Postprandial Hyperglycemia: Comparison
Please note this is a comparison between Version 1 by Daniela Jakubowicz and Version 2 by Camila Xu.

Postprandial hyperglycemia (PPHG) is strongly linked with the future development of cardiovascular complications in type 2 diabetes (T2D). . Hence, reducing postprandial glycemic excursions is essential in T2D treatment to slow progressive deficiency of β-cell function and prevent cardiovascular complications. Most of the metabolic processes involved in PPHG, i.e., β-cell secretory function, GLP-1 secretion, insulin sensitivity, muscular glucose uptake, and hepatic glucose production, are controlled by the circadian clock and display daily oscillation. Consequently, postprandial glycemia displays diurnal variation with a higher glycemic response after meals with the same carbohydrate content, consumed at dusk compared to the morning. T2D and meal timing schedule not synchronized with the circadian clock (i.e., skipping breakfast) are associated with disrupted clock gene expression and are linked to PPHG. In contrast, greater intake in the morning (i.e., high energy breakfast) than in the evening has a resetting effect on clock gene oscillations and beneficial effects on weight loss, appetite, and reduction of PPHG, independently of total energy intake. Therefore, resetting clock gene expression through a diet intervention consisting of meal timing aligned to the circadian clock, i.e., shifting most calories and carbohydrates to the early hours of the day, is a promising therapeutic approach to improve PPHG in T2D. This review will focus on recent studies, showing how a high-energy breakfast diet (Bdiet) has resetting and synchronizing actions on circadian clock genes expression, improving glucose metabolism, postprandial glycemic excursions along weight loss in T2D.

  • clock genes 2
  • big breakfast 3
  • PPHG 4
  • T2D 5
  • circadian rhythms
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References

  1. Monnier, L.; Lapinski, H.; Colette, C. Contributions of fasting and postprandial plasma glucose increments to the overall diurnal hyperglycemia of type 2 diabetic patients: Variations with increasing levels of HbA1c. Diabetes Care 2003, 26, 881–885.
  2. Ceriello, A.; Colagiuri, S.; Gerich, J.; Tuomilehto, J. Guideline for management of postmeal glucose. Nutr. Metab. Cardiovasc. Dis. 2008, 18, S17–S33.
  3. Szuszkiewicz-Garcia, M.M.; Davidson, J.A. Cardiovascular disease in diabetes mellitus: Risk factors and medical therapy. Endocrinol. Metab. Clin. N. Am. 2014, 43, 25–40.
  4. Bruce, D.G.; Chisholm, D.J.; Storlien, L.H.; Kraegen, E.W. Physiological importance of deficiency in early prandial insulin secretion in non-insulin-dependent diabetes. Diabetes 1988, 37, 736–744.
  5. Kahn, S.E. The Importance of β-Cell Failure in the Development and Progression of Type 2 Diabetes. J. Clin. Endocrinol. Metab. 2001, 86, 4047–4058.
  6. Del Prato, S. Loss of early insulin secretion leads to postprandial hyperglycaemia. Diabetologia 2003, 46.
  7. Fonseca, V. Clinical significance of targeting postprandial and fasting hyperglycemia in managing type 2 diabetes mellitus. Curr. Med. Res. Opin. 2003, 19, 631–635.
  8. Oike, H. Modulation of circadian clocks by nutrients and food factors. Biosci. Biotechnol. Biochem. 2017, 81, 863–870.
  9. Poggiogalle, E.; Jamshed, H.; Peterson, C.M. Circadian regulation of glucose, lipid, and energy metabolism in humans. Metabolism 2018, 84, 11–27.
  10. Panda, S. Circadian physiology of metabolism. Science 2016, 354, 1008–1015.
  11. Oosterman, J.E.; Kalsbeek, A.; La Fleur, S.E.; Belsham, D.D. Impact of nutrients on circadian rhythmicity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2015, 308, R337–R350.
  12. Koronowski, K.B.; Sassone-Corsi, P. Communicating clocks shape circadian homeostasis. Science 2021, 371, eabd0951.
  13. Javeed, N.; Matveyenko, A.V. Circadian etiology of type 2 diabetes mellitus. Physiology 2018, 33, 138–150.
  14. Froy, O.; Garaulet, M. The circadian clock in white and brown adipose tissue: Mechanistic, endocrine, and clinical aspects. Endocr. Rev. 2018, 39, 261–273.
