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GLP-1 and hunger modulate incentive motivation depending on insulin sensitivity in humans.
Hanssen, R, Kretschmer, AC, Rigoux, L, Albus, K, Edwin Thanarajah, S, Sitnikow, T, Melzer, C, Cornely, OA, Brüning, JC, Tittgemeyer, M
Molecular metabolism. 2021;:101163
Abstract
OBJECTIVE To regulate food intake, our brain constantly integrates external cues, such as the incentive value of a potential food reward, with internal state signals, such as hunger feelings. Incentive motivation refers to the processes that translate an expected reward into the effort spent to obtain the reward; the magnitude and probability of a reward involved in prompting motivated behaviour are encoded by the dopaminergic (DA) midbrain and its mesoaccumbens DA projections. This type of reward circuity is particularly sensitive to the metabolic state signalled by peripheral mediators, such as insulin or glucagon-like peptide 1 (GLP-1). While in rodents the modulatory effect of metabolic state signals on motivated behaviour is well documented, evidence of state-dependent modulation and the role of incentive motivation underlying overeating in humans is lacking. METHODS In a randomised, placebo-controlled, crossover design, 21 lean (body mass index [BMI] < 25 kg/m2) and 16 obese (BMI³ 30 kg/m2) volunteer participants received either liraglutide as a GLP-1 analogue or placebo on two separate testing days. Incentive motivation was measured using a behavioural task in which participants were required to exert physical effort using a handgrip to win different amounts of food and monetary rewards. Hunger levels were measured using visual analogue scales; insulin, glucose, and systemic insulin resistance as assessed by the homeostasis model assessment of insulin resistance (HOMA-IR) were quantified at baseline. RESULTS In this report, we demonstrate that incentive motivation increases with hunger in lean humans (F(1,42) = 5.31, p = 0.026, β = 0.19) independently of incentive type (food and non-food reward). This effect of hunger is not evident in obese humans (F(1,62) = 1.93, p = 0.17, β = -0.12). Motivational drive related to hunger is affected by peripheral insulin sensitivity (two-way interaction, F(1, 35) = 6.23, p = 0.017, β = -0.281). In humans with higher insulin sensitivity, hunger increases motivation, while poorer insulin sensitivity dampens the motivational effect of hunger. The GLP-1 analogue application blunts the interaction effect of hunger on motivation depending on insulin sensitivity (three-way interaction, F(1, 127) = 5.11, p = 0.026); no difference in motivated behaviour could be found between humans with normal or impaired insulin sensitivity under GLP-1 administration. CONCLUSION We report a differential effect of hunger on motivation depending on insulin sensitivity. We further revealed the modulatory role of GLP-1 in adaptive, motivated behaviour in humans and its interaction with peripheral insulin sensitivity and hunger. Our results suggest that GLP-1 might restore dysregulated processes of midbrain DA function and hence motivational behaviour in insulin-resistant humans.
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The endocrine effects of bitter tastant administration in the gastrointestinal system: intragastric versus intraduodenal administration.
Verbeure, W, Deloose, E, Tóth, J, Rehfeld, JF, Van Oudenhove, L, Depoortere, I, Tack, J
American journal of physiology. Endocrinology and metabolism. 2021;(1):E1-E10
Abstract
Bitter tastants are recently introduced as potential hunger-suppressive compounds, the so-called "Bitter pill." However, the literature about bitter administration lacks consistency in methods and findings. We want to test whether hunger ratings and hormone plasma levels are affected by: 1) the site of administration: intragastrically (IG) or intraduodenally (ID), 2) the bitter tastant itself, quinine hydrochloride (QHCl) or denatonium benzoate (DB), and 3) the timing of infusion. Therefore, 14 healthy, female volunteers participated in a randomized, placebo-controlled six-visit crossover study. After an overnight fast, DB (1 µmol/kg), QHCl (10 µmol/kg), or placebo were given IG or ID via a nasogastric feeding tube. Blood samples were taken 10 min before administration and every 10 min after administration for a period of 2 h. Hunger was rated at the same time points on a visual analogue scale. ID bitter administration did not affect hunger sensations, motilin, or acyl-ghrelin release compared with its placebo infusion. IG QHCl infusion tended to suppress hunger increase, especially between 50 and 70 min after infusion, simultaneously with reduced motilin values. Here, acyl-ghrelin was not affected. IG DB did not affect hunger or motilin, however acyl-ghrelin levels were reduced 50-70 minutes after infusion. Plasma values of glucagon-like peptide 1 and cholecystokinin were too low to be properly detected or to have any physiological relevance. In conclusion, bitter tastants should be infused into the stomach to reduce hunger sensations and orexigenic gut peptides. QHCl has the best potential to reduce hunger sensations, and it should be infused 60 min before food intake.NEW & NOTEWORTHY Bitter tastants are a potential new weight-loss treatment. This is a noninvasive, easy approach, which should be received with considerable enthusiasm by the public. However, literature about bitter administration lacks consistency in methods and findings. We summarize how the compound should be given based on: the site of administration, the best bitter compound to use, and at what timing in respect to the meal. This paper is therefore a fundamental step to continue research toward the further development of the "bitter pill."
