Journal of Obesity & Metabolic Syndrome

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June, 2022 | Vol.31 No.2

J Obes Metab Syndr 2022; 31(2): 161-168

Published online June 30, 2022 https://doi.org/10.7570/jomes22031

Copyright © Korean Society for the Study of Obesity.

Nutrient-Based Appetite Regulation

Jose M. Moris, Corrinn Heinold, Alexandra Blades, Yunsuk Koh *

Department of Health, Human Performance, and Recreation, Baylor University, Waco, TX, USA

Correspondence to:
Yunsuk Koh
https://orcid.org/0000-0001-9280-5786
Department of Health, Human Performance, and Recreation, Baylor University, 1312 S. 5th st, Waco, TX 76798, USA
Tel: +1-254-710-4002
Fax: +1-254-710-3527
E-mail: Yunsuk_koh@baylor.edu

Received: April 18, 2022; Reviewed : June 3, 2022; Accepted: June 11, 2022

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Regulation of appetite is dependent on crosstalk between the gut and the brain, which is a pathway described as the gut-brain axis (GBA). Three primary appetite-regulating hormones that are secreted in the gut as a response to eating a meal are glucagon-like peptide 1 (GLP-1), cholecystokinin (CCK), and peptide YY (PYY). When these hormones are secreted, the GBA responds to reduce appetite. However, secretion of these hormones and the response of the GBA can vary depending on the types of nutrients consumed. This narrative review describes how the gut secretes GLP-1, CCK, and PYY in response to proteins, carbohydrates, and fats. In addition, the GBA response based on the quality of the meal is described in the context of which meal types produce greater appetite suppression. Last, the beneficiary role of exercise as a mediator of appetite regulation is highlighted.

Keywords: Diet, Vagus nerve, Nucleus tractus solitarius, Energy intake, Weight loss, Education

Blunted appetite regulation is a hallmark of an advanced obesogenic state that hinders weight loss harder.1 The link between food intake and the drive to eat is the gut-brain axis (GBA), where appetite is regulated. The GBA is interconnected in the medulla of the brainstem, where the nucleus tractus solitarius (NTS) receives the vagus nerve (VN) afferent fibers input originating from the gut.2 For context, the gut is comprised of the stomach, small intestine, and large intestine. Distension and secretion of hormones elicited by food intake in the gut3 cause a signal that is received by the afferent branch of the VN. This signal is transmitted by the VN to the NTS,4 where subsequent upper brain regions (superior to the brainstem) are stimulated to suppress appetite and induce meal termination.2,5 A representation of GBA signaling to the brain is presented in Fig. 1.


In contrast, during a fasted state, the GBA can stimulate the VN to increase the desire to eat.6 Although the GBA is tightly regulated, there is evidence suggesting that people with obesity have a dysregulated GBA that predisposes them to greater food cravings and increased food intake due to a lack of appetite regulation.7,8 For optimal appetite regulation, fully functional neurotransmitter activity is required. For example, dopamine can promote cravings that lead to eating, while it is also required to induce the feeling of “reward” that is required to suppress appetite.5,7,9 Because dopamine has a potent role in regulating eating behavior, downregulation of its prefrontal cortex receptors that is driven by overstimulation of reward-like behaviors is a major factor of a dysregulated GBA.10-13 In the context of food intake, stimulation of the GBA and subsequent NTS signal and dopamine release differ based on the type of nutrient consumed. Because the GBA has many interrelated mechanisms to correctly regulate appetite,5,14 the scope of this narrative review is to describe the connection between the GBA and nutrient intake while elaborating how nutrient type can affect appetite regulation.

We briefly described modulation of appetite controlled by the GBA. However, appetite and hunger are not the same. Appetite refers to the cephalic (upper brain regions) regulation of eating,15 whereas hunger is a process or physiological drive that aims to initiate eating and is signaled by an array of physiological stimuli, such as the “growling and emptiness of the stomach”, a decrease in blood glucose, and an increase in ghrelin concentration.16-19 Based on these definitions, appetite can be experienced at any point, whereas hunger is experienced only under fasted conditions. Herein, throughout this review, we will only describe GBA responses as they relate to appetite (drive to eat).

