Defining and Promoting Pediatric Pulmonary Health: Understanding Sleep and Ventilatory Health

Abstract

Healthy sleep and optimal ventilatory control begin in early development and are crucial for positive child outcomes. This paper summarizes information presented at the Sleep and Ventilatory Control sessions of the National Heart, Lung, and Blood-sponsored 2021 Defining and Promoting Pediatric Pulmonary Health workshop. These sessions focused on pediatric sleep health, screening for sleep health and sleep disorders in primary care using the electronic health record, infant sleep and ventilatory control, and home sleep testing. Throughout this summary, we discuss key gaps in and barriers to promoting sleep and ventilatory health that were identified during the workshop sessions. We conclude with strategies to address these gaps and barriers and directions for future multidisciplinary research, patient care, and training.

Understanding Sleep and Ventilatory Health

Healthy sleep and optimal ventilatory control are crucial for positive child development, from birth through emerging adulthood. Pediatric sleep disorders (eg, obstructive sleep apnea syndrome [OSAS], insomnia) and poor sleep health (eg, short sleep duration) are prevalent across development^1–3 and associated with impairments in child physical health,^4,5 neurocognitive, and social-emotional functioning.^6,7 Poor ventilatory control (ie, inability to maintain adequate gas exchange in the presence of insults, such as upper or lower airway obstruction, neuromuscular weakness, and drugs) and related respiratory diseases (eg, acute respiratory infections, asthma) pose significant risks to child health and well-being and contribute to global pediatric morbidity and mortality.⁸

Promoting healthy sleep and ventilatory control is especially important given well-documented racial, ethnic, and socioeconomic sleep and respiratory health disparities.^9–12 Black or African American and/or Hispanic or Latinx children are more likely than their non-Hispanic or Latinx white peers to experience short and irregular sleep duration,^10,13 sleep disordered breathing (SDB) across its continuum of severity (ie, from mild snoring to severe OSAS),⁹ and asthma.¹⁴ After covarying for race and ethnicity, children living in lower-socioeconomic status homes and neighborhoods experience increased likelihood of short sleep duration,^15,16 SDB,^17,18 asthma,¹⁴ and other respiratory illnesses¹⁹ compared with those in higher- socioeconomic status contexts. These health disparities are not a result of biological or genetic differences.²⁰ Rather, inequitable exposures to adverse social and environmental factors, particularly racism and discrimination at multiple levels (ie, internalized, personally mediated, and systemic or structural),^21,22 directly contribute to observed disparities in the prevalence, diagnosis, and treatment of sleep and respiratory problems.^23,24 For example, despite having a greater likelihood of SDB compared with white children, Black children are less likely to receive timely evaluation and treatment (eg, via adenotonsillectomy) than white children.^25,26 Children with Medicaid insurance, often used as a proxy for family income, are less likely than those with private or commercial insurance to receive SDB care.²⁶

Comprehensive, effective, and equitable promotion of pediatric sleep and ventilatory health and treatment of sleep and respiratory disorders requires collaboration among primary care pediatricians, pulmonary and sleep specialists, and children and their families. Pediatric primary care is an ideal point of screening and identification for sleep²⁷ and respiratory health, as children typically see their pediatrician at least once per year, and families report high trust in their child’s pediatrician when making healthcare decisions.²⁸ However, many families face barriers in accessing pediatric specialty care, which can exacerbate existing health disparities.^29,30 Enhancing collaborative, multidisciplinary care among general pediatricians and pulmonary and sleep specialists could help ensure pediatric patients and their families receive the necessary specialty diagnosis and treatment of sleep disorders and respiratory diseases. Primary and specialty care providers must collaborate and coordinate with families to optimize care, enhance treatment engagement, promote health equity, and identify priorities for patient and family-centered research.^31,32 Patient or family and medical care team collaboration is critical given research showing that clinician implicit racial bias influences communication with families, treatment planning, and health outcomes.^33–35 Clinician racial bias is associated with poorer patient-rated visit communication and overall care.³⁶ Engaging in meaningful research partnerships with patients and families could help clinicians better understand families’ care perspectives and priorities for research that addresses bias and inequities families may face in healthcare. Because of racism and historical abuse in medicine and medical research, minoritized populations may also experience medical mistrust.^33,37 Partnerships among families, pediatricians, specialty care providers, and community organizations could help enhance family trust and engagement in healthcare.³⁸

This paper summarizes the Sleep and Ventilatory Control sessions of the National Heart, Lung, and Blood-sponsored 2021 Defining and Promoting Pediatric Pulmonary Health (DAP₃H 2021) workshop. This summary includes key gaps and related barriers in promoting sleep and ventilatory health identified during the workshop. We conclude by discussing strategies to address these gaps and barriers, including future directions for multidisciplinary research, patient care, and training.

