Abstract
We assessed the relationship between energy-adjusted amino acids (EAA) intakes and obesity risk using data on nutrient intakes derived from the Chinese food composition tables to determine dietary intakes (DI) among 1109 obese and 3009 normal weight subjects. Dietary patterns (DP) were identified using principal component analysis, multivariable-adjusted odds ratio (OR) and 95% confidence interval (CI) of obesity risk by quartiles of EAA intakes was estimated using logistic regression with two-sided P < 0.05. Multivariable-adjusted OR and 95% CI for obesity risk were 1.00, 0.801 (0.573, 1.119), 0.718 (0.504, 1.024) and 0.532 (0.353, 0.803) P-trend = 0.003 across energy-adjusted quartiles of total AA intakes. Similarly, higher DI of 13 AA; isoleucine, leucine, valine, lysine, cysteine, phenylalanine, tyrosine, threonine, histidine, aspartic acid, glutamic acid, proline, and serine were associated with lower risk of obesity. Furthermore, six DP; ‘Wheaten food and Rice’, ‘Fruit, Vegetables and Milk’, ‘Snack, Beverage and Ice cream’, ‘Potatoes, Soybean & Egg’, ‘Livestock & Poultry meat’ and ‘Fish’ were identified. Multivariable-adjusted OR and 95% CI across quartiles of DP adherence for obesity risk were 1.00, 0.737 (0.535, 1.017), 0.563 (0.406, 0.779), 0.724 (0.518, 1.011) P-trend = 0.018 for ‘Fruit, Vegetables and Milk’, 1.00, 0.734 (0.531, 1.013), 0.841(0.609, 1.161), 0.657 (0.478, 0.904) P-trend = 0.027 for ‘Potatoes, Soybean & Egg’ and 1.00, 1.106 (0.791, 1.548), 1.367(0.975, 1.917), 1.953 (1.399, 2.726) P-trend = 0.000 for ‘Fish’. Additionally, lower adherence to ‘Snack, Beverage and Ice cream’ and ‘Fish’ patterns is associated with a protective higher AA intake-obesity risk relationship. Energy-adjusted AA intakes were inversely associated with obesity risk, but the associations appear modifiable by DP adherence of respondents.
Similar content being viewed by others
References
Alberti KG, Zimmet P, Shaw J (2007) International Diabetes Federation: a consensus on Type 2 diabetes prevention. Diabet Med 24:451–463. https://doi.org/10.1111/j.1464-5491.2007.02157.x
Asghari G, Farhadnejad H, Teymoori F, Mirmiran P, Tohidi M, Azizi F (2017) High dietary intake of branched-chain amino acids is associated with an increased risk of insulin resistance in adults. J Diabet. https://doi.org/10.1111/1753-0407.12639
Bel-Serrat S et al (2014) The role of dietary fat on the association between dietary amino acids and serum lipid profile in European adolescents participating in the HELENA Study. Eur J Clin Nutr 68:464–473. https://doi.org/10.1038/ejcn.2013.284
Casperson SL, Sheffield-Moore M, Hewlings SJ, Paddon-Jones D (2012) Leucine supplementation chronically improves muscle protein synthesis in older adults consuming the RDA for protein. Clin Nutr 31:512–519. https://doi.org/10.1016/j.clnu.2012.01.005
Chaneton B et al (2012) Serine is a natural ligand and allosteric activator of pyruvate kinase M2. Nature 491:458–462. https://doi.org/10.1038/nature11540
Chartrand D, Da Silva MS, Julien P, Rudkowska I (2017) Influence of amino acids in dairy products on glucose homeostasis: the clinical evidence. Can J Diabet 41:329–337. https://doi.org/10.1016/j.jcjd.2016.10.009
Chen IF, Wu HJ, Chen CY, Chou KM, Chang CK (2016) Branched-chain amino acids, arginine, citrulline alleviate central fatigue after 3 simulated matches in taekwondo athletes: a randomized controlled trial. J Int Soc Sports Nutr 13:28. https://doi.org/10.1186/s12970-016-0140-0
