Mycoprotein reduces energy intake and postprandial insulin release without altering glucagon-like peptide-1 and peptide tyrosine-tyrosine concentrations in healthy overweight and obese adults: a randomised-controlled trial

Jeanne H Bottin, Jonathan R Swann, Eleanor Cropp, Edward S Chambers, Heather E Ford, Mohammed A Ghatei, Gary S Frost, Jeanne H Bottin, Jonathan R Swann, Eleanor Cropp, Edward S Chambers, Heather E Ford, Mohammed A Ghatei, Gary S Frost

Abstract

Dietary mycoprotein decreases energy intake in lean individuals. The effects in overweight individuals are unclear, and the mechanisms remain to be elucidated. This study aimed to investigate the effect of mycoprotein on energy intake, appetite regulation, and the metabolic phenotype in overweight and obese volunteers. In two randomised-controlled trials, fifty-five volunteers (age: 31 (95 % CI 27, 35) years), BMI: 28·0 (95 % CI 27·3, 28·7) kg/m2) consumed a test meal containing low (44 g), medium (88 g) or high (132 g) mycoprotein or isoenergetic chicken meals. Visual analogue scales and blood samples were collected to measure appetite, glucose, insulin, peptide tyrosine-tyrosine (PYY) and glucagon-like peptide-1 (GLP-1). Ad libitum energy intake was assessed after 3 h in part A (n 36). Gastric emptying by the paracetamol method, resting energy expenditure and substrate oxidation were recorded in part B (n 14). Metabonomics was used to compare plasma and urine samples in response to the test meals. Mycoprotein reduced energy intake by 10 % (280 kJ (67 kcal)) compared with chicken at the high content (P=0·009). All mycoprotein meals reduced insulin concentrations compared with chicken (incremental AUClow (IAUClow): -8 %, IAUCmedium: -12 %, IAUChigh: -21 %, P=0·004). There was no significant difference in glucose, PYY, GLP-1, gastric emptying rate and energy expenditure. Following chicken intake, paracetamol-glucuronide was positively associated with fullness. After mycoprotein, creatinine and the deamination product of isoleucine, α-keto-β-methyl-N-valerate, were inversely related to fullness, whereas the ketone body, β-hydroxybutyrate, was positively associated. In conclusion, mycoprotein reduces energy intake and insulin release in overweight volunteers. The mechanism does not involve changes in PYY and GLP-1. The metabonomics analysis may bring new understanding to the appetite regulatory properties of food.

Keywords: Appetite hormones; Energy intake; GAA guanidinoacetic acid; GI gastrointestinal; GLP-1 glucagon-like peptide-1; Gastric emptying; IAUC incremental AUC; Metabonomics; Mycoprotein; Obesity; Overweight; PYY peptide tyrosine-tyrosine; REE resting energy expenditure; T2DM type 2 diabetes mellitus.