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Effects of intranasal oxytocin in food intake and craving: A meta-analysis of clinical trials.
Chen, CY, Chiang, YC, Kuo, TC, Tam, KW, Loh, EW
Clinical nutrition (Edinburgh, Scotland). 2021;(10):5407-5416
Abstract
OBJECTIVE A rise of endogenous oxytocin (OT) is associated with anxiety and meal size reduction, and the effects of intranasal OT (INOT) have been examined in the management of food intake and craving. However, the discrepancy INOT effects in different disease populations are not entirely clear. RESEARCH DESIGN AND METHODS Updated systematic review and meta-analysis. By systematically searching the PubMed, Embase and Cochrane Library, we obtained 12 controlled trials. We performed meta-analyses to examine food intake, craving, anxiety or stress reduction on INOT administration, using standard mean difference (SMD) with a 95% confidence interval (CI) and a random-effects model. RESULTS This study examined 12 trials with 266 non-psychiatric and 157 psychiatric participants. The pooled results showed that single-dose INOT induced a significant lesser food intake in non-psychiatric subjects (SMD: -0.66 [95% CI: -1.18, -0.14]), but no effects was found in anorexia nervosa (AN) (SMD: 0.17 [95% CI: -0.32, 0.66]), bulimia nervosa (BN) and binge eating disorder (BED) (SMD: -0.41 [95% CI: -0.94, 0.11]), and schizophrenia (SMD: 0.04 [95% CI: -0.94, 1.02] subjects. Further analysis on leisure food also indicated an inhibition of consumption of chocolate biscuits in non-psychiatric subjects. Neither the non-psychiatric (SMD: -0.08 [95% CI: -0.50, 0.33]) nor the BN and BED (SMD: -0.08 [95% CI: -0.72, 0.88]) and schizophrenia subjects (SMD: -0.07 [95% CI: -1.05, 0.91]) demonstrated a difference in food craving or hunger compared with placebo. Anxiety or stress level was not influenced by INOT in any subgroup (non-psychiatric, SMD: 0.19 [95% CI: -0.22, 0.60]; AN, SMD: -0.01 [95% CI: -0.28, 0.88]; BN and BED: SMD: 0.00 [95% CI: -0.80, 0.80]). CONCLUSIONS Single-dose INOT significantly reduces food intake in nonpsychiatric subjects, and further studies are necessary to assess the long-term effects and safety in obese patients. Whether INOT could be a treatment option for patients with eating disorders remains to be investigated.
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The Hunger Games: Homeostatic State-Dependent Fluctuations in Disinhibition Measured with a Novel Gamified Test Battery.
