1. Introduction
Obesity is a global problem; worldwide 39% of adults are classified as being overweight and 13% as having obesity [
1]. It is now recognised that the development of obesity is influenced by a complex interaction between genetics and psychological factors, such as eating behaviours and food cravings.
Behaviours related to food intake which influence the frequency of eating, meal size, meal content, and attitude to meals are described as ‘eating behaviours’. Eating behaviours can influence the amount of energy consumed by an individual thus predisposing to an increased risk of obesity [
2]. The most commonly studied types of eating behaviours are uncontrolled eating (UE), emotional eating (EE), and cognitive restraint (CR). UE refers to a tendency to overeat, with the feeling of being out of control. EE reflects a propensity to overeat in response to negative emotions (i.e., when feeling lonely, anxious or depressed) [
3]. CR refers to a tendency to consciously restrict food intake instead of using physiological cues (i.e., hunger and satiety) as regulators of intake [
4]. Previous studies have shown an association of eating behaviours with weight gain and increasing body mass index (BMI) [
5,
6] which are directly related to food intake [
5].
Food craving is defined as a strong, irresistible desire to consume a specific type of food [
7], this desire is extremely common with some studies estimating it is experienced by more than 90% of the adult population [
8,
9]. Food cravings can be categorised by both appetitive and aversive components and can be prompted by certain emotional conditions, such as psychological or physical stress, anxiety, depression, anger, or psychological reactance to food [
10,
11]. Increased food cravings have been associated with increased BMI [
5,
12].
Fat mass (FM) and obesity-associated
FTO is the first obesity risk gene recognised by genome wide association studies (GWAS) and is the gene most strongly associated with an increase in BMI [
13]. Single-nucleotide polymorphisms (SNPs) that cluster in the first intron of the
FTO gene show the strongest association with BMI (∼0.35 kg/m
2 per allele), and obesity risk [
14,
15].
FTO is highly expressed in the hypothalamus, a region involved in the regulation of food intake and energy expenditure [
16,
17]. Previous studies have stated that the BMI-increasing allele A of the
FTO variant is associated with higher energy intake and higher fat and carbohydrates intake compared to TT homozygotes [
18,
19]
An influence of
FTO on eating behaviours has been shown, although the results are contradictory. Habron et al., suggest that the
FTO risk allele was associated with differences in eating behaviours in adults with overweight or obesity [
20] and similar findings have been shown in normal weight controls [
21]. In contrast, in a group of adolescents and children,
FTO genotype was associated with BMI but did not influence eating behaviour [
22]. The
FTO gene has been reported to influence food cravings, with individuals carrying the obesity-susceptible A allele having higher total food cravings compared to TT homozygotes which correlates with higher BMI [
23].
Sex and age also influence eating behaviours and food cravings. Previous studies highlight that females have higher scores for CR than males but report inconsistent sex effects for UE or EE [
24,
25,
26,
27]. Other studies found significant differences between sexes with females scoring higher on EE and CR but equal mean scores for UE [
3,
28,
29]. Löffler et al. found that females scored significantly higher than males in all subscales of eating behaviours and also found individuals over 60 years old had significantly higher mean scores than people under 60 years for CR, but lower mean scores for UE and EE [
30].
Regarding the effects of sex and age on food cravings, Imperatori et al. found that females with overweight or obesity were more likely to experience cravings than males [
31] and Chao et al. highlights that females had significantly higher cravings for sweets than males [
32]. A previous study also stated that women reported significantly more cravings for chocolate and for sweets than did men. However, craving for sweets declined with age among women [
33]. These findings are in agreement with another two studies that included older females in reporting a negative association between food cravings and age, although neither of these studied controlled for BMI [
34,
35]. Food cravings declined with age, but this age effect differed across variants of
FTO rs9939609: while TT homozygotes showed the typical age-related decline in food cravings, there was no such decline among A carriers, suggesting that they are at risk for increases in weight gain over the course of aging as fat mass often increases with age [
23]. The decline in food cravings with age may also be related to age-dependent changes in taste sensitivity that have been reported [
36,
37], and may also be responsible for age-related declines in food intake.