Cogate PG, Natali AJ, de Oliveira A, Alfenas RC, Hermsdorff HH (2015) Consumption of Branched-Chain Amino Acids Is Inversely Associated with Central Obesity and Cardiometabolic Features in a Population of Brazilian Middle-Aged Men: potential Role of Leucine Intake. J Nutr Health Aging 19:771–777. https://doi.org/10.1007/s12603-015-0522-z
Devries MC, Phillips SM (2015) Supplemental protein in support of muscle mass and health: advantage whey. J Food Sci 80(Suppl 1):A8–A15. https://doi.org/10.1111/1750-3841.12802
Dudgeon WD, Kelley EP, Scheett TP (2016) In a single-blind, matched group design: branched-chain amino acid supplementation and resistance training maintains lean body mass during a caloric restricted diet. J Int Soc Sports Nutr 13:1. https://doi.org/10.1186/s12970-015-0112-9
Feng RN et al (2013) Histidine supplementation improves insulin resistance through suppressed inflammation in obese women with the metabolic syndrome: a randomised controlled trial. Diabetologia 56:985–994. https://doi.org/10.1007/s00125-013-2839-7
Gannon NP, Schnuck JK, Vaughan RA (2018) BCAA metabolism and insulin sensitivity—dysregulated by metabolic status? Molecular Nutr Food Res. https://doi.org/10.1002/mnfr.201700756
Gojda J et al (2017) Chronic dietary exposure to branched chain amino acids impairs glucose disposal in vegans but not in omnivores. Eur J Clin Nutr. https://doi.org/10.1038/ejcn.2016.274
Gracia-Marco L et al (2017) Amino acids intake and physical fitness among adolescents. Amino acids 49:1041–1052. https://doi.org/10.1007/s00726-017-2393-6
Isanejad M et al (2017) Branched-chain amino acid, meat intake and risk of type 2 diabetes in the Women’s Health Initiative. Br J Nutr 117:1523–1530. https://doi.org/10.1017/s0007114517001568
Ispoglou T, White H, Preston T, McElhone S, McKenna J, Hind K (2016) Double-blind, placebo-controlled pilot trial of l-Leucine-enriched amino-acid mixtures on body composition and physical performance in men and women aged 65–75 years. Eur J Clin Nutr 70:182–188. https://doi.org/10.1038/ejcn.2015.91
Jennings A, MacGregor A, Pallister T, Spector T, Cassidy A (2016) Associations between branched chain amino acid intake and biomarkers of adiposity and cardiometabolic health independent of genetic factors: a twin study. Int J Cardiol 223:992–998. https://doi.org/10.1016/j.ijcard.2016.08.307
Kasaoka S et al (2004) Histidine supplementation suppresses food intake and fat accumulation in rats. Nutrition 20:991–996. https://doi.org/10.1016/j.nut.2004.08.006
Lau DC, Douketis JD, Morrison KM, Hramiak IM, Sharma AM, Ur E, Obesity Canada Clinical Practice Guidelines Expert P (2007) 2006 Canadian clinical practice guidelines on the management and prevention of obesity in adults and children [summary]. CMAJ 176:S1–13. https://doi.org/10.1503/cmaj.061409
Li Y-C et al (2016a) Relationships of dietary histidine and obesity in Northern Chinese Adults, an internet-based cross-sectional study. Nutrients 8:420
Li YC et al (2015) The ratio of dietary branched-chain amino acids is associated with a lower prevalence of obesity in young Northern Chinese Adults: an internet-based cross-sectional study. Nutrients 7:9573–9589. https://doi.org/10.3390/nu7115486
Li J, Sun C, Liu S, Li Y (2016b) Dietary protein intake and type 2 diabetes among women and men in Northeast China. Sci Rep 6:37604. https://doi.org/10.1038/srep37604
Liu Z, Jeppesen PB, Gregersen S, Bach Larsen L, Hermansen K (2016) Chronic exposure to proline causes aminoacidotoxicity and impaired beta-cell function: studies in vitro. Rev Diabet Stud 13:66–78. https://doi.org/10.1900/RDS.2016.13.66
MacLean DA, Graham TE (1993) Branched-chain amino acid supplementation augments plasma ammonia responses during exercise in humans. J Appl Physiol (1985) 74:2711–2717
