Introduction

In Portugal, newborns (NB) with less than 37 weeks of gestational age (GA), that is, preterm babies, make up around 10% of all NBs. Around 1% of these newborns are born with less than 32 weeks and/or less than 1500 g of birth weight or very low birth weight (VLBW), with around a thousand VLBW newborns being born in Portugal annually (^{Peixoto, Guimarães, Machado, et al., 2002}). The growth of these VLBW infants occurs mainly outside the mother's womb, in neonatal intensive care units (NICU), with a high risk of sequelae from both a nutritional point of view (^{Moreira, Matos, Rebelo Pacheco, Cunha, 2020}) and neurodevelopment (^{Matos, Costa, Rebelo Pacheco, Moreira, Cunha, Barroso, 2019}). This is a critical period of growth and differentiation of the central nervous system (CNS). Neuronal migration and synaptogenesis begin, and the process of apoptosis occurs, all contributing to an enormous brain plasticity during this period. Innate fetal activity results from central pattern generators that are organized into sets of neurons with increasingly numerous connections between them called networks (^{Hadders-Algra, 2000}a; ^{Hadders-Algra 2000b}; ^{Johnston, 2009}). Whether or not certain neuronal circuits are strengthened also depends on afferent information, which the environment plays a huge role in acquiring. Therefore, it is very important to maintain the NICU environment as close as possible to the in-utero environment (^{Newville, Ortega, & Maxwell, 2018}).

The fetal biological rhythm appears to be sensitive to day-night cycles through the secretion of maternal hormones and maternal physiological parameters. Fetal innate activity highlights a pattern of sleep organization that can be detected from 25 weeks of GA through heart rate (HR), respiratory rate, and sleep/wake periods (^{Bertelle, Sevestrem, Laou-Hap, Nagahapitiye & Sizun, 2007}). This can be assessed by active movements and HR and is classified into four stages from around 32 weeks: 1F: Quiet sleep - slow and regular HR, rare body movements, in a saccade, without eye movements; 2F: active sleep - regular HR, eye movements, large body movements mainly extension; 3F: waking up calmly - fast and regular HR, eye movements, no body movements; 4F: active awakening - rapid and irregular HR with prolonged periods of tachycardia, eye movements and continuous body movements (^{Bennet, Walker, Horne, 2018}). The distribution of waking and sleeping time varies with post-menstrual age.

Newborns, especially premature ones, do not yet have the ability to stay awake nor to demand food, and thus spend most of their time sleeping (^{Georgoulas, Jones, Laudiano-Dray, Meek, Fabrizi, and Whitehead. 2021}; ^{Cailleau, Weber, Cabon, Flamant, Roué, Favrais, et al., 2020}). In newborns, sleep distribution can be assessed by direct observation (^{Allen, 2012}; ^{Altimier & Philips, 2013}) and, in a more systematic way, by continuous video-EEG recording (^{Ryan, Mathieson, Livingstone, O'Sullivan, Dempsey, Boylan, 2023}). This last technique requires specific training, experience, and a lot of monitoring time and is not easily applicable in clinical practice (^{Ryan et al., 2023}).

Although premature babies' sleep varies with maturation, sleep after birth can be classified as quiet sleep (equivalent to REM sleep), active sleep (equivalent to NREM sleep), and indeterminate sleep, a state in which the characteristics of active sleep or quiet sleep are not present. The predominant sleep state in premature infants is approximately 80% active sleep, approximately 20% quiet sleep, 10% undifferentiated or transitional sleep, and only 10% awake. This variation changes, reducing active sleep to around 70%, quiet sleep to around 20%, and 20% of the time being awake, a pattern already very close to full-term newborns (^{Georgoulas, Jones, Laudiano-Dray, Meek, Fabrizi, and Whitehead. 2021}; ^{Cailleau, Weber, Cabon, Flamant, Roué, Favrais, et al., 2020}).

The importance of sleep manifests itself in the maturation of the CNS in the formation of synapses and, through neuronal plasticity, in their strengthening or weakening, leading to their elimination (apoptosis). Synaptic homeostasis depends on sleep-wake regulation; that is, the hyperstimulation of certain synapses that occurs during wakefulness is reduced during sleep, improving the ability to store new information and contributing to neuronal plasticity (^{Sun, Zhou, Cichon, Yang, 2020}; K^{uhn, Wolf, Maier, et al. 2016}).

Restful sleep, integrated with developmental care, contributes to better weight gain and reduces hospital stay. For this reason, care strategies that facilitate the NB’s peaceful sleep must be established as soon as possible and included in the neuroprotective measures that best suit each case (^{Altimier & Philips, 2013}; ^{Coughlin, 2017}). In this article, we seek to analyze the implementation of these measures and the impact they had on the length of stay in our Neonatal Special Care Unit (NSCU).

1. Methods

2. Results

The number of NB admitted to the NSCU below 37 weeks was 79 NBs in 2020, 80 NBs in 2021, and 104 NBs in 2022. The average GA was 33.1 weeks, 33.3 weeks GA and 33.2 weeks GA, respectively, with other characteristics mentioned in Table 1.

In the analyzed timeframe, hospitalized patients had similar characteristics in relation to maternal age, distribution by GA, birth weight, and sex. With the application of strategies to improve care, including sleep quality, the average length of stay was slightly longer in 2020, but when compared to the years 2021 and 2022, this difference was not statistically significant (Table 1).

