Consumption of a High-Protein Meal Replacement Leads to Higher Fat Oxidation, Suppression of Hunger, and Improved Metabolic Profile After an Exercise Session

Camila L P Oliveira, Normand G Boulé, Aloys Berg, Arya M Sharma, Sarah A Elliott, Mario Siervo, Sunita Ghosh, Carla M Prado, Camila L P Oliveira, Normand G Boulé, Aloys Berg, Arya M Sharma, Sarah A Elliott, Mario Siervo, Sunita Ghosh, Carla M Prado

Abstract

The aim of this study was to compare the impact of a high-protein meal replacement (HP-MR) versus a control (CON) breakfast on exercise metabolism. In this acute, randomized controlled, cross-over study, participants were allocated into two isocaloric arms: (a) HP-MR: 30% carbohydrate, 43% protein, and 27% fat; (b) CON: 55% carbohydrate, 15% protein, and 30% fat. Following breakfast, participants performed a moderate-intensity aerobic exercise while inside a whole-body calorimetry unit. Energy expenditure, macronutrient oxidation, appetite sensations, and metabolic blood markers were assessed. Forty-three healthy, normal-weight adults (24 males) participated. Compared to the CON breakfast, the HP-MR produced higher fat oxidation (1.07 ± 0.33 g/session; p = 0.003) and lower carbohydrate oxidation (-2.32 ± 0.98 g/session; p = 0.023) and respiratory exchange ratio (-0.01 ± 0.00; p = 0.003) during exercise. After exercise, increases in hunger were lower during the HP-MR condition. Changes in blood markers from the fasting state to post-exercise during the HP-MR condition were greater for insulin, peptide tyrosine-tyrosine, and glucagon-like peptide 1, and lower for low-density lipoprotein cholesterol, triglyceride, and glycerol. Our primary findings were that an HP-MR produced higher fat oxidation during the exercise session, suppression of hunger, and improved metabolic profile after it.

Keywords: appetite; energy metabolism; exercise; meal replacement; protein.

Conflict of interest statement

This was an investigator-initiated trial supported by Almased Wellness GmbH (Bienenbüttel, Germany). Per contractual agreement, the funder had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results. C.L.P.O. received travel fees from Almased Wellness GmbH. A.M.S. and C.M.P. received travel and speaker fees unrelated to this study. A.B. received consulting fees. C.M.P. is supported by a Canadian Institutes of Health Research New Investigator Salary Award, and a Campus Alberta Innovates Program.

Figures

Figure 1
Figure 1
(a) Overview of the experimental protocol and (b) activities performed during each condition. Abbreviations: CON: control; HP-MR: high-protein meal replacement; REE: resting energy expenditure; WBCU: whole-body calorimetry unit.
Figure 2
Figure 2
CONSORT flow diagram. CON, control diet; CONSORT, Consolidated Standards of Reporting Trials; HP-MR, high-protein meal replacement. Adapted from Oliveira, Boulé, Sharma, Elliott, Siervo, Ghosh, Berg, and Prado [25].
Figure 3
Figure 3
(a) Energy expenditure (EE), (b) respiratory exchange ratio (RER), (c) carbohydrate oxidation and (d) fat oxidation, during the exercise session following the consumption of the isocaloric high-protein meal replacement (HP-MR) and control (CON) breakfasts while participants were inside the whole-body calorimetry unit. Values are mean ± standard deviation. n = 43 (females n = 19; males n = 24). p-values represent significant difference between the HP-MR and CON groups, as assessed by mixed analysis of variance.
Figure 4
Figure 4
Changes in appetite sensations from after breakfast to after the exercise session during the HP-MR and CON intervention phases in (a) all participants (n = 43), (b) females (n = 19), and (c) males (n = 24). Values are mean ± standard deviation. * Significant difference (p = 0.014) in all participants (n = 43) between the HP-MR and CON interventions, as assessed by mixed analysis of variance. † Significant difference (p = 0.019) in females (n = 19) between the HP-MR and CON interventions, as assessed by mixed analysis of variance. Abbreviations: CON: control, standard North American diet; HP-MR: high-protein meal replacement; PFC: prospective food consumption.
Figure 5
Figure 5
Composite satiety score during the HP-MR and CON interventions in (a) all participants (n = 43), (b) females (n = 19), and (c) males (n = 24). Data are mean ± standard deviation. * Significant difference (p < 0.03) between the HP-MR and CON diets, as assessed by a mixed analysis of variance. Abbreviations: CON: control, standard North American diet; CSS: composite satiety score; HP-MR: high-protein meal replacement.

