normal and abnormal features of the
EEG in the preterm and term infant. Where relevant, it refers to the specific PMA at
which various features are seen. We focus specifically on normal state changes,
background features, graphoelements (or named neonatal EEG features), seizures, and
rhythmic or periodic patterns.

BEHAVIORAL STATE

Standardized descriptions of the behavioral state and sleep-wake cycling are particularly
useful in considering whether a neonatal record is normal or abnormal. Features of a full
term neonatal EEG and polysomnographic recording emerge over time in the premature
infant. A behavioral state is said to be present when features of that state are present for
one minute or longer (Box 2)

Awake

Term. A healthy term neonate is awake when the eyes are open and the EEG background
has continuous, low to medium voltage (25-50 µV peak-to-peak (pp))b mixed frequency
b
All voltages included in this manuscript refer to peak-to-peak (pp) values.
activity with a predominance of theta and delta and overriding beta activity.(Figure 1)
This is traditionally called activité moyenne, roughly meaning “average or medium” EEG
background activity. During wakefulness, term infants have irregular respirations and
there are spontaneous movements of the limbs and body.

Preterm. A healthy preterm infant is considered awake when the eyes are open. This
remains its premier clinical characteristic until 32-34 weeks PMA, when other
polysomnographic signs (irregular respiratory patterns, phasic or tonic chin EMG
activity, and the presence of small and large body movements) are also reliably
concordant with wakefulness. Brief portions of the awake EEG are continuous at 28
weeks PMA. The awake background is even more continuous by 32 weeks and
persistently continuous by 34 weeks and thereafter.

Sleep

Sleep in the neonate is classified as active, quiet, transitional, and indeterminate. Each
has distinctive EEG and polysomnographic features.

Active Sleep
Term. The healthy term neonate in active sleep has the eyes closed, intermittent periods
of rapid eye movements (REM), and irregular respirations with small and large body
movements. The EEG background shows activité moyenne, indistinguishable from that
of normal wakefulness.

Preterm. Tracé discontinu describes the normal discontinuous tracing encountered in

healthy preterm babies (Figures 1, 2a). This EEG pattern is characterized by bursts of
high voltage (50-300 µV pp) activity that are regularly interrupted by low voltage
interburst periods (< 25 µV pp).10 The duration of the low voltage interburst periods is
dependent on PMA, being longest in the youngest PMA infants. The bursts of EEG
activity have expected and recognizable constituents such as monorhythmic occipital
delta activity and other patterns that are described below. Tracé discontinu predominates
before 28 weeks PMA. Brief and inconsistent periods of continuous EEG activity occur
first in waking state and active sleep along with rapid eye movements (REM) at 25 weeks
PMA.11 Movements (face and body) in active sleep tend to be segmental myoclonus or
generalized myoclonic and tonic posturing. By 28-31 weeks PMA, there are some periods
with complete features of active sleep (eyes closed, REM, irregular respirations, body
movements and continuous EEG). After 34 weeks active sleep consistently has
continuous EEG activity.

Quiet Sleep
Term. In the healthy term neonate, quiet sleep is clinically characterized by eye closure,
absent REM, and scant body movements, except for occasional sucking activity or
generalized myoclonic “startles”. The quiet sleep EEG background near term, tracé
alternant, evolves from the less mature tracé discontinu in the preterm (Figures 1, 2b). It
shows the “alternating tracing” in which higher voltage bursts (50-150 µV pp), comprised
predominantly of delta activity and lasting roughly 4 to 10 seconds, alternate with
briefer, lower voltage (25-50 µV pp)12 interburst periods composed mostly of mixed theta
and delta activity. These interburst periods of tracé alternant, taken in isolation, greatly
resemble the characteristics of activité moyenne with its low to medium voltage, mixed
frequency activity. Tracé alternant gradually disappears with age and is minimal by 42
weeks and vanishes by 46 weeks. As tracé alternant fades, it is replaced in quiet sleep by
the more mature, fully continuous quiet sleep background comprised of non-stop, high
voltage (50-150 µV pp) delta and theta activity. Sleep spindles around 10-12 Hz first
appear within this continuous slow wave sleep pattern by 46 weeks PMA.

Preterm. In the very preterm neonate, most of the EEG background is discontinuous in
all behavioral states. With advancing PMA, wakefulness and active sleep are
distinguished from quiet sleep by greater periods of continuity. Tracé discontinu is the
defining feature of quiet sleep first emerging around 28 weeks PMA. By 34-36 weeks
tracé discontinu is seen only in quiet sleep. The amount of time with a tracé discontinu
pattern decreases with increasing PMA so that a term infant has rare, if any, periods of
tracé discontinu in quiet sleep.13 By 37-40 weeks, tracé alternant fully replaces tracé
discontinu as described above.

Transitional Sleep

In between states of waking, active sleep and quiet sleep, there are temporary transitional
periods in which typical features for a specific behavioral state are incomplete. These
transitional sleep states typically blend together clinical and EEG features of the original
and final behavioral states. Transitional sleep does not clearly satisfy the
polysomnographic and EEG background criteria for a specific state as defined above. For
example, in the transition from active sleep to quiet sleep, an infant might still show some
large body movement but deep regular respirations accompanied by an EEG that is
between activité moyenne and tracé alternant. This admixture of the two states is seen
until quiet sleep fully emerges and satisfies all the criteria for definite quiet sleep.
Transitional sleep can be thought of as a temporary period of indeterminate sleep, as
described below.

Indeterminate Sleep

Segments of the EEG in which the baby’s eyes are closed (indicating sleep) but in which
other clinical and EEG features do not permit definite assignment to active or quiet sleep
are designated as indeterminate sleep. These periods lack the anticipated features for
assignment to a unique sleep state. As above, transitional sleep is a temporary kind of
indeterminate sleep. Much of sleep is indeterminate in very preterm infants in whom
there is not a well established concordance between the EEG background and
polysomnographic variables. Only a small amount of total sleep time is indeterminate in
healthy term infants. A high percentage of total sleep time that is indeterminate would be
considered abnormal at term.

Sleep-wake cycling
Sleep-wake cycling is the pattern of alterations among behavioral states. Cycling is more
distinctive and easier to recognize in term babies, compared to preterm babies. It is also
easier to detect in long term recordings than brief routine tracings.11

Term. In the term infant, a complete sleep and waking cycle typically has a duration of
3-4 hours.14 An isolated sleep-only cycle typically lasts 40-70 minutes and progresses in a
somewhat orderly fashion. The awake term infant usually first falls into an active sleep
state. This is true until about four months after term equivalent age. Tracé alternant may
then appear in the first portion of quiet sleep and gradually be replaced by continuous
high voltage slow activity. Term neonates spend approximately 50-60% of the sleep
cycle in active sleep, 30-40% in quiet sleep and 10-15% in transitional sleep.