A common weight loss approach is to follow a hypocaloric diet that restricts overall nutrient intake. From an energy balance point of view, such an approach is logical and practical because consuming fewer calories than what is expended daily should lead to weight loss over time. However, this paradigm regularly contradicts itself, because a hypocaloric diet can lead to a reduction in energy expenditure. This concept is referred as the metabolic set point,20 where the body reduces the nonessential energetic demands to prevent energy deficiency and meet metabolic demands. Therefore, maintaining the weight loss achieved via a hypocaloric diet can be difficult. The challenges to sustaining a hypocaloric diet to achieve weight loss are related to the physiological abilities of our body to respond to energy intake. In essence, regardless of meal size, the GBA is not capable of sensing or determining caloric intake at a given meal.21 In contrast, meal content (macro and micronutrients) is the primary mediator of GBA stimulation. For example, a sugar-based snack might have the same caloric content as a protein-based snack. However, the protein-based snack will produce greater satiety signaling and reduce food intake in comparison to the sugar-based snack.22 That is why the nutrient content rather than the caloric intake, in combination with the stretching of gastrointestinal walls, determines the ability of the cells in the gut to secrete appetite-regulating hormones. Herein, a dysregulated GBA that cannot adequately sense the hormonal secretions from the gut will have a blunted capability to regulate appetite23,24 and can be associated with hedonic eating and promote an obesogenic state.

Protein intake

High consumption of protein or amino acids is a good method to reduce total energy intake by increasing satiety in comparison to that gained from carbohydrates and fats.25,26 Based on this, it is expected that the GBA can effectively sense the intake of protein and inhibit appetite accordingly. Specifically, when protein is consumed, enteroendocrine cells located in the small intestine secrete cholecystokinin (CCK),27 glucagon-like peptide 1 (GLP-1),28,29 and peptide YY (PYY).28-30 These three are defined as anorexigenic (appetite suppressant) hormones. When CCK is released, the nearby region of the small intestine that holds the VN afferents receives the signal from CCK when it binds to its CCK type 1 receptors (CCK1).31,32 When CCK binds to CCK1, the GBA mediates the passage of a satiety signal from the gut to the brain and suppresses appetite to help reduce food intake. Similarly, GLP-1 and PYY have the same effect of binding to their receptor located in VN afferents and producing an anorexigenic signal.33

Although the overall effect of protein intake is an anorexigenic response, the composition of the protein molecules is important. For example, the satiating effects of protein intake can be further increased by consuming proteins that contain specific amino acids like arginine,34,35 lysine,35 and glutamic acid.35 Compared to other amino acids, these have shown a greater ability to produce an anorexigenic response.35 This is an important consideration because it exemplifies how not only macronutrient type, but also quality in terms of composition are important. Leucine is an amino acid often thought to be a major precursor of an anorexigenic response. However, it is speculated that leucine acts differently than other amino acids, which produce an anorexigenic response by stimulating the GBA.36 In contrast, leucine stimulates protein synthesis and growth that are only possible if there is sufficient energy available. Therefore, it indirectly inhibits appetite by signaling that there are enough nutrients to synthesize proteins but does not react to nutrient type.35,37,38 More research is warranted to better understand how specific amino acids affect appetite regulation.

Carbohydrate intake

In contrast to protein intake, carbohydrates have a lower capability to stimulate the secretion of CCK.39 Furthermore, a carbohydrate-rich meal has a lower duration in its satiety-inducing effect compared to a protein-based meal. In part, the difference is attributed to gastric emptying, where carbohydrates can be digested faster than proteins.39,40 Therefore, from a satiety point of view, CCK will signal the GBA for longer and promote a longer satiety response when consuming protein rather than carbohydrates. Furthermore, a carbohydrate-rich meal elicits lower secretion of both GLP-1 and PYY and a shorter anorexigenic state compared to a protein-based meal.41 On this basis, if CCK, GLP-1, and PYY are secreted to a lesser extent under a carbohydrate-rich meal, then it is expected that long-term intake of a diet that favors carbohydrates would not be ideal to maintain good appetite control.