References

    1. Di Angelantonio E., Bhupathiraju S.N., Wormser D., Gao P., Kaptoge S., de Gonzalez A.B., Cairns B.J., Huxley R., Jackson C.L., Joshy G., et al. Body-mass index and all-cause mortality: Individual-participant-data meta-analysis of 239 prospective studies in four continents. Lancet. 2016;388:776–786. doi: 10.1016/S0140-6736(16)30175-1.
    1. Abdelaal M., le Roux C.W., Docherty N.G. Morbidity and mortality associated with obesity. Ann. Transl. Med. 2017;5:161. doi: 10.21037/atm.2017.03.107.
    1. Apovian C.M. Obesity: Definition, comorbidities, causes, and burden. Am. J. Manag. Care. 2016;22:s176–s185.
    1. Garvey W.T., Mechanick J.I., Brett E.M., Garber A.J., Hurley D.L., Jastreboff A.M., Nadolsky K., Pessah-Pollack R., Plodkowski R. American Association of Clinical Endocrinologists and American College of Endocrinology Comprehensive Clinical Practice Guidelines for Medical Care of Patients with Obesity. Endocr. Pract. 2016;22:1–203. doi: 10.4158/.
    1. Ravussin E., Ryan D.H. Three New Perspectives on the Perfect Storm: What’s Behind the Obesity Epidemic? Obesity. 2018;26:9–10. doi: 10.1002/oby.22085.
    1. Bray G.A., Frühbeck G., Ryan D.H., Wilding J.P. Management of obesity. Lancet. 2016;387:1947–1956. doi: 10.1016/S0140-6736(16)00271-3.
    1. Hall K.D., Heymsfield S.B., Kemnitz J.W., Klein S., Schoeller D.A., Speakman J.R. Energy balance and its components: Implications for body weight regulation. Am. J. Clin. Nutr. 2012;95:989–994. doi: 10.3945/ajcn.112.036350.
    1. Manore M.M., Larson-Meyer D.E., Lindsay A.R., Hongu N., Houtkooper L. Dynamic Energy Balance: An Integrated Framework for Discussing Diet and Physical Activity in Obesity Prevention-Is it More than Eating Less and Exercising More? Nutrients. 2017;9:905. doi: 10.3390/nu9080905.
    1. Keys A., Taylor H.L., Grande F. Basal metabolism and age of adult man. Metabolism. 1973;22:579–587. doi: 10.1016/0026-0495(73)90071-1.
    1. Johns D.J., Hartmann-Boyce J., Jebb S.A., Aveyard P. Diet or exercise interventions vs combined behavioral weight management programs: A systematic review and meta-analysis of direct comparisons. J. Acad. Nutr. Diet. 2014;114:1557–1568. doi: 10.1016/j.jand.2014.07.005.
    1. Hall K.D., Kahan S. Maintenance of Lost Weight and Long-Term Management of Obesity. Med. Clin. N. Am. 2018;102:183–197. doi: 10.1016/j.mcna.2017.08.012.
    1. Doucet É., McInis K., Mahmoodianfard S. Compensation in response to energy deficits induced by exercise or diet. Obes. Rev. 2018;19:36–46. doi: 10.1111/obr.12783.
    1. Dorling J., Broom D.R., Burns S.F., Clayton D.J., Deighton K., James L.J., King J.A., Miyashita M., Thackray A.E., Batterham R.L., et al. Acute and Chronic Effects of Exercise on Appetite, Energy Intake, and Appetite-Related Hormones: The Modulating Effect of Adiposity, Sex, and Habitual Physical Activity. Nutrients. 2018;10:1140. doi: 10.3390/nu10091140.
    1. Thackray A.E., Deighton K., King J.A., Stensel D.J. Exercise, Appetite and Weight Control: Are There Differences between Men and Women? Nutrients. 2016;8:583. doi: 10.3390/nu8090583.