Preterm. The proportion of time spent in any state also varies by age.11, 15 The first
rudimentary evidence of sleep cycling can be seen at 25 weeks PMA. At 27-34 weeks
PMA, 40-45% is spent in active sleep, 25-30% in quiet sleep, and 30% in indeterminate
sleep. Beyond 35 weeks PMA, infants spend 55-65% of the time in active sleep, 20% in
quiet sleep and 10-15% in indeterminate sleep. The duration of a sleep cycle (first active
sleep, then transitional sleep and finally quiet sleep) is 30-50 minutes for neonates <35
week PMA and increases to 50-65 minutes beyond 35 weeks PMA.

Unspecified State Changes. In a sick infant with disruption of normal background

features, it may be difficult or impossible to identify definite specific sleep states.
However, some infants can still have state changes, defined as cycling between distinctly
different EEG patterns as indicated by the amount of background discontinuity, voltages
or electrical frequencies with at least one minute in each unspecified state.

EEG BACKGROUND

The constituents of normal neonatal EEG background evolve with PMA. In the
following section, the features of both normal and abnormal EEG backgrounds will be
defined. (Box 3)

Continuity

Normal Continuity
EEG activity is continuous when there is uninterrupted, non-stop electrical activity with
less than 2 seconds of voltage attenuation <25 µV pp. The entire evolution of the normal
EEG background proceeds from the persistently discontinuous tracing in all behavioral
states in extremely premature infants to continuous EEG in all states in fully mature
infants.

Discontinuity
Discontinuous EEG activity is broadly recognized as higher voltage “bursts” of electrical
activity interrupted by lower voltage “interbursts”. The intervening periods of attenuation
are termed interburst intervals (IBI). The durations in seconds of the IBIs are a function
of age, being longest in very preterm infants and shortest during tracé alternant quiet
sleep at term. We define the IBI as a period in which activity is attenuated <25-50 µV pp
for two seconds or more. The literature has historically proposed various definitions for
classifying EEG patterns on the basis of IBI. The definitions offered here are attempted
compromises from these.12, 13 (Table 1) The background can still be called discontinuous
if there is modest activity within the IBI in a single electrode or a single transient in
multiple electrodes.

Normal Discontinuity. There is a progressive decrease in normal IBI durations with

increasing PMA.12, 13 Tracé discontinu, as defined above, is a normal discontinuous EEG
pattern in preterm infants (Figures 1, 2a). The electrical activity within the bursts includes
age-appropriate graphoelements such as rhythmic occipital delta activity and other
specific, named patterns that are described below. It is present in varying amounts from
26-40 weeks PMA. It appears first in wakefulness, active and quiet sleep (until 30 weeks
PMA), then only in quiet sleep, and is rarely seen in infants 38 weeks PMA or older.13

Tracé alternant, as already defined, depicts a point of transition from complete

discontinuity to full continuity. It is only seen in quiet sleep. In the transition from tracé
discontinu to tracé alternant, the durations of the IBIs shorten while their voltages swell
until all the gaps of immature discontinuity have been filled in. While bursts of 50-150
µV delta activity alternate with lower voltage theta activity of 25-50 µV, these lower
voltage periods never completely attenuate. In contrast to tracé discontinu, the voltages
are never less than 25 µV pp.12 (Figures 1, 2b) Like tracé discontinu, the abundance of
this pattern varies by age. Tracé alternant is first seen at 34-36 weeks PMA, becomes
minimal by 42 weeks and is no longer seen by 46 weeks PMA.

Excessive Background Discontinuity

In sick newborn infants who have experienced a variety of causes of encephalopathy
(such as HIE, intracerebral bleeding, sepsis-meningitis, etc.), the two main reported
categories of background abnormalities are pathologically excessive discontinuity and
abnormally low voltage for PMA.16 We suggest restricting the term “excessive
discontinuity” to abnormally discontinuous tracings with bursts that contain some
normal patterns and graphoelements separated by IBIs that are too prolonged or voltage
depressed for PMA, as defined by the parameters in Table 1 (Figures 1, 2c).10 This is an
area that can be addressed and better quantified by future study using standardized
methodology to correlate IBI with patient outcomes.

Burst Suppression
Further disruption of EEG continuity results in the more severe burst suppression pattern.
This consists of invariant, abnormally composed EEG bursts separated by prolonged and
abnormally low voltage IBIs periods, strictly defined as IBI voltages <5 µV pp (Figures
1, 2d). However the definition does allow for one electrode with sparse activity during
the IBI up to 15 µV pp, or less than two seconds with transient activity up to 15 µV pp, or
> 2:1 asymmetry in voltage in multiple electrodes.
In all cases, the EEG should be invariant, with no spontaneous discontinuity changes due
to internally mediated lability and no EEG change of reactivity due to external noxious
stimulation of the infant. The presence of high (> 100 µV pp) or low (<100 µV pp)
voltage activity in the bursts should be described. The composition of the bursts of the
EEG activity is characterized by non-specific theta, delta, beta and admixed sharp waves
but is devoid of specific graphoelements such as monorhythmic occipital delta activity,
delta brushes or other recognizable graphoelements. This is a key feature distinguishing
burst suppression from excess discontinuity: burst suppression has no normal features
within the bursts, while excessively discontinuous records have some normal patterns
identifiable within the bursts. Similarly, burst suppression is an invariant pattern, while
excess discontinuity contains some variability or reactivity.

If burst suppression occurs, typical burst and IBI duration should be recorded. Further
characterization should include a description of the “sharpness”of the components of a
typical burst (see below “Rhythmic and Periodic Patterns of Uncertain Significance”-
Modifier “Sharpness”). In some individuals, the bursts are composed entirely of non-
specific frequencies but in others, unequivocable sharp waves appear admixed within the
bursts.

Symmetry

Normal Symmetry. In the normal neonatal EEG, electrical voltages, frequencies, and the
distribution of specific, named graphoelements should be reasonably equally represented
between homologous regions of the two hemispheres. The left and right hemispheres
should be more or less electrographic mirror images of each other. This allows for
fleeting, transient asymmetries to occasionally occur, while still considering the record
symmetric overall.

Abnormal Asymmetry. The persistence of more than a 2:1 difference in voltages

between homologous regions of the two hemispheres, or a clear disparity of background
features, including the fundamental electrical frequencies and the distribution of specific
graphoelements between the two sides is abnormal. Since focal lesions (arterial ischemic
stroke, sinovenous thrombosis, localized bleeding, abscess, etc) account for up to 10% of
acute neonatal encephalopathies, EEG background asymmetries are not rare and may be
diagnostically relevant.

Synchrony

Synchrony is defined as the onset of bursts of activity that occur nearly simultaneously
between hemispheres in the discontinuous portions of the recording. For example, a
single burst within tracé discontinu would be considered synchronous if the onsets of the
left and right hemisphere bursts occur within 1.5 seconds of each other. The reader
assesses the percentage of bursts that are synchronous within the discontinuous portions
of the study.
Normal synchrony. The percentage of synchronized bursts is not a linear function of
PMA. Prior to 27-29 weeks PMA, EEG activity is almost completely synchronous.17, 18
Between 29 and 30 weeks PMA, EEG activity may only be about 70% synchronous.
From approximately 30 to 37 weeks PMA, more synchronous activity emerges until term
when the EEG is nearly 100% synchronous again.