Aim
The aim of the current study is to investigate the interactions between eating behaviours, food cravings and BMI. Previous findings indicate that when considering the influence of eating behaviours and food cravings on obesity, it is important to take into account other variables that are known to also influence these measures including genetics, age and sex. It is also important consider which associations are mediated by other relevant variables. This study therefore (1) investigates the interactions between eating behaviours, food cravings and BMI (2) determines the influence of FTO genotype, sex and age on these interactions and (3) uses mediation analysis to explore the role of these mediators in the interactions.
4. Discussion
The aim of this study was to explore the relationships between eating behaviours and food cravings, and examine the influence of sex, BMI, age and FTO genotype on these relationships. We used the TFEQ-R18, FCI, and genotyped for the rs9939609 FTO polymorphism to study 475 individuals. We analysed data from this group split by sex, FTO genotype and age (≤25 years versus >25 years old). We then used mediation analysis to investigate possible mechanisms underlying the association between some of the relationships observed. The main findings are as follows.
Mean scores for the three subscales of the TFEQ-R18 and the four subscales of the FCI were similar to values previously reported. There were no differences between mean scores for BMI, eating behaviours or food cravings split by sex, with only cravings for carbohydrate being higher in women. This agrees with previous studies [
28,
49], but is in contrast with others which found higher scores for eating behavior subscales in women [
30,
50]. This difference may be due to the age of the groups studied; the average age of our group was 31 years, whereas the average age of the participants in these two studies was 50 and 48 years respectively indicating that sex differences in eating behaviours may become more apparent with increasing age. When the group was analysed by genotype the AA + AT group had a mean BMI of 26.52 kg/m
2 compared to the TT genotype group who had a mean BMI of 24.62 kg/m
2, this is consistent with the findings of previous studies which also found that carriers of the risk allele A had higher BMI scores compared to people with the TT genotype [
13,
51]. We did not find differences in TFEQ-R18 or FCI scores when the groups were split by genotype, which is in agreement with a recent study of children by Rivas et al. [
52], which also did not find differences in subscale scores for the TFEQ-R18. This is in contrast to other findings which describe higher food cravings associated with the A allele in a group with an average age of 50 years [
23]. These differences agree with our findings presented in
Table 6 which demonstrate an influence of
FTO genotype on age-related eating behaviours.
We report highly significant relationships between eating behaviours and food cravings, with BMI increasing with age, whilst cravings for fatty food decreased, and UE and EE decreased with age, in agreement with earlier studies [
33,
34,
35]. The data presented in
Table 2 also confirms this; when the two age groups were compared the scores for cravings for carbohydrates and fat, and the scores for emotional eating and uncontrolled eating were all higher in the ≤25 years group compared to the >25 years group. This may reflect changes in eating patterns associated with stages of life; with younger people tending to consume less healthy food [
53,
54], it may also be due in part to age-related changes in taste sensitivity [
36,
37]. We also found that increased BMI was associated with a decrease in cravings for fatty foods but an increase in cognitive restraint, confirming previous results by Johnson et al. who also proposed that high cognitive restraint in normal weight individuals increases the risk of overeating tendencies when restraint is relaxed, thus leading to further increases in BMI [
55]. We found highly significant relationships between eating behaviours and food cravings; increased cognitive restraint correlated with lower cravings for fatty foods, sweet foods and fast foods, increased uncontrolled eating was associated with increased cravings for carbohydrates, and increased emotional eating was associated with lower cravings for fatty foods and fast foods. This is consistent with previous findings; decreased food cravings are associated with increased fMRI-FCR of brain regions that regulate executive control over ingestion [
56] and with cognitive reappraisal strategies, in particular those focusing on the benefits of not eating unhealthy foods, this could potentially increase the ability of individuals with obesity to inhibit appetitive motivation and reduce unhealthy food intake [
57].
