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Sleep and cognitive functioning in children with disabilities.

A substantial proportion of children who have learning problems also have sleep problems. Recent discoveries about how sleep insufficiency in children is related to their attention, learning, memory, and academic achievement have substantial implications for special education. Empirical evidence has been accumulating for years alongside emerging theory. Yet with few exceptions, sleep has probably not been a topic that researchers and practitioners in special education have considered related to their professional practice. Evidence summarized in this article documents that sufficient sleep is centrally related to the optimal academic achievement of children who have difficulty learning. Incorporating sleep into our screening, diagnostic, educational, and prevention practices for children with disabilities may yield substantial benefits.

ASSESSMENT OF CHILDREN'S SLEEP

Sleep is a multidimensional phenomenon, and multiple types of measures have been used to assess its various aspects. For example, duration of typical nightly sleep is of interest, as is duration and timing of daytime naps. Other measures address the quality of sleep, and some concern the presence and degree of daytime sleepiness. At the most subjective level, parents and sometimes children respond to questionnaires that include questions about the timing, regularity, length, and quality of sleep. Most questionnaires also have questions designed to screen for sleep disorders, and many include questions about sleepiness and other aspects of daytime functioning that are affected by sleep.

Frequently used measures include the Children's Sleep Habits Questionnaire (Owens, Spirito, & McGuinn, 2000), the Pediatric Sleep Questionnaire (Chervin, Hedger, Dillon, & Pituch, 2000), and the School Sleep Habits Survey (Wolfson & Carskadon, 1998). Two measures that assess only sleepiness in children are the Children's Report of Sleep Patterns--Sleepiness Scale (CRSP-S; Meltzer et al., 2012) and the Pediatric Daytime Sleepiness Scale (PDSS; Drake, Nickel, Burdevali, Roth, & Catherine, 2003). The CRSPS is a five-item scale that asks children how likely they are to fall asleep while (a) at school, (b) riding in a bus or car for a short time (less than 20 minutes), (c) playing, (d) eating, or (e) talking with someone else. It was shown to have good reliability and validity in a sample of 388 children ages 8 to 12. The PDSS is a 13-item scale that was developed for children at the middle school level and that demonstrated good reliability and validity in a sample of 450 children. Brief screening instruments such as BEARS (Owens & Dalzell, 2005) are appropriate for early identification and referral for further assessment. BEARS uses an interview format to inquire about bedtime problems (B), excessive daytime sleepiness (E), awakenings at night (A), regularity and length of sleep (R), and snoring (S).

Although the measures mentioned thus far have reasonably good reliability and validity and much research has been done with them, none of them has been standardized with a large representative sample. The Sleep Disorders Inventory for Students, which has separate versions for children and adolescents (Luginbuehl, 2003), and the Sleep Disturbance Scale for Children (Bruni et al., 1996) are the only currently available instruments that have been normed with substantial samples and that have met all of the psychometric criteria specified in a recent comprehensive review (Spruyt & Gozal, 2011). Assessment of sleep via questionnaires is strengthened by having parents and children keep sleep diaries and logs. Similar to questionnaires, these methods are considered subjective, but cross-checking questionnaire responses with logs allows for better confidence in measures such as typical bedtime and sleep duration.

Individual items pertaining to sleep appear on some multipurpose questionnaires. The Child Behavior Checklist (CBCL; Achenbach, 1991), which is very well known to educators, has six items that relate to sleep: overtired; sleeps less than most kids; sleeps more than most kids during day and/or night; trouble sleeping; nightmares; and talks in sleep. A recent study with 122 children, roughly half of whom had an anxiety or depressive disorder, compared children's parent-reported CBCL sleep item scores with a sleep diary, actigraphy, and two nights of polysomnography (described later in the article), and discovered that only one of the six items, trouble sleeping, correlated significantly with one objective measure, sleep latency as measured by diary (partial correlation = .25; p = .008) and actigraphy (partial correlation = .21; p = .029). None of the many measures attained through polysomnography were related to CBCL items (Gregory et al., 2011). The authors concluded that using only the items on the CBCL is not sufficient for a thorough assessment of children's sleep.