Carbohydrate is a broad term. A carbohydrate-rich meal implies that, from a given meal, the majority of the macronutrient content is allotted to carbohydrates and a lesser extent to proteins and fats. Therefore, a carbohydrate-rich meal yields a high concentration of its glucose building block upon digestion. As such, a food that has a high glycemic index is used to describe a carbohydrate-rich meal that has a low anorexigenic action.39 However, similar to the way amino acids determine the quality of proteins,42 the quality of carbohydrates is attributed to their digestibility. Digestible carbohydrates are metabolized into glucose,43 while non-digestible carbohydrates have minimal to no contribution to blood glucose and help to increase the bulk of food in the colon and to slow digestion.44 In the colon, non-digestible carbohydrates undergo fermentation, causing the release of short-chain fatty acids (SCFA).45 When produced, SCFA bind to nearby receptors that elicit secretion of GLP-146 and PYY.46,47 Even though SCFA does not promote the release of CCK because their carbon chains are too short,48 SCFA help to maintain an optimal GBA functionality by increasing the availability of enterocytes45 that help to reduce gut permeability. Well-controlled gut permeability prevents leakage of pro-inflammatory molecules that can trigger systemic inflammation and reduce the functionality of the GBA.49,50 Thus, simple carbohydrates (digestible) should be limited and complex carbohydrates (non-digestible) should be prioritized to maximize gut health and appetite suppression. Non-digestible carbohydrates remain longer within the gut and, like with protein intake, will induce a longer satiety response than digestible carbohydrates.51 In contrast, abundant consumption of digestible carbohydrates (those high in glycemic index) is associated with inability to regulate appetite, obesity, and other comorbidities,52 further warranting the need to prioritize non-digestible carbohydrates during meals.

Fat intake

As with protein and carbohydrate intake, consuming fat elicits the secretion of CCK, GLP-1, and PYY. However, a chronic high fat intake is associated with a reduced satiety effect by secretion of CCK53,54 and GLP-1.55 In contrast, PYY has shown the opposite response to a high-fat meal, where a high fat intake increases its secretion and effect.56,57 As such, with a high-fat diet, PYY can promote satiety, but the roles of CCK and GLP-1 will be limited. Importantly, like carbohydrates, fat can be categorized based on its molecular type. The two main categories of interest are saturated fats and polyunsaturated fats. For simplicity, saturated fats are considered “bad” for health, whereas polyunsaturated fats are generally considered “good” for health.58,59 As an example, consuming fried foods would primarily contribute saturated fats, whereas consuming avocados would primarily contribute polyunsaturated fats. In this context, a high intake of saturated fats is associated with excess eating and high blood glucose,58 along with metabolic derangements.60

Another aspect to consider is that availability of CCK, GLP-1, and PYY is associated with other factors. For example, in mice fed a high saturated fat diet, CCK concentration was chronically high after 18 weeks. However, the increase in CCK was not associated with an appetite regulatory response but, instead, to excess liver damage due to excess fat metabolism61 and hepatic cancer.62 Similarly, at the onset of type 2 diabetes, both a high-fat meal and a high-carbohydrate meal showed no increase in PYY postprandially,63 suggesting that the GBA is not regulating feeding responses normally. In contrast, consuming a meal that has been artificially sweetened causes no change in GLP-1,64 suggesting that long-term consumption of foods that distribute nutrients abnormally could chronically affect how the GBA regulates appetite by eliciting inadequate secretion of CCK, GLP-1, and PYY. However, novel evidence in gut physiology has demonstrated that GBA activity can differ based on the population of enteroendocrine cells irrespective of the type of nutrient intake. In other words, the ability for the GBA to regulate appetite, irrespective of gut hormones, is to some extent determined by the speed at which the VN is stimulated.65 As such, fast signal conductivity is critical within the GBA, which is why enteroendocrine cells in the gut are now known as neuropod cells.66,67 Therefore, the GBA not only relies on adequate gut hormonal release to regulate appetite, but also in the sensing of nutrients and subsequent signaling to the VN afferent fibers.

