Regional Disruption of Slow-Wave Sleep Homeostasis in Children with Sleep-Disordered Breathing

Abstract

Importance Sleep-disordered breathing (SDB) is common in childhood and is associated with attentional and behavioral impairments despite largely preserved sleep macrostructure and minimal abnormalities in conventional electroencephalographic measures. This discrepancy has contributed to the perception that sleep is relatively preserved in pediatric SDB and has limited understanding of the physiological mechanisms underlying morbidity. Objective To determine whether pediatric SDB is associated with disruption of the regional organization and homeostatic dynamics of slow-wave activity (SWA), a key physiological marker of sleep-dependent neural recovery and development. Design, Setting, and Participants Cross-sectional study of 62 children aged 4 to 12 years who underwent overnight polysomnography with high-density electroencephalography in a laboratory setting. Participants were recruited from clinical referrals and the community, spanning the full spectrum of SDB severity. Exposures SDB severity indexed by hypopnea index (HI), apnea-hypopnea index (AHI), and obstructive apnea index (OAI). Main Outcomes and Measures Regional electroencephalogram-derived SWA (0.5 to 4 Hz) topography and exponential decay parameters derived from frontal and posterior cortical regions. The frontal-to-posterior decay-rate ratio was evaluated as a summary measure of regional sleep homeostasis. Results In children with lower hypopnea index, SWA demonstrated the expected developmental pattern, with posterior predominance in younger children and a progressive shift toward a more balanced anterior-posterior distribution with age. Increasing HI was associated with attenuation or reversal of this spatial organization. Global SWA showed no meaningful association with SDB severity. In contrast, regional frontal and posterior decay parameters were strongly associated with HI (adjusted R2 = 0.53; p < 1e-6) but not OAI (adjusted R2 = 0.05; p = .95). The frontal-to-posterior decay-rate ratio showed the strongest association with HI {beta} = 4.15; 95% CI, 3.17-5.13; p < 1e-10; adjusted R2 = 0.55. Conclusions and Relevance Pediatric SDB was associated with regional disruption of slow-wave sleep homeostasis rather than global loss of deep sleep. These alterations affected both the spatial organization and temporal dynamics of SWA during a period of active cortical maturation and were not captured by conventional sleep metrics. Regional SWA dynamics may provide a developmentally sensitive marker of physiological disease burden in children with SDB.