Red Meat and Health – have we been blaming the wrong thing?


by Monica Mollica ~ trainergize.com

Frequent consumption of red and processed meat has been shown in population studies to be positively correlated with cardiovascular disease 1-3, cancer and type 2 diabetes. Recent meta-analyses also indicate that it increases total mortality 4. Hence, a high meat intake (regardless of its fat quantity and quality) is generally perceived to be unhealthy and something that should be avoided. However, although there are many studies documenting these associations, results are not always consistent and there are several methodological issues which weakens the strength of their findings (more on that in a bit).

In the same way as the putative health risks of red meat consumption is investigated, its documented health benefits (which I will cover below) are equally as important and must be given a fair chance in the establishment of public health messages in relation to red meat consumption. In this article I will therefore cover both the risks and benefits associated with red meat consumption, and after having taken all the scientific data into consideration, argue that meat has been unfairly blamed…

This is a long article (7 pages excluding references) so here’s a printer-friendly download version for you who prefer to read away from the computer and/or want to share it with others.

The “bad” side of meat – supposed harm to health

Cardiovascular disease (heart attack, stroke and coronary heart disease)

In a study that found a significant positive association between servings of red meat and the risk of coronary heart disease (adjusted for age), this effect became non-significant (meaning it could have occurred by chance) after controlling for age, body weight, smoking, alcohol, physical activity, energy intake and family history of coronary heart disease in the multivariate analysis 1. Another study reported found that red meat was associated with an increased risk of mortality from coronary heart disease, but their classification of red meat included processed meats 5. Similar inconsistencies have been observed in 1, 6, because there is no universal agreement of which meats should be classed as processed or not 7, 8. A recent meta-analysis from Harvard Medical School concluded that unprocessed red meat intake is not associated with coronary heart disease (relative risk per 100-g serving per day), while processed meat intake is associated with 42% higher risk of coronary heart disease (relative risk per 50-g serving per day) 9. This study also found that consumption of unprocessed or processed meat were not associated with stroke 9.

Much evidence is based on studies that have investigated dietary patterns rather than meat consumption in relation to risk of cardiovascular disease 2, 10-13. However, when looking at dietary pattern analyses and comparisons we have to remember that these types of studies make it impossible to isolate the effects of red meat alone, which is what the whole red meat – health diatribe is all about.

A typical Western dietary pattern has been identified that is high in red meat and meat products, low in fruit and vegetables and coupled with a sedentary lifestyle, smoking and high alcohol intake 14. This type of diet has been associated with a 22% greater risk of mortality from cardiovascular disease than a prudent dietary pattern that is high in fruit and vegetables, legumes, poultry and whole grains 15. Bearing in mind the very well documented health promoting effects of fruit and vegetables 16, this doesn’t come as a surprise.

Including red meat as part of the typical Western dietary pattern erroneously implies that red meat cannot be part of a healthy dietary pattern characterized by a high intake of for example fruit and vegetables, oily fish and legumes. This has been proven in several less frequently cited studies, which demonstrated that when red meat is included is such a healthy dietary pattern, it is not related with cardiovascular disease mortality 17, 18.

Cancer

Based on epidemiological studies it is assumed that meat, especially red meat, enhances risk for cancer, particularly of the colon, breast and prostate 19. One of the 10 universal guidelines for healthy nutrition in a report of the World Cancer Research Fund released at the end of 2007 is to “limit intake of red meat and avoid processed meat”, as a result of the “convincing evidence” for an association with an increased risk of colorectal cancer development 20. However, as it turns out, the allegedly “convincing evidence” is not at all that convincing 21. For those unfamiliar with scientific parlance, saying that something has “convincing evidence” is a very bold statement. According to the scientific norms, that kind of statement requires that all different types of studies behind the evidence point in the same direction. This, coupled with the fact that the World Cancer Research Fund presented its “convincing evidence” in only one page of text of the 517-page report, has made several leading cancer researchers raise their eye-brows 21, 22.

The flaws with World Cancer Research Fund report are obvious when we look at statistics for meat intake and colon cancer incidence. According to this report, if we decrease our meat intake, then our risk of colorectal cancer will decrease too… In the UK during the period 1963 to 1998 the intake of red meat decreased by 25% 23. Far from falling substantially, the incidence of colorectal cancer increased substantially! 23 Similarly, in Norway the intake of red meat has remained steady or has even decreased at a time when their risk of colorectal cancer increased by 50% 23. The lack of linkage between meat intake and colorectal cancer risk can be illustrated further by comparing the countries in the European Union. Meat consumption in the UK is less than that in any of the other EU and Mediterranean countries 24 and yet the colorectal cancer risk is much higher 23. Spain has a very much higher intake of red meat but still the third lowest colorectal cancer risk 23.

