Caveats for the Good and Bad of Dietary Red Meat
Abstract
:1. Introduction
2. Iron, Heme and Oxidative Injury
3. Meat, Iron, and Food Processing
4. Population Studies with Correlations between Red Meat Consumption and Chronic Diseases
5. Good and Bad Bacteria in Healthy Gut, Role of Iron
6. Significance of Dietary Antioxidants
7. Impact of Dietary Antioxidants and Gut Bacteria
8. Conclusion and Future Direction for Research
9. Addendum
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Cordain, L.; Eaton, S.B.; Miller, J.B.; Mann, N.; Hill, K. The paradoxical nature of hunter-gatherer diets: Meat-based, yet non-atherogenic. Eur. J. Clin. Nutr. 2002, 56, 42–52. [Google Scholar] [CrossRef]
- Lafarga, T.; Hayes, M. Bioactive peptides from meat muscle and by products: Generation, functionality and application as functional ingredients. Meat Sci. 2014, 98, 227–239. [Google Scholar] [CrossRef]
- Zhang, X.; Giovannucci, E.L.; Smith-Warner, S.A.; Wu, K.; Fuchs, C.S.; Pollak, M.; Willett, W.C.; Ma, J.A. Prospective study of intakes of zinc and heme iron and colorectal cancer risk in men and women. Cancer Cause Control 2011, 22, 1627–1637. [Google Scholar] [CrossRef] [PubMed]
- Herbert, V. Vitamin B12: Plant sources, requirements and assay. Am. J. Clin. Nutr. 1998, 48, 852–858. [Google Scholar] [CrossRef] [PubMed]
- Mann, N. Dietary lean red meat and human evolution. Eur. J. Nutr. 2000, 39, 71–79. [Google Scholar] [CrossRef] [PubMed]
- Mann, N. A brief history of meat in the human diet and current health implications. Meat Sci. 2018, 144, 169–179. [Google Scholar] [CrossRef] [PubMed]
- Pasricha, S.-R. Anemia: A comprehensive global estimate. Blood 2014, 123, 611–612. [Google Scholar] [CrossRef] [PubMed]
- Tappel, A. Heme of consumed red meat can act as a catalyst of oxidative damage and could initiate colon, breast and prostate cancers, heart disease and other diseases. Med. Hypotheses 2007, 68, 562–564. [Google Scholar] [CrossRef]
- Skaar, E.P. The battle for iron between bacterial pathogens and their vertebrate hosts. PLoS Pathog. 2010, 6, e1000949. [Google Scholar] [CrossRef]
- Bresgen, N.; Eckl, P.M. Oxidative stress and the homeodynamics of iron metabolism. Biomolecules 2015, 5, 808–847. [Google Scholar] [CrossRef]
- Brambilla, G.; Martelli, A. Genotoxic and carcinogenic risk to humans of drug-nitrite interaction products. Mutat Res. 2007, 635, 17–52. [Google Scholar] [CrossRef] [PubMed]
- Bingham, S.A.; Hughes, R.; Cross, A.J. Effect of white versus red meat on endogenous N-nitrosation in the human colon and further evidence of a dose response. J. Nutr. 2002, 132, 3522S–3525S. [Google Scholar] [CrossRef] [PubMed]
- Pierre, F.; Santarelli, R.; Taché, S.; Guéraud, F.; Corpet, D.E. Beef meat promotion of dimethylhydrazine-induced colorectal carcinogenesis biomarkers is suppressed by dietary calcium. Br. J. Nutr. 2008, 99, 1000–1006. [Google Scholar] [CrossRef] [PubMed]
- Rohrmann, S.; Zoller, D.; Hermann, S.; Linseisen, J. Intakes of heterocyclic aromatic amines from meats in the European Prospective into Cancer and Nutrition. Br. J. Nutr. 2006, 98, 1112–1115. [Google Scholar] [CrossRef]