Objective measurement of sleep is accomplished in several ways. Polysomnography is universally regarded as the gold standard for assessment of sleep quality and is the only method that determines the presence and durations of sleep stages (e.g., rapid eye movement, slow wave). Polysomnography requires spending the night in a sleep center, typically located at a hospital. In addition to measuring sleep stages, it can provide data for diagnosis of many clinical sleep disorders such as sleep apnea, which is characterized by low oxygen saturation levels and frequent brief awakenings (Iber, Ancoli-Israel, Chesson, & Quan, 2007; see Mindell & Owens, 2010, pp. 38-41 for a concise overview of polysomnography).

Another objective method in common use is actigraphy. Actigraphy has the advantage of easy use in children's homes and involves wearing a small device the size of a wristwatch that records movement between the time of going to bed and getting up. It is a reliable and valid method of determining sleep onset latency, the time between going to bed and falling asleep, the time between falling asleep and waking, night awakenings, and restlessness (Sadeh & Acebo, 2002). As in the case of questionnaires, diaries and logs most often accompany actigraphy for cross-validation.

Sleepiness is assessed objectively via the Multiple Sleep Latency Test, which is performed in a sleep center often on the morning and afternoon following overnight polysomnography. It consists of a series of scheduled naps, and the time taken to fall asleep (latency) is the measure of sleepiness, with shorter latencies indicative of greater sleepiness. A related assessment is the Maintenance of Wakefulness Test, which involves a series of trials during which a person tries to remain awake for specified periods of time (Littner et al., 2005).

Important to emphasize is that there is no single definitive measure of most aspects of sleep. Determination of sleep problems by subjective measures has generally related significantly, but at a low level, with objective measures. Sadeh (2008) has made the compelling argument that different kinds of measures provide different information, and all of them are useful. As with any construct, using multiple measures strengthens confidence in construct validity.

SLEEP RESEARCH WITH CHILDREN

Research on children's sleep can be organized into four categories: infancy and early childhood, clinical sleep disorders, typically developing children, and children with disorders. A summary of research in each of those categories follows.

INFANCY AND EARLY CHILDHOOD

There is a substantial amount of research on sleep problems manifesting in infancy and early childhood. Problems such as bedtime resistance, unwillingness to sleep apart from parents, night awakenings, and nightmares are common. Many such sleep problems receive the attention of primary care pediatricians, and there are numerous books available for parents and professionals (e.g., Mindell, 2005; Owens & Mindell, 2005). It is quite common for infants and toddlers to have some problems with sleep. Estimates based on parental reports are that between 25% and 30% of toddlers have problems with bedtime resistance and night wakings, and persistent problems are usually treated successfully by establishment of consistent sleep schedules and bedtime routines (Mindell & Owens, 2010).

CLINICAL SLEEP DISORDERS

Sleep disorders including obstructive sleep apnea, insomnia, and restless legs syndrome, diagnosed via polysomnography, have been studied in children for many years. Numerous other sleep disorders occur in children, including delayed sleep phase disorder, enuresis, narcolepsy, idiopathic hypersomnia, and Kleine-Levin syndrome. Excellent summaries of these disorders and how to diagnose and treat them have long been available in the medical literature (e.g., Mindell & Owens, 2010; Sheldon, Ferber, & Kryger, 2005), and recent years have seen a few publications directed to nonmedical audiences, such as school psychologists (Buckhalt & El-Sheikh, 2010; Buckhalt, Wolfson, & El-Sheikh, 2009, 2010; Donaldson & Owens, 2006). Sleep disorders are classified in two diagnostic systems, the International Classification of Sleep Disorders (American Academy of Sleep Medicine, 2005), and the Diagnostic and Statistical Manual of Mental Disorders (4th ed., text rev.; DSM-IV-TR; American Psychiatric Association, 2000). In this article, a distinction is made between sleep disorders and sleep problems that are problematic but do not rise to the level of a clinical disorder.

Although sleep disorders are becoming better understood, less known and of relevance to educators is that sleep disorders have been associated with problems in cognitive, emotional, and health domains, and these problems are related to academic performance and behavior. Over 50 studies since 2000 have demonstrated that cognitive and academic performance is impaired in children with sleep disorders, and numerous reviews have been published (Beebe, 2006; Blunden & Beebe, 2006; Blunden, Lushington, Lorenzen, Martin, & Kennedy, 2005). Importantly, it has been demonstrated that when children with obstructive sleep apnea have their tonsils and adenoids surgically removed, not only is their sleep improved, but their performance on cognitive tests also is higher (Montgomery-Downs, Crabtree, & Gozal, 2005).