Summary of Meeting

Pediatric Sleep Health

Pediatric sleep health is a multidimensional construct that conceptualizes sleep as a positive attribute, rather than a problem or disorder.^39,40 This approach allows sleep to be a target for health promotion and prevention at the individual, community, and population levels. Sleep health can be measured on a continuum, both objectively and subjectively, recognizing that sleep health will differ across individuals and situations.⁴⁰ It is important to conceptualize pediatric sleep health within a socio-ecological framework,⁴¹ as children are part of a complex and dynamic system. Each level of the system, including individual child factors, family and school factors, and neighborhood or community and broader socio-cultural factors, can directly and interactively promote or inhibit sleep (Fig 1). Healthy sleep is critical for every aspect of child health and well-being,^4,7 and focusing on sleep health is necessary for achieving health equity.²⁴

FIGURE 1.

Socio-ecological framework for pediatric sleep and ventilatory control and strategies to advance research and practice.

Peds B-SATED is a conceptual model defining multiple dimensions of pediatric sleep (Behaviors, Satisfaction with sleep, Alertness or sleepiness, sleep Timing, sleep Efficiency, sleep Duration).⁴⁰ This model extends Buysse’s well-established adult sleep health framework (SATED)³⁹ to pediatrics by integrating key developmental considerations (see Meltzer et al).⁴⁰ Sleep-related behaviors promote sleep include a consistent sleep-wake schedule and nightly bedtime routine, whereas caffeine, electronics, and the need for caregiver presence at sleep onset can interfere with sleep.⁴² Satisfaction with sleep or sleep quality is the subjective assessment of “good” versus “poor” sleep. This is the most difficult of the dimensions to quantify as it is a subjective and individual experience. One consideration for pediatrics is the reliance on caregiver report for younger children, which is likely influenced by caregivers’ own sleep quality. Alertness or sleepiness is the ability to maintain wakefulness during the day. In pediatrics, developmental stage needs to be considered as homeostatic drive (ie, the need or pressure to sleep) changes with development, making naps age appropriate in younger children.⁴³ Symptoms of sleepiness may differ in children compared with adults, including increased energy and difficulty with emotion regulation, concentration, and academics.

Sleep timing is the placement of sleep across a 24-hour day, including bedtimes, wake times, and naps. The timing of sleep is known to impact health outcomes⁴⁴ but can be influenced by many factors, including family work schedules, the child’s activities, homework, employment, and school start times.⁴⁰ Sleep efficiency captures the ease of falling asleep or returning to sleep. In many situations, sleep efficiency is captured by subjective caregiver report. As caregivers often become less involved with sleep as children get older, they may not be aware of how long a child or adolescent takes to fall asleep or return to sleep, unless the child complains of this at bedtime or wakes a caregiver during the night. Thus, it is important to ask children ages 8 years and older directly about sleep.^45,46 Finally, sleep duration is the total sleep obtained in a 24-hour period. Optimal sleep duration is associated with a range of health outcomes.⁷ Of note, there is not a single recommended sleep duration in pediatrics, but rather ranges of sleep duration that change at each developmental stage.⁴⁷ As the current recommendations are most commonly based on actual or obtained sleep, rather than sleep need, more research is needed to assess the biological sleep needs of prepubertal children.

