Sleep and neuropsychological development among infants and toddlers Wanqi Sun (wanqi@hku.hk) Department of Developmental and Behavioral Pediatrics, Shanghai Children’s Medical Center, 1678 Dong Fang Rd., 200127 Shanghai, China Department of Psychology, The University of Hong Kong, Pokfulam, HK Chia-huei Tseng (CH_Tseng@alumni.uci.edu) Department of Psychology, The University of Hong Kong, Pokfulam, HK Fan Jiang (fanjiang@shsmu.edu.cn) Karen Spruyt (spruytsleep@gmail.com) Yanrui Jiang (yanrui1027@126.com) Xiaojuan Xu (xxj_1109@163.com) Qi Zhu (zhuqi@scmc.com.cn) Department of Developmental and Behavioral Pediatrics, Shanghai Children’s Medical Center, 1678 Dong Fang Rd., 200127 Shanghai, China Ching-fan Sheu (csheu@mail.ncku.edu.tw) Institue of Education, National Cheng Kung University, Taiwan Abstract long been considered to be the product of central nervous Sleep quantity and quality have been verified to influence system (CNS) maturation (Bruni et al., 2010; Kohyama, cognitive function in adult and children, while little is known 1998). about such relation among young children. This study aims to In addition, early well-being is critical for later global explore the concurrent association between sleep and health. For instant, a longitudinal study shows that cognitive neuropsychological development in infants and toddlers. 1102 abilities such as attention, processing speed and memory children aged 2-30 months old from 16 hospitals in 8 during infancy and toddlerhood, are predictive for children’s provinces of China were involved in the survey. Main executive functions including working memory, inhibition caregivers were asked to fill out the Brief Infant Sleep Questionnaire (BISQ) and the Bayley Scales of Infant and shifting at 11 years old (Rose, Feldman, & Jankowski, Development I (BSID-I) was conducted to evaluate children’s 2012). neuropsychological development. Results showed that in Despite of the abundant evidences in children, only average infants slept 12.40 (12.30-12.51) hours over 24 hours, sporadic studies have explored the role of sleep in infants’ woke up 1.77 (1.69-1.84) times per night and woke 0.50 cognitive development with most of them coming from (0.45-0.54) hour through the night. Prolonged night waking laboratory settings with small sample sizes and narrow age duration was negatively associated with the Mental ranges (e.g., Ednick, Cohen, & McPhail, 2009), or clinical Development Index (MDI) only among toddlers aged 1-2.5 years old (β=-0.10, p=0.045). No association between sleep samples (e.g., snoring) (Piteo, Kennedy, et al., 2011; Piteo, and psychomotor development was found. This study Lushington, et al., 2011). Therefore, we conducted a large- underscores the high prevalent fragmental sleep in Chinese scale cross-sectional study aiming to disclose the relation infants and toddlers that indicates for concurrent slow between sleep and cognitive development among infants cognitive development. and toddlers. Keywords: infants; sleep; night waking; cognition development Methods Introduction From October 2012 to March 2013 in collaboration with The important role of sleep on cognitive function has been one downtown hospital and one suburban hospital in each of widely acknowledged in elderly population and healthy the eight provinces in mainland China (i.e., Inner Mongolia, adults (Pilcher & Huffcutt, 1996; Van Dongen, Maislin, Hunan, Hebei, Guangxi, Yunnan, Shandong, Zhejiang and Mullington, & Dinges, 2003; Yaffe, Falvey, & Hoang, Jiangsu), we recruited children who came in the clinic for 2014). Furthermore, a recent meta analysis has confirmed regular health examination. Shanghai Children’s Medical the positive relation between sleep duration and cognitive Centre Human Ethics Committee granted ethical approval performance among 5 to 12 years old children (Astill, Van for this study (SCMCIRB-2012047), and written informed der Heijden, Van Ijzendoorn, & Van Someren, 2012). consent was obtained from caregiver of each participant. Comparing with preschoolers and adults, infants and toddlers spend much more time on sleep when their brains Participants develop rapidly during the first few years (Peirano & In all, 1102 children within the age range of 2-30 month-old Algarín, 2007). On the other hand, the sleep-wake state has born over 37 weeks of gestational age were enrolled. 511 Children were excluded if they were twins or triplets, had any congenital diseases or adverse birth outcomes. Night waking duration Night waking frequency 3.0 1.2 Measures 1.0 2.5 Night waking duration Night waking frequency 2.0 Sleep assessment Parents or primary caregivers completed 0.8 (times/night) (hours) 1.5 the Chinese version of Brief Infant Sleep Questionnaire 0.6 (BISQ)(A Sadeh, 2004; AVI Sadeh & MINDELL, 2009) 0.4 1.0 adopted from the cross-culture study of Mindell et al. (2010) 0.2 0.5 The respondents were asked to describe their child’s sleep 0.0 0.0 2- 3- 4- 5- 6- 9- 12- 15- 18- 21- 24-30 during the last two weeks. Age (months) Cognition assessment General cognitive functioning was Figure 1: Night waking of children at different age assessed with the Bayley Scales of Infant Development periods. (BSID-I), the standardized diagnostic test of cognitive development delay for children aged 2-30 months in mainland China. Based on the test scoring, Mental Association between night waking and cognitive Development Index (MDI) and Psychomotor Development developments Index (PDI) were derived. All assessments were conducted The mean MDI and PDI score was 103.13 (102.12-104.14) by well-trained pediatricians. and 101.97 (101.03-102.91). There