Abstract
The application of metabolomics in nutritional research may be a useful tool to analyse and predict the response to a dietary intervention. The aim of this study was to examine metabolic changes in serum samples following exposure to an energy-restricted diet (−15 % of daily energy requirements) over a period of 8 weeks in overweight and obese older adults (n = 22) using a gas chromatography/mass spectrometry (GC/MS) metabolomic approach. After 8 weeks, there were significant reductions in weight (7 %) and metabolic improvement (glucose and lipid profiles). Metabolomic analysis found that total saturated fatty acids (SFAs), including palmitic acid (C16:0) and stearic acid (C18:0) and monounsaturated fatty acids (MUFAs), were significantly decreased after the 8-week intervention. Furthermore, palmitoleic acid (C16:1) was found to be a negative predictor of change in body fat loss. Both the total ω-6 and ω-3 polyunsaturated fatty acids (PUFAs) significantly decreased, although the overall total amounts of PUFAs did not. The branched chain amino acid (BCAA) isoleucine significantly decreased in the serum samples after the intervention. In conclusion, this study demonstrated that the weight loss intervention based on a hypocaloric diet identified changes in the metabolic profiles of serum in overweight and obese older adults, with a reduction in anthropometric and biochemical parameters also found.
Similar content being viewed by others
References
Attie AD, Krauss RM, Gray-Keller MP, Brownlie A, Miyazaki M, Kastelein JJ, Lusis AJ, Stalenhoef AF, Stoehr JP, Hayden MR et al (2002) Relationship between stearoyl-CoA desaturase activity and plasma triglycerides in human and mouse hypertriglyceridemia. J Lipid Res 43:1899–1907
Bjermo H, Riserus U (2010) Role of hepatic desaturases in obesity-related metabolic disorders. Curr Opin Clin Nutr Metab Care 13:703–708
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917
Brennan L (2013) Metabolomics in nutrition research: current status and perspectives. Biochem Soc Trans 41:670–673
Bruss MD, Khambatta CF, Ruby MA, Aggarwal I, Hellerstein MK (2010) Calorie restriction increases fatty acid synthesis and whole body fat oxidation rates. Am J Physiol Endocrinol Metab 298:E108–E116
Cao H, Gerhold K, Mayers JR, Wiest MM, Watkins SM, Hotamisligil GS (2008) Identification of a lipokine, a lipid hormone linking adipose tissue to systemic metabolism. Cell 134:933–944
Chen YJ, Chen CC, Li TK, Wang PH, Liu LR, Chang FY, Wang YC, Yu YH, Lin SP, Mersmann HJ et al (2012) Docosahexaenoic acid suppresses the expression of FoxO and its target genes. J Nutr Biochem 23:1609–1616
Chen SC, Lin YH, Huang HP, Hsu WL, Houng JY, Huang CK (2012) Effect of conjugated linoleic acid supplementation on weight loss and body fat composition in a Chinese population. Nutrition 28:559–565
Chong MF, Hodson L, Bickerton AS, Roberts R, Neville M, Karpe F, Frayn KN, Fielding BA (2008) Parallel activation of de novo lipogenesis and stearoyl-CoA desaturase activity after 3 d of high-carbohydrate feeding. Am J Clin Nutr 87:817–823
Chopra M, Galbraith S, Darnton-Hill I (2002) A global response to a global problem: the epidemic of overnutrition. Bull World Health Organ 80:952–958
Du Y, Meng Q, Zhang Q, Guo F (2012) Isoleucine or valine deprivation stimulates fat loss via increasing energy expenditure and regulating lipid metabolism in WAT. Amino Acids 43:725–734
Etxeberria U, de la Garza AL, Martinez JA, Milagro FI (2013) Diet-induced hyperinsulinemia differentially affects glucose and protein metabolism: a high-throughput metabolomic approach in rats. J Physiol Biochem 69:613–623