One main flaw (there are several!) with the epidemiological studies that have investigated the relation between meat intake and cancer, is that they haven’t separated the effects of processed and unprocessed meat, and not taking consideration to cooking methods 25. The most supported mechanism behind the putative carcinogenic effect of meat is the formation of mutagenic compounds, HCAs (heterocyclic aromatic amines) and PAHs (polycyclic aromatic hydrocarbons), when meat is cooked at high temperatures to a well-done state 26, 27. However, very few studies have assessed the method of cooking when measuring meat consumption. Therefore, in the largest studies, the effects of red meat per se have not been isolated from the effects of processing or cooking temperatures. Of the few studies which have considered these factors, some found an increased risk of colon cancer with high intakes of well or very well done red meat compared to low intakes 28, whilst others found no increase in risk 29, 30.

The diverging findings can be explained by the fact that approximately 80% of colon cancer cases are thought to be caused by modifiable diet and lifestyle factors 31 and red meat (whether processed or not) is only one factor among a myriad of other strongly influential factors, including intake of fruit and vegetables, physical activity level, obesity and smoking.
A notable study is further supporting this 32; here 265 000 Japanese persons were followed for 25 y. A detailed diet history was taken at recruitment and regularly updated. Vegetable intake was stratified into four intake groups (daily, often, sometimes, and never) and then analyzed in relation to meat consumption and cancer risk in each group. As expected, the daily vegetable intake group had very much lower cancer rates than the never vegetable eating group, with the other two groups intermediate. Interestingly, in the group who ate green-yellow vegetables daily, there was an inverse relation between meat intake and colorectal cancer, meaning that a higher meat intake in the context a vegetable rich dietary pattern actually is associated with a lower colorectal cancer incidence! In the group who never ate vegetables there was, as expected, a positive relation between meat intake and cancer of the colon and rectum (the higher the meat intake, the higher the cancer incidence). Thus is seems as if meat is a risk factor, then it is only manifest among those who do not eat sufficient amounts of the protective factors. This is supported by a recent study demonstrating that a high consumption of fruit and vegetables is associated with a reduced risk of colon cancer 33.

Type-2 diabetes

Intake of red meat has also been associated with type-2 diabetes 34. A meta-analysis that pooled the results from 12 population studies, found that when comparing high vs. low intake, the risk for type-2 diabetes was increased by 21% for unprocessed red meat and 41 % for processed red meat 34. However, the absolute amount eaten varied greatly, and because the included studies didn’t properly control for influencing variables like body weight and physical activity, the researchers themselves admitted that it is possible that these confounding factors could have explained the observed association, and not necessarily the meat intake 34. This is underscored by another study which found that the effect of unprocessed meat intake on type-2 diabetes is modified by body weight 35, which in turn is a function of physical activity and caloric intake.
In contrast, a more recent and more detailed meta-analysis, which pooled the results from 20 population studies, concluded that red meat intake is not associated with type-2 diabetes 9. In agreement with the previous meta-analysis, an association between processed meat intake and type-2 diabetes was found, even though the increase in risk was lower, 19% per 50 g serving/day 9.

All-cause mortality

In March 2012, a media attention grabbing study was published that investigated the association between red meat intake and mortality. This large study prospectively followed 37 698 men from the Health Professionals Follow-up Study (1986-2008) and 83 644 women from the Nurses’ Health Study (1980-2008) who were free of cardiovascular disease (CVD) and cancer at baseline. Diet was assessed by validated food frequency questionnaires and updated every 4 years. The results showed that, after having adjusted for major lifestyle and dietary risk factors, adding 1 serving (3 oz) of unprocessed red meat or processed red meat per day to one’s regular diet was associated with a 13% and 20% greater chance of dying from all causes, respectively.
It was also estimated that substitutions of 1 serving per day of other foods (including fish, poultry, nuts, legumes, low-fat dairy, and whole grains) for 1 serving per day of red meat were associated with a 7% to 19% lower mortality risk. It was further estimated that 9.3% of deaths in men and 7.6% in women in this study could have been prevented at the end of follow-up if all the individuals consumed fewer than 0.5 servings per day (approximately 42 g/d) of red meat. The conclusion of this study stated that red meat consumption is associated with an increased risk of total, CVD, and cancer mortality, and that substitution of other healthy protein sources for red meat is associated with a lower mortality risk 4.

My first question about this study was how it assessed lifestyle related risk factors. What jumped at me right off the bat when I was reading through the research publication was that the researchers, while using validated food frequency questionnaires, did not use validated lifestyle and physical activity assessment questionnaires. As I said in the meat – fat loss article, questionnaires are infamous for being inaccurate and bias prone. So if a questionnaire is used, it better be validated (which mean that what it is supposed to measure reasonably correlates to the results obtained with a more exact labor intensive measurement tool)! This fact, coupled with the finding that associations between diet and mortality are confounded by fitness 36, greatly weakens the conclusions drawn in this study.

To put the red meat – mortality data in context, and to illustrate the importance of fitness, I want to cite a study that investigated the association of cardiovascular fitness (measured by total duration during a maximal treadmill exercise test, and not a nonsense questionnaire!) and mortality 37. Compared with the least fit men and women, the most fit men and women had 43% and 53% lower risk for all-cause mortality, and 47% and 70% lower risk of cardiovascular disease mortality, respectively 38!!! Put this next to the meat – mortality data stating a 13-20% increase in mortality risk by eating red meat, and you get the point; red meat only plays a tiny, if any, role in the overall life style – mortality relation. It’s pretty obvious that the problem is not the red meat, but our lazy asses!!!

