Introduction
Sleep issues occur at higher rates in children with neurodevelopmental disorders than in the typical population. Little is known about the impact of COVID-19 on sleep issues in this population
Method
This integrative review aimed to characterize studies during the COVID-19 pandemic (2020–2022) addressing the prevalence and management of sleep issues in children and youth with neurodevelopmental disorders.Comprehensive database searches were used to identify articles, and 31 studies were considered suitable for this review.
Results
Most studies reported worsening sleep disturbances during COVID-19 restrictions. All studies were conducted when clinics were closed; only two studies addressed treatment options such as music therapy and sleep hygiene education and found improvement in sleep issues.
Discussion
Future research needs to concentrate on developing interventions to assist families remotely and empower families with a toolkit of preparedness in times of crisis
KEY WORDS
INTRODUCTION
A notable COVID-19 outbreak rapidly spread throughout many countries in December 2019; stay-at-home orders were issued to contain the virus in the ensuing months. These lockdown orders persisted for several weeks to months, causing a complete disruption of daily routines in the general population because of working from home, homeschooling, and reduced levels of physical activity and social gatherings (
Cheng et al., 2020
). During the COVID-19 restrictions, only 4.8% of children and 0.6% of youth met recommended activity guidelines, whereas leisure screen time and social media use were reported as much higher than before the COVID-19 lockdowns (Moore et al., 2021
).- Moore S.A.
- Sharma R.
- Martin Ginis K.A.
- Arbour-Nicitopoulos K.P.
Adverse Effects of the COVID-19 Pandemic on Movement and Play Behaviours of Children and Youth Living with Disabilities: Findings from the National Physical Activity Measurement (NPAM) Study.
International Journal of Environmental Research and Public Health. 2021; 18: 12950
Children with neurodevelopmental disorders (NDD) such as autism spectrum disorder (ASD) commonly have difficulties in behavior, communication, and sensory integration (
Masi et al., 2017
), have high vulnerability to lifestyle changes (Barkley and Fischer, 2011
), and often struggle with changes in routines (Touhy and Yazdani, 2018
). Children with NDD are also at higher risk for various sleep disturbances (Chen et al., 2021
; Esbensen and Schwichtenberg, 2016
). According to previous studies, sleep disturbance has been reported in 67.3% of children with ASD (Chen et al., 2021
), 28.5% to 44.8% of children with attention deficit hyperactivity disorder (ADHD; Sung et al., 2008
), and 24% to 86% of children with intellectual disabilities (Korb et al., 2021
). In addition, 35% to 95% of children with NDD reported sleep-related symptoms such as restless sleep, waking very early, and being tired during the daytime, but only 15% of them reported complaints about sleep problems (- Korb L.
- O'Regan D.
- Conley J.
- Dillon E.
- Briggs R.
- Courtenay K.
- Perera B.
Sleep: The neglected life factor in adults with intellectual disabilities.
BJPsych Bulletin. 2021; https://doi.org/10.1192/bjb.2021.122
Ashworth et al., 2013
).Thus, disruption to daily activities, educational routines, and scheduled therapies because of COVID-19 lockdowns may have been a source of stress leading to an exacerbation of sleep problems. Synthesizing information on the impact of COVID-19 restrictions on sleep is crucial to recovering from the pandemic and may also assist in preparing this vulnerable population for future public health stressors. In addition, this information is crucial to providers in addressing parental questions and concerns while providing therapeutic advice.
METHODS
The authors conducted an integrative review following the updated methodology described by
Whittemore and Knafl, 2005
, comprising a five-step process: (1) problem identification, (2) literature search, (3) data evaluation, (4) data analysis, and (5) presentation. The integrative review methodology allows researchers to summarize empirical studies with varied methodologies to better understand a health care phenomenon (Broome and Knafl, 1993
). Although the method explicitly allows for the inclusion of theoretical literature, the authors chose to restrict their analysis to empirical studies.Problem Identification
Sleep issues occur at higher rates in children with NDD than in the typical population. Little is known about the impact of COVID-19 on sleep issues in this population. This integrative review aimed to characterize empirical studies focused on sleep behaviors in children and youth, aged from birth to 21 years, with NDD during the COVID-19 pandemic (2020–2022).
Literature Search
The authors created comprehensive searches in PubMed, CINAHL, Embase (Embase.com), American Psychological Association PsycINFO (EBSCOhost), and Scopus to identify articles that addressed sleep issues in children with NDD during the COVID-19 pandemic. The search strategy focused on four broad sets of terms, including (1) sleep and sleep disorders, (2) neurodevelopmental disorders, (3) children, and (4) COVID. The search included keywords, database-specific controlled vocabulary terms (e.g., MESH, Emtree, etc.), Boolean operators, and term truncation, as necessary, to maximize search results. When appropriate, controlled vocabulary terms were “exploded,” a search process that simultaneously searches for a broad concept such as sleep disorders while searching for a list of specific sleep disorders. To maximize retrieval related to the COVID-19 pandemic, the authors used the Canadian Agency for Drugs and Technologies in Health PubMed and Scopus search strings and adapted the Embase search string, which was written for Ovid. Because the search strings were not written for CINAHL and American Psychological Association PsycINFO, the authors used them as a starting point to develop the COVID searches, substituting appropriate controlled vocabulary from each database (
Canadian Agency for Drugs and Technologies in Health 2022
). The searches were finalized and conducted in each database on May 6, 2022, and were limited to English-language articles published in 2020–2022. Interested readers can view the full text of the searches at https://doi.org/10.6084/m9.figshare.20186600.Canadian Agency for Drugs and Technologies in Health. (2022). CADTH COVID-19 search strings. https://covid.cadth.ca/literature-searching-tools/cadth-covid-19-search-strings/.
