Effects of a brown beans evening meal on metabolic risk markers and appetite regulating hormones at a subsequent standardized breakfast: a randomized cross-over study

Anne Nilsson, Elin Johansson, Linda Ekström, Inger Björck, Anne Nilsson, Elin Johansson, Linda Ekström, Inger Björck

Abstract

Background: Dietary prevention strategies are increasingly recognized as essential to combat the current epidemic of obesity and related metabolic disorders. The purpose of the present study was to evaluate the potential prebiotic effects of indigestible carbohydrates in Swedish brown beans (Phaseolus vulgaris var. nanus) in relation to cardiometabolic risk markers and appetite regulating hormones.

Methods: Brown beans, or white wheat bread (WWB, reference product) were provided as evening meals to 16 healthy young adults in a randomised crossover design. Glucose, insulin, appetite regulatory hormones, GLP-1, GLP-2, appetite sensations, and markers of inflammation were measured at a following standardised breakfast, that is at 11 to 14 h post the evening meals. Additionally, colonic fermentation activity was estimated from measurement of plasma short chain fatty acids (SCFA, including also branched chain fatty acids) and breath hydrogen (H2) excretion.

Results: An evening meal of brown beans, in comparison with WWB, lowered blood glucose (-15%, p<0.01)- and insulin (-16%, p<0.05) responses, increased satiety hormones (PYY 51%, p<0.001), suppressed hunger hormones (ghrelin -14%, p<0.05), and hunger sensations (-15%, p = 0.05), increased GLP-2 concentrations (8.4%, p<0.05) and suppressed inflammatory markers (IL-6 -35%, and IL-18 -8.3%, p<0.05) at a subsequent standardised breakfast. Breath H2 (141%, p<0.01), propionate (16%, p<0.05), and isobutyrate (18%, P<0.001) were significantly increased after brown beans compared to after WWB, indicating a higher colonic fermentative activity after brown beans.

Conclusions: An evening meal with brown beans beneficially affected important measures of cardiometabolic risk and appetite regulatory hormones, within a time frame of 11-14 h, in comparison to a WWB evening meal. Concentrations of plasma SCFA and H2 were increased, indicating involvement of colonic fermentation. Indigestible colonic substrates from brown beans may provide a preventive tool in relation to obesity and the metabolic syndrome.

Trial registration: ClinicalTrials.gov NCT01706042.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1. CONSORT flowchart, flow diagram of…
Figure 1. CONSORT flowchart, flow diagram of the study progress.
Figure 2. Mean incremental changes (Δ) in…
Figure 2. Mean incremental changes (Δ) in blood glucose concentrations after the standardized breakfast consumed 11 hours after evening meals composed of brown beans or WWB.
A significant treatment (type of evening meal) effect was found over the test period (p<0.05, PROC MIXED in SAS release 9.2; SAS Institute Inc, Cary, NC). n = 16 subjects.
Figure 3. Mean incremental changes (Δ) in…
Figure 3. Mean incremental changes (Δ) in serum insulin concentrations after the standardized breakfast consumed 11 hours after evening meals composed of brown beans or WWB.
A significant treatment (type of evening meal) effect was found over the test period (p<0.05, PROC MIXED in SAS release 9.2; SAS Institute Inc, Cary, NC). n = 16 subjects.
Figure 4. Concentrations of serum IL-6 fasting…
Figure 4. Concentrations of serum IL-6 fasting and after a standardized breakfast, consumed 11 hours after evening meals composed of brown beans or WWB.
A significant treatment effect (type of evening meal) was found over the test period (p<0.05, PROC MIXED in SAS release 9.2; SAS Institute Inc, Cary, NC). n = 16 subjects.
Figure 5. Concentrations of serum IL-18 fasting…
Figure 5. Concentrations of serum IL-18 fasting and after a standardized breakfast, consumed 11 hours after evening meals composed of brown beans or WWB.
A significant treatment effect (type of evening meal) and treatment*time interaction were found over the test period (p<0.05 and p<0.001, respectively, PROC MIXED in SAS release 9.2; SAS Institute Inc, Cary, NC). n = 16 subjects.
Figure 6. Concentrations of plasma PYY fasting…
Figure 6. Concentrations of plasma PYY fasting and after a standardized breakfast, consumed 11 hours after evening meals composed of brown beans or WWB.
A significant treatment effect (type of evening meal) was found over the test period (p<0.0001, PROC MIXED in SAS release 9.2; SAS Institute Inc, Cary, NC). n = 16 subjects.
Figure 7. Concentrations of plasma oxyntomodulin fasting…
Figure 7. Concentrations of plasma oxyntomodulin fasting and after a standardized breakfast, consumed 11 hours after evening meals composed of brown beans or WWB.
A significant treatment effect (type of evening meal) was found over the test period (p<0.05, PROC MIXED in SAS release 9.2; SAS Institute Inc, Cary, NC). n = 16 subjects.
Figure 8. Concentrations of plasma ghrelin fasting…
Figure 8. Concentrations of plasma ghrelin fasting and after a standardized breakfast, consumed 11 hours after evening meals composed of brown beans or WWB.
A significant treatment effect (type of evening meal) was found over the test period (p<0.05, PROC MIXED in SAS release 9.2; SAS Institute Inc, Cary, NC). n = 16 subjects.
Figure 9. Concentrations of plasma GLP-2 fasting…
Figure 9. Concentrations of plasma GLP-2 fasting and after a standardized breakfast, consumed 11 hours after evening meals composed of brown beans or WWB.
A tendency was found towards a meal*time interaction in the postprandial period after the standardized breakfast (p = 0.065, PROC MIXED in SAS release 9.2; SAS Institute Inc, Cary, NC), revealing a higher plasma GLP-2 in the later postprandial period when the subjects consumed brown beans as an evening meal compared with the WWB (60–180 min, p<0.05). n = 16 subjects.