  15. Jakubowicz, D.; Landau, Z.; Tsameret, S.; Wainstein, J.; Raz, I.; Ahren, B.; Chapnik, N.; Barnea, M.; Ganz, T.; Menaged, M.; et al. Reduction in Glycated Hemoglobin and Daily Insulin Dose Alongside Circadian Clock Upregulation in Patients with Type 2 Diabetes Consuming a Three-Meal Diet: A Randomized Clinical Trial. Diabetes Care 2019, dc191142.
  16. Jordan, S.D.; Lamia, K.A. AMPK at the crossroads of circadian clocks and metabolism. Mol. Cell. Endocrinol. 2013, 366, 163–169.
  17. Yoshino, J.; Imai, S.I. A clock ticks in pancreatic β cells. Cell Metab. 2010, 12, 107–108.
  18. Sadacca, L.A.; Lamia, K.A.; DeLemos, A.S.; Blum, B.; Weitz, C.J. An intrinsic circadian clock of the pancreas is required for normal insulin release and glucose homeostasis in mice. Diabetologia 2011, 54, 120–124.
  19. Rakshit, K.; Qian, J.; Ernst, J.; Matveyenko, A.V. Circadian variation of the pancreatic islet transcriptome. Physiol. Genom. 2016, 48, 677–687.
  20. Gil-Lozano, M.; Mingomataj, E.L.; Wu, W.K.; Ridout, S.A.; Brubaker, P.L. Circadian secretion of the intestinal hormone GLP-1 by the rodent L cell. Diabetes 2014, 63, 3674–3685.
  21. Dyar, K.A.; Ciciliot, S.; Wright, L.E.; Biensø, R.S.; Tagliazucchi, G.M.; Patel, V.R.; Forcato, M.; Paz, M.I.P.; Gudiksen, A.; Solagna, F.; et al. Muscle insulin sensitivity and glucose metabolism are controlled by the intrinsic muscle clock. Mol. Metab. 2014, 3, 29–41.
  22. Prasai, M.J.; Mughal, R.S.; Wheatcroft, S.B.; Kearney, M.T.; Grant, P.J.; Scott, E.M. Diurnal variation in vascular and metabolic function in diet-induced obesity: Divergence of insulin resistance and loss of clock rhythm. Diabetes 2013, 62, 1981–1989.
  23. Saad, A.; Man, C.D.; Nandy, D.K.; Levine, J.A.; Bharucha, A.E.; Rizza, R.A.; Basu, R.; Carter, R.E.; Cobelli, C.; Kudva, Y.C.; et al. Diurnal pattern to insulin secretion and insulin action in healthy individuals. Diabetes 2012, 61, 2691–2700.
  24. Basu, A.; Joshi, N.; Miles, J.; Carter, R.E.; Rizza, R.A.; Basu, R. Paradigm shifts in nocturnal glucose control in type 2 diabetes. J. Clin. Endocrinol. Metab. 2018, 103, 3801–3809.
  25. Lindgren, O.; Mari, A.; Deacon, C.F.; Carr, R.D.; Winzell, M.S.; Vikman, J.; Ahrén, B. Differential islet and incretin hormone responses in morning versus afternoon after standardized meal in healthy men. J. Clin. Endocrinol. Metab. 2009, 94, 2887–2892.
  26. Ruddick-Collins, L.C.; Johnston, J.D.; Morgan, P.J.; Johnstone, A.M. The Big Breakfast Study: Chrono-nutrition influence on energy expenditure and bodyweight. Nutr. Bull. 2018, 43, 174–183.
  27. Jamshed, H.; Beyl, R.A.; Manna, D.L.D.; Yang, E.S.; Ravussin, E.; Peterson, C.M. Early time-restricted feeding improves 24-hour glucose levels and affects markers of the circadian clock, aging, and autophagy in humans. Nutrients 2019, 11, 1234.