The importance of distinguishing between unprocessed and processed red meat

The most robust and reliable evidence to date of how unprocessed and processed red meat consumption may influence risk of cardio-metabolic diseases comes from the Harvard Medical School meta-analysis. The findings of different relationships of unprocessed versus processed red meat (bacon, hot dogs, salami etc.) consumption with coronary heart disease and type-2 diabetes (no effect of unprocessed red meat but increased risk with processed red meat, as outlined above) underscore the need to better characterize which particular components of meats that may increase cardio-metabolic risk 9. The Harvard researchers also criticized the World Cancer Research Fund – American Institute for Cancer Research statement that both red and processed meat consumption increases colorectal cancer (see above), because they didn’t distinguish between processed and unprocessed red meat 9.

At least in the United States, where most of the studies have been performed, processed meats contain, on average, similar saturated fat and lower cholesterol and heme iron compared with red meats, suggesting that differences in these constituents may not account for different associations with disease risk 9. This is a very important fact because both saturated fat, cholesterol and heme iron have been condemned for being the “meat evils”. From this data, we can draw the following conclusions:

1.) Unprocessed red meat per see is NOT harmful.

2.) Processed red meat can increase the risk for heart disease and type-2 diabetes, but this is not due to its content of saturated fat, cholesterol or heme iron.

Thus, it is other constituents in processed red meat that are contributing to the observed health risk association.

Processed meats contain preservatives and additives that can increase the risk of cardiovascular disease, type-2 diabetes or cancer. These may include nitrites, nitrates, and heterocyclic amines formed during cooking. Nitrosamines formed during cooking may be toxic to pancreatic cells 39. In addition, advanced glycation end products formed in meat and high fat products through heating and processing have been associated with insulin resistance in mice, and with diabetes complications in humans 40.
In particular, nitrates and their byproducts (eg, peroxynitrite) promote atherosclerosis and vascular dysfunction, reduce insulin secretion, and impair glucose tolerance, and streptozotocin, a nitrosamine-related compound, is a known diabetogenic compound. In observational studies in children, nitrites and nitrous compounds are associated with type 1 diabetes mellitus 41, 42, and nitrite concentrations in adults have been used as a biomarker of endothelial dysfunction 43 and impaired insulin resistance 44. However, the types of foods that are commonly replaced when individuals consume unprocessed versus processed meats could also account for their different associations with risk 9. Ask yourself if you are more likely to eat veggies with a piece of steak, or with a hot dog, bacon and egg combo, or a salami meal…?

The meat and potato war…

I want to bring up another point showing that red meat has been unfairly attacked. While meat is blamed for generating risky heterocyclic amines during high temperature cooking (for example over open flames), nobody talk about the high levels of acrylamide that are formed during the frying, roasting, or baking of carbohydrate rich foods, especially potatoes and cereal products 45, 46. And acrylamide possesses a range of hazardous effects and is known to induce carcinogenicity, genotoxicity, neurotoxicity and reproductive toxicity 45.

Let’s take a look at the average daily intakes for heterocyclic amines (from red meat) and acrylamide (from potatoes and cereals):

Average daily intakes for heterocyclic amines is in the range 2.5 – 26 ng/kg body weight/day 47-49.

Average daily intakes for acrylamide is in the range 370-490 ng/kg body weight/day 50, 51

This clearly shows that acrylamide intakes are 20 to 150 times higher than that of heterocyclic amines! Makes me wonder if the potato and celery industry has some lobbying going behind the public health recommendations that urge us to lower our red meat intake…

Red meat and fat intake

Many people avoid red meat because of its total fat, saturated fat and cholesterol content. In an upcoming article I critically examine and explain the flaws in the diet-heart hypothesis (ie, the presumed link between saturated fat intake and cardiovascular disease) that has led to the long-standing public health recommendations for limiting saturated fat intake as a means to prevent cardiovascular disease. If you are more concerned about the purported fat intake – obesity relation, check out my other article on meat and fat loss. As illustrated by the popularity of low-carb, high-fat diets (also a topic for another article) your fat intake will not automatically make you fat. For those of you who still have dietary fat phobia, here are the hard facts.