    1. Donnelly J.E., Hill J.O., Jacobsen D.J., Potteiger J., Sullivan D.K., Johnson S.L., Heelan K., Hise M., Fennessey P.V., Sonko B., et al. Effects of a 16-month randomized controlled exercise trial on body weight and composition in young, overweight men and women: The Midwest Exercise Trial. Arch. Intern. Med. 2003;163:1343–1350. doi: 10.1001/archinte.163.11.1343.
    1. Hagobian T.A., Sharoff C.G., Stephens B.R., Wade G.N., Silva J.E., Chipkin S.R., Braun B. Effects of exercise on energy-regulating hormones and appetite in men and women. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009;296:R233–R242. doi: 10.1152/ajpregu.90671.2008.
    1. Johnston B.C., Kanters S., Bandayrel K., Wu P., Naji F., Siemieniuk R.A., Ball G.D.C., Busse J.W., Thorlund K., Guyatt G., et al. Comparison of Weight Loss Among Named Diet Programs in Overweight and Obese Adults: A Meta-analysis. JAMA. 2014;312:923–933. doi: 10.1001/jama.2014.10397.
    1. Heymsfield S.B., van Mierlo C.A., van der Knaap H.C., Heo M., Frier H.I. Weight management using a meal replacement strategy: Meta and pooling analysis from six studies. Int. J. Obes. Relat. Metab. Disord. 2003;27:537–549. doi: 10.1038/sj.ijo.0802258.
    1. Astbury N.M., Piernas C., Hartmann-Boyce J., Lapworth S., Aveyard P., Jebb S.A. A systematic review and meta-analysis of the effectiveness of meal replacements for weight loss. Obes. Rev. 2019;20:569–587. doi: 10.1111/obr.12816.
    1. Kruschitz R., Wallner-Liebmann S., Lothaller H., Luger M., Ludvik B. Long-Term Weight-Loss Maintenance by a Meal Replacement Based Weight Management Program in Primary Care. Obes. Facts. 2017;10:76–84. doi: 10.1159/000454836.
    1. Feinman R.D., Fine E.J. Thermodynamics and metabolic advantage of weight loss diets. Metab. Syndr. Relat. Disord. 2003;1 doi: 10.1089/154041903322716688.
    1. Paddon-Jones D., Westman E., Mattes R.D., Wolfe R.R., Astrup A., Westerterp-Plantenga M. Protein, weight management, and satiety. Am. J. Clin. Nutr. 2008;87:1558s–1561s. doi: 10.1093/ajcn/87.5.1558S.
    1. Pesta D.H., Samuel V.T. A high-protein diet for reducing body fat: Mechanisms and possible caveats. Nutr. Metab. 2014;11:53. doi: 10.1186/1743-7075-11-53.
    1. Oliveira C.L.P., Boulé N.G., Sharma A.M., Elliott S., Siervo M., Ghosh S., Berg A., Prado C.M. Examining the effects of a high-protein total diet replacement on energy metabolism, metabolic blood markers, and appetite sensations in healthy adults: Protocol for two complementary, randomized, controlled, crossover trials. Trials. 2019;20:787. doi: 10.1186/s13063-019-3950-y.
    1. Oliveira C.L.P., Boulé N.G., Sharma A.M., Elliott S., Siervo M., Ghosh S., Berg A., Prado C.M. A high-protein total diet replacement increases energy expenditure and leads to negative fat balance in healthy, normal-weight adults. Am. J. Clin. Nutr. 2020 doi: 10.1093/ajcn/nqaa283.
    1. Godin G. The Godin-Shephard Leisure-Time Physical Activity Questionnaire. Health Fit. J. Can. 2011;4:18–22.
    1. Institute of Medicine . Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids (Macronutrients) The National Academies Press; Washington, DC, USA: 2005. p. 1357.
    1. Smith S.R., de Jonge L., Zachwieja J.J., Roy H., Nguyen T., Rood J.C., Windhauser M.M., Bray G.A. Fat and carbohydrate balances during adaptation to a high-fat diet. Am. J. Clin. Nutr. 2000;71:450–457. doi: 10.1093/ajcn/71.2.450.
