A review of potential metabolic etiologies of the observed association between red meat consumption and development of type 2 diabetes mellitus

Metabolism: Clinical and Experimental

Volumn 64, Issue 7, 2015, Pages 768-779

  Kim, Yoona ^a   Keogh, Jennifer ^a   Clifton, Peter ^a  

^a UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

Author keywords

Advanced glycation end products; Insulin resistance; Insulin sensitivity; Red and processed meat; Trimethylamine N oxide

Indexed keywords

ADVANCED GLYCATION END PRODUCT; AMINO ACID; BACTERIAL ENZYME; CARNITINE; CHOLINE; ENDOCRINE DISRUPTOR; FERRITIN; HEME; INSULIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; NITRIC ACID DERIVATIVE; NITRITE; PHOSPHATIDYLCHOLINE; S6 KINASE; SATURATED FATTY ACID; SODIUM; TRIMETHYLAMINE OXIDE;

FERRITIN BLOOD LEVEL; FOOD INTAKE; HUMAN; INSULIN RESISTANCE; INSULIN SENSITIVITY; IRON STORAGE; NON INSULIN DEPENDENT DIABETES MELLITUS; PRIORITY JOURNAL; PROCESSED MEAT; PROTEIN INTAKE; RED MEAT; REVIEW; RISK ASSESSMENT; ADVERSE EFFECTS; ANIMAL; CLINICAL TRIAL (TOPIC); DIABETES MELLITUS, TYPE 2; DIET; MEAT; RISK;

ANIMALS; CLINICAL TRIALS AS TOPIC; DIABETES MELLITUS, TYPE 2; DIET; HUMANS; MEAT; RISK;

EID: 84929656068     PISSN: 00260495     EISSN: 15328600     Source Type: Journal    
DOI: 10.1016/j.metabol.2015.03.008     Document Type: Review

References (122)

1. D.R. Whiting, L. Guariguata, C. Weil, and J. Shaw IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030 Diabetes Res Clin Pract 94 3 2011 311 321
2. A.D. Association Standards of medical care in diabetes-2006 Diabetes Care 29 2006 S4 S42
3. R. Sherwin, R. Anderson, J. Buse, M. Chin, D. Eddy, and J. Fradkin The prevention or delay of type 2 diabetes Diabetes Care 26 2003 S62 S69
4. E.L. Barr, P.Z. Zimmet, T.A. Welborn, D. Jolley, D.J. Magliano, and D.W. Dunstan Risk of cardiovascular and all-cause mortality in individuals with diabetes mellitus, impaired fasting glucose, and impaired glucose tolerance: the Australian Diabetes, Obesity, and Lifestyle Study (AusDiab) Circulation 116 2 2007 151 157
5. P. Zhang, X. Zhang, J. Brown, D. Vistisen, R. Sicree, and J. Shaw Global healthcare expenditure on diabetes for 2010 and 2030 Diabetes Res Clin Pract 87 3 2010 293 301
6. J. Lindstrom, A. Neumann, K.E. Sheppard, A. Gilis-Januszewska, C.J. Greaves, and U. Handke Take action to prevent diabetes-the IMAGE toolkit for the prevention of type 2 diabetes in Europe Horm Metab Res 42 Suppl. 1 2010 S37 S55
7. P.E. Schwarz, C.J. Greaves, J. Lindstrom, T. Yates, and M.J. Davies Nonpharmacological interventions for the prevention of type 2 diabetes mellitus Nat Rev Endocrinol 8 6 2012 363 373
8. C.T. McEvoy, C.R. Cardwell, J.V. Woodside, I.S. Young, S.J. Hunter, and M.C. McKinley A posteriori dietary patterns are related to risk of type 2 diabetes: findings from a systematic review and meta-analysis J Acad Nutr Diet 114 11 2014 1759 1775 [e4]
9. E. Koloverou, K. Esposito, D. Giugliano, and D. Panagiotakos The effect of Mediterranean diet on the development of type 2 diabetes mellitus: a meta-analysis of 10 prospective studies and 136,846 participants Metabolism 63 7 2014 903 911
10. B.J. Ko, K.H. Park, and C.S. Mantzoros Diet patterns, adipokines, and metabolism: where are we and what is next? Metabolism 63 2 2014 168 177