The appetite regulatory response to exercise is extensive and intricate,68 but this narrative review focuses on a few basic aspects. In general, frequent engagement in exercise improves appetite regulation by increasing the availability of CCK, GLP-1, and PYY.69 Depending on the intensity of exercise, adaptation of appetite-suppressing hormones can differ.70 In addition, the positive body composition changes attributed to exercise adaptations, i.e., reduced fat mass and increased fat-free mass, are associated with increased availability of appetite-regulating hormones.69,71-73 Therefore, frequent engagement in exercise is recommended to improve satiety and overall appetite control. An overall summary of recommendations for improved appetite control is presented in Fig. 2.

The process of appetite regulation is complex and multifactorial, and this review aimed to facilitate the understanding of this topic based on effects of nutrient type on the GBA and appetite regulation. A diet that contains adequate amounts of protein, non-digestible carbohydrates, and polyunsaturated fats is important to promote the availability of CCK, GLP-1, and PYY, which are critical to controlling appetite. Combining that type of diet with frequent exercise would be an effective approach for improving appetite regulation and body composition, which will provide long-term health improvements.

Study concept and design: JMM; analysis and interpretation of data: all authors; drafting of the manuscript: all authors; and critical revision of the manuscript: all authors.

Fig. 1. Illustration denoting the connection between the gut and brain through vagus nerve afferent fibers that subsequently signal appetite regulation once stimulated.
Fig. 2. Summary of recommendations that aim to improve appetite regulation.
  1. Andriessen C, Christensen P, Vestergaard Nielsen L, Ritz C, Astrup A, Meinert Larsen T, et al. Weight loss decreases self-reported appetite and alters food preferences in overweight and obese adults: observational data from the DiOGenes study. Appetite 2018;125:314-22.
    Pubmed CrossRef
  2. Berthoud HR, Neuhuber WL. Functional and chemical anatomy of the afferent vagal system. Auton Neurosci 2000;85:1-17.
    CrossRef
  3. Pavlov VA, Tracey KJ. The vagus nerve and the inflammatory reflex: linking immunity and metabolism. Nat Rev Endocrinol 2012;8:743-54.
    Pubmed KoreaMed CrossRef
  4. Yu CD, Xu QJ, Chang RB. Vagal sensory neurons and gut-brain signaling. Curr Opin Neurobiol 2020;62:133-40.
    Pubmed KoreaMed CrossRef
  5. Han W, Tellez LA, Perkins MH, Perez IO, Qu T, Ferreira J, et al. A neural circuit for gut-induced reward. Cell 2018;175:665-78.
    Pubmed KoreaMed CrossRef
  6. Chen J, Cheng M, Wang L, Zhang L, Xu D, Cao P, et al. A vagal-NTS neural pathway that stimulates feeding. Curr Biol 2020;30:3986-98.
    Pubmed CrossRef
  7. Blum K, Thanos PK, Gold MS. Dopamine and glucose, obesity, and reward deficiency syndrome. Front Psychol 2014;5:919.
    Pubmed KoreaMed CrossRef
  8. Val-Laillet D, Biraben A, Randuineau G, Malbert CH. Chronic vagus nerve stimulation decreased weight gain, food consumption and sweet craving in adult obese minipigs. Appetite 2010;55:245-52.
    Pubmed CrossRef
  9. Volkow ND, Wang GJ, Baler RD. Reward, dopamine and the control of food intake: implications for obesity. Trends Cogn Sci 2011;15:37-46.
    Pubmed KoreaMed CrossRef
