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 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.FIG. 1: Examples of EEG background classification by voltage.Preterm A healthy preterm infant is considered awake when the eyes are open. This remains its premier clinical characteristic until 32 to 34 weeks of 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 of 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, 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 (Figs. 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) (Clancy and Wusthoff, 2011). 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 of PMA. Brief and inconsistent periods of continuous EEG activity occur first in waking state and active sleep along with rapid eye movements at 25 weeks of PMA (Scher et al., 2005a). Movements (face and body) in active sleep tend to be segmental myoclonus or generalized myoclonic and tonic posturing. By 28 to 31 weeks of PMA, there are some periods with complete features of active sleep (eyes closed, rapid eye movements, irregular respirations, body movements, and continuous EEG). After 34 weeks, active sleep consistently has continuous EEG activity.FIG. 2: Examples illustrating the contrasts between tracé discontinu, tracé alternant, excessive discontinuity, and burst suppression. EEG tracings courtesy of Clancy and Wusthoff, 2011. A, In tracé discontinu, the bursts are separated by very low voltage, suppressed IBIs. There are no artifacts from EMG activity or movement, and the respiratory pattern is quite regular. B, 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. C, This excessively discontinuous record from a term infant with an acute encephalopathy showing prolonged IBIs, although with some normal features present during bursts, such as the conspicuous encoche frontale seen near its onset (arrow). D, Burst suppression, in contrast, contains prolonged, extremely suppressed IBIs and bursts composed exclusively of abnormal electrical activity.Quiet Sleep Term. In the healthy term neonate, quiet sleep is clinically characterized by eye closure, absence of rapid eye movements, 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 (Figs. 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) (Lamblin et al., 1999) 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 composed of nonstop, high-voltage (50–150 µV pp) delta and theta activity. Sleep spindles around 10 to 12 Hz first appear within this continuous slow wave sleep pattern by 46 weeks of 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 approximately 28 weeks of PMA. By 34 to 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 (Hahn et al., 1989). By 37 to 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 the 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 with preterm babies. It is also easier to detect in long-term recordings than brief routine tracings (Scher et al., 2005a). Term. In the term infant, a complete sleep and waking cycle typically has a duration of 3 to 4 hours (Scher et al., 2005b). An isolated sleep-only cycle typically lasts 40 to 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 4 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% to 60% of the sleep cycle in active sleep, 30% to 40% in quiet sleep, and 10% to 15% in transitional sleep. Preterm. The proportion of time spent in any state also varies by age (Curzi-Dascalova et al., 1988; Scher et al., 2005a). The first rudimentary evidence of sleep cycling can be seen at 25 weeks of PMA. At 27 to 34 weeks of PMA, 40% to 45% is spent in active sleep, 25% to 30% in quiet sleep, and 30% in indeterminate sleep. Beyond 35 weeks of PMA, infants spend 55% to 65% of the time in active sleep, 20% in quiet sleep, and 10% to 15% in indeterminate sleep. The duration of a sleep cycle (first active sleep, then transitional sleep and finally quiet sleep) is 30 to 50 minutes for neonates <35 weeks of PMA and increases to 50 to 65 minutes beyond 35 weeks of 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 1 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 (Table 3).TABLE 3: EEG BackgroundContinuity Normal Continuity EEG activity is continuous when there is uninterrupted, nonstop electrical activity with <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 to 50 µV pp for 2 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 (Hahn et al., 1989; Lamblin et al., 1999) (Table 4). 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.TABLE 4: Normal IBI Duration and AmplitudeNormal Discontinuity There is a progressive decrease in normal IBI durations with increasing PMA (Hahn et al., 1989; Lamblin et al., 1999). Tracé discontinu, as defined above, is a normal discontinuous EEG pattern in preterm infants (Figs. 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 to 40 weeks of PMA. It appears first in wakefulness, active and quiet sleep (until 30 weeks of PMA), then only in quiet sleep and is rarely seen in infants of 38-week PMA or older (Hahn et al., 1989). 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 to 150 µV delta activity alternate with lower voltage theta activity of 25 to 50 µV, these lower voltage periods never completely attenuate. In contrast to tracé discontinu, the voltages are never <25 µV pp (Lamblin et al., 1999) (Figs. 1, 2B). Like tracé discontinu, the abundance of this pattern varies by age. Tracé alternant is first seen at 34 to 36 weeks of PMA, which becomes minimal by 42 weeks and is no longer seen by 46 weeks of PMA. Excessive Background Discontinuity In sick newborn infants who have experienced a variety of causes of encephalopathy (such as HIE, intracerebral bleeding, septic meningitis, etc.), the two main reported categories of background abnormalities are pathologically excessive discontinuity and abnormally low voltage for PMA (Clancy et al., 2011). 