11. D. Aune, G. Ursin, and M. Veierød Meat consumption and the risk of type 2 diabetes: a systematic review and meta-analysis of cohort studies Diabetologia 52 11 2009 2277 2287
12. R. Micha, S.K. Wallace, and D. Mozaffarian Red and processed meat consumption and risk of incident coronary heart disease, stroke, and diabetes mellitus a systematic review and meta-analysis Circulation 121 21 2010 2271 2283
13. E.J. Feskens, D. Sluik, and G.J. van Woudenbergh Meat consumption, diabetes, and its complications Curr Diab Rep 13 2 2013 298 306
14. A. Pan, Q. Sun, A.M. Bernstein, M.B. Schulze, J.E. Manson, and W.C. Willett Red meat consumption and risk of type 2 diabetes: 3 cohorts of US adults and an updated meta-analysis Am J Clin Nutr 94 4 2011 1088 1096
15. B. Benedinelli, D. Palli, G. Masala, S.J. Sharp, M.B. Schulz, and M. Guevara Association between dietary meat consumption and incident type 2 diabetes: the EPIC-InterAct study Diabetologia 56 1 2013 47 59
16. J.A. Nettleton, M.F. Hivert, R.N. Lemaitre, N.M. McKeown, D. Mozaffarian, and T. Tanaka Meta-analysis investigating associations between healthy diet and fasting glucose and insulin levels and modification by loci associated with glucose homeostasis in data from 15 cohorts Am J Epidemiol 177 2 2013 103 115
17. G. Riccardi, R. Giacco, and A.A. Rivellese Dietary fat, insulin sensitivity and the metabolic syndrome Clin Nutr 23 4 2004 447 456
18. E.J. Feskens, S.M. Virtanen, L. Rasanen, J. Tuomilehto, J. Stengard, and J. Pekkanen Dietary factors determining diabetes and impaired glucose tolerance. A 20-year follow-up of the Finnish and Dutch cohorts of the Seven Countries Study Diabetes Care 18 8 1995 1104 1112
19. J.A. Marshall, D.H. Bessesen, and R.F. Hamman High saturated fat and low starch and fibre are associated with hyperinsulinaemia in a non-diabetic population: the San Luis Valley Diabetes Study Diabetologia 40 4 1997 430 438
20. D.R. Parker, S. Weiss, R. Troisi, P. Cassano, P. Vokonas, and L. Landsberg Relationship of dietary saturated fatty acids and body habitus to serum insulin concentrations: the Normative Aging Study Am J Clin Nutr 58 2 1993 129 136
21. D.J. Maron, J.M. Fair, and W.L. Haskell Saturated fat intake and insulin resistance in men with coronary artery disease. The Stanford Coronary Risk Intervention Project Investigators and Staff Circulation 84 5 1991 2020 2027
22. E.J. Mayer, B. Newman, C.P. Quesenberry, and J.V. Selby Usual dietary fat intake and insulin concentrations in healthy women twins Diabetes Care 16 11 1993 1459 1469
23. J. Mooy, P. Grootenhuis, Hd Vries, L. Bouter, P. Kostense, and R. Heine Determinants of specific serum insulin concentrations in a general Caucasian population aged 50 to 74 years (the Hoorn Study) Diabet Med 15 1 1998 45 52
24. E.J. Mayer-Davis, J.H. Monaco, H.M. Hoen, S. Carmichael, M.Z. Vitolins, and M.J. Rewers Dietary fat and insulin sensitivity in a triethnic population: the role of obesity. The Insulin Resistance Atherosclerosis Study (IRAS) Am J Clin Nutr 65 1 1997 79 87
25. R.M. van Dam, W.C. Willett, E.B. Rimm, M.J. Stampfer, and F.B. Hu Dietary fat and meat intake in relation to risk of type 2 diabetes in men Diabetes Care 25 3 2002 417 424
