Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-10T14:19:31.921Z Has data issue: false hasContentIssue false
  • English
  • Français

NMR-based metabonomic studies reveal changes in the biochemical profile ofplasma and urine from pigs fed high-fibre rye bread

Published online by Cambridge University Press:  08 March 2007

Hanne C. Bertram ,
Knud E. Bach Knudsen ,
Anja Serena ,
Anders Malmendal ,
Niels Chr. Nielsen ,
Xavier C. Fretté  and
Henrik J. Andersen
Hanne C. Bertram*
Affiliation:
Department of Food Science, Danish Institute of Agricultural Sciences, Box 50, DK-8830 Tjele, Denmark
Knud E. Bach Knudsen
Affiliation:
Department of Animal Health, Welfare and Nutrition, Danish Institute of Agricultural Sciences, Box 50, DK-8830 Tjele, Denmark
Anja Serena
Affiliation:
Department of Animal Health, Welfare and Nutrition, Danish Institute of Agricultural Sciences, Box 50, DK-8830 Tjele, Denmark
Anders Malmendal
Affiliation:
Department of Chemistry and Interdisciplinary Nanoscience Center (iNANO), University of Aarhus, Langelandsgade 140, DK-8000 Aarhus C, Denmark
Niels Chr. Nielsen
Affiliation:
Department of Chemistry and Interdisciplinary Nanoscience Center (iNANO), University of Aarhus, Langelandsgade 140, DK-8000 Aarhus C, Denmark
Xavier C. Fretté
Affiliation:
Department of Food Science, Danish Institute of Agricultural Sciences, Box 50, DK-8830 Tjele, Denmark
Henrik J. Andersen
Affiliation:
Department of Food Science, Danish Institute of Agricultural Sciences, Box 50, DK-8830 Tjele, Denmark
*
*Corresponding author: Dr Hanne C. Bertram, fax +45 89 99 15 64, email HanneC.Bertram@agrsci.dk
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

This study presents an NMR-based metabonomic approach to elucidate the overall endogenous biochemical effects of a wholegrain diet. Two diets with similar levels of dietary fibre and macronutrients, but with contrasting levels of wholegrain ingredients, were prepared from wholegrain rye (wholegrain diet (WGD)) and non-wholegrain wheat (non-wholegrain diet (NWD)) and fed to four pigs in a crossover design. Plasma samples were collected after 7 d on each diet, and 1H NMR spectra were acquired on these. Partial least squares regression discriminant analysis (PLSDA) on spectra obtained for plasma samples revealed that the spectral region at 3·25 parts per million dominates the differentiation between the two diets, as the WGD is associated with higher spectral intensity in this region. Spiking experiments and LC–MS analyses of the plasma verified that this spectral difference could be ascribed to a significantly higher content of betaine in WGD plasma samples compared with NWD samples. In an identical study with the same diets, urine samples were collected, and1H NMR spectra were acquired on these. PLS-DA on spectra obtained for urine samples revealed changes in the intensities of spectral regions, which could be ascribed to differences in the content of betaine and creatine/creatinine between the two diets, and LC–MS analyses verified a significantly lower content of creatinine in WGD urine samples compared with NWD urine samples. In conclusion, using an explorative approach, the present studies disclosed biochemical effects of a wholegrain diet on plasma betaine content and excretion of betaine and creatinine.

Keywords

NMRBetaineCreatinineWholegrainMetabolomics
Type
Research Article
Information
British Journal of Nutrition , Volume 95 , Issue 5 , May 2006 , pp. 955 - 962
Copyright
Copyright © The Nutrition Society 2006

