Original ArticleSleep, executive functioning and behaviour in children and adolescents with type 1 diabetes
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.
References (70)
- et al.
Depression in Type 1 diabetes in children: natural history and correlates
J Psychosom Res
(2002) The impact of inadequate sleep on children's daytime cognitive function
Semin Pediatr Neurol
(1996)Cognitive, behavioral, and functional consequences of inadequate sleep in children and adolescents
Pediatr Clin North Am
(2011)- et al.
Cognitive and behavioural performance in children with sleep-related obstructive breathing disorders
Sleep Med Rev
(2001) - et al.
Eczema and sleep and its relationship to daytime functioning in children
Sleep Med Rev
(2010) - et al.
Sleep and neurocognitive functioning in children with eczema
Int J Psychophysiol
(2013) The neurocognitive effects of sleep disruption in children and adolescents
Child Adolesc Psychiatr Clin N Am
(2009)- et al.
Alterations in sleep physiology in young children with insulin-dependent diabetes mellitus: relationship to nocturnal hypoglycemia
J Pediatr
(2000) - et al.
Interactions between hypoglycemia and sleep architecture in children with type 1 diabetes mellitus
J Pediatr
(2003) - et al.
Sleep deprivation and neurobehavioral functioning in children
Int J Psychophysiol
(2013)
Sleep disturbance scale for children: translation, cultural adaptation, and validation
Sleep Med
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
Cognitive functioning in children with early onset type 1 diabetes and severe hypoglycemia
J Pediatr
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
Inconsistent sleep schedules and daytime behavioral difficulties in school-aged children
Sleep Med
Sleep loss, learning capacity and academic performance
Sleep Med Rev
Relations between executive function and academic achievement from ages 5 to 17 in a large, representative national sample
Learn Individ Dif
The pathogenesis of insulin-dependent diabetes mellitus
N Engl J Med
Type 1 diabetes: pathogenesis and prevention
CMAJ
Australia's national trends in the incidence of Type 1 diabetes in 0–14-year-olds, 2000–2006
Diabet Med
Neuro-cognitive performance in children with type 1 diabetes–a meta-analysis
J Pediatr Psychol
Cognitive function in children with type 1 diabetes: a meta-analysis
Diabetes Care
The effects of type 1 diabetes on cognitive performance: a meta-analysis
Diabetes Care
Neuropsychological profiles of children with type 1 diabetes 6 years after disease onset
Diabetes Care
Factors associated with academic achievement in children with type 1 diabetes
Diabetes Care
Psychological adjustment in a French cohort of type 1 diabetic children
Diabetes Metab
Psychosocial status of children with diabetes in the first 2 years after diagnosis
Diabetes Care
Hyperglycemia and externalizing behavior in children with type 1 diabetes
Diabetes Care
Psychiatric morbidity and health outcome in Type 1 diabetes – perspectives from a prospective longitudinal study
Diabet Med
Adjustment to diabetes mellitus in preschoolers and their mothers
Diabetes Care
Neurocognitive Correlates of Type 1 Diabetes Mellitus in Childhood
Child Neuropsychol
The association between sleep disordered breathing, academic grades, and cognitive and behavioral functioning among overweight subjects during middle to late childhood
Sleep
Risk of behavioral and adaptive functioning difficulties in youth with previous and current sleep disordered breathing
Sleep
Impact of sleep duration on cognitive functions among preschoolers
Beijing Da Xue Xue Bao
Cognitive benefits of last night's sleep: daily variations in children's sleep behavior are related to working memory fluctuations
J Child Psychol Psychiatry
Cited by (41)
Sleep and type 1 diabetes mellitus management among children, adolescents, and emerging young adults: A systematic review
2021, Journal of Pediatric NursingCitation 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 MedicineCitation 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.