26. R.J. Heine, C. Mulder, C. Popp-Snijders, J. van der Meer, and E.A. van der Veen Linoleic-acid-enriched diet: long-term effects on serum lipoprotein and apolipoprotein concentrations and insulin sensitivity in noninsulin-dependent diabetic patients Am J Clin Nutr 49 3 1989 448 456
27. M. Uusitupa, U. Schwab, S. Makimattila, P. Karhapaa, E. Sarkkinen, and H. Maliranta Effects of two high-fat diets with different fatty acid compositions on glucose and lipid metabolism in healthy young women Am J Clin Nutr 59 6 1994 1310 1316
28. U.S. Schwab, L.K. Niskanen, H.M. Maliranta, M.J. Savolainen, Y.A. Kesaniemi, and M.I. Uusitupa Lauric and palmitic acid-enriched diets have minimal impact on serum lipid and lipoprotein concentrations and glucose metabolism in healthy young women J Nutr 125 3 1995 466 473
29. P. Fasching, K. Ratheiser, B. Schneeweiss, M. Rohac, P. Nowotny, and W. Waldhäusl No effect of short-term dietary supplementation of saturated and poly-and monounsaturated fatty acids on insulin secretion and sensitivity in healthy men Ann Nutr Metab 40 2 1996 116 122
30. J.C. Lovejoy, S.R. Smith, C.M. Champagne, M.M. Most, M. Lefevre, and J.P. DeLany Effects of diets enriched in saturated (palmitic), monounsaturated (oleic), or trans (elaidic) fatty acids on insulin sensitivity and substrate oxidation in healthy adults Diabetes Care 25 8 2002 1283 1288
31. B. Vessby, M. Uusitupa, K. Hermansen, G. Riccardi, A.A. Rivellese, and L.C. Tapsell Substituting dietary saturated for monounsaturated fat impairs insulin sensitivity in healthy men and women: The KANWU Study Diabetologia 44 3 2001 312 319
32. J.A. Paniagua, A. Gallego de la Sacristana, I. Romero, A. Vidal-Puig, J.M. Latre, and E. Sanchez Monounsaturated fat-rich diet prevents central body fat distribution and decreases postprandial adiponectin expression induced by a carbohydrate-rich diet in insulin-resistant subjects Diabetes Care 30 7 2007 1717 1723
33. F. Perez-Jimenez, J. Lopez-Miranda, M. Pinillos, P. Gomez, E. Paz-Rojas, and P. Montilla A Mediterranean and a high-carbohydrate diet improve glucose metabolism in healthy young persons Diabetologia 44 11 2001 2038 2043
34. N. Stefan, H.G. Wahl, A. Fritsche, H. Haring, and M. Stumvoll Effect of the pattern of elevated free fatty acids on insulin sensitivity and insulin secretion in healthy humans Horm Metab Res 33 7 2001 432 438
35. C. Yu, Y. Chen, G.W. Cline, D. Zhang, H. Zong, and Y. Wang Mechanism by which fatty acids inhibit insulin activation of insulin receptor substrate-1 (IRS-1)-associated phosphatidylinositol 3-kinase activity in muscle J Biol Chem 277 52 2002 50230 50236
36. S. Chiu, P.T. Williams, T. Dawson, R.N. Bergman, D. Stefanovski, and S.M. Watkins Diets High in Protein or Saturated Fat Do Not Affect Insulin Sensitivity or Plasma Concentrations of Lipids and Lipoproteins in Overweight and Obese Adults J Nutr 144 11 2014 1753 1759
37. M. Krssak, K. Falk Petersen, A. Dresner, L. DiPietro, S.M. Vogel, and D.L. Rothman Intramyocellular lipid concentrations are correlated with insulin sensitivity in humans: a 1H NMR spectroscopy study Diabetologia 42 1 1999 113 116
