Ontogeny of sleep and awake states in relation to breathing in preterm infants

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Abstract

This review will focus on the development of behavioural states and breathing during early developmental stages prior to term gestation. Although these behavioural states are immature during early development, their cyclicity is clearly seen. Preterm infants characteristically have a large proportion of indeterminate sleep and small amount of wakefulness. Whereas oxygenation is relatively stable during active and quiet sleep in ventilated preterm infants, indeterminate sleep and arousals are associated with hypoxaemic episodes. Arousals have also been linked to apnoea in spontaneously breathing infants. Since well-defined sleep cycles are beneficial for the oxygenation of preterm infants, we should explore ways to promote their natural sleep while they are exposed to neonatal intensive care. Care practices such as clustering procedures, kangaroo care and optimal positioning have been shown to improve the integrity of sleep. Optimizing the sleep cycling might improve the long-term outcome of preterm infants. More studies in this area are clearly needed.

Section snippets

Development of behavioural states and breathing in preterm infants

Anders et al.1 introduced scoring principles for behavioural states in newborn infants in 1971. The manual defined six behavioural states in a full-term newborn: three sleep states (Quiet sleep = non-rapid eye movement (NREM) sleep; Active sleep = rapid eye movement (REM) sleep; Indeterminate sleep) and three awake states (Quiet awake; Active awake; Crying; see Table 1). Since then, improved survival of preterm infants and technical advances have enhanced our understanding of behavioural states at

Development of fetal behavioural states and breathing

The distribution of fetal and neonatal states at the corresponding gestational ages seems to be strikingly similar despite the profoundly different environment in and ex utero (Fig. 1A–C). Fetal states have been classified analogously with newborn states using four categories22 excluding indeterminate sleep and crying (Table 3). Since fetal EEG recording is not available in human studies, fetal behavioural states are classified using heart rate pattern, eye movements and gross body movements as

Frequency and regularity

Respiratory frequency is higher during active sleep compared to quiet sleep in preterm infants from 35 weeks,38, 39, 40 leading to higher minute ventilation during REM sleep.41 Although breathing is more often regular during quiet sleep, in preterm infants irregular breathing may also occur during quiet sleep.2 During active sleep breathing is always irregular.

Paradoxical breathing

Paradoxical breathing, i.e. inward chest movement associated with abdominal expansion during inspiration, occurs more frequently during

Behavioural states and breathing in ventilated preterm infants

It is unclear if assisted ventilation itself alters sleep cycling and sleep structure. Karch et al.58 found more quiet sleep in ventilated infants. Curzi-Dascalova et al.3 concluded in their study that artificial ventilation does not alter sleep organization in preterm infants at 31–34 weeks of gestation. However, they found significantly shorter sleep cycles in ventilated infants compared to non-ventilated infants (39 min versus 60 min). In our study,7 a sleep cycle length of 60 min was observed

Experimental challenge situations

The ventilatory responses to changes in oxygen (O2) and carbon dioxide (CO2) are dependent on sleep states in preterm infants. Hyperoxia appears to lead to longer apnoea during active sleep. In response to hypoxia, a late decrease in ventilation was more prominent during active sleep and the awake state.57 This suggested that breathing has more ‘fetal’ features during active compared to quiet sleep while the ontogenically younger quiet sleep, showed more mature responses to O2 challenges. In a

Conclusions

Maturational trends in behavioural states are strikingly similar across studies despite a range of definitions and environments both intra- and extrauterine. The maturation of breathing occurs in synchrony with other behavioural state criteria.

Many studies comparing the development of breathing in relation to sleep states have, a priori, excluded other behavioural (non-sleep) states. Although this is understandable since measurements become technically much more challenging when infants are

Acknowledgements

This study was supplied by NIH grant HL62527.

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