Pediatrics

Impact of adiposity, age, sex and maternal feeding practices on eating in the absence of hunger and caloric compensation in preschool children

Abstract

Background/Objectives:

Between the ages of 3 and 5 years, children may become less responsive to internal cues of satiation and more responsive to external cues, which may induce overeating and lead to weight gain. This study aimed to compare eating in the absence of hunger (EAH) and caloric compensation in 3- to 6-year-old children, and to relate the measurements with children’s adiposity, age, sex and maternal feeding practices.

Methods:

According to a within-subject three sequential condition design, food intake in children (n=236) was measured at lunch during three sessions, once a week. The same meal (565 kcal) was offered at each session. The first session (control) was only composed of the meal. Thirty minutes before the second meal, children were offered an energy preload (137 kcal; caloric compensation condition). Ten minutes after the third meal, children were exposed to a post-meal snack (430 kcal; EAH condition). Individual caloric compensation score (COMPX) and EAH score were calculated. Maternal characteristics were measured by questionnaire. Child anthropometrics were measured by a medical doctor.

Results:

On average, children compensated 52±4 % of the energy preload and ate 24±1 % of the energy provided by their meal in the absence of hunger. COMPX and EAH score were not correlated and did not vary with children’s adiposity or age. EAH score was higher in boys (P=0.006). Maternal use of food as reward was associated with higher EAH score (P=0.01) but greater COMPX (P=0.005).

Conclusions:

As early as the age of 3 years children did not fully compensate the energy brought by a snack and ate in the absence of hunger. Parents should be advised to avoid these situations where overeating may occur and to limit the use of food as reward.

Introduction

The elevated rates of childhood overweight and obesity generate a need to better understand eating behaviors that may favor the early development of overweight. Eating in the absence of hunger (EAH) and caloric compensation are two experimental situations that enable researchers to evaluate how children react to challenging situations in which they may overeat. EAH refers to the susceptibility to eat palatable foods even if one is not hungry.1 Caloric compensation refers to the ability to compensate accurately for the energy content of an energy preload given before a meal.2, 3 Both EAH and caloric compensation have already been associated with overweight in children.4, 5, 6, 7, 8, 9 Only two studies have measured both EAH and caloric compensation in the same samples of children,4, 10 although they have not compared the two measurements within participants.

Preschool age is of interest because children’s energy intake (EI) may become more influenced by external cues than by internal cues of hunger and fullness. Reportedly, 5-year-old children, but not 3.5-year-old children, ate a greater amount when larger portions were presented to them.11 When 3- to 5-year-old children were focused on the amount of food remaining on their plate and received rewards for eating, they showed lower caloric compensation than children who were focused on their internal cues of fullness.12 Overeating could differ by sex. Specifically, girls may be more influenced by social desirability than boys8 and consequently, may restrain their intake of palatable foods in a EAH situation, which is supported by previous results.8, 13, 14, 15 Moreover, the maternal use of food to regulate preschool children’s emotions was associated with a higher intake of sweet foods in the absence of hunger when children were upset.16 Restricting access to palatable foods as well as two dimensions of maternal eating behavior (that is, dietary restriction and disinhibition) were positively associated with a higher level of EAH in girls.1, 5, 17

The first aim of the present study was to compare EAH and caloric compensation in 3- to 6-year-old French children. For the first time these two responses will be compared within participants. We hypothesized that children with better caloric compensation ability would eat less in the absence of hunger. The second aim of this study was to examine the influence of children’s characteristics (adiposity, age and sex) and of maternal eating behavior and feeding practices on EAH and caloric compensation in 3- to 6-year-old French children. We hypothesized that older or heavier children would be poorer compensators and would eat more in the absence of hunger than younger or normal-weight children, respectively. We assumed that boys would eat more in the absence of hunger than girls. We hypothesized that the mother’s dietary restriction, the maternal restriction of children’s access to snack food, the maternal use of foods to regulate children’s emotion or to reward them for good behavior would be associated to a lower caloric compensation and a higher level of EAH in children.

