Evaluation of Sleep Practices and Knowledge in Neonatal Healthcare

Background: Developmental care is designed to optimize early brain maturation by integrating procedures that support a healing environment. Protecting preterm sleep is important in developmental care. However, it is unclear to what extent healthcare professionals are aware of the importance of sleep and how sleep is currently implemented in the day-to-day care in the neonatal intensive care unit (NICU). Purpose: Identifying the current state of knowledge among healthcare professionals regarding neonatal sleep and how this is transferred to practice. Methods: A survey was distributed among Dutch healthcare professionals. Three categories of data were sought, including (1) demographics of respondents; (2) questions relating to sleep practices; and (3) objective knowledge questions relating to sleep physiology and importance of sleep. Data were analyzed using Spearman's rho test and Cramer's V test. Furthermore, frequency tables and qualitative analyses were employed. Results: The survey was completed by 427 participants from 34 hospitals in 25 Dutch cities. While healthcare professionals reported sleep to be especially important for neonates admitted in the NICU, low scores were achieved in the area of knowledge of sleep physiology. Most healthcare professionals (91.8%) adapted the timing of elective care procedures to sleep. However, sleep assessments were not based on scientific knowledge. Therefore, the difference between active sleep and wakefulness may often be wrongly assessed. Finally, sleep is rarely discussed between colleagues (27.4% regularly/always) and during rounds (7.5%-14.3% often/always). Implications: Knowledge about sleep physiology should be increased through education among neonatal healthcare professionals. Furthermore, sleep should be considered more often during rounds and handovers.

Despite growing awareness of the importance of early life sleep, recognizing the different sleep stages in infants may pose a challenge for healthcare professionals.Neonatal sleep consists of 2 main stages: active sleep and quiet sleep. 15,16Quiet sleep is easily detected as a sleep stage, since it is characterized by a still posture, closed eyes, and a regular heart and breathing rate. 17,18Active sleep, however, is characterized by frequent body and facial movements and twitches, rapid eye movements-sometimes with fluttering eyelids-and an irregular heart and breathing rate. 17,18Because of the appearance of this sleep stage, it can be difficult for the untrained eye to distinguish active sleep from wakefulness.
During active sleep-the neonatal equivalent of REM (rapid eye movement) sleep in older children and adults-endogenous generated brain activity is thought to be crucial for developing brain connectivity. 13,14In addition, quiet (non-REM) sleep is thought to be related to synaptic downscaling and pruning later in development. 19However, no human studies have been published on this topic.
The body of knowledge on the importance of sleep during early life and its relationship to brain development is growing. 11,12Protecting sleep in infants is considered to be an increasingly important factor in developmental care of (pre-)term infants.However, it is unclear to what extent sleep is currently considered in the dayto-day care at the neonatal ward.To our knowledge, no large-scale studies have been published on the subject of sleep education of neonatal healthcare professionals.Furthermore, since sleep is not a mandatory part of the Dutch healthcare education, the level of education and emphasis placed on sleep are unclear.Therefore, the purpose of the current research was to assess the level of knowledge about sleep among neonatal healthcare professionals.This may serve as a baseline for future intervention studies.The ultimate goal was to improve education about sleep among healthcare professionals.Improved education may lead to increased knowledge about sleep physiology and better sleep practices in the neonatal ward in accordance with the concepts of developmental care.
The aims of the current research were (1)  To investigate these aims, we conducted an e-survey among Dutch healthcare professionals working with neonates.The current research was designed to adhere to the SQUIRE-guidelines 20 (see Supplemental Digital Content Appendix A, available at: http:// links.lww.com/ANC/A222, for the checklist), as, in the future, we aim to use this work as a quality improvement initiative in neonatal care.

Participants and Data Acquisition
Between March 2021 and November 2021, a sleep practices and physiology survey was distributed electronically to Dutch healthcare professionals using our NICU nurses' and medical doctors' network via e-mail and via social media.Only healthcare professionals working in Dutch hospitals who are directly involved in neonatal care were invited to participate.Most participants were nurses, neonatologists, and members of the extended multidisciplinary team.Because of the nature of the study, approval by an institutional review board was not required.

The Survey
The survey used was derived from a study conducted by Hulst et al 21 investigating the level of knowledge and application of sleep health practices by healthcare professionals working in pediatric rehabilitation.This survey was adapted by experts in neonatal sleep (J.D., A.H.) to suit the population group of the current research.A pilot study (n = 60) was conducted in the Wilhelmina Children's Hospital, Utrecht, to assess feasibility among this specific group of healthcare professionals working with neonates.The survey was adapted afterward.The adapted survey was used for the current study and published as a Google Form.
The survey (see Supplemental Digital Content Appendix B, available at: http://links.lww.com/ANC/A223) consisted of both open and closed questions, with closed questions seeking answers from multiple-choice, yes/no, true/false, and Likert scale questions.The survey was divided into 3 distinct categories.These categories included (1) demographics; (2) practical questions; and (3) objective knowledge questions.