TYPICALLY DEVELOPING CHILDREN

A direction that has been taken recently in children's sleep research is the study of the relation of sleep to cognitive performance in school-age children who are typically developing and have no known sleep or other disorders. In these studies, sleep is typically assessed with self--and parent report questionnaires, sleep diaries, and actigraphy.

From their review of 15 studies that examined relations between sleep and measures of attention, learning, and memory, Kopasz et al. (2010) concluded that
 most studies support the hypothesis that sleep facilitates working
 memory as well as memory consolidation in children and adolescents.
 There is evidence that performance in abstract and complex tasks
 involving higher brain functions declines more strongly after sleep
 deprivation than performance in simple memory tasks. (p. 167)


Dewald, Meijer, Oort, Kerkhof, & Boegels (2010) reviewed 26 studies of relations between children's sleep duration, sleep quality, and daytime sleepiness and measures of school performance, concluding that
 All three sleep variables were significantly but modestly related
 to school performance. Sleepiness showed the strongest relation to
 school performance, followed by sleep quality and sleep duration.
 Effect sizes were larger for studies including younger participants
 which can be explained by dramatic prefrontal cortex changes. (p.
 179)


Although the majority of these studies have been correlational, stronger evidence for a causal relationship is provided by a few experimental studies that showed cognitive impairment following a mild reduction (1 hr) of sleep (e.g., Sadeh, Gruber, & Raviv, 2003).

A very large body of research with adults has documented the impact of sleep deprivation (experimentally induced) on cognitive functioning (Durmer & Dinges, 2005; Lim & Dinges, 2010), and there is no reason to believe that children and adolescents are not similarly affected. Important to note is that relations discovered in the studies reviewed by Kopasz et al. (2010) and Dewald et al. (2010) have involved relations of cognitive performance not to severe sleep deprivation, but to normal variations in children's sleep.

CHILDREN WITH DISORDERS

Studies of sleep have been done with children who have a wide range of various diagnosed disorders and conditions. Mindell and Owens (2010) summarized these and divided their discussion into three categories: neurodevelopmental disorders, medical disorders, and psychiatric disorders. The number of disorders is large, and only a few examples from each category will be described here. In studies of children with these disorders, sleep has been assessed with a wide range of both objective and subjective methods.

Among neurodevelopmental disorders that have been found to have associated sleep problems are autism spectrum disorder (ASD), Down syndrome, and Rett syndrome. For Down syndrome, the estimated prevalence of obstructive sleep apnea is between 30% and 80%. Representative of the many studies is De Miguel-Diez, Villa-Asensi, and Alvarez-Sala (2003), who reported that 54.6% of 108 children with Down syndrome met the clinical criteria for obstructive sleep apnea, and subjective sleep complaints occurred in 70% of the children. For Rett Syndrome, sleep apnea is less commonly seen than in Down syndrome, but children and parents often report trouble falling and staying asleep, frequent night wakings, and daytime problems associated with short sleep duration (Roane & Piazza, 2001). Mindell and Owens (2010) pointed out that sleep problems are especially prevalent in children with neurodevelopmental disorders who have craniofacial abnormalities, hypotonia, and obesity. These conditions are often associated with impaired breathing, and adequate respiration is necessary for good sleep.

In the category of medical disorders, Children with asthma are particularly prone to sleep problems due to insufficient respiration during sleep. For example, Fagnano et al. (2009) reported that 33% of 194 children enrolled in a school-based asthma intervention program had sleep disordered breathing assessed with a questionnaire. As would be expected, any illnesses associated with acute or chronic pain are typically accompanied by sleep problems. Among the many of these are juvenile rheumatoid arthritis (Bloom et al., 2002), migraine (Miller, Palermo, Powers, Scher, & Hershey, 2003), and cancer (Rosen & Brand, 2011). Tietze et al. (2012) provided a review of 61 studies of children who have sleep disturbances and a wide variety of medical disabilities.

