Review on Variants in Genes Associated with Cancer Risk and Red Meat Metabolism
DOI:
https://doi.org/10.6000/1929-5634.2013.02.02.8Keywords:
Red meat, processed meat, heterocyclic amines (HCAs), polycyclic aromatic hydrocarbons (PAHs), N-nitroso compounds (NOCs), cancers, xenobiotic metabolismAbstract
With the advent of human genome sequencing project, came the wave of personalized genomics. Scientists have now gone beyond scanning of individual genes and epigenetic variations that might alter an individual’s predisposition to developing complex diseases. Nutritional genomics is a science which is fast catching up. Efforts to explain the diet-gene interactions often recapitulate the effects of genetic makeup in determining the exact fate of the meal we ate last.
Diet-gene interactions play a major role in the metabolism and detoxification of food-derived mutagens and carcinogens. Heterocyclic amines (HCAs), polycyclic aromatic hydrocarbons (PAHs), and N-nitroso compounds (NOCs) are a class of mutagens or carcinogens found in red and processed meat that can lead to various types of cancers. Harboring unfavourable mutations or single nucleotide polymorphisms (SNPs) involved in metabolism of HCAs, PAHs, and NOCs can promote cancers. Increasing risks of several types of cancers, such as cancer of the colorectum, breast, prostate, esophagus, and lung, have been associated with high intake of red and processed meat. We attempt to compile some of the variants based on reports published during the past five years on variations involved in red meat metabolism which aims to provide useful insight in aiding us to regulate our red meat intake to avoid spurring of cancer.
References
Bofetta P, Nyberg F. Contribution of environmental factors to cancer risk. Br Med Bull 2003; 68: 71-94. http://dx.doi.org/10.1093/bmp/ldg023 DOI: https://doi.org/10.1093/bmp/ldg023
Cancer and the Environment - National Cancer Institute [Internet]. [cited 2013 Apr 9]. Available from: http: //www.cancer.gov/cancertopics/understandingcancer/environment/AllPages
Parkin DM, Boyd L, Walker LC. The fraction of cancer attributable to lifestyle and environmental factors in the UK in 2010. Br J Cancer 2011; 105(Suppl) S77-81. DOI: https://doi.org/10.1038/bjc.2011.489
Flood DM, Weiss NS, Cook LS, Emerson JC, Schwartz SM, Potter JD. Colorectal cancer incidence in Asian migrants to the United States and their descendants. Cancer Causes Control: CCC 2000; 11(5): 403-11. http://dx.doi.org/10.1023/A:1008955722425 DOI: https://doi.org/10.1023/A:1008955722425
Alwan A. Noncommunicable diseases: a major challenge to public health in the region: editorial / Ala’din Alwan.
Gonzalez CA, Riboli E. Diet and cancer prevention: Contributions from the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Eur JCancer (Oxford, England: 1990) 2010; 46(14): 2555-62. DOI: https://doi.org/10.1016/j.ejca.2010.07.025
Rohrmann S, Overvad K, Bueno-de-Mesquita HB, Jakobsen MU, Egeberg R, Tjonneland A, et al. Meat consumption and mortality - results from the European Prospective Investigation into Cancer and Nutrition. BMC Med 2013; 11(1): 63. http://dx.doi.org/10.1186/1741-7015-11-63 DOI: https://doi.org/10.1186/1741-7015-11-63
Park, Lue, Ed. The Smoked-Foods Cookbook: How to Flavor, Cure, and Prepare Savory Meats, Game, Fish, Nuts, and Cheese (Google eBook). Stackpole Books 1992; p. 216.
Schieberle HBWGP. Food Chemistry (Google eBook). Springer 2009; p. 1070.
Ferguson LR. Meat and cancer. Meat Sci 2010; 84(2): 308-13. http://dx.doi.org/10.1016/j.meatsci.2009.06.032 DOI: https://doi.org/10.1016/j.meatsci.2009.06.032
Voutsinas J, Wilkens LR, Franke A, Vogt TM, Yokochi LA, Decker R, et al. Heterocyclic amine intake, smoking, cytochrome P450 1A2 and N-acetylation phenotypes, and risk of colorectal adenoma in a multiethnic population. Gut 2013; 62(3): 416-22. http://dx.doi.org/10.1136/gutjnl-2011-300665 DOI: https://doi.org/10.1136/gutjnl-2011-300665
Falcó G, Domingo JL, Llobet JM, Teixidó A, Casas C, Müller L. Polycyclic aromatic hydrocarbons in foods: human exposure through the diet in Catalonia, Spain. J Food Prot 2003; 66(12): 2325-31. DOI: https://doi.org/10.4315/0362-028X-66.12.2325
Polynuclear aromatic compounds, Part 1, Chemical, environmental and experimental data. IARC monographs on the evaluation of the carcinogenic risk of chemicals to humans 1983; 32: 1-453.