- Augustsson, K.; Kerstin, S.; Margaretha, J.; Dickman, P.W.; Steineck, G. Dietary heterocyclic amines and cancer of the colon, rectum, bladder, and kidney: A population based study. Lancet 1999, 353, 703–707. [Google Scholar] [CrossRef]
- Ollberding, J.J.; Wilkens, L.R.; Henderson, B.E.; Kolonel, L.N.; Marchand, L.L. Meat consumption, heterocyclic amines and colorectal cancer risk: The multiethnic cohort study. Int. J. Cancer Res. 2012, 131, E1125–E1133. [Google Scholar] [CrossRef]
- Clarke, R.E.; Dordevic, A.L.; Tan, S.M.; Ryan, L.; Coughlan, M.T. Dietary advanced glycation and products and risk factors for chronic disease: A systematic review of randomized controlled trials. Nutrients 2016, 8, 125. [Google Scholar] [CrossRef]
- Turesky, R.J. Formation and biochemistry of carcinogenic heterocyclic aromatic amines in cooked meats. Toxicol. Lett. 2007, 168, 219–227. [Google Scholar] [CrossRef]
- Skog, K.I.; Johansson, M.A.; Jagerstad, M.I. Carcinogenic heterocyclic amines in model systems and cooked foods: A review on formation, occurrence and intake. Food Chem. Toxicol. 1998, 36, 9–10. [Google Scholar] [CrossRef]
- Lorenzo, J.M.; Purrinos, L.; Garcia Fontan, M.C.; Franco, D. Polycyclic aromatic hydrocarbons (PAH) in two Spanish traditional smoked sausage varieties “Androlla” and “Botillo”. Meat Sci. 2010, 86, 660–664. [Google Scholar] [CrossRef]
- Pohlmann, M.; Hitzel, A.; Schwagele, F.; Speer, K.; Wolfgang, J. Contents of polycyclic aromatic hydrocarbons (PAH) and phenolic substances in Frankfurter-type sausages depending on smoking conditions using glow smoke. Meat Sci. 2012, 96, 2760184. [Google Scholar] [CrossRef] [PubMed]
- Lorenzo, J.M.; Purriños, L.; Bermudez, R.; Cobas, N.; Figueiredo, M.; Fontán, M.C.G. Polycyclic aromatic hydrocarbons (PAHs) in two Spanish traditional smoked sausage varieties: “Chorizo gallego” and “Chorizo de cebolla. ” Meat Sci. 2011, 89, 105–109. [Google Scholar] [CrossRef] [PubMed]
- Bastide, N.M.; Pierre, F.H.F.; Corpet, D.E. Heme iron from meat and risk of colorectal cancer: A meta-analysis and review of mechanisms involved. Cancer Prev. Res. 2011, 4, 177–184. [Google Scholar] [CrossRef] [PubMed]
- Egeberg, R.; Olsen, A.; Christensen, J.; Halkjaer, J.; Jacobsen, M.U.; Overvad, K.; Tjonneland, A. Association between red meat and risks for colon and rectal cancer depend on the type of red meat consumed. J. Nutr. 2013, 143, 464–472. [Google Scholar] [CrossRef]
- Willett, W.C. Diet and cancer. Oncologist 2000, 5, 394–404. [Google Scholar] [CrossRef]
- de Oliveira Otto, M.C.; Alonso, A.; Lee, K.-H.; Delclos, G.L.; Bertoni, A.G.; Jiang, R.; Lima, J.A.; Symanski, E.; Jacobs, D.R., Jr.; Nettleton, J.A. Dietary Intakes of Zinc and Heme Iron from Red Meat, but Not from Other Sources, Are Associated with Greater Risk of Metabolic Syndrome and Cardiovascular Disease. J. Nutr. 2012, 142, 526–533. [Google Scholar] [CrossRef]
- Qiao, L.; Feng, Y. Intakes of heme iron and zinc and colorectal cancer incidence: A meta-analysis of prospective studies. Cancer Cause Control 2013, 24, 1175–1183. [Google Scholar] [CrossRef]
