Failure of sucrose replacement with the non-nutritive sweetener erythritol to alter GLP-1 or PYY release or test meal size in lean or obese people

Joost Overduin, Tinh-Hai Collet, Nenad Medic, Elana Henning, Julia M Keogh, Faye Forsyth, Cheryl Stephenson, Marja W Kanning, Rianne M A J Ruijschop, I Sadaf Farooqi, Agatha A van der Klaauw, Joost Overduin, Tinh-Hai Collet, Nenad Medic, Elana Henning, Julia M Keogh, Faye Forsyth, Cheryl Stephenson, Marja W Kanning, Rianne M A J Ruijschop, I Sadaf Farooqi, Agatha A van der Klaauw

Abstract

There is considerable interest in the effect of foods containing high intensity sweeteners on satiation. However, less is known about low-calorie bulk sweeteners such as erythritol. In this randomized three-way crossover study, we studied 10 lean and 10 obese volunteers who consumed three test meals on separate occasions: (a) control sucrose meal; (b) isovolumic meal with partial replacement of sucrose by erythritol; (c) isocaloric meal which contained more erythritol but equivalent calories to the control meal. We measured gut hormone levels, hunger and satiety scores, ad libitum food intake, sucrose preference and intake after the manipulations. There was a greater post-prandial excursion in glucose and insulin levels after sucrose than after the erythritol meals. There was no difference in GLP-1/PYY levels or subsequent energy intake and sucrose preference between sucrose control and isovolumic erythritol meals. In lean (but not obese) participants, hunger decreased to a greater extent after the isocaloric erythritol meal compared to the control meal (p = 0.003) reflecting the larger volume of this meal. Replacing sucrose with erythritol leads to comparable hunger and satiety scores, GLP-1 and PYY levels, and subsequent sucrose preference and intake.

Keywords: Erythritol; Glucagon-like peptide 1; Obesity; Peptide YY; Sweeteners.

Copyright © 2016 The Authors. Published by Elsevier Ltd.. All rights reserved.

Figures

Fig. 1
Fig. 1
Hunger and fullness scores after test breakfast, by type and group. Data are presented as mean ± standard error of the mean. In lean participants, hunger (top-left panel) and fullness scores (top-right panel) based on visual analogue scores (VAS) half-hourly after test breakfast consumption did not differ between the sucrose control (solid line) and the isovolumic erythritol meal (dashed line), while hunger scores were lowest and fullness scores highest after the isocaloric erythritol meal (dotted line, p = 0.003 and p = 0.02, respectively). In obese subjects, hunger and fullness scores were similar after consumption of the different test meals (bottom panels).
Fig. 2
Fig. 2
Glucose excursion and insulin secretion after test breakfast, by type and group. Data are presented as mean ± standard error of the mean. Plasma glucose excursion (left panels) and insulin secretion (right panels) peaked the most after sucrose control meal (solid line) compared to the sweetener meals (dashed and dotted lines, all p ≤ 0.007) in both study groups.
Fig. 3
Fig. 3
PYY and GLP-1 secretion after test breakfast, by type and group. Data are presented as mean ± standard error of the mean. In lean subjects, gut hormones glucagon-like peptide-1 (GLP-1, top-left panel) and peptide YY (PYY, top-right panel) increased similarly after the isovolumic erythritol (dashed line) and the sucrose control test breakfasts (solid line, p ≥ 0.76), while they increased more markedly after isocaloric erythritol meal consumption (dotted line, all p ≤ 0.04). The satiety response of GLP-1 and PYY after the different meals was similar in obese participants (bottom panels).

