Research in Developmental Disabilities 33 (2012) 1408–1417

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Research in Developmental Disabilities

Sleep disruption as a correlate to cognitive and adaptive behavior problems in autism spectrum disorders Matthew A. Taylor a, Kimberly A. Schreck a,*, James A. Mulick b a b

777 W. Harrisburg Pike, W311 Olmsted Building, Middletown, PA 17036, USA The Ohio State University, Nationwide Children’s Hospital Developmental Assessment Program, 187 West Schrock Road, Westerville, OH 43081, USA

A R T I C L E I N F O

A B S T R A C T

Article history: Received 1 February 2012 Accepted 6 March 2012 Available online 21 April 2012

Sleep problems associated with autism spectrum disorders (ASD) have been well documented, but less is known about the effects of sleep problems on day-time cognitive and adaptive performance in this population. Children diagnosed with autism or pervasive developmental disorder-not otherwise specified (PDD-NOS) (N = 335) from 1 to 10 years of age (M = 5.5 years) were evaluated for the relationships of Behavioral Evaluation of Disorders of Sleep (BEDS; Schreck, 1998) scores to measures of intelligence and adaptive behavior. Results suggested that children who slept fewer hours per night had lower overall intelligence, verbal skills, overall adaptive functioning, daily living skills, socialization skills, and motor development. Children who slept fewer hours at night with waking during the night had more communication problems. Breathing related sleep problems and fewer hours of sleep related most often to problems with perceptual tasks. The results indicate that quality of sleep – especially sleep duration – may be related to problems with day-time cognitive and adaptive functioning in children with autism and PDD-NOS. However, future research must be conducted to further understand these relationships. ß 2012 Elsevier Ltd. All rights reserved.

Keywords: Autism Sleep Adaptive behavior Intelligence Sleep disorders

1. Introduction In 1964, 17-year-old Robert Gardner broke the world record for sleep deprivation by staying awake for 264 h without the aid of stimulants (Ross, 1965). This lack of sleep greatly impaired Mr. Gardner’s ability to function. Gardner began to have trouble focusing his eyes by the second day of wakefulness. On day three, he experienced mood changes, nausea, and difficulty saying tongue twisters. In addition to his irritability, on the fourth day, Gardner experienced cognitive problems including difficulty concentrating and lapses in memory. Hallucinations and delusions followed, including mistaking a street sign for a person and believing that he was a famous football player being berated by fans. Throughout the rest of his marathon period of wakefulness, Gardner continued to experience these symptoms in addition to fragmented thinking, slurred speech, and blurred vision. Similarly, sleep disruption has been shown to impair typically developing (TD) children’s and adolescents’ day-time functioning. Schreck (2010) reviewed the diagnostic relationships of sleep problems to day-time behavior for children and adolescents finding significant relationships. Research has supported Schreck’s (2010) review, indicating that young children who sleep fewer hours per night continually experience more difficulty with perceptual tasks and cognitive ability measures

* Corresponding author at: Penn State Harrisburg, 777 West Harrisburg Pike, W311 Olmsted Building, Middletown, PA 17057-4898, USA. Tel.: +1 717 948 6048. E-mail addresses: [email protected] (M.A. Taylor), [email protected] (K.A. Schreck), [email protected] (J.A. Mulick). 0891-4222/$ – see front matter ß 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.ridd.2012.03.013