Participants and Methods

Overview

The study was conducted in preschools in Dijon, France in March 2011. According to a within-subject three sequential condition design, the study was composed of three sessions organized in the school canteen, at lunch time, once a week for a period of 3 weeks. Children were served the same meal ad libitum at each session. The first session, which was the control condition, was only composed of the meal. The control condition was conducted first to measure intake in an ordinary meal situation. Thirty minutes before the second meal, which was the caloric compensation condition, children were offered an energy-dense preload. Ten minutes after the third meal, which was the EAH condition, children were offered palatable foods. The EAH situation was the last session because it was expected that children would remember the unusual situation of access to palatable food after the meal, which might have influenced their intake in the subsequent situation(s).

Mothers were requested to complete questionnaires and report background characteristics, their feeding practices and their eating behavior.

Participants

The study was conducted according to the guidelines established in the Declaration of Helsinki and was approved by the local ethical committee (Comité de Protection des Personnes Est I Bourgogne, n 2010-53). Informed written consent was obtained from both parents before their child’s participation in the study. At the end of the study, parents received a 20-euro voucher.

A power calculation using R program, based on a previous study,6 indicated that a sample size of 200 participants would be needed to detect a correlation of r=0.19 and a significant difference in caloric compensation score (COMPX) (8±20%) across two groups, with an 80% power at an alpha of 0.05. Four preschools were selected to access a population of children from different socio-economic backgrounds and different ethnic origins. Families of all children registered in the four selected preschool canteens were contacted and invited to participate in the study in February 2011. The criteria for inclusion in the study were that those children did not have any chronic disease or food allergies.

Measurement of child’s EAH and caloric compensation

Before the study started, a practice trial of measurement of children’s food intake using a different menu was organized in each school to habituate children and staff to the presence of the experimenters. At each experimental session, children were seated at the same table, always with the same 3–7 children. They were offered a standard lunch composed of a fixed amount (±2 g) of grated carrot (50 g, 93 kcal 100 g-1, Pierre Martinet, Saint-Quentin Fallavier, France), bolognese lasagna with beef and tomato sauce (200 g, 119 kcal 100 g-1, Soulié Restauration, Rodez, France), semi-soft cheese (22 g, 300 kcal 100 g-1, BabyBel, Fromageries Bel, Paris, France), apple purée (100 g, 68 kcal 100 g-1, Hero, Allex, France), white bread (11 g, 250 kcal 100 g-1, Cypres, Longvic, France) and water (Carrefour, Boulogne-Billancourt, France). To ensure that children ate until being full, they could be served second portions of carrot (30 g) and lasagna (100 g) and ad libitum bread and water. Second services were proposed only for the first two courses of the meal to respect usual practices in the canteens. In total, apart from the bread, the meal provided 565 kcal. Consumption of bread was measured by counting the number of bread slices that were individually eaten. In each canteen, the average weight of a bread slice was determined by weighing 10 slices at the beginning of a meal. Individual leftovers were precisely weighed (±1 g). The energy-dense preload given before the second lunch was a chocolate bun (39 g, 137 kcal, Pasquier, Les Cerqueux, France). A solid preload was chosen to elicit higher compensation.18 The chocolate bun was selected as it was the most frequently chosen snack during a pretest session conducted with other preschool children (n=15). During the main study, children were asked to eat the preload in its entirety. An experimenter checked to ensure that all children did so. Only 18 of them did not, they were excluded from the caloric compensation lunch data analysis. In the EAH condition, 10 minutes after the lunch, children were taken to their usual classroom where they sat at individual tables and participated in a post-meal snack. The instruction was as follows: ‘We will stay here for ten minutes; you can draw and eat whatever you want’. Experimenters made sure that children did not speak to each other and did not put food into their pocket. At each table, a coloring activity and a box full of palatable foods were displayed. The post-meal snack was composed of 10 different foods (430 kcal): crackers (4.5 g, 24 kcal, Minizza, Belin, Mondelez, Clamart, France), chips (6 g, 36 kcal, Tuile salée, Carrefour), cherry tomatoes (25 g, 4 kcal), dried apricots (12 g, 26 kcal, Carrefour), fresh strawberries (50 g, 16 kcal, France), fruit biscuits (13 g, 46 kcal, barquette 3 chatons, LU, Mondelez), fruit candies (10 g, 42 kcal, Coeur Moelleux, Krema, Cadbury, Paris, France), chocolate bars (25 g, 140 kcal, Kinder maxi, Ferrero, Mont-Saint-Aignan, France), chocolate pieces (8 g, 44 kcal, Milka, Kraft Food, Mondelez) and gummy candies (15 g, 52 kcal, Smurf, Haribo, Marseille, France). Experimenters counted the number of foods eaten and calculated the energy consumed from these foods (kcal), in accordance with the producer’s information, nutrition facts or nutritional composition tables.

