Elsevier

Sleep Medicine

Volume 15, Issue 12, December 2014, Pages 1490-1499
Sleep Medicine

Original Article
Sleep, executive functioning and behaviour in children and adolescents with type 1 diabetes

https://doi.org/10.1016/j.sleep.2014.08.011Get rights and content

Highlights

  • We assessed behaviour, sleep, and executive functioning using parental report in children with type 1 diabetes (T1D) versus healthy controls.

  • Children with T1D had more problems with sleep initiation, sleep maintenance, and daytime sleepiness.

  • Children with T1D had mild deficits in behaviour and executive functioning.

  • Sleep quality was found to mediate deficits in behaviour and executive functioning.

  • The impact of T1D on sleep can mostly explain the neurocognitive and behavioural deficits in children with T1D.

Abstract

Objective

The aim of the study was to examine sleep, neurocognitive and behavioural functioning in children and adolescents with type 1 diabetes (T1D) compared to controls and to test whether sleep quality mediates the relationship between diabetes and neurocognitive and behavioural deficits.

Methods

Participants include 49 children and adolescents with T1D (recruited from a hospital clinic) and 36 healthy controls (age range = 6–16 years). Parents completed a survey consisting of the Sleep Disturbances Scale for Children, the Behavior Rating Inventory of Executive Functions, and the Behavior Assessment System for Children-2. Diabetic and demographic parameters were collated from medical records. The survey was posted to participants.

Results

Children with T1D compared to controls reported a higher frequency of sleep problems, and mild deficits in executive and behavioural functioning. Mediational analyses revealed that sleep quality fully mediated metacognitive functioning, externalised problematic behaviour, and internalised problematic behaviour, but not behavioural regulation.

Conclusions

Rather than the direct impact of T1D on daytime functioning, it is the consequent impact of T1D on sleep and the resulting sleep disruption which can explain much of the neurocognitive and behavioural deficits reported in children with T1D. Maintaining good nocturnal glycaemic control may play a much larger role than previously thought in regulating daytime functioning in children with T1D.

Introduction

Type 1 diabetes (T1D) is an autoimmune disorder characterised by the progressive loss of pancreatic islet β-cells resulting in a loss of insulin production [1], [2]. T1D is one of the most common chronic diseases of childhood years. In Australian children the incidence rate has increased to 21 per 100,000 person years [3]. Children with T1D are reported to have reduced neurocognitive performance (eg, executive functioning, sustained attention, psychomotor speed, learning and memory – and as a consequence – reduced intellectual and academic performance [4], [5], [6], [7], [8]) and a higher frequency of problematic behaviours (eg, depression, somatisation and social withdrawal [9], [10], [11], [12], [13], [14]). The neurocognitive and behavioural deficits in children with T1D have been attributed to poor glycaemic control [12], [15]. It is unclear, however, as to what degree sleep disruption modulates these effects. In otherwise healthy children without impaired glycaemic control, sleep disruption is associated with reduced cognitive performance and increased problematic behaviour [16], [17], [18], [19], [20], [21], [22]. Our group and others have also shown that sleep quality mediates daytime behaviour and neurocognitive functioning in children with a range of medical conditions, for example, upper airway obstruction and eczema [18], [23], [24], [25], [26], [27]. Taken together, these findings raise the possibility that sleep disruption may also contribute to the daytime deficits reported in children with T1D.

The literature reporting sleep data in children with T1D is limited. In a review of the literature using ‘children’, ‘sleep’, ‘type 1 diabetes’ and other variants as search keywords using Google Scholar, PubMed and PsychLit databases, we identified 12 studies that report objective sleep data. These include four polysomnographic [28], [29], [30], [31], seven questionnaire (including interview) [32], [33], [34], [35], [36], and one combined questionnaire, polysomnographic, and actigraphic study [37] (see Table 1). To date, sleep questionnaire data have been collected in 480, polysomnographic data in 114, and actigraphic data in 40 children with T1D. In general, the questionnaire findings indicate that children with T1D have more disturbed but longer sleep [32], [34], [39], however this has not been observed in all studies, Happe et al. [33] reports one group having no sleep differences compared to non-diabetic siblings/relatives [33] and the second compared to independent controls. Consistent with the questionnaire data all the polysomnographic studies reported that children with T1D report a greater number of nocturnal arousals compared to controls [28], [29], [31], [37]. Polysomnographic findings also indicate a higher frequency of central apnoea and a trend toward lighter sleep (more N2 and less N3 stage sleep) [31], [37]. The frequency of restless legs syndrome on self-report has also been examined with Happe et al. noting that it was similar to that of controls [33]. In summary, the findings in children with TID indicate that sleep problems are more frequent (eg, more nocturnal restlessness, longer periods of nocturnal wakefulness, longer and more frequent episodes of central apnoea, an increased prevalence of sleep disordered breathing and, paradoxically, a longer time spent sleeping), and are especially evident in children with poor glycaemic control [29], [31], [32], [37], [40].

