Nutrition Journal | |
Metabolomics reveals the metabolic shifts following an intervention with rye bread in postmenopausal women- a randomized control trial | |
Hannu Mykkänen3  Kaisa Poutanen2  Nadja Antl1  Katri Juntunen4  Kati Hanhineva3  Isabel Bondia-Pons2  Ali A Moazzami1  | |
[1] Department of Food Science, Swedish University of Agricultural Sciences, Uppsala, Sweden;VTT Technical Research Centre of Finland, P.O. Box 1000, Tietotie 2, Espoo, FI-02044, Finland;Department of Public Health and Clinical Nutrition, Clinical Nutrition, Food and Health Research Centre, University of Eastern Finland, Kuopio Campus, P.O. Box 1627, Kuopio, FIN 70211, Finland;City of Kuopio, Health Care Services, Health Care Unit, Suokatu 40 B, Kuopio, FI-70110, Finland | |
关键词: Single carbon metabolism; Postmenopausal; Homocysteine; Amino acid; NMR; Metabolomics; Wheat; Whole grain rye; | |
Others : 823884 DOI : 10.1186/1475-2891-11-88 |
|
received in 2012-05-20, accepted in 2012-10-11, 发布年份 2012 | |
【 摘 要 】
Background
Epidemiological studies have consistently shown that whole grain (WG) cereals can protect against the development of chronic diseases, but the underlying mechanism is not fully understood. Among WG products, WG rye is considered even more potent because of its unique discrepancy in postprandial insulin and glucose responses known as the rye factor. In this study, an NMR-based metabolomics approach was applied to study the metabolic effects of WG rye as a tool to determine the beneficial effects of WG rye on human health.
Methods
Thirty-three postmenopausal Finnish women with elevated serum total cholesterol (5.0-8.5 mmol/L) and BMI of 20–33 kg/m2 consumed a minimum of 20% of their daily energy intake as high fiber WG rye bread (RB) or refined wheat bread (WB) in a randomized, controlled, crossover design with two 8-wk intervention periods separated by an 8-wk washout period. At the end of each intervention period, fasting serum was collected for NMR-based metabolomics and the analysis of cholesterol fractions. Multilevel partial least squares discriminant analysis was used for paired comparisons of multivariate data.
Results
The metabolomics analysis of serum showed lower leucine and isoleucine and higher betaine and N,N-dimethylglycine levels after RB than WB intake. To further investigate the metabolic effects of RB, the serum cholesterol fractions were measured. Total- and LDL-cholesterol levels were higher after RB intake than after WB (p<0.05).
Conclusions
This study revealed favorable shifts in branched amino acid and single carbon metabolism and an unfavorable shift in serum cholesterol levels after RB intake in postmenopausal women, which should be considered for evaluating health beneficial effects of rye products.
【 授权许可】
2012 Moazzami et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20140713015147608.pdf | 231KB | download | |
Figure 1. | 19KB | Image | download |
【 图 表 】
Figure 1.
【 参考文献 】
- [1]Fardet A: New hypotheses for the health-protective mechanisms of whole-grain cereals: what is beyond fibre? Nutr Res Rev 2010, 23:65-134.
- [2]De Munter JS, Hu FB, Spiegelman D, Franz M, Van Dam RM: Whole grain, bran, and germ intake and risk of type 2 diabetes: a prospective cohort study and systematic review. PLoS Med 2007, 4:e261.
- [3]Murtaugh MA, Jacobs DR, Jacob B, Steffen LM, Marquart L: Epidemiological support for the protection of whole grains against diabetes. Proc Nutr Soc 2003, 62:143-149.
- [4]Jacobs DR, Andersen LF, Blomhoff R: Whole-grain consumption is associated with a reduced risk of noncardiovascular, noncancer death attributed to inflammatory diseases in the Iowa Women’s Health Study. Am J Clin Nutr 2007, 85:1606-1614.