Bastide NM, Pierre FHF, Corpet DE. Heme iron from meat and risk of colorectal cancer: a meta-analysis and a review of the mechanisms involved. Cancer Prev Res (Philadelphia, Pa.) 2011; 4(2): 177-84. http://dx.doi.org/10.1158/1940-6207.CAPR-10-0113 DOI: https://doi.org/10.1158/1940-6207.CAPR-10-0113
Fu D, Calvo JA, Samson LD. Balancing repair and tolerance of DNA damage caused by alkylating agents. Nature reviews. Cancer 2012; 12(2): 104-20. DOI: https://doi.org/10.1038/nrc3185
Lunn JC, Kuhnle G, Mai V, Frankenfeld C, Shuker DEG, Glen RC, et al. The effect of haem in red and processed meat on the endogenous formation of N-nitroso compounds in the upper gastrointestinal tract. Carcinogenesis 2007; 28(3): 685-90. http://dx.doi.org/10.1093/carcin/bgl192 DOI: https://doi.org/10.1093/carcin/bgl192
Belitsky GA, Yakubovskaya MG. Genetic polymorphism and variability of chemical carcinogenesis. Biochemistry 2008; 73(5): 543-54. DOI: https://doi.org/10.1134/S0006297908050076
Ferrucci LM, Cross AJ, Gunter MJ, Ahn J, Mayne ST, Ma X, et al. Xenobiotic metabolizing genes, meat-related exposures, and risk of advanced colorectal adenoma. J Nutrigenet Nutrigenomics 2010; 3(4-6): 170-81. http://dx.doi.org/10.1159/000324351 DOI: https://doi.org/10.1159/000324351
Evans WE, Relling MV. Pharmacogenomics: translating functional genomics into rational therapeutics. Science (New York, N.Y.) 1999; 286(5439): 487-91. http://dx.doi.org/10.1126/science.286.5439.487 DOI: https://doi.org/10.1126/science.286.5439.487
Nelson DR. Cytochrome P450 and the individuality of species. Arch Biochem Biophys 1999; 369(1): 1-10. http://dx.doi.org/10.1006/abbi.1999.1352 DOI: https://doi.org/10.1006/abbi.1999.1352
Smith TJ, Liao A, Wang LD, Yang GY, Starcic S, Philbert MA, et al. Characterization of xenobiotic-metabolizing enzymes and nitrosamine metabolism in the human esophagus. Carcinogenesis 1998; 19(4): 667-72. http://dx.doi.org/10.1093/carcin/19.4.667 DOI: https://doi.org/10.1093/carcin/19.4.667
Nebert DW, Dalton TP. The role of cytochrome P450 enzymes in endogenous signalling pathways and environmental carcinogenesis. Nat Rev Cancer 2006; 6(12): 947-60. http://dx.doi.org/10.1038/nrc2015 DOI: https://doi.org/10.1038/nrc2015
Shimada T. Xenobiotic-metabolizing enzymes involved in activation and detoxification of carcinogenic polycyclic aromatic hydrocarbons. Drug Metab Pharmacokinet 2006; 21(4): 257-76. http://dx.doi.org/10.2133/dmpk.21.257 DOI: https://doi.org/10.2133/dmpk.21.257
What are single nucleotide polymorphisms (SNPs)? US National Library of Medicine, National Institutes of Health, Department of Health & Human Services 2013.
Saito T, Egashira M, Kiyotani K, Fujieda M, Yamazaki H, Kiyohara C, et al. Novel nonsynonymous polymorphisms of the CYP1A1 gene in Japanese. Drug Metab Pharmacokinet 2003; 18(3): 218-21. http://dx.doi.org/10.2133/dmpk.18.218 DOI: https://doi.org/10.2133/dmpk.18.218
Inoue K, Asao T, Shimada T. Ethnic-related differences in the frequency distribution of genetic polymorphisms in the CYP1A1 and CYP1B1 genes in Japanese and Caucasian populations. Xenobiotica; the fate of foreign compounds in biological systems 2000; 30(3): 285-95. DOI: https://doi.org/10.1080/004982500237677
Zhu K, Hunter S, Payne-Wilks K, Sutcliffe C, Bentley C, Roland CL, et al. Potential differences in breast cancer risk factors based on CYP1A1 MspI and African-American-specific genotypes. Ethn Dis 2006; 16(1): 207-15.