Inclusion criteria were empirical studies that addressed children with NDD and sleep issues that specifically addressed the COVID-19 pandemic. For this review, children were defined as aged from birth to 21 years because the U.S. Individuals with Disabilities Education Act provides services through 21 years of age (1990). Articles were excluded if they did not describe a study methodology, were not in English, not available in full text, or did not specifically address the impact of the COVID-19 pandemic on sleep in children with NDD.
The Figure shows the steps of the study selection process using the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines (
Moher et al., 2009
). The authors used Covidence systematic review management system (https://www.covidence.org/) to collaborate on the review process. Covidence removes duplicate references and enables team members to screen titles and abstracts independently for inclusion and full-text articles for exclusion. When team members’ decisions differed, they discussed the studies via live meetings and email to reach a consensus. After completing all these steps, the authors identified 61 studies for full-text review and selected 31 studies for data extraction.
FIGUREPreferred Reporting Items For Systematic Reviews and Meta-Analyses flow diagram. . This figure appears in color online at www.jpedhc.org.
Moher et al., 2009
Data Evaluation
Studies were evaluated using the American Association of Critical Care Nurses Evidenced-Level hierarchy (
Peterson et al., 2014
). This system includes five levels, A through E, and is effective when quantitative and qualitative primary sources are included. Level A is the highest level of evidence and includes meta-analyses and meta-synthesis. Level E is the lowest level and includes case reports and expert opinions. All studies in this review met level C evidence, encompassing qualitative, descriptive, or correlational studies, integrative reviews, systematic reviews, or some randomized controlled trials that bear inconsistent results. Because relatively few empirical studies have been published that address the COVID-19 pandemic's impact on sleep in children with NDD, the authors chose the American Association of Critical Care Nurses hierarchy as the most appropriate method to evaluate the overall quality of studies. Evaluation methods also included ensuring that the studies fully addressed the research question and specific research method. The authors chose to eliminate case studies, which they concluded provided minimal evidence that could be used to address the research question.Data Analysis and Presentation
The authors constructed a matrix table to capture study characteristics, including setting/country purpose, research design, period, sample size and characteristics, and measurements/instruments. After extracting the data from the matrix, the authors reviewed it for accuracy and completeness. The authors then thematically analyzed the results matrix to find their commonalities and differences.
RESULTS
Samples
All 31 studies focused on children and youth with NDD, grouped or separated into specific populations. Twelve studies (39%) focused solely on ASD, whereas six (19%) enrolled participants with ADHD only. One study compared these two sample populations. Nine studies (29%) enrolled participants with neurodevelopmental disorders, including ASD, ADHD, learning disabilities, cerebral palsy (CP), or other physical, sensory, neurological, or cognitive diagnoses. Three individual publications emerged for CP, epilepsy, and fragile X syndrome. See Table 1 for sample sizes.
TABLE 1Summary of included studies
| Author (year), country | Purpose | Design | Period | Sample | Measurements |
|---|---|---|---|---|---|
Becker et al., 2021 ,United States | To examine changes in adolescent sleep before and during the COVID-19 pandemic in adolescents with and without ADHD | Prospective | From September 2019 to February 2020 and from May to June 2020 | 122 adolescents aged 15–17 years with and without ADHD | SHQ, SDSC, COVID-19 Adolescent Symptom and Psychological Experience Questionnaire, Coronavirus Health Impact Survey |
Berard et al., 2021 ,France | To examine the impact of COVID-19 containment and mitigation efforts on behaviors, communication, sleep, and nutrition | Cross-sectional, descriptive | April–May 2020 | 229 ASD children and youth part of the ELENA cohort aged 2–21 years | A four-part COVID-19 parent structured questionnaire, VABS-II, CSS of the ADOS-2 |
Bıyık et al., 2021 , Turkey | To investigate the effects of the COVID-19 pandemic on body structures and functions, activity and participation levels, and environmental factors of children with CP | Prospective | May to June 2020 | 103 children with CP aged 2–18 years | COVID-19 stay-at-home cerebral palsy parental questionnaire, GMFCS-FR |
Bompard et al., 2021 , Italy
Home-based music therapy for children with developmental disorders during the COVID-19 pandemic. Journal of Telemedicine and Telecare. 2021; https://doi.org/10.1177/1357633X20981213 | To investigate the feasibility and impact of a home-based music therapy program to sustain children with developmental disorders secondary to neurological diseases and their parents | Prospective, monocentric, noncontrolled pilot | May to March 2020 | 12 children with developmental delay | GMFCS, SDSC, PSI-SF |
Bruni et al., 2021a ,Italy | To evaluate different responses in two clinical conditions, ASD and ADHD, regarding sleep patterns and disturbances | Descriptive | May to June 2020 | Parents of 100 ASD, 236 ADHD patients, and 340 healthy controls aged 4–18 years | A modified version of the SDSC |
Bruni et al., 2021b ,Italy | To examine the impact of home confinement (lockdown) because of the COVID-19 pandemic on the sleep patterns of children and adolescents with ADHD | Descriptive | June 2020 | 992 children with ADHD, aged 5–17 years | A modified version of the SDSC |
Bruni et al., 2022 ,Italy | To evaluate the impact of the lockdown on sleep patterns and sleep disturbances with respect to the preceding conditions in children and adolescents with ASD | Descriptive | May to June 2020 | 111 participants with ASD, aged 1–18 years | A modified version of the Sleep Disturbance Scale for Children (SDSC) |
