The effect of meal frequency in a reduced-energy regimen on the gastrointestinal and appetite hormones in patients with type 2 diabetes: A randomised crossover study
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články, randomizované kontrolované studie
PubMed
28369078
PubMed Central
PMC5378398
DOI
10.1371/journal.pone.0174820
PII: PONE-D-16-45452
Knihovny.cz E-zdroje
- MeSH
- časové faktory MeSH
- diabetes mellitus 2. typu dietoterapie patologie patofyziologie psychologie MeSH
- dospělí MeSH
- ghrelin krev MeSH
- glukagonu podobný peptid 1 krev MeSH
- hlad fyziologie MeSH
- inzulinová rezistence MeSH
- jídla * fyziologie psychologie MeSH
- kalorická restrikce metody MeSH
- klinické křížové studie MeSH
- leptin krev MeSH
- lidé středního věku MeSH
- lidé MeSH
- pankreatický polypeptid krev MeSH
- peptid YY krev MeSH
- senioři MeSH
- tělesná hmotnost MeSH
- výsledek terapie MeSH
- žaludeční inhibiční polypeptid krev MeSH
- Check Tag
- dospělí MeSH
- lidé středního věku MeSH
- lidé MeSH
- mužské pohlaví MeSH
- senioři MeSH
- ženské pohlaví MeSH
- Publikační typ
- časopisecké články MeSH
- randomizované kontrolované studie MeSH
- Názvy látek
- ghrelin MeSH
- glukagonu podobný peptid 1 MeSH
- leptin MeSH
- pankreatický polypeptid MeSH
- peptid YY MeSH
- žaludeční inhibiční polypeptid MeSH
BACKGROUND: Appetite and gastrointestinal hormones (GIHs) participate in energy homeostasis, feeding behavior and regulation of body weight. We demonstrated previously the superior effect of a hypocaloric diet regimen with lower meal frequency (B2) on body weight, hepatic fat content, insulin sensitivity and feelings of hunger compared to the same diet divided into six smaller meals a day (A6). Studies with isoenergetic diet regimens indicate that lower meal frequency should also have an effect on fasting and postprandial responses of GIHs. The aim of this secondary analysis was to explore the effect of two hypocaloric diet regimens on fasting levels of appetite and GIHs and on their postprandial responses after a standard meal. It was hypothesized that lower meal frequency in a reduced-energy regimen leading to greater body weight reduction and reduced hunger would be associated with decreased plasma concentrations of GIHs: gastric inhibitory peptide (GIP), glucagon-like peptide-1(GLP-1), peptide YY(PYY), pancreatic polypeptide (PP) and leptin and increased plasma concentration of ghrelin. The postprandial response of satiety hormones (GLP-1, PYY and PP) and postprandial suppression of ghrelin will be improved. METHODS: In a randomized crossover study, 54 patients suffering from type 2 diabetes (T2D) underwent both regimens. The concentrations of GLP-1, GIP, PP, PYY, amylin, leptin and ghrelin were determined using multiplex immunoanalyses. RESULTS: Fasting leptin and GIP decreased in response to both regimens with no difference between the treatments (p = 0.37 and p = 0.83, respectively). Fasting ghrelin decreased in A6 and increased in B2 (with difference between regimens p = 0.023). Fasting PP increased in B2with no significant difference between regimens (p = 0.17). Neither GLP-1 nor PYY did change in either regimen. The decrease in body weight correlated negatively with changes in fasting ghrelin (r = -0.4, p<0.043) and the postprandial reduction of ghrelin correlated positively with its fasting level (r = 0.9, p<0.001). The postprandial responses of GIHs and appetite hormones were similar after both diet regimens. CONCLUSIONS: Both hypocaloric diet regimens reduced fasting leptin and GIP and postprandial response of GIP comparably. The postprandial responses of GIHs and appetite hormones were similar after both diet regimens. Eating only breakfast and lunch increased fasting plasma ghrelin more than the same caloric restriction split into six meals. The changes in fasting ghrelin correlated negatively with the decrease in body weight. These results suggest that for type 2 diabetic patients on a hypocaloric diet, eating larger breakfast and lunch may be more efficient than six smaller meals during the day.