Little J, Sharp L, Masson LF, Brockton NT, Cotton SC, Haites NE, et al. Colorectal cancer and genetic polymorphisms of CYP1A1, GSTM1 and GSTT1: a case-control study in the Grampian region of Scotland. Int J Cancer 2006; 119(9): 2155-64. http://dx.doi.org/10.1002/ijc.22093 DOI: https://doi.org/10.1002/ijc.22093
Moretti M, Dell’Omo M, Villarini M, Pastorelli R, Muzi G, Airoldi L, et al. Primary DNA damage and genetic polymorphisms for CYP1A1, EPHX and GSTM1 in workers at a graphite electrode manufacturing plant. BMC public health. 2007; 7: 270. http://dx.doi.org/10.1186/1471-2458-7-270 DOI: https://doi.org/10.1186/1471-2458-7-270
Cotterchio M, Boucher BA, Manno M, Gallinger S, Okey AB, Harper PA. Red meat intake, doneness, polymorphisms in genes that encode carcinogen-metabolizing enzymes, and colorectal cancer risk. Cancer Epidemiol Biomarkers Prev 2008; 17(11): 3098-107. http://dx.doi.org/10.1158/1055-9965.EPI-08-0341 DOI: https://doi.org/10.1158/1055-9965.EPI-08-0341
Küry S, Buecher B, Robiou-du-Pont S, Scoul C, Sébille V, Colman H, et al. Combinations of cytochrome P450 gene polymorphisms enhancing the risk for sporadic colorectal cancer related to red meat consumption. Cancer Epidemiol Biomarkers Prev 2007; 16(7): 1460-7. http://dx.doi.org/10.1158/1055-9965.EPI-07-0236 DOI: https://doi.org/10.1158/1055-9965.EPI-07-0236
Wang J, Joshi AD, Corral R, Siegmund KD, Marchand L Le, Martinez ME, et al. Carcinogen metabolism genes, red meat and poultry intake, and colorectal cancer risk. Int J Cancer 2012; 130(8): 1898-907. http://dx.doi.org/10.1002/ijc.26199 DOI: https://doi.org/10.1002/ijc.26199
Koutros S, Andreotti G, Berndt SI, Hughes Barry K, Lubin JH, Hoppin JA, et al. Xenobiotic-metabolizing gene variants, pesticide use, and the risk of prostate cancer. Pharmacogenet Genomics 2011; 21(10): 615-23. http://dx.doi.org/10.1097/FPC.0b013e3283493a57 DOI: https://doi.org/10.1097/FPC.0b013e3283493a57
Skjelbred CF, Saebø M, Hjartåker A, Grotmol T, Hansteen I-L, Tveit KM, et al. Meat, vegetables and genetic polymorphisms and the risk of colorectal carcinomas and adenomas. BMC Cancer 2007; 7: 228. http://dx.doi.org/10.1186/1471-2407-7-228 DOI: https://doi.org/10.1186/1471-2407-7-228
Eichholzer M, Rohrmann S, Barbir A, Hermann S, Teucher B, Kaaks R, et al. Polymorphisms in heterocyclic aromatic amines metabolism-related genes are associated with colorectal adenoma risk. Int J Mol Epidemiol Genet 2012; 3(2): 96-106.