References

    1. Adrian T.E., Ferri G.L., Bacarese-Hamilton A.J., Fuessl H.S., Polak J.M., Bloom S.R. Human distribution and release of a putative new gut hormone, peptide YY. Gastroenterology. 1985;89(5):1070–1077.
    1. Batterham R.L., Heffron H., Kapoor S., Chivers J.E., Chandarana K., Herzog H.…Withers D.J. Critical role for peptide YY in protein-mediated satiation and body-weight regulation. Cell Metabolism. 2006;4(3):223–233.
    1. Bellisle F., Drewnowski A. Intense sweeteners, energy intake and the control of body weight. European Journal of Clinical Nutrition. 2007;61(6):691–700.
    1. Benton D. Can artificial sweeteners help control body weight and prevent obesity? Nutrition Research Reviews. 2005;18(1):63–76.
    1. Brown R.J., Rother K.I. Non-nutritive sweeteners and their role in the gastrointestinal tract. Journal of Clinical Endocrinology and Metabolism. 2012;97(8):2597–2605.
    1. Brown R.J., Walter M., Rother K.I. Ingestion of diet soda before a glucose load augments glucagon-like peptide-1 secretion. Diabetes Care. 2009;32(12):2184–2186.
    1. Cardoso-Junior A., Coelho L.G., Savassi-Rocha P.R., Vignolo M.C., Abrantes M.M., de Almeida A.M.…Lemos Y.V. Gastric emptying of solids and semi-solids in morbidly obese and non-obese subjects: An assessment using the 13C-octanoic acid and 13C-acetic acid breath tests. Obesity Surgery. 2007;17(2):236–241.
    1. de Cock P. Erythritol. In: O'Donnell K., Kearsley M.W., editors. Sweeteners and sugar alternatives in food technology. 2nd ed. Wiley-Blackwell; 2012. pp. 215–241.
    1. Ford H.E., Peters V., Martin N.M., Sleeth M.L., Ghatei M.A., Frost G.S., Bloom S.R. Effects of oral ingestion of sucralose on gut hormone response and appetite in healthy normal-weight subjects. European Journal of Clinical Nutrition. 2011;65(4):508–513.
    1. Goossens J., Röper H. Erythritol: A new bulk sweetener. International Food Ingredients. 1994;1/2:27–33.
    1. Hu F.B. Resolved: There is sufficient scientific evidence that decreasing sugar-sweetened beverage consumption will reduce the prevalence of obesity and obesity-related diseases. Obesity Reviews. 2013;14(8):606–619.
    1. Jang H.J., Kokrashvili Z., Theodorakis M.J., Carlson O.D., Kim B.J., Zhou J.…Egan J.M. Gut-expressed gustducin and taste receptors regulate secretion of glucagon-like peptide-1. Proceedings of the National Academy of Sciences of the United States of America. 2007;104(38):15069–15074.
    1. van der Klaauw A.A., Keogh J.M., Henning E., Blackwood A., Haqq A.M., Purnell J.Q., Farooqi I.S. Postprandial total ghrelin suppression is modulated by melanocortin signaling in humans. Journal of Clinical Endocrinology and Metabolism. 2013;98(2):E288–E292.
    1. Kreymann B., Williams G., Ghatei M.A., Bloom S.R. Glucagon-like peptide-1 7-36: A physiological incretin in man. Lancet. 1987;2(8571):1300–1304.
    1. Lavin J.H., French S.J., Read N.W. The effect of sucrose- and aspartame-sweetened drinks on energy intake, hunger and food choice of female, moderately restrained eaters. International Journal of Obesity and Related Metabolic Disorders. 1997;21(1):37–42.
    1. Livesey G. Health potential of polyols as sugar replacers, with emphasis on low glycaemic properties. Nutrition Research Reviews. 2003;16(2):163–191.
    1. Lomenick J.P., Melguizo M.S., Mitchell S.L., Summar M.L., Anderson J.W. Effects of meals high in carbohydrate, protein, and fat on ghrelin and peptide YY secretion in prepubertal children. Journal of Clinical Endocrinology and Metabolism. 2009;94(11):4463–4471.
    1. Ma J., Bellon M., Wishart J.M., Young R., Blackshaw L.A., Jones K.L.…Rayner C.K. Effect of the artificial sweetener, sucralose, on gastric emptying and incretin hormone release in healthy subjects. American Journal of Physiology-Gastrointestinal and Liver Physiology. 2009;296(4):G735–G739.
    1. Mattes R.D., Popkin B.M. Nonnutritive sweetener consumption in humans: Effects on appetite and food intake and their putative mechanisms. American Journal of Clinical Nutrition. 2009;89(1):1–14.
    1. Munro I.C., Berndt W.O., Borzelleca J.F., Flamm G., Lynch B.S., Kennepohl E.…Modderman J. Erythritol: An interpretive summary of biochemical, metabolic, toxicological and clinical data. Food and Chemical Toxicology. 1998;36(12):1139–1174.
    1. Pepino M.Y., Tiemann C.D., Patterson B.W., Wice B.M., Klein S. Sucralose affects glycemic and hormonal responses to an oral glucose load. Diabetes Care. 2013;36(9):2530–2535.
    1. Peracchi M., Santangelo A., Conte D., Fraquelli M., Tagliabue R., Gebbia C., Porrini M. The physical state of a meal affects hormone release and postprandial thermogenesis. British Journal of Nutrition. 2000;83(6):623–628.
    1. Ranganath L.R., Beety J.M., Morgan L.M., Wright J.W., Howland R., Marks V. Attenuated GLP-1 secretion in obesity: Cause or consequence? Gut. 1996;38(6):916–919.
    1. Rogers P.J., Carlyle J.A., Hill A.J., Blundell J.E. Uncoupling sweet taste and calories: Comparison of the effects of glucose and three intense sweeteners on hunger and food intake. Physiology and Behavior. 1988;43(5):547–552.
    1. le Roux C.W., Batterham R.L., Aylwin S.J., Patterson M., Borg C.M., Wynne K.J.…Bloom S.R. Attenuated peptide YY release in obese subjects is associated with reduced satiety. Endocrinology. 2006;147(1):3–8.
    1. Sadler M., Stowell J.D. Calorie control and weight management. In: O'Donnell K., Kearsley M.W., editors. Sweeteners and sugar alternatives in food technology. 2nd ed. Wiley-Blackwell; 2012. pp. 77–89.
    1. Schofield W.N. Predicting basal metabolic rate, new standards and review of previous work. Human Nutrition. Clinical Nutrition. 1985;39(Suppl 1):5–41.
    1. Steinert R.E., Frey F., Topfer A., Drewe J., Beglinger C. Effects of carbohydrate sugars and artificial sweeteners on appetite and the secretion of gastrointestinal satiety peptides. British Journal of Nutrition. 2011;105(9):1320–1328.
    1. Suez J., Korem T., Zeevi D., Zilberman-Schapira G., Thaiss C.A., Maza O.…Elinav E. Artificial sweeteners induce glucose intolerance by altering the gut microbiota. Nature. 2014;514(7521):181–186.
    1. Swithers S.E., Martin A.A., Davidson T.L. High-intensity sweeteners and energy balance. Physiology and Behavior. 2010;100(1):55–62.
    1. Wölnerhanssen B.K., Cajacob L., Keller N., Doody A., Rehfeld J.F., Drewe J.…Meyer-Gerspach A.C. Gut hormone secretion, gastric emptying, and glycemic responses to erythritol and xylitol in lean and obese subjects. American Journal of Physiology. Endocrinology and Metabolism. 2016;310(11):E1053–E1061.
    1. Wu T., Bound M.J., Standfield S.D., Bellon M., Young R.L., Jones K.L.…Rayner C.K. Artificial sweeteners have no effect on gastric emptying, glucagon-like Peptide-1, or glycemia after oral glucose in healthy humans. Diabetes Care. 2013;36(12):e202–203.

Source: PubMed

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