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EPILEPSY (CW BAZIL, SECTION EDITOR)

Continuous Electroencephalography Monitoring in Neonates

Rene A. Shellhaas

Published online: 25 April 2012# Springer Science+Business Media, LLC 2012

Abstract As more critically ill term and premature neo-

nates are surviving their acute illness, their long-term neuro-developmental morbidity is being recognized. Continuous

monitoring of cerebral function, with electroencephalography

or derived digital trends, can provide key information

regarding seizures and background patterns, with direct

treatment and prognostic implications. Conventional video-

electroencephalography remains the gold standard for neona-

tal seizure diagnosis and quantification, but can be supple-

mented by digital trending modalities. Both conventional and

amplitude-integrated electroencephalography can provide

valuable data regarding the background trends. This review

describes indications and methods for continuous electroen-

cephalography monitoring in high-risk neonates.

Keywords Electroencephalography . EEG . Intensive care .

Neonatal . Seizure . Amplitude-integrated

electroencephalography . aEEG . Continuous

electroencephalography . Monitoring .Neonates

Introduction

Neonates requiring neurointensive care are at high risk for

death or long-term neurologic morbidity, including cerebral

palsy, developmental delay, and epilepsy. Although an increas-

ing array of interventions are available, such as therapeutic

hypothermia for those with hypoxic-ischemic encephalopathy

(HIE), adverse outcomes remain common. Clinical practicevaries, depending on the clinicians specialty training and local

resources [1], but there is an increasing trend toward neuro-

monitoring for high-risk term and preterm neonates. It is

difficult to distinguish the effects of neonatal seizures from

their underlying etiology, and we lack conclusive evidence that

treating neonatal seizures improves long-term outcome. How-

ever, recent data suggest that neonatal seizures may compound

the risk for brain injury and subsequent adverse outcome

among those with HIE [2, 3], and increased seizure severity

has been correlated with worse outcomes among infants with a

range of seizure etiologies [4, 5]. Additionally, in one study, the

duration of neonatal seizures was reduced with the introduction

of reduced montage electroencephalographic (EEG) moni-

toring [6], suggesting the possibility that EEG monitoring

could lead to improved outcomes by detecting seizures and

directing their management.

Indications for Neuromonitoring

Seizure detection is the most common indication for EEG

monitoring. In high-risk populations of neonates, seizures

are common [7, 8, 9, 10] and they often lack outward

clinical manifestations. Many studies have reported that

50 % or more of all neonatal seizures are subclinical [11,

12, 13, 14]. Since subclinical seizures cannot be detected

by bedside clinical observation, their diagnosis relies on

EEG. That most neonatal seizures lack outward clinical

manifestations should not be surprising, since newborns

cannot communicate the sensory phenomena described by

older children and adults during seizures (eg, a rising epi-

gastric sensation during temporal lobe seizures, or visual

phenomena associated with seizures involving the calcarine

R. A. Shellhaas (*)

Department of Pediatrics & Communicable Diseases,

Division of Pediatric Neurology, University of Michigan,

Room 12-733, C.S. Mott Childrens Hospital,

1540 East Hospital Drive SPC 4279,

Ann Arbor, MI 48109-4279, USA

e-mail: [email protected]

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cortex). Fluctuations in heart rate and/or blood pressure

often raise suspicion for seizures in at-risk neonates, but

these events in isolation are rarely caused by seizures [7,

15]. Although some neonates do express clinical manifes-

tations of their seizures, especially prior to administration of

antiseizure medication [13, 16], accurate distinction between

abnormal non-seizure paroxysmal events and clinically

apparent seizures is fraught with difficulties.The distinction between clinical seizures and electro-

graphic seizures is critical, as highlighted by two examples

from the literature:

1) Initial Apgar scores, pH, lactate, base deficit, need for

intubation, and elevated nucleated red blood cells have

been studied as predictors of seizures in newborns with

HIE. When only clinical seizures were evaluated, these

factors appeared to have good positive predictive value

(80 %) [17]. However, when stricter electrographic

criteria were applied, the positive predictive value was

significantly lower (

20 %) [18].2) In a prospective study of high-risk neonates, neonatal

intensive care unit (NICU) staff members were asked to

document suspected seizures while conventional video-

EEG was recorded. Only 9 % of electrographic seizures

(48 of 526) were recognized and documented by NICU

staff, while 78 % of documented paroxysmal events

(129 of 177) had no electrographic correlate (ie, the

events were not seizures) [12].