Voigt, K, Giddens, E, Stark, R, Frisch, E, Moskovsky, N, Kakoschke, N, Stout, JC, Bellgrove, MA, Andrews, ZB, Verdejo-Garcia, A
Nutrients. 2021;(6)
Abstract
Food homeostatic states (hunger and satiety) influence the cognitive systems regulating impulsive responses, but the direction and specific mechanisms involved in this effect remain elusive. We examined how fasting, and satiety, affect cognitive mechanisms underpinning disinhibition using a novel framework and a gamified test-battery. Thirty-four participants completed the test-battery measuring three cognitive facets of disinhibition: attentional control, information gathering and monitoring of feedback, across two experimental sessions: one after overnight fasting and another after a standardised meal. Homeostatic state was assessed using subjective self-reports and biological markers (i.e., blood-derived liver-expressed antimicrobial protein 2 (LEAP-2), insulin and leptin). We found that participants who experienced greater subjective hunger during the satiety session were more impulsive in the information gathering task; results were not confounded by changes in mood or anxiety. Homeostatic state did not significantly influence disinhibition mechanisms linked to attentional control or feedback monitoring. However, we found a significant interaction between homeostatic state and LEAP-2 on attentional control, with higher LEAP-2 associated with faster reaction times in the fasted condition only. Our findings indicate lingering hunger after eating increases impulsive behaviour via reduced information gathering. These findings identify a novel mechanism that may underpin the tendency to overeat and/or engage in broader impulsive behaviours.
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Hedonic Hunger Is Associated with Intake of Certain High-Fat Food Types and BMI in 20- to 40-Year-Old Adults.
Chmurzynska, A, Mlodzik-Czyzewska, MA, Radziejewska, A, Wiebe, DJ
The Journal of nutrition. 2021;(4):820-825
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Abstract
BACKGROUND Hedonic hunger occurs in response to a desire to consume food for pleasure. The μ-opioid system regulates the hedonic impact of food and the opioid receptor mu 1 gene (OPRM1) polymorphism has been associated with fat intake. OBJECTIVES The aim of this study was to determine whether the intake of high-fat food is associated with hedonic hunger and the OPRM1 polymorphism and whether these variables are related to BMI. METHODS Participants were 20- to 40-y-old women and men enrolled in Poznań, Poland in 2016-2018. The frequency of consumption of high-fat food was measured using a validated application for mobile devices. Hedonic hunger was assessed with the use of the Power of Food Scale (PFS). PFS1, PFS2, and PFS3 scores were generated for food available, food present, and food tasted, respectively. Genotyping of rs1799971 in the OPRM1 gene was performed using TaqMan probes. The associations were analyzed using linear regression or logistic regression, as appropriate. RESULTS Hedonic hunger scores were not associated with total high-fat food intake. Total PFS was associated with snack intake (β: 0.16, P = 0.0066). PFS1 was positively associated with healthy high-fat food intake (β: 0.27, P = 0.0001) and PFS2 with sweet high-fat food and fast-food intake (β: 0.27, P = 0.0030). OPRM1 genotype and hedonic hunger interacted on fast-food intake (β: -0.17; P < 0.0154). Total PFS and PFS2 increased the chance of having a BMI ≥ 25 kg/m2 (OR: 1.43; 95% CI: 1.03, 2.01; P = 0.0335 and OR: 1.89; 95% CI: 1.37, 2.61; P = 0.0001, respectively), whereas PFS3 decreased it (OR: 0.61; 95% CI: 0.41, 0.87; P = 0.0082). CONCLUSIONS Hedonic hunger is associated with the intake of selected types of high-fat food, but not with its total intake, in people aged 20-40 y. Associations between hedonic hunger and fast-food intake can be modified by OPRM1 genotype. Hedonic hunger is associated with BMI.
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Virtual grocery shopping and cookie consumption following intranasal insulin or placebo application.
Rodriguez-Raecke, R, Sommer, M, Brünner, YF, Müschenich, FS, Sijben, R
Experimental and clinical psychopharmacology. 2020;(4):495-500
Abstract
Insulin receptors are present in brain areas that are involved in the control of hunger and satiety, and intranasal insulin is assumed to have an anorexigenic effect. This known influence of insulin on satiety encouraged us to investigate the effect of intranasal insulin on feeding-related behaviors. The aim of the current study was to explore the influence of 40 IU of intranasal insulin on the grocery shopping behavior and cookie consumption in a group of 30 healthy young men, using a crossover randomized double-blind design. Using a virtual mock supermarket, we tested whether the intranasal administration of insulin influences purchase behavior in comparison to a placebo or control condition. The participants also provided hedonic ratings of food pictures, as well as their subjective feeling of hunger. We calculated an objective measure of hunger from the amount of cookies eaten. In contradiction to our hypotheses, no significant differences regarding ratings, calorie content of purchased food products, and cookie consumption were found between the treatment conditions. Our conclusion is that 40 IU intranasal insulin had no influence on the evaluation of pictured foods in healthy young men in our task. Acknowledging that previous studies have found effects for intranasal insulin and food cue processing, we suggest that future research should focus on chemosensory stimulation or cognitive tasks in behavioral experiments and carefully consider the doses of intranasal insulin. (PsycInfo Database Record (c) 2020 APA, all rights reserved).