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than children who sleep more (Gruber et al., 2010). The impact of sleep deprivation on children’s intellectual functioning also has been shown to impair their academic performance (Fredriksen, Rhodes, Reddy & Way, 2004; Wolfson & Carskadon, 1998). In addition to lack of sleep in general, specific sleep problems have been shown to have negative effects on cognitive functioning and academic performance in TD children and adolescents. For example, TD children diagnosed with or at risk for sleep-disordered breathing have exhibited more difficulty (a) defining vocabulary words (Suratt et al., 2007); (b) sustaining attention (Blunden, Lushington, Kennedy, Martin, & Dawson, 2000; Owens, Spirito, Marcotte, McGuinn, & Berkelhammer, 2000; Suratt et al., 2007), (c) planning and problem solving (Karpinski, Scullin, & Montgomery-Downs, 2008), (d) inhibiting behavior (Karpinski et al., 2008), (e) performing in school (Montgomery-Downs, Jones, Molfese, & Gozal, 2003; Urschitz et al., 2003), and (f) remembering (Blunden et al., 2000). Like children with sleep disordered breathing, individuals with other sleep problems (e.g., insomnia) also have experienced difficulties with concentration and memory (Fernandez-Mendoza et al., 2009). O’Brien (2009) has asserted that sleep problems (e.g., poor sleep hygiene, sleep restriction, circadian rhythm problems, sleep-disordered breathing, restless legs syndrome, narcolepsy, and insomnia) also have consistently impaired children’s attention. With the exception of restless leg syndrome, these sleep problems have also been associated with poor school performance (O’Brien, 2009). The understanding of the impacts of sleep problems on day-time functioning becomes more vital for children with developmental disabilities (DD), because they tend to have more sleep problems than TD children (Cotton & Richdale, 2006; Goodlin-Jones, Tang, Liu, & Anders, 2009; Richdale, Francis, Gavidia-Payne, & Cotton, 2000). The increased amount of sleep problems for this population in combination with the deficits associated with DD (e.g., cognitive deficits) may result in an even more significant impact of sleep problems on day-time behavior. For example, Wiggs and Stores (1996) have reported that children with DD who have experienced more bed-time settling problems, night waking, and early morning waking have displayed a greater intensity and number of disruptive day-time behaviors than those without sleep disturbances. Like children with DD in general, children with Autism Spectrum Disorders (ASD) have consistently been diagnosed with sleep problems (Couturier et al., 2005; Honomichl, Goodlin-Jones, Burnham, Gaylor, & Anders, 2002; Malow, Marzec, et al., 2006; Polimeni, Richdale, & Francis, 2005; Richdale & Prior, 1995; Souders et al., 2009). In fact, research has suggested that those with ASD have more sleep problems than TD children and those with other DDs (Allik, Larsson, & Smedje, 2006b; Giannotti et al., 2008; Krakowiak, Goodlin-Jones, Hertz-Picciotto, Croen, & Hansen, 2008; Miano et al., 2007; Paavonen et al., 2008; Schreck & Mulick, 2000; Souders et al., 2009; Tani et al., 2003). When compared with TD children, these problems have resulted in inefficient sleep, such as night waking or lack of sleep (Allik, Larsson, & Smedje, 2008; Bruni et al., 2007; Couturier et al., 2005; Elia et al., 2000; Giannotti et al., 2008; Goldman et al., 2009, 2011; Krakowiak et al., 2008; Limoges, Mottron, Bolduc, Berthiaume, & Godbout, 2005; Miano et al., 2007; Øyane & Bjorvatn, 2005; Paavonen et al., 2008; Patzold, Richdale, & Tonge, 1998; Schreck & Mulick, 2000; Souders et al., 2009; Wiggs & Stores, 2004). One category of sleep problems common in children with ASD, insomnia, presents as difficulty initiating or maintaining sleep (see Richdale & Schreck, 2009). Children who have ASD have been known to engage in escape behavior at bedtime in attempts to avoid having to go to sleep (Allik, Larsson, & Smedje, 2006a; Bruni et al., 2007; Giannotti et al., 2008; Goldman, Richdale, Clemons, & Malow, in press; Goldman et al., 2009; Paavonen et al., 2008). Even when children go to bed when asked, they often experience difficulty falling asleep (Allik et al., 2006a, 2006b; Allik et al., 2008; Bruni et al., 2007; Giannotti et al., 2008; Goldman et al., 2009, in press; Honomichl et al., 2002; Hoshino, Watanabe, Yashima, Kaneko, & Kumashiro, 1984; Limoges et al., 2005; Miano et al., 2007; Paavonen et al., 2008; Patzold et al., 1998; Richdale, 2001; Richdale & Prior, 1995; Segawa, 1985, as cited in Segawa, Katoh, Katoh, & Nomura, 1992; Souders et al., 2009; Takase, Taira, & Sasaki, 1998; Tani et al., 2003; Wiggs & Stores, 2004; Williams, Sears, & Allard, 2004). Remaining asleep also poses a challenge for this population, as most research has suggested that children with ASD often wake up during the night or early in the morning (Allik et al., 2006a, 2006b, 2008; Bruni et al., 2007; Giannotti et al., 2008; Goldman et al., 2009, in press; Honomichl et al., 2002; Hoshino et al., 1984; Limoges et al., 2005; Miano et al., 2007; Paavonen et al., 2008; Patzold et al., 1998; Richdale, 2001; Richdale & Prior, 1995; Segawa, 1985 as cited in Segawa et al., 1992; Souders et al., 2009; Takase et al., 1998; Tani et al., 2003; Wiggs & Stores, 2004; Williams et al., 2004). In addition to insomnia, children with ASD may experience circadian rhythm sleep disorders (i.e., delays in falling asleep, waking in a confused state, feeling sleepy during the day, and waking early in the morning). As discussed above, individuals with ASD often have difficulty maintaining and initiating sleep, suggesting problems establishing appropriate sleep-wake cycles. Preliminary research has supported this notion (Giannotti et al., 2008; Segawa et al., 1992). Children in this population have experienced other sleep-quality problems. These sleep-quality problems, such as parasomnias (e.g., confusional arousal, bedwetting, sleep walking, sleep terrors, nightmare disorders), sleep movement disorders (e.g., restless leg, teeth grinding, periodic leg movements, and stereotypic movements), and sleep disordered breathing likely have contributed to night-waking in ASD (Schreck, in preparation; Schreck & Mulick, 2000). These night waking episodes have disrupted sleep for children with ASD more so than children who are TD or have other DDs (Couturier et al., 2005; Goldman et al., 2011; Giannotti et al., 2008; Polimeni et al., 2005; Schreck & Mulick, 2000; Souders et al., 2009). These types of sleep problems associated with ASD have received considerably more attention from researchers than clarification of their day-time implications. Therefore, knowledge regarding the influence of sleep problems on cognition and adaptive functioning in this population has remained limited. Preliminary research has suggested that a history of decreased sleep duration or poor sleep quality for children with ASD has correlated with nonverbal intelligence deficits (Elia et al., 2000; Gabriels, Cuccaro, Hill, Ivers, & Goldson, 2005), communication problems (Schreck, Mulick, & Smith, 2004), and academic performance difficulties (Paavonen, Nieminen-von Wendt, Vanhala, Aronen, & von Wendt, 2003). However, not all

