Potential health hazards of eating red meat

Journal of Internal Medicine

Volumn 281, Issue 2, 2017, Pages 106-122

  Wolk, A ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

cancer; cardiovascular diseases; diabetes; environment; mortality; red meat

Indexed keywords

ADVANCED GLYCATION END PRODUCT; AMINO ACID DERIVATIVE; CARNITINE; ENDOCRINE DISRUPTOR; NITRATE; NITRITE; NITROSAMINE; SATURATED FATTY ACID; SODIUM; TRIMETHYLAMINE OXIDE;

BREAST CANCER; CANCER MORTALITY; CARDIOVASCULAR MORTALITY; CEREBROVASCULAR ACCIDENT; COHORT ANALYSIS; COLORECTAL CANCER; DIABETES MELLITUS; ENVIRONMENTAL IMPACT; EVIDENCE BASED PRACTICE; FOOD INTAKE; GLOBAL CHANGE; HEALTH HAZARD; HEART FAILURE; HUMAN; ISCHEMIC HEART DISEASE; MALIGNANT NEOPLASM; NON INSULIN DEPENDENT DIABETES MELLITUS; PANCREAS CANCER; PRACTICE GUIDELINE; PRIORITY JOURNAL; PROCESSED MEAT; PROSTATE CANCER; RED MEAT; REVIEW; ADVERSE EFFECTS; CARDIOVASCULAR DISEASES; CHRONIC DISEASE; DIABETES MELLITUS, TYPE 2; ENVIRONMENT; FEEDING BEHAVIOR; FOOD HANDLING; INCIDENCE; MORTALITY; NEOPLASMS;

CARDIOVASCULAR DISEASES; CHRONIC DISEASE; DIABETES MELLITUS, TYPE 2; ENVIRONMENT; FEEDING BEHAVIOR; FOOD HANDLING; HUMANS; INCIDENCE; MORTALITY; NEOPLASMS; RED MEAT;

EID: 84985914567     PISSN: 09546820     EISSN: 13652796     Source Type: Journal    
DOI: 10.1111/joim.12543     Document Type: Review

References (89)