The gap in the ability to accurately diagnose seizures by

clinical observation alone places infants at risk both for

under-treatment of ongoing seizures and for over-treatment

of events that are, in fact, not seizures. EEG, therefore,

improves the precision of seizure quantification, as well as

the differential diagnosis of paroxysmal events suspected to

be seizures. A sample of events that raise clinical suspicion

for seizures, and can be indications for EEG monitoring in

newborns, is provided in Table 1. This list is not meant to be

comprehensive; rather, it highlights some of the variety of

indications for neonatal EEG monitoring.

EEG monitoring is resource-intensive, requiring costly

equipment, available technologists, and clinical neurophysi-

ologists trained in neonatal EEG interpretation. Not all

infants in an intensive care setting can, or should, be moni-

tored. Rather, intensive monitoring should be targeted at

patients with high risk for abnormal brain function. Newborn

infants with demonstrated acute brain injury, especially those

with concomitant encephalopathy, should be considered at

high risk for seizures. Examples include infants with intracra-

nial hemorrhage or arterial ischemic stroke. Those with high

risk for acute injury, such as infants with encephalopathy who

require extracorporeal membrane oxygenation, newborns

with meningoencephalitis, or those with birth depression from

suspected perinatal asphyxia, may also benefit from EEG

monitoring. Since infants who require pharmacologic paraly-

sis cannot demonstrate any clinical sign associated with

seizures, those with comorbid risk for brain injury can also

be considered candidates for EEG monitoring. Newborns with

suspected cerebral dysgenesis or neonatal epilepsy syndromes

are also clearly at risk for seizures and should be considered

for EEG monitoring. For additional discussion of indications

for neonatal EEG monitoring, readers are referred to theAmerican Clinical Neurophysiology Societys recently pub-

lished guideline [20].

Methods for Continuous EEG Monitoring in Neonates

Conventional Video-EEG

Conventional video-EEG remains the gold standard for neo-

natal seizure detection and quantification. A modified Interna-

tional 1020 System for electrode placement is recommended

(Fig. 1) [20], with additional extracerebral leads including arespiratory channel and electrocardiogram, to assist with as-

sessment of behavioral state and identification of extracerebral

artifacts. Extraoculogram and surface electromyography leads

are often helpful, but are not always required (Fig. 2). The

American Clinical Neurophysiology Society offers guidelines

for the minimum standards for EEG recording [21]. Time-

locked video monitoring is strongly recommended for the

differential diagnosis of paroxysmal clinical events and is

often useful for distinguishing artifacts [20]. A bedside ob-

server is also of utmost importance, as this individual can alert

the EEG reviewer to clinically relevant events by pressing a

patient event marker, entering the event on the digital EEG file

at the bedside, and/or documenting in a flow sheet. Such

events could be typical paroxysmal episodes, administration

of neuroactive medications, or other interventions such as

chest percussion (which can cause artifact on the EEG).

Duration of Monitoring

In general a 60-minute, routine-length neonatal EEG is

adequate for assessment of the interictal background. The

duration is longer than that recommended for a typical older

child or adult, since it is imperative that the recording be of

sufficient length to capture both wakefulness and sleep, if

such state modulation exists. However, a routine-length

EEG is generally not considered sufficient to screen for

neonatal seizures among high-risk patients [20]. Rather,

it is recommended that high-risk neonates be monitored

with EEG for 24 h to evaluate for seizures. Studies have

indicated that most seizures will occur within 24 h of EEG

monitoring [7, 22], although among neonates with HIE who

are treated with therapeutic hypothermia, some data

suggest that continuing monitoring through the cooling and

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rewarming period is most appropriate [8, 9]. While few pub-lished data are available to support this practice, many centers

recommend continuing EEG monitoring until the newborn

infant has been seizure-free for 24 h, except in circumstances

when this is either not feasible or deemed by the treating

clinicians not to be in the infants best interest [20].