The last category of Mindell and Owens (2010), psychiatric disorders, includes depression, anxiety disorders, and attention deficit hyperactivity disorder (ADHD). That sleep is associated with depression and anxiety comes as no surprise because sleep problems are among symptoms used to define each in DSM-IV-TR (American Psychiatric Association, 2000). Chorney, Detweiler, Morris, and Kuhn (2008) reviewed studies of children and adolescents, concluded that there is much symptom overlap in diagnosis of sleep, anxiety, and depressive disorders, and offered recommendations for future research and current clinical practice. Further, it seems clear that bi-directional effects are likely present, with depression and anxiety leading to sleep problems, and the emotional dysregulation associated with insufficient sleep leading to anxiety or depression. Gregory and Sadeh (2012) reviewed studies of sleep problems in children and adolescents with a wide range of emotional and behavioral difficulties, including not only anxiety and depression, but also aggression, conduct disorders, and addiction.

SLEEP AND COGNITIVE FUNCTIONING IN CHILDREN WITH INTELLECTUAL DISABILITY, ADHD, AND ASD

The most research on relations between sleep and cognitive functioning in children with disabilities has been done with children whose primary impairments are intellectual disability (ID), ADHD, or ASD. Some reviews of sleep research with persons having these disabilities have been published. Doran, Harvey, and Homer (2006) provided a review that covers sleep in persons spanning a broad range of age and severity of developmental disability. Studies of infants, children, and adults are reviewed, and although for many studies the subtype of developmental disability is indicated (e.g., profound mental retardation, severe intellectual disability), in many other instances the general phrase "people with developmental disabilities" is used. Autism spectrum disorder is not a focus of the review, although two studies of sleep and ASD are mentioned briefly. Further, the studies reviewed cover a wide range of outcomes associated with sleep and disability, including mood, problematic behavior, motor control, attention, executive control, and learning.

A recent review of sleep in persons with pervasive developmental disorders (PDD), including ASD and PDD-not otherwise specified, was done by Holloway and Aman (2011b). Similar to Doran et al. (2006), the review covers a wide range of outcomes related to sleep, including internalizing behavior, affective symptoms, problem (externalizing) behavior, repetitive behavior, ADHD (only in children with PDD), adaptive behavior, receptive language, and intelligence.

Several reviews of sleep in persons with ADHD have also appeared, including those by Cortese, Konofal, Yareman, Mouren, and Lecendreux (2006), who found eight studies of children with ASD using objective sleep measures, and a subsequent meta-analysis of sixteen studies using both subjective and objective measures of children with ADHD (Cortese, Farone, Konofal, & Lecendreux, 2009). In that review, they concluded that children with ADHD had high levels of sleep problems measured by both parental report and objective measures (actigraphy and Multiple Sleep Latency Test). Longer sleep latency and lower quality sleep were found for children with ADHD compared to control children. Konofal, Lecendreux, and Cortese (2010) have provided another summary of this body of research and proposed clinical guidelines for treatment.

Although the literature relating sleep to these conditions is growing, gaps in knowledge remain. The present article will differ from those described previously in that the primary focus is relations of sleep only to cognitive functioning (learning, memory, and academic performance) and only in school-age children. Also, research on conditions that affect sleep and may co-occur with disability in children will be reviewed. Further needed research will be discussed along with implications for how research can inform special education practice. Databases searched for this article included PsycINFO, PsycARTICLES, PubMed, Medline, and Google Scholar with the search terms sleep, sleep disorder, sleep problems, intellectual disability, mental retardation, autism, autism spectrum disorder, ADHD, attention deficit hyperactivity disorder, attention, cognitive, learning, memory, and academic achievement in various combinations.

INTELLECTUAL DISABILITY

High rates of sleep problems have been reported in individuals with ID. Studies date back as far as the mid-1980s (Bartlett, Rooney, & Spedding, 1985), and although estimates are not precise because they are most often based on parent report, experts have estimated that up to 80% of children with ID have some kind of sleep problem at some time during childhood (Johnson, 1996). Numerous studies have shown that parents report these children to have difficulties with sleep onset and maintenance that exceed those of typically developing children (e.g., Stores, Stores, & Buckley, 1996), and these problems have been associated with greater stress in parents and increased frequencies of behavior problems in the children (Didden, Korzilius, van Aperlo, van Overloop, & de Vries, 2002; Richdale, Francis, Gavidia-Payne, & Cotton, 2000). Parents of children whose disabilities are more severe tend to report more severe sleep problems (Didden et al., 2002). Using parent reports of children ages 3 to 18, Robinson and Richdale (2004) reported that sleep problems lasted between 6 and 9 years with up to 76% of parents seeking treatment for their children. Many parents, however, needed more help in recognizing sleep problems and understanding available treatments. Pediatricians and child psychiatrists often prescribe medications to help children sleep, and reviews of the effectiveness of a wide range of medications (Holloway & Aman, 201 la; Turk, 2010) suggest that some have satisfactory results.