1. GBD 2013 Risk Factors Collaborators, Forouzanfar MH, Alexander L et al. Global, regional, and national comparative risk assessment of 79 behavioural, environmental and occupational, and metabolic risks or clusters of risks in 188 countries, 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 2015; 386: 2287–323.
2. Mills E. ADDITIVES | Functional. In: Jensen WK, ed. Encyclopedia of Meat Sciences. Oxford: Elsevier, 2004; 1–6.
3. Bouvard V, Loomis D, Guyton KZ et al. Carcinogenicity of consumption of red and processed meat. Lancet Oncol 2015; 16: 1599–600.
4. Lafarga T, Hayes M. Bioactive peptides from meat muscle and by-products: generation, functionality and application as functional ingredients. Meat Sci 2014; 98: 227–39.
5. WHO. Evaluation of Certain Food Additives and Contaminants. Geneva: WHO, 2002.
6. European Food Safety Authority. Cadmium dietary exposure in the European population. Scientific Report of EFSA. EFSA 2012; 10: 2551.
7. Serratosa J, Blass A, Rigau B et al. Residues from veterinary medicinal products, growth promoters and performance enhancers in food-producing animals: a European Union perspective. Rev Sci Tech 2006; 25: 637–53.
8. Rohrmann S, Zoller D, Hermann S, Linseisen J. Intake of heterocyclic aromatic amines from meat in the European Prospective Investigation into Cancer and Nutrition (EPIC)-Heidelberg cohort. Br J Nutr 2007; 98: 1112–5.
9. European Food Safety Authority. Opinion of the Scientific Panel on Contaminants in Food Chain on a request from the Commission related to fumonisins as undesirable substances in animal feed. EFSA 2005; 235: 1–32.
10. Clarke RE, Dordevic AL, Tan SM, Ryan L, Coughlan MT. Dietary advanced glycation end products and risk factors for chronic disease: a systematic review of randomised controlled trials. Nutrients 2016; 8: 125–40.
11. Harrison P, Bruinsma J, de Haen H et al. World agriculture: towards 2015/2030. Online www.Fao.Org.documents, 2002.
12. Anon. Livestock and Poultry: World Markets and Trade. United States Department of Agriculture's, 2011.
13. Feskens EJM, Sluik D, van Woudenbergh GJ. Meat consumption, diabetes, and its complications. Curr Diab Rep 2013; 13: 298–306.
14. Fretts AM, Follis JL, Nettleton JA et al. Consumption of meat is associated with higher fasting glucose and insulin concentrations regardless of glucose and insulin genetic risk scores: a meta-analysis of 50,345 Caucasians. Am J Clin Nutr 2015; 102: 1266–78.
15. Schoenaker DAJM, Mishra GD, Callaway LK, Soedamah-Muthu SS. The role of energy, nutrients, foods, and dietary patterns in the development of gestational diabetes mellitus: a systematic review of observational studies. Diabetes Care 2016; 39: 16–23.
16. Kim Y, Keogh J, Clifton P. A review of potential metabolic etiologies of the observed association between red meat consumption and development of type 2 diabetes mellitus. Metabolism 2015; 64: 768–79.
17. Badoud F, Lam KP, DiBattista A et al. Serum and adipose tissue amino acid homeostasis in the metabolically healthy obese. J Proteome Res 2014; 13: 3455–66.
18. Lynch CJ, Adams SH. Branched-chain amino acids in metabolic signalling and insulin resistance. Nat Rev Endocrinol 2014; 10: 723–36.
19. Fiehn O, Garvey WT, Newman JW, Lok KH, Hoppel CL, Adams SH. Plasma metabolomic profiles reflective of glucose homeostasis in non-diabetic and type 2 diabetic obese African-American women. PLoS ONE 2010; 5: e15234.
20. McCormack SE, Shaham O, McCarthy MA et al. Circulating branched-chain amino acid concentrations are associated with obesity and future insulin resistance in children and adolescents. Pediatr Obes 2013; 8: 52–61.
21. McGee H. On Food and Cooking: The Science and Lore of the Kitchen, Rev Upd edn. New York: Scribner, 2004.
22. Uribarri J, Woodruff S, Goodman S et al. Advanced glycation end products in foods and a practical guide to their reduction in the diet. J Am Diet Assoc 2010; 110: 911–6.e12.