Normal Asynchrony. As above, some degree of asynchrony is expected and normal

between 30 and 37 weeks PMA. By 38 weeks PMA the EEG should not show any
substantial amount of asynchrony.

Abnormal Asynchrony. This is defined as a clearly excessive percentage of EEG bursts

for PMA that occur asynchronously (greater than 1.5 seconds between onset of activity in
each hemisphere) during the discontinuous portions of the recording.

Voltage

Few studies have defined the normal boundaries for voltage (or amplitude) in premature
infants. Thus, there will be no attempt to offer normal voltage criteria for abnormality in
this group. The focus of this section will therefore be the boundaries of normal voltage
for the term infant. (Figure 1) Just as with the older child or adult, voltage abnormalities
should be interpreted with caution as many extracerebral conditions (such as poor
electrode impedance or inaccurate electrode placement, scalp edema, cephalohematoma,
and subdural hemorrhages) can artificially result in low voltage EEG activity or
interhemispheric voltage asymmetries. Strict voltage thresholds are therefore difficult to
determine.

Normal Voltage
A healthy term infant should have most EEG activity ≥ 25 µV pp in all behavioral states.

Borderline Low Voltage

This is defined as a continuous EEG background containing some normal activity and
graphoelements with representative voltages persistently at least 10 µV but less than 25
µV. The clinical significance of borderline low voltage is not certain.

Abnormally Low Voltage

Low Voltage Suppressed
There are various definitions in the literature of an abnormal background due to a low
voltage or “low voltage undifferentiated” pattern.19-21 We propose a definition of
persistently low voltage activity without normal background features. The fundamental
baseline voltage is less than 10 µV pp. The background can be interspersed with higher Comment [TT1]: <15uV invariant?
voltage (≥ 10 µV pp) transient activity for less than two seconds. In addition, the record Based on Holmes 1982, monod
1972. Monod say +/- reactive
is invariant, with no inherent lability, and unreactive, with no EEG changes from external
stimulation. This pattern suggests severe neurologic injury with diffuse death or
dysfunction of the cortical neuronal generators of EEG activity.
Electrocerebral inactivity (ECI)
This terminology is used to describe the absence of discernible cerebral electrical activity
≥ 2 µV pp when reviewed at a sensitivity of 2 µV/mm.22 The term ECI has largely
replaced the previous terms “electrocerebral silence” (ECS) and isoelectric recordings,
although their implications are the same. Published guidelines detail the technical
requirements needed for performing an EEG to assess for ECI.23 These are distinct from
the technical requirements for standard neonatal EEG recordings. If the EEG is not
performed according to these standards, the term ECI should not be applied. If there is no
discernible cerebral activity, but the recording was not conducted according to the ECI
guidelines, the report should indicate that the recording may be consistent with ECI, but
should specify ECI cannot be determined without the appropriate technical parameters.
ECI is a pattern which, when coupled with appropriate clinical examination and/or
neuroimaging, is used to determine cerebral death.22, 24-27 Clinicians are advised to
consult their institutions’ guidelines regarding the determination of brain death for
newborn infants, as practices vary.

Variability

Variability (lability) denotes conspicuous spontaneous EEG responses to internal stimuli

such as occur during typical sleep-wake cycling. It is first present by 25 weeks when the
EEG initially demonstrates nascent changes with biobehavioral state. Variability should
be increasingly apparent by 28 weeks PMA and well established by 30-31 weeks PMA.
The EEG responses can consist of changes in any electrical domain: frequency,
continuity, or voltage. It is important to note that arousals from sleep can result in
transient attenuation of EEG voltages which should not be mistaken for discontinuity.
Variability should be recorded as Yes, No, or Unclear/unknown/not applicable. For
example, variability would obviously be present in a 60 minute recording which captured
multiple behavioral states such as wakefulness, transitional, active and quiet sleep. The
last choice might apply, for example, in a 60 minute recording that captured only an
awake state

Reactivity

EEG reactivity is demonstrated when there is a conspicuous cerebral EEG response to

external stimulation. Like lability, these EEG responses also consist of changes in any
electrical domain: frequency, continuity, or voltage. The clinical and behavioral
components of reactivity can include crying, movement, EMG activity, and respiratory
pattern changes. It is important to note that after internal or external stimulation,
behavioral responses may induce artifacts from movement or EMG activity that may
mimic actual changes of the EEG background. Reactivity first appears at 30-32 weeks
PMA, but might not been seen with each and every external stimulation. Reactivity
should be recorded as Yes, No, or Unclear/unknown/not applicable. Strength and/or
nature of stimulus should be noted.

Dysmaturity
The traditional scenario in which the term dysmaturity was coined involved very
premature infants with chronic illnesses such as bronchopulmonary dysplasia. Over time,
their EEG background features sometimes failed to mature at the same rate as their PMA
progressed. There was eventually a gap between their actual PMA and their maturity as
suggested by the appearance of their EEG backgrounds. This disparity in maturity
between the actual PMA and their “EEG PMA” is termed dysmaturity, defined as an
EEG that would be normal for an infant at least two weeks younger than the stated PMA.
The persistently dysmature EEG is considered abnormal and is associated with an
increased risk of abnormal neurologic outcome.22, 28

NORMAL GRAPHOELEMENTS (DEVELOPMENTAL BACKGROUND

HALLMARKS)

In neonatal EEG, graphoelements are normal, expected, specific, named EEG

background patterns that first appear, peak and then fade during particular epochs of
neonatal development. They are characteristic of specific PMAs. They are part of the
composition of the normal EEG background and are thus typically symmetric. Not every
known type of specific graphoelement is included below; we have defined the most
commonly seen.(Box 4)

Monorythmic Delta Activity. This pattern occurs between 24 and 34 weeks PMA and
consists of moderately high voltage (up to 200µV pp) delta activity with a relatively
stereotyped morphology. It may be predominantly occipital, temporal and/or central, but
is rarely frontal.18 Is typically synchronous and symmetric, and often surface positive.

Delta Brushes. Delta brushes have been described under many names, including beta-
delta complexes, spindle-delta bursts, spindle-like fast waves, or ripples of prematurity.
These are most prominent between 24 and 36 weeks PMA and consist of a combination
of 0.3-1.5 Hz slow waves of 50-250 µV pp with superimposed fast activity (8-12 or 18-
22 Hz).12 Their peak expression is between 32 and 34 weeks PMA. They are maximal in
active sleep up to 32 weeks and after that are seen in wakefulness and quiet sleep then are
maximal in quiet sleep between 33 and 37 weeks PMA.17, 18 They are occasionally seen
in quiet sleep up to 40 weeks PMA.

Rhythmic Temporal Theta. This graphoelement occurs between 24 and 34 weeks PMA.
It typically consists of 25-120 µV pp theta frequency activity for short (two second)
bursts over the temporal region. It is typically symmetric, and maximal between 29 and
32 weeks PMA.12, 17, 18 Morphologically similar activity can be seen at the vertex and
occipital regions.