Çetin et al., 2020 , Turkey | To investigate the relationship between chronotype preference/sleep problems and symptom severity of children with ADHD and to assess the chronotype preference/sleep problems that may playa mediating role in the relationship between the reactions to trauma and the severity of ADHD symptoms | Cross-sectional | May 2020 | 76 children with ADHD, aged 8–12 years | CRIES-8, CSHQ, CCQ, T-DSM-IV-S |
Conti et al., 2020 ,
Behavioural and emotional changes during COVID-19 lockdown in an Italian paediatric population with neurologic and psychiatric disorders. Brain Sciences. 2020; 10: 1-15 Italy | To investigate lockdown-related emotional and behavioral changes in the pediatric neuropsychiatric population | Observational, longitudinal | Prepandemic September 2019 and February 2020; pandemic collection from April to May 2020 | 141 children with neuropsychiatric disorders aged 1.5–18 years | General questionnaire, CBCL |
Di Giorgio et al., 2021 , Italy | To investigate how the lockdown impacted children with FXS | Descriptive | April–May 2020 | 53 children with FXS, aged 3–16 years | Ad hoc survey questions about children's sleep habits, CAPES-DD |
Dondi et al., 2021 , Italy | To evaluate the effects of COVID-19 quarantine on sleep quality as an indicator of psychological well-being among children and adolescents | Cross-sectional | September–October 2020 | 6,210 children aged 0–18 years, including children affected with specific learning disabilities, ASD, other disabilities, chronic diseases, and multiple conditions | 78-question web-based survey |
Garcia et al., 2021 ,United States | To examine changes in physical activity, screen time, and sleep in adolescents with ASD because of the COVID-19 pandemic | Observational | April 2020 | Nine students with ASD, aged 16.87 ± 1.36 years | A survey measuring physical activity, screen time, and sleep duration before and during the pandemic |
Guller et al., 2021 ,
Those in the shadow of the pandemic: Impacts of the COVID-19 outbreak on the mental health of children with neurodevelopmental disorders and their parents. International Journal of Developmental Disabilities. 2021; https://doi.org/10.1080/20473869.2021.1930827 Turkey | To investigate the emotional and behavioral responses of children with neurodevelopmental disorders and their parents during the recent novel coronavirus disease (COVID-19) pandemic and the associated factors | Cross-sectional | April 2020 | 299 children and adolescents with neurodevelopmental disorders aged 2–18 years | Sociodemographic form and COVID-19 pandemic-related characteristics, HADS |
Huang et al., 2021 , China | To investigate the impact of the COVID-19 pandemic on ASD children and their families | Cross-sectional | May 2020 | 406 children with ASD, mean age 4.6 years (SD = 2.3) | 4-part online survey with some questions specific to sleep, SAS for parent anxiety |
Lugo-Marín et al., 2021 , Spain
COVID-19 pandemic effects in people with autism spectrum disorder and their caregivers: Evaluation of social distancing and lockdown impact on mental health and general status. Research in Autism Spectrum Disorders. 2021; 83101757 | To study the psychological impact of the lockdown because of the social emergency (COVID-19) in children/adolescents and adults diagnosed with ASD | Not specified | 8 weeks after lockdown | The sample was subdivided into two ASD groups, 37 children and adolescents (aged 3–17 years and 11 months), and 35 adults (aged ≥ 18 years) | CBCL, Symptom Checklist 90 revised (SCL-90) for adults |
Masi et al., 2021 , Australia | To examine the impact of the COVID-19 pandemic on child mental health and socioemotional and physical well-being (including sleep, diet, exercise, use of electronic media; caregiver perceptions of symptoms of child NDD and comorbidities), and caregiver mental health and well-being, social support and service use | Cross-sectional | May–June 2020 | 302 caregivers of children with neurodevelopmental disabilities aged 2–17 years | Child symptom severity and well-being, parent well-being, and service access and satisfaction questionnaire |
Mete Yesil et al., 2022 Turkey | To explore how the lives of children with special needs and their families were affected by the COVID-19 pandemic | Descriptive | Enrolled in April 2020 (approximately 6 weeks after the lockdown) | 117 children with DD, ASD, hearing or language impairments, and receiving special education, aged 4–6 years | Five-part questionnaire focusing on the amount of change caused by the COVID-19 pandemic on feeding, toilet habits, daily routines, development, physical activities, daily activities, one-on-one time durations with parents, screen time, and whether and how much they performed and maintained their previous educator-provided special education at home were collected using |
Micheletti et al., 2021 Argentina | To define the frequency and types of sleep problems in a sample of children with DDs, determine the proportion of pediatricians who addressed such difficulties, assess the effects of SH, and describe the impact of the COVID-19 pandemic on sleep | Quasi-experimental | May 2020 | 161 children with DDs, ages 1–6 years, who attended clinic visits between July 2019 and March 2020 with follow-up before July 2020 | Children's Sleep Habits Questionnaire, Spanish version (CSHQ-S), completed before and after interventions |
Moore et al., 2021 Canada
Adverse Effects of the COVID-19 Pandemic on Movement and Play Behaviours of Children and Youth Living with Disabilities: Findings from the National Physical Activity Measurement (NPAM) Study. International Journal of Environmental Research and Public Health. 2021; 18: 12950 | To assess parent-perceived changes in physical activity, sedentary behavior, and sleep quality and quantity because of COVID-19 restrictions | Not specified | April and May 2020 | 151 children with disabilities aged 4–17 years | Online survey adapted from the Canadian Health Measures Survey, amended version of the 2020 COVID-19 and Childhood Movement behaviors survey |
Mutluer et al., 2020 ,Turkey | To investigate how individuals with ASD responded to COVID-19 regarding their comprehension and adherence to implemented measures, changes in their behavioral problems, and how their caregivers’ anxiety levels relate to these behavioral changes | Not specified | During the last 1-month, COVID-19 measures were implemented | 87 individuals with ASD, mean age 13.96 ± 6.1, and age range of 3–29 years | ABC, PSQI, BAI |
