Bidirectional associations between sleep and dietary intake in 0–5 year old children: A systematic review with evidence mapping

Journal Pre-proof Bidirectional associations between sleep and dietary intake in 0-5 year old children: A systematic review with evidence mapping Aimee L. Ward, Andrew N. Reynolds, Sarahmarie Kuroko, Louise J. Fangupo, Barbara C. Galland, Rachael W. Taylor PII:

S1087-0792(19)30199-6

DOI:

https://doi.org/10.1016/j.smrv.2019.101231

Reference:

YSMRV 101231

To appear in:

Sleep Medicine Reviews

Received Date: 24 July 2019 Revised Date:

18 October 2019

Accepted Date: 1 November 2019

Please cite this article as: Ward AL, Reynolds AN, Kuroko S, Fangupo LJ, Galland BC, Taylor RW, Bidirectional associations between sleep and dietary intake in 0-5 year old children: A systematic review with evidence mapping, Sleep Medicine Reviews, https://doi.org/10.1016/j.smrv.2019.101231. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Elsevier Ltd. All rights reserved.

Title Bidirectional associations between sleep and dietary intake in 0-5 year old children: A systematic review with evidence mapping Running title Diet and sleep in young children Authors and affiliations Aimee L Ward1, Andrew N Reynolds1, Sarahmarie Kuroko1,2, Louise J Fangupo1, Barbara C Galland3, Rachael W Taylor1 1

Department of Medicine, University of Otago

2

Department of Human Nutrition, University of Otago

3

Department of Women’s and Children’s Health, University of Otago

Corresponding author Dr Aimee L Ward Department of Medicine, Dunedin School of Medicine, University of Otago PO Box 9054, Dunedin 9054, New Zealand 64 22 673 1278 · [email protected] · [email protected] Author contributions ALW and ANR contributed equally to this work. RWT, ANR, and ALW led the research. ANR developed the search strategy. SK and LF conducted article screening and quality assessments. ALW and ANR conducted screening checks and resolved conflicts. ANR conducted quality assessment checks and created associated figures. ALW created figures and tables. ALW, ANR, SK, and RWT drafted the manuscript, and ALW finalised it. All authors contributed to the review of drafts and read and approved the final manuscript. Conflicts of interest Authors declare no conflicts.

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Summary We have undertaken a systematic review examining the role of diet on sleep, and sleep on diet, in children aged 0-5 years. Controlled trials and cohort or cross-sectional studies were identified with online searches of PubMed, Medline, Embase, Scopus, and CENTRAL up to 1 June 2019, and hand searching of relevant publications. Searches, extraction, and risk of bias assessments were undertaken independently by at least two researchers. Fifty articles involving 72,491 children on a diverse range of topics were eligible. All five studies that investigated the effect of sleep on diet indicated that poorer sleep (measured by a variety of indices) was associated with greater dietary energy intake or poorer diet quality. Conversely, the findings regarding how diet might influence sleep were less consistent when considering feeding practices, energy and macronutrient intake, or micronutrient and small metabolite intake. Studies were typically of short duration and relied on subjective measures of sleep (66%) or diet (88%). While we identified a clear relationship between reduced sleep and poorer diets, future studies require improved methodological reporting and support from transdisciplinary collaborations to better understand the possible role of diet on sleep. Prospectively registered with PROSPERO International Prospective Register of Systematic Reviews (CRD42018091647).

Key words Children, dietary intake, sleep, obesity risk

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Glossary of terms ECG: electrocardiogram FFQ: food frequency questionnaire GI: glycaemic index Kcal: kilocalorie Macronutrient: for example, fat, protein, carbohydrate MCT: medium-chain triglycerides Micronutrient: for example, vitamins and minerals NOS: Newcastle Ottawa scale RBC: red blood cell RCT: randomised controlled trial Small metabolites: for example, amino acids and phenolic compounds SD: standard deviation Tryptophan: an amino acid that can be converted to serotonin and melatonin

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1.

Introduction While individual countries have reported a stabilisation of obesity rates in young

