Effects of whole grain rye, with and without resistant starch type 2 supplementation, on glucose tolerance, gut hormones, inflammation and appetite regulation in an 11-14.5 hour perspective; a randomized controlled study in healthy subjects

Jonna C Sandberg, Inger M E Björck, Anne C Nilsson, Jonna C Sandberg, Inger M E Björck, Anne C Nilsson

Abstract

Background: The prevalence of obesity is increasing worldwide and prevention is needed. Whole grain has shown potential to lower the risk of obesity, cardiovascular disease and type 2 diabetes. One possible mechanism behind the benefits of whole grain is the gut fermentation of dietary fiber (DF), e.g. non-starch polysaccharides and resistant starch (RS), in whole grain. The purpose of the study is to investigate the effect of whole grain rye-based products on glucose- and appetite regulation.

Method: Twenty-one healthy subjects were provided four rye-based evening test meals in a crossover overnight study design. The test evening meals consisted of either whole grain rye flour bread (RFB) or a 1:1 ratio of whole grain rye flour and rye kernels bread (RFB/RKB), with or without added resistant starch (+RS). White wheat flour bread (WWB) was used as reference evening meal. Blood glucose, insulin, PYY, FFA, IL-6 as well as breath H2 and subjective rating of appetite were measured the following morning at fasting and repeatedly up to 3.5 h after a standardized breakfast consisting of WWB. Ad libitum energy intake was determined at lunch, 14.5 h after evening test and reference meals, respectively.

Results: The evening meal with RFB/RKB + RS decreased postprandial glucose- and insulin responses (iAUC) (P < 0.05) and increased the gut hormone PYY in plasma the following morning 0-120 min after the standardized breakfast, compared to WWB (P = 0.01). Moreover, RFB increased subjective satiety and decreased desire to eat, and both RFB and RFB/RKB decreased feeling of hunger (AUC 0-210 min). All rye-based evening meals decreased or tended to decrease fasting FFA (P < 0.05, RFB/RKB: P = 0.057) and increased breath hydrogen concentration (0-120 min, P < 0.001). No effects were noted on energy intake at lunch or inflammatory marker IL-6 (0 + 180 min) after the rye-based evening meals, compared to WWB.

Conclusion: Whole grain rye bread has the potential to improve cardiometabolic variables in an 11-14.5 h perspective in healthy humans. The combination RFB/RKB + RS positively affected biomarkers of glucose- and appetite regulation in a semi-acute perspective. Meanwhile, RFB and RFB/RKB improved subjective appetite ratings. The effects probably emanate from gut fermentation events.

Trial registration: The study was registered at: ClinicalTrials.gov, register number NCT02347293 ( www.clinicaltrials.gov/ct2/show/NCT02347293 ). Registered 15 January 2015.

Keywords: Appetite regulation; Dietary fiber; Dietary prevention; Glucose regulation; Gut fermentation; Gut hormones; Obesity; Rye; Type 2 diabetes; Whole grain.

Figures

Fig. 1
Fig. 1
Incremental blood glucose- and serum insulin concentrations after a standardized breakfast following the evening meals Changes (Δ) in mean incremental concentrations of blood glucose (a) and serum insulin (b) from fasting concentrations in the morning after a standardized breakfast, 11–14 h following the rye-based test- or WWB reference evening meals. Values are means ± SEM. Repeated measures; mixed model in SAS. RFB, rye flour bread; RFB/RKB, 50/50 rye flour and rye kernel bread; + RS, added resistant starch; WWB, white wheat bread
Fig. 2
Fig. 2
Concentrations of plasma PYY and breath hydrogen after a standardized breakfast following the evening meals Mean concentrations of plasma PYY (a) and breath hydrogen excretion (b) in the morning after a standardized breakfast, 11–13 h respectively 11–14.5 h following the rye-based test- or WWB reference evening meals. Values are means ± SEM. Repeated measures; mixed model in SAS. RFB, rye flour bread; RFB/RKB, 50/50 rye flour and rye kernel bread; + RS, added resistant starch; WWB, white wheat bread
Fig. 3
Fig. 3
Subjective appetite ratings after a standardized breakfast following rye-based test- or WWB reference evening meal Data is presented as mean ± SEM of subjective appetite ratings (VAS) of satiety (a), hunger (b) and desire to eat (c) during the following 3.5 h after standardized breakfast in the morning, 11–14.5 h after intake of a rye-based evening meal or a WWB reference evening meal. Repeated measures; mixed model in SAS. RFB, rye flour bread; RFB/RKB, 50/50 rye flour and rye kernel bread; + RS, added resistant starch; WWB, white wheat bread