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researchers have discovered a significant relationship between sleep problems and IQ in a sample of children with autism (Mayes & Calhoun, 2009). Most of the research discussed above has focused on the influence of sleep problems on cognition and academic performance. However, it is also important to examine the impact of these problems on children’s ability to function pragmatically in their natural environment (i.e., adaptive behavior). In addition, some of the findings discussed (e.g., impaired academic performance and cognitive ability) may have been at least partially attributable to social and communication problems inherent in ASD. For example, scores on intelligence tests may have been lower than individuals’ true abilities due to their behavior during the test or inability to take the test. Thus, understanding of the relationship of adaptive behavior to sleep problems may help to clarify these relationships. To this date, we have been able to locate only one study that has investigated these effects of sleep problems to adaptive behavior in children with ASD (Krakowiak et al., 2008). Results of this study have remained equivocal with sleep and adaptive behavior associated, but not particularly for young children with ASD. Although only the previous study has specifically evaluated adaptive behavior, sleep-problems research has suggested links between sleep problems and adaptive behavior skills. For example, a young girl with ASD and sleep apnea showed great improvement in both sleep and social communication after undergoing a surgical procedure designed to correct disordered breathing during sleep (Malow, McGrew, Harvey, Henderson, & Stone, 2006). Additionally, Schreck et al. (2004) found that specific sleep problems predicted increased expression of autism symptoms that would likely affect adaptive behavior. Specifically, night waking and sensitivity to stimuli in the environment was significantly related to communication problems, while shorter sleep duration predicted social interaction problems. In another study, children classified as poor sleepers had greater social interaction problems than good sleepers (Goldman et al., 2011), suggesting a relationship between sleep disruption and adaptive behavior deficits. Although this research has suggested that sleep problems in autism may be related to these children’s cognitive and adaptive performance, significantly more research with this population must be conducted to understand the effects of these sleep problems. In fact, a recent special interest group meeting at the 2011 International Meeting for Autism Research (IMFAR) concluded that while sleep disturbances remain prevalent and significant in ASD, more research must be conducted to determine the impact of sleep disturbance on cognition and daily functioning in this population (Baker, 2011). The purpose of this study was to provide the initial steps toward meeting the IMFAR special interest group recommendations by delineating the relationships between the sleep behavior in children with ASD and subsequent day-time cognitive and adaptive performance. 2. Method 2.1. Participants Participant data was collected from a database of diagnostic testing for children seen at a pediatric hospital-affiliated disability assessment clinic. Children with a primary diagnosis (by a licensed psychologist) of Autism or PDD-NOS at the clinic were initially identified (N = 455). Participants also had scores in the files for the Behavioral Evaluation of Disorders of Sleep (BEDS; Schreck, 1998; Schreck, Mulick, & Rojahn, 2003). After eliminating participants according to this criterion, the participant numbers reduced to 335. Of the remaining 335 participants, autism was the most common diagnosis (n = 219), followed by PDD-NOS (n = 116). The final sample of children ranged in age from 1 to 18-years-old (M = 5.15 years; SD = 3.27). The majority were male (male: n = 296; female: n = 39), white (n = 240), and cognitively delayed. Full scale IQ scores were obtained for 300 participants and ranged from standard scores of 8 to 128, with a mean of 61.55 (SD = 19.05). Mean verbal IQ score for the sample was 67.09 (n = 106; SD = 18.31; range = 40–106), while the mean performance IQ score was 76.33 (n = 222; SD = 23.08; range = 32–145). General adaptive behavior domain scores (i.e., adaptive behavior composite, socialization, communication, daily living skills, and motor skills) were also collected based on the results of two adaptive behavior measures—the Scales of Independent Behavior-Revised (SIB-R; Bruininks, Woodcock, Weatherman, & Hill, 1997) and the Vineland Adaptive Behavior Scale (VABS; Sparrow, Balla, & Cicchetti, 1984). Scores for the adaptive measures included: (a) adaptive behavior composite (n = 247; M = 57.25; SD = 27.15; range = 0–124); (b) socialization (n = 241; M = 62.78; SD = 25.61; range = 0–113); (c) communication (n = 235; M = 53.99; SD = 26.25; range = 0–113); (d) motor (n = 236; M = 76.22; SD = 28.31; range = 0–143); (e) daily living skills (n = 241; M = 60.77; SD = 23.32; range = 0–124). Formal diagnoses of sleep problems from medical professionals were recorded in official psychological reports for 30 participants. In the psychological reports, the majority of these diagnoses were listed vaguely as ‘‘sleep problems’’ (n = 18), ‘‘dyssomnias’’ (n = 3), and ‘‘rule-out apnea’’ (n = 5). The psychology assessment reports also stated parental report of one or more of their children’s sleep problems (n = 115), including settling and sleep onset problems (n = 53), night waking (n = 46), co-sleeping (n = 19), and snoring or apnea (n = 10). Additional parent-report measures (i.e., BEDS responses) estimated that 18% of parents described their child as having a sleep problem. While 94 participants were reportedly taking medication at the time of evaluation, none were excluded from the present study, as an initial ANOVA (medication status  total BEDS score) indicated that children on medications continued to have more sleep problems than children not on medications [F(1, 275) = 8.52, p < .004].