Flock MR, Kris-Etherton PM (2013) Diverse physiological effects of long-chain saturated fatty acids: implications for cardiovascular disease. Curr Opin Clin Nutr Metab Care 16:133–140
Friedewald WT, Levy RI, Fredrickson DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18:499–502
Gibney MJ, Walsh M, Brennan L, Roche HM, German B, van Ommen B (2005) Metabolomics in human nutrition: opportunities and challenges. Am J Clin Nutr 82:497–503
Gong J, Campos H, McGarvey S, Wu Z, Goldberg R, Baylin A (2011) Adipose tissue palmitoleic acid and obesity in humans: does it behave as a lipokine? Am J Clin Nutr 93:186–191
Guo X, Li H, Xu H, Halim V, Zhang W, Wang H, Ong KT, Woo SL, Walzem RL, Mashek DG et al (2012) Palmitoleate induces hepatic steatosis but suppresses liver inflammatory response in mice. PLoS One 7:e39286
Hudgins LC, Hellerstein MK, Seidman CE, Neese RA, Tremaroli JD, Hirsch J (2000) Relationship between carbohydrate-induced hypertriglyceridemia and fatty acid synthesis in lean and obese subjects. J Lipid Res 41:595–604
Iggman D, Arnlov J, Vessby B, Cederholm T, Sjogren P, Riserus U (2010) Adipose tissue fatty acids and insulin sensitivity in elderly men. Diabetologia 53:850–857
Jakobsen MU, O’Reilly EJ, Heitmann BL, Pereira MA, Balter K, Fraser GE, Goldbourt U, Hallmans G, Knekt P, Liu S et al (2009) Major types of dietary fat and risk of coronary heart disease: a pooled analysis of 11 cohort studies. Am J Clin Nutr 89:1425–1432
Jiye A, Huang Q, Wang G, Zha W, Yan B, Ren H, Gu S, Zhang Y, Zhang Q, Shao F et al (2008) Global analysis of metabolites in rat and human urine based on gas chromatography/time-of-flight mass spectrometry. Anal Biochem 379:20–26
Kien CL, Bunn JY, Poynter ME, Stevens R, Bain J, Ikayeva O, Fukagawa NK, Champagne CM, Crain KI, Koves TR et al (2013) A lipidomics analysis of the relationship between dietary fatty acid composition and insulin sensitivity in young adults. Diabetes 62:1054–1063
Kroger J, Schulze MB (2012) Recent insights into the relation of Δ5 desaturase and Δ6 desaturase activity to the development of type 2 diabetes. Curr Opin Lipidol 23:4–10
Kurotani K, Sato M, Ejima Y, Nanri A, Yi S, Pham NM, Akter S, Poudel-Tandukar K, Kimura Y, Imaizumi K et al (2012) High levels of stearic acid, palmitoleic acid, and dihomo-gamma-linolenic acid and low levels of linoleic acid in serum cholesterol ester are associated with high insulin resistance. Nutr Res 32(669–675):e663
Labayen I, Diez N, Parra MD, Gonzalez A, Martinez JA (2004) Time-course changes in macronutrient metabolism induced by a nutritionally balanced low-calorie diet in obese women. Int J Food Sci Nutr 55:27–35
Laferrere B, Reilly D, Arias S, Swerdlow N, Gorroochurn P, Bawa B, Bose M, Teixeira J, Stevens RD, Wenner BR et al (2011) Differential metabolic impact of gastric bypass surgery versus dietary intervention in obese diabetic subjects despite identical weight loss. Sci Transl Med 3:80re82
Leidy HJ, Carnell NS, Mattes RD, Campbell WW (2007) Higher protein intake preserves lean mass and satiety with weight loss in pre-obese and obese women. Obesity (Silver Spring) 15:421–429
Lien LF, Haqq AM, Arlotto M, Slentz CA, Muehlbauer MJ, McMahon RL, Rochon J, Gallup D, Bain JR, Ilkayeva O et al (2009) The STEDMAN project: biophysical, biochemical and metabolic effects of a behavioral weight loss intervention during weight loss, maintenance, and regain. Omics 13:21–35