  28. Bo, S.; Fadda, M.; Castiglione, A.; Ciccone, G.; De Francesco, A.; Fedele, D.; Guggino, A.; Parasiliti Caprino, M.; Ferrara, S.; Vezio Boggio, M.; et al. Is the timing of caloric intake associated with variation in diet-induced thermogenesis and in the metabolic pattern? A randomized cross-over study. Int. J. Obes. 2015, 39, 1689–1695.
  29. Morgan, L.M.; Shi, J.W.; Hampton, S.M.; Frost, G. Effect of meal timing and glycaemic index on glucose control and insulin secretion in healthy volunteers. Br. J. Nutr. 2012, 108, 1286–1291.
  30. Ravussin, E.; Beyl, R.A.; Poggiogalle, E.; Hsia, D.S.; Peterson, C.M. Early Time-Restricted Feeding Reduces Appetite and Increases Fat Oxidation but Does Not Affect Energy Expenditure in Humans. Obesity 2019, 27, 1244–1254.
  31. Gibbs, M.; Harrington, D.; Starkey, S.; Williams, P.; Hampton, S. Diurnal postprandial responses to low and high glycaemic index mixed meals. Clin. Nutr. 2014, 33, 889–894.
  32. Nitta, A.; Imai, S.; Kajiyama, S.; Miyawaki, T.; Matsumoto, S.; Ozasa, N.; Hashimoto, Y.; Tanaka, M.; Fukui, M. Impact of different timing of consuming sweet snack on postprandial glucose excursions in healthy women. Diabetes Metab. 2019, 45, 369–374.
  33. Van Cauter, E.; Shapiro, E.T.; Tillil, H.; Polonsky, K.S. Circadian modulation of glucose and insulin responses to meals: Relationship to cortisol rhythm. Am. J. Physiol. Endocrinol. Metab. 1992, 262.
  34. Scheer, F.A.J.L.; Hilton, M.F.; Mantzoros, C.S.; Shea, S.A. Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc. Natl. Acad. Sci. USA 2009, 106, 4453–4458.
  35. Jakubowicz, D.; Wainstein, J.; Ahrén, B.; Bar-Dayan, Y.; Landau, Z.; Rabinovitz, H.R.; Froy, O. High-energy breakfast with low-energy dinner decreases overall daily hyperglycaemia in type 2 diabetic patients: A randomised clinical trial. Diabetologia 2015, 58, 912–919.
  36. Stenvers, D.J.; Jongejan, A.; Atiqi, S.; Vreijling, J.P.; Limonard, E.J.; Endert, E.; Baas, F.; Moerland, P.D.; Fliers, E.; Kalsbeek, A.; et al. Diurnal rhythms in the white adipose tissue transcriptome are disturbed in obese individuals with type 2 diabetes compared with lean control individuals. Diabetologia 2019, 62, 704–716.
  37. Morris, C.J.; Yang, J.N.; Garcia, J.I.; Myers, S.; Bozzi, I.; Wang, W.; Buxton, O.M.; Shea, S.A.; Scheer, F.A.J.L. Endogenous circadian system and circadian misalignment impact glucose tolerance via separate mechanisms in humans. Proc. Natl. Acad. Sci. USA 2015, 112, E2225–E2234.
  38. Wehrens, S.M.T.; Christou, S.; Isherwood, C.; Middleton, B.; Gibbs, M.A.; Archer, S.N.; Skene, D.J.; Johnston, J.D. Meal Timing Regulates the Human Circadian System. Curr. Biol. 2017, 27, 1768–1775.e3.
  39. Jakubowicz, D.; Barnea, M.; Wainstein, J.; Froy, O. High caloric intake at breakfast vs. dinner differentially influences weight loss of overweight and obese women. Obesity 2013, 21, 2504–2512.
  40. Jakubowicz, D.; Froy, O.; Wainstein, J.; Boaz, M. Meal timing and composition influence ghrelin levels, appetite scores and weight loss maintenance in overweight and obese adults. Steroids 2012, 77, 323–331.
  41. Sherman, H.; Frumin, I.; Gutman, R.; Chapnik, N.; Lorentz, A.; Meylan, J.; le Coutre, J.; Froy, O. Long-term restricted feeding alters circadian expression and reduces the level of inflammatory and disease markers. J. Cell. Mol. Med. 2011, 15, 2745–2759.