Anterior Dysrhythmia. Despite its somewhat misleading name, this is a normal

graphoelement. It first appears at 32 weeks and persists until 44 weeks PMA. It consists
of 50-100 µV pp delta waves which may occur in isolation or brief runs for a few seconds
over the frontal regions.12, 18 It is typically synchronous and symmetric.
Encoches Frontales. This pattern is intimately related to anterior dysrhythmia and the
two are often seen admixed over the frontal regions. (Figure 3a) Encoches frontales occur
between 34 and 44 weeks PMA and consist of 50-100 µV pp broad diphasic transients
(0.5-0.75 sec) with a small initial negative deflection and a larger positive deflection.10, 12,
18
Overall, they are typically synchronous and symmetric. They are often present in
transitional sleep and most abundant in the transition from active to quiet sleep.17, 18

EEG TRANSIENT PATTERNS

As opposed to the fundamental EEG background, which is the basic ongoing cerebral
electrical activity, there are also transient EEG patterns that may intermittently punctuate
the background. (Box 5)

Sharp Wave Transients

Many healthy neonates have normal, physiologic sharp wave transients while some sick
newborns show abnormal or excessive sharp wave transients that imply pathology. There
remains debate regarding the boundaries that separate physiologic from pathologic sharp
wave transients. Sharp wave transients are characterized by their negative or positive
polarity, duration, abundance, spatial distribution, and repetitive behavior.

A negative sharp wave transient has an initial and predominant deflection that is surface
negative. A positive sharp wave transient has an initial and predominant deflection that is
surface positive. Both need to be clearly distinct from the background as separate
transients and not just “sharply contoured background activity”. Sharp wave transients
lasting < 100 msecs are commonly called spikes. Sharp wave transients lasting 100-200
msecs are commonly called sharp waves. It is notable that the typical neonatal display of
15mm/seconds time compresses the appearance of the background, and many EEG
features will appear more sharply contoured than if the recording were viewed at the
typical adult or pediatric display setting of 30mm/sec.

Quantification of the abundance of sharp wave transients (the number of spike or sharp
waves per minute at a given location such as the central or temporal regions) should be
undertaken in the most continuous portions of the neonatal EEG: wakefulness or active
sleep. In the discontinuous portions of the record, particularly during tracé alternant, the
EEG bursts often have fleeting sharply contoured activity embedded within the
background, rather than truly distinct EEG transients separate from the background.
Sharp wave transients can appear at any electrode location. Sharp wave transients may
occur as single, solitary events or recur in brief repetitive runs or trains.

Physiologic Negative Sharp Waves.

Physiologic negative sharp waves lasting 100-200 msecs are commonly seen in the EEGs
of healthy near-term and term infants (Figure 3b). They are typically observed against the
backdrop of a normal EEG background for PMA. They appear in greatest abundance in
the mid-temporal, central and centro-temporal regions. They are rare in the frontal,
midline vertex and occipital regions. They are symmetrically distributed between
homologous regions of the hemispheres. They are mostly single, solitary transients but a
few may appear in brief trains or runs.28

Abnormal Negative Sharp Wave Transients

These appear as sharp waves or true spikes (Figure 3c). They most commonly arise in the
context of an abnormal EEG background for PMA. Although they may also appear in the
familiar mid-temporal, central or centro-temporal locations, they may be heavily
concentrated in one region or hemisphere, rather than being randomly or evenly
distributed spatially. They may also be seen in atypical locations such as the frontal,
midline vertex or occipital regions. They may be much more abundant compared to
physiologic negative sharp wave transients. Data for neonates who were assessed
developmentally at ≥ one year old indicate that negative sharp waves more frequent than
11 per hour for preterm and 13 per hour for term infants are abnormal.29-34 Abnormal
negative sharp EEG transients are more likely than physiologic negative sharp waves to
recur in brief runs or trains.35

Positive Sharp Wave Transients.

Historically, these were first described in the EEGs of preterm infants who developed
significant intraventricular hemorrhages. Positive sharp waves were described in the
Rolandic regions (positive Rolandic sharp waves or PRS), represented by electrodes C3
and C4, although it was later recognized than many were actually maximally situated at
the midline vertex (positive vertex sharp waves-PVS) with field spread to the adjacent
Rolandic regions.36 It is now appreciated that PRS and PVS are most closely
pathologically associated with underlying white matter injury including periventricular
leukomalacia.37

In the term infant, excessive positive sharp waves in the mid-temporal regions can signify
underlying focal pathology such a localized hemorrhage or white matter injury. However,
these are more difficult to judge since rare scattered temporal sharp waves can be
occasionally seen in apparently health term infants. Previous work suggests up to 3 per
hour for preterm and 1.5 per hour for term neonates may be normal.38, 39

Brief Rhythmic Discharges (BRD).

This transient EEG pattern consists of evolving rhythmic patterns of electrical activity
that share many characteristics with seizures but are very brief, with a duration less than
ten seconds.40-42 These have previously been alternatively described in the literature as
BIRDs (Brief Ictal/Interictal Rhythmic/Repetitive Discharges) and BERDs (Brief
Electrographic Rhythmic Discharges). Given that the true significance of these
discharges is uncertain, the operational term “BRD” will be used here. They are usually
seen in the context of an abnormal EEG background and/or confirmed electrographic
seizures. BRDs are rarely seen in isolation in a normal EEG. At this time, their
pathological significance is not fully understood. However, recent studies in adults
suggest that clinical behavior changes can coexist with epileptiform discharges under two
seconds in duration.43 Similarly, a case series demonstrated similar mortality and
neurologic disability for infants with BRDs as with seizures.41 Further study is needed to
better understand the basis and significance of brief rhythmic discharges in the neonate.

SEIZURES AND STATUS EPILEPTICUS

Neonatal Seizures

Neonatal seizures are traditionally classified as clinical-only, electroclinical or

electrographic-only seizures. A clinical-only seizure consists of a sudden paroxysm of
abnormal clinical changes that do not correlate with a simultaneous EEG seizure, These
clinical changes may include unnatural posturing, obligatory stereotyped movements,
sudden arrested behaviors or autonomic dysfunction (episodic tachycardia or
hypertension, flushing, pallor or salivation, etc.). An electroclinical seizure features
definite clinical seizure signs simultaneously coupled with an EEG seizure.44 An EEG-
only seizure refers to the presence of a definite EEG seizure that does not provoke any
specific outwardly visible clinical signs. For the purposes of this document, the term
"seizure" hereafter refers to electrographic seizures, with or without coupled clinical
signs of seizure.