1st Faculty of Medicine Charles University Prague Czech Republic
Department of Diabetology Institute for Clinical and Experimental Medicine Prague Czech Republic
Department of Steroid Hormones and Proteohormones Institute of Endocrinology Prague Czech Republic
Laboratory of Immunoanalysis University Hospital in Pilsen Pilsen Czech Republic
Zobrazit více v PubMed
Scharf MT, Ahima RS. Gut peptides and other regulators in obesity. Seminars in liver disease. 2004. November;24(4):335–47. 10.1055/s-2004-860863 PubMed DOI
Perry B, Wang Y. Appetite regulation and weight control: the role of gut hormones. Nutrition & diabetes. 2012;2:e26. PubMed PMC
Batterham RL, Cohen MA, Ellis SM, Le Roux CW, Withers DJ, Frost GS, et al. Inhibition of food intake in obese subjects by peptide YY3-36. The New England journal of medicine. 2003. September 4;349(10):941–8. 10.1056/NEJMoa030204 PubMed DOI
Salera M, Giacomoni P, Pironi L, Cornia G, Capelli M, Marini A, et al. Gastric inhibitory polypeptide release after oral glucose: relationship to glucose intolerance, diabetes mellitus, and obesity. The Journal of clinical endocrinology and metabolism. 1982. August;55(2):329–36. 10.1210/jcem-55-2-329 PubMed DOI
Meier JJ, Nauck MA. Is the diminished incretin effect in type 2 diabetes just an epi-phenomenon of impaired beta-cell function? Diabetes. 2010. May;59(5):1117–25. 10.2337/db09-1899 PubMed DOI PMC
English PJ, Ashcroft A, Patterson M, Dovey TM, Halford JC, Harrison J, et al. Fasting plasma peptide-YY concentrations are elevated but do not rise postprandially in type 2 diabetes. Diabetologia. 2006. September;49(9):2219–21. 10.1007/s00125-006-0344-y PubMed DOI
de Luis DA, Gonzalez Sagrado M, Conde R, Aller R, Izaola O. Decreased basal levels of glucagon-like peptide-1 after weight loss in obese subjects. Annals of nutrition & metabolism. 2007;51(2):134–8. PubMed
Reinehr T, de Sousa G, Roth CL. Fasting glucagon-like peptide-1 and its relation to insulin in obese children before and after weight loss. Journal of pediatric gastroenterology and nutrition. 2007. May;44(5):608–12. 10.1097/MPG.0b013e3180406a24 PubMed DOI
Iepsen EW, Lundgren J, Holst JJ, Madsbad S, Torekov SS. Successful weight loss maintenance includes long-term increased meal responses of GLP-1 and PYY3-36. European journal of endocrinology. 2016. June;174(6):775–84. 10.1530/EJE-15-1116 PubMed DOI
Chan JL, Stoyneva V, Kelesidis T, Raciti P, Mantzoros CS. Peptide YY levels are decreased by fasting and elevated following caloric intake but are not regulated by leptin. Diabetologia. 2006. January;49(1):169–73. 10.1007/s00125-005-0041-2 PubMed DOI
Kelly KR, Brooks LM, Solomon TP, Kashyap SR, O'Leary VB, Kirwan JP. The glucose-dependent insulinotropic polypeptide and glucose-stimulated insulin response to exercise training and diet in obesity. American journal of physiology Endocrinology and metabolism. 2009. June;296(6):E1269–74. 10.1152/ajpendo.00112.2009 PubMed DOI PMC
Munsters MJ, Saris WH. Effects of meal frequency on metabolic profiles and substrate partitioning in lean healthy males. PloS one. 2012;7(6):e38632 10.1371/journal.pone.0038632 PubMed DOI PMC
Leidy HJ, Campbell WW. The effect of eating frequency on appetite control and food intake: brief synopsis of controlled feeding studies. The Journal of nutrition. 2011. January;141(1):154–7. 10.3945/jn.109.114389 PubMed DOI
Raynor HA, Goff MR, Poole SA, Chen G. Eating Frequency, Food Intake, and Weight: A Systematic Review of Human and Animal Experimental Studies. Frontiers in nutrition. 2015;2:38 10.3389/fnut.2015.00038 PubMed DOI PMC
Howarth NC, Huang TT, Roberts SB, Lin BH, McCrory MA. Eating patterns and dietary composition in relation to BMI in younger and older adults. International journal of obesity. 2007. April;31(4):675–84. 10.1038/sj.ijo.0803456 PubMed DOI