    1. Austin G.L., Ogden L.G., Hill J.O. Trends in carbohydrate, fat, and protein intakes and association with energy intake in normal-weight, overweight, and obese individuals: 1971–2006. Am. J. Clin. Nutr. 2011;93:836–843. doi: 10.3945/ajcn.110.000141.
    1. Brouwer E. On simple formulae for calculating the heat expenditure and the quantities of carbohydrate and fat oxidized in metabolism of men and animals, from gaseous exchange (Oxygen intake and carbonic acid output) and urine-N. Acta Physiol. Pharmacol. Neerl. 1957;6:795–802.
    1. Koohkan S., McCarthy D.H., Berg A. The effect of a soy-yoghurt-honey product on excess weight and related health risk factors—A review. J. Nutr. Health Food Sci. 2017;5:1–10. doi: 10.15226/jnhfs.2017.00191.
    1. Flint A., Raben A., Blundell J.E., Astrup A. Reproducibility, power and validity of visual analogue scales in assessment of appetite sensations in single test meal studies. Int. J. Obes. Relat. Metab. Disord. 2000;24 doi: 10.1038/sj.ijo.0801083.
    1. Gilbert J.A., Gasteyger C., Raben A., Meier D.H., Astrup A., Sjodin A. The effect of tesofensine on appetite sensations. Obesity. 2012;20:553–561. doi: 10.1038/oby.2011.197.
    1. Coyle E.F., Jeukendrup A.E., Wagenmakers A.J., Saris W.H. Fatty acid oxidation is directly regulated by carbohydrate metabolism during exercise. Am. J. Physiol. 1997;273:E268–E275. doi: 10.1152/ajpendo.1997.273.2.E268.
    1. Prentice A.M. Manipulation of dietary fat and energy density and subsequent effects on substrate flux and food intake. Am. J. Clin. Nutr. 1998;67:535s–541s. doi: 10.1093/ajcn/67.3.535S.
    1. Spriet L.L. New insights into the interaction of carbohydrate and fat metabolism during exercise. Sports Med. 2014;44:S87–S96. doi: 10.1007/s40279-014-0154-1.
    1. Patterson R., Potteiger J. A comparison of normal versus low dietary carbohydrate intake on substrate oxidation during and after moderate intensity exercise in women. Eur. J. Appl. Physiol. 2011;111:3143–3150. doi: 10.1007/s00421-011-1950-z.
    1. San-Cristobal R., Navas-Carretero S., Martínez-González M.Á., Ordovas J.M., Martínez J.A. Contribution of macronutrients to obesity: Implications for precision nutrition. Nat. Rev. Endocrinol. 2020;16:305–320. doi: 10.1038/s41574-020-0346-8.
    1. Barwell N.D., Malkova D., Leggate M., Gill J.M.R. Individual responsiveness to exercise-induced fat loss is associated with change in resting substrate utilization. Metabolism. 2009;58:1320–1328. doi: 10.1016/j.metabol.2009.04.016.
    1. Zurlo F., Lillioja S., Esposito-Del Puente A., Nyomba B.L., Raz I., Saad M.F., Swinburn B.A., Knowler W.C., Bogardus C., Ravussin E. Low ratio of fat to carbohydrate oxidation as predictor of weight gain: Study of 24-h RQ. Am. J. Physiol. 1990;259:E650–E657. doi: 10.1152/ajpendo.1990.259.5.E650.
    1. Galgani J., Ravussin E. Energy metabolism, fuel selection and body weight regulation. Int. J. Obes. 2008;32:S109–S119. doi: 10.1038/ijo.2008.246.
    1. Mayer J., Marshall N.B., Vitale J.J., Christensen J.H., Mashayekhi M.B., Stare F.J. Exercise, food intake and body weight in normal rats and genetically obese adult mice. Am. J. Physiol. 1954;177:544–548. doi: 10.1152/ajplegacy.1954.177.3.544.
