From womb to crib: How fetal activity patterns in utero reveal postnatal sleep behavior

Abstract

ImportanceThe human circadian system, a critical biological mechanism governing the sleep-wake cycle, begins to oscillate before birth. Distinct fetal behavioral states have been described using short-duration ultrasound recordings, but the alignment of fetal activity with day and night cycles (i.e., diurnal rhythms) remains poorly understood due to the lack of long-term monitoring. Accordingly, a substantial knowledge gap exists concerning the evolution of fetal diurnal rhythms into infant sleep-wake cycles. ObjectiveTo investigate the development of fetal diurnal rhythms and their evolution into postnatal infant sleep, as well as the role of maternal factors and melatonin in shaping early circadian entrainment. MethodsIn this cohort study, conducted in 2022 and 2023, we collected over 20 000 hours of wearable acceleration and temperature data from 32 fetuses and their mothers during continuous 5-day monitoring in the third trimester of pregnancy. The cohort was subsequently followed longitudinally from the prenatal period through 6 months postpartum, with infant sleep outcomes assessed at three key time points (first postnatal weeks, 3 months, and 6 months) using sleep diaries and questionnaires. The first postnatal assessment additionally included breast milk and infant stool sample collection. ResultsMulti-level modelling revealed early diurnal rhythms in fetuses that align with maternal activity and circadian rhythms. Random Forest analyses identified fetal day/night sleep duration ratio - a simplified proxy for fetal circadian entrainment - as the strongest predictor of postnatal infant sleep, with fetuses preferring nighttime sleep maintaining this preference postnatally. Maternal sleep regularity (i.e., consistent sleep patterns characterized by low day-to-day variability in sleep timing) during pregnancy also predicted infant sleep, associating with a stronger preference for nighttime sleep in infants. Conclusions and relevanceThese findings highlight the potential influence of intrauterine and maternal factors on the evolution of circadian entrainment. Our study contributes to a broader understanding of the earliest emergence of circadian rhythms, supporting future research on their long-term health impacts. Maternal sleep regularity stands out as the earliest modifiable target for interventions, offering an actionable pathway to promote infant circadian entrainment, with potential long-term benefits for family dynamics and well-being.