Nontargeted metabolite profiling discriminates diet-specific biomarkers for consumption of whole grains, fatty fish, and bilberries in a randomized controlled trial

Journal of Nutrition

Volumn 145, Issue 1, 2015, Pages 7-17

  Hanhineva, Kati ^a   Lankinen, Maria A ^a   Pedret, Anna ^b   Schwab, Ursula ^a,b   Kolehmainen, Marjukka ^a   Paananen, Jussi ^a   de Mello, Vanessa ^a   Sola, Rosa ^b   Lehtonen, Marko ^a   Poutanen, Kaisa ^a,c   Uusitupa, Matti ^a   Mykkänen, Hannu ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b INSTITUT D INVESTIGACIÓ SANITÀRIA PERE VIRGILI IISPV   (Spain)

^c VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

Author keywords

Alkylresorcinol; CMPF; Dietary biomarker; Hippuric acid; Metabolomics; Nontargeted metabolite profiling

Indexed keywords

3 CARBOXY 4 METHYL 5 PROPYL 2 FURANPROPIONIC ACID; ALKENE DERIVATIVE; BIOLOGICAL MARKER; FATTY ACID DERIVATIVE; FURAN DERIVATIVE; HIPPURIC ACID; LIPID; POLYUNSATURATED FATTY ACID; RESORCINOL DERIVATIVE; UNCLASSIFIED DRUG; 3-CARBOXY-4-METHYL-5-PROPYL-2-FURANPROPANOIC ACID; PROPIONIC ACID DERIVATIVE;

ARTICLE; BLOOD LEVEL; BREAD; CONTROLLED STUDY; DIET THERAPY; DIETARY INTAKE; FATTY ACID BLOOD LEVEL; FISH; GRAIN; HUMAN; MAJOR CLINICAL STUDY; METABOLIC SYNDROME X; METABOLISM; METABOLITE; NONHUMAN; RANDOMIZED CONTROLLED TRIAL; VACCINIUM MYRTILLUS; ANIMAL; BLOOD; CEREAL; DIET; DIET RESTRICTION; DIET SUPPLEMENTATION; ELECTROSPRAY MASS SPECTROMETRY; FEEDING BEHAVIOR; FEMALE; FINLAND; FRUIT; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; METABOLOME;

TRITICUM AESTIVUM;

ANIMALS; BIOLOGICAL MARKERS; CEREALS; CHROMATOGRAPHY, LIQUID; DIET; FASTING; FEMALE; FINLAND; FISHES; FOOD HABITS; FOOD, FORTIFIED; FRUIT; FURANS; HUMANS; MALE; MASS SPECTROMETRY; METABOLIC SYNDROME X; METABOLOME; PROPIONATES; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; VACCINIUM MYRTILLUS;

EID: 84919776032     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.114.196840     Document Type: Article

References (55)