Somewhat surprising is that no study could be located that related individual differences within groups of children with ID to how sleep relates to various outcomes. In other words, it is clear from many studies over many years that ID is associated with sleep problems, but it would be helpful to know if within groups with the same disability, individual differences in sleep are related to differential cognitive functioning and performance.

Mechanisms responsible for these sleep problems are not completely understood, but some have speculated that comorbid conditions such as epilepsy in more severely affected children may be involved. Epilepsy is common in persons with severe ID (McGrother et al., 2006), and seizures have been related to nighttime awakenings, sleep fragmentation, and abnormal sleep stages (Kotagal & Yardi, 2008; Matos, Andersen, do Valle, & Tufik, 2010). Another mechanism that has been put forth as underlying sleep problems in children with ID is insufficient endogenous production of the hormone melatonin, which is produced in the pineal gland and regulated by an endogenous pacemaker in the superchiasmatic nucleus of the hypothalamus (Sajith & Clarke, 2007). Clinical trials of the effects of exogenous melatonin on sleep have shown that it helps in falling asleep and sleeping longer (Brzezinski, Vangel, & Wurtman, 2005), and results for children with ID are particularly strong. Braam et al. (2009) conducted a meta-analysis and concluded that with melatonin treatment, sleep onset latency was decreased by a mean of 34 min, and total sleep time was increased by an average of 50 min. Fewer numbers of wake-ups during the night were also reported. Although these studies showed that sleep could be improved, they did not include measures of cognitive outcomes. Still lacking is evidence that improving sleep will improve academic performance of children with intellectual disability.

ATTENTION DEFICIT HYPERACTIVITY DISORDER

Sleep problems are commonly reported by parents of children with ADHD (Cortese et al., 2009; Mayes et al., 2009). Even in children with ADHD who do not take stimulant medications, around 30% are reported by parents to have insomnia (O'Brien & Gozal, 2004). Further, because one of the primary cognitive effects of experimental sleep deprivation in adults is impaired sustained attention (Lim & Dinges, 2010), it is likely that some proportion of children diagnosed with ADHD actually have an undiagnosed sleep disorder. It is also likely that bidirectional effects are present, with sleep problems caused by mechanisms underlying ADHD and vice versa.

Problems in reaching definitive conclusions about these relations are due to inconsistent methods of identifying ADHD and the presence of comorbid conditions, including depression, anxiety, and behavior disorders (Yoon, Jain, & Shapiro, 2012). Cortese et al. (2006) identified 46 studies of sleep in children with ADHD, but only eight studies met rigorous methodological conditions and used objective sleep measures (i.e., polysomnography). In the eight studies, children with ADHD took longer to fall asleep, had more movement during sleep, and had more apnea-hypopnea episodes. Some other sleep parameters, however, showed no differences from controls. Using subjective parent reports on a normed sleep survey, Mayes et al. (2009) studied a large sample of children with ADHD separated into ADHD-Inattentive (ADHD-I) and ADHD-Combined (ADHD-C) groups with and without comorbid oppositional defiant disorder (ODD), anxiety, or depression. These children were compared with a control group with no known disorders matched for race, gender, and risk for sleep-disordered breathing. Differences in sleep were discovered as a function of ADHD type, comorbidity, and use of medication. Children with ADHD-I alone had fewest sleep problems and were not different from Controls. Those with ADHD-C, however, had more problems than Controls and children with ADHD-I. Comorbid anxiety or depression increased sleep problems, but ODD did not. Daytime sleepiness was higher in children with ADHD-I. Last, children taking medications for their disorder had greater difficulty falling asleep.

