Oral processing behaviours that promote children's energy intake are associated with parent-reported appetitive traits: Results from the GUSTO cohort
Introduction
An early predisposition to accumulate excess fat has been linked with genetic and epigenetic factors, as well as features of the early food environment (Chong, Teh, Poh, & Noor, 2014; Gluckman & Hanson, 2008; Lin et al., 2017; McAllister et al., 2009; Rhee, Phelan, & Mccaffery, 2012). It has been previously proposed that a pathway between genetic factors and future obesity risk is mediated by appetitive traits and eating behaviours that promote greater energy intakes, in what has been referred to as the ‘behavioural susceptibility theory of obesity’ (Llewellyn & Wardle, 2015). Variability in appetitive traits may help to explain why it is not the case that every child brought up in an obesogenic food environment will become obese. Instead, appetitive traits that promote overeating may increase a child's vulnerability to weight gain in an environment characterised by large portions and high availability of palatable, energy dense foods.
Behavioural studies in paediatric populations generally support the idea that children with healthy weight differ from children with overweight in certain appetitive traits. For example, it has been demonstrated that children with overweight tend to have poorer satiety responsiveness, are more responsive to external food cues, such as portion size or food availability, and show higher motivation to work for food compared to children with healthy weight (Jansen et al., 2003; Savage, Haisfield, Fisher, Marini, & Birch, 2012; Temple, Giacomelli, Roemmich, & Epstein, 2007). Psychometric measures have been developed to capture different aspects of these appetitive traits in children, of which the Children's Eating Behaviour Questionnaire (CEBQ: Wardle, Guthrie, Sanderson, & Rapoport, 2001) is considered to be the most comprehensive and widely used. This questionnaire measures eight dimensions of appetitive traits that describe food approach and food avoidance behaviours. Food approach behaviours captured in the CEBQ include food responsiveness, enjoyment of food, desire to drink and emotional over-eating, while food avoidance behaviours are comprised of slowness in eating, emotional under-eating, food fussiness and satiety responsiveness. Previous studies have demonstrated positive associations between food approach subscales of the CEBQ and children's BMI, while food avoidance behaviours have typically been associated with lower weight (Sleddens, Kremers, & Thijs, 2008; Viana, Sinde, & Saxton, 2008; Webber, Hill, Saxton, Van Jaarsveld, & Wardle, 2009). However, it is important to identify specific behaviours through which these appetitive traits are expressed.
Oral processing behaviours are hypothesised to be one of the behavioural markers of appetitive traits (Wardle & Carnell, 2009). Eating rate has been shown to be heritable (Llewellyn, Van Jaarsveld, Boniface, Carnell, & Wardle, 2008), consistent within an individual (Hubel, Laessle, Lehrke, & Jass, 2006; McCrickerd & Forde, 2017) and stable over time (Berkowitz et al., 2010). Studies in adult and child populations show that faster eating rates promote energy intake during an ad libitum meal and are linked with a higher risk of unhealthy weight gain and obesity (Chei, Toyokawa, & Kano, 2005; Drabman et al., 1977, 1979; Llewellyn et al., 2008; Maruyama et al., 2008; Ochiai et al., 2012, 2016; Ohkuma et al., 2015; Otsuka et al., 2006; Robinson et al., 2014; Sasaki, Katagiri, Tsuji, Shimoda, & Amano, 2003; Tanihara et al., 2011). We recently demonstrated that 4.5 year old children who ate a meal at faster rates consumed on average 75% more energy than children who ate at slower rates, and had higher BMI and whole-body and abdominal adiposity (Fogel et al., 2017a). Using an observational approach to objectively characterise a child's eating behaviours within a meal, we have identified an “obesogenic eating style” characterised by eating faster and taking larger bites that spend less time in mouth and are processed using fewer chews. Importantly, these oral processing behaviours consistently predicted higher energy intakes, particularly when combined with longer total meal duration (Fogel et al., 2017b). While overweight children were significantly more likely to eat faster, there were a number of healthy weight children who were also eating at faster rates (Fogel et al., 2017a), suggesting that perhaps this behaviour may only be problematic when it co-occurs with other appetitive traits that support increased energy intake and/or occurs in the presence of an obesogenic food environment.
Little is known about how oral processing behaviours relate to other appetitive traits. In the original studies that led to the development of the CEBQ, items from the slowness in eating subscale loaded together with the satiety responsivity subscale, indicating that these two behaviours may co-occur and be highly correlated and characterised by the same parent-reported behaviours (Wardle et al., 2001). One study that focused on selected subscales from the CEBQ has shown that slower measured eating rates were associated with higher satiety responsiveness, as well as lower food responsiveness and lower enjoyment of food in a sample of 4–5 year old children (Carnell & Wardle, 2007), highlighting that specific appetitive traits may underlie faster eating rates. Whether these appetitive traits map onto different parameters of children's oral processing such as bite size, chew rate or oral exposure per bite remains unclear. As one of the subscales of the CEBQ directly assesses child's slowness in eating, it is important to understand what parameters of oral processing, such as eating rate, eating duration or both, are captured in that parent-reported scale. More broadly, understanding how appetitive traits are linked with specific oral processing parameters will help design intervention strategies targeting specific oral processing behaviours (such as large bite size) that can be observed by parents, in an effort to reduce faster eating rates, which are a risk factor for overeating and unhealthy weight gain.