From the data of the first two sessions, a COMPX was calculated by dividing the difference in EI during the two lunches by the energy from the preload, with the result transformed to a percentage:19

A COMPX of 100 % reflects perfect compensation of the preload, values <100% reflect undercompensation, and values >100% reflect overcompensation.

The data from the third session were used to calculate an EAH score for each child by dividing the EI during the post-meal snack by the EI during the third meal session (EAH), with the result then transformed to a percentage:

An EAH score of 0% means that children did not eat anything in the absence of hunger; subsequently, the higher the score, the more the child ate during the snack period, proportional to their intake at the preceding lunch.

Children’s anthropometrics

Trained medical doctors from the ‘Mother and Child Welfare’ public organization measured weight (kg) in light clothes and without shoes to the nearest 0.1 kg using a digital scale (Soehnle, Benfeld, Germany). They measured height (cm) to the nearest 0.5 cm in a standing position without shoes using a stadiometer (Seca Leicester, Birmingham, UK); as well as waist circumference (cm) at navel to the nearest 0.1 cm using a tape measure. Body mass index (BMI) was calculated and transformed into age- and sex-standardized z-scores (z-BMI) based on the French reference data.20

Maternal feeding practices and eating behavior

Mothers reported information regarding their height (cm) and weight (kg), employment status, family income and level of education. Mothers filled out a section of the Comprehensive Feeding Practices Questionnaire21 evaluating their feeding practices: food as reward, emotion regulation, pressure, monitoring, child control and restriction for weight. Items were scored on five-point scales (from ‘never’ (1) to ‘always’ (5) for food as reward, pressure and restriction for weight; from ‘disagree’ (1) to ‘agree’ (5) for emotion regulation, monitoring and child control). Mothers were asked to evaluate three aspects of their own eating behavior: restriction, emotivity and externality by filling out the French version of the Dutch Eating Behavior Questionnaire.22, 23 Items were scored on five-point scales (from ‘never’ (1) to ‘very often’ (5)).

Statistical analysis

The SAS System for Windows version 9.3 (SAS Institute Inc., Cary, NC, USA) was used to analyze data. Significance was set at P<0.05. The results are expressed as mean±s.e.m. values and as parameter estimates±standard error. After calculation of the EAH score and COMPX, the normality of the distribution was checked and the EAH score was log-transformed.

To determine the difference in EI across the three lunches or across the three sessions, analysis of variances were run. The model tested a session effect, a site (school canteen) effect, a child effect nested within the site effect and being considered as random. Post hoc comparisons (Student’s t-tests) were used to compare the mean values across lunches or across sessions. Pearson correlations were calculated to study the individual stability of EI between the first and third lunches.

The median age was used to split the younger from the older children. The age and sex effects were tested using Student’s t-tests on EI at lunch, EI at the post-meal snack and COMPX or EAH score. Pearson correlations were calculated to determine the link between a child’s z-BMI and EI at lunch, EI at the post-meal snack and COMPX or EAH score. Pearson correlations were calculated to evaluate the association between COMPX and EAH score. The psychometric properties of questionnaires were checked using Cronbach’s α. Univariate and multivariate regressions were performed to test the associations between maternal feeding practices and the background characteristics of children (age, sex, z-BMI) and of mothers (BMI, level of education, ethnicity and income), and dimensions of maternal eating behavior. Only significant variables from multivariate analyses were included in models of further analyses. Stepwise regressions were performed separately to explain the variability of the COMPX or EAH score by the six scales of maternal feeding practices. Finally, multivariate regressions were conducted to explain each score by the selected maternal feeding practices; the background characteristics of children or mothers significantly associated with maternal feeding practices were entered as covariates.