Experimental studies of sleep with children are rare, but one recent publication provides strong evidence for the deleterious effect of reduced sleep on cognitive functioning of children with ADHD. Gruber et al. (2011) investigated the effect of one hour of sleep restriction over six consecutive nights on performance of the Conners Continuous Performance Test (CPT), a measure often used in ADHD diagnosis. Sleep was objectively measured using actigraphy, while parents completed nightly sleep logs and reported on children's daytime sleepiness. Restricting sleep led to poorer CPT scores in both healthy controls and children with ADHD. On a majority of CPT measures, performance of children with ADHD deteriorated from subclinical to clinical ranges (T > 60). More studies such as this are needed to determine if improving sleep in children with ADHD results in greater attention, learning, memory, and academic achievement.

As is the case with ID, mechanisms underlying these relations are not yet clear. In research with typically developing children and adults, it is believed that sufficient amounts of slow wave and rapid eye movement (REM) sleep are necessary both for optimal attention and encoding of information and for consolidation of memory. Memory is believed to be enhanced via connectivity between the prefrontal cortex and the hippocampus during sleep, and in the case of insufficient sleep, memory for recently learned material is diminished (Wang & Morris, 2010).

Treatment for sleep onset insomnia in children with behavior management and various medications has been successful in helping those children to sleep better (Cohen & Ancoli-Israel, 2004), and in the only study of long-term efficacy with melatonin treatment, effects remained after over 3 years. Not only was sleep improved, but improvement of mood and behavior was reported by parents in around two thirds of the cases (Hoebert, van der Heijden, van Geijlswijk, & Smits, 2009). Although parent satisfaction with improvements in sleep is laudable, research using direct measurement of sleep, mood, and behavior is needed. In a well-controlled experimental study, Prehn-Kristensen et al. (2011) compared performance on a procedural memory task in 16 children with ADHD and 16 control children both before and after a night of sleep. Children with ADHD, but not controls, showed improvement after sleep, and gains in skills were associated with greater time spent in slow wave sleep and REM density. More research of this type is needed to confirm that improving sleep will result in better cognitive performance in these children.

AUTISM SPECTRUM DISORDER

Much recent research has been devoted to understanding the causes of ASD, partly because of the steep rise in prevalence in recent years. Sleep is among the many difficulties studied in these children. Numerous recent reviews of this literature indicate that from 40% to 80% of these children have at least one sleep problem according to parent report, including reduced sleep duration, difficulties with going to sleep, and problems staying asleep at night (e.g., Cortesi, Giannotti, Ivanenko, & Johnson, 2010; Cotton & Richdale, 2010; Holloway & Aman, 2011b; Mayes & Calhoun, 2009; Richdale & Schreck, 2009). In the few studies that have used polysomnography and actigraphy to study sleep in persons with ASD, those objective measures have differentiated poor versus good sleepers on the basis of sleep latency and sleep quality (Goldman et al., 2009; Malow, Marzec, McGrew, Wang, & Stone, 2006).

Parents of children with ASD who experience sleep difficulties have typically sought the help of pediatricians, and they have recommended various remedies to alleviate the problems, including behavioral management, nutritional supplements and dietary changes, and medications (Lemmons, 2010). Behavioral intervention studies have been few, but Moon, Corkum, and Smith (2011) developed and implemented a manualized multicomponent sleep intervention for three children with ASD who also had primary insomnia and delayed sleep onset. Parents were taught behavioral interventions of fading, response cost, and positive reinforcement, and they were contacted weekly by telephone for guidance and support. Children's sleep was assessed with questionnaires, sleep diaries, and actigraphy. For all three children, mean latency of sleep onset was reduced, and the improvements were maintained at a 12-week follow-up. Similarly, Weiskop, Richdale, and Matthews (2005) reported success with behavior therapy in reducing sleep problems of six preschool children with ASD.

Glickman (2010) has proposed that disturbed sleep-wake patterns and abnormal hormonal profiles suggest an underlying impairment of the circadian timing system in children with ASD. Similar to the research described previously with ID, abnormal melatonin production is suspected to be related to poor sleep in children with ASD (Tordjman, Anderson, Pichard, Charby, & Touitou, 2005). As is the case for ID and ADHD, melatonin treatment has been found to be effective. Doyen et al. (2011) reviewed 17 studies of melatonin treatment and offered clinical treatment guidelines. Last, adenotonsillectomy has been reported to improve sleep in a case study of a 5-year-old child with ASD. The improvements in sleep were accompanied by improvements in social communication, attention, and reduced frequency of repetitive behaviors (Malow, McGrew, Harvey, Henderson, & Stone, 2006).

