American Clinical Neurophysiology Society Standardized EEG Terminology and Categorization for the Description of Continuous EEG Monitoring in Neonates

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 (Clancy et al., 1988; Murray et al., 2008). For these reasons, continuous video EEG monitoring is a useful tool in the intensive care nursery. The American Clinical Neurophysiology Society has recently produced guidelines regarding methods and indications for continuous EEG monitoring in neonates (Shellhaas et al., 2011). A challenge in EEG monitoring of neonates is to understand the clinical significance of various EEG patterns. In the adult population in intensive care unit, there has been extensive debate, for example, regarding the importance of fluctuating rhythmic patterns (Hirsch et al., 2004; Oddo et al., 2009; Orta et al., 2009; Vespa et al., 1999). The American Clinical Neurophysiology Society Critical Care Monitoring Committee has generated standardized terminology of rhythmic EEG patterns in the critically ill to facilitate multicenter collaborations to determine whether these patterns have clinical significance (Hirsch et al., 2005). 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 on this initial effort. Many of the studies on which these criteria are based used 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. It is hoped 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 the following (Table 1). Documentation of the patient’s postmenstrual age (PMA = gestational age, measured from the time of the last menstrual period + chronological age) at the time of recording (Engle, 2004) (We use the term PMA 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 approximately 2 weeks before conception.). a) Term = 37 up to 44 weeks of PMA b) Preterm = less than 37 weeks of PMA c) Post term = 44 to 48 weeks of PMA Documentation of neuroactive medications at the time of recording. This includes sedatives, hypnotics, anxiolytics, general anesthesia, and antiepileptic drugs. An ideal report would also document when these medications are administered during the recording. Documentation of the depth and duration of hypothermia during the recording, and whether it is spontaneous or induced. An ideal report would also document the clinical changes that have the potential to impact cerebral function. These would include sudden hemodynamic instability, rapid changes in respiratory function, or cardiorespiratory failure. Documentation of the number of hours of recording that cannot be interpreted as a result of technical problems. Detailed characterization of the background EEG features during the first hour of recording. Presence or absence of state changes must be included. Characterization of 1 hour of background recording within each 24-hour period of EEG monitoring. Characterization of additional epochs of background when there are relevant changes. Relevant changes include evidence for not only the increasing encephalopathy but also the new development of episodic state changes. 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. TABLE 1: Details to Include in Daily EEG ReportThe 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-week chronological age infant born at 35 weeks of estimated gestational age (PMA = 40 weeks) compared with 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, the age difference of a few weeks 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 infants. 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 1 minute or longer (Table 2).TABLE 2: Behavioral StateAwake 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)] mixed frequency activity with a predominance of theta and delta and overriding beta activity (Fig. 1) (all voltages included in this article refer to pp values). This is traditionally or EEG background term infants have and there are spontaneous of the and 1: of EEG background A healthy preterm infant is awake when the eyes are This clinical to weeks of when polysomnographic respiratory or and the of and are also with of the awake EEG are continuous at weeks of The awake background is continuous weeks and continuous weeks and in the neonate is as and has distinctive EEG and polysomnographic features. The healthy term neonate in has the eyes of rapid and with and The EEG background from that of normal the normal in healthy preterm This EEG is of high voltage µV activity that are low voltage interburst µV (Clancy and 2011). The duration of the low voltage interburst is on being in the PMA infants. The of EEG activity have expected and such as delta activity and patterns that are before weeks of and of continuous EEG activity first in state and with rapid at weeks of PMA et al., and in to be or and to weeks of there are with features of rapid and continuous has continuous EEG 2: the between and EEG of and In the are very low There are no from activity or and the respiratory is In this of there is an of high and low voltages but no that are There are no from activity or and the respiratory is This record from a term infant with an encephalopathy with normal features present during such as the in extremely and of abnormal In the healthy term is absence of rapid and for activity or The EEG background evolves from the less in the preterm It the in which voltage µV of delta activity and to with voltage µV et al., interburst of mixed theta and delta These interburst of in the of with low to medium mixed frequency with age and is weeks