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2.2. Materials 2.2.1. Intelligence Several different intelligence tests were used due to differences in the age of the children, language, and cognitive ability. However, due to the adequate concurrent validity of the tests (see Sattler, 2001), generalized intelligence scores were recorded from the equivalent domains for the test each individual was administered (e.g., either a WISC-IV; Wechsler, 2003) full scale score or WPPSI full scale score (Wechsler, 2002) was recorded under a generic variable named ‘‘full scale IQ’’). Verbal and performance IQ scores were also recorded. See Table 1 for tests and the domains used for each of the general score designations (i.e., verbal, performance, and full scale IQ). The most commonly administered intelligence tests included the Leiter International Performance Scale-Revised (Leiter-R; Roid & Miller, 1997) (n = 142), Developmental Profile II (DP-II; Alpern, Boll, & Shearer, 2000) (n = 132), Mullen Early Learning Scales (Mullen, 1995) (n = 102), and Stanford-Binet Intelligence Scales, Fifth Edition (Roid, 2003) (n = 60). In cases where multiple tests were administered to a child producing more than one full scale IQ score, the lowest score was used in the analysis because it would provide the most stringent estimate of the child’s functioning. In addition, individuals who were administered only nonverbal measures of intelligence such as the Leiter obtained only nonverbal IQ scores. 2.2.2. Adaptive behavior Two separate measures of adaptive functioning were administered to children in compiling the database for the study, (a) SIB-R (Bruininks et al., 1997) (n = 215) and (b) VABS (Sparrow et al., 1984) (n = 38). One or the other measure was usually administered to children included in this study. General adaptive behavior composite, socialization, communication, daily living skills, and motor skills scores were recorded from the measure of adaptive functioning that each individual had been administered. Equivalent domains for the adaptive behavior scales were determined using Wells, Condillac, Perry, and Factor (2009) (see Table 2 for VABS and SIB-R domains used for each adaptive behavior score as was done with the IQ tests). If individuals were administered both measures, the lowest scores were included in the analysis. 2.2.2.1. Scales of independent behavior-revised. The SIB-R (Bruininks et al., 1997), a measure of functional independence and adaptive functioning in school, home, employment, and community settings, can be used with any age group with or without DD. It assesses areas of adaptive functioning in domains including broad independence, social interaction and communication skills, personal living skills, motor skills, and community living skills. 2.2.2.2. Vineland adaptive behavior scales. The VABS (Sparrow et al., 1984) assesses adaptive behavior in children and adolescents from birth to 18-years-old along with low-functioning adults. In addition to an adaptive behavior composite score, the test yields scores in four behavior domains including communication, daily living skills, socialization, and motor skills. Normative data was gathered using a sample of 3000 participants aged from birth through 18 years, 11 months.