38. G. Perseghin, P. Scifo, F. De Cobelli, E. Pagliato, A. Battezzati, and C. Arcelloni Intramyocellular triglyceride content is a determinant of in vivo insulin resistance in humans: a 1H-13C nuclear magnetic resonance spectroscopy assessment in offspring of type 2 diabetic parents Diabetes 48 8 1999 1600 1606
39. L.M. Goff, J.D. Bell, P.W. So, A. Dornhorst, and G.S. Frost Veganism and its relationship with insulin resistance and intramyocellular lipid Eur J Clin Nutr 59 2 2005 291 298
40. N. Barnard, S. Levin, and C. Trapp Meat consumption as a risk factor for type 2 diabetes Nutrients 6 2 2014 897 910
41. S. Mannisto, J. Kontto, M. Kataja-Tuomola, D. Albanes, and J. Virtamo High processed meat consumption is a risk factor of type 2 diabetes in the Alpha-Tocopherol, Beta-Carotene Cancer Prevention study Br J Nutr 103 12 2010 1817 1822
42. D.S. Donovan, C.G. Solomon, E.W. Seely, G.H. Williams, and D.C. Simonson Effect of sodium intake on insulin sensitivity Am J Physiol 264 5 Pt 1 1993 E730 E734
43. M. Foo, A.E. Denver, S.W. Coppack, and J.S. Yudkin Effect of salt-loading on blood pressure, insulin sensitivity and limb blood flow in normal subjects Clin Sci (Lond) 95 2 1998 157 164
44. A.M. Sharma, K. Ruland, K.P. Spies, and A. Distler Salt sensitivity in young normotensive subjects is associated with a hyperinsulinemic response to oral glucose J Hypertens 9 4 1991 329 335
45. F.S. Facchini, C. DoNascimento, G.M. Reaven, J.W. Yip, X.P. Ni, and M.H. Humphreys Blood pressure, sodium intake, insulin resistance, and urinary nitrate excretion Hypertension 33 4 1999 1008 1012
46. T. Iwaoka, T. Umeda, M. Ohno, J. Inoue, S. Naomi, and T. Sato The effect of low and high NaCl diets on oral glucose tolerance Klin Wochenschr 66 16 1988 724 728
47. A. Raji, G.H. Williams, X. Jeunemaitre, P.N. Hopkins, S.C. Hunt, and N.K. Hollenberg Insulin resistance in hypertensives: effect of salt sensitivity, renin status and sodium intake J Hypertens 19 1 2001 99 105
48. O. Melander, L. Groop, and U.L. Hulthen Effect of salt on insulin sensitivity differs according to gender and degree of salt sensitivity Hypertension 35 3 2000 827 831
49. H. McGee On food and cooking: the science and lore of the kitchen Rev Upd edition ed 2007 Scribner
50. J. Uribarri, W. Cai, O. Sandu, M. Peppa, T. Goldberg, and H. Vlassara Diet-derived advanced glycation end products are major contributors to the body's AGE pool and induce inflammation in healthy subjects Ann N Y Acad Sci 1043 2005 461 466
51. I. Birlouez-Aragon, G. Saavedra, F.J. Tessier, A. Galinier, L. Ait-Ameur, and F. Lacoste A diet based on high-heat-treated foods promotes risk factors for diabetes mellitus and cardiovascular diseases Am J Clin Nutr 91 5 2010 1220 1226
52. S.M. Hofmann, H.-J. Dong, Z. Li, W. Cai, J. Altomonte, and S.N. Thung Improved insulin sensitivity is associated with restricted intake of dietary glycoxidation products in the db/db mouse Diabetes 51 7 2002 2082 2089
53. S. Yamagishi, S. Ueda, and S. Okuda Food-derived advanced glycation end products (AGEs): a novel therapeutic target for various disorders Curr Pharm Des 13 27 2007 2832 2836
54. D.L. White, and A. Collinson Red meat, dietary heme iron, and risk of type 2 diabetes: the involvement of advanced lipoxidation endproducts Adv Nutr 4 4 2013 403 411