  42. Hatori, M.; Vollmers, C.; Zarrinpar, A.; DiTacchio, L.; Bushong, E.A.; Gill, S.; Leblanc, M.; Chaix, A.; Joens, M.; Fitzpatrick, J.A.J.; et al. Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet. Cell Metab. 2012, 15, 848–860.
  43. Jakubowicz, D.; Wainstein, J.; Landau, Z.; Raz, I.; Ahren, B.; Chapnik, N.; Ganz, T.; Menaged, M.; Barnea, M.; Bar-Dayan, Y.; et al. Influences of Breakfast on Clock Gene Expression and Postprandial Glycemia in Healthy Individuals and Individuals with Diabetes: A Randomized Clinical Trial. Diabetes Care 2017, 40, 1573–1579.
  44. Chaix, A.; Zarrinpar, A.; Miu, P.; Panda, S. Time-restricted feeding is a preventative and therapeutic intervention against diverse nutritional challenges. Cell Metab. 2014, 20, 991–1005.
  45. Mekary, R.A.; Giovannucci, E.; Willett, W.C.; Van Dam, R.M.; Hu, F.B. Eating patterns and type 2 diabetes risk in men: Breakfast omission, eating frequency, and snacking. Am. J. Clin. Nutr. 2012, 95, 1182–1189.
  46. Nimitphong, H.; Siwasaranond, N.; Saetung, S.; Thakkinstian, A.; Ongphiphadhanakul, B.; Reutrakul, S. The relationship among breakfast time, morningness–eveningness preference and body mass index in Type 2 diabetes. Diabet. Med. 2018, 35, 964–971.
  47. Reutrakul, S.; Hood, M.M.; Crowley, S.J.; Morgan, M.K.; Teodori, M.; Knutson, K.L. The relationship between breakfast skipping, chronotype, and glycemic control in type 2 diabetes. Chronobiol. Int. 2014, 31, 64–71.
  48. Arble, D.M.; Bass, J.; Laposky, A.D.; Vitaterna, M.H.; Turek, F.W. Circadian timing of food intake contributes to weight gain. Obesity 2009, 17, 2100–2102.
  49. Wu, T.; Sun, L.; Zhuge, F.; Guo, X.; Zhao, Z.; Tang, R.; Chen, Q.; Chen, L.; Kato, H.; Fu, Z. Differential roles of breakfast and supper in rats of a daily three-meal schedule upon circadian regulation and physiology. Chronobiol. Int. 2011, 28, 890–903.
  50. Fuse, Y.; Hirao, A.; Kuroda, H.; Otsuka, M.; Tahara, Y.; Shibata, S. Differential roles of breakfast only (one meal per day) and a bigger breakfast with a small dinner (two meals per day) in mice fed a high-fat diet with regard to induced obesity and lipid metabolism. J. Circadian Rhythms 2012, 10.
  51. Sherman, H.; Genzer, Y.; Cohen, R.; Chapnik, N.; Madar, Z.; Froy, O. Timed high-fat diet resets circadian metabolism and prevents obesity. FASEB J. 2012, 26, 3493–3502.
  52. Reinke, H.; Asher, G. Crosstalk between metabolism and circadian clocks. Nat. Rev. Mol. Cell Biol. 2019, 20, 227–241.
  53. St-Onge, M.P.; Ard, J.; Baskin, M.L.; Chiuve, S.E.; Johnson, H.M.; Kris-Etherton, P.; Varady, K. Meal Timing and Frequency: Implications for Cardiovascular Disease Prevention: A Scientific Statement from the American Heart Association. Circulation 2017, 135, e96–e121.
  54. Ando, H.; Ushijima, K.; Yanagihara, H.; Hayashi, Y.; Takamura, T.; Kaneko, S.; Fujimura, A. Clock gene expression in the liver and adipose tissues of non-obese type 2 diabetic Goto-Kakizaki rats. Clin. Exp. Hypertens. 2009, 31, 201–207.