An electrographic seizure is a sudden, abnormal EEG event defined by a repetitive and

evolving pattern with a minimum 2µV pp voltage and duration of at least ten seconds. A
seizure is always an abnormal pattern and should not be confused with transient
background changes, such as those associated with drowsiness or arousal from sleep.
“Evolving” is defined as an unequivocal evolution in frequency, voltage, morphology or
location. In contrast, brief rhythmic repetitive discharges lasting less than ten seconds but
with evolution would be considered BRDs and not seizures. Likewise, rhythmic,
repetitive activity lasting more than ten seconds but without evolution would be
considered periodic discharges or rhythmic activity, but not a seizure (Figure 3c). While
2µV pp defines the boundaries of the beginning and end of each seizure, the voltages
predictably increase as the seizure evolves and can be up to 150µV pp or more. Unlike
seizures in older children and adults, there is no minimum electrical frequency required
in the definition of seizure. To be classified as separate seizures, ten seconds or more
must separate two distinct seizure events.45, 46

Several aspects of a seizure can be quantified. In the older child and adult, the ACNS
standardized research terminology describes the typical, minimum and maximum
frequency (Hz) during a seizure.8 This is of uncertain significance in the neonate. Seizure
location can be described in terms of the focus (site of onset) and maximal spread,
represented by the greatest number of electrodes involved. Recommended terminology
to describe seizure spread includes:
• Diffuse (D) - asynchronous involvement of all electrodes by focal seizures of
extensive geographic distribution. This contrasts with children and adults who can
have truly generalized, synchronous and symmetric activity.
• Bilateral independent (BI) – a seizure with activity occurring simultaneously in
two regions but which begin, evolve and behave independently of each other.
• Migrating (Mig) - seizure moves sequentially from one hemisphere to another
 • Lateralized (L) - all of the seizure propagates within a single hemisphere (LH or
RH).
• When a seizure is restricted to a confined region, it can be further described as
frontal (F), central (C), temporal (T),occipital (O) or Vertex (Z) or it can be
described more broadly as anterior quadrant (Ant), posterior quadrant (Post).
• When multiple seizures arise from a single general region, they can be classified
as unifocal onset.
• Multifocal (Mf) onset seizures originate from at least three independent foci with
at least one in each hemisphere. It is not uncommon for localized lesions such as a
stroke to precipitate unifocal seizures, while diffuse insults such as meningitis
may provoke multifocal onset seizures.
• .

Seizure burden has been quantified in various ways.1, 45, 47-49 We propose quantifying
seizure burden for clinical purposes using one of the following definitions:
1) Frequency: the number of seizures per hour, or
2) Percent of the record with seizures: the total summed duration of all the seizures
divided by the entire duration of an epoch of interest, or
3) Temporal-spatial quantification: The most detailed metric of seizure burden that could
be used for research purposes includes the total summed durations of seizures in each
region of interest, per hour.50 In this case, the neonatal montage could be collapsed into Comment [TT2]: should reference
five non-overlapping regions of interest: Fp3-T3, C3-O1, Fp4-T4, C4-O2 and Fz-Pz (or Mark's paper about interrater
reliability of one temporal spatial
alternatively Fp3-C3, T3-O1, Fp4-C4, T4-O2 and Fz-Pz). Thus, each single electrode is quantification system
counted only once. The total summed seizure durations can be calculated separately for
each of the five regions of interest, which provides a temporal-spatial metric of seizure
burden. Future work is needed to determine the relative utility of these more labor
intensive methods.

Status Epilepticus

The traditional definition of status epilepticus in children and adults is a single seizure
lasting more than 30 minutes or a series of seizures lasting at least 30 minutes between
which baseline brain function has not been restored.42 These criteria are difficult to apply
to neonates, given the difficulty assessing their mental status and the high incidence of
co-existing acute encephalopathy. Consequently, other definitions of neonatal status have
been offered.46 In consensus with the current literature, we propose a definition of status
epilepticus as present when the summed duration of seizures comprises ≥ 50% of an
arbitrarily defined one hour epoch. In other words, if half or more of any given hour of
recording shows seizures, status epilepticus exists for that epoch.

In a population of neonates with recorded electrographic seizures, the percentage of

recording time in which seizures are detected could range from 1% to 100%. It is
recognized that our definition of status is a somewhat arbitrary and that there are no data
that specifically justify the choice of 50% over any other percentage value as especially
meaningful or significant. Alternative research definitions of status could be explored
based on available data regarding typical durations of electrographic neonatal seizures. In
two studies in neonates, the median EEG seizure length was one minute, with 75% of
seizures lasting ≤2.5 minutes.45, 48 In these and another study, the range of individual
seizure duration was 10 seconds-46 minutes, and the mean seizure length was 2-4
minutes. 45, 46, 48 In future studies it will be useful to characterize different categories of
seizure burden and duration of status epilepticus as they relate to outcomes.

RHYTHMIC AND PERIODIC PATTERNS OF UNCERTAIN SIGNIFICANCE

Some rhythmic patterns do not demonstrate the unequivocal evolution in frequency,
morphology or location characteristic of seizures. These are targets of active
investigation in the older ICU population as they are common and their clinical
significance is unclear. Pathologic rhythmic and periodic patterns do occur in preterm
and term neonates but are not common.51 It is unclear whether research terminology that
has been developed in adults is applicable to the neonate.8 We discuss below the patterns
from the adult terminology which have been described previously in neonatal literature.

Patterns

Periodic. Periodic discharges (PD) are defined in the adult terminology as a pattern in
which waveforms have a relatively uniform morphology and duration, there is a
quantifiable interval between consecutive waveforms and the waveforms recur at nearly
regular intervals. “Discharges” are defined as waveforms with no more than three phases
[i.e. crosses the baseline no more than twice] or any waveform lasting 0.5 seconds or less,
regardless of number of phases). In contrast, bursts are defined as waveforms lasting
more than 0.5 seconds and having at least four phases [i.e. crosses the baseline at least
three times]. “Nearly regular intervals” is defined as having a cycle length (i.e., period)
varying by <50% from one cycle to the next in the majority (>50%) of cycle pairs.(Figure
3c). PD are not common in neonates, but can occur with acute destructive processes such
as HSV encephalitis, stroke or global hypoxia ischemia.51-53

Rhythmic. Rhythmic delta activity (RDA) is defined in the adult terminology as the
repetition of a waveform with relatively uniform morphology and duration but without an
interval between consecutive waveforms. To qualify as rhythmic, the duration of one
cycle (i.e., the period) of the rhythmic pattern must vary by <50% from the duration of
the subsequent cycle for the majority (>50%) of cycle pairs. Importantly, this EEG
pattern may not be abnormal in neonates and is consistent with some normal neonatal
graphoelements: rhythmic occipital delta activity and anterior dysrhythmia.

Duration
The periodic or rhythmic pattern must be present for at least six cycles (e.g. 1/second for
six seconds or 3/second for two seconds).

Location
Location can be described in terms of the focus (site of onset) and maximal spread
(maximal electrodes involved). Location can be Lateralized (L) or Diffuse (D).
Lateralized includes unilateral focal/regional/hemispheric and bilateral asymmetric
activity. In Diffuse activity (D), there is asynchronous involvement of all electrodes. The
term Diffuse can be applied to bilateral hemispheric involvement even if the activity has
a restricted field (e.g. bifrontal). Patterns may also be Bilateral Independent (BI) or
Multifocal (Mf).

Additional localizing information may include a description of the predominant location.