References

    1. Feldeisen SE, Tucker KL (2007) Nutritional strategies in the prevention and treatment of metabolic syndrome. Appl Physiol Nutr Metab. 32: 46–60.
    1. Tovar J, Nilsson A, Johansson M, Ekesbo R, Aberg AM, et al. (2012) A diet based on multiple functional concepts improves cardiometabolic risk parameters in healthy subjects. Nutrition & metabolism. 9: 29.
    1. Jenkins DJ, Kendall CW, Augustin LS, Franceschi S, Hamidi M, et al. (2002) Glycemic index: overview of implications in health and disease. Am J Clin Nutr. 76: 266S–73S.
    1. McKeown NM, Meigs JB, Liu S, Wilson PW, Jacques PF (2002) Whole-grain intake is favorably associated with metabolic risk factors for type 2 diabetes and cardiovascular disease in the Framingham Offspring Study. Am J Clin Nutr. 76: 390–8.
    1. Micallef MA, Garg ML (2009) Anti-inflammatory and cardioprotective effects of n-3 polyunsaturated fatty acids and plant sterols in hyperlipidemic individuals. Atherosclerosis. 204: 476–82.
    1. Thorburn A, Muir J, Proietto J (1993) Carbohydrate fermentation decreases hepatic glucose output in healthy subjects. Metabolism. 42: 780–5.
    1. Nilsson A, Östman E, Preston T, Bjorck I (2008) Effects of GI vs content of cereal fibre of the evening meal on glucose tolerance at a subsequent standardized breakfast. EJCN. 62: 712–20.
    1. Nilsson A, Granfeldt Y, Östman E, Preston T, Bjorck I (2006) Effects of GI and content of indigestible carbohydrates of cereal-based evening meals on glucose tolerance at a subsequent standardised breakfast. EJCN. 60: 1092–9.
    1. Nilsson AC, Östman EM, Holst JJ, Bjorck IM (2008) Including indigestible carbohydrates in the evening meal of healthy subjects improves glucose tolerance, lowers inflammatory markers, and increases satiety after a subsequent standardized breakfast. J Nutr. 138: 732–9.
    1. Nilsson AC, Östman EM, Knudsen KE, Holst JJ, Bjorck IM (2010) A cereal-based evening meal rich in indigestible carbohydrates increases plasma butyrate the next morning. J Nutr. 140: 1932–6.
    1. Papanikolaou Y, Fulgoni VL, 3rd (2008) Bean consumption is associated with greater nutrient intake, reduced systolic blood pressure, lower body weight, and a smaller waist circumference in adults: results from the National Health and Nutrition Examination Survey 1999–2002. J Am Coll Nutr. 27: 569–76.
    1. Sichieri R (2002) Dietary patterns and their associations with obesity in the Brazilian city of Rio de Janeiro. Obes Res. 10: 42–8.
    1. Sievenpiper JL, Kendall CW, Esfahani A, Wong JM, Carleton AJ, et al. (2009) Effect of non-oil-seed pulses on glycaemic control: a systematic review and meta-analysis of randomised controlled experimental trials in people with and without diabetes. Diabetologia. 52: 1479–95.
    1. Wong CL, Mollard RC, Zafar TA, Luhovyy BL, Anderson GH (2009) Food intake and satiety following a serving of pulses in young men: effect of processing, recipe, and pulse variety. J Am Coll Nutr. 28: 543–52.
    1. Tovar JG, Y Björck (1992) I (1992) Effect of Processing on Blood Glucose and Insulin Responses to Starch in Legumes. J. Agric. Food Chem. 40: 1846–1851.