References

    1. World Health Organization. World Health Statistics 2012. 2012. [cited 2016 7 June]; Available from: .
    1. Yao B, et al. Dietary fiber intake and risk of type 2 diabetes: a dose–response analysis of prospective studies. Eur J Epidemiol. 2014;29(2):79–88. doi: 10.1007/s10654-013-9876-x.
    1. Threapleton DE, et al. Dietary fibre intake and risk of cardiovascular disease: systematic review and meta-analysis. BMJ. 2013;347:f6879. doi: 10.1136/bmj.f6879.
    1. Ye EQ, et al. Greater whole-grain intake is associated with lower risk of type 2 diabetes, cardiovascular disease, and weight gain. J Nutr. 2012;142:1304–1313. doi: 10.3945/jn.111.155325.
    1. Sandberg JC, Björck IME, Nilsson AC. Rye-based evening meals favorably affected glucose regulation and appetite variables at the following breakfast; a randomized controlled study in healthy subjects. PLoS One. 2016;11(3):e0151985. doi: 10.1371/journal.pone.0151985.
    1. Johansson EV, et al. Effects of indigestible carbohydrates in barley on glucose metabolism, appetite and voluntary food intake over 16 h in healthy adults. Nutr J. 2013;12:46. doi: 10.1186/1475-2891-12-46.
    1. Nilsson AC, et al. 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. 2008;138(4):732–739.
    1. Priebe MG, et al. Factors related to colonic fermentation of nondigestible carbohydrates of a previous evening meal increase tissue glucose uptake and moderate glucose-associated inflammation. Am J Clin Nutr. 2010;91(1):90–97. doi: 10.3945/ajcn.2009.28521.
    1. Nilsson AC, et al. Effect of cereal test breakfasts differing in glycemic index and content of indigestible carbohydrates on daylong glucose tolerance in healthy subjects. Am J Clin Nutr. 2008;87(3):645–654.
    1. Nilsson A, et al. Effects of GI vs content of cereal fibre of the evening meal on glucose tolerance at a subsequent standardized breakfast. Eur J Clin Nutr. 2008;62(6):712–720. doi: 10.1038/sj.ejcn.1602784.
    1. Bodinham CL, Frost GS, Robertson MD. Acute ingestion of resistant starch reduces food intake in healthy adults. Br J Nutr. 2010;103(6):917–922. doi: 10.1017/S0007114509992534.
    1. Frolich W, Aman P, Tetens I. Whole grain foods and health - a Scandinavian perspective. Food Nutr Res. 2013;57(1):18503. doi: 10.3402/fnr.v57i0.18503.
    1. Blundell J, et al. Appetite control: methodological aspects of the evaluation of foods. Obes Rev. 2010;11(3):251–270. doi: 10.1111/j.1467-789X.2010.00714.x.
    1. Björck IME, Siljeström MA. In-vivo and in-vitro digestibility of starch in autoclaved pea and potato products. J Sci Food Agric. 1992;58(4):541–553. doi: 10.1002/jsfa.2740580414.
    1. Akerberg AK, et al. An in vitro method, based on chewing, to predict resistant starch content in foods allows parallel determination of potentially available starch and dietary fiber. J Nutr. 1998;128(3):651–660.
    1. Asp NG, et al. Rapid enzymatic assay of insoluble and soluble dietary fiber. J Agric Food Chem. 1983;31(3):476–482. doi: 10.1021/jf00117a003.
