Human protein status modulates brain reward responses to food cues

Griffioen-Roose, Sanne; Smeets, Paul A.M.; Heuvel, E. van den; Boesveldt, Sanne; Finlayson, Graham; Graaf, C. de

doi:10.3945/ajcn.113.079392

Cited by 71 publications

(66 citation statements)

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“…Other studies have attempted to examine underlying mechanisms for this phenomenon. Some insight might come from recent papers examining the brain's response to savory food cues (Griffioen-Roose et al, 2014). When adults were in a low-protein dietary state, brain response in the inferior orbitofrontal cortex (implicated in emotion and reward-driven decision-making) was higher for savory food odor and visual cues relative to a control condition, and the participants also exhibited a higher preference for savory foods (Griffioen-Roose et al, 2014).…”

Section: Discussionmentioning

confidence: 97%

“…Some insight might come from recent papers examining the brain's response to savory food cues (Griffioen-Roose et al, 2014). When adults were in a low-protein dietary state, brain response in the inferior orbitofrontal cortex (implicated in emotion and reward-driven decision-making) was higher for savory food odor and visual cues relative to a control condition, and the participants also exhibited a higher preference for savory foods (Griffioen-Roose et al, 2014). Additionally, another study found a relationship between a polymorphism in the FTO gene, which has been associated with body mass index and obesity risk, and greater total energy and protein intake, but lower carbohydrate intake (Qi et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

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Intake at a single, palatable buffet test meal is associated with total body fat and regional fat distribution in children

Fearnbach

Torgerson²,

Meyermann

et al. 2015

Appetite

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Previous studies testing the relationship between short-term, ad libitum test-meal intake and body composition in children have shown inconsistent relationships. The objective of this study was to determine whether children's intake at a palatable, buffet meal was associated with body composition, assessed by dual-energy X-ray absorptiometry (DXA). A sample of 71 children (4-6 years) participated in 4 sessions where ad libitum food intake was measured. Children's intake at two of the test-meals was retained for the present analysis: a baseline meal consisting of moderately palatable foods and a highly palatable buffet including sweets, sweet-fats, and savory-fats. On the last visit, anthropometrics and DXA were assessed to determine child body composition. Children consumed significantly more calories at the palatable buffet compared to the baseline test-meal. Children's total fat-free mass was positively associated with intake at both the baseline meal and the palatable buffet meal. Total energy intake at both meals and intake of savory-fats at the palatable buffet were positively associated with children's total fat mass, total percent body fat, and percent android fat. Intake of sweet-fats was associated with child fat-free mass index. Intake of sweets was not correlated with body composition. Children's intake at a palatable test-meal, particularly of savory-fat foods, was associated with measures of total and regional body fat.

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Section: Discussionmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 99%

Intake at a single, palatable buffet test meal is associated with total body fat and regional fat distribution in children

Fearnbach

Torgerson²,

Meyermann

et al. 2015

Appetite

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show abstract

“…Furthermore, a 14-d low-protein diet (0·5 g protein/kg body weight·per d) was found to increase protein intake, wanting, preference for savoury high-protein foods (22) and the neural activation to savoury food cues in brain reward regions (23) compared with a high-protein diet (2·0 g protein/kg body weight per·d). Although these data suggest that dietary macronutrients may also differentially affect food hedonics, the acute effects of macronutrient composition, and in particular dietary fat, on food hedonics has yet to be examined.…”

mentioning

confidence: 93%

Differing effects of high-fat or high-carbohydrate meals on food hedonics in overweight and obese individuals

et al. 2016

Self Cite

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Although the effects of dietary fat and carbohydrate on satiety are well documented, little is known about the impact of these macronutrients on food hedonics. We examined the effects of ad libitum and isoenergetic meals varying in fat and carbohydrate on satiety, energy intake and food hedonics. In all, sixty-five overweight and obese individuals (BMI = 30·9 (SD 3·8) kg/m 2 ) completed two separate test meal days in a randomised order in which they consumed high-fat/low-carbohydrate (HFLC) or low-fat/high-carbohydrate (LFHC) foods. Satiety was measured using subjective appetite ratings to calculate the satiety quotient. Satiation was assessed by intake at ad libitum meals. Hedonic measures of explicit liking (subjective ratings) and implicit wanting (speed of forced choice) for an array of HFLC and LFHC foods were also tested before and after isoenergetic HFLC and LFHC meals. The satiety quotient was greater after ad libitum and isoenergetic meals during the LFHC condition compared with the HFLC condition (P = 0·006 and P = 0·001, respectively), whereas ad libitum energy intake was lower in the LFHC condition (P < 0·001). Importantly, the LFHC meal also reduced explicit liking (P < 0·001) and implicit wanting (P = 0·011) for HFLC foods compared with the isoenergetic HFLC meal, which failed to suppress the hedonic appeal of subsequent HFLC foods. Therefore, when coupled with increased satiety and lower energy intake, the greater suppression of hedonic appeal for high-fat food seen with LFHC foods provides a further mechanism for why these foods promote better short-term appetite control than HFLC foods.Key words: Explicit liking: Implicit wanting: Macronutrient composition: Energy intake: Satiety: Food hedonicsThe role of dietary carbohydrate in the aetiology and treatment of obesity is controversial, with some arguing that carbohydrate intake has a more prominent role in promoting overconsumption and weight gain than dietary fat (1,2) . Although this view has been strongly debated (3) , it has long been established that dietary macronutrients exert a hierarchical effect on appetite-related processes such as satiety and short-term food intake (4) . When expressed relative to energy content rather than weight of food, protein exerts the strongest effect on satiety, followed by carbohydrate, whilst fat exerts the weakest effect (5) . This hierarchical effect has been demonstrated under a variety of laboratory and free-living conditions using subjective measures of appetite, biomarkers of satiety and food intake (6)(7)(8)(9)(10)(11) . However, the underlying metabolic and, in particular, behavioural mechanisms that promote overconsumption following the consumption of energy-dense, high-fat foods are not well understood.The differential effects of dietary macronutrients on satiety may relate to differences in pre-ingestive cognitive and sensory signals generated at the time of consumption (12) and/or the post-ingestive metabolic effects of these foods (13)(14)(15) . However, recent evidence suggests that the...

