Beneficial effects of a higher-protein breakfast on the appetitive, hormonal, and neural signals controlling energy intake regulation in overweight/obese, "breakfast-skipping," late-adolescent girls

Abstract

Background: Breakfast skipping is a common dietary habit practiced among adolescents and is strongly associated with obesity.

Objective: The objective was to examine whether a high-protein (HP) compared with a normal-protein (NP) breakfast leads to daily improvements in appetite, satiety, food motivation and reward, and evening snacking in overweight or obese breakfast-skipping girls.

Design: A randomized crossover design was incorporated in which 20 girls [mean ± SEM age: 19 ± 1 y; body mass index (in kg/m(2)): 28.6 ± 0.7] consumed 350-kcal NP (13 g protein) cereal-based breakfasts, consumed 350-kcal HP egg- and beef-rich (35 g protein) breakfasts, or continued breakfast skipping (BS) for 6 d. On day 7, a 10-h testing day was completed that included appetite and satiety questionnaires, blood sampling, predinner food cue-stimulated functional magnetic resonance imaging brain scans, ad libitum dinner, and evening snacking.

Results: The consumption of breakfast reduced daily hunger compared with BS with no differences between meals. Breakfast increased daily fullness compared with BS, with the HP breakfast eliciting greater increases than did the NP breakfast. HP, but not NP, reduced daily ghrelin and increased daily peptide YY concentrations compared with BS. Both meals reduced predinner amygdala, hippocampal, and midfrontal corticolimbic activation compared with BS. HP led to additional reductions in hippocampal and parahippocampal activation compared with NP. HP, but not NP, reduced evening snacking of high-fat foods compared with BS.

Conclusions: Breakfast led to beneficial alterations in the appetitive, hormonal, and neural signals that control food intake regulation. Only the HP breakfast led to further alterations in these signals and reduced evening snacking compared with BS, although no differences in daily energy intake were observed. These data suggest that the addition of breakfast, particularly one rich in protein, might be a useful strategy to improve satiety, reduce food motivation and reward, and improve diet quality in overweight or obese teenage girls. This trial was registered at clinicaltrials.gov as NCT01192100.

FIGURE 1.

Diagram of the 10-h testing day procedures. MU, University of Missouri; NP, normal protein.

FIGURE 2.

Perceived hunger (A) and fullness (B) responses throughout the testing days in 20 adolescent girls. The line graph displays the time course of change throughout the 10-h days in the BS (□), NP (△), and HP (•) patterns; the bar graphs depict total and specific time segment AUCs across the day. Post hoc pairwise comparison analyses were performed when main effects and interactions were detected. Different lowercase letters denote significance (P < 0.05) between testing days. The △ on the x-axis denotes the breakfast meal; the ▴ on the x-axis denotes the lunch meal. BS, breakfast skipping; HP, high protein; NP, normal protein.

FIGURE 3.

Desire to eat (A) and preoccupation with thoughts of food (B) throughout the testing days in 20 adolescent girls. The line graph displays the time course of change throughout the 10-h days in the BS (□), NP (△ ), and HP (•) patterns; the bar graphs depict total and specific time segment AUCs across the day. Post hoc pairwise comparison analyses were performed when main effects and interactions were detected. Different lowercase letters denote significance between testing days (P < 0.05). The △ on the x-axis denotes the breakfast meal; the ▴ on the x-axis denotes the lunch meal. BS, breakfast skipping; HP, high protein; NP, normal protein; PFC, prospective food consumption.

FIGURE 4.

Ghrelin (A) and PYY (B) responses throughout the testing days in 20 adolescent girls. The line graph displays the time course of change throughout the 10-h days in the BS (□), NP (△ ), and HP (•) patterns; the bar graphs depict total and specific time segment AUCs across the day. Post hoc pairwise comparison analyses were performed when main effects and interactions were detected. Different lowercase letters denote significance between testing days (P < 0.05). The △ on the x-axis denotes the breakfast meal; the ▴ on the x-axis denotes the lunch meal. BS, breakfast skipping; HP, high protein; NP, normal protein; PYY, peptide YY.

FIGURE 5.

(A, B) Brain activation contrast maps before dinner after the BS, NP, and HP testing days in 20 adolescent girls; all contrasts represent food greater than nonfood (animal) fMRI scans. Repeated-measures ANOVA examining the main effect of treatment with post hoc pairwise comparison analyses were performed when a main effect was detected. P < 0.01 represented significance. BS, breakfast skipping; COR, coronal view; HP, high protein; NP, normal protein.

FIGURE 6.

Energy intake throughout each testing day in 20 adolescent girls. Different lowercase letters denote significance when comparing BS (□), NP (▪), and HP (▪) breakfasts (P < 0.05). Repeated-measures ANOVA examining the main effect of treatment with post hoc pairwise comparison analyses was performed when a main effect was detected. BS, breakfast skipping; HP, high protein; NP, normal protein.