For diffuse (D), one can specify frontally-predominant, occipitally-predominant, midline
predominant or ‘generalized, not otherwise specified’. Frontally predominant is defined
as having an amplitude in anterior derivations that is at least 50% greater than that in
posterior derivations on an ipsilateral ear, average, or non-cephalic referential recording.
Occipitally predominant is defined as having an amplitude in posterior derivations that is
at least 50% greater than that in anterior derivations on an ipsilateral ear, average, or non-
cephalic referential recording. Midline predominant is defined as having an amplitude in
midline derivations that is at least 50% greater than in parasagittal derivations on an
average or non-cephalic referential recording. For lateralized (L), bilateral independent
(BI) or multifocal (Mf) patterns, one can specify the area(s) most involved (F, C, T, O, Z
or hemispheric if more specific localization is not possible) and whether the activity is
bilateral asymmetric or unilateral. If activity is bilateral but asymmetric (BI or Mf), the
most involved areas (F, C, T, O, Z or hemispheric) can be specified over both
hemispheres.

Modifiers
Rhythmic patterns can be further described using “modifier” terms according to the
ACNS Standardized Critical Care EEG Terminology 2012. The modifier “evolving”
does not apply to neonates since this defines a neonatal seizure. Three other modifiers
which differ from the adult terminology are discussed below.

Duration
If the pattern is not continuous, then the typical duration of pattern is specified. Duration
categories are provided, and the adult terminology also recommends recording the
longest continuous duration.
• ≥1 hour (“Very long”)
• 5-59 minutes (“Long”)
• 1-4.9minutes (“Intermediate duration”)
• 10-59 seconds (“Brief”)
• <10 seconds (“Very brief”; distinct from BRDs for lack of evolution)

In one study, periodic discharge duration in the preterm infant was less than one minute
and more than one minute for term infants.51 Only 4/592 preterm and term infants had
duration ≥10 minutes. Thus, while we define duration to be consistent with terminology
used in the ICU for adult EEG, we recognize very few neonatal EEG patterns will fall
into the “long” or “very long” categories.

Polarity
In neonatal recordings, polarity should be determined in the traditional bipolar montage
and should be specified for the predominant phase (phase with the greatest amplitude)
only for a typical discharge. Polarity applies only to PDs and the spike/sharp component
of SW, not RDA. Polarity is categorized as positive, negative, or unclear.

Sharpness
Sharpness applies only to PDs and the spike/sharp component of SW, but not to RDA.
Sharpness should be specified for a typical discharge for both the predominant phase
(phase with greatest amplitude) and the sharpest phase if different. Sharpness categories
include:
• Spiky waveforms have a duration measured at the EEG baseline <100 msecs.
• Sharp waveforms have a duration of 100-200 msecs.
• Sharply contoured theta and delta waveforms have a sharp wave morphology
(steep slope to one side of the wave and/or pointy at inflection point[s]) but are
too long in duration to qualify as a sharp wave.
• Blunt waveforms have a smooth or sinusoidal morphology.

CONCLUSION

This document is a collaborative effort to standardize the neonatal EEG terminology. We

hope this common language fosters more effective multicenter collaboration to determine
the significance of continuous EEG findings in critically ill neonates. Future work may
build upon this framework to establish the utility of the proposed terms and definitions,
both in the research and clinical realms. This terminology will be revised and updated
based upon feedback and future research.
REFERENCES