1. 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;141:639-44.
2. 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;77:385-91.
3. Laaksonen DE, Toppinen LK, Juntunen KS, Autio K, Liukkonen KH, Poutanen KS, Niskanen L, Mykkanen HM. Dietary carbohydrate modification enhances insulin secretion in persons with the metabolic syndrome. Am J Clin Nutr 2005;82:1218-27.
4. Adamsson V, Reumark A, Fredriksson IB, Hammarstrom E, Vessby B, Johansson G, Riserus U. Effects of a healthy Nordic diet on cardiovascular risk factors in hypercholesterolaemic subjects: a randomized controlled trial (NORDIET). J Intern Med 2011;269:150-9.
5. Kolehmainen M, Mykkanen O, Kirjavainen PV, Leppanen T, Moilanen E, Adriaens M, Laaksonen DE, Hallikainen M, Puupponen-Pimia R, Pulkkinen L, et al. Bilberries reduce low-grade inflammation in individuals with features of metabolic syndrome. Mol Nutr Food Res 2012;56:1501-10.
6. Lankinen M, Schwab U, Kolehmainen M, Paananen J, Poutanen K, Mykkanen H, Seppanen-Laakso T, Gylling H, Uusitupa M, Oresic M. Whole grain products, fish and bilberries alter glucose and lipid metabolism in a randomized, controlled trial: the Sysdimet study. PLoS ONE 2011;6:e22646.
7. de Mello VD, Schwab U, Kolehmainen M, Koenig W, Siloaho M, Poutanen K, Mykkanen H, Uusitupa M. A diet high in fatty fish, bilberries and wholegrain products improves markers of endothelial function and inflammation in individuals with impaired glucose metabolism in a randomised controlled trial: the Sysdimet study. Diabetologia 2011;54:2755-67.
8. Uusitupa M, Hermansen K, Savolainen MJ, Schwab U, Kolehmainen M, Brader L, Mortensen LS, Cloetens L, Johansson-Persson A, Onning G, et al. Effects of an isocaloric healthy Nordic diet on insulin sensitivity, lipid profile and inflammation markers in metabolic syndrome-a randomized study (SYSDIET). J Intern Med 2013;274:52-66.
9. Brennan L. Metabolomics in nutrition research: current status and perspectives. Biochem Soc Trans 2013;41:670-3.
10. O'Sullivan A, Gibney MJ, Brennan L. Dietary intake patterns are reflected in metabolomic profiles: potential role in dietary assessment studies. Am J Clin Nutr 2011;93:314-21.
11. Wishart DS. Metabolomics: applications to food science and nutrition research. Trends Food Sci Technol 2008;19:482-93.
12. Llorach R, Garcia-Aloy M, Tulipani S, Vazquez-Fresno R, Andres-Lacueva C. Nutrimetabolomic strategies to develop new biomarkers of intake and health effects. J Agric Food Chem 2012;60:8797-808.
13. Scalbert A, Brennan L, Manach C, Andres-Lacueva C, Dragsted LO, Draper J, Rappaport SM, van der Hooft JJ, Wishart DS. The food metabolome: a window over dietary exposure. Am J Clin Nutr 2014;99(6):1286-1308.
14. Rastas M, Seppänen R, Knuts L, Karvetti R, Varo P. Ruokien ravintoainesisältö. [Nutrient composition of foods.] 4th ed. Turku (Finland): Social Insurance Institution; 1997 (in Finnish).
15. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 1995;57:289-300.
16. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J. TM4 microarray software suite. Methods Enzymol 2006;411:134-93.
17. Buré C, Ayciriex S, Testet E, Schmitter JM. A single run LC-MS/MS method for phospholipidomics. Anal Bioanal Chem 2013;405:203-13.
18. Xia YQ, Jemal M. Phospholipids in liquid chromatography/mass spectrometry bioanalysis: comparison of three tandem mass spectrometric techniques for monitoring plasma phospholipids, the effect of mobile phase composition on phospholipids elution and the association of phospholipids with matrix effects. Rapid Commun Mass Spectrom 2009;23:2125-38.
19. Murphy RC, Axelsen PH. Mass spectrometric analysis of long-chain lipids. Mass Spectrom Rev 2011;30:579-99.
20. Pinheiro J, Bates D, DebRoy S, Sarkar D. R core team. Linear and nonlinear mixed effects models. 2009; R package version 3:1-96.