To date, Perfect and colleagues are the only group that have examined the relationship between sleep and daytime functioning in children with T1D [35], [37]. Perfect's group report that poor sleep habits were associated with an increased frequency of behavioural problems, reduced quality of life, higher diabetes-related worry, higher depression, and greater daytime sleepiness. They also report an association between sleep disruption and lower academic grades.

Perfect's findings raise the question as to the mechanism underlying the association between sleep disruption and impaired daytime function. A possible explanation may be the impact of sleep disruption on executive functioning. Sleep disruption is associated with impaired executive functioning in otherwise healthy children [41], [42] and this effect is potentially amplified by the added impaired glucose control in children with T1D. In addition to general daytime performance, of note is that optimum executive functioning is an important factor in a child's ability to also effectively plan and manage diabetes.

Therefore, the aims of the present study were to investigate sleep and daytime functioning in children with T1D compared to non-diabetic controls and to test whether sleep significantly contributes to the relationship between diabetes and daytime functioning. Based on the findings outlined above, it is hypothesised that both nocturnal hypoglycaemic and hyperglycaemia will result in sleep disruption, thereby impairing executive function and daytime behaviour in children with T1D.

Section snippets

Participants and procedure

Children and adolescents with T1D aged between 6 and 16 years were consecutively recruited over 4 months from the patient list of children attending the paediatric diabetes clinic of the Women's and Children's Hospital which is the tertiary referral centre for children in the state of South Australia and services a population base of 1.1 million. This was a sample of convenience and included approximately 20% of the diabetic clinic population. The minimum age was set at 6 years to enable

Demographics

Compared to controls, children with T1D had comparable age and gender distributions but significantly lower levels of maternal education and SES (Table 2). Given the significant group difference in SES, the latter was entered as an additional independent variable in the analyses investigating the effect of diabetic status on SDSC, BRIEF and BASC-2 scores. Participants were dichotomised according to the mean SES into Low and High SES groupings.

Sleep disturbance scale for children

Children with T1D compared to controls had

Discussion

In this study, children with T1D compared to controls had reduced executive functioning, a higher frequency of problematic behaviours and a higher frequency of sleep problems. The novelty of the current study is that it examined whether sleep itself mediated the relationship between TID, executive functioning, and daytime behaviour and found that it did. These findings highlight the importance of the clinical assessment of sleep problems in children during routine diabetic clinic visits.

Funding source

No external funding was secured for this study.

Financial disclosure

No financial relationships relevant to this article to disclose.

Conflict of interest

The ICMJE Uniform Disclosure Form for Potential Conflicts of Interest associated with this article can be viewed by clicking on the following link: http://dx.doi.org/10.1016/j.sleep.2014.08.011.

. ICMJE Form for Disclosure of Potential Conflicts of Interest form.

References (70)

  • FerreiraV.R. et al.

    Sleep disturbance scale for children: translation, cultural adaptation, and validation

    Sleep Med

    (2009)
  • DowdyE. et al.

    A factor analytic investigation of the BASC-2 behavioral and emotional screening system parent form: psychometric properties, practical implications, and future directions

    J Sch Psychol

    (2011)
  • StrudwickS.K. et al.

    Cognitive functioning in children with early onset type 1 diabetes and severe hypoglycemia

    J Pediatr

    (2005)
  • BlundenS.L. et al.

    The contribution of intermittent hypoxia, sleep debt and sleep disruption to daytime performance deficits in children: consideration of respiratory and non-respiratory sleep disorders

    Sleep Med Rev

    (2006)
  • BiggsS.N. et al.

    Inconsistent sleep schedules and daytime behavioral difficulties in school-aged children

    Sleep Med

    (2011)
  • CurcioG. et al.

    Sleep loss, learning capacity and academic performance

    Sleep Med Rev

    (2006)
  • BestJ.R. et al.