The Peds B-SATED framework points to several areas of research opportunity. For instance, research shows that family and cultural beliefs may influence sleep-related behaviors,⁴⁸ but more information within and across cultural groups is necessary. The field also needs to move beyond association studies of sleep and electronics and screen time to identify the causal impact of electronic usage on sleep.⁴⁰ Future studies should identify a consistent definition or measure of subjective sleep satisfaction (quality). Defining optimal sleep duration and understanding the impacts of too much sleep is another challenge for future research given emerging evidence showing that both insufficient sleep and prolonged sleep duration are linked to poor health.^49,50 Regarding alertness, a small number of studies have found racial and ethnic differences in naps for children,⁴³ however more research identifying contributors to these differences is needed. Peds-B-SATED can guide the assessment and evaluation of these child sleep health domains in relation to broad child functional outcomes.⁴⁰

In addition to previously described research gaps, there are also barriers to sleep health promotion in clinical care. Notably, most health care providers receive, on average, 4 hours of education on sleep throughout training, with almost no training in pediatric sleep or sleep health.^51,52 This limits the ability of primary care clinicians to include sleep health as a vital sign that is assessed as a health indicator, or at least include sleep health screening on par with diet and exercise.⁵³ There is a very limited number of specialized pediatric sleep providers,⁵⁴ thus sleep health gaps must be closed with ongoing education for primary care providers as well as support from sleep specialists. Peds-B-SATED could inform both the development of screening tools to assess multiple sleep health dimensions and the educational domains necessary to address during clinical training. Finally, there is a significant need for publicly available, evidence-based, and free sleep health education resources for children and their families.⁵⁵

Screening for Sleep Health and SDB Using the Electronic Health Record (EHR)

A number of studies have shown that using patient and family-facing surveys integrated with the electronic health record (EHR) can facilitate efficient and comprehensive well visit screening for common health concerns.⁵⁶ This approach can also enhance alignment with the American Academy of Pediatrics well visit screening guidelines (eg, adolescent depression)⁵⁷ and the uptake of evidence-based care. For example, in a cluster-randomized trial, implementing EHR-based clinical decision support (CDS) for asthma care increased primary care clinician adherence to evidence-based care guidelines.⁵⁸

However, only a handful of studies have examined EHR-based methods to screen for pediatric sleep health and sleep disorders in primary care, where sleep concerns tend to be under-identified and under-treated.²⁷ For example, using a developmentally tailored instrument to screen for multiple domains of sleep (bedtime problems, excessive daytime sleepiness, night awakenings, regularity and duration of sleep, and snoring) in primary care increased sleep documentation and the likelihood of clinicians identifying child sleep problems.⁵⁹ A small pilot study found that brief sleep screening accompanied by intervention for poor sleep health and behavioral sleep problems was feasible to implement and acceptable to primary care clinicians, although outcomes of sleep treatment were not assessed.⁶⁰ Another study found EHR-based screening and CDS for snoring and other SDB symptoms in primary care improved adherence to American Academy of Pediatrics guidelines¹ for SDB screening and management overall.⁶¹ However, there was significant variation in clinician adherence, with 20% of children with SDB symptoms not receiving any clinical guidance or referrals.⁶¹

There are several barriers to efficiently and comprehensively screening sleep health and SDB in primary care. Primarily, there is a paucity of large-scale research evaluating the implementation, acceptability, and utility of available sleep and SDB screening tools. In conducting this research, it will be important to address related implementation barriers, such as the challenge of effectively integrating screeners into different clinical workflows and EHR systems across providers and primary care settings. Additional barriers include limited clinician sleep training and education⁵¹ and the potential to overburden clinicians with EHR screeners and alerts, which could contribute to limited screener uptake and utility in clinical practice. The lack of caregiver and family knowledge about child sleep health and sleep disorder symptoms⁶² and few well-developed, free and easily accessible sleep health resources²⁷ also likely contribute to the under-identification and under-treatment of sleep problems in primary care. Finally, additional research that involves partnerships among primary care clinicians, sleep specialists, and patients and families is needed to achieve 2 goals: (1) develop educational resources for primary care clinicians and families and (2) evaluate on a large-scale, primary care-based screening tools and CDS for sleep health and SDB, which may help integrate families, primary care teams, and specialists.

Sleep in Infancy and Ventilatory Control

Maturation of ventilatory control evolves from the intrauterine period to weeks and months postnatally when it reaches adult levels.⁶³ During this critical window, intrauterine and postnatal environmental factors may delay and/or hinder the normal developmental trajectory of the neural components that govern ventilatory control. Intrauterine exposure to drugs, toxins, infections, multiple genetic conditions, and, in some cases, structural damage to brain centers that govern respiratory rhythmicity and chemosensitivity may contribute to long-term ventilatory instability. Prematurity is one condition that combines multiple factors that may have short and long-term sequelae on ventilatory control manifesting as SDB. Such that, a long period of ventilatory control maturation takes place postnatally during which infants are exposed to hypoxia or hyperoxia, sepsis, intracranial hemorrhage, and mechanical ventilation. There is limited knowledge on how disruptions of mechanisms of ventilatory control during this vulnerable period of development tracks into childhood and adulthood.