- [5]Mellen PB, Walsh TF, Herrington DM: Whole grain intake and cardiovascular disease: a meta-analysis. Nutr Metab Cardiovasc Dis 2008, 18:283-290.
- [6]Flint AJ, Hu FB, Glynn RJ, Jensen MK, Franz M, Sampson L, Rimm EB: Whole grains and incident hypertension in men. Am J Clin Nutr 2009, 90:493-498.
- [7]Larsson SC, Giovannucci E, Bergkvist L, Wolk A: Whole grain consumption and risk of colorectal cancer: a population-based cohort of 60,000 women. Br J Cancer 2005, 92:1803-1807.
- [8]Chan JM, Wang F, Holly EA: Whole grains and risk of pancreatic cancer in a large population-based case–control study in the San Francisco Bay Area, California. Am J Epidemiol 2007, 166:1174-1185.
- [9]Schatzkin A, Park Y, Leitzmann MF, Hollenbeck AR, Cross AJ: Prospective study of dietary fiber, whole grain foods, and small intestinal cancer. Gastroenterology 2008, 135:1163-1167.
- [10]Haas P, Machado MJ, Anton AA, Silva AS, De Francisco A: Effectiveness of whole grain consumption in the prevention of colorectal cancer: Meta-analysis of cohort studies. Int J Food Sci Nutr 2009, 60:1-13.
- [11]Rosen LA, Silva LO, Andersson UK, Holm C, Ostman EM, Bjorck IM: Endosperm and whole grain rye breads are characterized by low post-prandial insulin response and a beneficial blood glucose profile. Nutr J 2009, 8:42. BioMed Central Full Text
- [12]Olsen A, Egeberg R, Halkjaer J, Christensen J, Overvad K, Tjonneland A: Healthy aspects of the Nordic diet are related to lower total mortality. J Nutr 2011, 141:639-644.
- [13]Szmuilowicz ED, Stuenkel CA, Seely EW: Influence of menopause on diabetes and diabetes risk. Nat Rev Endocrinol 2009, 5:553-558.
- [14]Adams SH: Emerging perspectives on essential amino acid metabolism in obesity and the insulin-resistant state. Adv Nutr 2011, 2:445-456.
- [15]Moazzami AA, Zhang JX, Kamal-Eldin A, Aman P, Hallmans G, Johansson JE, Andersson SO: Nuclear Magnetic Resonance-Based Metabolomics Enables Detection of the Effects of a Whole Grain Rye and Rye Bran Diet on the Metabolic Profile of Plasma in Prostate Cancer Patients. J Nutr 2011, 141:2126-2132.
- [16]Lankinen M, Schwab U, Seppanen-Laakso T, Mattila I, Juntunen K, Mykkanen H, Poutanen K, Gylling H, Oresic M: Metabolomic analysis of plasma metabolites that may mediate effects of rye bread on satiety and weight maintenance in postmenopausal women. J Nutr 2011, 141:31-36.
- [17]Lankinen M, Schwab U, Gopalacharyulu PV, Seppanen-Laakso T, Yetukuri L, Sysi-Aho M, Kallio P, Suortti T, Laaksonen DE, Gylling H, et al.: Dietary carbohydrate modification alters serum metabolic profiles in individuals with the metabolic syndrome. Nutr Metab Cardiovasc Dis 2010, 20:249-257.
- [18]Fardet A, Canlet C, Gottardi G, Lyan B, Llorach R, Remesy C, Mazur A, Paris A, Scalbert A: Whole-grain and refined wheat flours show distinct metabolic profiles in rats as assessed by a 1H NMR-based metabonomic approach. J Nutr 2007, 137:923-929.
- [19]Juntunen KS, Laaksonen DE, Poutanen KS, Niskanen LK, Mykkanen HM: High-fiber rye bread and insulin secretion and sensitivity in healthy postmenopausal women. Am J Clin Nutr 2003, 77:385-391.
- [20]Tiziani S, Einwas AH, Lodi A, Ludwig C, Bunce CM, Viant MR, Gunther UL: Optimized metabolite extraction from blood serum for H-1 nuclear magnetic resonance spectroscopy. Anal Biochem 2008, 377:16-23.