    Relations between executive function and academic achievement from ages 5 to 17 in a large, representative national sample

    Learn Individ Dif

    (2011)
  • AtkinsonM.A. et al.

    The pathogenesis of insulin-dependent diabetes mellitus

    N Engl J Med

    (1994)
  • GillespieK.M.

    Type 1 diabetes: pathogenesis and prevention

    CMAJ

    (2006)
  • CatanzaritiL. et al.

    Australia's national trends in the incidence of Type 1 diabetes in 0–14-year-olds, 2000–2006

    Diabet Med

    (2009)
  • NaguibJ.M. et al.

    Neuro-cognitive performance in children with type 1 diabetes–a meta-analysis

    J Pediatr Psychol

    (2009)
  • GaudieriP.A. et al.

    Cognitive function in children with type 1 diabetes: a meta-analysis

    Diabetes Care

    (2008)
  • BrandsA.M. et al.

    The effects of type 1 diabetes on cognitive performance: a meta-analysis

    Diabetes Care

    (2005)
  • NorthamE.A. et al.

    Neuropsychological profiles of children with type 1 diabetes 6 years after disease onset

    Diabetes Care

    (2001)
  • McCarthyA.M. et al.

    Factors associated with academic achievement in children with type 1 diabetes

    Diabetes Care

    (2003)
  • CastroD. et al.

    Psychological adjustment in a French cohort of type 1 diabetic children

    Diabetes Metab

    (2000)
  • GreyM. et al.

    Psychosocial status of children with diabetes in the first 2 years after diagnosis

    Diabetes Care

    (1995)
  • McDonnellC.M. et al.

    Hyperglycemia and externalizing behavior in children with type 1 diabetes

    Diabetes Care

    (2007)
  • NorthamE.A. et al.

    Psychiatric morbidity and health outcome in Type 1 diabetes – perspectives from a prospective longitudinal study

    Diabet Med

    (2005)
  • WysockiT. et al.

    Adjustment to diabetes mellitus in preschoolers and their mothers

    Diabetes Care

    (1989)
  • DesrocherM. et al.

    Neurocognitive Correlates of Type 1 Diabetes Mellitus in Childhood

    Child Neuropsychol

    (2004)
  • BeebeD.W. et al.

    The association between sleep disordered breathing, academic grades, and cognitive and behavioral functioning among overweight subjects during middle to late childhood

    Sleep

    (2010)
  • PerfectM.M. et al.

    Risk of behavioral and adaptive functioning difficulties in youth with previous and current sleep disordered breathing

    Sleep

    (2013)
  • ZhouW.J. et al.

    Impact of sleep duration on cognitive functions among preschoolers

    Beijing Da Xue Xue Bao

    (2013)
  • KonenT. et al.

    Cognitive benefits of last night's sleep: daily variations in children's sleep behavior are related to working memory fluctuations

    J Child Psychol Psychiatry

    (2014)
  • Cited by (41)

    • Sleep and type 1 diabetes mellitus management among children, adolescents, and emerging young adults: A systematic review

      2021, Journal of Pediatric Nursing
      Citation Excerpt :

      While the Pittsburgh Sleep Quality Index (PSQI) clinical cutoff for poor sleep quality is above 5, adolescents and emerging young adults with T1DM had average PSQI scores between 4 and 5.37 (Adler et al., 2017; Patel et al., 2018; Turner et al., 2016). Of five studies using subjective sleep measures (Adler et al., 2017; Caruso et al., 2014; Estrada et al., 2012; Happe et al., 2005; Sivertsen et al., 2014), only one study reported differences in sleep quality and sleep disturbances between individuals with and without T1DM (Caruso et al., 2014). Specifically, those between 6 and 16 years old with T1DM were associated with increased problems in initiating and maintaining sleep, sleep-wake transition, and excessive daytime somnolence compared to healthy controls (Caruso et al., 2014).

    • Sleep disorders and executive function in children and adolescents with chronic kidney disease

      2019, Sleep Medicine
      Citation Excerpt :

      Children having SRBD assessed by polysomnography had increased rates of impaired BRI performance [44]. In children with type 1 diabetes mellitus the impact of disease on sleep and the resulting sleep disruption has been associated with neurocognitive and behavioral deficits [45]. In the present study, using parent-reported BRIEF scores, we demonstrated that children with CKD compared to controls had lower performance in nearly all the scales of executive function except working memory.

    View all citing articles on Scopus
    View full text