When EEG is requested to determine whether abnormal

paroxysmal events correspond to electrographic seizures,

the appropriate duration of monitoring is variable. If the

episodes have no obvious EEG correlate, it is recommended

that the EEG continue until several typical events have been

captured. If the inter-event EEG background is stable and

the events are not seizures, then monitoring for this purpose

can be discontinued.

Longitudinal assessment of encephalopathy can be compli-mented by serial routine-length EEGs. These recordings, which

must be of sufficient duration to capture sleep-wake cycling,

provide the clinician with information about the evolution of a

chronic encephalopathy. For example, serial assessments of a

preterm infants EEG should demonstrate maturation of normal

graphoelements and subsiding discontinuity, with increasingly

well-defined sleep-wake cycling. An infant whose EEG back-

ground patterns demonstrate features consistent with those

expected for infants of 2 or more weeks younger postmenstrual

age is said to have a dysmature EEG (eg, if a 36-week post-

menstrual age infants EEG background is more consistent with

that of a typical 33-week infant, the EEG is dysmature). Per-

sistently dysmature or frankly abnormal patterns are negative

prognostic indicators [23]. In general, the longer the EEG

background remains abnormal, the worse the infants neuro-

developmental prognosis.

There is evidence that therapeutic hypothermia modifies

the EEG background evolution among neonates with HIE.

In this particular circumstance, it may be reasonable to

continue conventional (or reduced-array) EEG monitoring

throughout cooling and rewarming, both for seizure detec-

tion and for evaluation of background trends over time,

since the data can assist with estimating prognosis. For

example, the absence of sleep-wake cycling on amplitude-

integrated electroencephalography (aEEG) after 24 h of age

is a poor prognostic indicator for infants with HIE who are

not cooled [24], but the window for emergence of sleep-

wake cycling lengthens to 48 h for those undergoing hypo-

thermia therapy [25]. Persistence of severe background ab-

normalities, such as burst suppression, beyond 24 to 30 h of

life corresponded to high risk of severe brain imaging ab-

normalities in a study assessing conventional EEG monitor-

ing among infants receiving therapeutic hypothermia [8].

Table 1 Indications for EEG

monitoring

aThese are the most reliable

manifestations of clinically

apparent neonatal seizures [19]bMore than 50 % of neonates

may demonstrate electroclinical

dissociation (clinical signs

vanish while electrographic

seizures continue) after

phenobarbital or phenytoin

are administered [13]

EEG electroencephalographic

Evaluation of abnormal paroxysmal events, such as:

Focal tonic, focal clonic, multifocal clonic episodesa

Intermittent forced eye deviation

Myoclonus

Unexplained apnea

Unexplained autonomic instability (eg, paroxysmal tachycardia or hypertension)

Brainstem-release phenomena (eg, oral automatisms or bicycling movements) Other abnormal movements

Surveillance for subclinical seizures

Initial diagnosis

Assessment of response to anti-seizure medicationsb

Evaluation for seizure recurrence during or after weaning of anti-seizure medications

Assessment of EEG background abnormalities

Assist in estimating prognosis

Amplitude-integrated electroencephalography is well suited for this purpose

Serial routine-length conventional electroencephalography may also be adequate

Fig. 1 The International 1020 System for electroencephalography

electrode placement, modified for neonates, includes the electrode

positions in the boxes. Additional extracerebral channels, including

respiratory and electrocardiogram tracings, are also necessary. Extra-

ocular and surface electromyography leads are often useful, but not

always required

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Amplitude-Integrated EEG

aEEG transforms raw EEG by filtering low (15 Hz) frequencies, rectifying and smoothing thesignal, with a semilogarithmic amplitude compression dis-

played at 6 cm/h [26, 27]. aEEG can be recorded indepen-

dently from, or in parallel with, conventional EEG. If a

single-channel aEEG is to be recorded in isolation, the

parietal electrode positions are recommended (P3 and P4;