  55. Vieira, E.; Burris, T.P.; Quesada, I. Clock genes, pancreatic function, and diabetes. Trends Mol. Med. 2014, 20, 685–693.
  56. Jakubowicz, D.; Wainstein, J.; Ahren, B.; Landau, Z.; Bar-Dayan, Y.; Froy, O. Fasting Until Noon Triggers Increased Postprandial Hyperglycemia and Impaired Insulin Response after Lunch and Dinner in Individuals with Type 2 Diabetes: A Randomized Clinical Trial. Diabetes Care 2015, 38, 1820–1826.
  57. Shimizu, H.; Hanzawa, F.; Kim, D.; Sun, S.; Laurent, T.; Umeki, M.; Ikeda, S.; Mochizuki, S.; Oda, H. Delayed first active-phase meal, a breakfastskipping model, led to increased body weight and shifted the circadian oscillation of the hepatic clock and lipid metabolism-related genes in rats fed a high-fat diet. PLoS ONE 2018, 13, e0206669.
  58. Kim, Y.H.; Lazar, M.A. Transcriptional control of circadian rhythms and metabolism: A matter of time and space. Endocr. Rev. 2021, 41, 707–732.
  59. Pilorz, V.; Astiz, M.; Heinen, K.O.; Rawashdeh, O.; Oster, H. The Concept of Coupling in the Mammalian Circadian Clock Network. J. Mol. Biol. 2020, 432, 3618–3638.
  60. Kuang, J.; Hou, X.; Zhang, J.; Chen, Y.; Su, Z. Identification of insulin as a novel retinoic acid receptor-related orphan receptor α target gene. FEBS Lett. 2014, 588, 1071–1079.
  61. Johnston, J.D. Physiological responses to food intake throughout the day. Nutr. Res. Rev. 2014, 27, 107–118.
  62. Sun, C.; Zhang, F.; Ge, X.; Yan, T.; Chen, X.; Shi, X.; Zhai, Q. SIRT1 Improves Insulin Sensitivity under Insulin-Resistant Conditions by Repressing PTP1B. Cell Metab. 2007, 6, 307–319.
  63. Biancolin, A.D.; Martchenko, A.; Mitova, E.; Gurges, P.; Michalchyshyn, E.; Chalmers, J.A.; Doria, A.; Mychaleckyj, J.C.; Adriaenssens, A.E.; Reimann, F.; et al. The core clock gene, Bmal1, and its downstream target, the SNARE regulatory protein secretagogin, are necessary for circadian secretion of glucagon-like peptide-1. Mol. Metab. 2020, 31, 124–137.
  64. Taira, A.; Arita, E.; Matsumoto, E.; Oohira, A.; Iwase, K.; Hiwasa, T.; Yokote, K.; Shibata, S.; Takiguchi, M. Systemic oscillator-driven and nutrient-responsive hormonal regulation of daily expression rhythms for gluconeogenic enzyme genes in the mouse liver. Chronobiol. Int. 2019, 36, 591–615.
  65. Pérez-Mendoza, M.; Rivera-Zavala, J.B.; Díaz-Muñoz, M. Daytime restricted feeding modifies the daily variations of liver gluconeogenesis: Adaptations in biochemical and endocrine regulators. Chronobiol. Int. 2014, 31, 815–828.
  66. Zhang, E.E.; Liu, Y.; Dentin, R.; Pongsawakul, P.Y.; Liu, A.C.; Hirota, T.; Nusinow, D.A.; Sun, X.; Landais, S.; Kodama, Y.; et al. Cryptochrome mediates circadian regulation of cAMP signaling and hepatic gluconeogenesis. Nat. Med. 2010, 16, 1152–1156.
  67. Hardie, D.G.; Ross, F.A.; Hawley, S.A. AMPK: A nutrient and energy sensor that maintains energy homeostasis. Nat. Rev. Mol. Cell Biol. 2012, 13, 251–262.
  68. Asher, G.; Gatfield, D.; Stratmann, M.; Reinke, H.; Dibner, C.; Kreppel, F.; Mostoslavsky, R.; Alt, F.W.; Schibler, U. SIRT1 Regulates Circadian Clock Gene Expression through PER2 Deacetylation. Cell 2008, 134, 317–328.