Data Analysis
Results of the adapted survey were analyzed using SPSS (released 2019; IBM SPSS Statistics for Windows, version 26.0.0.1;IBM Corp, Armonk, New York).

What This Study Adds
• Care is often adapted to perceived sleep stages.However, sleep assessments are not based on scientific knowledge.Therefore, the difference between active sleep and wakefulness is often wrongly assessed.
• Sleep is barely discussed during rounds and handovers.Tips are given to incorporate sleep in discussions during rounds and handovers.
• Education on sleep and access to automated sleep monitoring algorithms may improve the adaptation of elective care to sleep in the NICU.

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Evaluation of Sleep Practices and Knowledge in Neonatal Healthcare Frequency tables were used to explore demographic information, knowledge level, importance of sleep, and the extent to which sleep is considered in care.
Because of the nonparametric qualities of the data, Spearman's rho test was used to investigate (1)

Demographics
The survey was completed by 432 participants from 34 hospitals in 25 Dutch cities.Of the 34 hospitals, 8 were academic hospitals (level III; n = 114) and 27 were peripheral hospitals (level II; n = 317).Five respondents were eliminated from the study as they either had no experience in neonatal healthcare (n = 3) or did not work in a Dutch hospital (n = 2).Demographics are presented in Table 1.

Level of Knowledge
To test the knowledge that healthcare professionals have on sleep, multiple objective knowledge questions were asked (Table 2).For the most part, participants with a higher level of education, a higher number of working years, or older in age had higher scores on sleep knowledge.Nevertheless, lower age was related to a higher score on the true/false statement "Adults have relatively less deep sleep (nREM) compared to infants" (rho = −0.108,P = .025).Furthermore, less work experience with neonates was related to a higher score on the question, "When are you sure an infant is awake compared to active sleep?"(rho = −0.126,P = .009).Finally, physician assistants, resident physicians, and fellows could not distinguish sleep from wakefulness better than neonatologists, nurses, and pediatricians (Cramer's V = 0.128, P = .051).For a full overview of all associations between demographic characteristics and the objective knowledge questions, see Supplemental Digital Content Table 1 (available at: http://links.lww.com/ANC/A224).

Sleep in Healthcare Practice
To test the way sleep was considered in healthcare practices on the neonatal ward, several additional questions were asked.Most healthcare professionals indicate that they adapt elective care to sleep (eg, delay care when an infant is asleep) either always (13.1%) or as much as possible (78.7%).Hospital level was not associated with adapting sleep to care in practice (rho = 0.07, P = .16).However, most healthcare professionals indicate they always (0.5%), often (7.0%), or sometimes (58.8%) doubt whether an infant is awake or asleep.For a complete overview of all questions about sleep practices, see Figure 1.
Higher self-reported certainty of whether an infant is awake or asleep is associated with more frequent adaptation of elective care to sleep in accordance to developmental care principles (rho = 0.128, P = .008).However, both self-reported knowledge whether an infant is asleep (rho = −0.017,P = .734)and adapting elective care to sleep (rho = 0.025, P = .611)show no association with the knowledge question, "When are you sure an infant is awake compared to active sleep?"(Figure 2).Interestingly, healthcare professionals working at an academic (level III) hospital scored higher on the theoretical knowledge question about recognizing active sleep (rho = −0.11,P = 0.03).However, healthcare professionals working at a peripheral (level II) hospital reported more often that they were able to distinguish active sleep from wake (rho = 0.21, P < .000).

Origin of Knowledge
Regarding the origin of knowledge, 61.1% (n = 261) of participants indicated that knowledge about sleep was acquired from the workplace.In 5.4% (n = 23) of respondents, it was indicated that knowledge was acquired from education, while 30.2% (n = 129) indicated their knowledge was acquired from both workplace and education.Findings showed 63 respondents (15.0%) indicated they had acquired knowledge about sleep from other sources, mostly from personal experience as they had children of their own.A total of 22 respondents

General Remarks
The opportunity to give a general remark at the end of the survey was used by 39 of 428 respondents.After analysis of these remarks, it was clear that knowledge regarding neonatal sleep is considered very important and sharing this knowledgefor example, by education, scientific outreach-is key.For example, one respondent wrote: "Something to think about during rounds," and another respondent wrote, "Specific questions that make you think" (both quotes are translated from Dutch).