OTHER CONDITIONS THAT MAY BE PRESENT WITH DISABILITY AND EXACERBATE RISK

Numerous other conditions may exacerbate the risk of lowered cognitive functioning and academic achievement of children with disabilities through relations with sleep. Many children have asthma (Akinbami, Moorman, & Liu, 2010), and children with asthma have been shown to have high rates of sleep disorders because nighttime breathing is impaired. A good oxygen supply is necessary for optimal sleep, and in children with asthma, sleep problems have been linked to poor cognitive functioning (Desager, Nelen, Weyler, & De Backer, 2004). Accordingly, any child with a disability (such as those reviewed here) who also has asthma may be at increased risk for sleep problems and associated cognitive outcomes.

Another risk factor for sleep problems in children is obesity. Many more children than in the past have become overweight and obese (Jelalian, Wember, Bungeroth, & Birmhaer, 2007), and these children are prone to sleep problems because of airway obstruction (Amin & Daniels, 2002) due to fatty tissue around the trachea and also because leptin and ghrelin, hormones that affect appetite, are dysregulated with poor sleep (Weiss et al., 2010). Children with disabilities who are obese and overweight may be at increased jeopardy for sleep problems, and those who also have asthma or other respiratory problems are at even greater risk.

Low socioeconomic status (SES) is yet another risk factor for sleep problems because children from lower SES families have been found to sleep less well than their counterparts from higher SES families (Pagel, Forister, & Kwiatkowki, 2007). Moreover, the effects of poor sleep are exacerbated such that the relations between poor sleep and poor cognitive performance are stronger in children from lower SES families (Buckhalt, El-Sheikh, & Keller, 2007; Buckhalt, El-Sheikh, Keller, & Kelly, 2009). These findings have led to a hypothesis that some portion of the achievement gap related to social class may be explained by differences in sleep that are related to cognitive functioning (Buckhalt, 2011; Buckhalt & Staton, 2011).

Mechanisms through which differential effects by SES effects operate are not yet completely understood, but aspects of both the physical and psychosocial environment may be involved. In the physical domain, smaller homes, poor heating and ventilation, less noise insulation between rooms, and exposure to secondhand smoke have been considered. Greater degrees of family chaos (e.g., Evans, Gonella, Marcynyszyn, Gentile, & Salpekar, 2005), poor parental enforcement of bedtimes and caffeine intake, and greater degrees of stress due to multiple factors including interparental conflict (El-Sheikh, Buckhalt, Mize, & Acebo, 2006) have also all been suggested as possible mechanisms.

Poorer sleep and higher prevalence of sleep disorders have been reported for African American and Hispanic children and adults (independent of SES) in many studies (Boss, Smith, & Ishman, 2011; Ruiter, DeCoster, Jacobs, & Lichstein, 2010). Although confounding of ethnicity and social class may account for some of these disparities, other reasons are not yet well understood. What is clear is that any child with a disability who has one or more of these additional risk factors is especially likely to experience poor sleep.

IMPLICATIONS FOR SPECIAL EDUCATION

All children's cognitive functioning is affected by sleep disorders or by periodic or chronic mild levels of sleep deprivation. Children with disabilities for whom learning is challenging to begin with are made more vulnerable to problems in academic achievement when they sleep poorly. To some degree, the academic difficulties these children have may be related to sleep in addition to limitations that are caused by other aspects of their disabilities. What can special educators do to mitigate the problems caused by poor sleep?