Maddocks ODK et al (2017) Modulating the therapeutic response of tumours to dietary serine and glycine starvation. Nature 544:372–376. https://doi.org/10.1038/nature22056
Markova M et al (2017) Isocaloric diets high in animal or plant protein reduce liver fat and inflammation in individuals with type 2 diabetes. Gastroenterology 152:571–585.e578. https://doi.org/10.1053/j.gastro.2016.10.007
Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419
Mikulski T, Dabrowski J, Hilgier W, Ziemba A, Krzeminski K (2015) Effects of supplementation with branched chain amino acids and ornithine aspartate on plasma ammonia and central fatigue during exercise in healthy men. Folia Neuropathol 53:377–386
Mirmiran P, Bahadoran Z, Esfandyari S, Azizi F (2017a) Dietary protein and amino acid profiles in relation to risk of dysglycemia: findings from a prospective population-based study. Nutrients 9:971
Mirmiran P, Bahadoran Z, Ghasemi A, Azizi F (2017b) Contribution of dietary amino acids composition to incidence of cardiovascular outcomes: a prospective population-based study. Nutr Metab Cardiovasc Dis 27:633–641. https://doi.org/10.1016/j.numecd.2017.05.003
Na L et al (2015a) A snack dietary pattern increases the risk of hypercholesterolemia in Northern Chinese adults: a prospective cohort study. PloS One 10:e0134294. https://doi.org/10.1371/journal.pone.0134294
Na L et al (2015b) The Harbin Cohort Study on diet, nutrition and chronic non-communicable diseases: study design and baseline characteristics. PloS One 10:e0122598. https://doi.org/10.1371/journal.pone.0122598
Nagata C, Nakamura K, Wada K, Tsuji M, Tamai Y, Kawachi T (2013) Branched-chain amino acid intake and the risk of diabetes in a Japanese community: the Takayama study. Am J Epidemiol 178:1226–1232. https://doi.org/10.1093/aje/kwt112
Newsholme P, Bender K, Kiely A, Brennan L (2007) Amino acid metabolism, insulin secretion and diabetes. Biochem Soc Trans 35:1180–1186. https://doi.org/10.1042/bst0351180
Nuttall FQ, Gannon MC, Jordan K (2004) The metabolic response to ingestion of proline with and without glucose. Metabolism 53:241–246. https://doi.org/10.1016/j.metabol.2003.09.013
Okekunle AP et al (2017) Abnormal circulating amino acid profiles in multiple metabolic disorders. Diabet Res Clin Pract 132:45–58. https://doi.org/10.1016/j.diabres.2017.07.023
Okekunle AP, Wu X, Duan W, Feng R, Li Y, Sun C (2018) Dietary intakes of branched-chained amino acid and risk of type 2 diabetes in adults: the Harbin Cohort Study on diet, nutrition and chronic non-communicablediseases study. Can J Diabet. https://doi.org/10.1016/j.jcjd.2017.12.003
Palmnäs MSA et al (2018) Serum metabolomics of activity energy expenditure and its relation to metabolic syndrome and obesity. Sci Rep 8:3308. https://doi.org/10.1038/s41598-018-21585-6
Piccolo BD, Comerford KB, Karakas SE, Knotts TA, Fiehn O, Adams SH (2015) Whey protein supplementation does not alter plasma branched-chained amino acid profiles but results in unique metabolomics patterns in obese women enrolled in an 8-week weight loss trial. J Nutr 145:691–700. https://doi.org/10.3945/jn.114.203943
Qin LQ et al (2011) Higher branched-chain amino acid intake is associated with a lower prevalence of being overweight or obese in middle-aged East Asian and Western adults. J Nutr 141:249–254. https://doi.org/10.3945/jn.110.128520
Schmidt DS, Salahudeen AK (2007) Obesity-survival paradox-still a controversy? Semin Dial 20:486–492. https://doi.org/10.1111/j.1525-139X.2007.00349.x
Shang X, Scott D, Hodge AM, English DR, Giles GG, Ebeling PR, Sanders KM (2016) Dietary protein intake and risk of type 2 diabetes: results from the Melbourne Collaborative Cohort Study and a meta-analysis of prospective studies. Am J Clin Nutr 104:1352–1365. https://doi.org/10.3945/ajcn.116.140954