21. Niwa T, Takeda N, Maeda K, Shibata M, Tatematsu A. Accumulation of furancarboxylic acids in uremic serum as inhibitors of drug binding. Clin Chim Acta 1988;173:127-38.
22. Hannemann K, Puchta V, Simon E, Ziegler H, Ziegler G, Spiteller G. The common occurrence of furan fatty acids in plants. Lipids 1989;24:296-8.
23. Fujita T, Hada T, Higashino K. Origin of D- and L-pipecolic acid in human physiological fluids: a study of the catabolic mechanism to pipecolic acid using the lysine loading test. Clin Chim Acta 1999;287:145-56.
24. Suzuki Yesumi Y, Uramoto M, Kono Y, Sakurai A. Structural analyses of carbon chains in 5-alk(en)ylresorcinols of rye and wheat whole flour by tandem mass spectrometry. Biosci Biotechnol Biochem 1997;61:480-6.
25. Zhu Y, Conklin DR, Chen H, Wang L, Sang S. 5-Alk(en)ylresorcinols as the major active components in wheat bran inhibit human colon cancer cell growth. Bioorg Med Chem 2011;19:3973-82.
26. Holm PI, Ueland PM, Kvalheim G, Lien EA. Determination of choline, betaine, and dimethylglycine in plasma by a high-throughput method based on normal-phase chromatography-tandem mass spectrometry. Clin Chem 2003;49:286-94.
27. 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;58:2055-61.
28. VetterW,Wendlinger C. Furan fatty acids? Valuable minor fatty acids in food. Lipid Technology 2013;25:7-10.
29. Toshimitsu N. 3-Carboxy-4-methyl-5-propyl-2-furanpropionic acid. In: Desiderio DM, Nibbering NMM, editors. Uremic toxins. Hoboken (NJ): John Wiley&Sons; 2012. p. 87-98.
30. Watanabe H, Miyamoto Y, Otagiri M, Maruyama T. Update on the pharmacokinetics and redox properties of protein-bound uremic toxins. J Pharm Sci 2011;100:3682-95.
31. Boelaert J, Lynen F, Glorieux G, Eloot S, Van Landschoot M, Waterloos MA, Sandra P, Vanholder R. A novel UPLC-MS-MS method for simultaneous determination of seven uremic retention toxins with cardiovascular relevance in chronic kidney disease patients. Anal Bioanal Chem 2013;405:1937-47.
32. Ross AB. Present status and perspectives on the use of alkylresorcinols as biomarkers of wholegrain wheat and rye intake. J Nutr Metab 2012;462967.
33. Landberg R, Åman P, Kamal-Eldin A. A rapid gas chromatography-mass spectrometry method for quantification of alkylresorcinols in human plasma. Anal Biochem 2009;385:7-12.
34. Marklund M, Landberg R, Aman P, Kamal-Eldin A. Determination of alkylresorcinol metabolites in human urine by gas chromatographymass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 2010;878:888-94.
35. Landberg R, Marklund M, Kamal-Eldin A, Åman P. An update on alkylresorcinols-occurrence, bioavailability, bioactivity and utility as biomarkers. J Funct Foods 2014;7:77-89.
36. Zhu Y, Shurlknight KL, Chen X, Sang S. Identification and pharmacokinetics of novel alkylresorcinol metabolites in human urine, new candidate biomarkers for whole-grain wheat and rye intake. J Nutr 2014;144:114-22.
37. Landberg R, Linko AM, Kamal-Eldin A, Vessby B, Adlercreutz H, Aman P. Human plasma kinetics and relative bioavailability of alkylresorcinols after intake of rye bran. J Nutr 2006;136:2760-5.
38. van Dorsten FA, Grun CH, van Velzen EJ, Jacobs DM, Draijer R, van Duynhoven JP. The metabolic fate of red wine and grape juice polyphenols in humans assessed by metabolomics. Mol Nutr Food Res 2010;54:897-908.
39. Mulder TP, Rietveld AG, van Amelsvoort JM. Consumption of both black tea and green tea results in an increase in the excretion of hippuric acid into urine. Am J Clin Nutr 2005;81:256S-60S.
40. Valentova K, Stejskal D, Bednar P, Vostalova J, Cihalik C, Vecerova R, Koukalova D, Kolar M, Reichenbach R, Sknouril L, et al. Biosafety, antioxidant status, and metabolites in urine after consumption of dried cranberry juice in healthy women: a pilot double-blind placebocontrolled trial. J Agric Food Chem 2007;55:3217-24.