In 2020, 24 training sessions were held for professionals and groups of parents between January and October. In 2021, only individual training was carried out for parents due to the restrictions imposed by the pandemic, and in 2022, group training for parents was resumed from March onwards, with a total of 14 training sessions being carried out. In the informal analysis of the implementation of measures aimed at promoting healthy sleep at NSCU and the sessions held with families, they showed greater satisfaction and greater ease in caring for newborns

3. Discussion

The principles of promoting healthy sleep applied at NSCU are governed by the recommendations of the European Foundation for the Care of Newborn Infants (EFCNI) and the Newborn Individualized Developmental Care and Assessment Program (NIDCAP). The EFCNI has established European healthcare standards for NB. Care focused on the child's development in the family is an integral part of these standards. This care includes regulating exposure to light and noise, temperature control, touch (positioning and manipulation), nutrition, and peaceful and protected sleep (EFCNI 2019; ^{Altimier & Philips, 2013}). The application of these measures may contribute to a reduction in the length of stay (Altimier & Philips, 2013), although this was not verified in our sample.

NIDCAP, which is based on the assessment of the NB’s response and adaptation of care to it, also seeks to understand the NB’s needs through observation of their behavior at each moment of their evolution (^{Als & McAnulty 2011}). It is currently fully applied in some neonatal units in Portugal. In other units like ours, some of the measures recommended by NIDCAP are applied, but not the program as a whole. To apply these assumptions, professionals must have knowledge of innate fetal activity, which is similar in premature newborns (^{Allen 2012}).

It is also necessary to know the different stages of the NB’s behavior, as well as the language of the NB’s response to different interventions through the different systems: autonomic, motor, state, and self-regulation (^{Als & McAnulty 2011}).

Knowledge of this standard and teaching parents are essential as facilitators of the transition process in the provision of care from the health professional to the family (^{Barlow, Herath, Bartram-Torrance, Bennett, Wei, 2018}).

However, sleep states after birth may change from the first hours of life in the NICU. The constant need to carry out treatments, some of which are painful, intense light, loud noises, and the need for ventilation, whether invasive or non-invasive, influence the state of sleep (^{Ryan et al., 2023}). With certain pathologies, the change is even more pronounced, such as hypoxic-ischemic encephalopathy, intrauterine growth restriction (IUGR), loss of placental circulation (corticosteroids and progesterone), postnatal hypoxia and hemodynamic instability and inflammation (^{Allen 2012} ; ^{Bennet, 2018}). Based on this knowledge, the measures adopted at NSCU to allow a peaceful sleep are the optimization of the environment, management of rest, monitoring NB activity, comforting the NB, taking measures to initiate the child's sleep, positioning the NB, and monitoring the NB’s sleep.

During hospitalization, the transition to lying supine should be gradual after the postmenstrual age of 32 weeks, as it may affect sleep quality (^{Altimier & Philips, 2013}). The situations that may raise more doubts are bronchopulmonary dysplasia, respiratory malformations such as Pierre Robin Syndrome, prematurity apneas, gastroesophageal reflux (GER), hyperbilirubinemia and withdrawal syndrome (^{Goodstein, Stewart, Keels, Moon, 2021}).

In bronchopulmonary dysplasia, there may be an indication for a more gradual transition to the supine position. This transition is also necessary to define oxygen needs in babies who maintain this need at home (^{Goodstein, 2021}). Teaching parents about sleep and sleeping position after discharge, applied at NSCU, are in accordance with the recommendations of the American Academy of Paediatrics (AAP), which state that the sleeping position of premature babies should be the supine position (Goodstein et al. al., 2021).

The main limitation of the study is that we did not apply to the families of patients admitted to the NSCU, a measurable form of satisfaction results from the application of the strategies used, but, as we mentioned, the informal evaluation showed an increase in the satisfaction of these families. On the other hand, due to the pandemic, the restrictions imposed made it difficult to apply the strategies, and training for parents was also more limited (^{DGS, 2021}; ^{Jonet et al., 2021}).

We also consider it a limitation that the assessment of sleep quality and its staging were not carried out systematically. Perhaps the ideal way to obtain this data is continuous monitoring using video-EEG. However, this process is complex and laborious and requires experience (^{Ryan et al., 2023}), which was not the objective of our study.

The effectiveness of developmental care is more evident when it is applied as an integrated bundle (^{Altimier & Philips, 2013}). Therefore, the evaluation of the influence of these strategies on neurodevelopment, in the short and long term, should be part of future studies.

Conclusion

Premature birth occurs at a critical period of CNS growth and differentiation, with enormous neuronal plasticity. The environment, through afferent information, contributes to the strengthening, or not, of certain neuronal circuits.

Synaptic homeostasis occurs during sleep. That is, the hyperstimulation of certain synapses that occurs during wakefulness is reduced during sleep, contributing to neuronal plasticity.

Child-family-centered developmental care recommends evaluating the different stages of the NB’s activity with respect to sleep periods.

This care must involve the entire team and teaching the family, including preparation for discharge. In future studies, more objective forms of measuring these results should be used.

Authors' contribution

Conceptualization, M.C., D.T. and A.R.C.; data curation, M.C.; formal analysis, M.C., D.T. and A.R.C.; investigation, M.C., D.T. and A.R.C.; methodology, M.C., D.T. and A.R.C.; project administration, M.C., D.T. and A.R.C.; software, M.C.; supervision, M.C., D.T. and A.R.C.; validation, M.C., D.T. and A.R.C.; visualization, M.C., D.T. and A.R.C.; writing-original draft, M.C., D.T. and A.R.C.; writing-review and editing, M.C., D.T. and A.R.C.;

Conflict of interest

The authors declare no conflicts of interest.