  10. Avena NM, Rada P, Hoebel BG. Sugar and fat bingeing have notable differences in addictive-like behavior. J Nutr 2009;139:623-8.
    Pubmed KoreaMed CrossRef
  11. Labban RS, Alfawaz H, Almnaizel AT, Hassan WM, Bhat RS, Moubayed NM, et al. High-fat diet-induced obesity and impairment of brain neurotransmitter pool. Transl Neurosci 2020;11:147-60.
    Pubmed KoreaMed CrossRef
  12. Li X, Bäckman L, Persson J. The relationship of age and DRD2 polymorphisms to frontostriatal brain activity and working memory performance. Neurobiol Aging 2019;84:189-99.
    Pubmed CrossRef
  13. Johnson PM, Kenny PJ. Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats. Nat Neurosci 2010;13:635-41.
    Pubmed KoreaMed CrossRef
  14. Wang YB, de Lartigue G, Page AJ. Dissecting the role of subtypes of gastrointestinal vagal afferents. Front Physiol 2020;11:643.
    Pubmed KoreaMed CrossRef
  15. Timper K, Brüning JC. Hypothalamic circuits regulating appetite and energy homeostasis: pathways to obesity. Dis Model Mech 2017;10:679-89.
    Pubmed KoreaMed CrossRef
  16. Murray M, Vickers Z. Consumer views of hunger and fullness: a qualitative approach. Appetite 2009;53:174-82.
    Pubmed CrossRef
  17. de Bruin WE, Ward AL, Taylor RW, Jospe MR. 'Am I really hungry?': a qualitative exploration of patients' experience, adherence and behaviour change during hunger training: a pilot study. BMJ Open 2019;9:e032248.
    Pubmed KoreaMed CrossRef
  18. Amin T, Mercer JG. Hunger and satiety mechanisms and their potential exploitation in the regulation of food intake. Curr Obes Rep 2016;5:106-12.
    Pubmed KoreaMed CrossRef
  19. Berridge KC, Ho CY, Richard JM, DiFeliceantonio AG. The tempted brain eats: pleasure and desire circuits in obesity and eating disorders. Brain Res 2010;1350:43-64.
    Pubmed KoreaMed CrossRef
  20. Müller MJ, Geisler C, Heymsfield SB, Bosy-Westphal A. Recent advances in understanding body weight homeostasis in humans. F1000Res 2018;7:F1000.
    Pubmed KoreaMed CrossRef
  21. Lichtman SW, Pisarska K, Berman ER, Pestone M, Dowling H, Offenbacher E, et al. Discrepancy between self-reported and actual caloric intake and exercise in obese subjects. N Engl J Med 1992;327:1893-8.
    Pubmed CrossRef
  22. Mandel N, Brannon D. Sugar, perceived healthfulness, and satiety: when does a sugary preload lead people to eat more? Appetite 2017;114:338-49.
    Pubmed CrossRef
  23. Loper H, Leinen M, Bassoff L, Sample J, Romero-Ortega M, Gustafson KJ, et al. Both high fat and high carbohydrate diets impair vagus nerve signaling of satiety. Sci Rep 2021;11:10394.
    Pubmed KoreaMed CrossRef
  24. McDougle M, Quinn D, Diepenbroek C, Singh A, de la Serre C, de Lartigue G. Intact vagal gut-brain signalling prevents hyperphagia and excessive weight gain in response to high-fat high-sugar diet. Acta Physiol (Oxf) 2021;231:e13530.
    Pubmed KoreaMed CrossRef
  25. Moon J, Koh G. Clinical evidence and mechanisms of high-protein diet-induced weight loss. J Obes Metab Syndr 2020;29:166-73.
    Pubmed KoreaMed CrossRef
  26. Dehestani B, Stratford NR, le Roux CW. Amylin as a future obesity treatment. J Obes Metab Syndr 2021;30:320-5.
    Pubmed KoreaMed CrossRef
  27. Foltz M, Ansems P, Schwarz J, Tasker MC, Lourbakos A, Gerhardt CC. Protein hydrolysates induce CCK release from enteroendocrine cells and act as partial agonists of the CCK1 receptor. J Agric Food Chem 2008;56:837-43.
    Pubmed CrossRef
  28. van der Klaauw AA, Keogh JM, Henning E, Trowse VM, Dhillo WS, Ghatei MA, et al. High protein intake stimulates postprandial GLP1 and PYY release. Obesity (Silver Spring) 2013;21:1602-7.