Table 1 Intelligence tests and domains used for general intelligence scores. Test a

BSID-III DP-IIb DP-IIIc DASd K-ABCe Leiter-Rf Mulleng Stanford-Binet-Vh S-BITi WASIj WISC-IIIk WISC-IVl WPPSI-IIIm a

Age range

FSIQ

VIQ

PIQ

Birth–42 months Birth–9.5 years Birth–12 years 2.6–17.11 years 2.6–12.6 years 2–21 years Birth–68 months 2–89 years 6–20 years 6–89 years 6–16.11 years 6–16.11 years 2.6–7.3 years

Cognitive Scale Cognitive Cognitive General Conceptual Ability Mental Processing Composite N/A Early Learning Composite Full Scale IQ N/A Full Scale IQ Full Scale IQ Full Scale IQ Full Scale IQ

Language Scale Language Communication Verbal N/A N/A Expressive Language Verbal IQ N/A Verbal IQ Verbal IQ Verbal Comprehension Index Verbal IQ

N/A N/A N/A Nonverbal Nonverbal Leiter Full Scale N/A Performance IQ Nonverbal IQ Performance IQ Performance IQ Performance IQ Performance IQ

BSID-II = Bayley Scales of Infant Development-Third Edition (Bayley, 2005). DP-II = Developmental Profile II (Alpern et al., 2000). c DP-III = Developmental Profile III (Alpern, 2007). d DAS = Differential Ability Scales (Elliott, 1990). e K-ABC = Kaufman Assessment Battery for Children (Kaufman & Kaufman, 1983). f Leiter-R = Leiter International Performance Scale-Revised (Roid & Miller, 1997). g Mullen = Mullen Scales of Early Learning (Mullen, 1995). h Stanford-Binet-V = Stanford-Binet Intelligence Scales, Fifth Edition (Roid, 2003). i S-BIT = Stoelting Brief Nonverbal Intelligence Test (Roid & Miller, 1999). j WASI = Wechsler Abbreviated Scale of Intelligence (Wechsler, 1999). k WISC-III = Wechsler Intelligence Scale for Children-Third Edition (Wechsler, 1991). l WISC-IV = Wechsler Intelligence Scale for Children-Fourth Edition (Wechsler, 2003). m WPPSI-III = Wechsler Preschool and Primary Scale of Intelligence-Third Edition (Wechsler, 2002). b

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Table 2 Adaptive behavior tests and domains used for corresponding general adaptive behavior scores. Test a

VABS SIB-Rb a b

Age range

Adaptive behavior composite

Socialization

Communication

Daily living skills

Motor skills

Birth–18 Infancy–80+

Adaptive behavior composite Broad independence

Socialization Community living skills

Communication Social interaction and communication skills

Daily living skills Personal living skills

Motor skills Motor skills

VABS = Vineland Adaptive Behavior Scales (Sparrow et al., 1984). SIB-R = Scales of Independent Behavior-Revised (Bruininks et al., 1997).