Navarro-Soria et al., 2021 ,Spain | To evaluate the consequences of the lockdown in children and teenagers diagnosed with ADHD, sleep-related problems, and problems with executive functions | Associative-comparative and explanatory | April 2020 | 234 children divided into two groups, confined ADHD and confined non-ADHD, aged 6–18 years | STAIC self-assessment questionnaire, BEARS sleep-screening tool for sleep disorders in childhood, BDEFS- CA, short form |
Nithya et al., 2021 , India | To systematically assess the impact of the COVID-19 pandemic on ADL, play, and sensory behaviors of children with ASD | Cross-sectional | Approved January 2021. performed for 1 month | 100 children with ASD, ages 2 to above 10 years | A structured ADL, play, and sensory behavior questionnaire (45 items) |
Polónyiová et al., 2022 ,Slovakia | To explore how the first and second waves of the COVID-19 outbreak affected the mental health of families in Slovakia, focusing on comparing families with autistic children to a general sample. Focused on the prevalence of depression, anxiety, and stress symptoms among the parents and maladaptive behavior or sleep disturbances of their children and their correlations | Not specified | First wave from June to July 2020, and second wave from November to December 2020 | 332 caregivers, 155 having children with ASD (179 surveyed during the first wave and 153 during the second wave) | DASS-42 subscales of Vineland-3 questionnaire |
Rabbani et al., 2021 , Bangladesh | To evaluate behavioral patterns of risk and resilience for children with ASD | Longitudinal | November 2019–November 2020 | 150 children with ASD, aged 2–9 years | Two mCARE tools assessed 30 behavioral parameters |
Rosenthal et al., 2022 , United States | To examine the impact of COVID-19 on youth with ADHD during two stages of the pandemic | Longitudinal | May 2020 and March 2021 | 620 youth with ADHD and 614 individually matched controls participating in the ABCD study | Prepandemic functioning: KSADS-5, ABCD PMP, ABCD PMQ, ABCD SRPF Pandemic functioning: COVID RRR |
Scarselli et al., 2022 , Italy | To study the change in sleep habits of children with ASD during the COVID-19 pandemic | Not specified | April–June 2020 | 28 children with ASD, aged 2–6 years | CSHQ |
Swansburg et al., 2021 ,Canada | To understand the impact of the COVID-19 pandemic on lifestyle habits, mental health symptoms, and ADHD behaviors in children with ADHD | Not specified | May to June 2020 | 587 children with ADHD, aged 5–18 years | Survey with lifestyle questions; PHQ-9, GAD-7, SNAP-IV |
Tokatly Latzer et al., 2021 ,Israel | To explore and characterize in depth the experiences of parents and children with autism who have been going through the COVID-19 lockdown | Qualitative | April 2020 | 25 children with autism, aged 4–6 years | Semistructured telephone interviews |
Trivisano et al., 2020 , Italy | To assess how the COVID-19 pandemic has affected children with epilepsy | Not specified | May 2020 | 3,321 responses to the survey (96.6% caregivers of patients aged 0 to > 18 years), 59.7% of patients had an intellectual disability, and 44.3% had behavioral disturbances | 45-item questionnaire |
Türkoğlu et al., 2020 ,Turkey | To investigate the relationship between chronotype preference/sleep problems and symptom severity of children with ASD during the confinement and social isolation of the COVID-19 outbreak | Not specified | May 2020 | 46 drug-naive children with ASD, aged 4–17 years | AuBC, CSHQ, and CCQ |
Ueda et al., 2021 , Japan
The quality of life of children with neurodevelopmental disorders and their parents during the coronavirus disease 19 emergency in Japan. Scientific Reports. 2021; 11: 3042 | To evaluate how the QOL of children and their parents has been affected by changes in the sleep cycles of children with NDDs and stresses caused by mothers’ work patterns during the COVID-19 pandemic | Not specified | April–May 2020 | 136 school-age children with IDD, mean age 10.6 ± 2.6 | CBCL, WISC-IV, WHO-QOL-BREF, CES-D, STAI, PSI |
Note. ABC, aberrant behavior checklist; ABCD, Adolescent Brain Cognitive Development study; ADHD, attention deficit hyperactivity disorder; ADL, activities of daily living; ADOS-2, Autism Diagnostic Observation Schedule-2; ASD, autism spectrum disorder; AuBC, autism behavior checklist; BAI, Beck Anxiety Inventory; BDEFS-CA, Barkley Deficits in Executive Functioning Scale—Children and Adolescents; CAPES-DD, Child Adjustment and Parent Efficacy Scale-Developmental Disability; CBCL, Child Behavior Checklist; CCQ, Children's Chronotype Questionnaire; CES-D, Center for Epidemiologic Studies Depression scale; CP, cerebral palsy; CRIES-8, Children's Impact of Event Scale;
CSHQ, Children's Sleep Habits Questionnaire; CSS, calibrated severity score; DASS-42, Depression Anxiety and Stress Scale; DD, developmental disorders; FXS, fragile X syndrome;
GAD-7, generalized anxiety disorder 7; GMFCS, Gross Motor Function Classification System; GMFCS-FR, Gross Motor Function Classification System Family Report; HADS, Hospital anxiety and depression scale; KSADS-5, kiddie schedule for affective disorders and schizophrenia for DSM-5; NDD, neurodevelopmental disorders; PHQ-9, Patient Health Questionnaire 9;
PMQ, parental monitoring survey; PSI, Parental Stress Index; QOL, quality of life; PMP, parent medications survey inventory modified from PhenX; PSI-SF, Parent Stress Index-short form
PSQI, Pittsburgh Sleep Quality Index; RRR, rapid response research survey; SAS, Self-Rating Anxiety Scale; SDSC, Sleep Disturbance Scale for Children; SH, sleep hygiene; SHQ, Sleep Health Questionnaire; SNAP-IV, Swanson, Nolan, and Pelham Teacher and Parent Rating Scale; SRPF, School Risk and Protective Factors Survey; STAI, State-Trait Anxiety Inventory; STAIC, State-Trait Anxiety Inventory for Children; T-DSM-IV-S, Turgay DSM-IV Disruptive Behavior Disorders Rating Scale; VABS-II, Vineland Adaptive Behavior Scales, second edition; WHO-QOL-BREF, World Health Organization quality of life; WISC-IV, Wechsler Intelligence Scale for Children (fourth edition).