    1. Edholm O.G., Fletcher J.G., Widdowson E.M., McCance R.A. The energy expenditure and food intake of individual men. Br. J. Nutr. 1955;9:286–300. doi: 10.1079/BJN19550040.
    1. Hopkins M., King N.A., Blundell J.E. Acute and long-term effects of exercise on appetite control: Is there any benefit for weight control? Curr. Opin. Clin. Nutr. Metab. Care. 2010;13:635–640. doi: 10.1097/MCO.0b013e32833e343b.
    1. Blundell J.E., Gibbons C., Caudwell P., Finlayson G., Hopkins M. Appetite control and energy balance: Impact of exercise. Obes. Rev. 2015;16:67–76. doi: 10.1111/obr.12257.
    1. Drummen M., Tischmann L., Gatta-Cherifi B., Adam T., Westerterp-Plantenga M. Dietary Protein and Energy Balance in Relation to Obesity and Co-morbidities. Front. Endocrinol. 2018;9 doi: 10.3389/fendo.2018.00443.
    1. Dougkas A., Östman E. Protein-Enriched Liquid Preloads Varying in Macronutrient Content Modulate Appetite and Appetite-Regulating Hormones in Healthy Adults. J. Nutr. 2016;146:637–645. doi: 10.3945/jn.115.217224.
    1. Mattes R. Fluid calories and energy balance: The good, the bad, and the uncertain. Physiol. Behav. 2006;89:66–70. doi: 10.1016/j.physbeh.2006.01.023.
    1. Martens M.J., Lemmens S.G., Born J.M., Westerterp-Plantenga M.S. A solid high-protein meal evokes stronger hunger suppression than a liquefied high-protein meal. Obesity. 2011;19:522–527. doi: 10.1038/oby.2010.258.
    1. Zanchi D., Depoorter A., Egloff L., Haller S., Mählmann L., Lang U.E., Drewe J., Beglinger C., Schmidt A., Borgwardt S. The impact of gut hormones on the neural circuit of appetite and satiety: A systematic review. Neurosci. Biobehav. Rev. 2017;80:457–475. doi: 10.1016/j.neubiorev.2017.06.013.
    1. Perry B., Wang Y. Appetite regulation and weight control: The role of gut hormones. Nutr. Diabetes. 2012;2:e26. doi: 10.1038/nutd.2011.21.
    1. Freire R.H., Alvarez-Leite J.I. Appetite control: Hormones or diet strategies? Curr. Opin. Clin. Nutr. Metab. Care. 2020;23:328–335. doi: 10.1097/MCO.0000000000000675.
    1. Lejeune M.P., Westerterp K.R., Adam T.C., Luscombe-Marsh N.D., Westerterp-Plantenga M.S. 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. 2006;83:89–94. doi: 10.1093/ajcn/83.1.89.
    1. Batterham R.L., Heffron H., Kapoor S., Chivers J.E., Chandarana K., Herzog H., Le Roux C.W., Thomas E.L., Bell J.D., Withers D.J. Critical role for peptide YY in protein-mediated satiation and body-weight regulation. Cell Metab. 2006;4:223–233. doi: 10.1016/j.cmet.2006.08.001.
    1. Kavanagh K., Jones K.L., Zhang L., Flynn D.M., Shadoan M.K., Wagner J.D. High isoflavone soy diet increases insulin secretion without decreasing insulin sensitivity in premenopausal nonhuman primates. Nutr. Res. 2008;28:368–376. doi: 10.1016/j.nutres.2008.03.011.
    1. Lang V., Bellisle F., Alamowitch C., Craplet C., Bornet F.R.J., Slama G., Guy-Grand B. Varying the protein source in mixed meal modifies glucose, insulin and glucagon kinetics in healthy men, has weak effects on subjective satiety and fails to affect food intake. Eur. J. Clin. Nutr. 1999;53:959–965. doi: 10.1038/sj.ejcn.1600881.
    1. Nuttall F.Q., Gannon M.C. Metabolic response of people with type 2 diabetes to a high protein diet. Nutr. Metab. 2004;1:6. doi: 10.1186/1743-7075-1-6.