2.2.3. Sleep 2.2.3.1. Behavioral evaluation of disorders of sleep. The BEDS (Schreck, 1998; Schreck et al., 2003), a parent-report questionnaire based on the International Classification of Sleep Disorders (AASM: American Academy of Sleep Medicine, 1991), was developed for use with children (5–12 years). The BEDS consists of 107 items on a five-point Likert scale (0 = never; 1 = almost never; 2 = sometimes; 3 = almost always; 4 = always) measuring aspects of sleep quality. In addition to questions regarding specific sleep behaviors, four additional questions addressed general aspects of children’s sleep, including hours slept per night, hours slept in the last 24 h, hours napped during the day, and whether or not the parent perceives their child as having a sleep problem. Parents’ answers on the BEDS reflect their child’s sleep behavior over the last 6 months. Exploratory factor analyses on the original sample (N = 307) and confirmatory factor analyses of the 107 Likert scale items resulted in four factors based on 22 of the items. The four scales of the BEDS include Expressive Sleep Disturbances (9 items measuring behaviors, such as screaming during the night), Sensitivity to the environment (7 items measuring behaviors such as night-time fears and environmental discomfort), Disoriented Awakenings (4 items measuring behavior such as slow reaction times when waking), and Apnea (2 items measuring breathing difficulty during sleep). The four factors and BEDS total score have adequate internal consistency, and the test distinguishes between children with sleeping problems and those without (Schreck, Mulick, & Rojahn, 2005). See Schreck et al. (2003) for more information on the development of the BEDS. 2.3. Procedures Before collecting data, the Internal Review Board at Pennsylvania State University reviewed and approved the study. In constructing the database, we accessed patient files from 1999 to 2008 from a pediatric hospital-affiliated assessment clinic. The second author and graduate fellows at the pediatric hospital-affiliated assessment clinic constructed the database by recording de-identified demographic information (e.g., date of birth, gender, race, medications, past medical history, etc.), test scores on standardized diagnostic tests (e.g., adaptive behavior, intelligence, etc.), measures of sleep problems (BEDS), and diagnostic decisions (e.g., diagnoses of autism spectrum disorders, diagnoses of sleep disorders). 2.4. Data analysis All analyses were computed using the Statistical Package for Social Sciences (SPSS, 2008). Before analyzing the relationship between sleep and cognitive ability and adaptive functioning, Pearson correlation analyses were conducted to determine if the BEDS items measuring amount of sleep (i.e., hours slept per night, hours slept in last 24 h, and hours spent napping during the day), the BEDS Factors (i.e., Expressive Sleep Disturbances, Sensitivity to the Environment, Disoriented Awakenings, and Apnea), and the BEDS Total score were related to participants’ adaptive behavior (adaptive behavior composite, socialization, communication, motor skills, and daily living skills) or IQ domains (full scale, verbal, and performance). These analyses indicated that BEDS items were related to both IQ and adaptive behavior (see Tables 3 and 4 for the bivariate relationships among the variables). Because the BEDS items scores were significantly associated with IQ and adaptive behavior scores, we analyzed BEDS items to determine which BEDS factors and items predicted cognitive and adaptive functioning. Stepwise multiple linear regression analyses were conducted to determine if BEDS factor scores, BEDS total score, and the three additional BEDS items (hours of sleep per night, hours slept in the last 24 h, and hours napped per day) predicted intelligence scores (i.e., full scale IQ, verbal IQ, and performance IQ) and adaptive behavior scores (i.e., adaptive behavior composite, social skills, communication skills, daily living skills, and motor skills). These analyses were conducted separately for each of the intelligence scores and adaptive behavior scores.

3. Results 3.1. Intelligence Stepwise multiple regression analyses indicated that children’s IQ scores across all IQ domains (i.e., verbal, performance, and full scale) were related to their sleep quantity and sleep quality. We analyzed the predictive ability of BEDS factors (i.e.,

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Table 3 Bivariate correlations for BEDS factors and IQ scores. IQ

Factors

BEDS

Full scale Full scalea Verbalb Perfc Hours/nightd Hours/24e Hours napsf Parent reptg BEDS totalh ESDi Sens envj Dis awakek Apneal

a

Verbal .93** –

–

b

Perf

c

.74** .76** –

Hours/nightd

Hours/24e

Hours napsf

Parent reptg

BEDS totalh

.33** .38** .26** –

.27** .29** .23** .58** –

.12 .22* .17* .14* .38** –

.07 .07 .09 .23** .20** .08 –

.14* .06 .11 .38** .31** .05 .33** –

ESDi .06 .05 .02 .19 .18** .03 .23** .59** –

Sens envj

Dis awakek

Apneal

.03 .15 .04 .16** .09 .01 .26** .58** .30** .31**

.11 .20 .18** .06 .09 .04 .08 .16** .08 .08 .12* –

.02 .02 .07 .37** .25** .11 .26** .71** .42** – –

a

Full scale = full scale IQ. Verbal = verbal IQ. c Perf = performance IQ. d Hours/night = hours slept per night. e Hours/24 = hours slept in the last 24 h. f Hours naps = hours napped per day. g Parent rept = parent perception of whether their child has a sleep problem. h BEDS Total = BEDS Total Score. i ESD = BEDS Expressive Sleep Disturbances. j Sens env = BEDS Sensitivity to Environment. k Dis awake = BEDS Disoriented Awakening. l Apnea = BEDS Sleep Apnea. * p < .05. ** p < .01. b

Table 4 Bivariate correlations for BEDS factors and Adaptive Behavior Scores. Factors