23. Uribarri J, Cai W, Sandu O, Peppa M, Goldberg T, Vlassara H. 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 2005; 1043: 461–6.
24. Kellow NJ, Savige GS. Dietary advanced glycation end-product restriction for the attenuation of insulin resistance, oxidative stress and endothelial dysfunction: a systematic review. Eur J Clin Nutr 2013; 67: 239–48.
25. Vlassara H, Cai W, Crandall J et al. Inflammatory mediators are induced by dietary glycotoxins, a major risk factor for diabetic angiopathy. Proc Natl Acad Sci USA 2002; 99: 15596–601.
26. Cai W, He JC, Zhu L et al. 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 2004; 110: 285–91.
27. Uribarri J, Cai W, Ramdas M et al. Restriction of advanced glycation end products improves insulin resistance in human type 2 diabetes: potential role of AGER1 and SIRT1. Diabetes Care 2011; 34: 1610–6.
28. Rajpathak SN, Crandall JP, Wylie-Rosett J, Kabat GC, Rohan TE, Hu FB. The role of iron in type 2 diabetes in humans. Biochim Biophys Acta 2009; 1790: 671–81.
29. Fernández-Real JM, López-Bermejo A, Ricart W. Cross-talk between iron metabolism and diabetes. Diabetes 2002; 51: 2348–54.
30. Bashan N, Kovsan J, Kachko I, Ovadia H, Rudich A. Positive and negative regulation of insulin signaling by reactive oxygen and nitrogen species. Physiol Rev 2009; 89: 27–71.
31. Wilson JG, Lindquist JH, Grambow SC, Crook ED, Maher JF. Potential role of increased iron stores in diabetes. Am J Med Sci 2003; 325: 332–9.
32. Ferrannini E. Insulin resistance, iron, and the liver. Lancet 2000; 355: 2181–2.
33. Zhao Z, Li S, Liu G et al. Body iron stores and heme-iron intake in relation to risk of type 2 diabetes: a systematic review and meta-analysis. PLoS ONE 2012; 7: e41641.
34. Micha R, Wallace SK, Mozaffarian D. Red and processed meat consumption and risk of incident coronary heart disease, stroke, and diabetes mellitus: a systematic review and meta-analysis. Circulation 2010; 121: 2271–83.
35. Pan A, Sun Q, Bernstein AM et al. Red meat consumption and risk of type 2 diabetes: 3 cohorts of US adults and an updated meta-analysis. Am J Clin Nutr 2011; 94: 1088–96.
36. Portha B, Giroix MH, Cros JC, Picon L. Diabetogenic effect of N-nitrosomethylurea and N-nitrosomethylurethane in the adult rat. Ann Nutr Aliment 1980; 34: 1143–51.
37. de la Monte SM, Tong M, Lawton M, Longato L. Nitrosamine exposure exacerbates high fat diet-mediated type 2 diabetes mellitus, non-alcoholic steatohepatitis, and neurodegeneration with cognitive impairment. Mol Neurodegener 2009; 4: 54.
38. Hord NG, Tang Y, Bryan NS. Food sources of nitrates and nitrites: the physiologic context for potential health benefits. Am J Clin Nutr 2009; 90: 1–10.
39. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 2007; 87: 315–424.
40. Männistö S, Kontto J, Kataja-Tuomola M, Albanes D, Virtamo J. High processed meat consumption is a risk factor of type 2 diabetes in the Alpha-Tocopherol, Beta-Carotene Cancer Prevention study. Br J Nutr 2010; 103: 1817–22.
41. Donovan DS, Solomon CG, Seely EW, Williams GH, Simonson DC. Effect of sodium intake on insulin sensitivity. Am J Physiol 1993; 264: E730–4.
42. Foo M, Denver AE, Coppack SW, Yudkin JS. Effect of salt-loading on blood pressure, insulin sensitivity and limb blood flow in normal subjects. Clin Sci (Lond) 1998; 95: 157–64.
43. Facchini FS, DoNascimento C, Reaven GM, Yip JW, Ni XP, Humphreys MH. Blood pressure, sodium intake, insulin resistance, and urinary nitrate excretion. Hypertension 1999; 33: 1008–12.
44. Iwaoka T, Umeda T, Ohno M et al. The effect of low and high NaCl diets on oral glucose tolerance. Klin Wochenschr 1988; 66: 724–8.
45. Gao X, Liu X, Xu J, Xue C, Xue Y, Wang Y. Dietary trimethylamine N-oxide exacerbates impaired glucose tolerance in mice fed a high fat diet. J Biosci Bioeng 2014; 118: 476–81.