    1. Brighenti F (1998) Summary of the conclusion of the working group on Profibre interlaboratory study on determination of short chain fatty acids in blood. In: Functional Properties of Non-digestible Carbohydrates. F. Gullion. R. Amadò, M. T. Amaral-Collaco, H. Andersson, N. G. Asp, K. E. Bach Knudsen, M. Champ, J. Mathers, J. A. Robertson, I. Rowland, and J. Van Loo, ed. European Commission, DG XII, Science, Research and Development, Brussels, Belgium. 150–153.
    1. Björck IME, Siljeström M (1992) In-Vivo and In-Vitro Digestibility of Starch in Autoclaved Pea and Potato Products. J Sci Food Agric. 58: 541–553.
    1. Åkerberg AKE, Liljeberg HGM, Granfeldt YE, Drews A, Björck IM (1998) An in vitro method, based on chewing, to predict resistant starch content in foods allows parallel determination of potentially available starch and dietary fibre. J Nutr. 128: 651–659.
    1. Asp N-G, Johansson C-G, Hallmer H, Siljeström M (1983) Rapid enzymatic assay of insoluble and soluble dietary fibre. J Agric Food Chem. 31: 476–482.
    1. Hernandez-Salazar M, Osorio-Diaz P, Loarca-Pina G, Reynoso-Camacho R, Tovar J, et al. (2010) In vitro fermentability and antioxidant capacity of the indigestible fraction of cooked black beans (Phaseolus vulgaris L.), lentils (Lens culinaris L.) and chickpeas (Cicer arietinum L.). J Sci Food Agric. 90: 1417–22.
    1. Henningsson AM, Nyman EM, Bjorck IM (2001) Content of short-chain fatty acids in the hindgut of rats fed processed bean (Phaseolus vulgaris) flours varying in distribution and content of indigestible carbohydrates. Br J Nutr. 86: 379–89.
    1. Mortensen PB, Clausen MR, Bonnen H, Hove H, Holtug K (1992) Colonic fermentation of ispaghula, wheat bran, glucose, and albumin to short-chain fatty acids and ammonia evaluated in vitro in 50 subjects. JPEN. Journal of parenteral and enteral nutrition. 16: 433–9.
    1. Nyangale EP, Mottram DS, Gibson GR (2012) Gut microbial activity, implications for health and disease: the potential role of metabolite analysis. J Proteome Res. 11: 5573–85.
    1. Jie Z, Bang-Yao L, Ming-Jie X, Hai-Wei L, Zu-Kang Z, et al. (2000) Studies on the effects of polydextrose intake on physiologic functions in Chinese people. Am J Clin Nutr. 72: 1503–9.
    1. Smiricky-Tjardes MR, Grieshop CM, Flickinger EA, Bauer LL, Fahey GC Jr (2003) Dietary galactooligosaccharides affect ileal and total-tract nutrient digestibility, ileal and fecal bacterial concentrations, and ileal fermentative characteristics of growing pigs. Journal of animal science. 81: 2535–45.
    1. Cani PD, Lecourt E, Dewulf EM, Sohet FM, Pachikian BD, et al. (2009) Gut microbiota fermentation of prebiotics increases satietogenic and incretin gut peptide production with consequences for appetite sensation and glucose response after a meal. Am J Clin Nutr. 90: 1236–43.
    1. Cani PD, Neyrinck AM, Fava F, Knauf C, Burcelin RG, et al. (2007) Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia. 50: 2374–83.
    1. Xu BJ, Yuan SH, Chang SK (2007) Comparative analyses of phenolic composition, antioxidant capacity, and color of cool season legumes and other selected food legumes. J Food Sci. 72: S167–77.