    Pubmed KoreaMed CrossRef
  29. Somogyi E, Sigalet D, Adrian TE, Nyakas C, Hoornenborg CW, van Beek AP, et al. Ileal transposition in rats reduces energy intake, body weight, and body fat most efficaciously when ingesting a high-protein diet. Obes Surg 2020;30:2729-42.
    Pubmed KoreaMed CrossRef
  30. Lomenick JP, Melguizo MS, Mitchell SL, Summar ML, Anderson JW. Effects of meals high in carbohydrate, protein, and fat on ghrelin and peptide YY secretion in prepubertal children. J Clin Endocrinol Metab 2009;94:4463-71.
    Pubmed KoreaMed CrossRef
  31. Bowen J, Noakes M, Clifton PM. Appetite regulatory hormone responses to various dietary proteins differ by body mass index status despite similar reductions in ad libitum energy intake. J Clin Endocrinol Metab 2006;91:2913-9.
    Pubmed CrossRef
  32. Bowen J, Noakes M, Trenerry C, Clifton PM. Energy intake, ghrelin, and cholecystokinin after different carbohydrate and protein preloads in overweight men. J Clin Endocrinol Metab 2006;91:1477-83.
    Pubmed CrossRef
  33. Strader AD, Woods SC. Gastrointestinal hormones and food intake. Gastroenterology 2005;128:175-91.
    Pubmed CrossRef
  34. Nässl AM, Rubio-Aliaga I, Sailer M, Daniel H. The intestinal peptide transporter PEPT1 is involved in food intake regulation in mice fed a high-protein diet. PLoS One 2011;6:e26407.
    Pubmed KoreaMed CrossRef
  35. Jordi J, Herzog B, Camargo SM, Boyle CN, Lutz TA, Verrey F. Specific amino acids inhibit food intake via the area postrema or vagal afferents. J Physiol 2013;591:5611-21.
    Pubmed KoreaMed CrossRef
  36. Zampieri TT, Pedroso JA, Furigo IC, Tirapegui J, Donato J Jr. Oral leucine supplementation is sensed by the brain but neither reduces food intake nor induces an anorectic pattern of gene expression in the hypothalamus. PLoS One 2013;8:e84094.
    Pubmed KoreaMed CrossRef
  37. Zhang Y, Guo K, LeBlanc RE, Loh D, Schwartz GJ, Yu YH. Increasing dietary leucine intake reduces diet-induced obesity and improves glucose and cholesterol metabolism in mice via multimechanisms. Diabetes 2007;56:1647-54.
    Pubmed CrossRef
  38. Laeger T, Reed SD, Henagan TM, Fernandez DH, Taghavi M, Addington A, et al. Leucine acts in the brain to suppress food intake but does not function as a physiological signal of low dietary protein. Am J Physiol Regul Integr Comp Physiol 2014;307:R310-20.
    Pubmed KoreaMed CrossRef
  39. Reynolds RC, Stockmann KS, Atkinson FS, Denyer GS, Brand-Miller JC. Effect of the glycemic index of carbohydrates on day-long (10 h) profiles of plasma glucose, insulin, cholecystokinin and ghrelin. Eur J Clin Nutr 2009;63:872-8.
    Pubmed CrossRef
  40. Little TJ, Doran S, Meyer JH, Smout AJ, O'Donovan DG, Wu KL, et al. The release of GLP-1 and ghrelin, but not GIP and CCK, by glucose is dependent upon the length of small intestine exposed. Am J Physiol Endocrinol Metab 2006;291:E647-55.
    Pubmed CrossRef
  41. Parvaresh Rizi E, Loh TP, Baig S, Chhay V, Huang S, Caleb Quek J, et al. A high carbohydrate, but not fat or protein meal attenuates postprandial ghrelin, PYY and GLP-1 responses in Chinese men. PLoS One 2018;13:e0191609.
    Pubmed KoreaMed CrossRef
  42. Wolfe RR, Rutherfurd SM, Kim IY, Moughan PJ. Protein quality as determined by the Digestible Indispensable Amino Acid Score: evaluation of factors underlying the calculation. Nutr Rev 2016;74:584-99.