  69. Pinho, A.V.; Bensellam, M.; Wauters, E.; Rees, M.; Giry-Laterriere, M.; Mawson, A.; Ly, L.Q.; Biankin, A.V.; Wu, J.; Laybutt, D.R.; et al. Pancreas-specific Sirt1-deficiency in mice compromises β-cell function without development of hyperglycemia. PLoS ONE 2015, 10, e0128012.
  70. Nakahata, Y.; Sahar, S.; Astarita, G.; Kaluzova, M.; Sassone-Corsi, P. Circadian Control of the NAD+ Salvage Pathway by CLOCK-SIRT1. Science 2009, 324, 654–657.
  71. Wefers, J.; Van Moorsel, D.; Hansen, J.; Connell, N.J.; Havekes, B.; Hoeks, J.; Van Marken Lichtenbelt, W.D.; Duez, H.; Phielix, E.; Kalsbeek, A.; et al. Circadian misalignment induces fatty acid metabolism gene profiles and compromises insulin sensitivity in human skeletal muscle. Proc. Natl. Acad. Sci. USA 2018, 115.
  72. Vetter, C.; Devore, E.E.; Ramin, C.A.; Speizer, F.E.; Willett, W.C.; Schernhammer, E.S. Mismatch of sleep and work timing and risk of type 2 diabetes. Diabetes Care 2015, 38, 1707–1713.
  73. Kahleova, H.; Belinova, L.; Malinska, H.; Oliyarnyk, O.; Trnovska, J.; Skop, V.; Kazdova, L.; Dezortova, M.; Hajek, M.; Tura, A.; 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, 57, 1552–1560.
  74. Rabinovitz, H.R.; Boaz, M.; Ganz, T.; Jakubowicz, D.; Matas, Z.; Madar, Z.; Wainstein, J. Big breakfast rich in protein and fat improves glycemic control in type 2 diabetics. Obesity 2014, 22, E46–E54.
  75. Jakubowicz, D.; Wainstein, J.; Landau, Z.; Ahren, B.; Barnea, M.; Bar-Dayan, Y.; Froy, O. High-energy breakfast based on whey protein reduces body weight, postprandial glycemia and HbA 1C in Type 2 diabetes. J. Nutr. Biochem. 2017, 49, 1–7.
  76. Jakubowicz, D.; Froy, O.; Ahrén, B.; Boaz, M.; Landau, Z.; Bar-Dayan, Y.; Ganz, T.; Barnea, M.; Wainstein, J. Incretin, insulinotropic and glucose-lowering effects of whey protein pre-load in type 2 diabetes: A randomised clinical trial. Diabetologia 2014, 57, 1807–1811.
  77. Sutton, E.F.; Beyl, R.; Early, K.S.; Cefalu, W.T.; Ravussin, E.; Peterson, C.M. Early Time-Restricted Feeding Improves Insulin Sensitivity, Blood Pressure, and Oxidative Stress Even without Weight Loss in Men with Prediabetes. Cell Metab. 2018, 27, 1212–1221e.3.
  78. Lee, S.H.; Tura, A.; Mari, A.; Ko, S.H.; Kwon, H.S.; Song, K.H.; Yoon, K.H.; Lee, K.W.; Ahn, Y.B. Potentiation of the early-phase insulin response by a prior meal contributes to the second-meal phenomenon in type 2 diabetes. Am. J. Physiol. Endocrinol. Metab. 2011, 301.
  79. Jovanovic, A.; Gerrard, J.; Taylor, R. The second-meal phenomenon in type 2 diabetes. Diabetes Care 2009, 32, 1199–1201.
  80. Korsgaard, T.V.; Colding-Jørgensen, M. Time-dependent mechanisms in β-cells glucose sensing. J. Biol. Phys. 2006, 32, 289–306.
  81. Goginashvili, A.; Zhang, Z.; Erbs, E.; Spiegelhalter, C.; Kessler, P.; Mihlan, M.; Pasquier, A.; Krupina, K.; Schieber, N.; Cinque, L.; et al. Insulin granules. Insulin secretory granules control autophagy in pancreatic β cells. Science 2015, 347, 878–882.
