Exercise Training Reduces Reward for High-Fat Food in Adults With Overweight/Obesity

Kristine Beaulieu; Mark Hopkins; Catherine Gibbons; Pauline Oustric; Phillipa Caudwell; John Blundell; Grahamfinlayson

Disclosures

Med Sci Sports Exerc. 2020;52(4):900-908. 

In This Article

Discussion

This study examined the impact of a 12-wk supervised exercise intervention on state measures of food reward and trait characteristics of susceptibility to overeating in inactive individuals with overweight and obesity compared with nonexercising controls under conditions of HFAT and HCHO feeding. The 12-wk intervention led to improvements in body composition and fitness in exercisers, whereas there was a small increase in adiposity in controls. The mean group (exercisers–controls) differences in body weight and waist circumference were small but clinically meaningful according to agreed guidelines on obesity management[23] In exercisers, there was a reduction in food reward (specifically wanting) that was accompanied by improvements in eating behavior traits (clearly for binge eating and weakly for disinhibition), whereas no changes were apparent in controls.

The Impact of Exercise Training on Food Reward. In the current study, a 12-wk exercise intervention led to a small reduction in wanting scores for high-fat relative to low-fat foods in exercisers compared with controls, but no differences in liking were found. Differences in food reward between exercisers and controls suggested that liking and wanting were generally lower in exercisers than in controls, but this effect was small and the variability was high. The group differences were more apparent in the ITT analyses, where a larger sample size and power strengthened the analysis. The changes in wanting in the exercisers from positive toward negative values indicated greater wanting scores for low-fat relative to high-fat foods after the exercise intervention. Although this reduction in wanting scores for high-fat foods was accompanied by a small reduction in intake at an ad libitum dinner test meal in the high-fat condition (~544 kJ; data not reported in the current article),[28] overall HFAT daily intake remained unchanged after the exercise intervention. The reduction in wanting observed in the current study may not have been large enough to elicit meaningful changes in food intake, but provides insight for a potential mechanistic influence of exercise (with modest weight loss) on food reward, specifically wanting. It is also important to consider that the design of the probe meal days[1] contained two fixed meals, and thus, if all test meals had been ad libitum, perhaps larger effects on energy intake may have been observed (given that a small reduction was seen at the dinner meal), and[2] did not allow for choices between high-fat and low-fat foods to be made, as each probe day was specifically designed to contain either HFAT or HCHO foods. Therefore, future studies assessing reward for high-fat versus low-fat (or sweet vs savory/nonsweet) foods in response to exercise should also include a food choice component to the assessment of food intake with ad libitum test meals including foods varying in fat content/taste.

Furthermore, on an individual level, we have shown that an increase in food liking and wanting (particularly of high-fat foods) in response to acute exercise led to less-than-expected weight loss during a prior 12-wk exercise intervention.[7] This suggests a role for food reward in the compensatory eating response to exercise. Indeed, this may be related to changes in between-network connectivity occurring in the brain, specifically between the posterior cingulate cortex and a visuospatial network, with chronic exercise, as these have been found to be associated with changes in susceptibility to hunger assessed by the TFEQ.[29]

We have recently shown in a systematic review that reward for high-fat/energy food generally decreases after weight management interventions including a range of modes of weight loss.[6] The review found limited available evidence on exercise interventions; therefore, this study adds to the sparse literature in this area. Future studies could examine characteristics of exercise interventions (e.g., frequency, intensity, type, duration, and timing) that could potentially have a larger effect on reward, eating behavior, and food intake/choices than the effects demonstrated in the current study.

Cross-sectional differences in the reward value of foods (liking and wanting) have been observed in active compared with inactive men who differed in BMI,[30] whereas in individuals with similar BMI (healthy range), level of habitual physical activity did not seem to influence food reward.[31,32] Other studies using functional magnetic resonance imaging have found a reduction in the neural response to food cues with greater levels of habitual physical activity[33] and after exercise training,[12] with inconsistencies regarding the role of body fat loss or status in the responses observed. In individuals with overweight and obesity, a 6-month exercise training intervention was associated with attenuated neural response to food cues despite no effect on behavioral measures of appetite, raising the question of whether exercise could improve weight management through attenuated hedonic motivation to eat.[12] Interestingly, changes in the default mode network activity (reflecting an individual's internal mental state) during this 6-month intervention was positively associated with changes in fat mass as well as hunger (measured via TFEQ and in response to a test meal).[34]

In contrast to functional magnetic resonance imaging, the LFPQ methodology allows for a quantified behavioral assessment of food reward. Interestingly, in a study conducted in inactive individuals with overweight and obesity, 12 wk of exercise training (523–1046 kJ, 3 d·wk−1) did not affect liking or wanting scores measured by the LFPQ,[8] whereas the 12-wk intervention in the current study, at a higher dose of exercise (2092 kJ, 5 d·wk−1), reduced the wanting scores for high-fat food relative to nonexercising controls. The potential effects of exercise training dose (and other parameters of exercise such as those mentioned previously) on food reward warrant further investigation. Moreover, future studies combining the LFPQ with measures of neural activation[12] and changes in food intake would provide convincing evidence of the potency and specificity of exercise on food reward.