The fat content and fatty acid profile in red meat is often misunderstood. The first thing to note is that most of the fat can easily be trimmed off before cooking. There is confusion among consumers about the impact of lean meat and meat fat on human health, because it is commonly, but incorrectly thought that lean meat tissue has the same saturated fat content as the visible fat of meat. Once visible fat is trimmed, lean red meat often contains less than 5-10% lipid 52. And in high quality lean red meats, like the ones you can find at Eat To Grow, there is very little fat marbling within the meat. Lean meat is relatively higher in polyunsaturated fat and lower in saturated fat compared with the visible fat of meat 52. The saturated fat content of lean red meat is less than 2-3g/100g (3.5 oz) lean red meat (for example in Eat To Grow’s flank steak and beef tenderloin) compared with more than 37g/100g (3.5 oz) of visible fat from red meat. Eat To Grow’s meat cuts are also very low in cholesterol.
The main fat in lean meat tissue is in phospholipid form, which makes up the major portion of the cell membrane structure, and these are rich in polyunsaturated fats 53. The other main fat in lean meat is the “regular” fat (more precisely known as triglyceride or triacylglycerol) which is predominantly saturated and monounsaturated fat 53. The phospholipid fat in lean red meat is relatively constant and independent of the total fat content, whilst the content of “regular” fat increases as the total fat level increases 54. Therefore, as the total fat content of lean red meat increases there is an increase in saturated and monounsaturated fat content. In other words, the fatty acid composition of meat depends on the total lipid content of the meat 53-56.

In lean beef, over half and up to 70% of fatty acids are monounsaturated or polyunsaturated, which are the types recommended by health professional and government agencies such as the American Heart Association and the Dietary Guidelines for Americans 57, 58. Also, one-third of the saturated fat in red meat is stearic acid, which, unlike other long-chain saturated fatty acids, is neutral in its effects on blood cholesterol levels in humans 59, 60.

Lean beef contains around 10 g total fat (you can find even leaner cuts at Eat To Grow), no more than 4.5 g of saturated fat, and less than 95 mg cholesterol per 3-ounce serving 61. This fat profile readily fits into a heart-healthy diet. Based on the American Heart Association’s dietary fat recommendations, the total, saturated fat and cholesterol intake goals are 30%, 10%, and 300 mg, respectively 57. For an average person consuming a 2,000 calorie diet, the numbers will be 67 g total fat and 22 g saturated fat/day. As noted above, a 3-ounce serving of lean beef contains levels of total and saturated fat well below these limits, and cholesterol levels below the recommendation of <300 mg/day.

You could fit in 3-4 lean meat servings per day and still be within those targets. And there is overwhelming evidence showing that lean red meat is as effective as chicken in blood cholesterol lowering diets, and therefore has a well deserved place in diets for cholesterol and lipid control 52, 62-65.

The good side of meat – health promoting nutrients

The inordinate focus on red meat as the evil has distracted attention from its unique nutritional characteristics, which contribute to a healthy diet.

Meat is not only composed of fat and protein; it also contains essential nutrients which appear exclusively in meat (vitamin A, vitamin B12) and micronutrients for which meat is the major source because of either high concentrations or better bioavailability (folate, iron, selenium, zinc) 19, 66-69. In particular, vitamin A, folate and selenium are reported to be cancer-preventive 19, 66.

Red meat being the major source of vitamin B12 is especially notable because vitamin B12, together with folate and vitamin B6 (also found in ample amounts in red meat), is required by the methylation cycle, which keeps the level of homocysteine under control. Homocysteine is not only a risk factor for cardiovascular disease 70-72, but also for cognitive decline and dementia 73-76 and vascular injury 77. Thus, getting all these three vitamins in a highly bioavaliable form in one single food is a pretty good deal. An interesting effect of homocysteine is that it inhibits NO (nitric oxide) production in blood vessels and contributes to vascular dysfunction 78-80. NO is an essential vasodilatory molecule and many supplements are marketed as being NO-boosters (I will save a discussion about those supps for another article). The take home here is that by eating red meat you will ensure to cover you vitamin requirements for preventing homocysteine levels to rise, and thereby avoid the homocysteine-induced NO synthesis inhibition.

Also, the iron in meat is in an especially highly bioavaliable form called heme iron, which is much more bioavailable than non-haem iron found in plant sources67, 69, 81-83. Red meat in particular is recognized as a significant source of hem iron compared to poultry and fish 84. Iron is vital for many cellular processes in the body and, as a component of hemoglobin, is essential to maintaining adequate transport of oxygen in the blood. Therefore, even mild suboptimal status before the onset of anemia can negatively impact health 85. Iron-deficiency anemia is a major nutritional deficiency, being particularly prevalent among children and young women 85. Therefore, cutting out or lowering meat intakes could have a seriously negative impact on iron status and increase the risk for anemia.

Meat is a also a good source of vitamin D 69. In particular, the vitamin D metabolite 25-hydroxycholecalciferol [25(OH)D3] is found in significant quantities in meat and liver and is assumed to have a high biological activity, resulting in better and faster absorption from the diet compared with its parent compound 86. Furthermore, it has been suggested that components of meat protein may enhance the utilization of vitamin D in humans, particularly where exposure to sunshine is limited 87.
In addition, meat is a good source of choline, taurine, carnosine, coenzyme Q10, creatine and glutathione 88, 89. Glutathione levels in red meat are estimated to be 12-26mg/100g in beef 90 and most meats contain approximately twice the level of glutathione of poultry and up to ten times the content found in fish 88.