- [21]Hwang TL, Shaka AJ: Water Suppression That Works - Excitation Sculpting Using Arbitrary Wave-Forms and Pulsed-Field Gradients. J Magn Reson Series A 1995, 112:275-279.
- [22]Psychogios N, Hau DD, Peng J, Guo AC, Mandal R, Bouatra S, Sinelnikov I, Krishnamurthy R, Eisner R, Gautam B, et al.: The human serum metabolome. PLoS One 2011, 6:e16957.
- [23]Moazzami AA, Andersson R, Kamal-Eldin A: Changes in the metabolic profile of rat liver after alpha-tocopherol deficiency as revealed by metabolomics analysis. NMR Biomed 2011, 24:499-505.
- [24]van Velzen EJ, Westerhuis JA, van Duynhoven JP, van Dorsten FA, Hoefsloot HC, Jacobs DM, Smit S, Draijer R, Kroner CI, Smilde AK: Multilevel data analysis of a crossover designed human nutritional intervention study. J Proteome Res 2008, 7:4483-4491.
- [25]Westerhuis JA, Van Velzen EJ, Hoefsloot HC, Smilde AK: Multivariate paired data analysis: multilevel PLSDA versus OPLSDA. Metabolomics 2010, 6:119-128.
- [26]Yde CC, Westerhuis JA, Bertram HC, Bach Knudsen KE: Application of NMR-based metabonomics suggests a relationship between betaine absorption and elevated creatine plasma concentrations in catheterised sows. Br J Nutr 2012, 107:1603-1615.
- [27]Slavin JL, Jacobs D, Marquart L, Wiemer K: The role of whole grains in disease prevention. J Am Diet Assoc 2001, 101:780-785.
- [28]Wang TJ, Larson MG, Vasan RS, Cheng S, Rhee EP, McCabe E, Lewis GD, Fox CS, Jacques PF, Fernandez C, et al.: Metabolite profiles and the risk of developing diabetes. Nat Med 2011, 17:448-453.
- [29]Felig P, Marliss E, Cahill GF: Plasma amino acid levels and insulin secretion in obesity. N Engl J Med 1969, 281:811-816.
- [30]Patti ME, Brambilla E, Luzi L, Landaker EJ, Kahn CR: Bidirectional modulation of insulin action by amino acids. J Clin Invest 1998, 101:1519-1529.
- [31]Newgard CB, An J, Bain JR, Muehlbauer MJ, Stevens RD, Lien LF, Haqq AM, Shah SH, Arlotto M, Slentz CA, et al.: A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metab 2009, 9:311-326.
- [32]Krebs M, Krssak M, Bernroider E, Anderwald C, Brehm A, Meyerspeer M, Nowotny P, Roth E, Waldhausl W, Roden M: Mechanism of amino acid-induced skeletal muscle insulin resistance in humans. Diabetes 2002, 51:599-605.
- [33]Meigs JB, Shrader P, Sullivan LM, McAteer JB, Fox CS, Dupuis J, Manning AK, Florez JC, Wilson PW, D’Agostino RB, Cupples LA: Genotype score in addition to common risk factors for prediction of type 2 diabetes. N Engl J Med 2008, 359:2208-2219.
- [34]Lyssenko V, Jonsson A, Almgren P, Pulizzi N, Isomaa B, Tuomi T, Berglund G, Altshuler D, Nilsson P, Groop L: Clinical risk factors, DNA variants, and the development of type 2 diabetes. N Engl J Med 2008, 359:2220-2232.
- [35]Leinonen K, Liukkonen K, Poutanen K, Uusitupa M, Mykkanen H: Rye bread decreases postprandial insulin response but does not alter glucose response in healthy Finnish subjects. Eur J Clin Nutr 1999, 53:262-267.