55. M. Estévez Protein carbonyls in meat systems: A review Meat Sci 89 3 2011 259 279
56. M. Estévez, and M. Heinonen Effect of phenolic compounds on the formation of α-aminoadipic and γ-glutamic semialdehydes from myofibrillar proteins oxidized by copper, iron, and myoglobin J Agric Food Chem 58 7 2010 4448 4455
57. A. Martinaud, Y. Mercier, P. Marinova, C. Tassy, P. Gatellier, and M. Renerre Comparison of oxidative processes on myofibrillar proteins from beef during maturation and by different model oxidation systems J Agric Food Chem 45 7 1997 2481 2487
58. A. Promeyrat, T. Sayd, E. Laville, C. Chambon, B. Lebret, and P. Gatellier Early post-mortem sarcoplasmic proteome of porcine muscle related to protein oxidation Food Chem 127 3 2011 1097 1104
59. J. Uribarri, S. Woodruff, S. Goodman, W. Cai, X. Chen, and R. Pyzik Advanced glycation end products in foods and a practical guide to their reduction in the diet J Am Diet Assoc 110 6 2010 911 916 [e12]
60. F.J. Tessier, and I. Birlouez-Aragon Health effects of dietary Maillard reaction products: the results of ICARE and other studies Amino Acids 42 4 2012 1119 1131
61. H. Vlassara, W. Cai, J. Crandall, T. Goldberg, R. Oberstein, and V. Dardaine Inflammatory mediators are induced by dietary glycotoxins, a major risk factor for diabetic angiopathy Proc Natl Acad Sci 99 24 2002 15596 15601
62. W. Cai, J.C. He, L. Zhu, M. Peppa, C. Lu, and J. Uribarri High levels of dietary advanced glycation end products transform low-density lipoprotein into a potent redox-sensitive mitogen-activated protein kinase stimulant in diabetic patients Circulation 110 3 2004 285 291
63. Z. Zhao, C. Zhao, X.H. Zhang, F. Zheng, W. Cai, and H. Vlassara Advanced glycation end products inhibit glucose-stimulated insulin secretion through nitric oxide-dependent inhibition of cytochrome c oxidase and adenosine triphosphate synthesis Endocrinology 150 6 2009 2569 2576
64. O. Sandu, K. Song, W. Cai, F. Zheng, J. Uribarri, and H. Vlassara Insulin resistance and type 2 diabetes in high-fat-fed mice are linked to high glycotoxin intake Diabetes 54 8 2005 2314 2319
65. N.J. Kellow, and G.S. Savige Dietary advanced glycation end-product restriction for the attenuation of insulin resistance, oxidative stress and endothelial dysfunction: a systematic review Eur J Clin Nutr 67 3 2013 239 248
66. J. Uribarri, W. Cai, M. Ramdas, S. Goodman, R. Pyzik, and X. Chen Restriction of advanced glycation end products improves insulin resistance in human type 2 diabetes: potential role of AGER1 and SIRT1 Diabetes Care 34 7 2011 1610 1616
67. H. Vlassara, W. Cai, S. Goodman, R. Pyzik, A. Yong, and X. Chen Protection against loss of innate defenses in adulthood by low advanced glycation end products (AGE) intake: role of the antiinflammatory AGE receptor-1 J Clin Endocrinol Metab 94 11 2009 4483 4491
68. N. Tahara, Si Yamagishi, T. Matsui, M. Takeuchi, Y. Nitta, and N. Kodama Serum levels of advanced glycation end products (AGEs) are independent correlates of insulin resistance in nondiabetic subjects Cardiovasc Ther 30 1 2012 42 48
69. M. Negrean, A. Stirban, B. Stratmann, T. Gawlowski, T. Horstmann, and C. Gotting Effects of low- and high-advanced glycation endproduct meals on macro- and microvascular endothelial function and oxidative stress in patients with type 2 diabetes mellitus Am J Clin Nutr 85 5 2007 1236 1243