children, the global prevalence of obesity in children under the age of five continues to rise.[1] Weight status tracks from childhood onwards,[2] with overweight children likely to remain overweight as adults,[1] facing an increased risk of non-communicable diseases over the life course.[3] It is well-established that prevention is key to improving childhood obesity rates, and that infancy to early childhood is a critical period for developing healthy eating and activity habits that persist into later life.[1, 3, 4] While diet and physical activity have long been cornerstones of obesity prevention strategies, difficulties in modifying these behaviours in the long-term suggest that investment in other approaches is warranted.[5] Such an approach might be via sleep, given that short sleep duration has been identified as a strong, independent risk factor for obesity in children, including infants.[5-9] Indeed, two recent trials have determined that sleep interventions during infancy can benefit weight long-term.[10, 11] However, the mechanism(s) whereby insufficient sleep leads to increased weight gain are uncertain,[5, 12-14] although thought to be mediated primarily through an increase in dietary energy intake.[12] A recent systematic review and metaanalysis in children aged two to 18 years indicated that short sleep was associated with unhealthy dietary habits and positive energy balance.[15] These studies have shown that shorter sleep leads to a greater energy intake[16] or a preference for more calorie-dense and sweeter foods[16, 17] in teenagers, with similar outcomes observed among preschool[18] and school aged children.[19] However, there are challenges with assessing relationships between sleep and diet, particularly in infants and toddlers as their dietary needs and sleep requirements change rapidly,[20, 21] and subjective methods of data collection introduce bias. While studies have investigated associations between sleep and macronutrient intake (fat, protein, and

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carbohydrate), sleep and micronutrient intake (vitamins and minerals), and sleep and small metabolites (such as amino acids and phenolic compounds),[22] the possible bi-directional nature of the relationship between sleep and diet (where it is equally feasible that sleep affects diet as diet affects sleep) has not been explored.[23] Perhaps this is why, despite the considerable health impacts of obesity on population risk factors for non-communicable disease and premature mortality, few systematic reviews of sleep and diet have been conducted for children aged five years or younger. This review investigates the bidirectional associations between sleep and diet in children aged five years and younger. We define the eligible studies in this area with evidence mapping,[24] identifying knowledge gaps with a visual presentation of research topics and study types as well as the methods used to measure sleep and dietary intake in the existing literature. We conclude by suggesting future directions in the study of sleep and diet in children.

2.

Methods We followed PRISMA processes and reporting standards for systematic reviews and

meta-analyses.[25, 26] This review was prospectively registered in the PROSPERO International Prospective Register of Systematic Reviews (CRD42018091647). Literature searches, identification of eligible trials or studies, data extraction, and bias assessment were undertaken independently by at least two researchers (SK and LJF), with discrepancies resolved with an additional reviewer (ALW or ANR). Data extracted included citation details, study design, location, sample size, age range, sleep and diet measurements used, outcomes reported for sleep and diet, and key findings. 2.1 Search strategy and inclusion criteria

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Trials and cross-sectional or cohort studies were identified with online searches and hand searching of reference lists.[26] Working with a research librarian, we searched PubMed, Medline, Embase, Scopus, and the Cochrane Central Register of Controlled Trials from their inception to 1 June 2019 with no date or language restrictions applied. The search strategy is provided in Table 1. We included experimental trials, cross-sectional and cohort studies with a quantitative marker of sleep (any measure of sleep – duration, latency, overall quality, etc.) as either exposure or outcome, and a quantitative marker of dietary intake (any substance ingested orally) as the corresponding exposure or outcome. Parameters of dietary intake or sleep identified through qualitative methodologies were outside the scope of this review. Participants of eligible trials and studies were children aged five years or younger, or if results were reported from groups, as a mean age of less than six years. Comparison diets were required to be matched for additional lifestyle modifications such as physical activity. Studies and trials of only participants with pre-existing chronic conditions were excluded, as was the purposeful sampling of children who were overweight or obese. Reviewers identified eligible trials and studies by screening titles, abstracts and where appropriate full texts with the use of the online search management tool Covidence.[27] Table 1. Search strategy Research question: How is sleep related to diet in children aged younger than 5 years? (PROSPERO International Prospective Register of Systematic Reviews, CRD42018091647 Search platforms

Search terms

PubMed; Medline; Embase; Scopus; Cochrane Central Register of Controlled Trials; hand-searching of identified trials

infant OR new born OR newborn OR preschool* OR child* OR prepubert* OR pre-pubert* OR pre pubert* OR school age AND sleep* OR nap OR slumber AND nutri* OR food OR kilojoule OR calorie OR energy intake OR diet* No restrictions by date or language applied.

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Additional punctuation included if required by search platform.

Exclusions

• •

Studies of children aged >6 years Purposeful sampling of children with chronic conditions

2.2 Risk of bias assessment We used the Cochrane Risk of Bias tool[28] for trials and the Newcastle Ottawa Scale (NOS)[29] to assess risk of bias of each observational study. 2.3 Data analysis We used evidence mapping to understand what has been done to date in this research area and to identify research gaps and future research needs.[24, 30] We defined the pool of identified studies by characteristics including study type, topic, sleep measures used, dietary measures used, and age group. Cross-sectional studies are reported separately given the inability to assess association direction with this study design. As indicated by our PROSPERO registration, we initially intended to undertake meta-analyses where relevant, but differing study characteristics such as study design, participant age, and exposure and outcome parameters reported meant that just two studies were able to be included in any meta-analysis. As it is considered that four studies are required to present confident findings,[31] we opted not to conduct meta-analyses in this review.