Outcome Measures
Each of the 31 studies examined sleep in various ways. Six validated sleep instruments were employed in 11 quantitative studies. These tools included: the Sleep Habits Survey (
Wolfson et al., 2003
), original or modified versions of the Sleep Disturbance Scale for Children (SDSC; Bruni et al., 1996
), Children's Sleep Habits Questionnaire (CSHQ; Owens et al., 2000
), Children's Chronotype Questionnaire (CCQ; Zavada et al., 2005
), Pittsburgh Sleep Quality (Buysse et al., 1989
), or BEARS sleep-screening tool (Owens and Dalzell, 2005
). Four studies assessed sleep using components of validated behavior assessment tools such as the Child Behavior Checklist (Achenbach and Edelbrock, 1991
), Vineland Adaptive Behavior Scale (Sparrow and Cicchetti, 1989
), Canadian Health Measures Survey (adapted version; Tremblay et al., 2007
), Patient Health Questionnaire (Spitzer et al., 1999
), and the COVID-19 Stay-at-Home Cerebral Palsy Parental Questionnaire (Bıyık et al., 2021
). The remainder of the quantitative studies included ad hoc sleep questions in surveys or study-specific instruments (e.g., mCare tools). The one qualitative study employed a semistructured phone interview (Tokatly Latzer et al., 2021
).Findings
Findings are grouped by sample types and data collection measures.
ASD, ADHD, and controls: Validated sleep tool
During the lockdown, one study examined all 3 groups using the SDSC (
Bruni et al., 2021a
). Children with ADHD demonstrated later bedtime and rise time than those with ASD or controls. Both clinical groups significantly demonstrated a reduced sleep duration compared with controls. These two groups also had an increase in hypnic jerks, rhythmic movement disorders, night awakenings, restless sleep, sleepwalking, and daytime sleepiness over the control group. All groups had increased anxiety at bedtime, difficulties falling asleep, and daytime sleepiness.ASD: Validated sleep tools
Using the SDSC, one study found a significant increase in sleep disturbances, difficulty falling asleep, anxiety at bedtime, sleep terrors, and daytime sleepiness (
Bompard et al., 2021
). Parents reported the following factors impacting their child's sleep: lack of obliged rise time, lack of sports activities, increased screen time, more time spent with family, and changes in routine (- Bompard S.
- Liuzzi T.
- Staccioli S.
- D'Arienzo F.
- Khosravi S.
- Giuliani R.
- Castelli E.
Home-based music therapy for children with developmental disorders during the COVID-19 pandemic.
Journal of Telemedicine and Telecare. 2021; https://doi.org/10.1177/1357633X20981213
Bompard et al., 2021
). A Pittsburgh Sleep Quality study reported significant changes in sleep disturbance, duration, and quality during the pandemic (- Bompard S.
- Liuzzi T.
- Staccioli S.
- D'Arienzo F.
- Khosravi S.
- Giuliani R.
- Castelli E.
Home-based music therapy for children with developmental disorders during the COVID-19 pandemic.
Journal of Telemedicine and Telecare. 2021; https://doi.org/10.1177/1357633X20981213
Mutluer et al., 2020
). Parents who were asked to complete one copy of the CSHQ with reference to behaviors during the pandemic and one copy with reference to prepandemic behaviors reported that 89.3% of children had clinically significant sleep disturbances during the pandemic (Scarselli et al., 2022
). However, these parents reported that sleep disturbances present before the pandemic either did not change or improve (Scarselli et al., 2022
). Employing both the CSHQ and CCQ, researchers reported that children with ASD had significantly greater sleep problems and chronotype score (eveningness) during home confinement, and sleep problems mediated the relationship between chronotype score and severity of autism symptoms (Türkoğlu et al., 2020
).ASD: Surveys
When parents were asked to rate changes in their child's sleep during the pandemic, most respondents reported no change in sleep (55.5%), but when a change was reported, it was perceived as worsening (
Berard et al., 2021
). These authors also performed a multivariate analysis that revealed that a higher Autism Diagnostic Observation Schedule-2 score was associated with a decreased probability of improvement in sleep, and belonging to a single-parent home was associated with worsening sleep (Berard et al., 2021
). An observational study of nine adolescents with ASD found that while sleep and wake times may have shifted, there were no reported differences in sleep duration prepandemic or during the pandemic (Garcia et al., 2021
). A larger survey discovered that half the parents reported sleep problems in their children and reduced outdoor activity. These families also reported a lack of professional support during the pandemic (Huang et al., 2021
). Similar findings were reported in Spain, in which 56% of caregivers reported sleep quality worsened in their children with ASD (Lugo-Marín et al., 2021
). A parent survey that focused on activities of daily living, play, and sensory behaviors identified 67% of the sample as having inconsistent sleep routines; the occupation of homemaker was 2.51 times more likely to report difficulty in managing their child's sleep schedule (- Lugo-Marín J.