70. N.G. Hord, Y. Tang, and N.S. Bryan Food sources of nitrates and nitrites: the physiologic context for potential health benefits Am J Clin Nutr 90 1 2009 1 10
71. P. Pacher, J.S. Beckman, and L. Liaudet Nitric oxide and peroxynitrite in health and disease Physiol Rev 87 1 2007 315 424
72. E.R. Stadtman, and R.L. Levine Protein oxidation Ann N Y Acad Sci 899 1 2000 191 208
73. K. Krapfenbauer, R. Birnbacher, H. Vierhapper, K. Herkner, D. Kampel, and G. Lubec Glycoxidation, and protein and DNA oxidation in patients with diabetes mellitus Clin Sci (Lond) 95 3 1998 331 337
74. D. Gradinaru, C. Borsa, C. Ionescu, and D. Margina Advanced oxidative and glycoxidative protein damage markers in the elderly with type 2 diabetes J Proteomics 92 2013 313 322
75. B. Portha, M.H. Giroix, J.C. Cros, and L. Picon Diabetogenic effect of N-nitrosomethylurea and N-nitrosomethylurethane in the adult rat Ann Nutr Aliment 34 5-6 1980 1143 1151
76. S.M. de la Monte, M. Tong, M. Lawton, and L. Longato Nitrosamine exposure exacerbates high fat diet-mediated type 2 diabetes mellitus, non-alcoholic steatohepatitis, and neurodegeneration with cognitive impairment Mol Neurodegener 4 1 2009 54
77. R.M. van Dam, E.B. Rimm, W.C. Willett, M.J. Stampfer, and F.B. Hu Dietary patterns and risk for type 2 diabetes mellitus in U.S. men Ann Intern Med 136 3 2002 201 209
78. M.B. Schulze, J.E. Manson, W.C. Willett, and F.B. Hu Processed meat intake and incidence of Type 2 diabetes in younger and middle-aged women Diabetologia 46 11 2003 1465 1473
79. S.N. Rajpathak, J.P. Crandall, J. Wylie-Rosett, G.C. Kabat, T.E. Rohan, and F.B. Hu The role of iron in type 2 diabetes in humans BBA-Gen Subjects 1790 7 2009 671 681
80. N.W. Hua, R.A. Stoohs, and F.S. Facchini Low iron status and enhanced insulin sensitivity in lacto-ovo vegetarians Br J Nutr 86 04 2001 515 519
81. J.M. Fernández-Real, A. López-Bermejo, and W. Ricart Cross-talk between iron metabolism and diabetes Diabetes 51 8 2002 2348 2354
82. S. Swaminathan, V.A. Fonseca, M.G. Alam, and S.V. Shah The role of iron in diabetes and its complications Diabetes Care 30 7 2007 1926 1933
83. N. Bashan, J. Kovsan, I. Kachko, H. Ovadia, and A. Rudich Positive and negative regulation of insulin signaling by reactive oxygen and nitrogen species Physiol Rev 89 1 2009 27 71
84. E. Ferrannini Insulin resistance, iron, and the liver Lancet 355 9222 2000 2181 2182
85. A. Green, R. Basile, and J.M. Rumberger Transferrin and iron induce insulin resistance of glucose transport in adipocytes Metabolism 55 8 2006 1042 1045
86. T.-P. Tuomainen, K. Nyyssönen, R. Salonen, A. Tervahauta, H. Korpela, and T. Lakka Body iron stores are associated with serum insulin and blood glucose concentrations: population study in 1,013 eastern Finnish men Diabetes Care 20 3 1997 426 428
87. J.G. Wilson, J.H. Lindquist, S.C. Grambow, E.D. Crook, and J.F. Maher Potential role of increased iron stores in diabetes Am J Med Sci 325 6 2003 332 339
88. A. Ascherio, E.B. Rimm, E. Giovannucci, W.C. Willett, and M.J. Stampfer Blood donations and risk of coronary heart disease in men Circulation 103 1 2001 52 57