Figures

Fig. 1
Fig. 1
Protocol of the study visits. Participants arrived at 08.30 hours in a fasted state. The test meal consisted of a standardised mycoprotein or chicken risotto. The ad libitum meal was consumed 180 min after the test meal until the participant was fully satisfied. Paracetamol was given in part B as a surrogate measurement of gastric emptying. VAS, visual analogue scale.
Fig. 2
Fig. 2
Fullness ratings over time at low (a), medium (b) and high (c) protein contents following the consumption of mycoprotein and chicken. Values are means, with standard errors. * P≤0·05 on repeated-measures linear mixed model and post hoc comparisons with Bonferroni’s correction. , Low chicken; , low mycoprotein; , medium chicken; , medium mycoprotein; , high chicken; , high mycoprotein.
Fig. 3
Fig. 3
Energy intake at ad libitum meal (a) and during the following 24 h (b). Values are means, with standard errors represented by bar charts. * P≤0·05, ** P≤0·01 difference between mycoprotein and chicken analysed with repeated-measures linear mixed model and post hoc comparisons with Bonferroni’s correction. , , , Chicken; , , , mycoprotein; , low protein; , medium protein; , high protein.
Fig. 4
Fig. 4
Plasma concentrations of glucagon-like peptide-1 (GLP-1) and peptide tyrosine-tyrosine (PYY) following the consumption of mycoprotein and chicken. Values are means, with standard errors. , High chicken; , high mycoprotein.
Fig. 5
Fig. 5
Plasma glucose and serum insulin concentrations at low, medium and high-protein contents and insulin sensitivity following the consumption of mycoprotein and chicken. (a–c) Plasma glucose concentrations at low (a), medium (b) and high (c) protein contents. (d–f) Serum insulin concentrations at low (d), medium (e) and high (f) protein contents. * P≤0·05, ** P≤0·01, *** P≤0·001 difference between mycoprotein and chicken analysed by repeated-measures linear mixed model and post hoc comparisons at each time point with Bonferroni’s correction. (g–i) Matsuda (g), Insulinogenic (h) and Disposition (i) indices. Values are means, with standard errors and log-transformed before analysis. * P≤0·05 difference between mycoprotein and chicken analysed by repeated-measures linear mixed model and post hoc comparisons with Bonferroni’s correction. , Low chicken; , low mycoprotein; , medium chicken; , medium mycoprotein; , high chicken; , high mycoprotein; , , , chicken; , , , mycoprotein; , low protein; , medium protein; , high protein.
Fig. 6
Fig. 6
Appetite ratings following the consumption of mycoprotein and chicken: hunger (a), nausea (b), desire to eat (c), prospective food intake (d), fullness (e) and IAUC for all appetite ratings (f). Values are means, with standard errors. IAUC, incremental AUC. , Chicken; , mycoprotein.
Fig. 7
Fig. 7
Serum paracetamol concentrations (a) and gastric emptying rate (b) following the consumption of mycoprotein and chicken. (a) Values are means, with standard errors. (b) Values are mean gastric emptying percentages for all participants with a non-linear fit of the curve. , Chicken; , mycoprotein; , non-linear fit (chicken); , non-linear fit (mycoprotein).
Fig. 8
Fig. 8
Energy expenditure (per kg lean mass) (a), RER (b), carbohydrate oxidation (c), fat oxidation (d) following the consumption of mycoprotein and chicken. Values are means, with standard errors. CHO, carbohydrate. , Chicken; , mycoprotein.
Fig. 9
Fig. 9
Orthogonal projection to latent structures-discriminant analysis models comparing the urinary metabolic profiles of volunteers following chicken and mycoprotein intake (a) and the plasma metabolic profiles 30 v. 180 min after mycoprotein consumption (b). Colour corresponds to the correlation of the metabolites to class discrimination ((a) mycoprotein v. chicken; (b) 30 v. 180 min post-mycoprotein consumption). Colour indicates the strength of correlation. N-acetylcarnitine, carnitine and anserine increase following chicken intake. Guanidinoacetic acid and unknown (2·48) increase following mycoprotein intake. Valine, isoleucine, leucine, and N-acetyl-glycoprotein increase at 180 min. Glucose decreases at 180 min. ppm, Parts per million.
Fig. 10
Fig. 10
Orthogonal projection to latent structure models showing metabolic variation associated with fullness following mycoprotein (a) and chicken (b) intake. (a) Colour indicates the correlation of the metabolites with fullness. After mycoprotein intake, creatinine and the deamination product of isoleucine, α-keto-β-methyl-N-valerate, were inversely related to fullness and β-hydroxybutyrate was positively associated. (b) Significant associations are shown in red. After chicken intake, paracetamol-glucuronide was positively associated with fullness and creatinine was negatively associated.