    Pubmed KoreaMed CrossRef
  43. Perrotti N, Santoro D, Genovese S, Giacco A, Rivellese A, Riccardi G. Effect of digestible carbohydrates on glucose control in insulin-dependent diabetic patients. Diabetes Care 1984;7:354-9.
    Pubmed CrossRef
  44. Grabitske HA, Slavin JL. Low-digestible carbohydrates in practice. J Am Diet Assoc 2008;108:1677-81.
    Pubmed CrossRef
  45. Park JH, Kotani T, Konno T, Setiawan J, Kitamura Y, Imada S, et al. Promotion of intestinal epithelial cell turnover by commensal bacteria: role of short-chain fatty acids. PLoS One 2016;11:e0156334.
    Pubmed KoreaMed CrossRef
  46. Christiansen CB, Gabe MB, Svendsen B, Dragsted LO, Rosenkilde MM, Holst JJ. The impact of short-chain fatty acids on GLP-1 and PYY secretion from the isolated perfused rat colon. Am J Physiol Gastrointest Liver Physiol 2018;315:G53-65.
    Pubmed CrossRef
  47. Larraufie P, Martin-Gallausiaux C, Lapaque N, Dore J, Gribble FM, Reimann F, et al. SCFAs strongly stimulate PYY production in human enteroendocrine cells. Sci Rep 2018;8:74.
    Pubmed KoreaMed CrossRef
  48. McLaughlin JT, Lomax RB, Hall L, Dockray GJ, Thompson DG, Warhurst G. Fatty acids stimulate cholecystokinin secretion via an acyl chain length-specific, Ca2+-dependent mechanism in the enteroendocrine cell line STC-1. J Physiol 1998;513(Pt 1):11-8.
    Pubmed KoreaMed CrossRef
  49. Klingbeil EA, Cawthon C, Kirkland R, de La Serre CB. Potato-resistant starch supplementation improves microbiota dysbiosis, inflammation, and gut-brain signaling in high fat-fed rats. Nutrients 2019;11:2710.
    Pubmed KoreaMed CrossRef
  50. Wang SZ, Yu YJ, Adeli K. Role of gut microbiota in neuroendocrine regulation of carbohydrate and lipid metabolism via the microbiota-gut-brain-liver axis. Microorganisms 2020;8:527.
    Pubmed KoreaMed CrossRef
  51. Johansson EV, Nilsson AC, Östman EM, Björck IM. Effects of indigestible carbohydrates in barley on glucose metabolism, appetite and voluntary food intake over 16 h in healthy adults. Nutr J 2013;12:46.
    Pubmed KoreaMed CrossRef
  52. Lennerz B, Lennerz JK. Food addiction, high-glycemic-index carbohydrates, and obesity. Clin Chem 2018;64:64-71.
    Pubmed KoreaMed CrossRef
  53. Swartz TD, Savastano DM, Covasa M. Reduced sensitivity to cholecystokinin in male rats fed a high-fat diet is reversible. J Nutr 2010;140:1698-703.
    Pubmed CrossRef
  54. Nefti W, Chaumontet C, Fromentin G, Tomé D, Darcel N. A high-fat diet attenuates the central response to within-meal satiation signals and modifies the receptor expression of vagal afferents in mice. Am J Physiol Regul Integr Comp Physiol 2009;296:R1681-6.
    Pubmed CrossRef
  55. Richards P, Pais R, Habib AM, Brighton CA, Yeo GS, Reimann F, et al. High fat diet impairs the function of glucagon-like peptide-1 producing L-cells. Peptides 2016;77:21-7.
    Pubmed KoreaMed CrossRef
  56. Essah PA, Levy JR, Sistrun SN, Kelly SM, Nestler JE. Effect of macronutrient composition on postprandial peptide YY levels. J Clin Endocrinol Metab 2007;92:4052-5.
    Pubmed CrossRef
  57. Helou N, Obeid O, Azar ST, Hwalla N. Variation of postprandial PYY 3-36 response following ingestion of differing macronutrient meals in obese females. Ann Nutr Metab 2008;52:188-95.
    Pubmed CrossRef
  58. Dziedzic B, Szemraj J, Bartkowiak J, Walczewska A. Various dietary fats differentially change the gene expression of neuropeptides involved in body weight regulation in rats. J Neuroendocrinol 2007;19:364-73.
