Elsevier

Early Human Development

Volume 113, October 2017, Pages 87-103
Early Human Development

Review of sleep-EEG in preterm and term neonates

https://doi.org/10.1016/j.earlhumdev.2017.07.003Get rights and content

Abstract

Neonatal sleep is a crucial state that involves endogenous driven brain activity, important for neuronal survival and guidance of brain networks. Sequential EEG-sleep analysis in preterm infants provides insights into functional brain integrity and can document deviations of the biologically pre-programmed process of sleep ontogenesis during the neonatal period.

Visual assessment of neonatal sleep-EEG, with integration of both cerebral and non-cerebral measures to better define neonatal state, is still considered the gold standard. Electrographic patterns evolve over time and are gradually time locked with behavioural characteristics which allow classification of quiet sleep and active sleep periods during the last 10 weeks of gestation. Near term age, the neonate expresses a short ultradian sleep cycle, with two distinct active and quiet sleep, as well as brief periods of transitional or indeterminate sleep. Qualitative assessment of neonatal sleep is however challenged by biological and environmental variables that influence the expression of EEG-sleep patterns and sleep organization. Developing normative EEG-sleep data with the aid of automated analytic methods, can further improve our understanding of extra-uterine brain development and state organization under stressful or pathological conditions. Based on those developmental biomarkers of normal and abnormal brain function, research can be conducted to support and optimise sleep in the NICU, with the ultimate goal to improve therapeutic interventions and neurodevelopmental outcome.

Introduction

Intensive monitoring of the vulnerable preterm and critically ill term neonate, has been increasingly complemented with bed-side neuromonitoring to achieve optimal insight into neurological well-being [1], [2], [3]. Serial electro-encephalography (EEG) monitoring over time can document actual normal or altered brain function and provides insight into the progress of brain maturation during this period of intensive neonatal care [1], [4], [5], with the ultimate goal to improve therapeutic interventions and long-term neurodevelopmental outcome.

Neonates spend most of their time resting in the sleeping state. Previous research has highlighted the important role of neonatal sleep as a state that involves endogenous driven brain activity, crucial for neuronal survival and guidance of brain networks [6], [7], [8], [9] and relate the impact of sleep on cognitive, psychomotor and behavioural development in both animal [10], [11] as well as human studies [12], [13], [14], [15], [16]. Moreover, sleep ontogenesis is a specific, pre-programmed process of the maturing brain that manifests itself within a certain time window that begins in utero with rapid and major changes during the neonatal periods and infancy, and more subtle changes throughout childhood [11], [17]. It's a complex and highly regulated neurologic function requiring the integration of different brain networks, influenced by the interplay between genetic endowment and environmental inputs, which allows for manifestations of neuroplasticity [6], [8].

Qualitative assessment of neonatal sleep is therefore an essential and valuable measure of functional brain integrity [11], [18], and recognition of sleep-wake states can be useful in the day-to-day monitoring, for assessing optimal periods for feeding and neonatal care, to support and optimise sleep in the NICU [19], as well as give insight in the sleep architecture of infants with sleep related problems (e.g. increased risk of sudden infant death syndrome, sleep apnoea).

This review discusses sleep in the preterm and term neonate and its relationship to brain development, measured with video-EEG polysomnography. We preface this with a short overview of monitoring tools and focus on the maturation of electrographic patterns. To summarize, we assess what is currently known regarding qualitative and quantitative sleep-EEG assessment in the neonatal period.

Section snippets

Monitoring techniques

Conventional video-EEG-polysomnography studies are using a combination of behavioural and EEG characteristics for visual sleep-wake scoring to differentiate recognizable sleep EEG patterns in the preterm and full-term neonate, since neither of these characteristics alone are considered as gold standard [17], [20], [21]. To yield high quality EEG-polysomnography recordings and document specific temporal and regional electrographic changes in brain activity, a reduced 10–20 position with 9

Sleep EEG patterns according to age (Figs. 1–8)

The development of different behavioural states in humans is species-specific and can be divided in quiet sleep (QS or non-REM sleep (NREM)), active sleep (AS or Rapid-Eye Movement (REM)), and wakefulness. These behavioural states are usually defined by a combination of behavioural, cardiorespiratory and EEG state specific criteria which emerge coherently over time, concurrent with the process of rapid brain maturation during foetal and early life [39].

