Skip to main content
Top
Published in: Journal of Gastroenterology 4/2017

01-04-2017 | Review

A critical overview on the biological and molecular features of red and processed meat in colorectal carcinogenesis

Authors: Arunan Jeyakumar, Lakal Dissabandara, Vinod Gopalan

Published in: Journal of Gastroenterology | Issue 4/2017

Login to get access

Abstract

A recent investigation by the World Health Organisation (WHO) has found that the consumption of processed meat and potentially red meat promotes carcinogenesis and can increase the risk of colorectal cancer. This literature review aims to summarise both the red and processed meat molecules associated with colorectal carcinogenesis and investigate their relationship with the pathogenic process of colorectal cancer. Literature relating to the carcinogenic effect of red and processed meat molecules was critically reviewed. There are multiple molecules present in red and processed meat with a potential carcinogenic effect on colorectal tissues. Processed meat is more carcinogenic compared to red meat because of the abundance of potent nitrosyl-heme molecules that form N-nitroso compounds. Studies have also noted that other molecules such as polycyclic aromatic hydrocarbons and heterocyclic amines have potential mechanisms for the initiation of colorectal cancer pathogenesis. The non-human sugar molecule N-glycolylneuraminic acid may account for the carcinogenic effects of pork despite its heme content being comparable to that of chicken. Red meat products, especially those that have been processed, have a wide variety of carcinogenic molecules known to increase the risk of colorectal cancer. Thus, the outcome of this review is consistent with the recent findings of WHO.
Literature
2.
go back to reference Power DG, Gloglowski E, Lipkin SM. Clinical genetics of hereditary colorectal cancer. Hematol Oncol Clin North Am. 2010;24:837–59.CrossRefPubMed Power DG, Gloglowski E, Lipkin SM. Clinical genetics of hereditary colorectal cancer. Hematol Oncol Clin North Am. 2010;24:837–59.CrossRefPubMed
5.
go back to reference Bouvard V, Loomis D, Guyton KZ, International Agency for Research on Cancer Monograph Working Group, et al. Carcinogenicity of consumption of red and processedmeat. Lancet Oncol. 2015;16:1599–600.CrossRefPubMed Bouvard V, Loomis D, Guyton KZ, International Agency for Research on Cancer Monograph Working Group, et al. Carcinogenicity of consumption of red and processedmeat. Lancet Oncol. 2015;16:1599–600.CrossRefPubMed
6.
go back to reference Norat T, Bingham S, Ferrari P, et al. Meat, fish, and colorectal cancer risk: the European Prospective Investigation into cancer and nutrition. J Natl Cancer Inst. 2005;97:906–16.CrossRefPubMedPubMedCentral Norat T, Bingham S, Ferrari P, et al. Meat, fish, and colorectal cancer risk: the European Prospective Investigation into cancer and nutrition. J Natl Cancer Inst. 2005;97:906–16.CrossRefPubMedPubMedCentral
7.
go back to reference Larsson SC, Rafter J, Holmberg L, et al. Red meat consumption and risk of cancers of the proximal colon, distal colon and rectum: the Swedish Mammography Cohort. Int J Cancer. 2005;113:829–34.CrossRefPubMed Larsson SC, Rafter J, Holmberg L, et al. Red meat consumption and risk of cancers of the proximal colon, distal colon and rectum: the Swedish Mammography Cohort. Int J Cancer. 2005;113:829–34.CrossRefPubMed
8.
go back to reference English DR, MacInnis RJ, Hodge AM, et al. Red meat, chicken, and fish consumption and risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev. 2004;13:1509–14.PubMed English DR, MacInnis RJ, Hodge AM, et al. Red meat, chicken, and fish consumption and risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev. 2004;13:1509–14.PubMed
9.
go back to reference Lindahl G, Lundström K, Tornberg E. Contribution of pigment content, myoglobin forms and internal reflectance to the colour of pork loin and ham from pure breed pigs. Meat Sci. 2001;59:141–51.CrossRefPubMed Lindahl G, Lundström K, Tornberg E. Contribution of pigment content, myoglobin forms and internal reflectance to the colour of pork loin and ham from pure breed pigs. Meat Sci. 2001;59:141–51.CrossRefPubMed
10.
go back to reference Sen AR, Naveena BM, Muthukumar M, et al. Colour, myoglobin denaturation and storage stability of raw and cooked mutton chops at different end point cooking temperature. J Food Sci Technol. 2014;51:970–5.CrossRefPubMed Sen AR, Naveena BM, Muthukumar M, et al. Colour, myoglobin denaturation and storage stability of raw and cooked mutton chops at different end point cooking temperature. J Food Sci Technol. 2014;51:970–5.CrossRefPubMed
11.