- [36]Juntunen KS, Laaksonen DE, Autio K, Niskanen LK, Holst JJ, Savolainen KE, Liukkonen KH, Poutanen KS, Mykkanen HM: Structural differences between rye and wheat breads but not total fiber content may explain the lower postprandial insulin response to rye bread. Am J Clin Nutr 2003, 78:957-964.
- [37]Kallio P, Kolehmainen M, Laaksonen DE, Pulkkinen L, Atalay M, Mykkanen H, Uusitupa M, Poutanen K, Niskanen L: Inflammation markers are modulated by responses to diets differing in postprandial insulin responses in individuals with the metabolic syndrome. Am J Clin Nutr 2008, 87:1497-1503.
- [38]Juntunen KS, Niskanen LK, Liukkonen KH, Poutanen KS, Holst JJ, Mykkanen HM: Postprandial glucose, insulin, and incretin responses to grain products in healthy subjects. Am J Clin Nutr 2002, 75:254-262.
- [39]Bondia-Pons I, Nordlund E, Mattila I, Katina K, Aura AM, Kolehmainen M, Oresic M, Mykkanen H, Poutanen K: Postprandial differences in the plasma metabolome of healthy Finnish subjects after intake of a sourdough fermented endosperm rye bread versus white wheat bread. Nutr J 2011, 10:116. BioMed Central Full Text
- [40]Ludwig DS: The glycemic index: physiological mechanisms relating to obesity, diabetes, and cardiovascular disease. JAMA 2002, 287:2414-2423.
- [41]Bruce SJ, Guy PA, Rezzi S, Ross AB: Quantitative measurement of betaine and free choline in plasma, cereals and cereal products by isotope dilution LC-MS/MS. J Agric Food Chem 2010, 58:2055-2061.
- [42]Bertram HC, Bach Knudsen KE, Serena A, Malmendal A, Nielsen NC, Frette XC, Andersen HJ: NMR-based metabonomic studies reveal changes in the biochemical profile of plasma and urine from pigs fed high-fibre rye bread. Br J Nutr 2006, 95:955-962.
- [43]Bertram HC, Malmendal A, Nielsen NC, Straadt IK, Larsen T, Knudsen KE, Laerke HN: NMR-based metabonomics reveals that plasma betaine increases upon intake of high-fiber rye buns in hypercholesterolemic pigs. Mol Nutr Food Res 2009, 53:1055-1062.
- [44]Wang Z, Klipfell E, Bennett BJ, Koeth R, Levison BS, Dugar B, Feldstein AE, Britt EB, Fu X, Chung YM, et al.: Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 2011, 472:57-63.
- [45]Delgado-Reyes CV, Garrow TA: High sodium chloride intake decreases betaine-homocysteine S-methyltransferase expression in guinea pig liver and kidney. Am J Physiol Regul Integr Comp Physiol 2005, 288:R182-R187.
- [46]Ratnam S, Wijekoon EP, Hall B, Garrow TA, Brosnan ME, Brosnan JT: Effects of diabetes and insulin on betaine-homocysteine S-methyltransferase expression in rat liver. Am J Physiol Endocrinol Metab 2006, 290:E933-E939.
- [47]Clarke R, Daly L, Robinson K, Naughten E, Cahalane S, Fowler B, Graham I: Hyperhomocysteinemia: an independent risk factor for vascular disease. N Engl J Med 1991, 324:1149-1155.
- [48]Kang SS, Wong PW, Malinow MR: Hyperhomocyst(e)inemia as a risk factor for occlusive vascular disease. Annu Rev Nutr 1992, 12:279-298.
- [49]Vizzardi E, Bonadei I, Zanini G, Frattini S, Fiorina C, Raddino R, Dei Cas L: Homocysteine and heart failure: an overview. Recent Pat Cardiovasc Drug Discov 2009, 4:15-21.
- [50]Olthof MR, Van Vliet T, Verhoef P, Zock PL, Katan MB: Effect of homocysteine-lowering nutrients on blood lipids: results from four randomised, placebo-controlled studies in healthy humans. PLoS Med 2005, 2:e135.