When the group was split by sex analysis showed that the relationships between age and decreasing food cravings were stronger in women compared to men. However, the relationships between eating behaviours and food cravings were not affected by sex. FTO genotype influenced some of the relationships between BMI, age, eating behaviours and food cravings; in particular the inverse relationship between BMI and fatty food craving was stronger in the AA + AT genotype group compared to the TT group. We also saw an effect of the FTO genotype on the relationship between age and emotional eating, with age-related decline in this behavior only present in the AA + AT genotype group.
We split the group into a younger and older age group based on assumptions of life changes that could induce eating behaviours. We observed clear differences between the ≤25 years group compared to the >25 years group. The inverse relationships between CR and EE with food cravings for fatty, sweet and fast foods were much stronger in the ≤25 years group compared to the >25 years group. In the case of the relationship between sweet food cravings and emotional eating there was a negative correlation in the ≤25 years group, but in the >25 years group there was a significant positive correlation. There was also a strong relationship between age and BMI in the >25 years group but not in the ≤25 years group.
We used mediation analysis to investigate these relationships. This showed that in the ≤25 years group for both cravings for fatty food and cravings for sweet food CR mediated almost all of the relationships with BMI, demonstrating that it is very likely that the people in this group with higher BMI are using CR to suppress food cravings. This was in contrast to the >25 years group where this pattern was not seen. In the ≤25 years group sweet cravings were strongly influenced by sex, with a more pronounced inverse relationship between BMI and sweet cravings seen in women. When CR was first investigated as an eating behavior the strong correlation observed between CR and BMI led to the conclusion that CR was a type of unhealthy eating behavior [
4], and that people who restrained were more susceptible to binge eating, thereby leading to increased BMI. Thus, CR as an eating behavior was seen to drive an increase in BMI. However, many early studies were carried out in participants with overweight or obesity and in older demographic groups; in these groups CR may indeed be driving an increase in BMI. In contrast the data presented here supports that in younger age groups BMI may drive CR rather than the other way round, a suggestion which has also been made in other papers [
29,
57]. We have observed the same association between CR and BMI seen in previous studies, but in the ≤25 years group this was particularly associated with a decrease in food cravings. We therefore propose that in people ≤25 years, who are perhaps more self-conscious about their weight, CR is used to suppress food cravings, particularly in people with a raised BMI, hence the association between BMI and CR. This may instill habitual eating behaviours, which in later life increases the susceptibility to the cycles of restraint and binge-eating associated in some older populations with increased BMI [
58]. Evidence to support this theory is provided by Rocks et al. who studied undergraduate students and found that this group, with a similar age and background to our ≤25 years group, demonstrated high dissatisfaction with body weight and high rates of disordered eating behaviours [
59]. An additional possibility is that BMI also mediates the effect of age on eating behaviours and food cravings.
Our study has limitations; although many of the participants were drawn from the same geographical area there may be demographic differences between the ≤25 years group who were mostly undergraduate students, and the >25 years group who were a mixture of staff, students and people from outside the university. In addition the lifestyle and eating habits of the ≤25 years group in our study may not be fully representative of the general population in this age category. As some of the participants were friends and family of the students at the university they may share similar tastes, food preferences and cultural background which may also have influenced the results.
We did not collect detailed data on socio-economic status, education, marriage status or ethnicity in the current study so in future studies these potential confounders will be considered. The division into two age groups with a cut-off of 25 years was based on previous work that shows that life events such co-habiting, employment and having children are associated with changes in eating behaviour [
38,
39,
40]; in our study group the age of 25 reflects a point after which these life events start to have an effect, in future studies collection of data on these variables will allow for their inclusion in the analysis. We chose to examine the effect of
FTO genotype as this has been reported to be the most influential gene on BMI, in the future investigating a wider range of target genes would potentially reveal more information about the influence of genetics on the variables studied. A limitation of the use of self-reported questionnaires is that participants may not always be honest when answering, and the degree to which this is an issue may vary with weight status. In future studies we plan to standardise the conditions under which the questionnaires were completed to minimise this effect, and to incorporate food frequency questionnaires and DEXA analysis into our study protocol.