  82. Efendic, S.; Portwood, N. Overview of incretin hormones. Horm. Metab. Res. 2004, 36, 742–746.
  83. Richards, J.; Diaz, A.N.; Gumz, M.L. Clock genes in hypertension: Novel insights from rodent models. Blood Press Monit. 2014, 19, 249–254.
  84. Garaulet, M.; Gómez-Abellán, P.; Alburquerque-Béjar, J.J.; Lee, Y.C.; Ordovás, J.M.; Scheer, F.A.J.L. Timing of food intake predicts weight loss effectiveness. Int. J. Obes. 2013, 37, 604–611.
  85. Rains, T.M.; Leidy, H.J.; Sanoshy, K.D.; Lawless, A.L.; Maki, K.C. A randomized, controlled, crossover trial to assess the acute appetitive and metabolic effects of sausage and egg-based convenience breakfast meals in overweight premenopausal women. Nutr. J. 2015, 14.
  86. Park, Y.M.; Heden, T.D.; Liu, Y.; Nyhoff, L.M.; Thyfault, J.P.; Leidy, H.J.; Kanaley, J.A. A high-protein breakfast induces greater insulin and glucose-dependent insulinotropic peptide responses to a subsequent lunch meal in individuals with type 2 diabetes. J. Nutr. 2015, 145, 452–458.
  87. Bendtsen, L.Q.; Lorenzen, J.K.; Larsen, T.M.; van Baak, M.; Papadaki, A.; Martinez, J.A.; Handjieva-Darlenska, T.; Jebb, S.A.; Kunešová, M.; Pfeiffer, A.F.; et al. Associations between dairy protein intake and body weight and risk markers of diabetes and CVD during weight maintenance. Br. J. Nutr. 2014, 111, 944–953.
  88. Pasiakos, S.M. Metabolic advantages of higher protein diets and benefits of dairy foods on weight management, glycemic regulation, and bone. J. Food Sci. 2015, 80, A2–A7.
  89. Gunnerud, U.J.; Heinzle, C.; Holst, J.J.; Östman, E.M.; Björck, I.M.E. Effects of pre-meal drinks with protein and amino acids on glycemic and metabolic responses at a subsequent composite meal. PLoS ONE 2012, 7, e44731.
  90. Nilsson, M.; Holst, J.J.; Björck, I.M. Metabolic effects of amino acid mixtures and whey protein in healthy subjects: Studies using glucose-equivalent drinks. Am. J. Clin. Nutr. 2007, 85, 996–1004.
  91. Frid, A.H.; Nilsson, M.; Holst, J.J.; Björck, I.M.E. Effect of whey on blood glucose and insulin responses to composite breakfast and lunch meals in type 2 diabetic subjects. Am. J. Clin. Nutr. 2005, 82, 69–75.
  92. Ma, J.; Stevens, J.E.; Cukier, K.; Maddox, A.F.; Wishart, J.M.; Jones, K.L.; Clifton, P.M.; Horowitz, M.; Rayner, C.K. Effects of a protein preload on gastric emptying, glycemia, and gut hormones after a carbohydrate meal in diet-controlled type 2 diabetes. Diabetes Care 2009, 32, 1600–1602.
  93. Mignone, L.E. Whey protein: The “whey” forward for treatment of type 2 diabetes? World J. Diabetes 2015, 6, 1274.
  94. Jakubowicz, D.; Froy, O. Biochemical and metabolic mechanisms by which dietary whey protein may combat obesity and Type 2 diabetes. J. Nutr. Biochem. 2013, 24, 1–5.
  95. Gillespie, A.L.; Calderwood, D.; Hobson, L.; Green, B.D. Whey proteins have beneficial effects on intestinal enteroendocrine cells stimulating cell growth and increasing the production and secretion of incretin hormones. Food Chem. 2015, 189, 120–128.
  96. Xu, G.; Hong, X.; Tang, H.; Jiang, S.; Liu, F.; Shen, Z.; Li, Z.; Zhang, W. Ghrelin regulates GLP-1 production through mTOR signaling in L cells. Mol. Cell. Endocrinol. 2015, 416, 9–18.
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