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Meal induced gut hormone secretion is altered in aerobically trained compared to sedentary young healthy males

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Abstract

Postprandial insulin release is lower in healthy aerobically trained (T) compared to untrained (UT) individuals. This may be mediated by a lower release of the two incretin hormones [glucagon like peptide-1 (GLP-1) and glucose-dependent insulinotropic polypeptide (GIP)] in T. The aim of this study was to assess and compare gut hormone response and satiety changes after a liquid meal intake in young, healthy T and UT males. Postprandial gut hormone release and subjective feelings of hunger, satiety, fullness and prospective food consumption were assessed before and frequently for the following 3 h after a 200 ml liquid meal (1,260 kJ and 27, 41 and 32 energy % as protein, carbohydrates and fat, respectively) in ten T and ten UT young, healthy male subjects. The insulin and GIP responses were markedly lower in T than UT and correlated during the first 30 min after the liquid meal. Baseline GLP-1 concentration was higher in T versus UT, but the response in the following 3 h after a liquid meal was similar in T and UT. Satiety measures did not differ between groups throughout the test. It is possible that in aerobically T subjects, a lower GIP release is partly responsible for a lower postprandial incretin stimulated insulin secretion.

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Abbreviations

IL-6:

Interleukin-6

PP:

Pancreatic polypeptide

PFC:

Prospective food consumption

T:

Aerobically trained

UT:

Untrained

VO2max:

Maximal oxygen uptake

FFA:

Free fatty acids

DPP-4:

Dipeptidyl peptidase-4

GLP-2:

Glucagon-like peptide-2

AUC:

Area under the curve

BMI:

Body mass index

LBM:

Lean body mass

GIP:

Glucose-dependent insulinotropic polypeptide

GLP-1:

Glucagon-like peptide-1

PYY:

Peptide YY

VIP:

Vasoactive intestinal polypeptide

References

  • Aarnio P, Lauritsen T, Dela F (2001) Insulin secretion and glucose kinetics during exercise with and without pharmacological alpha(1)- and alpha(2)-receptor blockade. Diabetes 50:1834–1843

    Article  PubMed  CAS  Google Scholar 

  • Brooks GA, Mercier J (1994) Balance of carbohydrate and lipid utilization during exercise: the “crossover” concept. J Appl Physiol 76:2253–2261

    PubMed  CAS  Google Scholar 

  • Broom DR, Stensel DJ, Bishop NC, Burns SF, Miyashita M (2007) Exercise-induced suppression of acylated ghrelin in humans. J Appl Physiol 102:2165–2171

    Article  PubMed  CAS  Google Scholar 

  • Broom DR, Batterham RL, King JA, Stensel DJ (2009) Influence of resistance and aerobic exercise on hunger, circulating levels of acylated ghrelin, and peptide YY in healthy males. Am J Physiol Regul Integr Comp Physiol 296:R29–R35

    Article  PubMed  CAS  Google Scholar 

  • Caudwell P, Finlayson G, Gibbons C, Hopkins M, King N, Naslund E, Blundell JE (2013) Resting metabolic rate is associated with hunger, self-determined meal size, and daily energy intake and may represent a marker for appetite. Am J Clin Nutr 97:7–14

    Article  PubMed  CAS  Google Scholar 

  • Dela F, Mikines KJ, Von LM, Galbo H (1991) Effect of training on response to a glucose load adjusted for daily carbohydrate intake. Am J Physiol 260:E14–E20

    PubMed  CAS  Google Scholar 

  • Dela F, Mikines KJ, Von LM, Secher NH, Galbo H (1992) Effect of training on insulin-mediated glucose uptake in human muscle. Am J Physiol 263:E1134–E1143

    PubMed  CAS  Google Scholar 

  • Dupre J, Ross SA, Watson D, Brown JC (1973) Stimulation of insulin secretion by gastric inhibitory polypeptide in man. J Clin Endocrinol Metab 37:826–828

    Article  PubMed  CAS  Google Scholar 

  • Essen-Gustavsson B, Henriksson J (1984) Enzyme levels in pools of microdissected human muscle fibres of identified type. Adaptive response to exercise. Acta Physiol Scand 120:505–515

    Article  PubMed  CAS  Google Scholar 

  • Faerch K, Borch-Johnsen K, Holst JJ, Vaag A (2009) Pathophysiology and aetiology of impaired fasting glycaemia and impaired glucose tolerance: does it matter for prevention and treatment of type 2 diabetes? Diabetologia 52:1714–1723

    Article  PubMed  CAS  Google Scholar 

  • Galbo H (1983) Hormonal and metabolic adaptation to exercise. Thieme-Stratton Inc, New York

    Google Scholar 

  • Galbo H, Holst JJ, Christensen NJ (1975) Glucagon and plasma catecholamine responses to graded and prolonged exercise in man. J Appl Physiol 38:70–76

    PubMed  CAS  Google Scholar 

  • Greenberg GR, Pokol-Daniel S (1994) Neural modulation of glucose-dependent insulinotropic peptide (GIP) and insulin secretion in conscious dogs. Pancreas 9:531–535

