Sanne Griffioen-Roose

Protein status elicits compensatory changes in food intake and food preferences

Background: Protein is an indispensable component within the human diet. It is unclear, however, whether behavioral strategies exist to avoid shortages. Objective: The objective was to investigate the effect of a low protein status compared with a high protein status on food intake and food preferences. Design: We used a randomized crossover design that consisted of a 14-d fully controlled dietary intervention involving 37 subjects [mean ± SD age: 21 ± 2 y; BMI (in kg/m2): 21.9 ± 1.5] who consumed individualized, isoenergetic diets that were either low in protein [0.5 g protein · kg body weight (BW)−1 · d−1] or high in protein (2.0 g protein · kg BW−1 · d−1). The diets were followed by an ad libitum phase of 2.5 d, during which a large array of food items was available, and protein and energy intakes were measured. Results: We showed that in the ad libitum phase protein intake was 13% higher after the low-protein diet than after the high-protein diet (253 ± 70 compared with 225 ± 63 g, P < 0.001), whereas total energy intake was not different. The higher intake of protein was evident throughout the ad libitum phase of 2.5 d. In addition, after the low-protein diet, food preferences for savory high-protein foods were enhanced. Conclusions: After a protein deficit, food intake and food preferences show adaptive changes that suggest that compensatory mechanisms are induced to restore adequate protein status. This indicates that there are human behavioral strategies present to avoid protein shortage and that these involve selection of savory high-protein foods. This trial was registered with the Dutch Trial register at http://www.trialregister.nl as NTR2491.

Susceptibility to Overeating Affects the Impact of Savory or Sweet Drinks on Satiation, Reward, and Food Intake in Nonobese Women

Taste is involved in food preference and choice, and it is thought that it can modulate appetite and food intake. The present study investigated the effect of savory or sweet taste on satiation, reward, and food intake and according to individual differences in eating behavior traits underlying susceptibility to overeating. In a crossover design, 30 women (BMI = 22.7 ± 2.3; age = 21.9 ± 2.6 y) consumed a fixed energy preload (360 kJ/g) with a savory, sweet, or bland taste before selecting and consuming items from a test meal ad libitum. Sensations of hunger were used to calculate the satiating efficiency of the preloads. A computerized task was used to examine effects on food reward (explicit liking and implicit wanting). The Three Factor Eating Questionnaire was used to compare individual differences in eating behavior traits. Satiation and total food intake did not differ according to preload taste, but there was an effect on explicit liking and food selection. The savory preload reduced liking and intake of high-fat savory foods compared to sweet or bland preloads. The eating behavior trait disinhibition interacted with preload taste to determine test meal intake. Higher scores were associated with increased food intake after the sweet preload compared to the savory preload. Independent of preload taste, disinhibition was associated with lower satiating efficiency of the preloads and enhanced implicit wanting for high-fat sweet food. Savory taste has a stronger modulating effect on food preference than sweet or bland taste and may help to preserve normal appetite regulation in people who are susceptible to overeating.

The effect of within-meal protein content and taste on subsequent food choice and satiety

It is posed that protein intake is tightly regulated by the human body. The role of sensory qualities in the satiating effects of protein, however, requires further clarification. Our objective was to determine the effect of within-meal protein content and taste on subsequent food choice and satiety. We used a cross-over design whereby sixty healthy, unrestrained subjects (twenty-three males and thirty-seven females) with a mean age of 20·8 (SD 2·1) years and a mean BMI of 21·5 (SD 1·6) kg/m2 were offered one of four isoenergetic preloads (rice meal) for lunch: two low in protein (about 7 % energy derived from protein) and two high in protein (about 25 % energy from protein). Both had a sweet and savoury version. At 30 min after preload consumption, subjects were offered an ad libitum buffet, consisting of food products differing in protein content (low/high) and taste (sweet/savoury). In addition, the computerised Leeds Food Preference Questionnaire (LFPQ) was run to assess several components of food reward. The results showed no effect of protein content of the preloads on subsequent food choice. There was an effect of taste; after eating the savoury preloads, choice and intake of sweet products were higher than of savoury products. No such preference was seen after the sweet preloads. No differences in satiety were observed. To conclude, within one eating episode, within-meal protein content in these quantities seems not to have an effect on subsequent food choice. This appears to be mostly determined by taste, whereby savoury taste exerts the strongest modulating effect. The results of the LFPQ provided insight into underlying processes.