Children with disabilities should be screened for sleep disorders, and there are numerous screening tools available that are easy to use. The BEARS instrument (Owens & Dalzell, 2005) was originally developed for pediatric residents and can easily and efficiently be used by teachers. It uses an interview rather than a paper and pencil questionnaire format and there are only a few questions in five categories. The parent or child is asked about bedtime problems ("Does your child have any problems at bedtime?"), excessive daytime sleepiness ("Does your child have difficulty waking in the mornings, seem sleepy during the day, or take naps?"), awakenings during the night ("Does your child wake up a lot at night? Any sleepwalking or nightmares?"), duration and regularity of sleep ("What time does your child go to bed and get up on school days? Weekends?"), and snoring ("Does your child snore?"). For children who are positively screened, teachers may ask parents to complete one of the more comprehensive sleep questionnaires. Those children suspected to have a sleep disorder should be referred for further diagnosis by a pediatric sleep specialist. Sleep treatment centers are available in every U.S. state and Canadian province, and can be located by consulting the web site of the American Academy of Sleep Medicine (http://www.aasmnet.org/) or the National Sleep Foundation (http://www.sleepfoundation.org/). Diagnoses typically require an overnight stay in a sleep center for polysomnography, a procedure that measures electroencephalogram, electrocardiogram, electromyogram, oxygen saturation, and the length of time spent in all of the four stages of sleep. Treatments may include behavioral management, melatonin or other medications, adenotonsillectomy, and various appliances for obstructive sleep apnea.

Although some children will be found to have sleep disorders, many more will have sleep problems that fall short of a clinical diagnosis. A child does not have to have a serious disorder for insufficient sleep to affect school performance. Teachers can consult with parents about ways to improve the sleep of their children. Parents can help children by setting earlier bedtimes that are consistent from night to night and by limiting or eliminating caffeinated beverages, especially during the afternoon and evening. Limiting use of televisions, computers, and any other devices with screens late in the day is facilitative of better sleep not only because they increase arousal, but because exposure to screens may delay the onset of melatonin production. Because allergies can impair airflow during sleep, reducing exposure to allergens may be helpful. Adequate and clean beds and bedding are necessary for good sleep, and when possible, bed-sharing with others and with pets should be avoided. More extensive information about ways to improve children's sleep may be found in books intended for parents (e.g., Mindell, 2005; Owens & Mindell, 2005), books intended for sleep practitioners (e.g., Mindell & Owens, 2010; Sheldon et al., 2005), and in publications directed to professionals who work with children in schools (e.g., Buckhalt & El-Sheikh, 2010; Buckhalt, Wolfson, & El-Sheikh, 2009).

Children's sleep occurs at home and it is often difficult for educators to influence what parents and children do there. Besides screening, identification of at-risk children, and consultation with parents, there are some other actions educators can take. Information about sleep can be infused into the health education curriculum, and although no programs have yet targeted children with disabilities, some prevention and intervention programs with children have been successful (Cain, Gradisar, & Moseley, 2011; Moseley & Gradisar, 2009; Schlarb, Velten-Schurian, Poets, & Hautzinger, 2011; see review by Blunden, Chapman, & Rigney, 2012). Because children with sleep problems are almost certain to be sleepy at school, the timing of classroom tests and individual-and group-administered testing should be considered. Although assessment textbooks and test manuals advise modifications or delays in testing for children who are ill and for many other situations such as fatigue, none mentions that sleepy children are not likely to perform at optimal or even typical levels (Holthaus, 2009). Later school start times have been initiated by a growing number of school districts, with possible benefits for all children (Wolfson, Spaulding, Dandrow, & Baroni, 2007) but especially for the large number of children with disabilities who may experience sleep problems and sleepiness at school.

Just as we learned decades ago that hungry children do not learn well, it stands to reason that sleepy children are not optimally responsive to educational intervention, no matter how qualified the teacher and no matter how much empirical support exists for the teaching method or curriculum. Screening for sleep disorders and sleep insufficiency should perhaps become as routine as screening for vision and hearing problems before developing diagnosis and remediation plans.

REFERENCES

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JOSEPH A. BUCKHALT

Auburn University

Address correspondence concerning this article to Joseph A. Buckhalt, Department of Special Education, Rehabilitation, and Counseling, Auburn University, Haley Center 2084, Auburn, AL 36849-5222 (e-mail: buckhja@auburn.edu).

This research was supported by grants awarded to Mona El-Sheikh by the National Science Foundation (0339115 and 0623936) and the National Institutes of Health (R01 HL0932936). The content is solely the responsibility of the author and does not necessarily represent the official views of the National Science Foundation or the National Institutes of Health.

Manuscript submitted March 2011; accepted May 2012.

JOSEPH A. BUC:KHALT, Professor, Department of Special Education, Rehabilitation, and Counseling, Auburn University, Alabama.
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