Duval K, Strychar I, Cyr MJ, Prud'homme D, Rabasa-Lhoret R, Doucet E. Physical activity is a confounding factor of the relation between eating frequency and body composition. The American journal of clinical nutrition. 2008. November;88(5):1200–5. PubMed
Palmer MA, Capra S, Baines SK. Association between eating frequency, weight, and health. Nutrition reviews. 2009. July;67(7):379–90. 10.1111/j.1753-4887.2009.00204.x PubMed DOI
McCrory MA, Campbell WW. Effects of eating frequency, snacking, and breakfast skipping on energy regulation: symposium overview. The Journal of nutrition. 2011. January;141(1):144–7. 10.3945/jn.109.114918 PubMed DOI
Kahleova H, Belinova L, Malinska H, Oliyarnyk O, Trnovska J, Skop V, et al. Eating two larger meals a day (breakfast and lunch) is more effective than six smaller meals in a reduced-energy regimen for patients with type 2 diabetes: a randomised crossover study. Diabetologia. 2014. August;57(8):1552–60. 10.1007/s00125-014-3253-5 PubMed DOI PMC
Kahleova H, Belinova L, Hill M, Pelikanova T. Do patients with type 2 diabetes still need to eat snacks? European journal of clinical nutrition. 2015. June;69(6):755–6. 10.1038/ejcn.2015.46 PubMed DOI
Yildiz BO, Suchard MA, Wong ML, McCann SM, Licinio J. Alterations in the dynamics of circulating ghrelin, adiponectin, and leptin in human obesity. Proceedings of the National Academy of Sciences of the United States of America. 2004. July 13;101(28):10434–9. 10.1073/pnas.0403465101 PubMed DOI PMC
English PJ, Ghatei MA, Malik IA, Bloom SR, Wilding JP. Food fails to suppress ghrelin levels in obese humans. The Journal of clinical endocrinology and metabolism. 2002. June;87(6):2984 10.1210/jcem.87.6.8738 PubMed DOI
Malinska H, Kahleova H, Topolcan O, Vrzalova J, Oliyarnyk O, Kazdova L, et al. Postprandial oxidative stress and gastrointestinal hormones: is there a link? PloS one. 2014;9(8):e103565 10.1371/journal.pone.0103565 PubMed DOI PMC
Purnell JQ, Cummings D, Weigle DS. Changes in 24-h area-under-the-curve ghrelin values following diet-induced weight loss are associated with loss of fat-free mass, but not with changes in fat mass, insulin levels or insulin sensitivity. International journal of obesity. 2007. February;31(2):385–9. 10.1038/sj.ijo.0803401 PubMed DOI
Cummings DE, Weigle DS, Frayo RS, Breen PA, Ma MK, Dellinger EP, et al. Plasma ghrelin levels after diet-induced weight loss or gastric bypass surgery. The New England journal of medicine. 2002. May 23;346(21):1623–30. 10.1056/NEJMoa012908 PubMed DOI
Moran LJ, Luscombe-Marsh ND, Noakes M, Wittert GA, Keogh JB, Clifton PM. The satiating effect of dietary protein is unrelated to postprandial ghrelin secretion. The Journal of clinical endocrinology and metabolism. 2005. September;90(9):5205–11. 10.1210/jc.2005-0701 PubMed DOI
Batterham RL, Le Roux CW, Cohen MA, Park AJ, Ellis SM, Patterson M, et al. Pancreatic polypeptide reduces appetite and food intake in humans. The Journal of clinical endocrinology and metabolism. 2003. August;88(8):3989–92. 10.1210/jc.2003-030630 PubMed DOI
Neary NM, Small CJ, Druce MR, Park AJ, Ellis SM, Semjonous NM, et al. Peptide YY3-36 and glucagon-like peptide-17-36 inhibit food intake additively. Endocrinology. 2005. December;146(12):5120–7. 10.1210/en.2005-0237 PubMed DOI
Mishra AK, Dubey V, Ghosh AR. Obesity: An overview of possible role(s) of gut hormones, lipid sensing and gut microbiota. Metabolism: clinical and experimental. 2016. January;65(1):48–65. PubMed
Mann JI, De Leeuw I, Hermansen K, Karamanos B, Karlstrom B, Katsilambros N, et al. Evidence-based nutritional approaches to the treatment and prevention of diabetes mellitus. Nutrition, metabolism, and cardiovascular diseases: NMCD. 2004. December;14(6):373–94. PubMed