Human protein status modulates brain reward responses to food cues

BACKGROUND Protein is indispensable in the human diet, and its intake appears tightly regulated. The role of sensory attributes of foods in protein intake regulation is far from clear. OBJECTIVE We investigated the effect of human protein status on neural responses to different food cues with the use of functional magnetic resonance imaging (fMRI). The food cues varied by taste category (sweet compared with savory) and protein content (low compared with high). In addition, food preferences and intakes were measured. DESIGN We used a randomized crossover design whereby 23 healthy women [mean ± SD age: 22 ± 2 y; mean ± SD body mass index (in kg/m(2)): 22.5 ± 1.8] followed two 16-d fully controlled dietary interventions involving consumption of either a low-protein diet (0.6 g protein · kg body weight(-1) · d(-1), ~7% of energy derived from protein, approximately half the normal protein intake) or a high-protein diet (2.2 g protein · kg body weight(-1) · d(-1), ~25% of energy, approximately twice the normal intake). On the last day of the interventions, blood oxygen level-dependent (BOLD) responses to odor and visual food cues were measured by using fMRI. The 2 interventions were followed by a 1-d ad libitum phase, during which a large array of food items was available and preference and intake were measured. RESULTS When exposed to food cues (relative to the control condition), the BOLD response was higher in reward-related areas (orbitofrontal cortex, striatum) in a low-protein state than in a high-protein state. Specifically, BOLD was higher in the inferior orbitofrontal cortex in response to savory food cues. In contrast, the protein content of the food cues did not modulate the BOLD response. A low protein state also increased preferences for savory food cues and increased protein intake in the ad libitum phase as compared with a high-protein state. CONCLUSIONS Protein status modulates brain responses in reward regions to savory food cues. These novel findings suggest that dietary protein status affects taste category preferences, which could play an important role in the regulation of protein intake in humans. This trial was registered at www.trialregister.nl/trialreg/admin/rctview.asp?TC=3288 as NTR3288.

Satiation Due to Equally Palatable Sweet and Savory Meals Does Not Differ in Normal Weight Young Adults

Sensory properties are greatly involved in the process of satiation. Regarding the nature of sensory signals, an important distinction can be made between sweet and savory taste. It is unclear, however, whether sweet and savory differ in their influence on satiation. Our objective was to investigate the difference between a sweet and savory taste on satiation, independent of palatability, texture, energy density, and macronutrient composition. A crossover design was used, consisting of 3 test conditions in which 2 tastes (sweet and savory) were compared. Sixty-four healthy, nonsmoking, unrestrained participants (18 males and 46 females), with a mean age of 22.3 +/- 2.4 y and a mean BMI of 21.6 +/- 1.7 kg/m(2), enrolled. Rice was used as a test meal served in either a sweet or savory version. The meals were similar in palatability, texture, energy density, and macronutrient composition. Ad libitum intake, eating rate, and changes in pleasantness and appetite during the meals were measured. Ad libitum intake did not differ between the 2 meals; participants ate a mean of 314 +/- 144 g of the sweet meal and 333 +/- 159 g of the savory meal. Eating rate (sweet, 38 +/- 14 g/min; savory, 37 +/- 14 g/min) and changes in pleasantness and appetite during the meals were similar. Homogeneous meals with a sweet or savory taste, similar in palatability, texture, energy density, and macronutrient composition, do not differ in their influence on satiation in normal weight young adults.

Taste of a 24-h diet and its effect on subsequent food preferences and satiety ☆

The objective of this study was to investigate the effect of taste of a 24-h diet on subsequent food preferences (food choice and intake of specific food categories) and satiety. We used a crossover design, consisting of a 24-h fully controlled dietary intervention, during which 39 healthy subjects consumed diets that were predominantly sweet tasting, savory tasting, or a mixture. The diets were similar in energy content, macronutrient composition, and number of different products used. Following the intervention an ad libitum lunch buffet was offered the next day, consisting of food items differing in taste (sweet/savory) and protein content (low/high) and intake was measured. The results showed that the taste of the diet significantly altered preference for food according to their taste properties (p<0.0001); after the savory diet, intake of sweet foods was higher than of savory foods. After the sweet diet, savory foods tended to be preferred (p=0.07). No interaction was seen between the taste of the diet and food preference according to their protein content (p=0.67). No differences in total energy intake (kJ) at the ad libitum lunch buffet were observed (p=0.58). It appears that in healthy subjects, taste of a 24-h diet largely affects subsequent food preferences in terms of sensory appetite, whereby savory taste exerts the strongest modulating effect. Taste of a 24-h diet has no effect on macronutrient appetite.

To like or not to like : Neural substrates of subjective flavor preferences

Flavor preferences vary; what one enjoys may be disgusting to another. Previous research has indicated several brain regions associated with flavor preferences. However, by using different stimuli or different internal states to obtain differences in liking, results of these studies may be confounded. Therefore, we used one target stimulus (grapefruit juice) and fMRI to compare brain activation patterns between participants that either liked (n=16) or disliked (n=18) this stimulus. Our first aim was to investigate whether differential neural activation exists that accounts for the difference in subjective flavor preference for the target stimulus. Secondly, multivariate analysis was used to investigate whether differences in subjective liking for the target revealed similar activation patterns as differences in general liking for a sweet and bitter solution. A direct comparison of likers and dislikers of the target stimulus revealed only small differences in activations in orbitofrontal cortex (OFC) and dorsal anterior cingulate cortex (dACC). However, when using multivariate analysis, a broader activation pattern (including OFC, dACC, pregenual anterior cingulate, anterior insula and ventral striatum) was identified that discriminated likers from dislikers with an 88% success rate. Interestingly though, little overlap was found between this pattern and the pattern that discriminates liking for the sweet and bitter solutions and lesser voxels contributed to the former compared with the latter. These differences between patterns discerning innate versus learned preferences may suggest that different mechanisms are at work and highlight the importance of elucidating the neural processes of how subjective preferences are learned and acquired.