Adaptive behavior a

ABCa Socb Comc DLSd Motore Hours/nightf Hours/24g Hours napsh Parent repti BEDS Totalj ESDk Sens envl Dis awakem Apnean a

b

ABC

Soc

–

.90** –

Com

BEDS c

.85** .76** –

DLS

d

.85** .70** .70** –

Motor .82** .69** .52** .71** –

e

Hours/nightf

Hours/24g

.36** .36** .28** .30** .33** –

.30** .32** .21** .21** .23** .58** –

ABC = adaptive behavior composite. Soc = socialization. Com = communication. d DLS = daily living skills. e Motor = motor skills. f Hours/night = hours slept per night. g Hours/24 = hours slept in the last 24 h. h Hours naps = hours napped during day. i Parent rept = parent perception of whether their child has a sleep problem. j BEDS Total = BEDS Total Score. k ESD = BEDS Expressive Sleep Disturbances. l Sens env = BEDS Sensitivity to Environment. m Dis awake = BEDS Disoriented Awakening. n Apnea = BEDS Sleep Apnea. * p < .05. ** p < .01. b c

Hours napsh

Parent repti

.25** .26** .16* .13 .26** .14* .38**

.05 .02 .07 .08 .06 .23** .20** .08

– –

BEDS totj

ESDk

Sens envl

Dis awakem

Apnea

.21** .17* .16* .17* .14* .38** .31** .05 .33** –

.16* .12 .22** .15* .10 .19 .18** .03 .23** .59** –

.20** .11 .02 .15* .21** .37** .25** .11 .26** .71** .42** –

.18** .11 .07 .16* .24** .16** .09 .01 .26** .58** .30** .31** –

.12 .11 .03 .06 .11 .06 .09 .04 .08 .16** .08 .08 .12* –

n

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Expressive Sleep Disturbances, Sensitivity to the Environment, Disoriented Awakenings, and Apnea), BEDS total, and number of hours slept (i.e., hours slept per night, hours slept in the last 24 h, hours napped per day) for full scale IQ, verbal IQ, and performance IQ scores. Analyses of the relationships between sleep variables and IQ revealed that children who slept more hours per night had higher full scale and verbal IQ scores (full scale IQ: R2 = .11; p < .01; verbal IQ: R2 = .15; p < .01). Additionally, hours slept per night in combination with reports of apnea (BEDS Sleep Apnea factor) predicted performance IQ scores (R2 = .10; p < .01). Fewer hours slept per night coupled with a higher frequency of parent-reported symptoms of apnea was strongly associated with decreased ability to perform nonverbal tasks. 3.2. Adaptive behavior Stepwise multiple regression analyses were also conducted to determine which BEDS factors (i.e., Expressive Sleep Disturbances, Sensitivity to the Environment, Disoriented Awakenings, and Apnea), BEDS total score, and questions addressing number of hours slept (i.e., hours slept per night, hours slept in the last 24 h, hours napped per day) predicted specific adaptive behavior domain scores. Parental report of more hours slept per night singularly predicted better daily living skills (R2 = .09; p < .01). The combination of more total hours slept per night and hours napped during the day significantly predicted better Adaptive Behavior Composite (R2 = .18; p < .01); motor skills scores (R2 = .16; p < .01), and socialization scores (R2 = .17; p < .01). More hours slept per night in combination with fewer episodes of night waking with screaming (BEDS Expressive Sleep Disturbance score) and more sensitivity to sleeping environment disturbances (BEDS Sensitivity to the Environment scores) significantly predicted children’s higher communication scores (R2 = .14; p < .01). In other words, children who slept more on average per night without waking showed better developed communication skills. See Table 5 for stepwise multiple regression. Table 5 Stepwise multiple regression predicting IQ & adaptive behavior. Scale scores Intelligence Scale Scores Full scale F R2 Predictors Verbal F R2 Predictors Performance F R2 Predictors General Adaptive Behavior Adaptive behavior composite F R2 Predictors Socialization F R2 Predictors Communication F R2 Predictors

Daily living skills F R2 Predictors Motor skills F R2 Predictors *

p < .05. ** p < .01.