Ferrannini E. The theoretical bases of indirect calorimetry: a review. Metabolism. 1988. March;37(3):287–301. PubMed
Hagstromer M, Oja P, Sjostrom M. The International Physical Activity Questionnaire (IPAQ): a study of concurrent and construct validity. Public health nutrition. 2006. September;9(6):755–62. PubMed
Baecke JA, Burema J, Frijters JE. A short questionnaire for the measurement of habitual physical activity in epidemiological studies. The American journal of clinical nutrition. 1982. November;36(5):936–42. PubMed
Kellar KL, Iannone MA. Multiplexed microsphere-based flow cytometric assays. Experimental hematology. 2002. November;30(11):1227–37. PubMed
Meloun M, Hill M, Militky J, Kupka K. Transformation in the PC-aided biochemical data analysis. Clinical chemistry and laboratory medicine: CCLM / FESCC. 2000. June;38(6):553–9. PubMed
Mekary RA, Giovannucci E, Willett WC, van Dam RM, Hu FB. Eating patterns and type 2 diabetes risk in men: breakfast omission, eating frequency, and snacking. The American journal of clinical nutrition. 2012. May;95(5):1182–9. 10.3945/ajcn.111.028209 PubMed DOI PMC
Reutrakul S, Hood MM, Crowley SJ, Morgan MK, Teodori M, Knutson KL. The relationship between breakfast skipping, chronotype, and glycemic control in type 2 diabetes. Chronobiology international. 2014. February;31(1):64–71. 10.3109/07420528.2013.821614 PubMed DOI
Jakubowicz D, Wainstein J, Ahren B, Bar-Dayan Y, Landau Z, Rabinovitz HR, et al. High-energy breakfast with low-energy dinner decreases overall daily hyperglycaemia in type 2 diabetic patients: a randomised clinical trial. Diabetologia. 2015. May;58(5):912–9. 10.1007/s00125-015-3524-9 PubMed DOI
Blom WA, de Graaf C, Lluch A, Stafleu A, Schaafsma G, Hendriks HF. Postprandial ghrelin responses are associated with the intermeal interval in time-blinded normal weight men, but not in obese men. Physiology & behavior. 2009. March 23;96(4–5):742–8. PubMed
de Luis DA, Sagrado MG, Conde R, Aller R, Izaola O. Changes of ghrelin and leptin in response to hypocaloric diet in obese patients. Nutrition. 2008. February;24(2):162–6. 10.1016/j.nut.2007.11.001 PubMed DOI
DelParigi A, Tschop M, Heiman ML, Salbe AD, Vozarova B, Sell SM, et al. High circulating ghrelin: a potential cause for hyperphagia and obesity in prader-willi syndrome. The Journal of clinical endocrinology and metabolism. 2002. December;87(12):5461–4. 10.1210/jc.2002-020871 PubMed DOI
Cummings DE, Frayo RS, Marmonier C, Aubert R, Chapelot D. Plasma ghrelin levels and hunger scores in humans initiating meals voluntarily without time- and food-related cues. American journal of physiology Endocrinology and metabolism. 2004. August;287(2):E297–304. 10.1152/ajpendo.00582.2003 PubMed DOI
Schindler K, Prager G, Ballaban T, Kretschmer S, Riener R, Buranyi B, et al. Impact of laparoscopic adjustable gastric banding on plasma ghrelin, eating behaviour and body weight. European journal of clinical investigation. 2004. August;34(8):549–54. 10.1111/j.1365-2362.2004.01382.x PubMed DOI
Wagenknecht M, Hainer V, Kunesova M, Bellisle F, Parizkova J, Braunerova R, et al. [Relationships between the "eating inventory" factors, socioeconomic status, anthropometric body adiposity indexes and health risks in Czech population]. Casopis lekaru ceskych. 2007;146(3):284–6, 7–91. Vztahy mezi faktory "dotazniku jidelnich zvyklosti", socioekonomickym stavem, antropometrickymi ukazateli akumulace tuku a zdravotnimi riziky u ceske populace. PubMed
Wren AM, Small CJ, Ward HL, Murphy KG, Dakin CL, Taheri S, et al. The novel hypothalamic peptide ghrelin stimulates food intake and growth hormone secretion. Endocrinology. 2000. November;141(11):4325–8. 10.1210/endo.141.11.7873 PubMed DOI