    1. McCleary BV, Murphy A, Mugford DC. Measurement of total fructan in foods by enzymatic/spectrophotometric method: collaborative study. J AOAC Int. 2000;83(2):356–364.
    1. Theander O, et al. Total dietary fiber determined as neutral sugar residues, uronic acid residues, and Klason lignin (the Uppsala method): collaborative study. J AOAC Int. 1995;78(4):1030–1044.
    1. Loosveld A-MA, Grobet PJ, Delcour JA. Contents and structural features of water-extractable arabinogalactan in wheat flour fractions. J Agric Food Chem. 1997;45(6):1998–2002. doi: 10.1021/jf960901k.
    1. Zhou J, et al. Dietary resistant starch upregulates total GLP-1 and PYY in a sustained day-long manner through fermentation in rodents. Am J Physiol Endocrinol Metab. 2008;295(5):E1160–E1166. doi: 10.1152/ajpendo.90637.2008.
    1. Reaven GM, et al. Measurement of plasma glucose, free fatty acid, lactate, and insulin for 24 h in patients with NIDDM. Diabetes. 1988;37(8):1020–1024. doi: 10.2337/diab.37.8.1020.
    1. Belfort R, et al. Dose-response effect of elevated plasma free fatty acid on insulin signaling. Diabetes. 2005;54(6):1640–1648. doi: 10.2337/diabetes.54.6.1640.
    1. Tolhurst G, et al. Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes. 2012;61(2):364–371. doi: 10.2337/db11-1019.
    1. Canfora EE, Jocken JW, Blaak EE. Short-chain fatty acids in control of body weight and insulin sensitivity. Nat Rev Endocrinol. 2015;11(10):577–591. doi: 10.1038/nrendo.2015.128.
    1. Batterham RL, et al. Inhibition of food intake in obese subjects by peptide YY3–36. N Engl J Med. 2003;349(10):941–948. doi: 10.1056/NEJMoa030204.
    1. De Silva A, Bloom SR. Gut hormones and appetite control: a focus on PYY and GLP-1 as therapeutic targets in obesity. Gut Liver. 2012;6(1):10–20. doi: 10.5009/gnl.2012.6.1.10.
    1. Tan T, Bloom S. Gut hormones as therapeutic agents in treatment of diabetes and obesity. Curr Opin Pharmacol. 2013;13(6):996–1001. doi: 10.1016/j.coph.2013.09.005.
    1. Cooper JA. Factors affecting circulating levels of peptide YY in humans: a comprehensive review. Nutr Res Rev. 2014;27(1):186–197. doi: 10.1017/S0954422414000109.
    1. Ibrugger S, et al. Second meal effect on appetite and fermentation of wholegrain rye foods. Appetite. 2014;80:248–256. doi: 10.1016/j.appet.2014.05.026.
    1. Ekstrom LM, Bjorck IM, Ostman EM. On the possibility to affect the course of glycaemia, insulinaemia, and perceived hunger/satiety to bread meals in healthy volunteers. Food Funct. 2013;4(4):522–529. doi: 10.1039/c2fo30251a.
    1. Rosen LA, et al. Postprandial glycemia, insulinemia, and satiety responses in healthy subjects after whole grain rye bread made from different rye varieties. 1. J Agric Food Chem. 2011;59(22):12139–12148. doi: 10.1021/jf2019825.
    1. Isaksson H, et al. Rye kernel breakfast increases satiety in the afternoon - an effect of food structure. Nutr J. 2011;10:31. doi: 10.1186/1475-2891-10-31.

Source: PubMed

Sponsorer og samarbejdspartnere

Medicinske tilstande

Narkotikainterventioner

3
Abonner