    Article  PubMed  CAS  Google Scholar 

  • Hansen L, Lampert S, Mineo H, Holst JJ (2004) Neural regulation of glucagon-like peptide-1 secretion in pigs. Am J Physiol Endocrinol Metab 287:E939–E947

    Article  PubMed  CAS  Google Scholar 

  • Hartmann B, Johnsen AH, Orskov C, Adelhorst K, Thim L, Holst JJ (2000) Structure, measurement, and secretion of human glucagon-like peptide-2. Peptides 21:73–80

    Article  PubMed  CAS  Google Scholar 

  • Hilsted J, Galbo H, Sonne B, Schwartz T, Fahrenkrug J, de Muckadell OB, Lauritsen KB, Tronier B (1980) Gastroenteropancreatic hormonal changes during exercise. Am J Physiol 239:G136–G140

    PubMed  CAS  Google Scholar 

  • Holloszy JO (2008) Regulation by exercise of skeletal muscle content of mitochondria and GLUT4. J Physiol Pharmacol 59(Suppl 7):5–18

    PubMed  Google Scholar 

  • Holloszy JO, Skinner JS, Barry AJ, Cureton TK (1964) Effect of physical conditioning on cardiovascular function. A ballistocardiographic study. Am J Cardiol 14:761–770

    Article  PubMed  CAS  Google Scholar 

  • Holst JJ (1982) Evidence that enteroglucagon (II) is identical with the C-terminal sequence (residues 33–69) of glicentin. Biochem J 207:381–388

    PubMed  CAS  Google Scholar 

  • Holst JJ (2007) The physiology of glucagon-like peptide 1. Physiol Rev 87:1409–1439

    Article  PubMed  CAS  Google Scholar 

  • Holst JJ, Orskov C, Nielsen OV, Schwartz TW (1987) Truncated glucagon-like peptide I, an insulin-releasing hormone from the distal gut. FEBS Lett 211:169–174

    Article  PubMed  CAS  Google Scholar 

  • Kelly KR, Brooks LM, Solomon TP, Kashyap SR, O’Leary VB, Kirwan JP (2009) The glucose-dependent insulinotropic polypeptide and glucose-stimulated insulin response to exercise training and diet in obesity. Am J Physiol Endocrinol Metab 296:E1269–E1274

    Article  PubMed  CAS  Google Scholar 

  • King NA, Lluch A, Stubbs RJ, Blundell JE (1997) High dose exercise does not increase hunger or energy intake in free living males. Eur J Clin Nutr 51:478–483

    Article  PubMed  CAS  Google Scholar 

  • King NA, Hopkins M, Caudwell P, Stubbs RJ, Blundell JE (2008) Individual variability following 12 weeks of supervised exercise: identification and characterization of compensation for exercise-induced weight loss. Int J Obes (Lond) 32:177–184

    Article  CAS  Google Scholar 

  • King JA, Wasse LK, Ewens J, Crystallis K, Emmanuel J, Batterham RL, Stensel DJ (2011) Differential acylated ghrelin, peptide YY3-36, appetite, and food intake responses to equivalent energy deficits created by exercise and food restriction. J Clin Endocrinol Metab 96:1114–1121

    Article  PubMed  CAS  Google Scholar 

  • Kjaer M, Galbo H (1988) Effect of physical training on the capacity to secrete epinephrine. J Appl Physiol 64:11–16

    PubMed  CAS  Google Scholar 

  • Legakis IN, Mantzouridis T, Saramantis A, Phenekos C, Tzioras C, Mountokalakis T (2000) Human galanin secretion is increased upon normal exercise test in middle-age individuals. Endocr Res 26:357–364

    Article  PubMed  CAS  Google Scholar 

  • Leidy HJ, Gardner JK, Frye BR, Snook ML, Schuchert MK, Richard EL, Williams NI (2004) Circulating ghrelin is sensitive to changes in body weight during a diet and exercise program in normal-weight young women. J Clin Endocrinol Metab 89:2659–2664

    Article  PubMed  CAS  Google Scholar 

  • Manshouri M, Ghanbari-Niaki A, Kraemer RR, Shemshaki A (2008) Time course alterations of plasma obestatin and growth hormone levels in response to short-term anaerobic exercise training in college women. Appl Physiol Nutr Metab 33:1246–1249

    Article  PubMed  CAS  Google Scholar 

  • Martins C, Truby H, Morgan LM (2007) Short-term appetite control in response to a 6-week exercise programme in sedentary volunteers. Br J Nutr 98:834–842

    PubMed  CAS  Google Scholar 

  • Martins C, Kulseng B, King NA, Holst JJ, Blundell JE (2010) The effects of exercise-induced weight loss on appetite-related peptides and motivation to eat. J Clin Endocrinol Metab 95:1609–1616