3.

Results Of 10,898 records initially identified, 17 eligible trials of 2,678 participants, 16

eligible cohort studies of 65,265 participants, and 17 eligible cross-sectional studies of 4,548 participants were identified (see Figure 1). Identified trials and studies were from North America (38%), Europe (38%), Asia (10%), the Middle East (6%), South/Central America (4%), Australia (2%), and Africa (2%). An evidence map summarising the included studies

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by topic and study type is shown in Figure 2. Most studies (90%) considered how diet and dietary habits influenced parameters of sleep, rather than examining the reverse. Further evidence mapping of the methodologies used to identify exposure and outcome, and by participant age, are shown in Figures 3-6. Methods used to measure both sleep and diet outcomes varied (see Figures 3 & 4), and were mainly subjective (66% and 88%, respectively); some studies used a combination of subjective and objective measures. Subjective measures of sleep included retrospective recalls (40%), sleep diaries (12%), and parental query of sleep habits and patterns (14%). Subjective measures of dietary intake included 24-hour diet recalls (8%), diet records or diaries (26%), food frequency questionnaires ranging from 4 to 211 items (26%) and various other dietary habit questionnaires (12%). Objective methods for measuring sleep (duration, latency, and quality) included actigraphy (33%) and direct observation methods such as ECG, tracking eye movements, and watching infants sleep (14%). Objective diet measures included the use of biomarkers (9%) or the provision of food in experimental studies (22%). Although the largest study (n=48,222) included was undertaken in children aged 3-5 years, the predominant age of participants across all studies was 12 months or less (57% of studies). A description of each identified study is found in Table S1. As indicated previously, no metaanalyses were possible because of the small number of comparable studies due to differing study characteristics. 3.1 The influence of sleep on dietary intake One trial [18] and two cohort studies[32, 33] considered the influence of sleep on dietary intake. All three indicated that poor sleep in terms of reduced duration, or poorer efficiency, had an unfavourable effect on dietary intake (Table 2). All studies were of participants over 15 months of age. The trial showed that restricting sleep by an average of 2.3 hours over just one night in pre-schoolers (aged 3-4 years) resulted in a 21% increase in

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caloric intake the following day compared with baseline.[18] In particular, children consumed more sugar and carbohydrate (by 25% and 26%, respectively).[18] One cohort study also found that shorter sleep resulted in higher energy intake in early childhood.[33] Restricting sleep may influence the timing of eating, as indicated by one cohort study which demonstrated that shorter sleepers consumed more calories at night, with toddlers in the shortest sleeping group (<10 hours a night) consuming an average of 166 kcal at night, whereas those in the longest sleeping group (>13 hours per night) consumed an average of just 46 kcal per night.[32]

Table 2. Summary of associations reported across included papers examining the effects of sleep variables on dietary intake* Favourable on diet Mixed/Null Unfavourable on diet outcome outcome Reduced duration 0 0 3 (100%)[18, 32, 33] Poorer efficiency 0 0 1 (100%)[18] Total 0 0 4 (100%) *The number of diet outcomes may not be equal to the number of papers cited, in order to account for all outcomes reported

3.2 The influence of feeding practices on sleep 3.2.1 Breastfeeding and sleep One trial[34] and six cohort studies[35-40] examined the effect of breastfeeding on sleep. Findings were mixed overall as summarised in Table 3, with most findings indicating an adverse (67%) effect of breastfeeding in the short term, although actual differences in sleep parameters between groups were small. One birth cohort investigated breastfeeding duration and its effect on sleep trajectories at the age of 2, 3 and 5-6 years and discovered that infants who were predominately breastfed for more than four months were more likely to have better sleep latency at all ages, when compared with those who were breastfed for a shorter period of time.[36] Four studies reported that breastfeeding may be associated with