89. R. Jiang, J. Ma, A. Ascherio, M.J. Stampfer, W.C. Willett, and F.B. Hu Dietary iron intake and blood donations in relation to risk of type 2 diabetes in men: a prospective cohort study Am J Clin Nutr 79 1 2004 70 75
90. J.M. Fernández-Real, A. López-Bermejo, and W. Ricart Iron stores, blood donation, and insulin sensitivity and secretion Clin Chem 51 7 2005 1201 1205
91. H. Zheng, M. Patel, R. Cable, L. Young, and S.D. Katz Insulin sensitivity, vascular function, and iron stores in voluntary blood donors Diabetes Care 30 10 2007 2685 2689
92. F.S. Facchini Effect of phlebotomy on plasma glucose and insulin concentrations Diabetes Care 21 12 1998 2190
93. L. Valenti, A.L. Fracanzani, P. Dongiovanni, E. Bugianesi, G. Marchesini, and P. Manzini Iron depletion by phlebotomy improves insulin resistance in patients with nonalcoholic fatty liver disease and hyperferritinemia: evidence from a case-control study Am J Gastroenterol 102 6 2007 1251 1258
94. F.S. Facchini, and K.L. Saylor Effect of iron depletion on cardiovascular risk factors: studies in carbohydrate-intolerant patients Ann N Y Acad Sci 967 2002 342 351
95. J.M. Fernandez-Real, G. Penarroja, A. Castro, F. Garcia-Bragado, I. Hernandez-Aguado, and W. Ricart Blood letting in high-ferritin type 2 diabetes: effects on insulin sensitivity and beta-cell function Diabetes 51 4 2002 1000 1004
96. A. Borai, C. Livingstone, I. Kaddam, and G. Ferns Selection of the appropriate method for the assessment of insulin resistance BMC Med Res Methodol 11 2011 158
97. G.L. Hold Western lifestyle: a 'master' manipulator of the intestinal microbiota? Gut 63 1 2014 5 6
98. X. Gao, X. Liu, J. Xu, C. Xue, Y. Xue, and Y. Wang Dietary trimethylamine N-oxide exacerbates impaired glucose tolerance in mice fed a high fat diet J Biosci Bioeng 118 4 2014 476 481
99. R.A. Koeth, Z. Wang, B.S. Levison, J.A. Buffa, E. Org, and B.T. Sheehy Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis Nat Med 19 5 2013 576 585
100. Z. Wang, E. Klipfell, B.J. Bennett, R. Koeth, B.S. Levison, and B. Dugar Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease Nature 472 7341 2011 57 63
101. W.H. Tang, Z. Wang, B.S. Levison, R.A. Koeth, E.B. Britt, and X. Fu Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk N Engl J Med 368 17 2013 1575 1584
102. F. Badoud, K.P. Lam, A. DiBattista, M. Perreault, M.A. Zulyniak, and B. Cattrysse Serum and adipose tissue amino acid homeostasis in the metabolically healthy obese J Proteome Res 13 7 2014 3455 3466
103. C.J. Lynch, and S.H. Adams Branched-chain amino acids in metabolic signalling and insulin resistance Nat Rev Endocrinol 10 12 2014 723 736
104. O. Fiehn, W.T. Garvey, J.W. Newman, K.H. Lok, C.L. Hoppel, and S.H. Adams Plasma metabolomic profiles reflective of glucose homeostasis in non-diabetic and type 2 diabetic obese African-American women PLoS One 5 12 2010 e15234
105. S.E. McCormack, O. Shaham, M.A. McCarthy, A.A. Deik, T.J. Wang, and R.E. Gerszten Circulating branched-chain amino acid concentrations are associated with obesity and future insulin resistance in children and adolescents Pediatr Obes 8 1 2013 52 61
106. T. Linn, B. Santosa, D. Gronemeyer, S. Aygen, N. Scholz, and M. Busch Effect of long-term dietary protein intake on glucose metabolism in humans Diabetologia 43 10 2000 1257 1265