The major innovative aspect of this current study is that exercise training affected wanting rather than liking for high-fat foods. However, this effect was small and the clinical relevance for weight management cannot be determined. Wanting may be interpreted as the anticipatory reward (i.e., motivation or desire to eat before the consumption), whereas liking is the pleasure to eat.[35] It could be hypothesized that exercise affects wanting more than liking, as exercise has an indirect effect on dietary habits and rather affects cognition and executive function.[36] This strengthening of cognitive processes such as inhibitory control would be expected to have an effect on wanting rather than liking for high-fat food.[36] On the contrary, diet interventions may have a greater effect on liking, as they are directly manipulating food patterns. In a recent systematic review, three dietary interventions reduced liking; however, wanting was not measured in these studies.[6] Our study demonstrates that, in assessing effects on food reward, it is necessary to measure both liking and wanting as differing responses may be seen. We show beneficial effects of exercise on the hedonic motivation to eat through a small reduction in wanting scores for high-fat relative to low-fat foods, but not liking. Changes in food reward did not seem to be associated with changes in body weight; however, associations between fasting leptin and food reward in response to exercise training have previously been shown with or without controlling for body fat.[9] It remains unknown whether the influence of chronic exercise on wanting is due to improvements in cognitive processes, to a modulation of the brain reward system or to other mechanisms. A better understanding of the neurocognitive effect of exercise and its relationship with food reward and eating behaviors is needed. It is also important to acknowledge, as shown in Figure 1, that large individual variability in the food reward responses existed, and more studies should be conducted to identify the reasons for such differences.

Exercise Training and Eating Behaviors Promoting Overconsumption

Regarding the assessment of eating behavior traits, a week–group interaction showed that binge eating decreased in exercisers in response to the exercise intervention, whereas no changes were observed in controls. Disinhibition also showed a small decrease in exercisers, with a weaker week–group interaction, but corroborates an earlier exercise training study from our group that also found a reduction in disinhibition.[10] Interestingly, the changes in eating behaviors in that study were more pronounced in those who lost more weight compared with those who lost less weight in response to the exercise intervention.[10]

Cross-sectional studies in lean individuals matched for BMI ranging in physical activity levels suggest little influence of physical activity on eating behavior traits.[31,32] However, across a larger range of BMI, negative associations were observed between time spent in moderate-to-vigorous physical activity and disinhibition and binge eating, but these weakened after controlling for body fat,[37] and also a study by Shook et al.[38] found greater disinhibition in their lowest quintile of moderate-to-vigorous physical activity but not when controlling for body weight. Further evidence examining the effects of exercise on other trait markers of susceptibility to overeating is inconsistent, with a 6-month exercise training study reporting no effect on food cravings,[12] whereas another study suggested that physical activity could modulate craving control.[39] This latter study showed that individuals who increased total exercise time over a 1-yr free-living period had a reduction in the difficulty to resist food cravings.[39]

This could mean that the effect of chronic exercise and habitual physical activity on trait measures of susceptibility to overeating may be more influenced by or dependent on body weight/composition. Indeed, in the current study, changes in eating behaviors were associated with changes in body weight (more strongly in the whole group than in the exercisers alone). In contrast, food liking and wanting are considered as more state dependent, with acute exercise able to modulate short-term food reward responses,[7,40] and did not seem to be influenced by changes in body weight. The effects of chronic exercise and body weight/composition on trait and state markers of overeating remain to be fully understood.

Furthermore, it has been suggested that chronic exercise may reduce binge eating through a mechanistic effect on the reward system.[11] In the current study, correlational analyses suggested potential associations between changes in wanting and changes in trait binge eating in the whole sample; however, the uncertainty in our data does not allow for any conclusions to be made at this time regarding the effect of exercise on this relationship. Clearly, more work is needed to elucidate the effect of chronic exercise on the food reward and neurocognitive systems as well as on psychological eating behavior traits.

Liking and Wanting in Response to HFAT and HCHO Feeding Conditions. Prior baseline analyses of the current study showed that not only are high-fat (and energy-dense) foods less satiating than HCHO foods (lower satiety quotient response) and lead to an overconsumption of energy, but also consumption of these foods modulates liking and wanting.[15] In the present study and in line with our previous findings,[15] we show that regardless of the exercise intervention, liking and wanting scores for high-fat relative to low-fat foods were dependent on the composition of the foods consumed. Moreover, the composition of the food consumed interacted with the hunger state of the participants, showing a greater liking and wanting scores after consumption of HFAT foods compared with HCHO foods (for wanting, this effect was more prominent in the controls). However, food composition did not interact with the reward responses to exercise training. This emphasizes the importance of the energy density of the diet in determining both homeostatic (satiety and energy intake) and food reward (liking and wanting) responses. It also suggests that exercise-induced improvements in appetite control are unlikely to (on their own) overcome the overconsumption of energy typically seen with high-fat foods, as the palatable nature of energy-dense foods can offset homeostatic satiation and satiety signals.[13]

Limitations. Despite the present study being among the few in this area to include a nonexercising control group, the relatively small number of controls compared with exercisers adds some additional uncertainty (i.e., increased size of CI) to the study outcomes. In addition, this study was not a randomized controlled trial; exercisers and controls were recruited separately. Although the exercise intervention in exercisers was supervised and closely monitored for adherence, no free-living exercise or food intake data were collected in the controls to confirm that they had not changed their behavior during the 12 wk. Furthermore, the menstrual cycle of female participants was not considered and may have affected the appetite responses. However, because the study was 12 wk in duration, the female participants should have been in the same phase of their cycle at both baseline and postintervention measures days. The interrelationships between exercise and changes in body composition make it difficult to tease out specific contributors (whether direct or indirect) to the changes in appetite observed in the current study. A future study design could attempt to control body weight during exercise training with a systematic dietary protocol or compare well-defined subgroups of weight loss responders and nonresponders to exercise with a nonexercise control group.

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