46. Koeth RA, Wang Z, Levison BS et al. Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat Med 2013; 19: 576–85.
47. Wang Z, Klipfell E, Bennett BJ et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 2011; 472: 57–63.
48. Ding S, Fan Y, Zhao N et al. High-fat diet aggravates glucose homeostasis disorder caused by chronic exposure to bisphenol A. J Endocrinol 2014; 221: 167–79.
49. Alonso-Magdalena P, Quesada I, Nadal A. Endocrine disruptors in the etiology of type 2 diabetes mellitus. Nat Rev Endocrinol 2011; 7: 346–53.
50. Kaluza J, Wolk A, Larsson SC. Red meat consumption and risk of stroke: a meta-analysis of prospective studies. Stroke 2012; 43: 2556–60.
51. Haring B, Misialek JR, Rebholz CM et al. Association of dietary protein consumption with incident silent cerebral infarcts and stroke: the Atherosclerosis Risk in Communities (ARIC) study. Stroke 2015; 46: 3443–50.
52. Bernstein AM, Sun Q, Hu FB, Stampfer MJ, Manson JE, Willett WC. Major dietary protein sources and risk of coronary heart disease in women. Circulation 2010; 122: 876–83.
53. Nettleton JA, Steffen LM, Loehr LR, Rosamond WD, Folsom AR. Incident heart failure is associated with lower whole-grain intake and greater high-fat dairy and egg intake in the Atherosclerosis Risk in Communities (ARIC) study. J Am Diet Assoc 2008; 108: 1881–7.
54. Ashaye A, Gaziano J, Djoussé L. Red meat consumption and risk of heart failure in male physicians. Nutr Metab Cardiovasc Dis 2011; 21: 941–6.
55. Kaluza J, Akesson A, Wolk A. Processed and unprocessed red meat consumption and risk of heart failure: prospective study of men. Circ Heart Fail 2014; 7: 552–7.
56. Kaluza J, Åkesson A, Wolk A. Long-term processed and unprocessed red meat consumption and risk of heart failure: a prospective cohort study of women. Int J Cardiol 2015; 193: 42–6.
57. Marmot M, Atinmo T, Byers T et al. Food, Nutrition, Physical Activity, and the Prevention of Cancer: A Global Perspective. Washington, DC, USA: World Cancer Research Fund/American Institute for Cancer Research, 2007.
58. Guo J, Wei W, Zhan L. Red and processed meat intake and risk of breast cancer: a meta-analysis of prospective studies. Breast Cancer Res Treat 2015; 151: 191–8.
59. Wu K, Spiegelman D, Hou T et al. Associations between unprocessed red and processed meat, poultry, seafood and egg intake and the risk of prostate cancer: a pooled analysis of 15 prospective cohort studies. Int J Cancer 2016; 138: 2368–82.
60. Xue X-J, Gao Q, Qiao J-H, Zhang J, Xu C-P, Liu J. Red and processed meat consumption and the risk of lung cancer: a dose-response meta-analysis of 33 published studies. Int J Clin Exp Med 2014; 7: 1542–53.
61. Chan DSM, Lau R, Aune D et al. Red and processed meat and colorectal cancer incidence: meta-analysis of prospective studies. PLoS ONE 2011; 6: e20456.
62. Zhu H, Yang X, Zhang C et al. Red and processed meat intake is associated with higher gastric cancer risk: a meta-analysis of epidemiological observational studies. PLoS ONE 2013; 8: e70955.
63. Qu X, Ben Q, Jiang Y. Consumption of red and processed meat and risk for esophageal squamous cell carcinoma based on a meta-analysis. Ann Epidemiol 2013; 23: 762–70.e1.
64. Larsson SC, Wolk A. Red and processed meat consumption and risk of pancreatic cancer: meta-analysis of prospective studies. Br J Cancer 2012; 106: 603–7.
65. Luo J, Yang Y, Liu J et al. Systematic review with meta-analysis: meat consumption and the risk of hepatocellular carcinoma. Aliment Pharmacol Ther 2014; 39: 913–22.
66. Alexander DD, Cushing CA. Quantitative assessment of red meat or processed meat consumption and kidney cancer. Cancer Detect Prev 2009; 32: 340–51.
67. Li F, An S, Hou L, Chen P, Lei C, Tan W. Red and processed meat intake and risk of bladder cancer: a meta-analysis. Int J Clin Exp Med 2014; 7: 2100–10.
