The metabolic signature associated with the Western dietary pattern: a cross-sectional study

Annie Bouchard-Mercier, Iwona Rudkowska, Simone Lemieux, Patrick Couture, Marie-Claude Vohl, Annie Bouchard-Mercier, Iwona Rudkowska, Simone Lemieux, Patrick Couture, Marie-Claude Vohl

Abstract

Background: Metabolic profiles have been shown to be associated to obesity status and insulin sensitivity. Dietary intakes influence metabolic pathways and therefore, different dietary patterns may relate to modifications in metabolic signatures. The objective was to verify associations between dietary patterns and metabolic profiles composed of amino acids (AAs) and acylcarnitines (ACs).

Methods: 210 participants were recruited in the greater Quebec City area between September 2009 and December 2011. Dietary patterns had been previously derived using principal component analysis (PCA). The Prudent dietary pattern was characterised by higher intakes of vegetables, fruits, whole grain products, non-hydrogenated fat and lower intakes of refined grain products, whereas the Western dietary pattern was associated with higher intakes of refined grain products, desserts, sweets and processed meats. Targeted metabolites were quantified in 37 participants with the Biocrates Absolute IDQ p150 (Biocrates Life Sciences AG, Austria) mass spectrometry method (including 14 amino acids and 41 acylcarnitines).

Results: PCA analysis with metabolites including AAs and ACs revealed two main components explaining the most variance in overall data (13.8%). PC1 was composed mostly of medium- to long-chain ACs (C16:2, C14:2, C14:2-OH, C16, C14:1-OH, C14:1, C10:2, C5-DC/C6-OH, C12, C18:2, C10, C4:1-DC/C6, C8:1 and C2) whereas PC2 included certain AAs and short-chain ACs (xLeu, Met, Arg, Phe, Pro, Orn, His, C0, C3, C4 and C5). The Western dietary pattern correlated negatively with PC1 and positively with PC2 (r = -0.34, p = 0.05 and r = 0.38, p = 0.03, respectively), independently of age, sex and BMI.

Conclusion: These findings suggest that the Western dietary pattern is associated with a specific metabolite signature characterized by increased levels of AAs including branched-chain AAs (BCAAs) and short-chain ACs.

Trial registration: ClinicalTrials.gov NCT01343342.

Figures

Figure 1
Figure 1
ACs and AAs associated with PC1 and PC2. Metabolites with absolute factor loadings ≥ 0.50 were regarded as significant contributors to the PC. The blue line and squares represent PC1 and the red line and squares represent PC2.
Figure 2
Figure 2
PC2 scores according to tertiles of saturated fat intake. PC2 scores and tertile of saturated fat intake (means ± SE). Means with different letters are significantly different. Means of saturated fat intake according to tertiles: tertile 1 (4.72-10.13%, n = 12), tertile 2 (10.29-11.30%, n = 13) and tertile 3 (11.51-14.72%, n = 12). Tertile 1 versus tertile 3: p = 0.005. Tertile 1 versus tertile 2: p = 0.40. Tertile 2 versus tertile 3: p = 0.05.