- Gisbert-Gustemps L.
- Setien-Ramos I.
- Español-Martín G.
- Ibañez-Jimenez P.
- Forner-Puntonet M.
- Arteaga-Henríquez G.
- Soriano-Día A.
- Duque-Yemail J.D.
- Ramos-Quiroga J.A.
COVID-19 pandemic effects in people with autism spectrum disorder and their caregivers: Evaluation of social distancing and lockdown impact on mental health and general status.
Research in Autism Spectrum Disorders. 2021; 83101757
Nithya et al., 2021
). When comparing children with ASD to a control group, children with ASD demonstrated a significantly later bedtime, but as the COVID-19 lockdown progressed, sleep routines partially returned to pre-COVID-19 condition (Polónyiová et al., 2022
).ASD: Study-specific tools
A longitudinal study that used two mCare tools to gather pre-lockdown, lockdown, and post-lockdown information on 30 behavioral parameters found four behaviors (i.e., aggression, lack of concentration, pain sensitivity, sleep problems) were negatively impacted during the lockdown (
Rabbani et al., 2021
).ASD: Qualitative
Through a semistructured phone interview, researchers found sleep to be a common topic. Challenges were shared about children with ASD having difficulties falling asleep, frequent awakenings, or night terrors. The situation was compounded by closed outpatient clinics; some parents explored new ways to deal with their child's sleep issues (e.g., obtaining melatonin from another country;
Tokatly Latzer et al., 2021
).ADHD: Validated sleep tools
In a prospective study, parents completed the Sleep Habits Survey and adolescents with ADHD completed the SDSC; findings indicated shifts in sleep/wake schedules and longer sleep duration with clinically elevated rates of difficulties initiating and maintaining sleep; more worried/afraid effect, and less time outdoors correlated with more delayed sleep/wake behaviors (
Becker et al., 2021
). In a large sample of children and adolescents with ADHD, a modified version of the SDSC showed that the imposed COVID-19 lockdown affected sleep-wake rhythm dramatically from previous bedtime behaviors. These changes were associated with increased screen time (Bruni et al., 2021b
). One study that used both the CSHQ and CCQ along with the perception of trauma found eveningness chronotypes exhibited higher trauma symptoms and sleep problems, higher trauma scores were associated with higher chronotype scores, sleep problems, and oppositional defiant disorder symptoms, sleep levels mediated the relationship between trauma and oppositional defiant disorder symptoms, and sleep levels mediated the relationship between trauma and chronotype scores (Çetin et al., 2020
). When comparing children and adolescents with and without ADHD, those with ADHD were more negatively affected by the lockdown and had higher reported sleep problems, anxiety, and executive function issues (Navarro-Soria et al., 2021
).ADHD: Surveys
The Adolescent Brain and Cognitive Development Study compared youth with ADHD and matched controls without ADHD and found 1 year into the pandemic that youth with ADHD exhibited greater sleep problems with medium effect sizes (d = −0.52); the combined main effects of ADHD medication, ADHD diagnostic status, and screen time were significant predictors of sleep problems (
Rosenthal et al., 2022
). In a study investigating lifestyle behaviors in children with ADHD during the pandemic, these youth showed worsening changes in sleep, eating, screen time, and exercise with reported correlations to depression, anxiety, and ADHD symptoms (Swansburg et al., 2021
).Neurodevelopmental groups: Validated sleep tools
A prospective noncontrolled pilot study using the SDSC investigated the impact of a home-based music therapy intervention and observed significant improvements in sleep quality and reduction of parental stress in a cohort of children with developmental delay (
Bompard et al., 2021
). A quasi-experimental study using the CSHQ-S before and after pediatricians addressed sleep hygiene found half of the children with developmental delay had sleep problems that worsened during the pandemic, insomnia being most prevalent; pediatricians addressed sleep hygiene in only 45% of cases, but the intervention was found to be beneficial for most cases (- Bompard S.
- Liuzzi T.
- Staccioli S.
- D'Arienzo F.
- Khosravi S.
- Giuliani R.
- Castelli E.
Home-based music therapy for children with developmental disorders during the COVID-19 pandemic.
Journal of Telemedicine and Telecare. 2021; https://doi.org/10.1177/1357633X20981213
Micheletti et al., 2021
).Neurodevelopmental groups: Surveys
The Child Behavior Checklist subscale for sleep problems revealed a clinically worsening condition during the pandemic in younger children with neurological and/or psychiatric disorders (
Conti et al., 2020
). A large web-based survey examined sleep disorders in children aged < 18 years, including those with disabilities, ASD, chronic disorders, and specific learning disabilities; results indicated more difficulties falling asleep, staying asleep, and increased frequency of nightmares and/or sleep terrors with additional analyses identifying multiple risk factors (- Conti E.