Conclusion

Red meat, when part of healthy diet combined with regular exercise, does not pose any harm. Actually, in this context, red meat, thanks to it providing high quality protein together with valuable nutrients, is actually a very sound strategy for both health promotion, sports performance and muscle growth. The scientific reports on the detrimental health effects of red meat have to be interpreted with their methodological flaws in mind, and evaluated against the background diet. The meat-potato war clearly illustrates this. Also, there is compelling evidence showing that the supply of beneficial protective dietary factors, and people’s lifestyles, are probably more important that our red meat intake per see.

While high-heat food preparation causes formation of cancer-promoting substances, meat also contains cancer-protecting nutrients (vitamin A, folate and selenium). The latter can be optimized by a diet rich in fruit and vegetables, which contain a myriad of bioactive cancer-protective substances. Also, the amount of cooking dependent cancer-promoting substances can be reduced by avoiding open flame grilling and well done meats.

So the answer the question in the title “have we been blaming the wrong thing?” = YES!

Looking at all the scientific evidence, it is safe to say that the most appropriate conclusion to be drawn is that it is laziness, manifested as lack of regular physical activity, and lack of veggies that are the culprits behind the associations, and not the red meat!

Meat is a popular food especially among bodybuilders and strength athletes. Taking into consideration the intense training regimens these individuals partake in, if you are one of them, or if you train regularly just for health promotion, you have nothing to fear. To the contrary, thanks to the high quality protein red meat supplies, eating it together with your veggies is a smart strategy to build muscle, increase performance, and improve your health. For those who are concerned about preservatives or cattle chemicals, there are great high quality meat options. If you want to pump your muscles like the pros with high quality meat that hasn’t been pumped, get some from Eat To Grow!

www.trainergize.com

About the Author:
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Monica Mollica has a Bachelor’s and Master’s degree in Nutrition from the University of Stockholm, Sweden, and is an ISSA Certified Personal Trainer. She works a dietary consultant, health journalist and writer for www.BrinkZone.com, and is also a web designer and videographer.

Monica has admired and been fascinated by muscular and sculptured strong athletic bodies since childhood, and discovered bodybuilding as an young teenager. Realizing the importance of nutrition for maximal results in the gym, she went for a BSc and MSc with a major in Nutrition at the University.

During her years at the University she was a regular contributor to the Swedish bodybuilding magazine BODY, and she has published the book (in Swedish) “Functional Foods for Health and Energy Balance”, and authored several book chapters in Swedish publications.

It was her insatiable thirst for knowledge and scientific research in the area of bodybuilding and health that brought her to the US. She has completed one semester at the PhD-program “Exercise, Nutrition and Preventive Health” at Baylor University Texas, at the department of Health Human Performance and Recreation, and worked as an ISSA certified personal trainer. Today, Monica is sharing her solid experience by doing dietary consultations and writing about topics related to health, fitness, bodybuilding, anti-aging and longevity.

References:

1. Hu FB, Stampfer MJ, Manson JE, et al. Dietary saturated fats and their food sources in relation to the risk of coronary heart disease in women. The American journal of clinical nutrition. 1999;70(6):1001-1008.

2. Hu FB, Rimm EB, Stampfer MJ, et al. Prospective study of major dietary patterns and risk of coronary heart disease in men. The American journal of clinical nutrition. 2000;72(4):912-921.

3. Menotti A, Kromhout D, Blackburn H, et al. Food intake patterns and 25-year mortality from coronary heart disease: cross-cultural correlations in the Seven Countries Study. The Seven Countries Study Research Group. European journal of epidemiology. 1999;15(6):507-515.

4. Pan A, Sun Q, Bernstein AM, et al. Red meat consumption and mortality: results from 2 prospective cohort studies. Archives of internal medicine. 2012;172(7):555-563.

5. Kelemen LE, Kushi LH, Jacobs DR, Jr., et al. Associations of dietary protein with disease and mortality in a prospective study of postmenopausal women. American journal of epidemiology. 2005;161(3):239-249.

6. Steffen LM, Kroenke CH, Yu X, et al. Associations of plant food, dairy product, and meat intakes with 15-y incidence of elevated blood pressure in young black and white adults: the Coronary Artery Risk Development in Young Adults (CARDIA) Study. The American journal of clinical nutrition. 2005;82(6):1169-1177; quiz 1363-1164.

7. Chao A, Thun MJ, Connell CJ, et al. Meat consumption and risk of colorectal cancer. JAMA : the journal of the American Medical Association. 2005;293(2):172-182.

8. (WCRF/AICR) WCRFAIfCR. Food, nutrition and the prevention of cancer: A global perspective. Washington, DC:: American Institute for Cancer Research 2007.

9. 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(21):2271-2283.

10. Iqbal R, Anand S, Ounpuu S, et al. Dietary patterns and the risk of acute myocardial infarction in 52 countries: results of the INTERHEART study. Circulation. 2008;118(19):1929-1937.

11. Panagiotakos D, Pitsavos C, Chrysohoou C, et al. Dietary patterns and 5-year incidence of cardiovascular disease: a multivariate analysis of the ATTICA study. Nutrition, metabolism, and cardiovascular diseases : NMCD. 2009;19(4):253-263.