Results

Sample characteristics

A total of 276 parents consented to the participation of their children. Children who did not attend either the first meal or the third meal sessions were excluded (n=40). Finally, 236 children (n=109 girls and 127 boys) participated. A tree diagram of sample loss is displayed in Figure 1. On average, children were aged 4.5±0.06 years (min: 2.6 years; max: 6.5 years). The younger group was aged 3.7±0.04 years (min: 2.6 years; max: 4.4 years, n=118) and the older group was aged 5.3±0.05 years (min: 4.4 years; max: 6.5 years, n=118). Mean waist circumference was 52.4±0.3 cm (min: 44.2 cm; max: 77.5 cm) and mean z-BMI was 0.13±0.08 (min: −2.3; max: 5.8). No significant difference in adiposity was observed between the two age groups. Thirteen children (5.5 %; n=5 girls and 8 boys) were overweight (z-BMI >2).24 Questionnaires were collected from 219 parents and only data from mothers were analyzed (n=193). Some maternal characteristics are presented in Table 1. The majority of mothers were born in France (76 %) and were well educated (20 % had no diploma, 32% had a high school degree or less, 47 % had a higher degree than high school).

Figure 1
figure1

Sample size at each step of the study.

Table 1 Maternal characteristics measured by questionnaire (n=193)

EI at lunch

The EI at each meal and the relationship between EI and children’s characteristics are described in Figure 2. The gram weight consumed at each meal is described in Supplementary Figure 1.

Figure 2
figure2

Energy intake at each session. Three identical lunches were organized in four preschool canteens with French children (n=236) once a week. The first lunch was a control session (CTR). Thirty minutes before the lunch of the second session (Caloric compensation, CC), children were offered a 137-kcal preload (gray bar). Ten minutes after the lunch of the third session (Eating in the Absence of Hunger, EAH), children were offered palatable foods; their mean intake is represented with a black bar. Values are the mean±s.e.m. Mean energy intakes during lunches (white bars) without a common lower case letter differ (P<0.001). Mean total intakes without a common upper case letter differ (P<0.0001).

There was no difference in EI between the control lunch and the lunch before the post-meal snack. Moreover, the correlation between EI from the two meals was significant (r=0.67, P<0 .001), revealing a good stability of EI within children. EI from the lunch after the 137-kcal preload was significantly lower than EI from the two other lunches (P<0.0001). EI from the first session was lower than total EI from the second session (preload+meal), which was lower than total EI from the third session (meal+post-meal snack) (P<0.0001). EI at the control lunch increased with children’s z-BMI (r=0.28; P<0.0001), was higher for boys than girls (441±10 vs 401±10 kcal, P=0.0057) and was higher for older than younger children (442±10 vs 403±11 kcal, P=0.009). The same results were observed at the second and the third lunches (not shown).

COMPX and EAH score

The mean COMPX was 52.5±4.4 % (min: −124.7 %; max: 214.5 %; n=203). The EI from the post-meal snack was 90±5 kcal and the mean EAH score was 23.5±1.4 % (min: 0 %; max: 144.9 %; n=221). During the post-meal snack, 8% of the children did not eat anything. COMPX and EAH scores were not correlated with each other (r=0.05; P=0.46).

Relationship between COMPX or EAH scores and children’s characteristics

The COMPX was not related to children’s age group, z-BMI, waist circumference or sex. The EAH score was not related to children’s age group, to waist circumference or to z-BMI but was higher in boys than in girls (27.2±2.0 vs 19.0±1.9 %; P=0.006), even after adjustment for body weight (data not shown). EI from the post-meal snack was also higher in boys than in girls (107±7 vs 71±6 kcal; P=0.0001) but was not related to the age group. EI from the post-meal snack was positively related to z-BMI (r=0.14; P=0.03).

Relationship between maternal feeding practices and children’s COMPX and EAH score

Mothers’ scores of feeding practices and of eating behavior are presented in Table 2. Food as reward was the only maternal feeding practice that was significantly associated with the COMPX (P=0.011). This association was also observed (P=0.005) when adjusted for mothers’ age, ethnicity, restriction and externality. The COMPX increased by 17±5 % when food as reward increased by one point on a five-point scale.