References

    1. Newby PK, Tucker KL. Empirically derived eating patterns using factor or cluster analysis: a review. Nutr Rev. 2004;62:177–203. doi: 10.1111/j.1753-4887.2004.tb00040.x.
    1. Bhupathiraju SN, Tucker KL. Coronary heart disease prevention: nutrients, foods, and dietary patterns. Clin Chim Acta. 2011;412:1493–1514. doi: 10.1016/j.cca.2011.04.038.
    1. Yusof AS, Isa ZM, Shah SA. Dietary patterns and risk of colorectal cancer: a systematic review of cohort studies (2000–2011) Asian Pac J Cancer Prev. 2012;13:4713–4717. doi: 10.7314/APJCP.2012.13.9.4713.
    1. Esmaillzadeh A, Kimiagar M, Mehrabi Y, Azadbakht L, Hu FB, Willett WC. Dietary patterns, insulin resistance, and prevalence of the metabolic syndrome in women. Am J Clin Nutr. 2007;85:910–918.
    1. Schulze MB, Hoffmann K, Manson JE, Willett WC, Meigs JB, Weikert C. et al.Dietary pattern, inflammation, and incidence of type 2 diabetes in women. Am J Clin Nutr. 2005;82:675–684.
    1. Heidemann C, Hoffmann K, Spranger J, Klipstein-Grobusch K, Mohlig M, Pfeiffer AF. et al.A dietary pattern protective against type 2 diabetes in the European Prospective Investigation into Cancer and Nutrition (EPIC)–Potsdam Study cohort. Diabetologia. 2005;48:1126–1134. doi: 10.1007/s00125-005-1743-1.
    1. Esposito K, Kastorini CM, Panagiotakos DB, Giugliano D. Prevention of type 2 diabetes by dietary patterns: a systematic review of prospective studies and meta-analysis. Metab Syndr Relat Disord. 2010;8:471–476. doi: 10.1089/met.2010.0009.
    1. Janssen I. The public health burden of obesity in Canada. Can J Diabetes. 2013;37:90–96. doi: 10.1016/j.jcjd.2013.02.059.
    1. Abbasi F, Brown BW Jr, Lamendola C, McLaughlin T, Reaven GM. Relationship between obesity, insulin resistance, and coronary heart disease risk. J Am Coll Cardiol. 2002;40:937–943. doi: 10.1016/S0735-1097(02)02051-X.
    1. Ceglarek U, Leichtle A, Brugel M, Kortz L, Brauer R, Bresler K. et al.Challenges and developments in tandem mass spectrometry based clinical metabolomics. Mol Cell Endocrinol. 2009;301:266–271. doi: 10.1016/j.mce.2008.10.013.
    1. Laferrere B, Reilly D, Arias S, Swerdlow N, Gorroochurn P, Bawa B. et al.Differential metabolic impact of gastric bypass surgery versus dietary intervention in obese diabetic subjects despite identical weight loss. Sci Transl Med. 2011;3:80re2.
    1. Newgard CB, An J, Bain JR, Muehlbauer MJ, Stevens RD, Lien LF. 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. doi: 10.1016/j.cmet.2009.02.002.
    1. Tai ES, Tan ML, Stevens RD, Low YL, Muehlbauer MJ, Goh DL. et al.Insulin resistance is associated with a metabolic profile of altered protein metabolism in Chinese and Asian-Indian men. Diabetologia. 2010;53:757–767. doi: 10.1007/s00125-009-1637-8.
    1. Newgard CB. Interplay between lipids and branched-chain amino acids in development of insulin resistance. Cell Metab. 2012;15:606–614. doi: 10.1016/j.cmet.2012.01.024.
    1. Xu J, Yang S, Cai S, Dong J, Li X, Chen Z. Identification of biochemical changes in lactovegetarian urine using 1H NMR spectroscopy and pattern recognition. Anal Bioanal Chem. 2010;396:1451–1463. doi: 10.1007/s00216-009-3338-z.
    1. May DH, Navarro SL, Ruczinski I, Hogan J, Ogata Y, Schwarz Y. et al.Metabolomic profiling of urine: response to a randomised, controlled feeding study of select fruits and vegetables, and application to an observational study. Br J Nutr. 2013;110:1760–1770. doi: 10.1017/S000711451300127X.
    1. Menni C, Zhai G, Macgregor A, Prehn C, Romisch-Margl W, Suhre K. et al.Targeted metabolomics profiles are strongly correlated with nutritional patterns in women. Metabolomics. 2013;9:506–514. doi: 10.1007/s11306-012-0469-6.
    1. 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;93:314–321. doi: 10.3945/ajcn.110.000950.
    1. Rudkowska I, Paradis AM, Thifault E, Julien P, Tchernof A, Couture P. et al.Transcriptomic and metabolomic signatures of an n-3 polyunsaturated fatty acids supplementation in a normolipidemic/normocholesterolemic Caucasian population. J Nutr Biochem. 2012;24:54–61.
    1. Bouchard-Mercier A, Paradis AM, Rudkowska I, Lemieux S, Couture P, Vohl MC. Associations between dietary patterns and gene expression profiles of healthy men and women: a cross-sectional study. Nutr J. 2013;12:24. doi: 10.1186/1475-2891-12-24.
    1. Goulet J, Nadeau G, Lapointe A, Lamarche B, Lemieux S. Validity and reproducibility of an interviewer-administered food frequency questionnaire for healthy French-Canadian men and women. Nutr J. 2004;3:13. doi: 10.1186/1475-2891-3-13.
    1. Paradis AM, Godin G, Perusse L, Vohl MC. Associations between dietary patterns and obesity phenotypes. Int J Obes (Lond) 2009;33:1419–1426. doi: 10.1038/ijo.2009.179.
    1. Hu FB, Rimm E, Smith-Warner SA, Feskanich D, Stampfer MJ, Ascherio A. et al.Reproducibility and validity of dietary patterns assessed with a food-frequency questionnaire. Am J Clin Nutr. 1999;69:243–249.
    1. Sherzai A, Heim LT, Boothby C, Sherzai AD. Stroke, food groups, and dietary patterns: a systematic review. Nutr Rev. 2012;70:423–435. doi: 10.1111/j.1753-4887.2012.00490.x.
    1. Alhazmi A, Stojanovski E, McEvoy M, Garg ML. The association between dietary patterns and type 2 diabetes: a systematic review and meta-analysis of cohort studies. J Hum Nutr Diet. 2013. Epub ahead of print.
    1. Wang TJ, Larson MG, Vasan RS, Cheng S, Rhee EP, McCabe E. et al.Metabolite profiles and the risk of developing diabetes. Nat Med. 2011;17:448–453. doi: 10.1038/nm.2307.
    1. Lackey DE, Lynch CJ, Olson KC, Mostaedi R, Ali M, Smith WH. et al.Regulation of adipose branched-chain amino acid catabolism enzyme expression and cross-adipose amino acid flux in human obesity. Am J Physiol Endocrinol Metab. 2013;304:E1175–E1187. doi: 10.1152/ajpendo.00630.2012.
    1. Xu HE, Lambert MH, Montana VG, Parks DJ, Blanchard SG, Brown PJ. et al.Molecular recognition of fatty acids by peroxisome proliferator-activated receptors. Mol Cell. 1999;3:397–403. doi: 10.1016/S1097-2765(00)80467-0.
    1. Coll T, Eyre E, Rodriguez-Calvo R, Palomer X, Sanchez RM, Merlos M. et al.Oleate reverses palmitate-induced insulin resistance and inflammation in skeletal muscle cells. J Biol Chem. 2008;283:11107–11116. doi: 10.1074/jbc.M708700200.
    1. Stephenson EJ, Camera DM, Jenkins TA, Kosari S, Lee JS, Hawley JA. et al.Skeletal muscle respiratory capacity is enhanced in rats consuming an obesogenic Western diet. Am J Physiol Endocrinol Metab. 2012;302:E1541–E1549. doi: 10.1152/ajpendo.00590.2011.
    1. Pranprawit A, Wolber FM, Heyes JA, Molan AL, Kruger MC. Short-term and long-term effects of excessive consumption of saturated fats and/or sucrose on metabolic variables in Sprague Dawley rats: a pilot study. J Sci Food Agric. 2013;93:3191–3197. doi: 10.1002/jsfa.6240.

Source: PubMed

3
Prenumerera