Association between slow-wave activity, cognition and behaviour in children with sleep-disordered breathing

Highlights

• Children originally diagnosed with sleep-disordered breathing (SDB) during early childhood continue to show reduced behavioural and cognitive performance compared with control children three years following complete resolution of disease.

• Irrespective of the severity of the original disease, improvements in slow-wave activity and the number of respiratory events have concomitant improvements in daytime functioning, although not to the control levels.

• Irrespective of whether SDB completely resolves or not, children whose quantitative sleepiness improved over time have improved sustained attention and a reduction in externalising behaviours.

Abstract

Background

It has been suggested that impaired dissipation of slow-wave activity (SWA) in children with sleep-disordered breathing (SDB) may be a potential mechanism for daytime dysfunction. We aimed to examine whether resolution of SDB resulted in normalisation of SWA dissipation and whether this was associated with improved cognition and behaviour.

Methods

Children (aged 3–6 y) diagnosed with SDB and age-matched non-snoring control children were followed up for 3 y after a baseline study. At the follow-up, children were categorised into control (N = 13), resolved SDB (N = 15) and unresolved SDB (N = 14). Delta activity on the electroencephalogram over the sleep period was used to calculate SWA and a battery of cognitive assessments and behaviour questionnaires were conducted at both time points.

Results

There was no change in the average SWA between the baseline and follow-up and no differences between the groups. Cognitive and behavioural performance in the resolved group did not improve to control levels. However, decreased SWA at the beginning of the sleep period (β = −0.04, p = 0.002) and a decrease in obstructive apnoea–hypopnoea index (β = −2.2, p = 0.022) between the baseline and follow-up predicted improvements in measures of sustained attention. Increased SWA at the beginning of the sleep period between the baseline and follow-up predicted worsening of externalising behaviour (β = 0.02, p = 0.039).

Conclusions

This study suggests that resolution of SDB is not associated with changes in the dissipation of SWA. However, the association between decreases in SWA and improvements in cognitive and behavioural outcomes suggest that irrespective of disease, children whose quantitative sleepiness improves have improved attention and reduced externalising behaviours.

Introduction

Sleep-disordered breathing (SDB) in children describes a continuum of nocturnal respiratory disturbance. Severity of SDB ranges from primary snoring (PS), which is characterised by snoring without gas-exchange abnormalities or observed sleep disturbances, to obstructive sleep apnoea (OSA), characterised by apnoeas, intermittent hypoxia, hypercarbia and repeated arousals from sleep [1]. Several studies have highlighted that irrespective of the severity of the disease SDB is associated with cognitive [2], [3], [4], [5], [6], [7], [8] and behavioural [2], [3], [7], [8], [9], [10] deficits in children.

The prevailing mechanistic theory linking SDB to cognitive and behavioural dysfunction relates to hypoxic insult and repeated arousals from sleep [11]. However, children with PS do not experience the same level of hypoxia or sleep fragmentation as children with OSA, suggesting that there are still unknown mechanisms contributing to the neurocognitive and behavioural deficits associated with SDB [12]. An alternate explanation may be an interruption to slow-wave delta activity in the brain during non-rapid eye movement sleep (NREM), quantified as slow-wave activity (SWA) [13].

SWA is a physiological marker of the homeostatic regulation of sleep and is indicative of neuronal maturation and neuronal recovery [14], [15], [16], [17]. SWA is expressed as delta power (amplitude by frequency) and is greatest at the beginning of the sleep period, gradually dissipating over the sleep period. This profile represents a quantitative measure of the pressure to sleep [14] and is reflective of daytime sleepiness [18]. We have shown that children with SDB have altered SWA, presenting with significantly greater amounts of SWA at the beginning of the sleep period compared with healthy controls, together with reduced physiological decay of SWA over the course of the night [13]. This suggests that these children are sleepier than their non-snoring counterparts at the start of the night and the restorative function of sleep is not met. Considering the role of SWA in cortical maturation and the suggestion that children with SDB have greater physiological sleepiness, these impairments in the homeostatic function may provide an explanation for cognitive and behavioural deficits in children at all severities of SDB.

This study aimed to investigate whether resolution of SDB, either from spontaneous recovery or as a result of treatment, is associated with changes in SWA and whether these changes are reflected in neurocognitive or behavioural outcomes. We hypothesised that SWA would be no different from that of non-snoring children following a resolution of SDB and that any changes in SWA would be associated with concomitant improvements in cognition and behaviour.