Enriori PJ, Evans AE, Sinnayah P, Jobst EE, Tonelli-Lemos L, Billes SK, et al. Diet-induced obesity causes severe but reversible leptin resistance in arcuate melanocortin neurons. Cell metabolism. 2007. March;5(3):181–94. 10.1016/j.cmet.2007.02.004 PubMed DOI
Wauters M, Considine RV, Yudkin JS, Peiffer F, De Leeuw I, Van Gaal LF. Leptin levels in type 2 diabetes: associations with measures of insulin resistance and insulin secretion. Hormone and metabolic research = Hormon- und Stoffwechselforschung = Hormones et metabolisme. 2003. February;35(2):92–6. 10.1055/s-2003-39054 PubMed DOI
Hickey MS, Israel RG, Gardiner SN, Considine RV, McCammon MR, Tyndall GL, et al. Gender differences in serum leptin levels in humans. Biochemical and molecular medicine. 1996. October;59(1):1–6. PubMed
Hellstrom L, Wahrenberg H, Hruska K, Reynisdottir S, Arner P. Mechanisms behind gender differences in circulating leptin levels. Journal of internal medicine. 2000. April;247(4):457–62. PubMed
Nicklas BJ, Katzel LI, Ryan AS, Dennis KE, Goldberg AP. Gender differences in the response of plasma leptin concentrations to weight loss in obese older individuals. Obesity research. 1997. January;5(1):62–8. PubMed
Halaas JL, Gajiwala KS, Maffei M, Cohen SL, Chait BT, Rabinowitz D, et al. Weight-reducing effects of the plasma protein encoded by the obese gene. Science. 1995. July 28;269(5223):543–6. PubMed
Mauvais-Jarvis F. Sex differences in metabolic homeostasis, diabetes, and obesity. Biology of sex differences. 2015;6:14 10.1186/s13293-015-0033-y PubMed DOI PMC
Lutz TA. Amylinergic control of food intake. Physiology & behavior. 2006. November 30;89(4):465–71. PubMed
Kahn SE, D'Alessio DA, Schwartz MW, Fujimoto WY, Ensinck JW, Taborsky GJ Jr., et al. Evidence of cosecretion of islet amyloid polypeptide and insulin by beta-cells. Diabetes. 1990. May;39(5):634–8. PubMed
Young A. Inhibition of food intake. Advances in pharmacology. 2005;52:79–98. 10.1016/S1054-3589(05)52005-2 PubMed DOI
Aronne L, Fujioka K, Aroda V, Chen K, Halseth A, Kesty NC, et al. Progressive reduction in body weight after treatment with the amylin analog pramlintide in obese subjects: a phase 2, randomized, placebo-controlled, dose-escalation study. The Journal of clinical endocrinology and metabolism. 2007. August;92(8):2977–83. 10.1210/jc.2006-2003 PubMed DOI
Roth JD, Roland BL, Cole RL, Trevaskis JL, Weyer C, Koda JE, et al. Leptin responsiveness restored by amylin agonism in diet-induced obesity: evidence from nonclinical and clinical studies. Proceedings of the National Academy of Sciences of the United States of America. 2008. May 20;105(20):7257–62. 10.1073/pnas.0706473105 PubMed DOI PMC
Lutz TA. The interaction of amylin with other hormones in the control of eating. Diabetes, obesity & metabolism. 2013. February;15(2):99–111. PubMed
Gerner T, Johansen OE, Olufsen M, Torjesen PA, Tveit A. The post-prandial pattern of gut hormones is related to magnitude of weight-loss following gastric bypass surgery: a case-control study. Scandinavian journal of clinical and laboratory investigation. 2014. April;74(3):213–8. 10.3109/00365513.2013.877594 PubMed DOI
DePaula AL, Macedo AL, Rassi N, Machado CA, Schraibman V, Silva LQ, et al. Laparoscopic treatment of type 2 diabetes mellitus for patients with a body mass index less than 35. Surgical endoscopy. 2008. March;22(3):706–16. 10.1007/s00464-007-9472-9 PubMed DOI
Verdich C, Flint A, Gutzwiller JP, Naslund E, Beglinger C, Hellstrom PM, et al. A meta-analysis of the effect of glucagon-like peptide-1 (7–36) amide on ad libitum energy intake in humans. The Journal of clinical endocrinology and metabolism. 2001. September;86(9):4382–9. 10.1210/jcem.86.9.7877 PubMed DOI