- Sgandurra G.
- De Nicola G.
- Biagioni T.
- Boldrini S.
- Bonaventura E.
- Buchignani B.
- Della Vecchia S.
- Falcone F.
- Fedi C.
- Gazzillo M.
- Marinella G.
- Mazzullo C.
- Micomonaco J.
- Pantalone G.
- Salvati A.
- Sesso G.
- Simonelli V.
- Tolomei G.
- Battini R.
Behavioural and emotional changes during COVID-19 lockdown in an Italian paediatric population with neurologic and psychiatric disorders.
Brain Sciences. 2020; 10: 1-15
Dondi et al., 2021
). Delayed sleep phase and dyssomnia were the most frequently reported sleep problems in a survey investigating emotional and behavioral responses of children with neurodevelopmental disorders to the pandemic (Guller et al., 2021
). Two similarly designed studies reported reduced sleep quality and worsening sleep in children with neurodevelopmental disabilities and comorbidities (- Guller B.
- Yaylaci F.
- Eyuboglu D.
Those in the shadow of the pandemic: Impacts of the COVID-19 outbreak on the mental health of children with neurodevelopmental disorders and their parents.
International Journal of Developmental Disabilities. 2021; https://doi.org/10.1080/20473869.2021.1930827
Masi et al., 2021
; Mete Yesil et al., 2022
). The National Physical Activity Measurement Study surveyed parents of children and youth with developmental, physical, and/or sensory type of disabilities and reported a slight increase in sleep quantity, and parent capacity and opportunity to support a child's sleep was associated with better sleep quality (Moore et al., 2021
). Worsening sleep patterns in children with neurodevelopmental disorders was one of several factors associated with low quality of life for both parents and children during COVID-19 (- Moore S.A.
- Sharma R.
- Martin Ginis K.A.
- Arbour-Nicitopoulos K.P.
Adverse Effects of the COVID-19 Pandemic on Movement and Play Behaviours of Children and Youth Living with Disabilities: Findings from the National Physical Activity Measurement (NPAM) Study.
International Journal of Environmental Research and Public Health. 2021; 18: 12950
Ueda et al., 2021
).- Ueda R.
- Okada T.
- Kita Y.
- Ozawa Y.
- Inoue H.
- Shioda M.
- Kono Y.
- Kono C.
- Nakamura Y.
- Amemiya K.
- Ito A.
- Sugiura N.
- Matsuoka Y.
- Kaiga C.
- Kubota M.
- Ozawa H.
The quality of life of children with neurodevelopmental disorders and their parents during the coronavirus disease 19 emergency in Japan.
Scientific Reports. 2021; 11: 3042
Specific conditions: Surveys
A prospective investigation on the functional health status of children with CP reported that 17.5% experienced a decrease in sleep duration, whereas 25.2% experienced an increase in sleep duration (
Bıyık et al., 2021
). Children with fragile X syndrome demonstrated significant sleep changes during the lockdown, including difficulties falling asleep, longer falling asleep time, and frequency of night awakenings (Di Giorgio et al., 2021
). During the lockdown, sleep disorders worsened by 17 %, with 2.2% needing pharmacological treatment (Trivisano et al., 2020
).DISCUSSION
The impact of the COVID-19 pandemic and subsequent lockdowns was a universal phenomenon. The studies selected in this review represented various countries that experienced similar restrictions. Although studies varied in the number of participants, tools used to measure changes in sleep, and study design, all participant sampling focused on children with NDD. A common hypothesis among the studies was that children with NDD have higher rates of reported sleep problems at the most typical times.
All but two studies that enrolled ASD participants reported worsening sleep behaviors. A noted difference between the two studies was the sample size.
Scarselli et al., 2022
had 28 participants who had clinically significant sleep problems before the pandemic and reported that sleep problems either did not change or improved. Garcia et al., 2021
enrolled nine participants and reported no changes in sleep duration but only shifts in sleep times.Several studies with ASD participants investigated correlations with sleep. Children with higher Autism Diagnostic Observation Schedule-2 scores, belonging to single-parent households, the occupation of homemakers, and less time outdoors was associated with worsened sleep (
Berard et al., 2021
; Huang et al., 2021
; Nithya et al., 2021
).All studies with ADHD participants reported consistent worsening sleep problems and other behavioral changes. Predictors of sleep quality in this population included ADHD medication, diagnostic status, and screen time (
Rosenthal et al., 2022
). Screen time also affected sleep-wake rhythms (Bruni et al., 2021b
). Worsening changes in several lifestyle behaviors, including sleep, were associated with anxiety, depression, and ADHD symptoms (Swansburg et al., 2021
). Sleep was also a mediator of behavior and perception of trauma during COVID-19 (Çetin et al., 2020
).Only two studies addressed treatment options for children with developmental delays and saw improvements in addressing sleep issues (
Bompard et al., 2021
; - Bompard S.
- Liuzzi T.
- Staccioli S.
- D'Arienzo F.
- Khosravi S.
- Giuliani R.
- Castelli E.
Home-based music therapy for children with developmental disorders during the COVID-19 pandemic.
Journal of Telemedicine and Telecare. 2021; https://doi.org/10.1177/1357633X20981213
Micheletti et al., 2021
). All studies included in this review were conducted when clinics were closed, and behavioral support and treatment options were minimally available. Without treatment options, the quality of life for families was challenged (Ueda et al., 2021
).- Ueda R.
- Okada T.
- Kita Y.
- Ozawa Y.
- Inoue H.
- Shioda M.