Ultrasound observations have documented a

Sleep state and sleep wake cycling across early brain development

A rough, rudimentary sleep wake cycle, based on alternating periods with and without eye movements related to EEG discontinuity, have been described in preterm infants of 24–30 weeks of GA (Table 1) [40], [41]. In our own cohort with PMA between 27 and 31 weeks, we found a slightly shorter cycle duration between two successive QS periods based on quantitative analysis (for detailed description of this study group see [37]). This is comparable to results of visual EEG-assessment of Curzi

Automated sleep-EEG analysis

Automated detection of sleep periods and quantification of sleep may document alterations in cortical function during extra-uterine brain development and accelerate the more subjective visual assessment.

Detection of sleep is, however, challenging during this period of rapid brain maturation, because of the biological and technical variability in EEG background patterns. Moreover, multiple sleep-EEG studies indicate that newborn state recognition is more comprehensively assessed when integrating

Future directions

Studies of qualitative and quantitative assessment of preterm sleep have not been widely reported and improvements in neonatal medicine (Kangaroo Care, Newborn Individualized Developmental Care and Assessment Program (NIDCAP), non-invasive ventilation [86]) over the last decade have changed the sleeping conditions of those vulnerable preterm infants and ask for a more recent and updated assessment of preterm and neonatal sleep to complement those data. Further attempts to fully automate EEG

Conclusion

Sequential EEG-sleep analysis during the neonatal period provides crucial insights into functional brain integrity and documents deviations of the biologically pre-programmed process of sleep ontogenesis. Visual assessment of neonatal sleep-EEG, with integration of both cerebral and non-cerebral measures to better define neonatal state, is considered the gold standard, however future studies on inter-rater agreement are definitely needed to improve its validity.

Developing qualitative and

Conflict of interest

None

Funding

This research was funded by the Wellcome Trust Centre [grant number 098461/Z/12/Z] (Sleep, Circadian Rhythms & Neuroscience Institute), the RCUK Digital Economy Programme [grant number EP/G036861/1] (Oxford Centre for Doctoral Training in Healthcare Innovation), IWT [grant number TBM 110697-NeoGuard], Bijzonder Onderzoeksfonds KU Leuven (BOF): The effect of perinatal stress on the later outcome in preterm babies [grant number C24/15/036], iMinds Medical Information Technologies (SBO-2016),

Acknowledgments

The authors would like to thank the parents and infants involved in this study and the staff at the UZ Leuven NICU.

References (86)

  • M. Mirmiran

    The function of fetal/neonatal rapid eye movement sleep

    Behav. Brain Res.

    (1995)
  • A.A. Dos Santos et al.

    Behavior and EEG concordance of active and quiet sleep in preterm very low birth weight and full-term neonates at matched conceptional age

    Early Hum. Dev.

    (2014)
  • S. Granot et al.

    Influence of respiratory acidosis and blood glucose on cerebral activity of premature infants

    Pediatr. Neurol.

    (2012)
  • M.S. Scher et al.

    Maturational trends of EEG-sleep measures in the healthy preterm neonate

    Pediatr. Neurol.

    (1995)
  • J. Werth et al.

    Unobtrusive sleep state measurements in preterm infants - a review

    Sleep Med. Rev.

    (2017)
  • M. Andre et al.

    Electroencephalography in premature and full-term infants. Developmental features and glossary

    Neurophysiol. Clin.

    (2010)
  • M.L. Nunes et al.

    Maturational changes of neonatal electroencephalogram: a comparison between intra uterine and extra uterine development

    Clin. Neurophysiol.

    (2014)
  • J.G. Nijhuis et al.

    Are there behavioural states in the human fetus?

    Early Hum. Dev.