Table 2 Description of maternal feeding practices and eating behavior scores measured by questionnaire (n=193)

Food as reward was also the only maternal feeding practice that was significantly associated with the EAH score (P=0.023). This association was also found (P=0.011) when adjusted for children’s sex, mothers’ age, ethnicity, restriction and externality. The EAH score increased by 2±1 % when food as reward increased by one point on a five-point scale.

Discussion

The present study evaluated how French children aged from 3 to 6 years behaved when they were placed in two challenging situations where overeating was possible. In comparison with their intake at a control lunch, we observed that they compensated only partially (~50 %) for the energy from a preload given 30 min before lunch. When children were offered a snack 10 min after lunch, they ate in the absence of hunger ~25% of the energy from their lunch. This study revealed for the first time that children who did not compensate for the energy from the preload were not necessarily the same children who ate in the absence of hunger. Contrary to our expectations, no age and no adiposity effects on COMPX and EAH score were observed in this sample of children ranging from 3 to 6 years. This study showed that EAH was higher in boys than in girls; and that maternal use of food as reward was associated with higher EAH score but greater COMPX.

The fact that children who ate in the absence of hunger did not necessarily show lower caloric compensation ability may be related to the assumption that EAH may reflect responses to external cues, and caloric compensation to internal cues. The caloric compensation situation is used to study how EI is compensated regarding food composition,18 which helps understanding the factors involved in energy homeostasis. EAH is mainly used to reflect the children overeating regarding external factors, and indicates disinhibited eating.1, 8 Our observation may also be due to the differences between the two situations: different foods were offered at different states of hunger. This suggests that children may differ in their sensitivity to these two types of cues; or, not exclusively, that these two types of responses may be controlled at different levels.25

Contrary to our hypothesis, older children did not present a lower COMPX and a higher score of EAH. In previous cross-sectional studies conducted with children aged 2–10 years,26 5–12 years4 or 6–9 years,27 older children showed poorer COMPX than younger children. Similarly, previous cross-sectional studies conducted with children aged 5–18 years,15 7–12 years8 and 13–17 years28 showed that older children ate more in the absence of hunger than younger children. The absence of age effects in the present study may be attributed to the smaller age range than in previous studies.

Here, correlations showed that heavier children did not eat more in the absence of hunger and were not poorer compensators. This is not consistent with previous studies showing in preschool children a relationship between weight status and caloric compensation6 or EAH.5 However, several studies conducted with children younger than 7 years observed no association between weight status and EAH1, 10, 17 or caloric compensation.29, 30 Moreover, most of the studies which showed that overweight children were poorer compensators and ate more in the absence of hunger than normal-weight children were conducted with older children.3, 10, 11, 12 This suggests that lack of caloric compensation or EAH may be a consequence of overweight and obesity. Moreover, only <6% of the children in the present study were overweight, against ~50% in a study which found a relationship between weight status and eating behavior;3 this may also explain the absence of relationship in the present study. Further studies are needed to describe better the development of these two behaviors with age and the parallel development of overweight.

Concerning the effect of sex, no difference in caloric compensation was observed between girls and boys, which is consistent with previous studies.4, 27, 30, 31 However, the present study confirmed that girls ate less in the absence of hunger than boys, as showed in previous studies.8, 13, 14, 15 This sex effect may be related to the fact that girls are more influenced by social desirability than boys8 and, consequently, may restrain their intake of palatable foods.

Among the six maternal feeding practices reported,21 only the use of food as reward was positively associated with EAH score and COMPX. The positive association between the use of food as reward and EAH score confirmed our hypothesis and is consistent with the fact that foods offered during the post-meal snack were mostly palatable. In fact, it was previously described that the more mothers used food as reward, the higher was the intake of unhealthy foods in children32 and the higher was the preference for the foods used as reward,33 which are usually palatable and unhealthy. Affective value of the foods used as reward may be high, making them very attractive, even in the absence of hunger.32, 34 Children who are used to be regularly offered foods as reward may also have found more natural to eat the foods that were presented to them after a meal compared with children who are rarely offered foods as reward. The present study showed that the more mothers reported to use food as reward, the better the children compensated the preload during the following lunch. To explain this surprising result, we hypothesize that a frequent use of food as reward may regularly expose children to the challenging situation of eating outside of mealtime, which may be associated with children’s better ability to adapt to this situation. We previously showed that caloric compensation ability was improved after repeated exposure to a preload.35