and it is in the continuous background of µV delta and theta to first within this continuous weeks of In the very preterm of the EEG background is in behavioral and are from greater of is the of first emerging approximately weeks of to is only in The of time with a with increasing PMA that a term infant has of in et al., 37 to 40 as In between of and there are in which features for a specific behavioral state are These clinical and EEG features of the and behavioral not the polysomnographic and EEG background criteria for a specific as For example, in the from to an infant but an EEG that is between and This of the two is and the criteria for can be of as a period of as of the EEG in which the eyes are but in which clinical and EEG features not to or are as These the features for to a is a of of the is in very preterm infants in there is not a between the EEG background and polysomnographic a of time is in healthy term infants. A high of time that is would be abnormal at cycling is the of behavioral is distinctive and to recognize in term compared with preterm It is also to in recordings than et al., In the term a and has a duration of to hours et al., An 40 to and in a The awake term infant first an This is about term may in the first of and be continuous Term neonates approximately to of the in to in and to in The of time in state also age et al., 1988; et al., The first evidence of cycling can be at weeks of to weeks of to is in to in and in 35 weeks of infants to of the time in in and to in The duration of a and is to for neonates weeks of PMA and to to 35 weeks of state changes. In a infant with of normal background features, it may be or to identify specific However, infants can have state changes, as cycling between EEG patterns as the of background or with at 1 minute in each EEG BACKGROUND The of normal neonatal EEG background with In the following the features of both normal and abnormal EEG will be (Table EEG EEG activity is continuous when there is activity with of voltage µV The of the normal EEG background from the in behavioral in extremely premature infants to continuous EEG in in infants. EEG activity is as voltage of activity voltage The of are termed interburst intervals The in of the are a function of age, being in very preterm infants and during at We the as a period in which activity is to µV pp for 2 or The has historically various for EEG patterns on the of The are from these et al., et al., (Table The background can be there is activity within the in a single or a single in and There is a in normal with increasing PMA et al., et al., 1999). as is a normal EEG in preterm infants The activity within the includes graphoelements such as rhythmic delta activity and named patterns that are It is present in from to 40 weeks of It first in and weeks of only in and is in infants of PMA or older et al., as a of from to It is only in In the from to the of the voltages the of have been of to µV delta activity with voltage theta activity of to these voltage In contrast to the voltages are µV pp et al., the of this is first at to weeks of which weeks and is no longer weeks of In infants have a of of encephalopathy as the two of background are and low voltage for PMA (Clancy et al., 2011). We the term to with that normal patterns and graphoelements that are or voltage for as the in (Clancy and 2011). This is an that can be and future standardized to correlate with of EEG in the This of EEG and low voltage as voltages µV pp However, the definition for with activity during the up to µV pp or less than 2 with activity up to µV pp or in voltage in In the EEG should be with no spontaneous changes of and no EEG of of of the infant. The of high µV or low µV voltage activity in the should be The of the of the EEG activity is and but is of specific graphoelements such as delta delta or This is a from has no normal features within the have normal patterns within the is an variability or and duration should be characterization should include a of the of the of a and and of In the are of but in within the In the normal neonatal and the of named graphoelements should be between of the two The and should be or less of each This for to considering the record The of than a difference in voltages between of the two or a of background features, the and the of specific graphoelements between the two is abnormal. for up to of neonatal EEG background are not and may be is as the of of activity that between in the of the recording. For example, a single within would be the of the and within of each The the of that are within the of the The of is not a function of to weeks of EEG activity is (Clancy et al., et al., and weeks of EEG activity may only be approximately approximately to 37 weeks of activity term when the EEG is of is expected and normal between and 37 weeks of weeks of the EEG should not of This is as a of EEG for PMA that than between the of activity in each during the of the recording. studies have the normal for voltage (or in premature infants. there will be no to normal voltage criteria for in this The focus of this will be the of normal voltage for the term infant (Fig. 1). as with the older child or adult, voltage should be interpreted with many as or and can result in low voltage EEG activity or voltage voltage are to A healthy term infant should have EEG activity µV pp in behavioral This is as a continuous EEG background normal activity and graphoelements with voltages at µV but The