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“…A corollary to this hypothesis is that a reduction in the dietary protein concentration would increase total energy intake, due to overconsumption of carbohydrates and fat, in an effort to meet protein requirements. Consistent with this, moderately protein deficient diets were found to produce hyperphagia in rodents [6][7][8][9] and in some 1,10,11 but not all human studies 12,13 , whereas, severe protein restriction below a certain threshold leads to a reduction in food intake in rodents 9,14 . However, little is known of the underlying mechanisms by which moderate protein deficiency elicits such behavioural and metabolic adaptations and promotes positive energy balance with consequent predisposition to obesity and other metabolic disorders.…”

mentioning

confidence: 67%

“…Although the low protein-induced hyperphagia is associated with a central orexigenic drive 11,[15][16][17][18] , the peripheral signals that transmit information to central neural networks are poorly defined. To discern potential peripheral mediators, we focussed on circulating concentrations of amino acids, anorexigenic gut hormones, and peripheral serotonergic 5HT3, β -adrenergic and FGF21 signaling.…”

Section: Discussionmentioning

confidence: 99%

0476 Low protein diets produce divergent effects on energy balance

Zapata

Pezeshki

Singh

et al. 2016

Journal of Animal Science

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Diets deficient in protein often increase food consumption, body weight and fat mass; however, the underlying mechanisms remain poorly understood. We compared the effects of diets varying in protein concentrations on energy balance in obesity-prone rats. We demonstrate that protein-free (0% protein calories) diets decreased energy intake and increased energy expenditure, very low protein (5% protein) diets increased energy intake and expenditure, whereas moderately low protein (10% protein) diets increased energy intake without altering expenditure, relative to control diet (15% protein). These diet-induced alterations in energy expenditure are in part mediated through enhanced serotonergic and β-adrenergic signaling coupled with upregulation of key thermogenic markers in brown fat and skeletal muscle. The protein-free and very low protein diets decreased plasma concentrations of multiple essential amino acids, anorexigenic and metabolic hormones, but these diets increased the tissue expression and plasma concentrations of fibroblast growth factor-21. Protein-free and very low protein diets induced fatty liver, reduced energy digestibility, and decreased lean mass and body weight that persisted beyond the restriction period. In contrast, moderately low protein diets promoted gain in body weight and adiposity following the period of protein restriction. Together, our findings demonstrate that low protein diets produce divergent effects on energy balance.The consumption of protein triggers adaptive responses in ingestive behavior, energy expenditure and metabolism that are under homeostatic controls. The 'protein leverage' hypothesis posits that protein intake is tightly regulated in several species including rats, mice and humans, which consume to acquire their required protein rather than meet requirements for fats and carbohydrates [1][2][3] . An increase in dietary protein density would decrease intake of carbohydrates and fats with consequent reduction in energy intake. There is substantial evidence that high protein diets promote satiety, weight loss and improve glycemic control 4,5 . A corollary to this hypothesis is that a reduction in the dietary protein concentration would increase total energy intake, due to overconsumption of carbohydrates and fat, in an effort to meet protein requirements. Consistent with this, moderately protein deficient diets were found to produce hyperphagia in rodents 6-9 and in some 1,10,11 but not all human studies 12,13 , whereas, severe protein restriction below a certain threshold leads to a reduction in food intake in rodents 9,14 . However, little is known of the underlying mechanisms by which moderate protein deficiency elicits such behavioural and metabolic adaptations and promotes positive energy balance with consequent predisposition to obesity and other metabolic disorders.The hyperphagic effects of moderately low protein diets are purported to be through multiple mechanisms. These include imbalances in plasma and brain amino acid concentrations in rats [15][16][17] ,...

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Human protein status modulates brain reward responses to food cues

Cited by 71 publications

References 36 publications

Intake at a single, palatable buffet test meal is associated with total body fat and regional fat distribution in children

Intake at a single, palatable buffet test meal is associated with total body fat and regional fat distribution in children

Differing effects of high-fat or high-carbohydrate meals on food hedonics in overweight and obese individuals

0476 Low protein diets produce divergent effects on energy balance

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