    Article  PubMed  CAS  Google Scholar 

  • Martins C, Kulseng B, Rehfeld JF, King NA, Blundell JE (2013) Effect of chronic exercise on appetite control in overweight and obese individuals. Med Sci Sports Exerc 45:805–812

    Article  PubMed  Google Scholar 

  • Mikines KJ, Sonne B, Tronier B, Galbo H (1989) Effects of training and detraining on dose-response relationship between glucose and insulin secretion. Am J Physiol 256:E588–E596

    PubMed  CAS  Google Scholar 

  • Nappo F, Esposito K, Cioffi M, Giugliano G, Molinari AM, Paolisso G, Marfella R, Giugliano D (2002) Postprandial endothelial activation in healthy subjects and in type 2 diabetic patients: role of fat and carbohydrate meals. J Am Coll Cardiol 39:1145–1150

    Article  PubMed  CAS  Google Scholar 

  • O’Connor AM, Johnston CF, Buchanan KD, Boreham C, Trinick TR, Riddoch CJ (1995) Circulating gastrointestinal hormone changes in marathon running. Int J Sports Med 16:283–287

    Article  PubMed  Google Scholar 

  • Orskov C, Holst JJ, Knuhtsen S, Baldissera FG, Poulsen SS, Nielsen OV (1986) Glucagon-like peptides GLP-1 and GLP-2, predicted products of the glucagon gene, are secreted separately from pig small intestine but not pancreas. Endocrinology 119:1467–1475

    Article  PubMed  CAS  Google Scholar 

  • Orskov C, Rabenhoj L, Wettergren A, Kofod H, Holst JJ (1994) Tissue and plasma concentrations of amidated and glycine-extended glucagon-like peptide I in humans. Diabetes 43:535–539

    Article  PubMed  CAS  Google Scholar 

  • Ravussin E, Lillioja S, Anderson TE, Christin L, Bogardus C (1986) Determinants of 24-hour energy expenditure in man. Methods and results using a respiratory chamber. J Clin Invest 78:1568–1578

    Article  PubMed  CAS  Google Scholar 

  • Rocca AS, Brubaker PL (1999) Role of the vagus nerve in mediating proximal nutrient-induced glucagon-like peptide-1 secretion. Endocrinology 140:1687–1694

    Article  PubMed  CAS  Google Scholar 

  • Romon M, Gomila S, Hincker P, Soudan B, Dallongeville J (2006) Influence of weight loss on plasma ghrelin responses to high-fat and high-carbohydrate test meals in obese women. J Clin Endocrinol Metab 91:1034–1041

    Article  PubMed  CAS  Google Scholar 

  • Scheid JL, de Souza MJ, Leidy HJ, Williams NI (2011) Ghrelin but not peptide YY is related to change in body weight and energy availability. Med Sci Sports Exerc 43:2063–2071

    Article  PubMed  CAS  Google Scholar 

  • Soffer EE, Merchant RK, Duethman G, Launspach J, Gisolfi C, Adrian TE (1993) Effect of graded exercise on esophageal motility and gastroesophageal reflux in trained athletes. Dig Dis Sci 38:220–224

    Article  PubMed  CAS  Google Scholar 

  • Tschop M, Weyer C, Tataranni PA, Devanarayan V, Ravussin E, Heiman ML (2001) Circulating ghrelin levels are decreased in human obesity. Diabetes 50:707–709

    Article  PubMed  CAS  Google Scholar 

  • Vilsboll T, Krarup T, Madsbad S, Holst JJ (2003) Both GLP-1 and GIP are insulinotropic at basal and postprandial glucose levels and contribute nearly equally to the incretin effect of a meal in healthy subjects. Regul Pept 114:115–121

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank the laboratory technician Jeppe Bach for his technical assistance during the study.

Conflict of interest

The authors declare that there is no conflict of interest associated with this manuscript.

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Authors and Affiliations

  1. Department of Biomedical Sciences, Center for Healthy Aging, Xlab, University of Copenhagen, Blegdamsvej 3b, 2200, Copenhagen, Denmark

    Michael Taulo Lund, Lærke Taudorf, Jørn Wulff Helge & Flemming Dela

  2. Department of Biomedical Sciences, The Novo Nordisk Foundation Center for Basic Metabolic Research, University of Copenhagen, Blegdamsvej 3b, 2200, Copenhagen, Denmark

    Bolette Hartmann & Jens Juel Holst

Authors
  1. Michael Taulo Lund
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  2. Lærke Taudorf
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  3. Bolette Hartmann
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  4. Jørn Wulff Helge
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  5. Jens Juel Holst
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  6. Flemming Dela
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Corresponding author

Correspondence to Michael Taulo Lund.

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Communicated by Keith Phillip George.

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Lund, M.T., Taudorf, L., Hartmann, B. et al. Meal induced gut hormone secretion is altered in aerobically trained compared to sedentary young healthy males. Eur J Appl Physiol 113, 2737–2747 (2013). https://doi.org/10.1007/s00421-013-2711-y

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  • DOI: https://doi.org/10.1007/s00421-013-2711-y

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