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various unfavourable sleep outcomes, such as more night wakings,[39] higher arousability,[37] more fragmented sleep,[39] or shorter sleep duration[35, 38] in participants ranging from one day to 18 months of age. The single trial, a 2x2 design, randomised mother/child dyads to receive either a “Soothe/Sleep” or “Introduction of Solids” intervention (or both interventions), with measurements at 2-3 weeks of age, two weeks after introduction to solids, and at one year.[34] Parents in this trial learned soothing strategies to minimise feeding for non-hunger-related fussiness and to prolong sleep duration (“Sooth/Sleep” group), or were taught about hunger and satiety cues (“Introduction of Solids” group). Infant breastfeeding status at 16 weeks was included in the models to test whether the effects of the intervention differed by feeding mode, and analyses indicated a significantly positive interaction between breastfeeding status and nocturnal sleep, indicating increased sleep duration among breastfed infants.[34] 3.2.2 Introduction of solids and sleep Two trials[41, 42] and four cohort studies[36, 43-45] evaluated how the early (at or before three months of age) introduction of solids or complementary foods (such as thickeners in milk/formula, excluding cereals) influenced sleep outcomes in infants, with most studies (83%) reporting favourable effects on sleep (Table 3). Results indicated that the early introduction of solids or complementary foods may be associated with positive effects on sleep variables, including a reduction in the number of sleep episodes,[43] improvements in the sleep pattern,[41] or increases in the duration of longest overnight sleep bouts.[42-44] However, it should be noted that the differences between groups were minimal; one cohort study reported that the introduction of thickeners in milk or formula reduced the odds of belonging to the “short sleeper” trajectory (OR=0.35; CI: 0.13; 0.95).[36] Interestingly, the single study reporting the opposite finding, that is, that the early introduction of solids was associated with shorter sleep duration[45] had the longest follow-up (6-24 months). While

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these findings suggest that early introduction of solids might have an immediate benefit on sleep parameters in infants, this advantage does not appear to be sustained in the longer term.

Table 3. Summary of associations reported across included papers examining the effects of feeding practices on sleep outcomes* Favourable on sleep Unfavourable on outcome Mixed/Null sleep outcome Breastfeeding 2 (22%)[34, 36] 1 (11%)[40] 6 (67%)[35, 37-39] Introduction of solids 5 (83%)[36, 41-44] 0 1 (17%)[45] Total 7 (46%) 1 (7%) 7 (46%) *The number of outcomes related to feeding practices may not be equal to the number of papers cited, to account for all outcomes reported 3.3 The influence of dietary intake on sleep Nine trials[46-54] and four cohort studies[55-58] were identified that considered whether manipulation of infant formula, alcohol, or food intake was related to sleep outcomes. All five trials investigating manipulation of infant formula found a favourable effect on sleep, and both studies that explored the effects of alcohol in breastmilk found adverse effects on sleep, while findings regarding food intake and sleep were mixed (Table 4). 3.3.1 Infant formula composition and sleep Several trials have manipulated the composition of infant formula to determine potential effects on sleep. One showed that total sleep time was higher for neonates receiving varying levels of medium-chain triglycerides (MCT) in infant formula than for infants consuming the control variant, with a dose response effect apparent.[49] Three trials investigated the effect of tryptophan supplementation, reporting that milk with high concentrations of tryptophan increased total sleep time and sleep efficiency in infants when consumed at night,[46] reduced mean sleep latency,[48] or led infants to enter quiet sleep and active sleep phases significantly earlier than infants consuming control formulas.[50] Data from one trial indicated that while sleep duration was increased in 48-hour old infants who received balanced-formula, compared with carbohydrate-fed and water-fed groups

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throughout the observation period, the act of feeding rather than the composition of bottle contents also settled these newborns.[47] 3.3.2 Alcohol in breastmilk and sleep Both trials investigating the effect of alcohol in breastmilk on infant sleep indicated that infants exposed to alcohol in breastmilk exhibited poorer sleep/wake rhythms.[51, 52] Infants spent less time sleeping during the 3.5 hours after breastfeeding when mothers had consumed alcohol than controls (56.8 minutes and 78.2 minutes, respectively), and this was attributable to a shortening in the longest sleeping bout and the amount of time spent in active sleep.[51] Another trial replicated these results, finding that infants exhibited significantly less active sleep during the 3.5 hours immediately following exposure to alcohol, reporting additionally that compensatory increases in active sleep were observed in the next 24 hours, in the absence of alcohol.[52] 3.3.2 Food and macronutrient intake and sleep Except for two studies that reported mixed/null results, studies included in this category suggest that ‘more healthy’ eating choices have a beneficial effect on sleep, and ‘less healthy’ eating patterns have an adverse effect on sleep. For macronutrients, manipulation of the diet by substituting saturated fat with unsaturated fat at age 13 months was associated with longer sleep duration at 2 years of age.[55] In terms of food patterns, lower intakes of fruit and vegetables or higher intakes of processed and fast foods have been associated with shorter sleep duration.[57, 58] One cohort reported infants who were introduced to vegetables and fruits at an earlier stage had longer overnight sleep bouts at nine months of age than infants who were introduced to vegetables and fruits at a later age.[56] Findings from a cohort study were similar, indicating that participants with higher scores for a “processed and fast food” dietary pattern exhibited shorter sleep.[58] Inconclusive findings were reported by two trials investigating whether sleep was affected by consumption of fatty