DISCUSSION
This  Results showed that, using self-assessment, onethird of healthcare professionals were always certain whether an infant was asleep or awake, while half of the respondents sometimes knew whether an infant was asleep or awake.However, less than 15% of all respondents gave a correct answer to the objective knowledge question assessing whether participants knew the difference between wake and active sleep.This corresponds with a similar small study, including only 30 nurses, finding that 20% of nurses were able to select the correct characteristics of active sleep. 22Findings indicate that self-reported knowledge may not always align with knowledge tested using science-based questions, with participants tending to "overclaim" their personal expertise favorably, in other words, "overprecision." 23In the context of neonatal sleep, it is difficult to correctly distinguish wake and sleep, since active sleep may resemble waking activity to inexperienced observers. 17,18igher self-reported knowledge was related to more frequent adaption of elective care to sleep.This might imply that healthcare professionals may adapt elective care to their own perception of sleep and wake.However, neither self-reported knowledge nor adaption of elective care was associated with giving the right or wrong answer to the objective knowledge question, "When are you sure an infant is awake compared to being in active sleep?"Therefore, the infant may still be unnecessarily disturbed and woken up for care procedures due to a lack of expertise and knowledge on the difference between being awake and being in active sleep.This specific phenomenon has, to our knowledge, not previously been studied in neonates.Previous work complements this finding, describing a decrease in the quality of sleep in hospital among children between 1 and 18 years old 24 and adults 25 is largely attributed to awakenings by staff for care procedures.
Participants reported to have acquired their sleep knowledge via multiple sources, with work experience and education being prefilled answers.From these two, work experience was most commonly reported to be the source of knowledge about sleep.The work/ education dichotomy, knowledge on neonatal sleep was mainly acquired via one's private life, for example, when raising children of their own.Interestingly, less work experience is associated with higher scores on objective knowledge questions.Besides, physician assistants, resident physicians, and fellows were better able to distinguish sleep from wake than neonatologists, nurses, and pediatricians.The former group consists of healthcare professionals who are at the start of their careers; thus, they might possess more knowledge from recent education.Given the increased interest in neonatal and preterm sleep, 11,12 recent education might include more information about this subject.Acquiring knowledge at the workplace poses risks including healthcare professionals acting on insufficient or outdated knowledge.Furthermore, this poses the need for education-both healthcare curricula and refresher training-to teach new scientific findings regarding sleep.
Nevertheless, knowledge acquisition in the workplace should not be discarded.Bedside teaching is shown to have several benefits, including increased

FIGURE 2
The association between objective knowledge, self-reported knowledge, and adapting elective care to sleep.de Groot et al active learning, motivation, patients' understandings, problem-solving, and decision-making skills. 26f healthcare professionals know more about sleep, they can teach parents how to support infant sleep both in the neonatal unit and at home.However, in the study of Hulst et al, 21 parents were found to have a similar level of knowledge about sleep compared with healthcare professionals, again stressing the need for educating healthcare professionals on sleep.
Sleep is infrequently discussed during rounds despite developmental care practices being common in Dutch healthcare settings.Infant-and familycentered developmental care is focused on supporting sleep by timing procedures around the sleep cycle, involving parents in settling the infant to sleep, creating a quiet, calm, and dark environment, and encouraging skin-to-skin care, which may improve sleep organization. 10To optimally apply these strategies, there is a need for greater discussion of sleep among the neonatal clinical team and parents.

Strengths and Limitations
A limitation is that the survey used was not entirely validated.To ensure the reliability and replicability, several actions were undertaken.The survey was first formulated on the basis of a survey developed by Hulst et al. 21After receiving feedback on this survey from our pilot study, changes were made accordingly.Furthermore, when analyzing the results, the team always worked in pairs of 2 or 3 during the qualitative analyses to avoid any bias.
To the best of our knowledge, this research stands out as the first nationwide study to evaluate sleep practices and knowledge among neonatal healthcare professionals.One of its key strengths lies in this aspect.The survey is filled in by a large number and a high variety of healthcare professionals throughout the country, including both academic and peripheral hospitals.Furthermore, the survey itself clearly contributed to the distribution of knowledge and served as a reminder to the importance of sleep.For example, one respondent wrote: "Something to think about during rounds," and another respondent wrote, "Specific questions that make you think" (both quotes are translated from Dutch).With this, the survey already contributed to our final goal of increasing awareness and knowledge about neonatal sleep in hospitals.