- Alavanja, M.C.R.; Field, R.W.; Sinha, R. Lung cancer risk and red meat consumption among Iowa women. Lung Cancer 2001, 34, 37–46. [Google Scholar] [CrossRef]
- Schulze, M.B.; Manson, J.E.; Willett, W.X.; Hu, F.B. Processed meat intake and incidence of Type 2 diabetes in younger and middle-aged women. Diabetologia 2003, 46, 1465–1473. [Google Scholar] [CrossRef]
- Song, Y.; Mason, J.E.; Buring, J.E.; Liu, S. A prospective study of red meat consumption and type 2 diabetes in middle-aged and elderly women: The women’s health study. Diabetes Care 2004, 27, 2108–2115. [Google Scholar] [CrossRef]
- Diallo, A.; Deschasaux, M.; Partula, V.; Latino-Martel, P.; Srour, B.; Hercberg, S.; Galan, P.; Fassier, P.; Guéraud, F.; Pierre, F.H.; et al. Dietary iron intake and breast cancer risk: Modulation by an antioxidant supplementation. Oncotarget 2016, 7, 79008–79016. [Google Scholar] [CrossRef] [PubMed]
- Bouvard, V.; Loomis, D.; Guyton, K.Z.; Grosse, Y.; El Ghissassi, F.; Benbrahim-Talloa, L.; Guha, N.; Mattock, H.; Straif, K. Carcinogenicity of consumption of red and processed meat. Lancet 2015, 16, 1599–1600. [Google Scholar] [CrossRef] [Green Version]
- Boyle, P.; Boffetta, P.; Autier, P. Diet, nutrition and cancer: Public, media and scientific confusion. Ann. Oncol. 2008, 19, 1665–1667. [Google Scholar] [CrossRef] [PubMed]
- Truswell, A.S. Problems with red meat in the WORF2. Am. J. Clin. Nutr. 2009, 89, 1274–1275. [Google Scholar] [CrossRef]
- Alexander, D.D.; Cushing, C.A. Red meat and colorectal cancer: A critical summary of prospective epidemiologic studies. Obes. Rev. 2011, 12, e472–e493. [Google Scholar] [CrossRef]
- Alexander, D.D.; Weed, D.L.; Cushing, C.A.; Lowe, K.A. Meta-analysis of prospective studies of red meat consumption and colorectal cancer. Eur. J. Cancer Prev. 2011, 20, 293–307. [Google Scholar] [CrossRef]
- Alexander, D.D.; Weed, D.L.; Miller, P.E.; Mohamed, M.A. Red meat and colorectal cancer: A quantitative update on the state of epidemiologic science. J. Am. Coll. Nutr. 2015, 34, 521–543. [Google Scholar] [CrossRef] [Green Version]
- Enstrom, J.E. Colorectal cancer and consumption of beef and fat. Br. J. Cancer 1975, 32, 432–439. [Google Scholar] [CrossRef] [Green Version]
- Bylsma, L.C.; Alexander, D.D. A review and meta-analysis of prospective studies of red and processed meat, meat cooking methods, heme iron, heterocyclic amines and prostate cancer. Nutr. J. 2015, 14, 125. [Google Scholar] [CrossRef] [Green Version]
- Ng, O. Iron, microbiota and colorectal cancer. Wien. Med. Wochenschr. 2016, 166, 431–436. [Google Scholar] [CrossRef]
- Sobhani, I.; Tap, J.; Roudot-Thoraval, F.; Roperch, J.P.; Letulle, S.; Langella, P.; Corthier, G.; Tran Van Nhieu, J.; Furet, J.P. Microbial dysbiosis in colorectal cancer (CRC) patients. PLoS ONE 2011, 6, e16393. [Google Scholar] [CrossRef] [PubMed]
- Gold, J.S.; Bayar, S.; Salem, R.R. Association of Streptococcus bovis bacteremia with colonic neoplasia and extra colonic malignancy. Arch. Surg. 2004, 139, 760–765. [Google Scholar]
- Moore, W.E.; Moore, L.H. Intestinal floras of populations that have a high risk of colon cancer. Appl. Environ. Microbiol. 1995, 61, 3202–3207. [Google Scholar] [PubMed]