This study documented for the first time the level of COMPX at a meal after an energy-dense preload in preschool French children. This level was similar to COMPX measured in previous Scottish and American studies.6, 27, 30 The present study documented also for the first time the level of EAH in preschool French children. The EI from the EAH snack, 90±5 kcal, was lower than in previous studies conducted with 5-year-old American children, 125±8 kcal36 and 258±38 kcal.4 In the present study, the total energy offered during the post-meal snack was lower than in previous studies. Moreover, the children were likely surprised by the unusual situation of eating a snack in a classroom.

The present study should be viewed in terms of its strengths and limitations. The measurements of eating behavior were conducted in the children’s usual meal context. As children were seated with other children, peers may have influenced their food intake.34, 37 However, tables were, as far as possible, composed of the same children across the three sessions. The within-subject three sequential design may also be considered to be a limitation. It could be suggested that a boredom effect could appear along the sessions, but no significant difference in mean intake was observed between the first and the third meals, as described in Figure 2, dismissing such a boredom effect. The partial level of energy adjustment may be because intake was measured only at the lunch after the preload consumption, and was not measured at the following eating occasions. Observational studies conducted in children across several days showed that energy adjustment at a particular lunch was less accurate than daily EI adjustment.38, 39 Nevertheless, an experimental study conducted in 3- to 5-year-old children testing the effect of reducing energy density of multiple meals did not observe adjustment of EI on the subsequent meals.40 A large number of children was a strength allowing us to observe a link between EAH behavior and maternal feeding practices. The large sample did not enable us to measure the interactions between children and parents’ feeding by video recording. Nevertheless, previous studies conducted with a similar or smaller sample than that used in the present study recorded parental feeding practices via questionnaire.1, 10, 17, 19

In summary, this study highlighted for the first time that caloric compensation and EAH are two non-correlated eating behaviors. In both cases, we observed that when placed in a challenging eating situation, most children tend to overeat and that large individual differences were observed. Contrary to our hypothesis, the individual differences were not related to the child’s age. This result suggested that from the age of 3 years, children may present eating behaviors that are liable to favor overeating. In particular, children are likely to eat more palatable foods in the absence of hunger if their mothers more frequently used food as reward. Even if with the present age range and sample of children, no relationships were found between poor caloric compensation or EAH and weight status, one can suppose that children regularly confronted to challenging situations where overeating is observed would gain weight. The present study underlines the importance of detecting impaired food intake control from the age of 3 years and may offer practical advice to parents to prevent the development of overeating in children.

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Acknowledgements

We thank H Lillette, A Le Grand and E Marchand for welcoming us to their institutions; V De Anfrasio, S Chambaron, F Durey (ChemoSens platform), V Feyen, J Fontaine, M Gaillet, F Sourdot and S Wagner for assisting with data collection; L Marty for assisting with data analysis; P Emmett and M Vingerhoeds for contributing recommendations to improve the manuscript. ER, SI, SN and VB designed the research study; ER, SN and VB conducted the research; ER, SI, CC and SN analyzed the data; ER, SI and SN wrote the paper. SN was primarily responsible for the content of the final manuscript. All of the authors read and approved the final manuscript. The research was supported by the European Community’s Seventh Framework Program (FP7/2007-2013) under the grant agreement no. FP7-245012-HabEat’, the Regional Council of Burgundy (France), the European Funding for Regional Economical Development (FEDER) and the Fondation Louis Bonduelle. This trial was registered as NCT01843712 at ClinicalTrials.gov.

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Remy, E., Issanchou, S., Chabanet, C. et al. Impact of adiposity, age, sex and maternal feeding practices on eating in the absence of hunger and caloric compensation in preschool children. Int J Obes 39, 925–930 (2015). https://doi.org/10.1038/ijo.2015.30

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