Like many chronic health conditions, primary and specialty care providers may respond to the acute manifestations of SDB until the tip of the iceberg is no longer appreciated. Therefore, potential persistent ventilatory instability that progresses into subclinical and chronic stages may be discounted. It may not be recognized until further acute manifestations of SDB become apparent that aberrant ventilatory control is considered. This episodic management of a potentially chronic condition could underlie long-term morbidities manifesting in late childhood or adulthood. However, evidence in support of this hypothesis is yet to be confirmed.

Aberrant ventilatory control and SDB may vary by age of onset and resolution and by its chronicity. Limited knowledge is available about the different phenotypes of SDB that begin from infancy or are of late onset. Although the early origin of some pulmonary and cardiovascular diseases has been studied, the early origin of adult SDB is yet to be determined. Likewise, the clinical significance of long term, undiagnosed SDB on mental, neurocognitive, metabolic, and cardiovascular health needs to be fully investigated. Particularly, simple and reliable tools that assist in determining duration of exposure starting from infancy to older age are needed.

Although traditionally, many of these epidemiologic questions have been addressed by establishing cohorts that are followed for decades, the recent effective digital connectivity of health care systems creates the unique opportunity to conduct real-world research. Integrating general pediatricians with specialty providers may be one way of filling the gaps in care for children who demonstrate chronic SDB. Essential elements to overcome gaps in care include brief tools to administer in the pediatrician’s visit and an infrastructure for data sharing and cross talk between providers. An infrastructure, such as the Pediatric Learning Health System (Pedsnet),⁶⁴ that tracks clinical course as well as patients’ and medical providers’ reported outcomes could bridge clinicians and researchers to improve clinical care and answer seminal research questions.

Home Sleep Testing

In-laboratory polysomnography (PSG) is the gold standard for diagnosing OSAS in children.¹ However, in-laboratory PSG presents challenges for families and clinicians. First, there are only a small number of dedicated pediatric sleep laboratories in the United States and around the world, limiting PSG access. Because of the paucity of in laboratory-polysomnography, it is estimated that only 10% of the 500 000 children undergoing adenotonsillectomy annually in the United States have preoperative PSG.^65,66 Therefore, it is unknown whether these children had OSAS and indeed required surgery. Second, in addition to the expense of the PSG itself, in-laboratory testing often requires families to make significant changes to their schedule, including travel to the testing site. This is a particular challenge for families of children with special needs or with added childcare costs for siblings left at home. Third, although home sleep diagnostics have been available for several years, with home sleep apnea testing (HSAT) used in pediatric research,^67,68 the role for HSAT in clinical pediatric sleep medicine is yet to be ascertained. As a result, the American Academy of Sleep Medicine does not recommend the use of HSAT for diagnosing OSAS in children,⁶⁹ which has created a significant barrier for families and clinicians, as insurance will not cover pediatric HSAT.

Several research gaps must be addressed to advance the use of HSAT in pediatric sleep. Studies are needed to demonstrate the feasibility of HSAT in larger groups of diverse children, with and without developmental disabilities. In addition, the role of HSAT in clinical decision-making needs to be established. Furthermore, randomized controlled trials of HSAT versus in-laboratory PSG are warranted. Finally, patient and family-centered outcomes must be taken into consideration when designing trials and interpreting results.

In addition to HSAT, it is important to establish whether the many commercially available wearable devices that report the ability to track sleep have a role in medicine. A comprehensive review of these accelerometer-based devices is outside the scope of this paper. Of note, however, substantial variation exists in the extent to which commercially available wearable devices accurately assess different aspects of pediatric sleep.⁷⁰ Furthermore, many device scoring algorithms are proprietary, limiting opportunities for independent validation research, and the rapid device production and innovation makes it challenging for research to keep pace.⁷¹ Nonetheless, these devices could provide useful data about sleep patterns over multiple nights, which may assist providers in assessing and treating sleep health concerns.