The aim of the current study was to investigate whether parent-reported appetitive traits are linked with children's oral processing behaviours at 4.5 and 6 years old. We further sought to explore whether appetitive traits reported by parents in the CEBQ could predict children's prospective oral processing behaviours. We hypothesised that faster eating rates and the associated oral processing parameters would be positively associated with food approach behaviours (i.e. enjoyment if food, desire to drink, emotional over-eating) and negatively associated with food avoidance behaviours (i.e. food fussiness, satiety responsiveness and emotional under-eating). We further hypothesised that the slowness in eating subscale would be negatively associated with eating rates and positively associated with meal duration.
Section snippets
Sample
The participants in this study were child and mother pairs from the Growing Up in Singapore Towards healthy Outcomes (GUSTO) cohort (N = 1247), who attended an ad libitum lunch at 4.5 and 6 years of age. Eligibility criteria and the GUSTO study profile are described elsewhere (Soh et al., 2014). Selection criteria for participation in the lunch task are described in the participant flowchart (Supplementary material A). At 4.5 years (±2 months; Time 1), 484 children and their mothers attended a
Statistical analysis
Items within the subscales of the CEBQ have been averaged to control for the missing data from individual questions, in line with previously published approaches (Carnell & Wardle, 2007). Mean scores for the subscales of the CEBQ and oral processing behaviours at Time 1 and Time 2 are presented in supplementary material B. Scores for individual CEBQ subscales did not show normal distribution at either time point, so they were log transformed, which improved normality. Correlation analyses
Unadjusted cross-sectional associations between CEBQ and oral processing behaviours
Cross-sectional unadjusted associations between children's scores on the CEBQ subscales and oral processing behaviours measured at Time 1 and Time 2 are presented in Table 2. At Time 1, children who had higher scores for slowness in eating ate food at slower rates, and had a lower rate of chewing, compared to children rated lower in slowness in eating. There was a non-significant trend for children with higher food fussiness scores to eat at slower rates. The association between higher scores
Discussion
The aim of this study was to investigate whether parent-reported appetitive traits are associated with, and predictive of, children's oral processing behaviours and energy intake. The results show that parent-reported appetitive traits are linked with children's measured oral processing behaviours, predict changes in oral processing behaviours over time, and to some extent may be moderated by BMI.
Children with higher scores for food enjoyment, and lower scores for food fussiness, slowness in
Conclusions
The current study showed that children's appetitive traits reported in the CEBQ were associated with the oral processing behaviours they exhibit when consuming a meal. These associations were stronger among children with higher BMI. Oral processing behaviours, such as eating rate, may be the behavioural markers of appetitive traits and a mediator between appetite and energy intakes, particularly among children with higher weight. Future studies should further investigate these associations at
Ethics approval and consent to participate
Informed written consent was obtained from participants, and the study was approved by the National Healthcare Group Domain Specific Review Board and SingHealth Centralized Institutional Review Board.
Conflicts of interest
K. M. G., Y. S. L., Y.-S. C. and CGF have received reimbursement for speaking at conferences sponsored by companies selling nutritional products. They are part of an academic consortium that has received research funding from Abbott Nutrition, Nestec and Danone. Lisa Fries is an employee of Nestec SA, working at the Nestlé Research Center. The other authors have no financial or personal conflict of interests.
Funding
This work is supported by the Translational Clinical Research (TCR) Flagship Program on Developmental Pathways to Metabolic Disease funded by the National Research Foundation (NRF) and administered by the National Medical Research Council (NMRC), Singapore-NMRC/TCR/004-NUS/2008; NMRC/TCR/012-NUHS/2014. Additional funding is provided by the Singapore Institute for Clinical Sciences, A*STAR and Nestec SA. KMG is supported by the National Institute for Health Research through the NIHR Southampton
Authors' contributions
This study was conceived and designed by CGF, AF, MFFC and LRF. Analyses were performed and interpreted by AF, KMC and CGF. ATG, JYT and MJC collected the data. AF, KMC and CGF prepared the draft manuscript with input from LRF, QPL and MFFC. YSC, KHT, FY, LPS, MJM, BFPB, YSL and KMG were responsible for conception and recruitment for the GUSTO cohort.
All authors reviewed and approved the final draft.
Clinical trial registry number
Acknowledgements
The GUSTO study group includes: Allan Sheppard, Amutha Chinnadurai, Anne Eng Neo Goh, Anne Rifkin-Graboi, Anqi Qiu, Arijit Biswas, Bee Wah Lee, Birit F.P. Broekman, Boon Long Quah, Borys Shuter, Chai Kiat Chng, Cheryl Ngo, Choon Looi Bong, Christiani Jeyakumar Henry, Claudia Chi, Cornelia Yin Ing Chee, Yam Thiam Daniel Goh, Doris Fok, E Shyong Tai, Elaine Tham, Elaine Quah Phaik Ling, Evelyn Chung Ning Law, Evelyn Xiu Ling Loo, Fabian Yap, Falk Mueller-Riemenschneider, George Seow Heong Yeo,
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