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 4 (Figs. 1, 2C) (Clancy and Wusthoff, 2011). 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 (Figs. 1, 2D). However, the definition does allow for one electrode with sparse activity during the IBI up to 15 µV pp or less than 2 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 because of internally mediated lability and no EEG change of reactivity because of 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 nonspecific 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, whereas excessively discontinuous records have some normal patterns identifiable within the bursts. Similarly, burst suppression is an invariant pattern, whereas excess discontinuity contains some variability or reactivity. If burst suppression typical burst and IBI duration should be Further characterization should include a of the of the of a typical burst and and of In some the bursts are composed of nonspecific but in sharp waves appear admixed within the bursts. Normal In the normal neonatal electrical voltages, and the of specific, named graphoelements should be between of the two The and should be more or less of each This for transient to while still considering the record The of more than a difference in voltages between of the two or a of background features, the electrical frequencies and the of specific graphoelements between the two is abnormal. bleeding, for up to 10% of acute neonatal EEG background are not and may be is defined as the onset of bursts of activity that occur between in the discontinuous portions of the recording. For example, a single burst within tracé discontinu would be considered if the of the and bursts occur within seconds of each The the percentage of bursts that are within the discontinuous portions of the Normal The percentage of bursts is not a function of PMA. 27 to weeks of PMA, EEG activity is completely (Clancy et al., et al., and 30 weeks of PMA, EEG activity may only be approximately approximately 30 to 37 weeks of PMA, more activity emerges until term when the EEG is Normal As above, some of is expected and normal between 30 and 37 weeks of PMA. By weeks of PMA, the EEG should not show any amount of This is defined as a clearly excessive percentage of EEG bursts for PMA that occur than seconds between the onset of activity in each during the discontinuous portions of the recording. studies have defined 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 abnormalities should be interpreted with because many (such as electrode or electrode and can result in low voltage EEG activity or voltage voltage are difficult to Normal A healthy term infant should have most EEG activity µV pp in all behavioral states. This is defined as a continuous EEG background some normal activity and graphoelements with voltages persistently at least 10 µV but <25 The clinical significance of low voltage is not voltage suppressed. There are various definitions in the literature of an abnormal background because of a low voltage or voltage pattern et al., et al., et al., We a definition of persistently low voltage activity without normal background features. The voltage is µV pp. The background can be with higher voltage µV pp) transient activity for <2 In the record is invariant, with no and with no EEG changes from external This pattern severe neurologic with or of the cortical of EEG activity. This terminology is used to describe the absence of cerebral electrical activity µV pp when at a of 2 and The term has replaced the terms and recordings, although their are the guidelines the technical for an EEG to for Clinical Neurophysiology These are from the technical for neonatal EEG recordings. If the EEG is not to these the term should not be If there is no cerebral activity, 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 pattern when with clinical is used to determine cerebral 1989; and 1989; and et al., are to their guidelines regarding the of brain for newborn as conspicuous spontaneous EEG to such as that occur during typical sleep–wake It is first present by 25 weeks when the EEG changes with state. should be by 28 weeks of PMA and by 30 to 31 weeks of PMA. The EEG can of changes in any electrical or It is to note that from sleep can result in transient attenuation of EEG voltages, which should not be for should be recorded as or For example, variability would be present in a recording, which multiple behavioral states such as wakefulness, transitional, active, and quiet sleep. The last might for example, in a recording that only an awake state. of EEG is when there is a conspicuous cerebral EEG to external Like these EEG also of changes in any electrical or The clinical and behavioral of reactivity can include movement, EMG activity, and respiratory pattern changes. It is to note that after or external behavioral may artifacts from movement or EMG activity that may changes of the EEG first appears at 30 to 32 weeks of PMA, but it might not been seen with each and external should be recorded as or of should be noted. The in which the term very premature infants with such as their EEG background features to mature at the same as their PMA There a between their PMA and their as by the of their EEG This in between the PMA and their is termed defined as an EEG that would be normal for an infant at least 2 weeks than the PMA. The persistently EEG is considered abnormal and is with an risk of abnormal neurologic et al., and BACKGROUND In neonatal graphoelements are and named EEG background patterns that first appear and then during particular epochs of neonatal are characteristic of specific are a of the composition of the normal EEG background and are typically of specific is included we have defined the most seen (Table Normal This pattern occurs between and 34 weeks of PMA and consists of high voltage to µV pp) delta activity with a

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