Oral processing behaviours that promote children's energy intake are associated with parent-reported appetitive traits: Results from the GUSTO cohort

Abstract

Oral processing behaviours associated with faster eating rates have been consistently linked to increased energy intakes, but little is known about their links to children's appetitive traits. This study used the Child Eating Behaviour Questionnaire (CEBQ) to explore cross-sectional and prospective associations between parent-reported appetitive traits and observed oral processing behaviours. Participants were 195 children from the Growing Up in Singapore Towards healthy Outcomes cohort, who participated in a video-recorded ad libitum lunch at 4.5 (Time 1) and 6 years (Time 2). Their mothers completed the CEBQ around the same time points. Children's bites, chews and swallows were coded, and used to calculate their eating rate, bite size, chews per bite, chew rate, oral exposure time and oral exposure per bite. At Time 1, children with higher scores in slowness in eating had lower eating and chew rates. At Time 2, higher scores for food enjoyment and lower for satiety responsiveness, slowness in eating, and food fussiness were linked with higher eating rates and greater energy intakes (r > 0.16, p < 0.05). Post-hoc analyses revealed that these associations were moderated by BMI and only present among children with higher BMI. Faster eating rates mediated the associations between greater food enjoyment, lower slowness in eating, lower food fussiness and higher intakes of energy. Children with higher slowness in eating scores had lower increases in eating rates over time, and children with higher BMI who had greater food enjoyment and food responsiveness scores had greater increases in eating rates over time. The findings suggest that oral processing behaviours linked with increased obesity risk may be underpinned by appetitive traits and may be one of the behavioural pathways through which these appetitive traits influence energy intakes.

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.