68. Wallin A, Orsini N, Wolk A. Red and processed meat consumption and risk of ovarian cancer: a dose-response meta-analysis of prospective studies. Br J Cancer 2011; 104: 1196–201.
69. Ishikawa S, Tamaki S, Ohata M, Arihara K, Itoh M. Heme induces DNA damage and hyperproliferation of colonic epithelial cells via hydrogen peroxide produced by heme oxygenase: a possible mechanism of heme-induced colon cancer. Mol Nutr Food Res 2010; 54: 1182–91.
70. Knöbel Y, Weise A, Glei M, Sendt W, Claussen U, Pool-Zobel BL. Ferric iron is genotoxic in non-transformed and preneoplastic human colon cells. Food Chem Toxicol 2007; 45: 804–11.
71. Klaunig JE, Kamendulis LM. The role of oxidative stress in carcinogenesis. Annu Rev Pharmacol Toxicol 2004; 44: 239–67.
72. Hebels DGAJ, Sveje KM, de Kok MC et al. Red meat intake-induced increases in fecal water genotoxicity correlate with pro-carcinogenic gene expression changes in the human colon. Food Chem Toxicol 2012; 50: 95–103.
73. O'Callaghan NJ, Toden S, Bird AR, Topping DL, Fenech M, Conlon MA. Colonocyte telomere shortening is greater with dietary red meat than white meat and is attenuated by resistant starch. Clin Nutr 2012; 31: 60–4.
74. Toden S, Belobrajdic DP, Bird AR, Topping DL, Conlon MA. Effects of dietary beef and chicken with and without high amylose maize starch on blood malondialdehyde, interleukins, IGF-I, insulin, leptin, MMP-2, and TIMP-2 concentrations in rats. Nutr Cancer 2010; 62: 454–65.
75. Derry MM, Raina K, Agarwal C, Agarwal R. Identifying molecular targets of lifestyle modifications in colon cancer prevention. Front Oncol 2013; 3: 119.
76. Key TJ, Fraser GE, Thorogood M et al. Mortality in vegetarians and nonvegetarians: detailed findings from a collaborative analysis of 5 prospective studies. Am J Clin Nutr 1999; 70: 516S–24S.
77. Larsson SC, Orsini N. Red meat and processed meat consumption and all-cause mortality: a meta-analysis. Am J Epidemiol 2014; 179: 282–9.
78. Wang X, Lin X, Ouyang YY et al. Red and processed meat consumption and mortality: dose-response meta-analysis of prospective cohort studies. Public Health Nutr 2016; 19: 893–905.
79. Bellavia A, Larsson SC, Bottai M, Wolk A, Orsini N. Differences in survival associated with processed and with nonprocessed red meat consumption. Am J Clin Nutr 2014; 100: 924–9.
80. Abete I, Romaguera D, Vieira AR, Lopez de Munain A, Norat T. Association between total, processed, red and white meat consumption and all-cause, CVD and IHD mortality: a meta-analysis of cohort studies. Br J Nutr 2014; 112: 762–75.
81. Steinfeld H, Gerber P, Wassenaar T, Castel V, Rosales M, de Haan C. Livestock's Long Shadow. Rome: FAO, 2006.
82. Aston LM, Smith JN, Powles JW. Impact of a reduced red and processed meat dietary pattern on disease risks and greenhouse gas emissions in the UK: a modelling study. BMJ Open 2012; 2: e001072.
83. Alexandratos N, Bruinsma J, Bödeker G et al. World Agriculture: Towards 2030/2050. Interim Report. Prospects for Food, Nutrition, Agriculture and Major Commodity Groups. London: Wiley, 2006.
84. de Abreu Silva EO, Marcadenti A. Higher red meat intake may be a marker of risk, not a risk factor itself. Arch Intern Med 2009; 169: 1538–9; author reply 1539.
85. Fogelholm M, Kanerva N, Männistö S. Association between red and processed meat consumption and chronic diseases: the confounding role of other dietary factors. Eur J Clin Nutr 2015; 69: 1060–5.
86. Nordic Council of Ministers. Nordic Nutrition Recommendations 2012 – Integrating Nutrition and Physical Activity. Copenhagen: Nordic Council of Ministers, 2014.
87. Anon. http://www.livsmedelsverket.se/en/food-habits-health-and-environment/dietary-guidelines/vuxna/red-and-processed-meat/ accessed 15 March 2016.
88. DeSalvo KB, Olson R, Casavale KO. Dietary guidelines for Americans. JAMA 2016; 315: 457–8.
89. Kromhout D, Spaaij CJK, de Goede J, Weggemans RM. The 2015 Dutch food-based dietary guidelines. Eur J Clin Nutr 2016; 70: 869–78.