Son DO, Satsu H, Shimizu M (2005) Histidine inhibits oxidative stress- and TNF-α-induced interleukin-8 secretion in intestinal epithelial cells. FEBS Letters 579:4671–4677. https://doi.org/10.1016/j.febslet.2005.07.038
Suenaga R et al (2008) Intracerebroventricular injection of l-arginine induces sedative and hypnotic effects under an acute stress in neonatal chicks. Amino Acids 35:139–146. https://doi.org/10.1007/s00726-007-0610-4
Sun X et al (2014) Histidine supplementation alleviates inflammation in the adipose tissue of high-fat diet-induced obese rats via the NF-κB- and PPARγ-involved pathways. Br J Nutr 112:477–485. https://doi.org/10.1017/S0007114514001056
Volek JS et al (2013) Whey protein supplementation during resistance training augments lean body mass. J Am Coll Nutr 32:122–135. https://doi.org/10.1080/07315724.2013.793580
Wang WW, Qiao SY, Li DF (2009) Amino acids and gut function. Amino Acids 37:105–110. https://doi.org/10.1007/s00726-008-0152-4
Willett W, Stampfer MJ (1986) Total energy intake: implications for epidemiologic analyses. Am J Epidemiol 124:17–27
Wu G (2009) Amino acids: metabolism, functions, and nutrition. Amino Acids 37:1–17. https://doi.org/10.1007/s00726-009-0269-0
Yang Y (2009) China food composition. Peking University Medical Press, Beijing
Yazdi FT, Clee SM, Meyre D (2015) Obesity genetics in mouse and human: back and forth, and back again. Peer J 3:e856. https://doi.org/10.7717/peerj.856
Ye J, Mancuso A, Tong X, Ward PS, Fan J, Rabinowitz JD, Thompson CB (2012) Pyruvate kinase M2 promotes de novo serine synthesis to sustain mTORC1 activity and cell proliferation. Proc Natl Acad Sci USA 109:6904–6909. https://doi.org/10.1073/pnas.1204176109
Zheng Y et al (2016) Cumulative consumption of branched-chain amino acids and incidence of type 2 diabetes. Int J Epidemiol. https://doi.org/10.1093/ije/dyw143
Zhou BF (2002) Effect of body mass index on all-cause mortality and incidence of cardiovascular diseases–report for meta-analysis of prospective studies open optimal cut-off points of body mass index in Chinese adults. Biomed Environ Sci 15:245–252
Acknowledgements
This work was supported by the National Key R&D Program of China (2017YFC1307401) and the National Natural Science Foundation of China (81573134). In addition, APO was supported by the China Scholarship Council (2015BSZ778). The funders had no role in the design of the study; data acquisition, analyses or interpretation; writing of the manuscript, and in the decision to publish these results.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Authorship
APO, YL and CHS planned the study. APO and XYW analyzed and interpreted the data. APO and RNF drafted the manuscript. XYW contributed to the discussion, reviewed and edited the manuscript. YL and CHS revised the manuscript for important intellectual content and are the guarantors of this study with full access to all the data and takes responsibility for the integrity, accuracy and analysis of the data. All authors approved the final version of the submitted manuscript.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Additional information
Handling Editor: F. Blachier.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Okekunle, A.P., Wu, X., Feng, R. et al. Higher intakes of energy-adjusted dietary amino acids are inversely associated with obesity risk. Amino Acids 51, 373–382 (2019). https://doi.org/10.1007/s00726-018-2672-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00726-018-2672-x