References

Anderson, JW, Hanna, TJ, Peng, X&Kryscio, RJWhole grain foods and heart disease risk. J Am Coll Nutr 2000 19.S291–S299.CrossRefGoogle ScholarPubMed
Anon Betaine Monograph. Altern Med Rev 2003 8, 193–196.Google Scholar
Antolini, F, Valente, F, Ricciardi, D&Fagugli, RMNormalization of oxidative stress parameters after kidney transplants is secondary to full recovery of renal function. Clin Nephrol 2004 62, 131–137.CrossRefGoogle ScholarPubMed
Armstrong, LE, Roti, MW, Hatch, HL, et al.. Rehydration with fluids containing betaine: running performance and metabolism in a 31 C environment. Med Sci Sports Exerc 2003 35, S311, Abstr.CrossRefGoogle Scholar
Bach Knudsen, KE, Serena, A, Kjær, AKB, Jørgensen, H&Engberg, RRye bread enhances the production and plasma concentration of butyrate but not the plasma concentrations of glucose and insulin in pigs. J Nutr 2005 135, 1696–1704.CrossRefGoogle Scholar
Bach Knudsen, KE, Serena, A, Kjær, AKB, Tetens, I, Heinonen, S-M, Nurmi, T&Adlercreutz, HRye bread in the diet of pigs enhances the formation of enterolactone and increases its levels in plasma, urine and feces. J Nutr 2003 133, 1368–1375.CrossRefGoogle ScholarPubMed
Balkan, J, Öztezcan, S, Küçük, M, Çevikbas, U, Koçak-Toker, N&Uysal, MThe effect of betaine treatment on triglyceride levels and antioxidative stress in the liver of ethanol-treated guinea pigs. Exp Toxicol Pathol 2004 55.505–509.CrossRefGoogle ScholarPubMed
Beckonert, O, Bollard, ME, Ebbels, TMD, Keun, HC, Antii, H, Holmes, E, Lindon, JC&Nicholson, JKNMR-based metabonomic toxicity classification: hierarchical cluster analysis and knearest-neighbour approaches. Anal Chim Acta 2003 490, 3–15.CrossRefGoogle Scholar
Beckwith-Hall, BM, Holmes, E, Lindon, JC, Gounarides, J, Vickers, A, Shapiro, M&Nicholson, JKNMR-based metabonomic studies on the biochemical effects of commonly used drug carrier vehicles in the rat. Chem Res Toxicol 2002 15, 1136–1141.CrossRefGoogle ScholarPubMed
Borsook, ME&Borsook, HTreatment of cardiac compensation with betaine and glycosamine. Ann West Med Surg 1951 5, 830–855Google Scholar
Burg, MMolecular basis of osmotic regulation. Am J Physiol 1995 268, F983–F996.Google ScholarPubMed
Caldas, T, Demont-Caulet, N, Ghazi, A&Richarme, GThermoprotection by glycine betaine and choline. Microbiology 1999 145, 2543–2548.CrossRefGoogle ScholarPubMed
Chamruspollert, M, Pesti, GM&Bakalli, RIThe influence of labile dietary methyl donors on the arginine requirement of young broiler chicks. Poult Sci 2002 81, 1142–1148.CrossRefGoogle ScholarPubMed
Coen, M, Lenz, EM, Nicholson, JK, Wilson, ID, Pognan, F&Lindon, JCAn integrated metabonomic investigation of acetaminophen toxicity in the mouse using NMR spectroscopy. Chem Res Toxicol 2003 16, 295–303.CrossRefGoogle ScholarPubMed
Craig, SBetaine in human nutrition. Am J Clin Nutr 2004 80, 539–549.CrossRefGoogle ScholarPubMed
Ebbels, T, Keun, H, Beckonert, O, Antti, H, Bollard, M, Holmes, E, Lindon, JC&Nicholson, JKToxicity classification frommetabonomic data using a density superposition approach:'CLOUDS'. Anal Chim Acta 2003 490, 109–122.CrossRefGoogle Scholar
Frontiera, MS, Stabler, SP, Kolhouse, JF&Allen, RHRegulation of methionine metabolism: effects of nitrous oxide and excess dietary methionine. J Nutr Biochem 1994 5, 28–38.CrossRefGoogle Scholar
Fung, TT, Hu, FB, Pereira, MA, Liu, S, Stampfer, MJ, Colditz, GA&Willett, WCWhole-grain intake and the risk of type 2 diabetes: a prospective study in men. Am J Clin Nutr 2002 76, 535–540.CrossRefGoogle ScholarPubMed