References

    1. Bensaid A, Tomé D, Gietzen D, et al. (2002) Protein is more potent than carbohydrate for reducing appetite in rats. Physiol Behav 75, 577–582.
    1. Poppitt SD, McCormack D & Buffenstein R (1998) Short-term effects of macronutrient preloads on appetite and energy intake in lean women. Physiol Behav 64, 279–285.
    1. Geliebter AA (1979) Effects of equicaloric loads of protein, fat, and carbohydrate on food intake in the rat and man. Physiol Behav 22, 267–273.
    1. Stubbs RJ, van Wyk MC, Johnstone AM, et al. (1996) Breakfasts high in protein, fat or carbohydrate: effect on within-day appetite and energy balance. Eur J Clin Nutr 50, 409–417.
    1. Lejeune MP, Westerterp KR, Adam TC, et al. (2006) Ghrelin and glucagon-like peptide 1 concentrations, 24-h satiety, and energy and substrate metabolism during a high-protein diet and measured in a respiration chamber. Am J Clin Nutr 83, 89–94.
    1. Booth DA, Chase A & Campbell AT (1970) Relative effectiveness of protein in the late stages of appetite suppression in man. Physiol Behav 5, 1299–1302.
    1. Barkeling B, Rossner S & Bjorvell H (1990) Effects of a high-protein meal (meat) and a high-carbohydrate meal (vegetarian) on satiety measured by automated computerized monitoring of subsequent food intake, motivation to eat and food preferences. Int J Obes 14, 743–751.
    1. Westerterp-Plantenga MS, Lejeune MP, Nijs I, et al. (2004) High protein intake sustains weight maintenance after body weight loss in humans. Int J Obes Relat Metab Disord 28, 57–64.
    1. Wycherley TP, Moran LJ, Clifton PM, et al. (2012) Effects of energy-restricted high-protein, low-fat compared with standard-protein, low-fat diets: a meta-analysis of randomized controlled trials. Am J Clin Nutr 96, 1281–1298.
    1. Krieger JW, Sitren HS, Daniels MJ, et al. (2006) Effects of variation in protein and carbohydrate intake on body mass and composition during energy restriction: a meta-regression. Am J Clin Nutr 83, 260–274.
    1. Leidy HJ, Carnell NS, Mattes RD, et al. (2007) Higher protein intake preserves lean mass and satiety with weight loss in pre-obese and obese women. Obesity 15, 421–424.
    1. Vitaglione P, Lumaga RB, Stanzione A, et al. (2009) Beta-glucan-enriched bread reduces energy intake and modifies plasma ghrelin and peptide YY concentrations in the short term. Appetite 53, 338–344.
    1. Lin N, Li Y, Tang L, et al. (2013) In vivo effect of oat cereal beta-glucan on metabolic indexes and satiety-related hormones in diet-induced obesity C57-Bl mice. Mol Nutr Food Res 57, 1291–1294.
    1. Beck EJ, Tosh SM, Batterham MJ, et al. (2009) Oat beta-glucan increases postprandial cholecystokinin levels, decreases insulin response and extends subjective satiety in overweight subjects. Mol Nutr Food Res 53, 1343–1351.
    1. Clark MJ & Slavin JL (2013) The effect of fibre on satiety and food intake: a systematic review. J Am Coll Nutr 32, 200–211.
    1. Isken F, Klaus S, Osterhoff M, et al. (2010) Effects of long-term soluble vs. insoluble dietary fiber intake on high-fat diet-induced obesity in C57BL/6J mice. J Nutr Biochem 21, 278–284.
    1. Wanders AJ, Jonathan MC, van den Borne JJ, et al. (2013) The effects of bulking, viscous and gel-forming dietary fibres on satiation. Br J Nutr 109, 1330–1337.
    1. Brighenti F, Benini L, Del Rio D, et al. (2006) Colonic fermentation of indigestible carbohydrates contributes to the second-meal effect. Am J Clin Nutr 83, 817–822.
    1. Cani PD, Dewever C & Delzenne NM (2004)) Inulin-type fructans modulate gastrointestinal peptides involved in appetite regulation (glucagon-like peptide-1 and ghrelin) in rats. Br J Nutr 92, 521–526.
    1. Turnbull WH & Ward T (1995) Mycoprotein reduces glycemia and insulinemia when taken with an oral-glucose-tolerance test. Am J Clin Nutr 61, 135–140.
    1. Burley VJ, Paul WA & Blundell JE (1993) Influence of a high-fiber food (myco-protein) on appetite – effects on satiation (within meals) and satiety (following meals). Eur J Clin Nutr 47, 409–418.
    1. Turnbull WH, Walton J & Leeds AR (1993) Acute effects of mycoprotein on subsequent energy intake and appetite variables. Am J Clin Nutr 58, 507–512.
    1. Williamson DA, Geiselman PJ, Lovejoy J, et al. (2006) Effects of consuming mycoprotein, tofu or chicken upon subsequent eating behaviour, hunger and safety. Appetite 46, 41–48.