    1. Parkar SG, Stevenson DE, Skinner MA (2008) The potential influence of fruit polyphenols on colonic microflora and human gut health. Int J Food Microbiol. 124: 295–8.
    1. Zhong Y, Cai D, Cai W, Geng S, Chen L, et al. (2009) Protective effect of galactooligosaccharide-supplemented enteral nutrition on intestinal barrier function in rats with severe acute pancreatitis. Clin Nutr. 28: 575–80.
    1. Cani PD, Possemiers S, Van de Wiele T, Guiot Y, Everard A, et al. (2009) Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut. 58: 1091–103.
    1. Wellen KE, Hotamisligil GS (2005) Inflammation, stress, and diabetes. J Clin Invest. 115: 1111–9.
    1. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, et al. (2007) Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 56: 1761–72.
    1. Stanley S, Wynne K, Bloom S (2004) Gastrointestinal satiety signals III. Glucagon-like peptide 1, oxyntomodulin, peptide YY, and pancreatic polypeptide. Am J Physiol Gastrointest Liver Physiol. 286: G693–7.
    1. Dalvi PS, Belsham DD (2012) Glucagon-like peptide-2 directly regulates hypothalamic neurons expressing neuropeptides linked to appetite control in vivo and in vitro. Endocrinology. 153: 2385–97.
    1. Ahren B (2007) GLP-1-based therapy of type 2 diabetes: GLP-1 mimetics and DPP-IV inhibitors. Curr Diab Rep. 7: 340–7.
    1. Baggio LL, Huang Q, Brown TJ, Drucker DJ (2004) Oxyntomodulin and glucagon-like peptide-1 differentially regulate murine food intake and energy expenditure. Gastroenterology. 127: 546–58.
    1. Musch MW, Bookstein C, Xie Y, Sellin JH, Chang EB (2001) SCFA increase intestinal Na absorption by induction of NHE3 in rat colon and human intestinal C2/bbe cells. Am J Physiol Gastrointest Liver Physiol. 280: G687–93.
    1. Zhou J, Martin RJ, Tulley RT, Raggio AM, McCutcheon KL, et al. (2008) Dietary resistant starch upregulates total GLP-1 and PYY in a sustained day-long manner through fermentation in rodents. Am J Physiol Endocrinol Metab. 295: E1160–6.
    1. Tolhurst G, Heffron H, Lam YS, Parker HE, Habib AM, et al. (2012) Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes. 61: 364–71.
    1. Al-Lahham SH, Roelofsen H, Priebe M, Weening D, Dijkstra M, et al. (2010) Regulation of adipokine production in human adipose tissue by propionic acid. Eur J Clin Invest. 40: 401–7.
    1. Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature. 444: 860–7.
    1. Al-Lahham S, Roelofsen H, Rezaee F, Weening D, Hoek A, et al. (2012) Propionic acid affects immune status and metabolism in adipose tissue from overweight subjects. Eur J Clin Invest. 42: 357–64.
    1. Åkerberg AKE, Liljeberg H, Bjorck I (1998) Effects of amylose/amylopectin ratio and baking conditions on resistant starch formation and glycaemic indices. journal of cereal science. 28: 71–80.
    1. Howlett JF, Betteridge VA, Champ M, Craig SA, Meheust A, et al... (2010) The definition of dietary fiber - discussions at the Ninth Vahouny Fiber Symposium: building scientific agreement. Food & nutrition research. 54.

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