was no gender difference regarding to MDI and PDI scores (p>0.05). Statistical analyses Parental education levels were highly correlated (r=0.73, An initial examination of the data was performed to test for p<0.001) and both were significantly associated with MDI normality and outliers. If normality was not fulfilled then and PDI (p<0.001). the data was transformed accordingly, e.g., night waking Partial correlation, controlled for age, showed that infant duration was analyzed by log10 (raw data +1) night waking frequency and total night waking duration transformation. were negatively associated with MDI (r=-0.06, p=0.040; r=- The MDI and PDI across gender, parental education level 0.08, p=0.014), but not associated with PDI (r=-0.01, and area were compared by ANOVA. The associations p=0.740; r=-0.04, p=0.229). Infant total sleep duration was between sleep parameters and Bayley scores were tested by correlated with neither the MDI nor the PDI (r=-0.03, partial correlation adjusted for children’s age. Linear p=0.342; r<0.01, p=0.885). regression analysis was applied to test the predictive effect Linear regressions indicated that prolonged night of sleep parameter on Bayley scores. Children’s age, gender, waking duration had an adverse impact on MDI only among maternal education level and recruited province were toddlers aged 1-2.5 years old (β=-0.10, p=0.045). Neither entered as control confounders in each model. The statistical total sleep duration or night waking frequency predicted for significance level was set at 0.05. MDI in the model (Table 1). Table 1: Linear regression model of Bayley MDI. Results Age <12m 12m-30m The mean age of the 1102 children was 371.95 (375.24- Beta t p Beta t p 386.56) days, 53.8% (593/1102) of the sample were boys. Boys and girls were of similar age (t(1100)=-1.16, p=0.246). Total sleep duration -0.03 -0.77 0.445 0.04 0.93 0.354 Night waking frequency -0.03 -0.78 0.449 0.02 0.44 0.661 Infant sleep and night waking Night waking duration# <-0.01 -0.03 0.980 -0.10 -2.01 0.045 On average, infants slept 12.40 (12.30-12.51) hrs every day. No differences of total sleep were found between girls and # Night waking duration was log transformed. boys (t(1089)=0.88, p=0.378). Figure 1 showed infants’ night waking frequency and duration across age groups. In general, infant woke up 1.77 Discussion (1.69-1.84) times per night and woke 0.50 (0.45 - 0.54) hr This study underscores the high prevalent and long lasting through the night. Overall, boys woke up more frequently night waking problem among Chinese infants and toddlers than girls (t(1097)=2.22, p=0.027). No differences of total with equivalent total sleep duration comparing with night waking duration were found between girls and boys previous meta-analysis (Galland Taylor, B.J., Elder, D.E., & (t(1082)=1.56, p=0.145). Herbison, P., Galland, Taylor, Elder, & Herbison, 2012). Moreover, longer night waking duration is predictive for slower cognitive development especially during the transition period from infancy to toddlerhood. 512 The current results showed that night waking duration values as our results could be referenced for future parental- negatively predicted for cognitive development only among educated sleep intervention programs to effectively improve toddlers beyond one year old and highlighted the sleep in young children (Bonuck & Grant, 2012; Hall, impairments of sleep fragmentation. Previous study Saunders, Clauson, Carty, & Janssen, 2006; Price, Wake, involving 1385 Chinese Kindergarten children aged 5.7 Ukoumunne, & Hiscock, 2012). years old also showed that children with parental reported difficulties in maintaining sleep scored peculiarly lower in verbal IQ (tested by Wechsler Preschool and Primary Scale Acknowledgments of Intelligence-Revised) (Liu et al., 2012). We’d like to acknowledge the children and their families for More and more studies reveal the importance of infant their participation. We thanked the 16 hospital in 8 sleep quality, rather than sleep duration, which associates provinces for their corporations. The study was supported with infants’ cognitive functions. On one hand, frequent and by Chinese National Natural Science Foundation persistent night waking definitely disturbed sleep continuity, (81172685); the Ministry of Science and Technology of and the consequent increasing of stress level could impair China (2010CB535000); Ministry of Health (201002006); infants’ mental performance (Anders, Keener, & Kraemer, Shanghai Science and Technology Commission 1985; Charmandari, Kino, Souvatzoglou, & Chrousos, (12411950405，13QH1401800); Shanghai Key Discipline 2003). Alternatively, both night waking and impaired cognition could be resulted from CNS diseases and other of Public Health ;Shanghai Municipal Committee of life stress events such as early problematic parenting Education (11SG19，HJTY-2010-A09), AFINS research (Bernier, Carlson, & Whipple, 2010; DeLeon & Karraker, project (AFINS-HOPE-2011025), Shengyuan Research 2007). On the other hand, night waking could be a Project. representation of circadian sleep dysregulation that has been suggested as a predictor for later poor cognitive regulation References (Bernier & Carlson, 2010; Dearing, McCartney, Marshall, & Anders, T. F., Keener, M. A., & Kraemer, H. (1985). Sleep- Warner, 2001). wake state organization, neonatal assessment and The positive effect of sleep on motor development in development in premature infants during the first year of children was not supported in the current study. A previous life. II. 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