clinical significance of low voltage is not voltage There are various in the of an abnormal background of a low voltage or voltage et al., et al., et al., We a definition of low voltage activity without normal background features. The voltage is µV The background can be with voltage µV activity for In the record is with no and with no EEG changes from This neurologic with or of the cortical of EEG This terminology is used to describe the absence of cerebral activity µV pp when at a of 2 and The term has the terms and recordings, are the guidelines the technical for an EEG to for Clinical Neurophysiology These are from the technical for neonatal EEG recordings. the EEG is not to these the term should not be there is no cerebral but the recording not to the the report should that the recording may be with but should that cannot be without the technical is a when with clinical is used to determine cerebral and and et al., are to guidelines regarding the of brain for as spontaneous EEG to such as that during sleep–wake It is first present weeks when the EEG changes with should be weeks of PMA and to weeks of The EEG can of changes in or It is to note that from can result in of EEG which should not be for should be recorded as or For example, variability would be present in a recording, which behavioral such as and The last for example, in a recording that only an awake of EEG is when there is a cerebral EEG to these EEG also of changes in or The clinical and behavioral of can include and respiratory changes. It is to note that or behavioral may from or activity that may changes of the EEG first at to weeks of but it not been with each and should be recorded as or of should be noted. The in which the term very premature infants with such as EEG background features to at the same as PMA There a between PMA and as the of EEG This in between the PMA and is termed as an EEG that would be normal for an infant at 2 weeks than the The EEG is abnormal and is with an risk of abnormal neurologic et al., and BACKGROUND In neonatal graphoelements are and named EEG background patterns that first and during particular epochs of neonatal are of specific are a of the of the normal EEG background and are of specific is included we have the (Table This occurs between and weeks of PMA and of high voltage to µV delta activity with a It may be but is (Clancy et al., and and have been many or of These are between and weeks of PMA and of a of to of to µV pp with activity or et al., 1999). is between and weeks of are in up to weeks and that are in and and are in between and 37 weeks of PMA (Clancy et al., et al., are in up to 40 weeks of This occurs between and weeks of It of to µV pp theta frequency activity for over the It is and between and weeks of PMA (Clancy et al., et al., et al., similar activity can be at the and this is a normal It first at weeks and 44 weeks of It of to µV pp delta which may in or for a few over the (Clancy et al., et al., 1999). It is and This is to and the two are over the (Fig. between and 44 weeks of PMA and of to µV pp with a initial and a (Clancy and et al., et al., 1999). are and are present in and in the from to (Clancy et al., et al., the between and are present and in both A is in the in the periodic are in the These and in the same The first are with to the EEG which is the cerebral there are also EEG patterns that may the background (Table EEG Many healthy neonates have abnormal or that There regarding the that separate from are or and A has an initial and that is A has an initial and that is to be from the background as separate and not background are to are It is that the neonatal of time the of the and many EEG features will than the recording at the adult or of of the of number of or minute at a such as the or should be in the continuous of the neonatal or In the of the particularly during the EEG have activity within the rather than EEG separate from the can at may as or in or to are in the of healthy and term infants (Fig. are the of a normal EEG background for in in the and are in the and are between of the are but a few may in or et al., These as or (Fig. in the of an abnormal EEG background for may also in the or may be in or rather than being or may also be in such as the or may be compared with for neonates at 1 or older that than hour for preterm and hour for term infants are abnormal et al., and and et al., et al., et al., EEG are than to in or these first in the of preterm infants in the and it that many at the with to the (Clancy and It is that and are with et al., In the term in the can such a or However, these are to can be in term infants. that up to hour for preterm and hour for term neonates may be normal and et al., This EEG of rhythmic patterns of activity that many with seizures but are very with a duration of et al., et al., These have been in the as and rhythmic that the significance of these is the term rhythmic will be used are in the of an abnormal EEG background are in in a normal this significance is not However, studies in that clinical changes can with 2 in duration et al., a similar and neurologic for infants with as with seizures et al., 2011). is to understand the and significance of in the neonate. seizures are traditionally as clinical or only A clinical only seizure of a sudden of abnormal clinical changes that not correlate with a EEG These clinical changes may include sudden or or or An seizure features clinical seizure with an EEG seizure and