Lin J, Forman MR, Wang J, Grossman HB, Chen M, Dinney CP, et al. Intake of red meat and heterocyclic amines, metabolic pathway genes and bladder cancer risk. Int J Cancer 2012; 131(8): 1892-903. http://dx.doi.org/10.1002/ijc.27437 DOI: https://doi.org/10.1002/ijc.27437
Wright JL, Neuhouser ML, Lin DW, Kwon EM, Feng Z, Ostrander EA, et al. AMACR polymorphisms, dietary intake of red meat and dairy and prostate cancer risk. Prostate 2011; 71(5): 498-506. http://dx.doi.org/10.1002/pros.21267 DOI: https://doi.org/10.1002/pros.21267
Chen M, Cassidy A, Gu J, Delclos GL, Zhen F, Yang H, et al. Genetic variations in PI3K-AKT-mTOR pathway and bladder cancer risk. Carcinogenesis 2009; 30(12): 2047-52. http://dx.doi.org/10.1093/carcin/bgp258 DOI: https://doi.org/10.1093/carcin/bgp258
Food, Nutrition, Physical Activity, and the Prevention of Cancer: a Global Perspective [Internet]. [cited 2013 Mar 14]. Available from: http: //eprints.ucl.ac.uk/4841/1/4841.pdf
Cross AJ, Ferrucci LM, Risch A, Graubard BI, Ward MH, Park Y, et al. A large prospective study of meat consumption and colorectal cancer risk: an investigation of potential mechanisms underlying this association. Cancer Res 2010; 70(6): 2406-14. http://dx.doi.org/10.1158/0008-5472.CAN-09-3929 DOI: https://doi.org/10.1158/0008-5472.CAN-09-3929
Aune D, De Stefani E, Ronco A, Boffetta P, Deneo-Pellegrini H, Acosta G, et al. Meat consumption and cancer risk: a case-control study in Uruguay. Asian Pac J Cancer Prev 2009; 10(3): 429-36.
De Stefani E, Ronco AL, Boffetta P, Deneo-Pellegrini H, Correa P, Acosta G, et al. Nutrient-derived dietary patterns and risk of colorectal cancer: a factor analysis in Uruguay. Asian Pac J Cancer Prev: APJCP 2012; 13(1): 231-5. http://dx.doi.org/10.7314/APJCP.2012.13.1.231 DOI: https://doi.org/10.7314/APJCP.2012.13.1.231
Takachi R, Tsubono Y, Baba K, Inoue M, Sasazuki S, Iwasaki M, et al. Red meat intake may increase the risk of colon cancer in Japanese, a population with relatively low red meat consumption. Asia Pac J Clin Nutr 2011; 20(4): 603-12.
Takata Y, Shu X-O, Gao Y-T, Li H, Zhang X, Gao J, et al. Red meat and poultry intakes and risk of total and cause-specific mortality: results from cohort studies of chinese adults in shanghai. PloS One 2013; 8(2): e56963. http://dx.doi.org/10.1371/journal.pone.0056963 DOI: https://doi.org/10.1371/journal.pone.0056963
Pancione M, Remo A, Colantuoni V. Genetic and epigenetic events generate multiple pathways in colorectal cancer progression. Patholog Res Int 2012; 2012: 509348. DOI: https://doi.org/10.1155/2012/509348
Kang GH. Four molecular subtypes of colorectal cancer and their precursor lesions. Arch Pathol Lab Med 2011; 135(6): 698-703. DOI: https://doi.org/10.5858/2010-0523-RA.1
Norat T, Bingham S, Ferrari P, Slimani N, Jenab M, Mazuir M, et al. Meat, fish, and colorectal cancer risk: the European Prospective Investigation into cancer and nutrition. J Natl Cancer Inst 2005; 97(12): 906-16. http://dx.doi.org/10.1093/jnci/dji164 DOI: https://doi.org/10.1093/jnci/dji409
Brevik A, Joshi AD, Corral R, Onland-Moret NC, Siegmund KD, Le Marchand L, et al. Polymorphisms in base excision repair genes as colorectal cancer risk factors and modifiers of the effect of diets high in red meat. Cancer Epidemiol Biomarkers Prev 2010; 19(12): 3167-73. http://dx.doi.org/10.1158/1055-9965.EPI-10-0606 DOI: https://doi.org/10.1158/1055-9965.EPI-10-0606
Sandhu MS, White IR, Mcpherson K. Systematic review of the prospective cohort studies on meat consumption and colorectal cancer risk: a meta-analytical approach. Cancer Epidemiol Biomarkers Prev 10(5): 439-46.