12. van Dam RM, Grievink L, Ocke MC, et al. Patterns of food consumption and risk factors for cardiovascular disease in the general Dutch population. The American journal of clinical nutrition. 2003;77(5):1156-1163.

13. Zyriax BC, Algenstaedt P, Hess UF, et al. Factors contributing to the risk of cardiovascular disease reflected by plasma adiponectin: data from the coronary risk factors for atherosclerosis in women (CORA) study. Atherosclerosis. 2008;200(2):403-409.

14. Kontogianni MD, Panagiotakos DB, Pitsavos C, et al. Relationship between meat intake and the development of acute coronary syndromes: the CARDIO2000 case-control study. European journal of clinical nutrition. 2008;62(2):171-177.

15. Heidemann C, Schulze MB, Franco OH, et al. Dietary patterns and risk of mortality from cardiovascular disease, cancer, and all causes in a prospective cohort of women. Circulation. 2008;118(3):230-237.

16. Mozaffarian D, Appel LJ, Van Horn L. Components of a cardioprotective diet: new insights. Circulation. 2011;123(24):2870-2891.

17. Harriss LR, English DR, Powles J, et al. Dietary patterns and cardiovascular mortality in the Melbourne Collaborative Cohort Study. The American journal of clinical nutrition. 2007;86(1):221-229.

18. Guallar-Castillon P, Rodriguez-Artalejo F, Tormo MJ, et al. Major dietary patterns and risk of coronary heart disease in middle-aged persons from a Mediterranean country: the EPIC-Spain cohort study. Nutrition, metabolism, and cardiovascular diseases : NMCD. 2012;22(3):192-199.

19. Biesalski HK. Meat and cancer: meat as a component of a healthy diet. European journal of clinical nutrition. 2002;56 Suppl 1:S2-11.

20. (WCRF) WCRF. Food, nutrition, physical activity, and the prevention of cancer 2007.

21. Truswell AS. Problems with red meat in the WCRF2. The American journal of clinical nutrition. 2009;89(4):1274-1275; author reply 1275-1276.

22. Boyle P, Boffetta P, Autier P. Diet, nutrition and cancer: public, media and scientific confusion. Annals of oncology : official journal of the European Society for Medical Oncology / ESMO. 2008;19(10):1665-1667.

23. Hill M. Meat, cancer and dietary advice to the public. European journal of clinical nutrition. 2002;56 Suppl 1:S36-41.

24. Hill MJ. Meat and colo-rectal cancer. The Proceedings of the Nutrition Society. 1999;58(2):261-264.

25. McAfee AJ, McSorley EM, Cuskelly GJ, et al. Red meat consumption: an overview of the risks and benefits. Meat science. 2010;84(1):1-13.

26. Alaejos MS, Gonzalez V, Afonso AM. Exposure to heterocyclic aromatic amines from the consumption of cooked red meat and its effect on human cancer risk: a review. Food additives & contaminants Part A, Chemistry, analysis, control, exposure & risk assessment. 2008;25(1):2-24.

27. Bingham SA, Hughes R, Cross AJ. Effect of white versus red meat on endogenous N-nitrosation in the human colon and further evidence of a dose response. The Journal of nutrition. 2002;132(11 Suppl):3522S-3525S.

28. Butler LM, Sinha R, Millikan RC, et al. Heterocyclic amines, meat intake, and association with colon cancer in a population-based study. American journal of epidemiology. 2003;157(5):434-445.

29. Shin A, Shrubsole MJ, Ness RM, et al. Meat and meat-mutagen intake, doneness preference and the risk of colorectal polyps: the Tennessee Colorectal Polyp Study. International journal of cancer Journal international du cancer. 2007;121(1):136-142.

30. Wu K, Giovannucci E, Byrne C, et al. Meat mutagens and risk of distal colon adenoma in a cohort of U.S. men. Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology. 2006;15(6):1120-1125.

31. Willett WC. Diet, nutrition, and avoidable cancer. Environmental health perspectives. 1995;103 Suppl 8:165-170.

32. Hirayama T. Life Style and Mortality 1990.

33. van Duijnhoven FJ, Bueno-De-Mesquita HB, Ferrari P, et al. Fruit, vegetables, and colorectal cancer risk: the European Prospective Investigation into Cancer and Nutrition. The American journal of clinical nutrition. 2009;89(5):1441-1452.

34. Aune D, Ursin G, Veierod MB. Meat consumption and the risk of type 2 diabetes: a systematic review and meta-analysis of cohort studies. Diabetologia. 2009;52(11):2277-2287.

35. Villegas R, Shu XO, Gao YT, et al. The association of meat intake and the risk of type 2 diabetes may be modified by body weight. International journal of medical sciences. 2006;3(4):152-159.

36. Heroux M, Janssen I, Lam M, et al. Dietary patterns and the risk of mortality: impact of cardiorespiratory fitness. International journal of epidemiology. 2010;39(1):197-209.

37. Lee DC, Artero EG, Sui X, et al. Mortality trends in the general population: the importance of cardiorespiratory fitness. J Psychopharmacol. 2010;24(4 Suppl):27-35.