An EEG only seizure refers to the of a EEG seizure that not specific visible clinical For the of this the term refers to seizures, with or without clinical of seizure (Table and seizure is a abnormal EEG a and with a 2 µV pp voltage and duration of at A seizure is an abnormal and should not be with background changes, such as with or from is as an in or In rhythmic but with would be and not activity than but without would be periodic or rhythmic activity but not a seizure (Fig. 2 µV pp the of the beginning and end of each the voltages as the seizure evolves and can be up to µV pp or seizures in older and there is no frequency in the definition of be as separate seizures, or must separate two seizure (Clancy and et al., of a seizure can be In the older child and adult, the American Clinical Neurophysiology Society standardized research terminology the and frequency during a seizure (Hirsch et al., 2005). This is of significance in the neonate. can be in terms of the focus of and the number of terminology to describe seizure includes the of seizures of extensive This with and can have and a seizure with activity in two but which and of each seizure from to of the seizure within a single or When a seizure is to a it can be as or or it can be as and When seizures from a single general can be as seizures from at with at in each It is not for such as a to seizures, such as may has been in various (Clancy and et al., Murray et al., et al., et al., 2011). We seizure for clinical of the following the number of seizures hour or of the record with the duration of the seizures the duration of an of or The of seizure that be used for research includes the of seizures in each of hour et al., In this the neonatal be of and (or and each single is only The seizure can be calculated for each of the of which provides a of seizure is to determine the of these The definition of status in and is a single seizure than or a of seizures at between which brain function has not been These criteria are to to the status and the high of of neonatal status have been et al., In consensus with the we a status as present when the duration of seizures of an In or of hour of recording seizures, status exists for that In a population of neonates with recorded seizures, the of recording time in which seizures are from to It is that definition of status is a and that there are no that specifically the of over as especially or research of status be based on the regarding of neonatal In two studies in the EEG seizure 1 with of seizures (Clancy and and In these and the of seizure duration to and the seizure 2 to (Clancy and et al., and In future it will be useful to of seizure and duration of status as to rhythmic patterns not the in or of These are of in the older population in intensive care are and clinical significance is rhythmic and periodic patterns in preterm and term neonates but are not and It is whether research terminology that has been in is to the neonate (Hirsch et al., 2005). We the patterns from the adult which have been in neonatal (Table and of are in the adult terminology as a in which have a and there is a between and the at are as with no than the no than or or of number of In are as than and at the at is as a from to the in the of (Fig. are not in neonates but can with such as or et al., et al., and delta activity is in the adult terminology as the of a with and duration but without an between as the duration of the of the rhythmic must from the duration of the for the of this EEG may not be abnormal in neonates and is with normal neonatal rhythmic delta activity and The periodic or rhythmic must be present for at for or for 2 can be in terms of the focus of and can be or includes and In there is of The term can be to the activity has a may also be or information may include a of the For can or not is as an in that is at greater than that in on an or recording. is as an in that is at greater than that in on an or recording. is as an in that is at greater than in on an or recording. For or can the or or specific is not and whether the activity is or activity is but the or or can be over both patterns can be terms to the American Clinical Neurophysiology Society Standardized Critical Care EEG The not to neonates this a neonatal that from the adult terminology are the is not continuous, the duration of is are and the adult terminology also recording the continuous duration. hour to 1 to to from for of In periodic duration in the preterm infant less than 1 minute and than 1 minute in term infants and of preterm and term infants duration we duration to be with terminology used in the intensive care for adult we recognize that very few neonatal EEG patterns will the or In neonatal recordings, should be in the and should be for the with the only for a only to periodic and the of not rhythmic delta is as or only to periodic and the of but not to rhythmic delta should be for a for both the with and the include the have a duration measured at the EEG have a duration of to theta and delta have a to of the at but are in duration to as a have a or This document is a collaborative to the neonatal EEG terminology. We this multicenter collaboration to determine the significance of continuous EEG in critically ill may on this to establish the of the terms and definitions, both in the research and clinical This terminology will be and based on the feedback and future research.

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