    1. Batterham RL, Cohen MA, Ellis SM, et al. (2003) Inhibition of food intake in obese subjects by peptide YY3-36. N Engl J Med 349, 941–948.
    1. Kreymann B, Williams G, Ghatei MA, et al. (1987) Glucagon-like peptide-1 7-36: a physiological incretin in man. Lancet 2, 1300–1304.
    1. Matsuda M & DeFronzo RA (1999) Insulin sensitivity indices obtained from oral glucose tolerance testing – comparison with the euglycemic insulin clamp. Diabetes Care 22, 1462–1470.
    1. Seltzer HS, Allen EW, Herron AL Jr, et al. (1967) Insulin secretion in response to glycemic stimulus: relation of delayed initial release to carbohydrate intolerance in mild diabetes mellitus. J Clin Invest 46, 323–335.
    1. Bergman RN, Phillips SL & Cobelli C (1981) Physiologic evaluation of factors controlling glucose tolerance in man: measurement of insulin sensitivity and beta-cell glucose sensitivity from the response to intravenous glucose. J Clin Invest 68, 1456–1467.
    1. Näslund E, Bogefors J, Grybäck P, et al. (2000) Gastric emptying: comparison of scintigraphic, polyethylene glycol dilution, and paracetamol tracer assessment techniques. Scand J Gastroenterol 35, 375–379.
    1. Weir JB (1949) New methods for calculating metabolic rate with special reference to protein metabolism. J Physiol 109, 1–9.
    1. Frayn KN (1983) Calculation of substrate oxidation rates in vivo from gaseous exchange. J Appl Physiol Respir Environ Exerc 55, 628–634.
    1. Beckonert O, Keun HC, Ebbels TM, et al. (2007) Metabolic profiling, metabolomic and metabonomic procedures for NMR spectroscopy of urine, plasma, serum and tissue extracts. Nat Protoc 2, 2692–2703.
    1. Bertenshaw EJ, Lluch A & Yeomans MR (2009) Dose-dependent effects of beverage protein content upon short-term intake. Appetite 52, 580–587.
    1. Astbury NM, Stevenson EJ, Morris P, et al. (2010) Dose-response effect of a whey protein preload on within-day energy intake in lean subjects. Br J Nutr 104, 1858–1867.
    1. Belza A, Ritz C, Sørensen MQ, et al. (2013) Contribution of gastroenteropancreatic appetite hormones to protein-induced satiety. Am J Clin Nutr 97, 980–989.
    1. Naslund E, Bogefors J, Grybäck P, et al. (2000) Gastric emptying: comparison of scintigraphic, polyethylene glycol dilution, and paracetamol tracer assessment techniques. Scand J Gastroenterol 35, 375–379.
    1. Glerup H, Bluhme H, Villadsen GE, et al. (2007) Gastric emptying: a comparison of three methods. Scand J Gastroenterol 42, 1182–1186.
    1. Raben A, Agerholm-Larsen L, Flint A, et al. (2003) Meals with similar energy densities but rich in protein, fat, carbohydrate, or alcohol have different effects on energy expenditure and substrate metabolism but not on appetite and energy intake. Am J Clin Nutr 77, 91–100.
    1. Slavin JL (2005) Dietary fiber and body weight. Nutrition 21, 411–418.
    1. Udall JN, Lo CW, Young VR, et al. (1984) The tolerance and nutritional value of two microfungal foods in human subjects. Am J Clin Nutr 40, 285–292.
    1. Edwards DG & Cummings JH (2010) The protein quality of mycoprotein. Proc Nutr Soc 69, E331.
    1. Marks LI (2005) Effects of mycoprotein food stuffs on glycaemic responses and other factors beneficial to health. Thesis, School of Biomedical Sciences, Faculty of Life and Health Sciences, Ulster.
    1. Marks LI, Gallagher A, Strain JJ, et al. (2004) Can differences in filament length of mycoprotein explain the effects of mycoprotein on glycaemic responses, appetite variables, and gastric emptying in healthy subjects? Proc Nutr Soc 63, 86A.
    1. Miri T, Cox PW & Fryer PJ (2003) In-situ visualisation of hyphal structure and arrangement in mycoprotein pastes. Biotechnol Lett 25, 295–300.
    1. Sjolin J, Hjort G, Friman G, et al. (1987) Urinary excretion of 1-methylhistidine: a qualitative indicator of exogenous 3-methylhistidine and intake of meats from various sources. Metabolism 36, 1175–1184.
    1. Jordi J, Herzog B, Camargo SM, et al. (2013) Specific amino acids inhibit food intake via the area postrema or vagal afferents. J Physiol 591, Pt 22, 5611–5621.
    1. Alamshah A, Spreckley E, McGavigan AK, et al. (2014) L-arginine promotes gut hormone release and reduces appetite in rodents. Endocrine Society’s 96th Annual Meeting and Expo, 2014, Chicago. OR45-2.

Source: PubMed

3
Subscribe