Lopez-Alvarenga JC, Ebbesson SO, Ebbesson LO, Tejero ME, Voruganti VS, Comuzzie AG (2010) Polyunsaturated fatty acids effect on serum triglycerides concentration in the presence of metabolic syndrome components. The Alaska–Siberia Project. Metabolism 59:86–92
Lorente-Cebrian S, Costa AG, Navas-Carretero S, Zabala M, Martinez JA, Moreno-Aliaga MJ (2013) Role of omega-3 fatty acids in obesity, metabolic syndrome, and cardiovascular diseases: a review of the evidence. J Physiol Biochem
Magkos F, Bradley D, Schweitzer GG, Finck BN, Eagon JC, Ilkayeva O, Newgard CB, Klein S (2013) Effect of roux-en-Y gastric bypass and laparoscopic adjustable gastric banding on branched-chain amino acid metabolism. Diabetes 62:2757–2761
Marques-Lopes I, Ansorena D, Astiasaran I, Forga L, Martinez JA (2001) Postprandial de novo lipogenesis and metabolic changes induced by a high-carbohydrate, low-fat meal in lean and overweight men. Am J Clin Nutr 73:253–261
Mathus-Vliegen EM (2012) Prevalence, pathophysiology, health consequences and treatment options of obesity in the elderly: a guideline. Obes Facts 5:460–483
Morris C, Grada CO, Ryan M, Roche HM, De Vito G, Gibney MJ, Gibney ER, Brennan L (2013) The relationship between aerobic fitness level and metabolic profiles in healthy adults. Mol Nutr Food Res 57:1246–1254
Morris C, O’Grada C, Ryan M, Roche HM, Gibney MJ, Gibney ER, Brennan L (2012) The relationship between BMI and metabolomic profiles: a focus on amino acids. Proc Nutr Soc 71:634–638
Moussavi N, Gavino V, Receveur O (2008) Could the quality of dietary fat, and not just its quantity, be related to risk of obesity? Obesity (Silver Spring) 16:7–15
Muhlhausler BS, Ailhaud GP (2013) Omega-6 polyunsaturated fatty acids and the early origins of obesity. Curr Opin Endocrinol Diabetes Obes 20:56–61
Munro IA, Garg ML (2012) Dietary supplementation with n-3 PUFA does not promote weight loss when combined with a very-low-energy diet. Br J Nutr 108:1466–1474
Newgard CB, An J, Bain JR, Muehlbauer MJ, Stevens RD, Lien LF, Haqq AM, Shah SH, Arlotto M, Slentz CA et al (2009) A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metab 9:311–326
Newman AB, Lee JS, Visser M, Goodpaster BH, Kritchevsky SB, Tylavsky FA, Nevitt M, Harris TB (2005) Weight change and the conservation of lean mass in old age: the Health, Aging and Body Composition Study. Am J Clin Nutr 82:872–878, quiz 915-876
Ni Raghallaigh S, Bender K, Lacey N, Brennan L, Powell FC (2012) The fatty acid profile of the skin surface lipid layer in papulopustular rosacea. Br J Dermatol 166:279–287
Norli HR, Christiansen A, Holen B (2010) Independent evaluation of a commercial deconvolution reporting software for gas chromatography mass spectrometry analysis of pesticide residues in fruits and vegetables. J Chromatogr A 1217:2056–2064
Ntambi JM, Miyazaki M (2004) Regulation of stearoyl-CoA desaturases and role in metabolism. Prog Lipid Res 43:91–104
Paillard F, Catheline D, Duff FL, Bouriel M, Deugnier Y, Pouchard M, Daubert JC, Legrand P (2008) Plasma palmitoleic acid, a product of stearoyl-CoA desaturase activity, is an independent marker of triglyceridemia and abdominal adiposity. Nutr Metab Cardiovasc Dis 18:436–440
Pan DA, Lillioja S, Milner MR, Kriketos AD, Baur LA, Bogardus C, Storlien LH (1995) Skeletal muscle membrane lipid composition is related to adiposity and insulin action. J Clin Invest 96:2802–2808
Rezzi S, Ramadan Z, Fay LB, Kochhar S (2007) Nutritional metabonomics: applications and perspectives. J Proteome Res 6:513–525
Ryan M, McInerney D, Owens D, Collins P, Johnson A, Tomkin GH (2000) Diabetes and the Mediterranean diet: a beneficial effect of oleic acid on insulin sensitivity, adipocyte glucose transport and endothelium-dependent vasoreactivity. Qjm 93:85–91