Ferrucci LM, Cross AJ, Graubard BI, Brinton LA, McCarty CA, Ziegler RG, et al. Intake of meat, meat mutagens, and iron and the risk of breast cancer in the prostate, lung, colorectal, and ovarian cancer screening trial. Br J Cancer 2009; 101(1): 178-84. http://dx.doi.org/10.1038/sj.bjc.6605118 DOI: https://doi.org/10.1038/sj.bjc.6605118
Fu Z, Deming SL, Fair AM, Shrubsole MJ, Wujcik DM, Shu X-O, et al. Well-done meat intake and meat-derived mutagen exposures in relation to breast cancer risk: the Nashville Breast Health Study. Breast Cancer Res Treat 2011; 129(3): 919-28. http://dx.doi.org/10.1007/s10549-011-1538-7 DOI: https://doi.org/10.1007/s10549-011-1538-7
Lima FEL de, Latorre M do RD de O, Costa MJ de C, Fisberg RM. Diet and cancer in Northeast Brazil: evaluation of eating habits and food group consumption in relation to breast cancer. Cad Saude Publica 2008; 24(4): 820-8. http://dx.doi.org/10.1590/S0102-311X2008000400012 DOI: https://doi.org/10.1590/S0102-311X2008000400012
Ronco AL, De Stefani E, Deneo-Pellegrini H. Risk factors for premenopausal breast cancer: a case-control study in Uruguay. Asian Pac J Cancer Prev 2012; 13(6): 2879-86. http://dx.doi.org/10.7314/APJCP.2012.13.6.2879 DOI: https://doi.org/10.7314/APJCP.2012.13.6.2879
Punnen S, Hardin J, Cheng I, Klein EA, Witte JS. Impact of meat consumption, preparation, and mutagens on aggressive prostate cancer. PloS One 2011; 6(11): e27711. http://dx.doi.org/10.1371/journal.pone.0027711 DOI: https://doi.org/10.1371/journal.pone.0027711
John EM, Stern MC, Sinha R, Koo J. Meat consumption, cooking practices, meat mutagens, and risk of prostate cancer. Nutr Cancer 2011; 63(4): 525-37. http://dx.doi.org/10.1080/01635581.2011.539311 DOI: https://doi.org/10.1080/01635581.2011.539311
Amin M, Jeyaganth S, Fahmy N, Bégin LR, Aronson S, Jacobson S, et al. Dietary habits and prostate cancer detection: a case-control study. Can Urol Assoc J 2008; 2(5): 510-5. DOI: https://doi.org/10.5489/cuaj.918
Sinha R, Park Y, Graubard BI, Leitzmann MF, Hollenbeck A, Schatzkin A, et al. Meat and meat-related compounds and risk of prostate cancer in a large prospective cohort study in the United States. Am J Epidemiol 2009; 170(9): 1165-77. http://dx.doi.org/10.1093/aje/kwp280 DOI: https://doi.org/10.1093/aje/kwp280
Keszei AP, Schouten LJ, Goldbohm RA, Van den Brandt PA. Red and processed meat consumption and the risk of esophageal and gastric cancer subtypes in The Netherlands Cohort Study. Ann Oncol 2012; 23(9): 2319-26. http://dx.doi.org/10.1093/annonc/mdr615 DOI: https://doi.org/10.1093/annonc/mdr615
Cross AJ, Freedman ND, Ren J, Ward MH, Hollenbeck AR, Schatzkin A, et al. Meat consumption and risk of esophageal and gastric cancer in a large prospective study. Am J Gastroenterol 2011; 106(3): 432-42. http://dx.doi.org/10.1038/ajg.2010.415 DOI: https://doi.org/10.1038/ajg.2010.415
O’Doherty MG, Cantwell MM, Murray LJ, Anderson LA, Abnet CC. Dietary fat and meat intakes and risk of reflux esophagitis, Barrett’s esophagus and esophageal adenocarcinoma. Int J Cancer 2011; 129(6): 1493-502. http://dx.doi.org/10.1002/ijc.26108 DOI: https://doi.org/10.1002/ijc.26108
De Stefani E, Ronco AL, Boffetta P, Deneo-Pellegrini H, Acosta G, Mendilaharsu M. Meat consumption, meat cooking and risk of lung cancer among Uruguayan men. Asian Pac J Cancer Prev: APJCP 2010; 11(6): 1713-7.