38. Kodama S, Saito K, Tanaka S, et al. Cardiorespiratory fitness as a quantitative predictor of all-cause mortality and cardiovascular events in healthy men and women: a meta-analysis. JAMA : the journal of the American Medical Association. 2009;301(19):2024-2035.

39. LeDoux SP, Woodley SE, Patton NJ, et al. Mechanisms of nitrosourea-induced beta-cell damage. Alterations in DNA. Diabetes. 1986;35(8):866-872.

40. Peppa M, Goldberg T, Cai W, et al. Glycotoxins: a missing link in the “relationship of dietary fat and meat intake in relation to risk of type 2 diabetes in men”. Diabetes care. 2002;25(10):1898-1899.

41. Parslow RC, McKinney PA, Law GR, et al. Incidence of childhood diabetes mellitus in Yorkshire, northern England, is associated with nitrate in drinking water: an ecological analysis. Diabetologia. 1997;40(5):550-556.

42. Virtanen SM, Jaakkola L, Rasanen L, et al. Nitrate and nitrite intake and the risk for type 1 diabetes in Finnish children. Childhood Diabetes in Finland Study Group. Diabetic medicine : a journal of the British Diabetic Association. 1994;11(7):656-662.

43. Kleinbongard P, Dejam A, Lauer T, et al. Plasma nitrite concentrations reflect the degree of endothelial dysfunction in humans. Free radical biology & medicine. 2006;40(2):295-302.

44. Pereira EC, Ferderbar S, Bertolami MC, et al. Biomarkers of oxidative stress and endothelial dysfunction in glucose intolerance and diabetes mellitus. Clinical biochemistry. 2008;41(18):1454-1460.

45. Carere A. Genotoxicity and carcinogenicity of acrylamide: a critical review. Annali dell’Istituto superiore di sanita. 2006;42(2):144-155.

46. Felton JS, Knize MG. A meat and potato war: implications for cancer etiology. Carcinogenesis. 2006;27(12):2367-2370.

47. Layton DW, Bogen KT, Knize MG, et al. Cancer risk of heterocyclic amines in cooked foods: an analysis and implications for research. Carcinogenesis. 1995;16(1):39-52.

48. Zimmerli B, Rhyn P, Zoller O, et al. Occurrence of heterocyclic aromatic amines in the Swiss diet: analytical method, exposure estimation and risk assessment. Food additives and contaminants. 2001;18(6):533-551.

49. Augustsson K, Skog K, Jagerstad M, et al. Assessment of the human exposure to heterocyclic amines. Carcinogenesis. 1997;18(10):1931-1935.

50. Konings EJ, Baars AJ, van Klaveren JD, et al. Acrylamide exposure from foods of the Dutch population and an assessment of the consequent risks. Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association. 2003;41(11):1569-1579.

51. Dybing E, Sanner T. Risk assessment of acrylamide in foods. Toxicological sciences : an official journal of the Society of Toxicology. 2003;75(1):7-15.

52. Li D, Siriamornpun S, Wahlqvist ML, et al. Lean meat and heart health. Asia Pacific journal of clinical nutrition. 2005;14(2):113-119.

53. Sinclair AJ, Slattery WJ, O’Dea K. The analyses of polyunsaturated fatty acids in meat by capillary gas liquid chromatography. . Journal of the science of food and agriculture. 1982;33:771-776.

54. Sinclair AJ, O’Dea K. The lipid levels and fatty acid compositions of the lean portions of Australian beef and lamb. . Food Technol Aust. 1987;35:228-231.

55. McDonald IW, Scott TW. Foods of ruminant origin with elevated content of polyunsaturated fatty acids. World review of nutrition and dietetics. 1977(26):144-207.

56. Hornstein L, Crowe PF, Hiner R. Composition of lipids in some beef muscles. Journal of food science. 1967;32:650-655.

57. Krauss RM, Eckel RH, Howard B, et al. AHA Dietary Guidelines: revision 2000: A statement for healthcare professionals from the Nutrition Committee of the American Heart Association. Stroke; a journal of cerebral circulation. 2000;31(11):2751-2766.

58. U.S. Department of Health and Human Services USDoA. Dietary Guidelines for Americans, 2005. 2005.

59. Kris-Etherton PM, Griel AE, Psota TL, et al. Dietary stearic acid and risk of cardiovascular disease: intake, sources, digestion, and absorption. Lipids. 2005;40(12):1193-1200.

60. Hunter JE, Zhang J, Kris-Etherton PM. Cardiovascular disease risk of dietary stearic acid compared with trans, other saturated, and unsaturated fatty acids: a systematic review. The American journal of clinical nutrition. 2010;91(1):46-63.

61. U.S. Department of Agriculture ARS. USDA Nutrient Database for Standard Reference. 2006.

62. Davidson MH, Hunninghake D, Maki KC, et al. Comparison of the effects of lean red meat vs lean white meat on serum lipid levels among free-living persons with hypercholesterolemia: a long-term, randomized clinical trial. Archives of internal medicine. 1999;159(12):1331-1338.