1. Murray DM, Boylan GB, Ali I, Ryan CA, Murphy BP, Connolly S. Defining the
gap between electrographic seizure burden, clinical expression and staff recognition of
neonatal seizures. Arch Dis Child Fetal Neonatal Ed 2008;93:F187-191.
2. Clancy RR, Legido A, Lewis D. Occult neonatal seizures. Epilepsia 1988;29:256-
261.
3. Shellhaas RA, Chang T, Tsuchida T, et al. The American Clinical
Neurophysiology Society's Guideline on Continuous Electroencephalography Monitoring
in Neonates. J Clin Neurophysiol 2011.
4. Hirsch LJ, Claassen J, Mayer SA, Emerson RG. Stimulus-induced rhythmic,
periodic, or ictal discharges (SIRPIDs): a common EEG phenomenon in the critically ill.
Epilepsia 2004;45:109-123.
5. Vespa PM, Nenov V, Nuwer MR. Continuous EEG monitoring in the intensive
care unit: early findings and clinical efficacy. J Clin Neurophysiol 1999;16:1-13.
6. Oddo M, Carrera E, Claassen J, Mayer SA, Hirsch LJ. Continuous
electroencephalography in the medical intensive care unit. Crit Care Med 2009;37:2051-
2056.
7. Orta DS, Chiappa KH, Quiroz AZ, Costello DJ, Cole AJ. Prognostic implications
of periodic epileptiform discharges. Arch Neurol 2009;66:985-991.
8. Hirsch LJ, Brenner RP, Drislane FW, et al. The ACNS subcommittee on research
terminology for continuous EEG monitoring: proposed standardized terminology for
rhythmic and periodic EEG patterns encountered in critically ill patients. J Clin
Neurophysiol 2005;22:128-135.
9. Engle WA. Age terminology during the perinatal period. Pediatrics
2004;114:1362-1364.
10. Brain Monitoring: Normal Neonatal EEG [computer program]. Ambler, PA:
Moberg Multimedia, 2011.
11. Scher MS, Johnson MW, Holditch-Davis D. Cyclicity of neonatal sleep behaviors
at 25 to 30 weeks' postconceptional age. Pediatr Res 2005;57:879-882.
12. Lamblin MD, Andre M, Challamel MJ, et al. [Electroencephalography of the
premature and term newborn. Maturational aspects and glossary]. Neurophysiol Clin
1999;29:123-219.
13. Hahn JS, Monyer H, Tharp BR. Interburst interval measurements in the EEGs of
premature infants with normal neurological outcome. Electroencephalogr Clin
Neurophysiol 1989;73:410-418.
14. Scher MS. Electroencephalography of the newborn : normal and abnormal
features. In: Niedermeyer E, Lopes da Silva FH, eds. Electroencephalography, 5th ed.
Philadelphia: Lippincott Williams and Wilkins, 2005: 937-990.
15. Curzi-Dascalova L, Peirano P, Morel-Kahn F. Development of sleep states in
normal premature and full-term newborns. Dev Psychobiol 1988;21:431-444.
16. Clancy RR, Dicker L, Cho S, et al. Agreement between long-term neonatal
background classification by conventional and amplitude-integrated EEG. J Clin
Neurophysiol 2011;28:1-9.
17. Mizrahi EM, Hrachovy RA, Kellaway P, Stockard-Pope JE. Atlas of neonatal
electroencephalography, 3rd ed. Philadelphia: Lippincott Williams & Wilkins, 2004.
18. Clancy RA, Bergqvist AGC, Dlugos DJ. Neonatal Electroencephalography. In:
Ebersole JS, Pedley TA, eds. Current practice of clinical electroencephalography, 3rd ed.
Philadelphia: Lippincott Williams & Wilkins, 2003: 106-234.
19. Tharp BR, Cukier F, Monod N. The prognostic value of the electroencephalogram
in premature infants. Electroencephalogr Clin Neurophysiol 1981;51:219-236.
20. Monod N, Pajot N, Guidasci S. The neonatal EEG: statistical studies and
prognostic value in full-term and pre-term babies. Electroencephalogr Clin Neurophysiol
1972;32:529-544.
21. Holmes G, Rowe J, Hafford J, Schmidt R, Testa M, Zimmerman A. Prognostic
value of the electroencephalogram in neonatal asphyxia. Electroencephalogr Clin
Neurophysiol 1982;53:60-72.
22. Holmes GL, Lombroso CT. Prognostic value of background patterns in the
neonatal EEG. J Clin Neurophysiol 1993;10:323-352.
23. Guideline 3: Minimum technical standards for EEG recording in suspected
cerebral death. J Clin Neurophysiol 2006;23:97-104.
24. Ashwal S. Brain death in the newborn. Clin Perinatol 1989;16:501-518.
25. Ashwal S, Schneider S. Brain death in the newborn. Pediatrics 1989;84:429-437.
26. Volpe JJ. Brain death determination in the newborn. Pediatrics 1987;80:293-297.
27. Nakagawa TA, Ashwal S, Mathur M, Mysore M. Clinical Report--Guidelines for
the Determination of Brain Death in Infants and Children: An Update of the 1987 Task
Force Recommendations. Pediatrics 2011.
28. Biagioni E, Bartalena L, Biver P, Pieri R, Cioni G. Electroencephalographic
dysmaturity in preterm infants: a prognostic tool in the early postnatal period.
Neuropediatrics 1996;27:311-316.
29. Scher MS, Bova JM, Dokianakis SG, Steppe DA. Physiological significance of
sharp wave transients on EEG recordings of healthy pre-term and full-term neonates.
Electroencephalogr Clin Neurophysiol 1994;90:179-185.
30. Statz A, Dumermuth G, Mieth D, Duc G. Transient EEG patterns during sleep in
healthy newborns. Neuropediatrics 1982;13:115-122.
31. Biagioni E, Boldrini A, Bottone U, Pieri R, Cioni G. Prognostic value of
abnormal EEG transients in preterm and full-term neonates. Electroencephalogr Clin
Neurophysiol 1996;99:1-9.
32. Clancy RR, Spitzer AR. Cerebral cortical function in infants at risk for sudden
infant death syndrome. Ann Neurol 1985;18:41-47.
33. Rowe JC, Holmes GL, Hafford J, et al. Prognostic value of the
electroencephalogram in term and preterm infants following neonatal seizures.
Electroencephalogr Clin Neurophysiol 1985;60:183-196.
34. Karbowski K, Nencka A. Right mid-temporal sharp EEG transients in healthy
newborns. Electroencephalogr Clin Neurophysiol 1980;48:461-469.
35. Clancy RR. Interictal sharp EEG transients in neonatal seizures. J Child Neurol
1989;4:30-38.
36. Clancy RR, Tharp BR. Positive rolandic sharp waves in the
electroencephalograms of premature neonates with intraventricular hemorrhage.
Electroencephalogr Clin Neurophysiol 1984;57:395-404.
37. Novotny EJ, Jr., Tharp BR, Coen RW, Bejar R, Enzmann D, Vaucher YE.
Positive rolandic sharp waves in the EEG of the premature infant. Neurology
1987;37:1481-1486.
38. Scher MS, Bova JM, Dokianakis SG, Steppe DA. Positive temporal sharp waves
on EEG recordings of healthy neonates: a benign pattern of dysmaturity in pre-term
infants at post-conceptional term ages. Electroencephalogr Clin Neurophysiol
1994;90:173-178.
39. Chung HJ, Clancy RR. Significance of positive temporal sharp waves in the
neonatal electroencephalogram. Electroencephalogr Clin Neurophysiol 1991;79:256-263.
40. Oliveira AJ, Nunes ML, Haertel LM, Reis FM, da Costa JC. Duration of rhythmic
EEG patterns in neonates: new evidence for clinical and prognostic significance of brief
rhythmic discharges. Clin Neurophysiol 2000;111:1646-1653.
41. Nagarajan L, Palumbo L, Ghosh S. Brief Electroencephalography Rhythmic
Discharges (BERDs) in the Neonate With Seizures: Their Significance and Prognostic
Implications. J Child Neurol 2011.
42. Shewmon DA. What is a neonatal seizure? Problems in definition and
quantification for investigative and clinical purposes. J Clin Neurophysiol 1990;7:315-
368.
43. D'Ambrosio R, Hakimian S, Stewart T, et al. Functional definition of seizure
provides new insight into post-traumatic epileptogenesis. Brain 2009;132:2805-2821.
44. Mizrahi EM, Kellaway P. Characterization and classification of neonatal seizures.
Neurology 1987;37:1837-1844.
45. Clancy RR, Legido A. The exact ictal and interictal duration of
electroencephalographic neonatal seizures. Epilepsia 1987;28:537-541.
46. Scher MS, Hamid MY, Steppe DA, Beggarly ME, Painter MJ. Ictal and interictal
electrographic seizure durations in preterm and term neonates. Epilepsia 1993;34:284-
288.
47. Pisani F, Copioli C, Di Gioia C, Turco E, Sisti L. Neonatal seizures: relation of
ictal video-electroencephalography (EEG) findings with neurodevelopmental outcome. J
Child Neurol 2008;23:394-398.
48. Shellhaas RA, Clancy RR. Characterization of neonatal seizures by conventional
EEG and single-channel EEG. Clin Neurophysiol 2007;118:2156-2161.
49. McBride MC, Laroia N, Guillet R. Electrographic seizures in neonates correlate
with poor neurodevelopmental outcome. Neurology 2000;55:506-513.
50. Scher MS, He BQ, Mazumdar S, Painter MJ, Alvin J, Redmond CK. A Reliability
Study of a Neonatal Seizure Scoring System. J Epilepsy 1994;7:273-278.
51. Scher MS, Beggarly M. Clinical significance of focal periodic discharges in
neonates. J Child Neurol 1989;4:175-185.
52. Sainio K. Granstrom ML. Pettay O. Donner M. EEG in neonatal herpes simplex
encephalitis. EEG Clin Neurophysiol 1983; 56:556-561.
53. Mikati MA. Feraru E. Krishnamoorthy K. Lombroso CT. Neonatal herpes
simplex meningoencephalitis: EEG investigations and clinical correlates. Neurology
1990; 40:1433-1437.
Figure legends
Box 1. DETAILS TO INCLUDE IN DAILY EEG REPORT

Box 2. BEHAVIORAL STATE

Figure 1. Examples of EEG background classification by voltage.

Figure 2. Examples illustrating the contrasts between tracé discontinu, tracé alternant,
excessive discontinuity, and burst suppression. EEG tracings courtesy of Clancy, RR and
Wusthoff, CJ. Brain monitoring: Normal Neonatal EEG. Moberg Multimedia. Ambler,
PA. 2011

Figure 2a. In tracé discontinu, the bursts are separated by very low voltage, suppressed
interburst intervals. There are no artifacts from EMG activity or movement and the
respiratory pattern is quite regular.