    1. Liu D., Zhen W., Yang Z., Carter J.D., Si H., Reynolds K.A. Genistein Acutely Stimulates Insulin Secretion in Pancreatic β-Cells Through a cAMP-Dependent Protein Kinase Pathway. Diabetes. 2006;55:1043–1050. doi: 10.2337/diabetes.55.04.06.db05-1089.
    1. Parks E.J. Effect of dietary carbohydrate on triglyceride metabolism in humans. J. Nutr. 2001;131:2772s–2774s. doi: 10.1093/jn/131.10.2772S.
    1. Wolfe B.M., Piche L.A. Replacement of carbohydrate by protein in a conventional-fat diet reduces cholesterol and triglyceride concentrations in healthy normolipidemic subjects. Clin. Invest. Med. 1999;22:140–148.
    1. Brown L., Rosner B., Willett W.W., Sacks F.M. Cholesterol-lowering effects of dietary fiber: a meta-analysis. Am. J. Clin. Nutr. 1999;69:30–42. doi: 10.1093/ajcn/69.1.30.
    1. Sánchez-Muniz F.J. Dietary fibre and cardiovascular health. Nutr. Hosp. 2012;27:31–45.
    1. Reshef L., Olswang Y., Cassuto H., Blum B., Croniger C.M., Kalhan S.C., Tilghman S.M., Hanson R.W. Glyceroneogenesis and the triglyceride/fatty acid cycle. J. Biol. Chem. 2003;278 doi: 10.1074/jbc.R300017200.
    1. Boulé N., Prud’homme D. Physical Activity in Obesity Management. [(accessed on 29 October 2020)]; Available online:
    1. Goodpaster B.H., Katsiaras A., Kelley D.E. Enhanced Fat Oxidation through Physical Activity Is Associated With Improvements in Insulin Sensitivity in Obesity. Diabetes. 2003;52:2191. doi: 10.2337/diabetes.52.9.2191.
    1. Burton F.L., Malkova D., Caslake M.J., Gill J.M. Energy replacement attenuates the effects of prior moderate exercise on postprandial metabolism in overweight/obese men. Int. J. Obes. 2008;32:481–489. doi: 10.1038/sj.ijo.0803754.
    1. Westerterp-Plantenga M.S., Lejeune M.P., Smeets A.J., Luscombe-Marsh N.D. Sex differences in energy homeostatis following a diet relatively high in protein exchanged with carbohydrate, assessed in a respiration chamber in humans. Physiol. Behav. 2009;97:414–419. doi: 10.1016/j.physbeh.2009.03.010.
    1. Lori A., Nori G. Modulation of Appetite by Gonadal Steroid Hormones. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2006;361:1251. doi: 10.1098/rstb.2006.1860.
    1. Cornier M.-A., Salzberg A.K., Endly D.C., Bessesen D.H., Tregellas J.R. Sex-based differences in the behavioral and neuronal responses to food. Physiol. Behav. 2010;99:538–543. doi: 10.1016/j.physbeh.2010.01.008.
    1. Brennan I.M., Feltrin K.L., Nair N.S., Hausken T., Little T.J., Gentilcore D., Wishart J.M., Jones K.L., Horowitz M., Feinle-Bisset C. Effects of the phases of the menstrual cycle on gastric emptying, glycemia, plasma GLP-1 and insulin, and energy intake in healthy lean women. Am. J. Physiol. Gastrointest. Liver Physiol. 2009;297:G602–G610. doi: 10.1152/ajpgi.00051.2009.
    1. Buffenstein R., Poppitt S.D., McDevitt R.M., Prentice A.M. Food intake and the menstrual cycle: A retrospective analysis, with implications for appetite research. Physiol. Behav. 1995;58:1067–1077. doi: 10.1016/0031-9384(95)02003-9.
    1. Asarian L., Geary N. Sex differences in the physiology of eating. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2013;305:R1215–R1267. doi: 10.1152/ajpregu.00446.2012.

Source: PubMed

3
Subscribe