The Pediatric Scoring Challenge

Obstructive sleep apnea syndrome (OSAS) in children is associated with gas exchange abnormalities and sleep disturbance.¹ In general, children with OSAS have preserved sleep architecture.² When compared with that of adults, obstructive events in children are not as frequently terminated by arousals. Thus, the study of frequency of arousals, as a potential marker for sleep disturbance in children, has been an interesting topic of research.

The definition of arousal
“Arousal” is defined as a transient intrusion of wakefulness into sleep. In contrast, when an arousal lasts for longer than 15 seconds,³ and/or with a behavioral component (eye opening or crying), it is called an awakening. Arousal during sleep is a key mechanism by which sleep becomes a reversible process, in the face of a noxious environmental stimulus. This, presumably, forms a very important protective mechanism for the living organism.

Variable definitions of arousal have been used. In the1960s, Rechtschaffen and Kales defined “movement arousal” as any increase in electromyographic activity accompanied by changes in the electrooculogram or EEG channel.³ Then, in 1992, the American Sleep Disorders Association (ASDA) defined arousal mainly based on EEG changes.⁴ This has frequently been termed “cortical arousals” or “EEG arousals.” More recently, “autonomic” or “subcortical” arousals have been used to define the autonomic activation that occurs spontaneously or in association with a respiratory event.

Since its publication, the ASDA-defined EEG arousals have gained wide popularity and acceptance. According to the ASDA (now the American Academy of Sleep Medicine or AASM), an EEG arousal is defined as an abrupt shift in EEG frequency, which may include theta, alpha, and/or frequencies greater than 16 Hz, but not spindles.⁴ By definition, they should be preceded by sleep, of at least 10 seconds duration, and should last for at least 3 seconds. A concurrent submental electromyographic amplitude is required if they are scored in REM.

As the ASDA explained, the minimum duration criterion is a methodological as opposed to a physiological decision, as identification and agreement on events of shorter duration are difficult to achieve in adult studies.⁴

Subtypes of EEG Arousals
Three subtypes of EEG arousals are seen in children with OSAS, which include the following:

Spontaneous arousals: These are referred to as arousals that are present in normal sleep and are termed “spontaneous” as they are believed to be physiological, meaning that they do not constitute a disturbance of the normal sleep process.

Respiratory-related arousals: These are arousals that are associated with respiratory events. Currently, the association has been loosely defined as those arousals immediately following a respiratory event.

Respiratory arousals are both protective and deleterious. On the one hand, they are regarded as a protective reflex, since they reestablish an open passage for the upper airway.⁵ On the other hand, frequent arousals have been associated with significant sleep fragmentation, and daytime symptoms.⁶

Arousals related to environmental stimuli: These include arousals related to various environmental stimuli, such as loud noises, tactile stimuli, and temperature changes. Under normal circumstance, these arousals should be present in small numbers during nocturnal sleep.

Arousals in Children
The frequency of arousals during nocturnal sleep is termed the arousal index. This is defined as the number of arousals per hour of total sleep time. In adults, the spontaneous arousal index increases linearly with age.^7,8 Data in children, however, suggest a fairly constant index of around seven to nine per hour across the age group (see Table 1). Note that arousals in infants are very different from those in children. Specific rules for scoring arousals in infants have been published,⁹ but are beyond the scope of the present discussion.

Table 1. Spontaneous arousal indices in children.

In general, children are much less arousable than adults.² Obstructive apneas in adults are frequently followed by arousals. In contrast, only approximately 30% of the obstructive apneas are followed by EEG arousals in children.¹⁵ Does this reflect that children with OSAS are more protected from developing arousals than the adults? Or does this mean that the EEG arousal is not a sensitive measure in children?

The key idea for quantifying EEG arousals by the ASDA is that these arousals are considered deleterious when present in significant numbers.⁴ This is because they cause fragmentation of sleep, rather than simply causing slight shortening of duration of sleep. The other key idea is that spontaneous arousals are considered normal as they presumably do not disrupt the normal sleep process.

Following this idea, for respiratory arousals to disrupt normal sleep, they have to either result in a different arousal pattern or exceed a certain “physiological threshold” in number. Whether respiratory arousals are different from spontaneous arousals at the EEG level is still unknown. But at least they appear identical by gross visual inspection on the surface EEGs. On the other hand, although the threshold model appeared reasonable, the threshold level beyond which sleep becomes significantly disrupted is still unclear.

Table 2. Arousal indices in children with OSAS.

Regardless of the above models, children are much less arousable in response to a obstructive apnea than adults. Most obstructive apneas in children are not followed by arousals, and the total arousal index is only modestly elevated in most children with OSAS (see Table 2 ). Thus, children with OSAS appear to have a depressed arousability when compared with adults. Recent work by Moreira et al showed that children with OSAS have similar arousability to controls in response to nonrespiratory (acoustic) stimuli.¹⁶ This suggests that the depression in arousability is not global. Alternatively, the obstructive apnea in children may not be as strong a stimulus to EEG arousal as in adults.

In summary, because children with OSAS are less arousable by obstructive apneas than adults, their overall arousal index tends to be lower. The link between the arousal index and the degree of sleepiness in children with OSAS has not been clearly established.

Issues in Scoring Children
Currently, controversy exists on the duration criteria for arousals in children. It is known that obstructive events of shorter duration are clinically relevant in children.¹ Thus, it is reasonable to hypothesize that shorter arousals are also clinically important in children. Along with this, some have proposed a few modifications for scoring arousals in children. Various authors have suggested duration criteria as short as 1 second.^18-21
Similar to that reported in adults by the ASDA, the scoring of arousals shorter than 3 seconds in children has been technically difficult and unreliable. Available data show that even in the research setting, the interscorer agreement for scoring such shorter arousals is very poor (see Table 3).

Table 3. Interscorer agreement for scoring shorter arousals in children.

In search of a better way to quantify sleep disruption in children with OSAS, sleep scientists have proposed several other indices in recent years. In particular, autonomic arousals such as pulse transit time arousal index¹³ and sleep pressure score²³ have been reported. In addition, some suggest that the cyclic alternating pattern is more sensitive than ASDA arousals in description of the degree of sleep fragmentation in OSAS.^12,24

Summary
In conclusion, the mean arousal index in normal children (excluding infants) is approximately seven to nine per hour of total sleep time. Age does not seem to have a significant impact on the arousal index. Children with OSAS have a higher arousal index than normal children; however, respiratory arousals in children with mild to moderate OSAS did not outnumber spontaneous arousals. Whether these respiratory arousals have a major impact on the pathophysiology of OSAS in children remains to be studied. Various modified ASDA arousal criteria and studies on autonomic arousals and the cyclic alternating pattern have been published; however, at the present moment, arousal scoring in children should follow the ASDA criteria until a new reliable standard has been established.

Tat-Kong Wong, MD, MBBS, is director of the Pediatric Sleep Service at the Pamela Youde Nethersole Eastern Hospital, Hong Kong. Carole Marcus, MD, MBChB, is professor of pediatrics at the University of Pennsylvania, Philadelphia, and director of the Sleep Center at Children’s Hospital of Philadelphia.

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