    Pubmed CrossRef
  59. Hartmann H, Pauli LK, Janssen LK, Huhn S, Ceglarek U, Horstmann A. Preliminary evidence for an association between intake of high-fat high-sugar diet, variations in peripheral dopamine precursor availability and dopamine-dependent cognition in humans. J Neuroendocrinol 2020;32:e12917.
    Pubmed CrossRef
  60. Luukkonen PK, Sädevirta S, Zhou Y, Kayser B, Ali A, Ahonen L, et al. Saturated fat is more metabolically harmful for the human liver than unsaturated fat or simple sugars. Diabetes Care 2018;41:1732-9.
    Pubmed KoreaMed CrossRef
  61. Tucker RD, Ciofoaia V, Nadella S, Gay MD, Cao H, Huber M, et al. A cholecystokinin receptor antagonist halts nonalcoholic steatohepatitis and prevents hepatocellular carcinoma. Dig Dis Sci 2020;65:189-203.
    Pubmed KoreaMed CrossRef
  62. Gay MD, Safronenka A, Cao H, Liu FH, Malchiodi ZX, Tucker RD, et al. Targeting the cholecystokinin receptor: a novel approach for treatment and prevention of hepatocellular cancer. Cancer Prev Res (Phila) 2021;14:17-30.
    Pubmed KoreaMed CrossRef
  63. Viardot A, Heilbronn LK, Herzog H, Gregersen S, Campbell LV. Abnormal postprandial PYY response in insulin sensitive nondiabetic subjects with a strong family history of type 2 diabetes. Int J Obes (Lond) 2008;32:943-8.
    Pubmed CrossRef
  64. Steinert RE, Frey F, Töpfer A, Drewe J, Beglinger C. Effects of carbohydrate sugars and artificial sweeteners on appetite and the secretion of gastrointestinal satiety peptides. Br J Nutr 2011;105:1320-8.
    Pubmed CrossRef
  65. Buchanan KL, Rupprecht LE, Kaelberer MM, Sahasrabudhe A, Klein ME, Villalobos JA, et al. The preference for sugar over sweetener depends on a gut sensor cell. Nat Neurosci 2022;25:191-200.
    Pubmed KoreaMed CrossRef
  66. Kaelberer MM, Buchanan KL, Klein ME, Barth BB, Montoya MM, Shen X, et al. A gut-brain neural circuit for nutrient sensory transduction. Science 2018;361:eaat5236.
    Pubmed KoreaMed CrossRef
  67. Bai L, Sivakumar N, Mesgarzadeh S, Ding T, Ly T, Corpuz TV, et al. Enteroendocrine cell types that drive food reward and aversion. bioRxiv [Preprint].  2021 [cited 2022 Jun 10]. Available from: https://doi.org/10.1101/2021.11.05.467492.
    CrossRef
  68. Hubner S, Boron JB, Koehler K. The effects of exercise on appetite in older adults: a systematic review and meta-analysis. Front Nutr 2021;8:734267.
    Pubmed KoreaMed CrossRef
  69. Quist JS, Blond MB, Gram AS, Steenholt CB, Janus C, Holst JJ, et al. Effects of active commuting and leisure-time exercise on appetite in individuals with overweight and obesity. J Appl Physiol (1985) 2019;126:941-51.
    Pubmed CrossRef
  70. Jahan-mihan A, Magyari P, Pinkstaff SO, Sciences AM. The effect of intensity of exercise on appetite and food intake regulation in post-exercise period: a randomized trial. J Exerc Nutr 2021;4:12.
  71. Wang M, Baker JS, Quan W, Shen S, Fekete G, Gu Y. A preventive role of exercise across the coronavirus 2 (SARS-CoV-2) pandemic. Front Physiol 2020;11:572718.
    Pubmed KoreaMed CrossRef
  72. Hunter GR, Brock DW, Byrne NM, Chandler-Laney PC, Del Corral P, Gower BA. Exercise training prevents regain of visceral fat for 1 year following weight loss. Obesity (Silver Spring) 2010;18:690-5.
    Pubmed KoreaMed CrossRef
  73. Flack KD, Hays HM, Moreland J. The consequences of exercise-induced weight loss on food reinforcement: a randomized controlled trial. PLoS One 2020;15:e0234692.
    Pubmed KoreaMed CrossRef