63. Melanson K, Gootman J, Myrdal A, et al. Weight loss and total lipid profile changes in overweight women consuming beef or chicken as the primary protein source. Nutrition. 2003;19(5):409-414.

64. Mann N. Dietary lean red meat and human evolution. European journal of nutrition. 2000;39(2):71-79.

65. Cordain L, Eaton SB, Miller JB, et al. The paradoxical nature of hunter-gatherer diets: meat-based, yet non-atherogenic. European journal of clinical nutrition. 2002;56 Suppl 1:S42-52.

66. Ferguson LR. Meat and cancer. Meat science. 2010;84(2):308-313.

67. Cosgrove M, Flynn A, Kiely M. Consumption of red meat, white meat and processed meat in Irish adults in relation to dietary quality. The British journal of nutrition. 2005;93(6):933-942.

68. Davey GK, Spencer EA, Appleby PN, et al. EPIC-Oxford: lifestyle characteristics and nutrient intakes in a cohort of 33 883 meat-eaters and 31 546 non meat-eaters in the UK. Public health nutrition. 2003;6(3):259-269.

69. Wyness L, Weichselbaum E, O’Connor A, et al. Red meat in the diet: an update. Nutrition Bulletin. 2011;36:34-77.

70. Scott JM. Folate and vitamin B12. The Proceedings of the Nutrition Society. 1999;58(2):441-448.

71. Yilmaz N. Relationship between paraoxonase and homocysteine: crossroads of oxidative diseases. Archives of medical science : AMS. 2012;8(1):138-153.

72. McCully KS. Homocysteine, vitamins, and vascular disease prevention. The American journal of clinical nutrition. 2007;86(5):1563S-1568S.

73. Selhub J, Troen A, Rosenberg IH. B vitamins and the aging brain. Nutrition reviews. 2010;68 Suppl 2:S112-118.

74. Vogel T, Dali-Youcef N, Kaltenbach G, et al. Homocysteine, vitamin B12, folate and cognitive functions: a systematic and critical review of the literature. International journal of clinical practice. 2009;63(7):1061-1067.

75. Haan MN, Miller JW, Aiello AE, et al. Homocysteine, B vitamins, and the incidence of dementia and cognitive impairment: results from the Sacramento Area Latino Study on Aging. The American journal of clinical nutrition. 2007;85(2):511-517.

76. Tucker KL, Qiao N, Scott T, et al. High homocysteine and low B vitamins predict cognitive decline in aging men: the Veterans Affairs Normative Aging Study. The American journal of clinical nutrition. 2005;82(3):627-635.

77. Upchurch GR, Jr., Welch GN, Loscalzo J. Homocysteine, EDRF, and endothelial function. The Journal of nutrition. 1996;126(4 Suppl):1290S-1294S.

78. Stuhlinger MC, Tsao PS, Her JH, et al. Homocysteine impairs the nitric oxide synthase pathway: role of asymmetric dimethylarginine. Circulation. 2001;104(21):2569-2575.

79. Dayal S, Lentz SR. ADMA and hyperhomocysteinemia. Vasc Med. 2005;10 Suppl 1:S27-33.

80. Stuhlinger MC, Oka RK, Graf EE, et al. Endothelial dysfunction induced by hyperhomocyst(e)inemia: role of asymmetric dimethylarginine. Circulation. 2003;108(8):933-938.

81. Wheby MS, Suttle GE, Ford KT, 3rd. Intestinal absorption of hemoglobin iron. Gastroenterology. 1970;58(5):647-654.

82. Hazell T, Ledward DA, Neale RJ. Iron availability from meat. The British journal of nutrition. 1978;39(3):631-638.

83. Layrisse M, Cook JD, Martinez C, et al. Food iron absorption: a comparison of vegetable and animal foods. Blood. 1969;33(3):430-443.

84. Johnston J, Prynne CJ, Stephen AM, et al. Haem and non-haem iron intake through 17 years of adult life of a British Birth Cohort. The British journal of nutrition. 2007;98(5):1021-1028.

85. Gibson S, Ashwell M. The association between red and processed meat consumption and iron intakes and status among British adults. Public health nutrition. 2003;6(4):341-350.

86. Groff J, Gropper S, Junt S. Advanced Nutrition and Human Metabolism. Minneapolis/St Paul, MN: West Publishing Co. 1995.

87. Dunnigan MG, Henderson JB. An epidemiological model of privational rickets and osteomalacia. The Proceedings of the Nutrition Society. 1997;56(3):939-956.

88. Williams P. Nutritional composition of red meat. Nutrition & Dietetics. 2007;64:S113-S119.

89. Purchas RW, Rutherfurd SM, Pearce PD, et al. Concentrations in beef and lamb of taurine, carnosine, coenzyme Q(10), and creatine. Meat science. 2004;66(3):629-637.

90. Jones DP, Coates RJ, Flagg EW, et al. Glutathione in foods listed in the National Cancer Institute’s Health Habits and History Food Frequency Questionnaire. Nutr Cancer. 1992;17(1):57-75.  


  

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