- Hecke, T.V.; Camp, J.V.; De Smet, S. Oxidation during digestion of meat: Interactions with the diet and Helicobacter pylori gastritis and implications on human health. Compr. Rev. Food Sci. Food Saf. 2017, 16, 214–233. [Google Scholar] [CrossRef] [Green Version]
- Kortman, G.A.M.; Raffatellu, M.; Swinkels, D.W.; Tjalsma, H. Nutritional iron turned inside out: Intestinal stress from gut microbial perspective. FES Microbiol. Rev. 2014, 38, 1202–1234. [Google Scholar] [CrossRef] [Green Version]
- Pantopoulos, K. Inherited disorders of iron overload. Front. Nutr. 2018, 5, 103. [Google Scholar] [CrossRef] [Green Version]
- Toden, S.; Bird, A.R.; Topping, D.L.; Conlon, M.A. High red meat diets induce greater number of colonic DNA double-shared breaks than white meat in rats: Attenuation by high amylose maize starch. Carcinogenesis 2007, 28, 2355–2362. [Google Scholar] [CrossRef]
- Toden, S.; Bird, A.R.; Topping, D.L.; Conlon, M.A. Resistant starch prevent colonic DNA damage induced by high dietary cooked red meat or casein in rats. Cancer Biol. Ther. 2014, 25, 72–79. [Google Scholar] [CrossRef] [Green Version]
- Jaeffi, T.; Kortman, G.A.M.; Moretti, D.; Chassard, C.; Holding, P.; Dostra, A.; Boekhout, J.; Timmerman, H.M.; Swinkels, D.W.; Tjalsma, H.; et al. Iron fortification adversely affects the gut microbiome, increases pathogen abundance and induces intestinal inflammation in Kenyan infants. Gut 2015, 64, 731–742. [Google Scholar]
- Shen, Q.; Chen, Y.A.; Touchy, K.M. A comparative in vitro investigation into the effects of cooked meats on the human fecal microbiota. Anaerobe 2010, 16, 572–577. [Google Scholar] [CrossRef]
- Zhu, Y.; Lin, X.; Li, H.; Li, Y.; Shi, X.; Zhao, F.; Xu, X.; Li, C.; Zhou, G. Intake of meat proteins substantially increased the relative abundance of genus Lactobacillus in rat feces. PLoS ONE 2016, 11, e0152678. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Salvin, J.L.; Lloyd, B. Health benefits of fruits and vegetables. Adv. Nutr. 2012, 3, 506–516. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dagfinn, A.; Giovannucci, E.; Foffetta, P.; Fadnes, L.T.; Norat, T.; Greenwood, D.G.; Riboli, E.; Vatten, L.J.; Tonstad, S. Fruit and vegetable intake and the risk of cardiovascular disease, total cancer and all-cause mortality—A systematic review and dose-response meta-analysis of prospective studies. Int. J. Epidemiol. 2017, 46, 1029–1056. [Google Scholar]
- Carlsen, M.H.; Halvorsen, B.L.; Holte, K.; Bohn, S.K.; Dragland, S.; Sampson, L.; Willey, C.; Senoo, H.; Umezono, Y.; Sanada, C.; et al. The total antioxidant content of more than 3100 foods, beverages, spices, herbs and supplements used worldwide. Nutr. J. 2010, 9, 3. [Google Scholar] [CrossRef] [PubMed]
- Vamanu, E. Polyphenolic nutraceuticals to combat oxidative stress through microbiota modulation. Front Pharmacol. 2019, 10, 402–494. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, S.Y.; Wle, G.A.; Cho, Y.A.; Kang, H.H.; Ryu, K.A.; Yoo, M.K.; Jun, S.; Kim, S.A.; Ha, K.; Kim, J.; et al. The role of red meat and flavonoid consumption on cancer prevention: The Korean cancer screening examination cohort. Nutrients 2017, 9, 938. [Google Scholar] [CrossRef] [Green Version]