41. Jin Y, Alimbetov D, George T, Gordon MH, Lovegrove JA. A randomised trial to investigate the effects of acute consumption of a blackcurrant juice drink on markers of vascular reactivity and bioavailability of anthocyanins in human subjects. Eur J Clin Nutr 2011;65:849-56.
42. Krupp D, Doberstein N, Shi L, Remer T. Hippuric acid in 24-hour urine collections is a potential biomarker for fruit and vegetable consumption in healthy children and adolescents. J Nutr 2012;142:1314-20.
43. Nurmi T, Mursu J, Heinonen M, Nurmi A, Hiltunen R, Voutilainen S. Metabolism of berry anthocyanins to phenolic acids in humans. J Agric Food Chem 2009;57:2274-81.
44. Del Bo' C, Riso P, Brambilla A, Gardana C, Rizzolo A, Simonetti P, Bertolo G, Klimis-Zacas D, Porrini M. Blanching improves anthocyanin absorption from highbush blueberry (Vaccinium corymbosum L.) puree in healthy human volunteers: a pilot study. J Agric Food Chem 2012;60:9298-304.
45. Bondia-Pons I, Barri T, Hanhineva K, Juntunen K, Dragsted LO, Mykkanen H, Poutanen K. UPLC-QTOF/MS metabolic profiling unveils urinary changes in humans after a whole grain rye versus refined wheat bread intervention.Mol Nutr Food Res 2013;57(3):412-22.
46. Pekkinen J, Rosa NN, Savolainen OI, Keski-Rahkonen P, Mykkanen H, Poutanen K, Micard V, Hanhineva K. Disintegration of wheat aleurone structure has an impact on the bioavailability of phenolic compounds and other phytochemicals as evidenced by altered urinary metabolite profile of diet-induced obese mice. Nutr Metab (Lond) 2014;11:7075-11-1.
47. Altorf-van der Kuil W, Brink EJ, Boetje M, Siebelink E, Bijlsma S, Engberink MF, van't Veer P, Tome D, Bakker SJ, van Baak MA, et al. Identification of biomarkers for intake of protein from meat, dairy products and grains: a controlled dietary intervention study. Br J Nutr 2013;110:810-22.
48. Ross AB, Zangger A, Guiraud SP. Cereal foods are the major source of betaine in the Western diet-analysis of betaine and free choline in cereal foods and updated assessments of betaine intake. Food Chem 2014;145:859-65.
49. Moazzami AA, Bondia-Pons I, Hanhineva K, Juntunen K, Antl N, Poutanen K, Mykkanen H. Metabolomics reveals the metabolic shifts following an intervention with rye bread in postmenopausal women-a randomized control trial. Nutr J 2012;11:88.
50. Moazzami AA, Zhang JX, Kamal-Eldin A, Aman P, Hallmans G, Johansson JE, Andersson SO. Nuclear magnetic resonance-based metabolomics enable 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;141:2126-32.
51. Ross AB, Bruce SJ, Blondel-Lubrano A, Oguey-Araymon S, Beaumont M, Bourgeois A, Nielsen-Moennoz C, Vigo M, Fay LB, Kochhar S, et al. A whole-grain cereal-rich diet increases plasma betaine, and tends to decrease total and LDL-cholesterol compared with a refined-grain diet in healthy subjects. Br J Nutr 2011;105:1492-502.
52. Price RK, Keaveney EM, Hamill LL, Wallace JM, Ward M, Ueland PM, McNulty H, Strain JJ, Parker MJ, Welch RW. Consumption of wheat aleurone-rich foods increases fasting plasma betaine and modestly decreases fasting homocysteine and LDL-cholesterol in adults. J Nutr 2010;140:2153-7.
53. Servillo L, Giovane A, Balestrieri ML, Ferrari G, Cautela D, Castaldo D. Occurrence of pipecolic acid and pipecolic acid betaine (homostachydrine) in citrus genus plants. J Agric Food Chem 2012;60:315-21.
54. Struys EA, Jakobs C. Metabolism of lysine in alpha-aminoadipic semialdehyde dehydrogenase-deficient fibroblasts: evidence for an alternative pathway of pipecolic acid formation. FEBS Lett 2010;584:181-6.
55. Pekkinen J, Olli K, Huotari A, Tiihonen K, Keski-Rahkonen P, Lehtonen M, Auriola S, Kolehmainen M, Mykkanen H, Poutanen K, et al. Betaine supplementation causes increase in carnitine metabolites in the muscle and liver of mice fed a high-fat diet as studied by nontargeted LC-MS metabolomics approach. Mol Nutr Food Res 2013;57:1959-68.