Fig. 1), since these are over the cerebrovascular watershed

zones [26] and may detect more seizures than electrodes

positioned over the frontal regions [28]. Most modern aEEG

devices utilize dual-channel recordings, recorded from

central-parietal channels (C3P3 and C4P4). In some

NICUs, both aEEG and conventional EEG are assessed

simultaneously. Most often, this is accomplished by display-

ing the digital trend on the bedside monitor for review by

the patients primary medical team, while the full conven-

tional EEG is recorded and interpreted offline by a clinical

neurophysiologist. This best of both worlds scenario

allows clinical staff to identify concerning changes in the

aEEG background patterns and then contact the clinical

neurophysiologist for confirmation of the findings. More

recently, conventional EEG monitoring groups have sug-

gested employing eight-channel aEEG displays for rapid

detection of background changes and seizures [29, 30].

aEEG can provide prognostically significant data regard-

ing the electrographic background in neonates. The signal is

displayed on a markedly compressed time scale, which

allows the reviewer to assess background trends for multiple

hours of recording on a single screen (Fig. 3). This modality

has been studied in numerous clinical scenarios, including

prematurity [31, 32], HIE [25, 33], congenital heart disease

[34], and so forth. The advantage of this modality is that it is

relatively simple to implement, and does not necessarily

require the skills of an experienced clinical neurophysiolo-

gist. However, there is an important learning curve and a

rigorous curriculum for continuous quality improvement is

strongly suggested [35]. In many NICUs the neonatologists

perform and analyze aEEG independently, although ideally

the clinical neurophysiology service should be involved.aEEG background is interpreted according to a simple

system, based on the amplitude of the upper and lower

margins of the band [36], or a complex pattern recognition

system [27], which utilizes terminology adapted from con-

ventional EEG parlance. Both systems have merits, with

increased interindividual reliability using the simple system

[37] but richer texture in interpretation via the complex

system.

Although aEEG is clearly useful for electrographic back-

ground interpretation, its use for seizure detection is more

controversial. For many years, researchers have reported

that aEEG can be used to detect some seizures [38], but

the limitations of this technique are now being appreciated

[28, 3941]. Neonatal seizures are, by nature, brief and

spatially restricted [42]. More than half of neonatal seizures

last less than 90 s, which translates to a deflection of about

1.4 mm on a typical aEEG screen display [41]. Although the

addition of dual aEEG channels with display of the

corresponding raw EEG improves seizure detection [40],

a significant learning curve remains, and novices are less

likely than experts to detect seizures [41]. Note, too, that the

raw aEEG tracing remains subject to the filtering and

other processing inherent to aEEG, so its appearance is

somewhat different from a single channel recorded using

conventional EEG.

Detailed review of the literature is required to make

certain important distinctions regarding the accuracy of

aEEG for seizure detection. Most studies report relatively

good specificity, but the sensitivity for seizure detection is

generally quite low. Some studies discuss the sensitivity of

this method for detecting seizure-positive records (ie, at least

one seizure detected in a given aEEG tracing containing

seizures), while others report the sensitivity and specificity

Fig. 2 This conventional

electroencephalography was

recorded from a term infant

with hypoxic-ischemic enceph-

alopathy, using the International

1020 System for electrode

placement, modified for neo-

nates, along with extracerebral

channels including respiratory

(not functioning in this screen-shot), electrocardiogram, chin

electromyography, and extrao-

culograms. The black arrows

indicate a focal seizure at the

central vertex (Cz electrode)

with spread to the right central

region (C4 electrode). This

seizure had no clinical correlate


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for the detection of individual seizures. Using single-channel