- Stocker, R.; Yamamoto, Y.; McDonagh, A.F.; Glazer, A.N.; Ames, B.N. Bilirubin is an antioxidant of possible physiological importance. Science 1987, 235, 1043–1046. [Google Scholar] [CrossRef]
- Takei, R.; Inoue, T.; Sonoda, N.; Ogawa, Y. Bilirubin induces visceral obesity and insulin resistance by suppression of inflammatory cytokines. PLoS ONE 2019, 14, e0223392. [Google Scholar] [CrossRef]
- Martin, O.C.B.; Naud, N.; Taché, S.; Debrauwer, L.; Chevolleau, S.; Dupuy, J.; Chantelauze, C.; Durand, D.; Pujols-Guillot, E.; Blas-Y-Estrada, F.; et al. Targeting colon luminal lipid peroxidation limits colon carcinogenesis associated with red meat consumption. Cancer Prev. Res. 2018, 11, 569–580. [Google Scholar] [CrossRef] [Green Version]
- Bellavia, A.; Stilling, F.; Wolk, A. High red meat intake and all-cause cardiovascular and cancer mortality: Is the risk modified by fruit and vegetable intake? Am. J. Clin. Nutr. 2016, 10, 1137–1143. [Google Scholar] [CrossRef] [Green Version]
- Sasso, A.; Latella, G. Dietary components that counteract the increased risk of colorectal cancer related to red meat consumption. Int. J. Food Sci. Nutr. 2018, 69, 536–548. [Google Scholar] [CrossRef] [PubMed]
- Zeraatkar, D.; Han, M.A.; Guyatt, G.H.; Vernooij, R.W.; El Dib, R.; Cheung, K.; Milio, K.; Zworth, M.; Bartoszko, J.J.; Valli, C.; et al. Red and Processed Meat Consumption and Risk for All-Cause Mortality and Cardiometabolic Outcomes: A Systematic Review and Meta-analysis of Cohort Studies. Ann. Intern. Med. 2019. [Google Scholar] [CrossRef] [PubMed]
- Han, M.A.; Zeraatkar, D.; Guyatt, G.H.; Vernooij, R.W.M.; El Dib, R.; Zhang, Y.; Algarni, A.; Leung, G.; Storman, D.; Valli, C.; et al. Reduction of Red and Processed Meat Intake and Cancer Mortality and Incidence: A Systematic Review and Meta-analysis of Cohort Studies. Ann. Intern. Med. 2019. [Google Scholar] [CrossRef] [PubMed]
- Vernooij, R.W.M.; Zeraatkar, D.; Han, M.A.; El Dib, R.; Zworth, M.; Milio, K.; Sit, D.; Lee, Y.; Gomaa, H.; Valli, C.; et al. Patterns of Red and Processed Meat Consumption and Risk for Cardiometabolic and Cancer Outcomes: A Systematic Review and Meta-analysis of Cohort Studies. Ann. Intern. Med. 2019. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Valli, C.; Montserrat Rabassa, M.; Johnston, B.C.; Kuijpers, R.; Prokop-Dorner, A.; Zajac, J.; Storman, D.; Storman, M.; Bala, M.M.; Solà, I.; et al. Health-Related Values and Preferences Regarding Meat Consumption: A Mixed-Methods Systematic Review. Ann. Intern. Med. 2019. [Google Scholar] [CrossRef] [PubMed]
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Omaye, A.T.; Omaye, S.T. Caveats for the Good and Bad of Dietary Red Meat. Antioxidants 2019, 8, 544. https://doi.org/10.3390/antiox8110544
Omaye AT, Omaye ST. Caveats for the Good and Bad of Dietary Red Meat. Antioxidants. 2019; 8(11):544. https://doi.org/10.3390/antiox8110544
Chicago/Turabian StyleOmaye, Anthony T., and Stanley T. Omaye. 2019. "Caveats for the Good and Bad of Dietary Red Meat" Antioxidants 8, no. 11: 544. https://doi.org/10.3390/antiox8110544