- Kono Y.
- Kono C.
- Nakamura Y.
- Amemiya K.
- Ito A.
- Sugiura N.
- Matsuoka Y.
- Kaiga C.
- Kubota M.
- Ozawa H.
The quality of life of children with neurodevelopmental disorders and their parents during the coronavirus disease 19 emergency in Japan.
Scientific Reports. 2021; 11: 3042
Overall, this integrative review uncovered a trend toward worsening sleep problems in a sample of international studies focusing on children with NDD. These studies underscored that sleep behaviors rarely occur in isolation but can predict, mediate, or be associated with other personal or environmental factors. All studies included in this review measured sleep using subjective instruments. Strong evidence supports the use of actigraphy to objectively monitor and track sleep in children with neurodevelopment disorders (
Alder et al., 2020
; Yavuz-Kodat et al., 2019
). The actigraph device measures sleep in-home setting and are considered an objective method for measuring sleep onset, sleep-wake patterns, and sleep duration. Future studies should consider this method to provide objective and detailed data to obtain valuable information about this population. Future research will also need to develop interventions that consider personal or environmental factors to assist families during periods of isolation and when clinical support are lacking. It would behoove clinicians to assimilate techniques that easily transfer to home-based interventions and that can empower families with a toolkit of preparedness in times of crises.The authors would like to add one final note. Providing in-depth assessment and treatment options for sleep problems in children with NDD is beyond the scope of this integrative review. Comprehensive practice guidelines for treating insomnia and disrupted sleep in ASD have been developed by a subcommittee of the American Academy of Neurology (
Williams Buckley et al., 2020
). These guidelines provide evidenced-based recommendations for both nonpharmacologic and pharmacological treatment options. We encourage clinicians to refer to these guidelines and develop their sleep assessment and treatment toolkit on the basis of the unique needs of their practice population. Because the first crucial step to effectively addressing sleep problems is gaining a thorough understanding of the scope and characteristics of the chief concerns, we offer Table 2, which includes a summary of validated sleep assessment tools and additional resources for ease of reference.- Williams Buckley A.
- Hirtz D.
- Oskoui M.
- Armstrong M.J.
- Batra A.
- Bridgemohan C.
- Coury D.
- Dawson G.
- Donley D.
- Findling R.L.
- Gaughan T.
- Gloss D.
- Gronseth G.
- Kessler R.
- Merillat S.
- Michelson D.
- Owens J.
- Pringsheim T.
- Sikich L.
- Ashwal S.
Practice guideline: Treatment for insomnia and disrupted sleep behavior in children and adolescents with autism spectrum disorder: Report of the Guideline Development, Dissemination, and Implementation Subcommittee of the American Academy of Neurology.
Neurology,. 2020; 94: 392-404
TABLE 2Validated sleep assessment tools often used in children with NDD
| Screening tool | Description | Reference |
|---|---|---|
| BEARS | BEARS is divided into 5 major sleep domains (B = Bedtime Issues, E = Excessive Daytime Sleepiness, A = Night Awakenings, R = Regularity and Duration of Sleep, S = Snoring). Each sleep domain has a set of age-appropriate “trigger questions” for use in the clinical interview | Owens and Dalzell, 2005 |
| CSHQ | The 33-item scale consists of eight subscales: (1) Bedtime Resistance; (2) Sleep Onset Delay; (3) Sleep Duration; (4) Sleep Anxiety; (5) Night Wakings; (6) parasomnias; (7) Sleep-Disordered Breathing; and (8) Daytime Sleepiness | Owens et al., 2000 |
| FISH | The 22-item scale gathers comprehensive sleep habits information about daytime habits, prebedtime habits, presence of a bedtime routine, sleep environment, and parental behaviors surrounding bedtime | Malow et al., 2009 |
| MSPSQ | Fifty-one items are structured in two parts: Part 1 targets sleep quantity and quality, and Part 2 targets specific sleep disorders. The 36 items scored on a Likert scale pertain to six common sleep problem categories: bedtime resistance/struggles, sleep onset delay, parasomnias, sleep-disordered breathing, sleep anxiety, and daytime sleepiness | Simonds and Parraga, 1982 |
| Sleep diaries | Various diaries are available to record information on a nightly basis. Preferred measurement for more detailed assessment of sleep-wake rhythms. Highly correlated to actigraphy for monitoring sleep schedule | Sadeh, 2008 |
| Sleep Disturbance Scale for Children | 26 Likert-type items were divided into six categories items into six categories: disorders of initiating and maintaining sleep, sleep breathing disorders, disorders of arousal/nightmares, sleep-wake transition disorders, disorders of excessive somnolence, and sleep hyperhidrosis (nighttime sweating) | Bruni et al., 1996 |
Note. CSHQ, Children's Sleep Habits Questionnaire; FISH, family inventory of sleep habits; MSPSQ, Modified Simonds and Parraga Sleep Questionnaire; SDSC, Sleep Disturbance Scale for Children. Additional resources:
Autism Treatment Network 2010
, Autism Treatment Network. (2010). Sleep Toolkit. https://hollandbloorview.ca/sites/default/files/migrate/files/ATNAIRPPhysicianASDSleepToolkitHandout.pdf.
Mindell and Owens, 2015
and Accardo, 2018
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Article Info
Publication History
Published online: October 10, 2022
Publication stage
In Press Corrected ProofFootnotes
Conflicts of interest: None to report.
Identification
Copyright
Copyright © 2022 by the National Association of Pediatric Nurse Practitioners. Published by Elsevier Inc. All rights reserved.
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