Moderate alcohol consumption stimulates food intake and food reward of savoury foods

The aim of this study was to investigate whether food reward plays a role in the stimulating effect of moderate alcohol consumption on subsequent food intake. In addition, we explored the role of oral and gut sensory pathways in alcohols effect on food reward by modified sham feeding (MSF) or consumption of a preload after alcohol intake.In a single-blind crossover design, 24 healthy men were randomly assigned to either consumption of vodka/orange juice (20 g alcohol) or orange juice only, followed by consumption of cake, MSF of cake or no cake. Food reward was evaluated by actual food intake measured by an ad libitum lunch 45 min after alcohol ingestion and by behavioural indices of wanting and liking of four food categories (high fat, low fat, sweet and savoury).Moderate alcohol consumption increased food intake during the ad libitum lunch by 11% (+338 kJ, P = 0.004). Alcohol specifically increased intake (+127 kJ, P <0.001) and explicit liking (P = 0.019) of high-fat savoury foods. Moreover, moderate alcohol consumption increased implicit wanting for savoury (P = 0.013) and decreased implicit wanting for sweet (P = 0.017) before the meal. Explicit wanting of low-fat savoury foods only was higher after alcohol followed by no cake as compared to after alcohol followed by cake MSF (P = 0.009), but not as compared to alcohol followed by cake consumption (P = 0.082). Both cake MSF and cake consumption had no overall effect on behavioural indices of food reward.To conclude, moderate alcohol consumption increased subsequent food intake, specifically of high-fat savoury foods. This effect was related to the higher food reward experienced for savoury foods. The importance of oral and gut sensory signalling in alcohols effect on food reward remains largely unclear.

Supersize my brain : A cross-sectional voxel-based morphometry study on the association between self-reported dietary restraint and regional grey matter volumes

Restrained eaters do not eat less than their unrestrained counterparts. Proposed underlying mechanisms are that restrained eaters are more reward sensitive and that they have worse inhibitory control. Although fMRI studies assessed these mechanisms, it is unknown how brain anatomy relates to dietary restraint. Voxel-based morphometry was performed on anatomical scans from 155 normal-weight females to investigate how regional grey matter volume correlates with restraint. A positive correlation was found in several areas, including the parahippocampal gyrus, hippocampus, striatum and the amygdala (bilaterally, p<0.05, corrected). A negative correlation was found in several areas, including the inferior frontal gyrus, superior frontal gyrus, supplementary motor area, middle cingulate cortex and precentral gyrus (p<0.05, corrected). That higher restraint relates to higher grey matter volume in reward-related areas and lower grey matter volume in regions involved in inhibition, provides a neuroanatomical underpinning of theories relating restraint to increased reward sensitivity and reduced inhibitory capacity.

Neural Processing of Calories in Brain Reward Areas Can be Modulated by Reward Sensitivity.

A foods reward value is dependent on its caloric content. Furthermore, a foods acute reward value also depends on hunger state. The drive to obtain rewards (reward sensitivity), however, differs between individuals. Here, we assessed the association between brain responses to calories in the mouth and trait reward sensitivity in different hunger states. Firstly, we assessed this in data from a functional neuroimaging study (van Rijn et al., 2015), in which participants (n = 30) tasted simple solutions of a non-caloric sweetener with or without a non-sweet carbohydrate (maltodextrin) during hunger and satiety. Secondly, we expanded these analyses to regular drinks by assessing the same relationship in data from a study in which soft drinks sweetened with either sucrose or a non-caloric sweetener were administered during hunger (n = 18) (Griffioen-Roose et al., 2013). First, taste activation by the non-caloric solution/soft drink was subtracted from that by the caloric solution/soft drink to eliminate sweetness effects and retain activation induced by calories. Subsequently, this difference in taste activation was correlated with reward sensitivity as measured with the BAS drive subscale of the Behavioral Activation System (BAS) questionnaire. When participants were hungry and tasted calories from the simple solution, brain activation in the right ventral striatum (caudate), right amygdala and anterior cingulate cortex (bilaterally) correlated negatively with BAS drive scores. In contrast, when participants were satiated, taste responses correlated positively with BAS drive scores in the left caudate. These results were not replicated for soft drinks. Thus, neural responses to oral calories from maltodextrin were modulated by reward sensitivity in reward-related brain areas. This was not the case for sucrose. This may be due to the direct detection of maltodextrin, but not sucrose in the oral cavity. Also, in a familiar beverage, detection of calories per se may be overruled by a conditioned response to its flavor. In conclusion, the brain reward response to calories from a long chain starch sugar (maltodextrin) varies with trait reward sensitivity. The absence of this effect in a familiar beverage warrants further research into its relevance for real life ingestive behavior.