Future Research
Currently (pre-)term infant sleep-and therefore developmental care-may be disturbed because of lack of knowledge about sleep and sleep behavior in the neonatology ward.More knowledge about neonatal sleep may cause a plethora of positive changes.When healthcare professionals are knowledgeable on infant sleep physiology, they are more likely to educate parents in this area.This way, parent-based developmental care can continue beyond the hospital into the infant's home.Important sources of knowledge may be behavioral sleep scales 17,18 and the NIDCAP (Newborn Individualized Developmental Care and Assessment Program) or FINE (Family and Infant Neurodevelopment Education) manuals. 6,9,10Future research should focus on the best way for healthcare professionals and parents to acquire this knowledge.
A small step in this direction has already been made by our group.A Dutch e-Learning course about pediatric sleep is available and is promoted as refresher training for professionals and in general for nonprofessionals.This may be beneficial to all healthcare professionals, as it is shown that sleep knowledge can be successfully increased through provision of sleep education, both when delivered face-to-face and through online webinars. 27In addition, Toivonen et al 28 found that the quality of family-centered care was successfully improved in multiple hospitals by an educational intervention that utilizes a mentor system.Based on their findings, a one-on-one personal mentor program could further increase sleep-protective care.
Preterm infants have a higher rate of sleep difficulties than term born infants, as was extensively reviewed by Bennet et al. 29 However, to the best of our knowledge, no evidence-based guidelines have been published specifically for infants during the period after the hospital (NICU) stay.Even for healthy infants, currently little evidence exists regarding interventions to promote good sleep. 30,31Furthermore, most interventions developed to improve infant sleep in the first 6 months after birth seem to mainly target parent mood instead of infant sleep quality. 32Future research should aim to develop evidence-based practice guidelines for infant sleep and more specifically for infant sleep after NICU discharge.

Recommendations for Practice
Two areas for improvement were identified.First, knowledge on sleep physiology should be improved.Most healthcare professionals can accurately describe the importance of sleep and identify areas for which sleep may be important.However, to adapt elective care to sleep, healthcare professionals should also be able to assess sleep stages based on the current scientific consensus.
Recently, our research group published a review 18 and a behavioral scoring system 17 on sleep stages.It should be noted that the current consensus about the appearance of active sleep may resemble discomfort, according to frequently used comfort scales. 33However, discussions on our ward have shown that, with close examination, healthcare professionals are able to distinguish active sleep in infants who show signs of discomfort.In healthcare curricula, a module on sleep can be added.
Besides individual study of scientific sources on sleep, both formal education and refresher training Second, sleep is infrequently discussed during rounds and handovers.To increase discussions about sleep between colleagues, it is important to have insight into the sleep schedule of infants in the NICU.It is not possible to continuously manually assess sleep.Currently, several algorithms exist to assess preterm sleep stages. 34However, these still have to be validated on the bedside.
Nevertheless, sleep can still be discussed during handovers without continuous monitoring to increase awareness and understanding of sleep.If the ABCDE method (structured assessment of Airway, Breathing, Circulation, Disability, Exposure) is used, sleep can be discussed during Disability, when neurology is discussed, or during Exposure, when environment is discussed.It depends on the hospital and the practitioner when things such as pain and comfort are discussed.Of course, it is important to stay objective in your assessment.For example, we recommend to not say an infant was "sound asleep" but to describe which behavior you saw during checks (eg, lots of movements or not at all), how easily the infant woke up during care procedures, and/or whether the infant was groggy or alert.Finally, we recommend to discuss sleep at the end of the discussion, so all things that may have disturbed sleep (eg, medical procedures, bradycardias, or apneas) are known.

CONCLUSION
Healthcare professionals are highly motivated and willing to adapt elective care to optimize sleep in neonates admitted to the neonatology department.However, these current practices do not seem to be based on theoretical background.General scores on theoretical knowledge questions were low.Besides, healthcare professionals who scored high on theoretical knowledge questions were not more likely to adapt elective care to optimize sleep.Therefore, knowledge about neonatal sleep among healthcare professionals should be improved using education in curricula and refresher training.

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Evaluation of Sleep Practices and Knowledge in Neonatal Healthcare should include a module about sleep.This is currently been implemented in a refresher training for nurses in our hospital and yields very positive reactions and more awareness about sleep during care.The refresher training comprises a 1-hour lecture about the importance of sleep, the biological background of sleep, the development of sleep and sleep stages, and the appearance of sleep stages in preterm infants.

TABLE 2 .
Knowledge of Sleep

TABLE 3 .
Association Between Importance of Sleep and Discussing Sleep Sleep practices.de Groot et al

TABLE 4 .
The Importance of Sleep in Infant Health and Well-being a a All significant P values are indicated with an asterisk, with one asterisk (*) meaning P < .05 and 2 asterisks (**) meaning P < .01.