Verdich C, Toubro S, Buemann B, Lysgard Madsen J, Juul Holst J, Astrup A. The role of postprandial releases of insulin and incretin hormones in meal-induced satiety—effect of obesity and weight reduction. International journal of obesity and related metabolic disorders: journal of the International Association for the Study of Obesity. 2001. August;25(8):1206–14. PubMed
Kim BJ, Carlson OD, Jang HJ, Elahi D, Berry C, Egan JM. Peptide YY is secreted after oral glucose administration in a gender-specific manner. The Journal of clinical endocrinology and metabolism. 2005. December;90(12):6665–71. 10.1210/jc.2005-0409 PubMed DOI
Chandarana K, Drew ME, Emmanuel J, Karra E, Gelegen C, Chan P, et al. Subject standardization, acclimatization, and sample processing affect gut hormone levels and appetite in humans. Gastroenterology. 2009. June;136(7):2115–26. 10.1053/j.gastro.2009.02.047 PubMed DOI
le Roux CW, Batterham RL, Aylwin SJ, Patterson M, Borg CM, Wynne KJ, et al. Attenuated peptide YY release in obese subjects is associated with reduced satiety. Endocrinology. 2006. January;147(1):3–8. 10.1210/en.2005-0972 PubMed DOI
Stock S, Leichner P, Wong AC, Ghatei MA, Kieffer TJ, Bloom SR, et al. Ghrelin, peptide YY, glucose-dependent insulinotropic polypeptide, and hunger responses to a mixed meal in anorexic, obese, and control female adolescents. The Journal of clinical endocrinology and metabolism. 2005. April;90(4):2161–8. 10.1210/jc.2004-1251 PubMed DOI
Batterham RL, ffytche DH, Rosenthal JM, Zelaya FO, Barker GJ, Withers DJ, et al. PYY modulation of cortical and hypothalamic brain areas predicts feeding behaviour in humans. Nature. 2007. November 1;450(7166):106–9. 10.1038/nature06212 PubMed DOI
Belinova L, Kahleova H, Malinska H, Topolcan O, Vrzalova J, Oliyarnyk O, et al. Differential acute postprandial effects of processed meat and isocaloric vegan meals on the gastrointestinal hormone response in subjects suffering from type 2 diabetes and healthy controls: a randomized crossover study. PloS one. 2014;9(9):e107561 10.1371/journal.pone.0107561 PubMed DOI PMC
McClean PL, Irwin N, Cassidy RS, Holst JJ, Gault VA, Flatt PR. GIP receptor antagonism reverses obesity, insulin resistance, and associated metabolic disturbances induced in mice by prolonged consumption of high-fat diet. American journal of physiology Endocrinology and metabolism. 2007. December;293(6):E1746–55. 10.1152/ajpendo.00460.2007 PubMed DOI
Meier JJ. The contribution of incretin hormones to the pathogenesis of type 2 diabetes. Best practice & research Clinical endocrinology & metabolism. 2009. August;23(4):433–41. PubMed
Skrha J, Hilgertova J, Jarolimkova M, Kunesova M, Hill M. Meal test for glucose-dependent insulinotropic peptide (GIP) in obese and type 2 diabetic patients. Physiological research / Academia Scientiarum Bohemoslovaca. 2010;59(5):749–55. PubMed
Weiss EP, Albert SG, Reeds DN, Kress KS, Ezekiel UR, McDaniel JL, et al. Calorie Restriction and Matched Weight Loss From Exercise: Independent and Additive Effects on Glucoregulation and the Incretin System in Overweight Women and Men. Diabetes care. 2015. July;38(7):1253–62. 10.2337/dc14-2913 PubMed DOI PMC
Ishii S, Osaki N, Shimotoyodome A. The Effects of a Hypocaloric Diet on Diet-Induced Thermogenesis and Blood Hormone Response in Healthy Male Adults: A Pilot Study. Journal of nutritional science and vitaminology. 2016;62(1):40–6. 10.3177/jnsv.62.40 PubMed DOI
Solomon TP, Haus JM, Kelly KR, Rocco M, Kashyap SR, Kirwan JP. Improved pancreatic beta-cell function in type 2 diabetic patients after lifestyle-induced weight loss is related to glucose-dependent insulinotropic polypeptide. Diabetes care. 2010. July;33(7):1561–6. 10.2337/dc09-2021 PubMed DOI PMC
Tai MM, Castillo P, Pi-Sunyer FX. Meal size and frequency: effect on the thermic effect of food. The American journal of clinical nutrition. 1991. November;54(5):783–7. PubMed