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fish compared with meat (chicken, lamb or beef),[54] and whether differing glycaemic properties of milk influenced sleep in toddlers aged almost two years.[53]

Table 4. Summary of associations reported across included papers examining the effects of dietary intake on sleep outcomes* Favourable on Unfavourable on sleep outcome Mixed/Null sleep outcome Composition of formula 6 (100%)[46-50] 0 0 Alcohol 0 0 2 (100%)[51, 52] Food & macronutrients 3 (44%)[55, 56] 2 (28%)[53, 54] 2 (28%)[57, 58] Total 9 (60%) 2 (13%) 4 (27%) *The number of sleep outcomes related to supplemented infant formula, alcohol, and food intake on sleep is not be equal to the number of papers cited, to account for all outcomes reported

3.4 The influence of micronutrient and small metabolite intake on sleep Four trials[59-62] and one cohort[63] were identified. Within these studies, 57% of findings were mixed/null regarding effects on sleep (Table 5). One trial reported iron supplementation increased night time sleep duration and decreased frequency of night waking,[61] whereas nicotine in breastmilk negatively altered infant sleep/wake patterns.[62] A third trial observed no differences in sleep duration in infants who received zinc supplemented milk compared with placebo.[60] Two studies investigated caffeine intake, both via breastmilk and dietary intake. Findings from a double blind RCT suggested no difference in directly observed sleep between infants who received caffeine when compared to controls.[59] One cohort study supported these null findings by reporting no change in sleep duration or sleep pattern in infants receiving caffeine via breastmilk compared with those whose mothers did not consume caffeine.[63]

Table 5. Summary of associations reported across included papers examining the effects of micronutrient intake on sleep outcomes* Favourable on Unfavourable on 13

sleep outcome Mixed/Null sleep outcome [60] Zinc supplementation 0 1 (100%) 0 Iron supplementation 2 (100%)[61] 0 0 Nicotine (in breastmilk) 0 0 1 (100%)[62] Caffeine 0 3 (100%)[59, 63] 0 Total 2 (29%) 4 (57%) 1 (14%) *The number of sleep outcomes related to micronutrient intake may not be equal to the number of papers cited, to account for all outcomes reported

3.5 Cross-sectional associations between sleep and diet 3.5.1 Studies presented as investigating how sleep affects diet and/or eating behaviour Two cross-sectional studies presented their findings in terms of how different measures of sleep influenced energy intake, dietary quality, or eating behaviour using wellknown, validated tools for assessing outcomes of interest.[64, 65] One examined sleep duration in relation to energy intake, showing that shorter sleep was associated with higher energy intakes.[64] Shorter sleep duration was also associated with poorer quality diets in both studies[64, 65] and with greater emotional overeating and greater food responsiveness in one study.[64]. Having a more variable sleep pattern in terms of greater differences in sleep duration and timing from weekends to weekdays was also related to diets of lower quality overall.[65] Table 6. Summary of associations reported across included cross-sectional studies examining sleep’s effect on diet* Favourable on Unfavourable on diet diet outcome Mixed/Null outcome Reduced sleep duration 0 0 3 (100%)[64, 65] Increased sleep variability 0 0 1 (100%)[65] Total 0 0 4 (100%) *The number of diet outcomes is not be equal to the number of papers cited, to account for all outcomes reported

3.5.2. Studies presented as investigating how feeding practices/diet affects sleep Thirteen cross-sectional studies presented their findings in terms of how different measures of diet or eating behaviour influenced sleep. Nine studies[66-74] considered how breastfeeding might affect different sleep outcomes, with an additional study investigating 14

specifically how demand feeding influenced sleep in new-born infants.[75] Those studies reporting favourable effects of breastfeeding on sleep tended to be in very young infants (under 34 weeks), finding that although breastfed infants woke more in the night, they slept longer overall,[70] or had improvements in sleep efficiency.[71] Studies of participants ranging from one day to 18 months old reported that breastfeeding may be associated with unfavourable sleep outcomes, such as more night wakings,[66, 67, 70, 72, 73] or shorter sleep duration.[66, 67] Other studies reported null or mixed effects on sleep patterns.[68, 69, 74] One explanation for the discrepant findings with regard to breastfeeding and sleep illustrated by Table 3 may be because a comparison of on-demand feeding with scheduled feeding found support for the hypothesis that wakefulness is related to the timing of feeding rather than the type of milk, or how it is offered, to newborns.[75] Four cross-sectional studies[76-78] were identified that considered whether food intake was related to sleep outcomes. In terms of macronutrients, two studies have indicated that higher carbohydrate intake, particularly at the evening meal, was associated with longer sleep duration in toddlers aged 18-24 months[76, 77], with one study finding no effect of dietary composition on sleep duration.[79] One cross-sectional study reported higher sugar intake was associated with shorter sleep duration in children[78] whereas another found no differences in sleep duration in toddlers who consumed caffeinated beverages compared with those who did not.[80]