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Changes in weight control behaviors and hedonic hunger in a commercial weight management program adapted for individuals with type 2 diabetes.
Schulte, EM, Tuerk, PW, Wadden, TA, Garvey, WT, Weiss, D, Hermayer, KL, Aronne, LJ, Becker, LE, Fujioka, K, Miller-Kovach, K, et al
International journal of obesity (2005). 2020;(5):990-998
Abstract
BACKGROUND A WW (formerly Weight Watchers) program adapted for persons with type 2 diabetes mellitus (T2DM) previously was found to be more effective than standard care (SC) intervention for weight loss, improved glycemic control, and weight- and diabetes-related quality of life measures. With data from the same national trial, this study examined whether WW adapted for persons with T2DM also increased engagement in weight control behaviors and decreased hedonic hunger, each of which could contribute to improved diabetes management. INTERVENTION AND METHODS Individuals with T2DM (n = 563) and overweight or obesity participated in a 12-month, 16-site, randomized trial of WW with diabetes counseling or SC. Hierarchical linear modeling (HLM) evaluated whether 12-month changes in weight control behaviors (Eating Behavior Inventory; EBI) and hedonic hunger (Power of Food Scale; PFS) differed by treatment condition. If a significant treatment effect was found, 12-month changes in EBI/PFS were regressed on 12-month changes in HbA1c and percent weight loss to explore potential treatment differences in these associations. RESULTS EBI scores increased significantly over the 12-months (p < 0.001), with greater improvements in WW than SC (p < 0.001). PFS decreased significantly in the 12-months (p < 0.001), with no differences between treatment groups (p = 0.15). HLM analyses that followed up on the significant treatment effect for 12-month change in EBI revealed no significant differences by treatment condition for the relationship between change in EBI scores and change in HbA1c (p = 0.14) or percent weight loss (p = 0.32). Across all participants, 12-month improvements in EBI and PFS were related to improved HbA1c (r = 0.22; -0.13, respectively) and greater percent weight loss (r = 0.41; -0.18, respectively) (ps < 0.01). CONCLUSIONS WW with diabetes counseling produced greater engagement in weight control behaviors in those with T2DM than did SC. Across both groups, improved weight control behaviors and hedonic hunger were related to improved glycemic control and weight loss.
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Effects of liraglutide on appetite, food preoccupation, and food liking: results of a randomized controlled trial.
Tronieri, JS, Wadden, TA, Walsh, O, Berkowitz, RI, Alamuddin, N, Gruber, K, Leonard, S, Bakizada, ZM, Chao, AM
International journal of obesity (2005). 2020;(2):353-361
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BACKGROUND Some weight loss medications, including liraglutide 3.0 mg, are thought to facilitate weight loss by improving appetite control. However, no studies have evaluated their long-term appetitive effects. SUBJECTS/METHODS This study examined changes in appetite in a subsample of 113 adults with obesity (76.1% female, 55.8% white, BMI = 38.8 ± 4.8 kg/m2) who participated in a 52-week trial. Participants were randomized to intensive behavioral therapy alone (IBT-alone), IBT with liraglutide 3.0 mg/day (IBT-liraglutide), or IBT-liraglutide combined with a 12-week meal replacement diet (Multi-component). Participants rated their hunger, fullness after meals, liking of meals, and food preoccupation (all as experienced over the past week) using visual analogue scales (0-100 mm). Ratings were completed at baseline and eight subsequent visits over the year. RESULTS At week 52, participants treated by IBT-alone lost 6.2 ± 1.6% of baseline weight, compared with 11.8 ± 1.6% and 12.1 ± 1.5% in the IBT-liraglutide and Multi-component groups, respectively. Compared to IBT-alone, IBT-liraglutide participants reported larger reductions at week 6 in hunger (-0.3 ± 4.2 vs -16.8 ± 4.0 mm, p = .005) and food preoccupation (+0.2 ± 3.7 vs -16.3 ± 3.6 mm, p = .002) and larger increases in fullness (-5.1 ± 3.2 vs +9.8 ± 3.0 mm, p = .001). These significant differences persisted at all assessments through week 24. There were no differences between IBT-alone and IBT-liraglutide in meal liking. IBT-alone and Multi-component participants differed in hunger at week 6, and in food preoccupation at all assessments through week 24. Multi-component participants reported reduced liking of meals relative to the IBT-alone and IBT-liraglutide groups through weeks 40 and 52, respectively. There were no other differences among any groups at week 52. CONCLUSIONS Consistent with short-term studies, IBT-liraglutide participants reported greater improvements in hunger, fullness, and food preoccupation than those assigned to IBT-alone. Differences in appetite persisted for 24 weeks but were not maintained at week 52, despite the relatively greater weight losses in the liraglutide-treated participants at the trial's end.