aEEG, without the corresponding raw EEG, results in a 25 %

to 38 % sensitivity for detecting seizure positive aEEG records

[39, 41] a n d 2 5 % t o 5 6 %for individual seizure detection [40,

41]. Expert aEEG readers sensitivity is better than novices

[41]. Adding a second aEEG channel, along with the raw

EEG, improved sensitivity to 76 %, with 78 % specificity,

for two expert reviewers [40]. Given the limited ability to

identify seizures, aEEG is not considered an equivalent sub-

stitute for conventional EEG monitoring for the purpose of

seizure detection, although it is likely better than no electro-graphic monitoring at all. The consistently high specificity is

reassuring, since this implies that few infants would be treated

based on aEEG monitoring when they do not, in fact, have

seizures.

Other Methods for Digital EEG Trend Analysis

Since conventional EEG monitoring generates a tremendous

amount of data and trained clinical neurophysiologists are

rarely available for real-time 24-h/day assessments, many

centers are turning to digital trend analysis techniques to

complement and streamline EEG interpretation. Research

specific to neonatal EEG is lacking, compared with the

literature for older individuals, but this is clearly an area of

great scientific and clinical interest.

Envelope Trend Analysis

Envelope trend analysis relies on the EEGs amplitude. This

modality presents the median EEG amplitude for successive

epochs, thereby reducing noise created by brief high-

amplitude artifacts. Envelope trend can identify some neo-

natal seizures [43], but brief seizures that are of low ampli-

tude or are associated with movement artifact are difficult to

detect reliably. Further study is required before this comes

into widespread practice.

Density Spectral Array

Density spectral array uses fast Fourier transform and dis-

plays the spectral power of the recorded EEG. Time is

plotted on the x-axis, with frequency on the y-axis, and

power represented by a grayscale or color code. The neuro-

physiologist can select the specific electrodes of interest, or

the power can be averaged for a set of electrodes (eg, an

entire hemisphere). Analysis of the raw EEG is required to

confirm seizures detected with this method, since artifacts

can lead to increased power and result in false-positives.

Spectral edge frequency varies with sleep-wake cycling in

healthy term neonates [44]. This modality has been evaluated

in isolation [30] and in conjunction with aEEG [45], to allow

for efficient interpretation at the bedside, with promising

results.

Automated Seizure Detection

Automated seizure detection is the focus of many research

teams [4648]. Neonatal-specific algorithms are required,

since electrographic features of neonatal EEG are distinct

from those of older individuals. Currently, commercially

available algorithms are in use both for conventional EEG

and aEEG, but they lack specificity and sensitivity. This is

an area of great interest and active innovation.

Fig. 3 This sample amplitude-

integrated electroencephalogra-

phy (aEEG) screenshot was

recorded from a term neonate

with hypoxic-ischemic enceph-

alopathy. Ten seconds ofraw

EEG tracing are displayed

above approximately 3 h of the

corresponding left and right

hemisphere aEEG traces


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Conclusions

Although neonates with acute and chronic cerebral dysfunc-

tion are at high risk for mortality and neurodevelopmental

morbidity, there are opportunities to modify their outcomes.

Interventions, such as therapeutic hypothermia, are emerg-

ing, and new treatments for neonatal seizures are on the

horizon. Certain subpopulations of neonates have substan-tial risk for seizures, most of which are subclinical, and

these seizures may amplify underlying brain injury and

impact long-term prognosis. The only way to accurately

diagnose and quantify these seizures is through EEG, with

long-term conventional EEG monitoring as the diagnostic

modality of choice. aEEG can be employed as a complemen-

tary tool, and is particularly useful for the assessment of

electrographic background evolution over time. Other digital

trending modalities are emerging, and may supplement and

streamline EEG interpretation. With an increasingly keen

focus on clinical neonatal neurology, and an active and rich

research environment, there is hope that outcomes for thesehigh-risk patients will be optimized.

Disclosure Conflicts of interest: R.A. Shellhaas: has received grant

support from NICHD (5K23HD068402-02), Child Neurology Foun-

dation Shields Fellowship Award, and University of Michigans Janette

Ferrantino Award and Woodson Biostatistics Fund.

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