    (1982)
  • M.F. Vecchierini et al.

    EEG patterns in 10 extreme premature neonates with normal neurological outcome: qualitative and quantitative data

    Brain Dev.

    (2003)
  • I. Kostovic et al.

    The development of cerebral connections during the first 20–45 weeks' gestation

    Semin. Fetal Neonatal Med.

    (2006)
  • M.D. Lamblin et al.

    Electroencephalography of the premature and term newborn. Maturational aspects and glossary

    Neurophysiol. Clin.

    (1999)
  • S. Vanhatalo et al.

    Development of neonatal EEG activity: from phenomenology to physiology

    Semin. Fetal Neonatal Med.

    (2006)
  • K. Palmu et al.

    Sleep wake cycling in early preterm infants: comparison of polysomnographic recordings with a novel EEG-based index

    Clin. Neurophysiol.

    (2013)
  • M. Mirmiran et al.

    Circadian rhythm generation in the cultured suprachiasmatic nucleus

    Brain Res. Bull.

    (1995)
  • E.J. Mulder et al.

    Emergence of behavioural states in fetuses of type-1-diabetic women

    Early Hum. Dev.

    (1987)
  • K. Watanabe

    Neurophysiological aspects of neonatal seizures

    Brain Dev.

    (2014)
  • E. Shany et al.

    In and ex utero maturation of premature infants electroencephalographic indices

    Clin. Neurophysiol.

    (2014)
  • C. Guyer et al.

    Very preterm infants show earlier emergence of 24-hour sleep-wake rhythms compared to term infants

    Early Hum. Dev.

    (2015)
  • M.S. Scher et al.

    Functional brain maturation in neonates as measured by EEG-sleep analyses

    Clin. Neurophysiol.

    (2003)
  • E. Biagioni et al.

    Distribution of sleep and wakefulness EEG patterns in 24-h recordings of preterm and full-term newborns

    Early Hum. Dev.

    (2005)
  • M.S. Scher et al.

    Neurophysiologic assessment of brain maturation after an 8-week trial of skin-to-skin contact on preterm infants

    Clin. Neurophysiol.

    (2009)
  • M.G. Welch et al.

    Electroencephalographic activity of preterm infants is increased by family nurture intervention: a randomized controlled trial in the NICU

    Clin. Neurophysiol.

    (2014)
  • R. Feldman et al.

    Maternal-preterm skin-to-skin contact enhances child physiologic organization and cognitive control across the first 10 years of life

    Biol. Psychiatry

    (2014)
  • A. Piryatinska et al.

    Automated detection of neonate EEG sleep stages

    Comput. Methods Prog. Biomed.

    (2009)
  • M. Tolonen et al.

    Development of the spontaneous activity transients and ongoing cortical activity in human preterm babies

    Neuroscience

    (2007)
  • N. Koolen et al.

    Line length as a robust method to detect high-activity events: automated burst detection in premature EEG recordings

    Clin. Neurophysiol.

    (2014)
  • H.J. Niemarkt et al.

    Quantitative analysis of maturational changes in EEG background activity in very preterm infants with a normal neurodevelopment at 1 year of age

    Early Hum. Dev.

    (2010)
  • N. Koolen et al.

    Automated classification of neonatal sleep states using EEG

    Clin. Neurophysiol.

    (2017)
  • C.L. Collins et al.

    Randomized controlled trial to compare sleep and wake in preterm infants < 32 weeks of gestation receiving two different modes of non-invasive respiratory support

    Early Hum. Dev.

    (2015)
  • K.K. Iyer et al.

    Cortical burst dynamics predict clinical outcome early in extremely preterm infants

    Brain

    (2015)
  • M.J. Benders et al.

    Early brain activity relates to subsequent brain growth in premature infants

    Cereb. Cortex

    (2015)
  • H.P. Roffwarg et al.

    Ontogenetic development of the human sleep-dream cycle

    Science

    (1966)
  • M. Mirmiran et al.

    Role of REM sleep in brain development and plasticity

  • Cited by (0)

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