Table 7. Summary of associations reported across included cross-sectional studies examining feeding practices or diet’s effect on sleep* Favourable on Unfavourable on sleep outcome Mixed/Null sleep outcome [70, 71] [68, 69, 74] Breastfeeding 3 (23%) 3 (23%) 7 (54%)[66, 67, 70, 72, 73] Macronutrients 2 (40%)[76, 77] 2 (40%)[79, 80] 1 (20%)[78] [80] Caffeine 0 1 (100%) 0 Total 5 (26%) 6 (32%) 8 (42%) *The number of sleep outcomes is not be equal to the number of papers cited, to account for all outcomes reported

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4.

Risk of Bias Risk of bias summaries are shown in Figure 6. Most trials were of unclear risk of bias

for their sequence generation and allocation concealment and blinding of participants and staff. High risk of bias was identified for sequence generation (4 of 17), blinding of participants (3 of 17), and then one study each for blinding of outcomes, incomplete outcome data, or other (no washout period in a cross over design with likely carryover effects). Only one (7%) of the 17 trials considered the adequacy of their sample size. For cohort studies, eight of the nine domains in the Newcastle Ottawa Scale (NOS) were considered (the domain ‘evidence of outcome of interest present before study commenced’ was not considered.) The average NOS score was 5.1 out of eight, with ‘exposure measurement obtained within a structured interview’ and ‘outcome blinding’ poorly represented. There were also serious concerns with adequacy of follow up, and adequate controlling of confounders, such as measures of socioeconomic status. For cross-sectional studies, the average NOS score was 4.6 out of eight. Cross-sectional studies were varied in their analysis methods and did not often feature models adjusted for known confounders. Few studies presented evidence that non-responders differed from those participating in the study. Participants (infants and children) were often recruited from sources not reflective of the general population, and sample size credibility was not often addressed.

5.

Discussion This systematic review of sleep and diet among children aged five years and younger

illustrates that poor sleep is consistently associated with poor dietary outcomes, although the number of studies included was small. A greater number of studies had examined the effect of diet on sleep, with variable findings. Much of the literature was cross-sectional in nature,

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with no ability to determine direction of the relationship. Meta-analysis of data was not possible due to heterogeneity between studies regarding design, measures, or outcomes, limiting our ability to draw reliable conclusions about the relationship between sleep and diet in this age group. This does not, however, diminish the importance of the relationship between sleep and diet in this age group. The benefit of this systematic review is therefore clear: to collate what we have found and what has been done previously, to provide overall direction on what the results of multiple studies suggest, and to comment on the methodologies of this field, so to improve what is reported going forward. Compared with the number of studies and trials screened at the full text level, there are relatively few studies that isolate sleep and diet from other lifestyle factors so as to compare them in children under the age of five years, and what has been done shows little consistency, with few exceptions. The biggest exception was studies looking at the effect of sleep on dietary intake. This was the only research focus to exhibit a consistent association with poorer sleep variables (duration and quality), with all included studies indicating a negative impact on dietary intake (100% of included studies) and could be indicative of the way forward in sleep-diet research. One common reason why infants and young children are fed in ways that are not in accordance with existing guidelines is to help them sleep.[81, 82] Cultural practices intended to help infants sleep often involve feeding to soothe,[82, 83] with qualitative research indicating that parents are mostly concerned with meeting their child’s immediate needs, rather than longer-term implications.[82] Any effect of breastfeeding on indices of sleep health may be a function of age, with studies in younger infants demonstrating some benefit whereas breastfeeding in older infants tended to be negatively associated with different measures of sleep. This discrepancy may occur because often, younger infants sleep in closer proximity to the mother (compared with older infants). Such proximity allows for easier