Predictors

28.78** .11 (1) Hours slept per night 14.29** .15 (1) Hours slept per night 8.54** .10 (1) Hours slept per night (2) Sleep Apnea

19.57 .18 (1) Hours slept per night (2) Hours napped 17.57 .17 (1) Hours slept per night (2) Hours napped 9.31 .14 (1) Hours slept per night (2) Expressive Sleep Disturbances (3) Sensitivity to Environment 16.34 .09 (1) Hours slept per night 16.65 .16 (1) Hours slept per night (2) Hours napped

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4. Discussion By reporting these relationships among specific cognitive skills, adaptive behavior, and sleep factors for children with ASD, this study took the first step toward meeting the recommendations made by the IMFAR special interest group on sleep. In this study, children with ASD who slept fewer hours on average per night were more likely to perform worse overall with respect to intelligence and verbal skills than children who slept longer. This result corroborated Gruber et al.’s (2010) observations, but was in direct contrast to previous research indicating no relationship or an inverse relationship between sleep quantity and IQ (Mayes & Calhoun, 2009). We also determined that sleep disruption impaired more than just overall cognitive ability. Perceptual and verbal skills also declined with disrupted sleep. For example, children with ASD who slept for fewer hours and suffered from parentreported nighttime breathing problems showed less ability to complete nonverbal tasks (e.g., puzzles, mazes, block building, etc.). Similar relationships among apnea and cognitive ability (i.e., memory, attention, vocabulary, and executive functioning) have been established for TD children (Blunden et al., 2000; Karpinski et al., 2008; Owens et al., 2000; Suratt et al., 2007). For children with ASD, only relationships existed between apnea treatment and improvement in social communication skills and increases in autism symptoms (Malow, McGrew, et al., 2006; Schreck et al., 2004). This study may be the first to indicate a possible relationship between apnea and perceptual tasks for children with ASD. The difficulties with cognitive skills (i.e., perceptual and verbal ability) may also generalize to adaptive behavior problems. Although the one other study evaluating adaptive behavior for young children with ASD did not report a significant relationship between adaptive behavior and sleep disruption (Krakowiak et al., 2008), our results suggested that a relationship may exist between sleep duration, sleep problems, and adaptive behavior deficits. Specifically, we found that children who slept less on average per night displayed more deficits in skills needed to complete typical daily living tasks (e.g., hygiene, eating, toileting, etc.). To our knowledge, this is the first study to examine the relationship of sleep disturbance to the ability to complete daily living activities. The children’s difficulties with completing daily living activities, such as pouring water, brushing hair, may be due to motor difficulties, as those children who slept less on average both at night and during the day had more difficulty with all adaptive behavior tasks, especially motor and social skills. Finally, children who slept more on average per night without waking and were less bothered by environmental stimuli within their sleeping environment (e.g., noises, lights, uncomfortable beds, etc.) showed better ability to effectively communicate with others during the day. This result remains consistent with Schreck et al. (2004), who reported that children who awoke more at night and were more sensitive to the night time environmental stimuli showed more communication patterns during the day typically found with children with an ASD (e.g., echolalia). This study’s attempt to delineate specific cognitive skills and adaptive behavior influenced by sleep deprivation and disruption contradicted Krakowiak et al.’s (2008) general evaluation of adaptive behavior for young children with autism. Our inclusion of specific cognitive and adaptive domains provides a significant stepping stone for future research. Future research should attempt to correct limitations in this study, such as not verifying parent report of sleep problems and varying assessment materials. Future researchers also must elaborate on these findings. Specific diagnostic sleep disorders must be evaluated in conjunction with these types of specific cognitive and adaptive skills. Further analysis of specific motoric, social, communicative, and daily living skill deficits could be related to verified sleep disorders. Performance on tasks that appear to be impaired by sleep disruption before and after successful treatment of the sleep disorder will provide the best test of a causal relation between sleep disruption and the impaired performances suggested by this study. As these relationships develop among sleep disorders and cognitive ability and adaptive behavior, clinicians and medical practitioners must be educated on the importance of identifying and treating sleep within the ASD population. With treatment of sleep problems, children’s day-time functioning improves (Johnson, Giannotti, & Cortesi, 2009; Malow, McGrew, et al., 2006; Minde, Faucon, & Falkner, 1994; Rooney, Alfano, Walsh, & Parr, 2011). If professionals do not identify sleep problems as a possible contributor to day-time deficits, treatments for skill development and implementation may be incomplete and insufficient. Acknowledgements The authors wish to express appreciation for their hospitality to the staff and postdoctoral fellows at The Nationwide Children’s Hospital. Without access to their data, cooperation, and inclusion of sleep assessment in psychological evaluations, this study would not have been possible. The authors would also like to thank Eric Butter for his assistance with locating research assistants to enter data. Finally, thank you to Lindsay Knapp and Preeti Kumar for their assistance in preparation and editing of the manuscript. References Allik, H., Larsson, J.-O., & Smedje, H. (2006a). 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