Figure 2b. In this example of tracé alternant, however, there is an alternating pattern of
high and low voltages, but no periods that are consistently suppressed. There are no
artifacts from EMG activity or movement and the respiratory pattern is quite regular.

Figure 2c. This excessively discontinuous record from a term infant with an acute
encephalopathy shows prolonged interburst intervals, though with some normal features
present during bursts, such as the conspicuous encoche frontale seen near its onset
(arrow).

Figure 2d. Burst suppression, in contrast, contains prolonged, extremely suppressed

interburst intervals and bursts comprised exclusively of abnormal electrical activity.

Box 3. EEG BACKGROUND

Table 1. Normal interburst interval (IBI) duration and amplitude. Values for IBI
duration and amplitude vary with postmenstrual age.

Box 4. NORMAL GRAPHOELEMENTS

Box 5. EEG TRANSIENT PATTERNS

Figure 3. Examples illustrating the contrasts between encoches frontales, physiologic
sharp waves, and pathologic sharp waves.

Figure 3a. Encoches frontales are present and synchronous in both frontal regions.

Figure 3b. A physiologic sharp wave is seen in the 13th second on this page, in the right
mid-temporal region (T4).
Figure 3c. Pathologic periodic sharp waves are seen in the left anterior quadrant. These
occur frequently, and repetitively in the same location. The first three are highlighted
with arrows.

Box 6. SEIZURES AND STATUS EPILEPTICUS

Box 7. RHYTHMIC AND PERIODIC PATTERNS OF UNCERTAIN SIGNIFICANCE

Figures and Tables

Box 1

DETAILS TO INCLUDE IN DAILY EEG REPORT

• Patient Postmenstrual Age
• Neuroactive medications in use during recording
• Use of hypothermia during recording
• Clinical changes that may impact cerebral function
• Documentation of duration of recording (in hours) uninterpretable due to technical problems
• Characterization of background features during first hour of monitoring
• Characterization of one hour of background within each subsequent 24 hour epoch
• Characterization of additional epochs when background changes
• Seizure onset, burden, and resolution
• Presence, onset, and resolution of status epilepticus
Box 2

BEHAVIORAL STATE
• Awake
• Asleep
o Active Sleep
o Quiet Sleep
• Transitional Sleep
• Indeterminate Sleep
• Sleep-wake Cycling
Figure 1.
Figure 1. Examples of EEG background classification by voltage.

Tracé Tracé Burst

Alternant Discontinu Supression
50

Activité moyenne
(awake or active sleep)

Voltage
(μV) 25
IBI
Borderline low
voltage
voltage ≥25 μV
10
Low Voltage Suppressed
5
2
0 Electrocerebral Inactivity

IBI voltage IBI voltage

0 to <25 μV 0 to <5 μV

Continuous EEGs Discontinuous EEGs

Figure 2. Examples illustrating the contrasts between tracé discontinu, tracé alternant, excessive discontinuity, and burst
suppression. EEG tracings courtesy of Clancy, RR and Wusthoff, CJ. Brain monitoring: Normal Neonatal EEG. Moberg
Multimedia. Ambler, PA. 2011.

Figure 2a. In tracé discontinu, the bursts are separated by very low voltage, suppressed interburst intervals. There are no
artifacts from EMG activity or movement and the respiratory pattern is quite regular.
Figure 2b. In this example of tracé alternant, however, there is an alternating pattern of high and low voltages, but no periods
that are consistently suppressed. There are no artifacts from EMG activity or movement and the respiratory pattern is quite
regular.
Figure 2c. This excessively discontinuous record from a term infant with an acute encephalopathy shows prolonged interburst
intervals, though with some normal features present during bursts, such as the conspicuous encoche frontale seen near its
onset (arrow).
Figure 2d. Burst suppression, in contrast, contains prolonged, extremely suppressed interburst intervals and bursts comprised
exclusively of abnormal electrical activity.
Box 3

EEG BACKGROUND
• Continuity
- Normal Continuity
- Normal Discontinuity
- Excessive Discontinuity
- Burst Suppression
• Symmetry
• Synchrony
• Voltage
- Normal voltage
- Borderline low voltage
- Abnormally low voltage

Low Voltage Suppressed

Electrocerebral inactivity
• Variability
• Reactivity
• Dysmaturity
Table 1. Normal interburst interval (IBI) duration and amplitude. Values for IBI duration and amplitude vary with
postmenstrual age.
Postmenstrual Age Maximum Voltage of
interburst interburst
interval
< 30 weeks 35 seconds <25μV
30-33 weeks 20 seconds <25μV
34-36 weeks 10 seconds ~25μV
37-40 weeks 6 seconds >25μV
Box 4

NORMAL GRAPHOELEMENTS
• Monorhythmic Delta Activity
• Delta Brushes
• Rhythmic Temporal Theta
• Anterior Dysrhythmia
• Encoches Frontales
Box 5

EEG TRANSIENT PATTERNS

• Negative Sharp Wave Transients
o Physiologic Negative Sharp Waves
o Abnormal Negative Sharp Waves
• Positive Sharp Transients
• Brief Rhythmic Discharges (BRD)
Figure 3. Examples illustrating the contrasts between encoches frontales, physiologic sharp waves, and pathologic
sharp waves.

Figure 3a. Encoches frontales are present and synchronous in both frontal regions.
Figure 3b. A physiologic sharp wave is seen in the 13th second on this page, in the right mid-temporal region (T4).
Figure 3c. Pathologic periodic sharp waves are seen in the left anterior quadrant. These occur frequently, and
repetitively in the same location. The first three are highlighted with arrows.
Box 6

SEIZURES AND STATUS EPILEPTICUS

• Seizures
- Duration ≥ 10 seconds
- Location

Diffuse (D)

Lateralized (L)
• Hemispheric- left (LH), right (RH)

Focal
• Frontal (F)
• Central (C)
• Temporal (T)
• Occipital (O)
• Vertex (Z)
• Quadrant- anterior (Ant), posterior (Post)

Bilateral Independent (BI)

Multifocal (Mf)

Migrating (Mig)
- Seizure Burden

Number of seizures per hour or

Summed duration of seizures divided by duration of epoch
• Status Epilepticus- summed duration of seizures totals ≥ 50% of a 1hr epoch
Box 7

RHYTHMIC AND PERIODIC PATTERNS OF UNCERTAIN SIGNIFICANCE

• Pattern
- Periodic discharges (PD )
- Rhythmic delta activity (RDA)
• Duration
• Location
- Lateralized (L)

Focal

Hemispheric- left (LH), right (RH)

Bilateral asymmetric
- Diffuse (D)
- Bilateral Independent (BI)
- Multifocal (Mf)
• Modifiers (subset of ACNS Standardized Critical Care EEG Terminology 2012)
- Duration
- Polarity
- Sharpness