To address these gaps, a patient-centered research approach is needed. Academic research centers have historically worked in silos. Partnering with general pediatric practices in the community, including through research networks,⁷² would increase referrals of children with suspected SDB to clinical trials. This partnership must benefit families, academic research centers, and primary care practices. For studies of HSAT or consumer wearables, engagement could improve if research personnel were deployed to primary care practices to perform device set up, minimizing family travel time and expense, and providing opportunities for partnering with primary care providers as research colleagues. Finally, patient and family-centered outcomes have been long neglected in pediatric sleep research. Qualitative and mixed methods research in primary care are needed to inform future clinical trials, with family advisory boards established to review proposed primary care research and ensure the inclusion of patient and family-centered outcomes.^31,32

Discussion

Collectively, these workshop sessions underscore the need for multidisciplinary research to address salient gaps in knowledge and barriers to promoting optimal sleep health and ventilatory control in primary care. The following section describes strategies to address these gaps that were identified in workshop small group discussions. Participants included the session speakers, research scientists, sleep medicine specialists, pulmonologists, general and community pediatricians, family members of children affected by respiratory disease, and representatives from the National Institutes of Health. Strategies are presented in Fig 1 and Table 1, and are contextualized in a socio-ecological framework.

TABLE 1.

Knowledge Gaps and Opportunities in Sleep and Ventilatory Control Research

Gap	Opportunities
Key aspects of sleep health are poorly understood.	• Examine multiple inclusive domains of pediatric sleep health to better define normative trends across typically developing samples and among children with co-occurring chronic health, behavioral health, and/or neurodevelopmental conditions. • Identify optimal sleep duration, as well as the impacts of too much sleep, based on observed data. • Establish a consistent method to measure sleep quality. • Identify causal or mechanistic drivers linking multiple domains of sleep health with child functional outcomes. • Understand how sleep health may vary developmentally and according to familial and cultural beliefs, values, and norms.
Knowledge about ventilatory control is limited, especially during infancy.	• Examine natural trajectories of ventilatory control from birth to better understand its etiology and to identify biomarkers. • Identify phenotypes of sleep disordered breathing longitudinally and across age groups. • Investigate the clinical significance of long-term undiagnosed sleep disordered berathing on mental, neurobehavioral, metabolic, and cardiovascular health.
There are significant barriers to identifying and treating sleep health concerns and poor ventilatory control.	• Develop and evaluate efficient, automated screening tools to identify problems with sleep health and ventilatory control in primary care and other outpatient child healthcare settings. • Create educational and interventional resources that are easily accessible and effective for primary care clinicians and other outpatient providers. • Examine the feasibility, acceptability, and validity of home sleep apnea testing across socio-demographically diverse patient populations, including those with co-occurring conditions. • Establish an infrastructure to enhance communication about and shared decision-making for sleep and ventilatory control problems across primary care clinicians, pulmonary and sleep medicine providers, and families.

Build Longitudinal Cohorts Focused on Pediatric Sleep and Ventilatory Control

Building birth or prenatal cohorts is one strategy to address critical gaps in knowledge about the etiology of sleep and ventilatory control patterns and disorders. Birth cohort studies are crucial for identifying key risk factors and exposures during the prenatal or postnatal period, as well as to longitudinally examine the health status of the newborn through childhood and ideally adulthood.^73,74 Prospective studies also allow investigators to focus on a myriad of longitudinal outcomes that can encompass pulmonary symptoms, diseases, biomarkers, lung function,⁷⁵ sleep duration and continuity, SDB,⁷⁶ and related neurobehavioral outcomes.^77,78 Collaboration with obstetrician-gynecologists and primary care pediatrician colleagues are instrumental to develop these cohorts, ensure adequate follow-up, and limit attrition.

Foster Implementation Science

The field of implementation science focuses on developing, evaluating, and disseminating strategies to enhance the systematic uptake of evidence-based practices.^79,80 Such practices could include a specific intervention or treatment, adherence to a clinical practice guideline, or screening tool or diagnostic method.⁸⁰ A major goal of implementation science research is to speed the translation of effective practices to usual care settings,⁸⁰ a process that historically has occurred over 1 to 2 decades.⁸¹ Applying implementation science models, theories, and frameworks⁸² to sleep and ventilatory control research could help reduce the observed gaps in care described above. For example, research is needed to identify the best strategies to effectively translate and scale screening tools that could be integrated in the EHR to better assess and address sleep health and SDB in primary care. Applying an implementation science framework, such as RE-AIM,⁸³ to design a study comparing the reach, effectiveness, adoption, implementation, and maintenance of 2 different implementation strategies⁸⁴ for deploying a primary care-based sleep screening tool could help to advance this work.