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A Laboratory-Based Study of the Priming Effects of Food Cues and Stress on Hunger and Food Intake in Individuals with Obesity.
Chao, AM, Fogelman, N, Hart, R, Grilo, CM, Sinha, R
Obesity (Silver Spring, Md.). 2020;(11):2090-2097
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Abstract
OBJECTIVE This study aimed to assess the effects of exposures to food cues and stress on hunger and food intake and examine whether cue responses differ by weight status. METHODS In a laboratory-based experimental study, participants (n = 138) were exposed to stress, neutral, and food cues delivered using an individualized script-driven imagery task on three separate days. After each cue exposure, participants ate high- and low-calorie snack foods ad libitum (Food Snack Test). Hunger was measured by visual analog scales. RESULTS Food cues elicited significantly greater increases in hunger compared with neutral and stress stimuli. Cue-induced hunger did not differ by weight status. Participants consumed a similar number of total calories across stimuli. In response to food cue provocation, participants with obesity consumed [mean (SE)] 81.0% (4.0%) of calories from high-calorie foods, which was significantly greater than participants with normal weight (63.5% [3.6%]; P = 0.001). After the stress cue, participants with obesity consumed 81.4% (4.0%) of calories from high-calorie foods, which was significantly more than participants with normal weight (70.2% [3.6%]; P = 0.04). Energy intake from high-calorie foods did not differ by weight status after the neutral cue. CONCLUSIONS Among individuals with obesity, exposure to food and stress cues shifted consumption to high-calorie snack foods within a well-controlled experimental setting.
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Appetite Control across the Lifecourse: The Acute Impact of Breakfast Drink Quantity and Protein Content. The Full4Health Project.
Crabtree, DR, Buosi, W, Fyfe, CL, Horgan, GW, Manios, Y, Androutsos, O, Giannopoulou, A, Finlayson, G, Beaulieu, K, Meek, CL, et al
Nutrients. 2020;(12)
Abstract
Understanding the mechanisms of hunger, satiety and how nutrients affect appetite control is important for successful weight management across the lifecourse. The primary aim of this study was to describe acute appetite control across the lifecourse, comparing age groups (children, adolescents, adults, elderly), weight categories, genders and European sites (Scotland and Greece). Participants (n = 391) consumed four test drinks, varying in composition (15% (normal protein, NP) and 30% (high protein, HP) of energy from protein) and quantity (based on 100% basal metabolic rate (BMR) and 140% BMR), on four separate days in a double-blind randomized controlled study. Ad libitum energy intake (EI), subjective appetite and biomarkers of appetite and metabolism (adults and elderly only) were measured. The adults' appetite was significantly greater than that of the elderly across all drink types (p < 0.004) and in response to drink quantities (p < 0.001). There were no significant differences in EI between age groups, weight categories, genders or sites. Concentrations of glucagon-like peptide 1 (GLP-1) and peptide YY (PYY) were significantly greater in the elderly than the adults (p < 0.001). Ghrelin and fasting leptin concentrations differed significantly between weight categories, genders and sites (p < 0.05), while GLP-1 and PYY concentrations differed significantly between genders only (p < 0.05). Compared to NP drinks, HP drinks significantly increased postprandial GLP-1 and PYY (p < 0.001). Advanced age was concomitant with reduced appetite and elevated anorectic hormone release, which may contribute to the development of malnutrition. In addition, appetite hormone concentrations differed between weight categories, genders and geographical locations.