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breastfeeding and potentially for infants to be able to settle back to sleep more easily than occurs for older infants who may sleep separately. By contrast, findings for infant formula were more consistent, with five of six trials indicating that manipulation of formula to contain greater amounts of MCT, carbohydrate, or tryptophan resulted in better sleep. Medium-chain triglycerides are considered a rapid source of energy that is easy to assimilate in young infants, whose digestive function is immature.[49] Tryptophan concentration is an amino acid that can be converted to serotonin and melatonin (both of which are involved in good sleep health), that is exhibited in higher levels in breastmilk.[71] Similarly, existing literature investigating the timing of the introduction of solids or non-cereal based complementary feeding was reasonably consistent regarding its effect on sleep in infants, showing that early introduction was associated with better sleep overall, although it is unclear whether the effects on sleep are long-lasting. Those studies examining the effect of dietary intake on sleep reported variable results, although there was some consistency in studies of dietary quality, with higher quality diets leading to improved sleep outcomes, such as longer sleep duration, better sleep latency, better sleep efficiency, and improved sleep/wake rhythms. Limited information was available on macronutrient intakes and sleep outcomes, however there was some consistency in the few studies that looked at dietary patterns and sleep outcomes. Higher intakes of vegetables and fruits and lower intakes of processed of fast foods were associated with improved sleep outcomes, providing some support to the theory that healthier diets lead to healthier sleep. Dietary variability was singled out as being related to poorer sleep quality, lending support to the notion that a healthy diet must be sustainable in order to fully support healthy sleep, especially in the long term. Overall, our findings were inconclusive. The potential for interactions between diet and sleep in this age group to influence health status later in life are undeniable. It is well established that early lifestyle habits, such

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as healthy eating patterns and regular physical activity, strongly predict future health risk and health status. Previous studies among other age groups have identified that sleep is linked independently to both dietary intake and physical activity[9, 13, 84-89] as well as other factors related to what we eat, such as cardiometabolic risk factors or important mediators such as body weight and body fatness.[90-92] Recent experimental studies have identified sleep as a lifestyle factor for obesity risk,[16, 18, 19] one that has been shown to be modifiable in controlled trials.[18, 19] While short term (i.e. days or weeks) sleep outcomes dominate the literature, one large cohort study of 48,922 children aged three to five years included in this review explored longer term effects of sleep and found a higher risk of overweight and obesity among those sleeping less than ten hours per night, suggesting a link between sleep and diet among those younger than five years.[40] Additionally, a cohort study included in this review (n=1,303) found a linear relationship between shorter sleep and higher energy intake in early childhood.[33] This review process has highlighted a need for additional studies, particularly with meticulous measurements of both sleep and diet, during the pre-school years. While polysomnography is a recognised gold standard for the measurement of sleep variables,[93] actigraphy has advanced in recent years to provide an objective measure of sleep and allows assessment of habitual sleep patterns as opposed to polysomnography that is usually limited to a single night. Adherence to actigraphy is usually high, even among young children, and it provides an accurate measure of sleep duration and quality, and of sleep latency if collected in concert with sleep diary data.[94] However, there are still some issues regarding the accurate assessment of wake time using actigraphy, which requires further algorithm development.[95] Increased use of objective measures of sleep should enable meta-analyses or methods of synthesising data from multiple research groups in the future with in turn should increase our understanding of how sleep and diet interact. Accurate measures of

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dietary intake can also be an issue, and while cutting-edge measures such as biomarkers of dietary intake and image-capture via wearable camera technology can mitigate these issues, they are seldom used, with self-report measures of dietary intake more common. The assessment of social confounders, such as parental dietary and sleep practices measured consistently across studies, could also provide important context to support child sleep and dietary data as parental characteristics are likely to influence those of their children. Our review has several strengths, such as the use of evidence mapping to depict the landscape of sleep and diet research in very young children and to provide comment on future reporting in this field. We assessed all included studies with established risk of bias tools, but trials in this field did not commonly report sufficient detail to be adequately assessed. Rigorous adherence to guidelines of reporting requirements for observational and intervention studies[96, 97] of future publications is therefore necessary to improve transparency in the study of the relationship between sleep and diet. Our review is not without limitations. First, one third of included studies were cross-sectional, limiting our ability to discern the direction of the relationship between sleep and diet in young children. We chose to separate these studies according to the author’s interpretation of whether they were suggesting that diet affects sleep, or sleep affects diet, but acknowledge the difficulties in this assumption. Diversity in the studies identified by this review precluded quantitative synthesis of results, and a grading of the evidence. While adjusting for measures of socio economic status was not routinely applied by the identified studies, there is recognition that, for example, maternal socio economic status is difficult to assess because income or work status change with maternity leave. Furthermore, we identified insufficient numbers of studies to consider publication bias, which may be present and influence readers’ interpretation of Figures 2-5. Future endeavours to meta-analyse topics within this field will rely on the adequate reporting of trials and studies in this field, as well as the inclusion of

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more longitudinal and controlled studies be conducted to better understand the bidirectional relationship between sleep and diet in this age group.

6.