Other articles in this issue provide more detail about other areas of pulmonary health that could benefit from implementation science methods to enhance uptake of available tools, such as pulmonary function testing. Locating clinical intervention research studies along the continuum of implementation science methods (see Lane-Fall et al⁸⁰) could help researchers identify where and how to integrate these methods into their work. In the area of sleep medicine, some studies have begun to adapt evidence-based behavioral sleep strategies for children with downstream implementation in mind⁸⁵ and to test adult insomnia treatment implementation strategies at the clinician level,⁸⁶ but overall, there are few studies applying these methods to pediatric sleep and ventilatory control intervention research.

Build Multidisciplinary Collaboration and Training

Clinical practice, research, and training in sleep and ventilatory health should include multidisciplinary collaborations between pulmonary and sleep medicine specialists, primary care clinicians, academic medical settings, community primary care practices and organizations, and families. Establishing clinical and training partnerships among primary and specialty care clinics can enhance the early detection of sleep and ventilatory control problems and encourage collaborative care between medical teams. Primary and specialty care integration is particularly important given that many families face barriers to accessing specialty care^29,30 but typically visit a pediatrician at least once per year. These primary and specialty care collaborations should also focus on including families and community members to ensure these key informants help to drive clinical research priorities and the adaptation of evidence-based care guidelines into practice-based settings. Multidisciplinary research may also facilitate innovation in sleep and pulmonary science, especially regarding the etiology and management of sleep and ventilatory control problems across development and diverse child populations. Multidisciplinary collaboration might include partnerships with schools and community organizations serving children and families, given the impacts of poor sleep health and ventilatory control problems on overall child functioning. Finally, leveraging existing pediatric primary care networks to implement large-scale research projects in both academic medical setting-affiliated and community-based sites is necessary for enhancing the reach and generalizability of sleep and ventilatory control research.

Increase Diversity, Equity, and Inclusion in All Aspects of Clinical Research

Racism has rightfully been recognized as a social determinant of health.^23,87 Therefore, it is our duty to take necessary steps to equitably recruit and retain a diverse pool of both research participants and research investigators. For research participants, we need to build programs across and within communities to foster trust in research participation⁸⁸ and to reach families in their own environment.^89,90 Researchers also have their own implicit and explicit biases when approaching diverse populations. To mitigate this, it is recommended that researchers use existing tools to be cognizant about their biases (eg, https://www.projectimplicit.net/), to integrate a health equity lens into all aspects of their research,⁹¹ and include a diverse group of participants, ideally representing the population to be studied. Historically, the distribution of researchers has been skewed toward male sex and white race.^92,93 Thus, National Institutes of Health and other funding agencies need to continue and expand initiatives to increase the diversity of researchers, such as through internships or summer training programs for undergraduates, diversity specific awards (K01), and grant supplements to increase diversity.

Conclusions

Continuing to work in siloed lines of research and practice will not address the multiple socio-ecological factors that contribute to healthy sleep and optimal ventilatory control in children. The interdependency of sleep and pulmonary health provides a strong argument to adopt a holistic approach to prevent, treat, and manage primary pulmonary and sleep conditions as well as their comorbidities. Taking a multidisciplinary approach to address gaps in pediatric sleep and ventilatory control research, clinical care, and training has the potential to make a significant impact on the health and wellbeing of children and their families. The strategies we have proposed to advance pediatric sleep and pulmonary health represent initial steps in the ongoing collaborative work necessary for supporting and enhancing these vital signs of child health.

Glossary

CDS

clinical decision support

EHR

electronic health record

HSAT

home sleep apnea testing

OSAS

obstructive sleep apnea syndrome

Peds-B-SATED

conceptual model for pediatric sleep health including behavior, satisfaction, alertness, timing, efficiency, and duration

PSG

polysomnography

SDB

sleep disordered breathing