Ghyczy, M&Boros, MElectrophilic methyl groups present in the diet ameliorate pathological states induced by reductive and oxidative stress: a hypothesis. Br J Nutr 2001 85, 409–414.CrossRefGoogle ScholarPubMed
Griffin, JL, Anthony, DC, Campbell, SJ, Gauldie, J, Pitossi, F, Styles, P&Sibson, NRStudy of cytokine induced neuropathology by high resolution proton NMR spectroscopy of rat urine. FEBS Lett 2004 568, 49–54.CrossRefGoogle ScholarPubMed
Holmes, E, Nicholls, AW, Lindon, JC, et al.. Development of a model for classification of toxin-induced lesions using 1H NMR spectroscopy of urine combined with pattern recognition. NMR Biomed 1998 11, 235–244.3.0.CO;2-V>CrossRefGoogle Scholar
James, SJ, Cutler, P, Melnyk, S, Jernigan, S, Janak, L, Gaylor, DW&Neubrander, JAMetabolic biomarkers of increased oxidative stress and impaired methylation capacity in children with autism. Am J Clin Nutr 2004 80, 1611–1617.CrossRefGoogle ScholarPubMed
Kamal-Eldin, A, Pouru, A, Eliasson, C&Åman, PAlkylresorcinols as antioxidants: hydrogen donation and peroxyl radicalscavenging effects. J Sci Food Agric 2000 81, 353–356.3.0.CO;2-X>CrossRefGoogle Scholar
Keshavarz, K&Fuller, HIRelationship of arginine and methionine in the nutrition of the chick and the significance of creatine biosynthesis in their interaction. J Nutr 1971 101, 217–222.CrossRefGoogle ScholarPubMed
Keun, HC, Ebbels, TMD, Antti, H, et al.. Analytical reproducibility in 1H NMR-based metabonomic urinalysis. Chem Res Toxicol 2002 15, 1380–1386.CrossRefGoogle ScholarPubMed
Kim, SK, Choi, KH&Kim, YCEffect of acute betaine administration on hepatic metabolism of S-amino acids in rats and mice. Biochem Pharmacol 2003 65, 1565–1574.CrossRefGoogle ScholarPubMed
Lenz, EM, Wilson, ID, Timbrell, JA&Nicholson, JKA 1H NMR spectroscopic study of the biochemical effects of ifosfamide in the rat: evaluation of potential biomarkers. Biomarkers 2000 5, 424–435.Google Scholar
Levi, F, Pasche, C, Lucchini, F, Chatenoud, L, Jacobs, DR Jr&La Vecchia, CRefined and whole grain cereals and the risk of oral, oesophageal and laryngeal cancer. Eur J Clin Nutr 2000 54, 487–489.CrossRefGoogle ScholarPubMed
Lindon, JC, Nicholson, JK&Everett, JRNMR spectroscopy of biofluids. Ann Rep NMR Spectrom 1999 38, 1–88.CrossRefGoogle Scholar
Linko, AM, Ross, AB, Kamal-Eldin, A, Serena, A, Kjar, AKB, Jørgensen, H, Peñalvo, JL, Adlercreutz, H, Åman, P&Back Knudsen, KEKinetics of the appearance of cereal alkylresorcinols in pig plasma. Br J Nutr 2006 95, 282–287.CrossRefGoogle ScholarPubMed
McGregor, DO, Dellow, WJ, Robson, RA, Lever, M, George, PM&Chambers, STBetaine supplementation decreases postmethionine hyperhomocysteinemia in chronic renal failure. Kidney Int 2002 61, 1040–1046.CrossRefGoogle ScholarPubMed
McKeown, NM, Meigs, JB, Liu, S, Wilson, PW&Jacques, PFWhole-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 2002 76, 390–398.CrossRefGoogle ScholarPubMed
Martens, H&Dardenne, PValidation and verification of regression in small data sets. Chemometrics Intell Lab Syst 1998 44, 99–121.CrossRefGoogle Scholar
Matthews, JO, Southern, LL, Higbie, AD, Persica, MA&Bidner, TDEffects of betaine on growth, carcass characteristics, pork quality, and plasma metabolites of finishing pigs. J Anim Sci 2001 79, 722–728.CrossRefGoogle ScholarPubMed
Miller, ER&Ullrey, DEThe pig as a model for human nutrition. Annu Rev Nutr 1987 7, 361–382.CrossRefGoogle Scholar
Nicholson, JK, Buckingham, MJ&Sadler, PJHigh resolution 1H n.m.r. studies of vertebrate blood and plasma. Biochem J 1983 211, 605–615.CrossRefGoogle ScholarPubMed