Lam TK, Cross AJ, Consonni D, Randi G, Bagnardi V, Bertazzi PA, et al. Intakes of red meat, processed meat, and meat mutagens increase lung cancer risk. Cancer Res 2009; 69(3): 932-9. http://dx.doi.org/10.1158/0008-5472.CAN-08-3162 DOI: https://doi.org/10.1158/0008-5472.CAN-08-3162
Tasevska N, Sinha R, Kipnis V, Subar AF, Leitzmann MF, Hollenbeck AR, et al. A prospective study of meat, cooking methods, meat mutagens, heme iron, and lung cancer risks. Am J Clin Nutr 2009; 89(6): 1884-94. http://dx.doi.org/10.3945/ajcn.2008.27272 DOI: https://doi.org/10.3945/ajcn.2008.27272
Linos E, Willett W. Meat, dairy, and breast cancer: do we have an answer? 1, 2 2009; 455-6. DOI: https://doi.org/10.3945/ajcn.2009.28340
Hessels D, Verhaegh GW, Schalken JA, Witjes JA. Applicability of biomarkers in the early diagnosis of prostate cancer. Expert Rev Mol Diagn 2004; 4(4): 513-26. http://dx.doi.org/10.1586/14737159.4.4.513 DOI: https://doi.org/10.1586/14737159.4.4.513
Kumar-Sinha C, Shah RB, Laxman B, Tomlins SA, Harwood J, Schmitz W, et al. Elevated alpha-methylacyl-CoA racemase enzymatic activity in prostate cancer. Am J Pathol 2004; 164(3): 787-93. http://dx.doi.org/10.1016/S0002-9440(10)63167-7 DOI: https://doi.org/10.1016/S0002-9440(10)63167-7
Isa F, Xie L-P, Hu Z, Zhong Z, Hemelt M, Reulen RC, et al. Dietary consumption and diet diversity and risk of developing bladder cancer: results from the South and East China case-control study. Cancer Causes Control: CCC 2013. DOI: https://doi.org/10.1007/s10552-013-0165-5
Wu JW, Cross AJ, Baris D, Ward MH, Karagas MR, Johnson A, et al. Dietary intake of meat, fruits, vegetables, and selective micronutrients and risk of bladder cancer in the New England region of the United States. Br J Cancer 2012; 106(11): 1891-8. http://dx.doi.org/10.1038/bjc.2012.187 DOI: https://doi.org/10.1038/bjc.2012.187
Chan JM, Gong Z, Holly EA, Bracci PM. Dietary patterns and risk of pancreatic cancer in a large population-based case-control study in the san francisco bay area. Nutr Cancer 2013; 65(1): 157-64. http://dx.doi.org/10.1080/01635581.2012.725502 DOI: https://doi.org/10.1080/01635581.2012.725502
Chuang S-C, Jenab M, Heck JE, Bosetti C, Talamini R, Matsuo K, et al. Diet and the risk of head and neck cancer: a pooled analysis in the INHANCE consortium. Cancer Causes Control: CCC 2012; 23(1): 69-88. http://dx.doi.org/10.1007/s10552-011-9857-x DOI: https://doi.org/10.1007/s10552-011-9857-x
Lagiou P, Talamini R, Samoli E, Lagiou A, Ahrens W, Pohlabeln H, et al. Diet and upper-aerodigestive tract cancer in Europe: the ARCAGE study. Int J Cancer 2009; 124(11): 2671-6. http://dx.doi.org/10.1002/ijc.24246 DOI: https://doi.org/10.1002/ijc.24246
Kallianpur AR, Lee S-A, Xu W-H, Zheng W, Gao Y-T, Cai H, et al. Dietary iron intake and risk of endometrial cancer: a population-based case-control study in Shanghai, China. Nutr Cancer 2010; 62(1): 40-50. http://dx.doi.org/10.1080/01635580903191544 DOI: https://doi.org/10.1080/01635580903191544
Jiménez-Colmenero F, Carballo J, Cofrades S. Healthier meat and meat products: their role as functional foods. Meat Sci 2001; 59(1): 5-13. http://dx.doi.org/10.1016/S0309-1740(01)00053-5 DOI: https://doi.org/10.1016/S0309-1740(01)00053-5
Sesink AL, Termont DS, Kleibeuker JH, Van der Meer R. Red meat and colon cancer: dietary haem-induced colonic cytotoxicity and epithelial hyperproliferation are inhibited by calcium. Carcinogenesis 2001; 22(10): 1653-9. http://dx.doi.org/10.1093/carcin/22.10.1653 DOI: https://doi.org/10.1093/carcin/22.10.1653
Marianski S, Mariański A, Marianski R. Meat Smoking and Smokehouse Design. Bookmagic LLC 2009; p. 317.
Published
How to Cite
Issue
Section
License
Policy for Journals/Articles with Open Access
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are permitted and encouraged to post links to their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work
Policy for Journals / Manuscript with Paid Access
Authors who publish with this journal agree to the following terms:
- Publisher retain copyright .
- Authors are permitted and encouraged to post links to their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work .