Santanasto AJ, Glynn NW, Newman MA, Taylor CA, Brooks MM, Goodpaster BH, Newman AB (2011) Impact of weight loss on physical function with changes in strength, muscle mass, and muscle fat infiltration in overweight to moderately obese older adults: a randomized clinical trial. J Obes 2011
Shah SH, Crosslin DR, Haynes CS, Nelson S, Turer CB, Stevens RD, Muehlbauer MJ, Wenner BR, Bain JR, Laferrere B et al (2012) Branched-chain amino acid levels are associated with improvement in insulin resistance with weight loss. Diabetologia 55:321–330
Smilowitz JT, Wiest MM, Watkins SM, Teegarden D, Zemel MB, German JB, Van Loan MD (2009) Lipid metabolism predicts changes in body composition during energy restriction in overweight humans. J Nutr 139:222–229
Sumner LW, Mendes P, Dixon RA (2003) Plant metabolomics: large-scale phytochemistry in the functional genomics era. Phytochemistry 62:817–836
van Dijk SJ, Feskens EJ, Bos MB, Hoelen DW, Heijligenberg R, Bromhaar MG, de Groot LC, de Vries JH, Muller M, Afman LA (2009) A saturated fatty acid-rich diet induces an obesity-linked proinflammatory gene expression profile in adipose tissue of subjects at risk of metabolic syndrome. Am J Clin Nutr 90:1656–1664
Van Gaal LF, Mertens IL, De Block CE (2006) Mechanisms linking obesity with cardiovascular disease. Nature 444:875–880
Walsh MC, Brennan L, Malthouse JP, Roche HM, Gibney MJ (2006) Effect of acute dietary standardization on the urinary, plasma, and salivary metabolomic profiles of healthy humans. Am J Clin Nutr 84:531–539
Warensjo E, Ohrvall M, Vessby B (2006) Fatty acid composition and estimated desaturase activities are associated with obesity and lifestyle variables in men and women. Nutr Metab Cardiovasc Dis 16:128–136
Warensjo E, Riserus U, Vessby B (2005) Fatty acid composition of serum lipids predicts the development of the metabolic syndrome in men. Diabetologia 48:1999–2005
Weckwerth W, Morgenthal K (2005) Metabolomics: from pattern recognition to biological interpretation. Drug Discov Today 10:1551–1558
Witham MD, Avenell A (2010) Interventions to achieve long-term weight loss in obese older people: a systematic review and meta-analysis. Age Ageing 39:176–184
Xie B, Waters MJ, Schirra HJ (2012) Investigating potential mechanisms of obesity by metabolomics. J Biomed Biotechnol 2012:805683
Zong G, Ye X, Sun L, Li H, Yu Z, Hu FB, Sun Q, Lin X (2012) Associations of erythrocyte palmitoleic acid with adipokines, inflammatory markers, and the metabolic syndrome in middle-aged and older Chinese. Am J Clin Nutr 96:970–976
Acknowledgments
The authors wish to thank the volunteers for their participation in the study and the physician Blanca E. Martínez de Morentín, the nurse Salomé Pérez, as well as the technician Verónica Ciaurriz for excellent technical assistance in the University of Navarra. We thank Ciara Morris and Martina Wallace from University College Dublin for their contribution to this study. Aurora Pérez-Cornago gratefully acknowledges the pre-doctoral research grant from the “Asociación de Amigos Universidad de Navarra”, as well as the mobility grant from the Spanish Government.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Perez-Cornago, A., Brennan, L., Ibero-Baraibar, I. et al. Metabolomics identifies changes in fatty acid and amino acid profiles in serum of overweight older adults following a weight loss intervention. J Physiol Biochem 70, 593–602 (2014). https://doi.org/10.1007/s13105-013-0311-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13105-013-0311-2