107. M. Krebs, M. Krssak, E. Bernroider, C. Anderwald, A. Brehm, and M. Meyerspeer Mechanism of amino acid-induced skeletal muscle insulin resistance in humans Diabetes 51 3 2002 599 605
108. M.M. Robinson, M. Soop, T.S. Sohn, D. Morse, J. Schimke, and K. Klaus High insulin combined with essential amino acids stimulates skeletal muscle mitochondrial protein synthesis while decreasing insulin sensitivity in healthy humans J Clin Endocrinol Metab 99 12 2014 E2574 E2583
109. M. van Nielen, E.J. Feskens, A. Rietman, E. Siebelink, and M. Mensink Partly replacing meat protein with soy protein alters insulin resistance and blood lipids in postmenopausal women with abdominal obesity J Nutr 144 9 2014 1423 1429
110. Y. Morimoto, A. Steinbrecher, L.N. Kolonel, and G. Maskarinec Soy consumption is not protective against diabetes in Hawaii: the Multiethnic Cohort Eur J Clin Nutr 65 2 2011 279 282
111. A. Pan, O.H. Franco, J. Ye, W. Demark-Wahnefried, X. Ye, and Z. Yu Soy protein intake has sex-specific effects on the risk of metabolic syndrome in middle-aged and elderly Chinese J Nutr 138 12 2008 2413 2421
112. S.E. Serrano, J. Braun, L. Trasande, R. Dills, and S. Sathyanarayana Phthalates and diet: a review of the food monitoring and epidemiology data Environ Health 13 1 2014 43
113. P. Alonso-Magdalena, I. Quesada, and A. Nadal Endocrine disruptors in the etiology of type 2 diabetes mellitus Nat Rev Endocrinol 7 6 2011 346 353
114. A.K. Sakhi, I.T. Lillegaard, S. Voorspoels, M.H. Carlsen, E.B. Loken, and A.L. Brantsaeter Concentrations of phthalates and bisphenol A in Norwegian foods and beverages and estimated dietary exposure in adults Environ Int 73 2014 259 269
115. T. Fierens, G. Vanermen, M. Van Holderbeke, S. De Henauw, and I. Sioen Effect of cooking at home on the levels of eight phthalates in foods Food Chem Toxicol 50 12 2012 4428 4435
116. S. Ding, Y. Fan, N. Zhao, H. Yang, X. Ye, and D. He High-fat diet aggravates glucose homeostasis disorder caused by chronic exposure to bisphenol A J Endocrinol 221 1 2014 167 179
117. T.T. Fung, M. Schulze, J.E. Manson, W.C. Willett, and F.B. Hu Dietary patterns, meat intake, and the risk of type 2 diabetes in women Arch Intern Med 164 20 2004 2235 2240
118. H. Mohammad Monirul Does Consumer Behaviour on Meat Consumption Increase Obesity? Empirical Evidence from European Countries 2013
119. A.B. Mark, M.W. Poulsen, S. Andersen, J.M. Andersen, M.J. Bak, and C. Ritz Consumption of a diet low in advanced glycation end products for 4 weeks improves insulin sensitivity in overweight women Diabetes Care 37 1 2014 88 95
120. Z. Zhao, S. Li, G. Liu, F. Yan, X. Ma, and Z. Huang Body iron stores and heme-iron intake in relation to risk of type 2 diabetes: a systematic review and meta-analysis PLoS One 7 7 2012 e41641
121. W. Bao, Y. Rong, S. Rong, and L. Liu Dietary iron intake, body iron stores, and the risk of type 2 diabetes: a systematic review and meta-analysis BMC Med 10 2012 119
122. S.K. Kunutsor, T.A. Apekey, J. Walley, and K. Kain Ferritin levels and risk of type 2 diabetes mellitus: an updated systematic review and meta-analysis of prospective evidence Diabetes Metab Res Rev 29 4 2013 308 318