Conclusion It is increasingly apparent that obesity in young children often persists into

adolescence and adulthood,[3, 34] as habits laid down in childhood tend to continue into later life,[2] indicating that children may be an ideal population to target with sleep interventions for obesity prevention.[18, 19, 34] Instead of simply including sleep alongside a host of other lifestyle factors, researchers should design studies that isolate sleep measures in order to assess the associations between sleep and dietary intake among young children. To enable this, and to standardise measurement of exposure and outcome, sleep must be considered a viable exposure in its own right, one that influences health outcomes alongside other lifestyle factors such as diet and physical activity. International collaborations, transdisciplinary networks, and regular exposure within scientific discussions and conferences are necessary to highlight the need for sleep research in non-communicable disease risk and management investigations. Future mechanistic studies, observational studies and controlled trials of high reporting quality are all necessary to consider causal pathways or to highlight new tools or sleep intervention approaches for obesity prevention throughout the life course. We have undertaken this review to identify what has been done to date investigating relationships between sleep and diet in young children, so that the field may develop from its own infancy to support future evidence-based health policy and population guidelines. It is important that the immediate and longer-term interrelationships between sleep and diet are better understood in infants and young children, so that health messages can be more sensitive to parents’ concerns about their infant or young child’s sleep and eating, and interventions to fight obesity can be more effective.

21

7.

Acknowledgments The authors wish to thank Dr Josie Athens and Dr Pouya Saeedi for their generous

time in translating some full text articles for review. The authors are also grateful for the guidance of their research librarian, Richard German.

Practice points 1. Sleep could be an effective life-style based tool in managing obesity. 2. In children aged five years and younger, better sleep appears to result in healthier quality dietary intake, and poorer sleep appears to result in poorer quality dietary intake. 3. The early introduction of solids seems to have a favourable effect on infant sleep; however, large cohort studies are needed to see if these effects are long- or short-term in nature. 4. Alongside the recognised benefits of breastfeeding in terms of maternal and infant health outcomes, breastfeeding may also have a favourable long-term effect on child sleep.

Research agenda 1. Researchers examining the influence of diet on sleep and vice versa need to consider the potential for bidirectionality. 2. Randomized clinical trials that manipulate sleep in young children could better evaluate and inform on sleep as an obesity management intervention. 3. Standardising methods of collecting data about sleep and diet are crucial in order to harness the power of sleep for improving child health. 4. The field requires more longitudinal and controlled studies to disentangle the bidirectional effects of sleep on diet in this young age group, given the strong relationship between sleep and obesity and potential for successful early intervention.

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Figure captions

Fig. 1. Flow chart of study selection Fig. 2. Evidence map: Included studies by type and topic Fig. 3. Methods used to measure sleep by study topic Fig. 4. Methods used to measure dietary intake or eating behaviour by study topic Fig. 5. Evidence map: Included studies by age and topic Fig. 6. Risk of bias summaries for identified trials, cohort studies, and cross-sectional studies

33

10,898 records identified through database searches through to 20 March 2018 • 4,055 OVID • 4,134 Scopus • 2,301 PubMed • 408 CENTRAL

5,033 duplicates removed 5,865 records screened after duplicates removed n= 5,147 abstracts did not meet inclusion criteria removed 718 full-text articles assessed for eligibility (5 not in English)

50 studies included for data extraction after full text screening • 17 randomised controlled trials • 16 cohort studies • 17 cross sectional studies

Fig. 1. Flow chart of study selection

668 articles that did not meet inclusion criteria removed • 149 wrong population • 290 wrong outcome or comparator • 216 wrong design or inadequate data • 13 not peer-reviewed or duplicate data

Numbers do not equal included papers as some studies used more than one tool. Direct observation: refers to directly observing infant sleep, in one case also employing HR monitoring, one recording eye movements, and another using ECG Recall: refers to any tool used to retrospectively gain sleep information (bed time, wake time, and sleep habits), either by interview or in writing, without using a validated survey. This includes parental query. Record: refers to any tool used to keep track of sleep in real time (such as a diary) Other survey: refers to any other survey tool. Examples include BISQ (5 studies), Children's Sleep Wake Scale (2 studies), Children’s Sleep Hygiene Scale (one study)

Numbers do not equal included papers as some studies used more than one tool. Provided: refers to the provision of something taken by mouth 24-hour diet recall: refers specifically to the use of 24-hour diet recalls Food record/diary: refers to any tool used to keep track of diet in real time (such as a diet record) FFQ: refers to any food frequency questionnaire (they ranged from 4-211 items) Other survey: refers to any other survey tool. Examples include Child Eating Behaviour Questionnaire for toddlers (CEBQ-T - one study), Bright Futures Nutrition Questionnaire for Infants (one study) Parental query: refers to the use of any questionnaire to establish diet practice/pattern (such as bottle versus breastfeeding)

Fig. 6. Risk of bias summaries for identified trials, cohort studies, and cross sectional studies