Nicholson, JK&Wilson, IDHigh resolution proton nuclear magnetic resonance spectroscopy of biological fluids. Progr NMR Spectrom 1989 21, 449–501.CrossRefGoogle Scholar
Olthof, MR, van Vliet, T, Boelsma, E&Verhoef, PLow dose betaine supplementation leads to immediate and long term lowering of plasma homocysteine in healthy men and women. J Nutr 2003 133, 4135–4138.CrossRefGoogle ScholarPubMed
Ozturk, F, Ucar, M, Ozturk, IC, Vardi, N&Batcioglu, KCarbon tetrachloride-induced nephrotoxicity and protective effect of betaine in Sprague-Dawley rats. Urology 2003 62, 353–356.CrossRefGoogle ScholarPubMed
Pereira, MA, Jacobs, DR, Pins, JJ Jr, Raatz, SK, Gross, MD, Slavin, JL&Seaquist, EREffect of whole grains on insulin sensitivity in overweight hyperinsulinemic adults. Am J Clin Nutr 2002 75, 848–855.CrossRefGoogle ScholarPubMed
Saarinen, MT, Kettunen, H, Pulliainen, K, Peuranen, S, Tiihonen, K&Remus, JA novel method to analyze betaine in chicken liver: effect of dietary betaine and choline supplementation on the hepatic betaine concentration in broiler chicks. J Agric Food Chem 2001 49, 559–563.CrossRefGoogle ScholarPubMed
Schwab, U, TÖrrÖnen, A, Toppinen, L, Alfthan, G, Saarinen, M&Aro, A, Uusitupa, MBetaine supplementation decreases plasma homocysteine concentrations but does not affect body weight, body composition, or resting energy expenditure in human subjects. Am J Clin Nutr 2002 76, 961–967.CrossRefGoogle ScholarPubMed
Schwahn, BC, Hafner, D, Hohlfeld, T, Balkenhol, N, Laryea, MD&Wendel, UPharmacokinetics of oral betaine in healthy subjects and patients with homocystinuria. Br J Clin Pharmacol 2003 55, 6–13.CrossRefGoogle ScholarPubMed
Slavin, JL, Jacobs, D, Marquart, L&Wiemer, KThe role of whole grains in disease prevention. J Am Diet Assoc 2001 101, 780–785.CrossRefGoogle ScholarPubMed
Slavin, JL, Martini, M, Jacobs, DR Jr&Marquart, LPlausible mechanisms for the protectiveness of whole grains. Am J Clin Nutr 1999 70, 459S–486S.CrossRefGoogle ScholarPubMed
Slow, S, Lever, M, Lee, MB, George, PM&Chambers, STBetaine analogues alter homocysteine metabolism in rats. Int J Biochem Cell Biol 2004 36, 870–880.CrossRefGoogle ScholarPubMed
Solanky, KS, Bailey, NJC, Beckwith-Hall, BM, Davis, A, Bingham, S, Holmes, E, Nicholson, JK&Cassidy, AApplication ofbiofluid 1H nuclear magnetic resonance-based metabonomic techniques for the analysis of the biochemical effects of dietary isoflavones on human plasma profile. Anal Biochem 2003b 323, 197–204.CrossRefGoogle ScholarPubMed
Solanky, KS, Bailey, NJC, Holmes, E, Lindon, JC, Davis, AL, Mulder, TPJ, Van Duynhoven, JPM, Nicholson, JKNMR-based metabonomic studies on the biochemical effects of epicatechin in the rat. J Agric Food Chem 2003a 51, 4139–4145.CrossRefGoogle ScholarPubMed
Steenge, GR, Verhoef, P, Katan, MBBetaine supplementation lowers plasma homocysteine in healthy men and women. J Nutr 2003 133, 1291–1295.CrossRefGoogle ScholarPubMed
Truswell, ASCereal grains and coronary heart disease. Eur J Clin Nutr 2002 56, 1–14.CrossRefGoogle ScholarPubMed
Waters, NJ, Holmes, E, Williams, A, Waterfield, CJ, Farrant, RD&Nicholson, JKNMR and pattern recognition studies on the time-related metabolic effects of a-naphthylisothiocyanate on liver, urine, and plasma in the rat: an integrative metabonomic approach. Chem Res Toxicol 2001 14, 1401–1412.CrossRefGoogle Scholar
Wray-Cahen, D, Fernández-Fígares, I, Virtanen, E, Steele, N, Caperna, TJBetaine improves growth, but does not induce whole body or hepatic oxidation in swine (Sus scrofa domestica). Comp Biochem Physiol A Mol Integr Physiol 2004 137, 131–140.CrossRefGoogle ScholarPubMed