go back to reference Santarelli RL, Pierre F, Corpet DE. Processed meat and colorectal cancer: a review of epidemiologic and experimental evidence. Nutr Cancer. 2008;60:131–44.CrossRefPubMedPubMedCentral Santarelli RL, Pierre F, Corpet DE. Processed meat and colorectal cancer: a review of epidemiologic and experimental evidence. Nutr Cancer. 2008;60:131–44.CrossRefPubMedPubMedCentral
12.
go back to reference Fritz W, Soós K. Smoked food and cancer. Bibl Nutr Dieta. 1980;29:57–64. Fritz W, Soós K. Smoked food and cancer. Bibl Nutr Dieta. 1980;29:57–64.
13.
go back to reference Tricker AR. N-nitroso compounds and man: sources of exposure, endogenous formation and occurrence in body fluids. Eur J Cancer Prev. 1997;6:226–68.CrossRefPubMed Tricker AR. N-nitroso compounds and man: sources of exposure, endogenous formation and occurrence in body fluids. Eur J Cancer Prev. 1997;6:226–68.CrossRefPubMed
14.
go back to reference Schwartz S, Ellefson M. Quantitative fecal recovery of ingested hemoglobin-heme in blood: comparisons by HemoQuant assay with ingested meat and fish. Gastroenterology. 1985;89:19–26.CrossRefPubMed Schwartz S, Ellefson M. Quantitative fecal recovery of ingested hemoglobin-heme in blood: comparisons by HemoQuant assay with ingested meat and fish. Gastroenterology. 1985;89:19–26.CrossRefPubMed
15.
go back to reference Bastide NM, Pierre FH, Corpet DE. Heme iron from meat and risk of colorectal cancer: a meta-analysis and a review of the mechanisms involved. Cancer Prev Res. 2011;4:177–84.CrossRef Bastide NM, Pierre FH, Corpet DE. Heme iron from meat and risk of colorectal cancer: a meta-analysis and a review of the mechanisms involved. Cancer Prev Res. 2011;4:177–84.CrossRef
16.
go back to reference Qiao L, Feng Y. Intakes of heme iron and zinc and colorectal cancer incidence: a meta-analysis of prospective studies. Cancer Causes Control. 2013;24:1175–83.CrossRefPubMed Qiao L, Feng Y. Intakes of heme iron and zinc and colorectal cancer incidence: a meta-analysis of prospective studies. Cancer Causes Control. 2013;24:1175–83.CrossRefPubMed
17.
go back to reference Pierre F, Freeman A, Taché S, et al. Beef meat and blood sausage promote the formation of azoxymethane-induced mucin-depleted foci and aberrant crypt foci in rat colons. J Nutr. 2004;134:2711–6.PubMed Pierre F, Freeman A, Taché S, et al. Beef meat and blood sausage promote the formation of azoxymethane-induced mucin-depleted foci and aberrant crypt foci in rat colons. J Nutr. 2004;134:2711–6.PubMed
18.
go back to reference Gilsing AM, Fransen F, de Kok TM, Goldbohm AR, Schouten LJ, de Bruïne AP, van Engeland M, van den Brandt PA, de Goeij AF, Weijenberg MP. Dietary heme iron and the risk of colorectal cancer with specific mutations in KRAS and APC. Carcinogenesis. 2013;34(12):2757–66.CrossRefPubMed Gilsing AM, Fransen F, de Kok TM, Goldbohm AR, Schouten LJ, de Bruïne AP, van Engeland M, van den Brandt PA, de Goeij AF, Weijenberg MP. Dietary heme iron and the risk of colorectal cancer with specific mutations in KRAS and APC. Carcinogenesis. 2013;34(12):2757–66.CrossRefPubMed
19.
go back to reference Sesink AL, Termont DS, Kleibeuker JH, et al. Red meat and colon cancer: the cytotoxic and hyperproliferative effects of dietary heme. Cancer Res. 1999;59:5704–9.PubMed Sesink AL, Termont DS, Kleibeuker JH, et al. Red meat and colon cancer: the cytotoxic and hyperproliferative effects of dietary heme. Cancer Res. 1999;59:5704–9.PubMed
20.
21.
go back to reference Barrera G. Oxidative stress and lipid peroxidation products in cancerprogression and therapy. ISRN Oncol. 2012;2012:137289.PubMedPubMedCentral Barrera G. Oxidative stress and lipid peroxidation products in cancerprogression and therapy. ISRN Oncol. 2012;2012:137289.PubMedPubMedCentral
22.
go back to reference Riess ML, Camara AK, Kevin LG, et al. Reduced reactive O2 species formation and preserved mitochondrial NADH and [Ca2+] levels during short-term 17 °C ischemia in intact hearts. Cardiovasc Res. 2004;61:580–90.CrossRefPubMed Riess ML, Camara AK, Kevin LG, et al. Reduced reactive O2 species formation and preserved mitochondrial NADH and [Ca2+] levels during short-term 17 °C ischemia in intact hearts. Cardiovasc Res. 2004;61:580–90.CrossRefPubMed
24.
go back to reference Barrera G, Pizzimenti S, Dianzani MU. Lipid peroxidation: control of cell proliferation, cell differentiation and cell death. Mol Aspects Med. 2008;29:1–8.CrossRefPubMed Barrera G, Pizzimenti S, Dianzani MU. Lipid peroxidation: control of cell proliferation, cell differentiation and cell death. Mol Aspects Med. 2008;29:1–8.CrossRefPubMed
25.
go back to reference Leuratti C, Watson MA, Deag EJ, et al. Detection of malondialdehyde DNA adducts in human colorectal mucosa: relationship with diet and the presence of adenomas. Cancer Epidemiol Biomarkers Prev. 2002;11:267–73.PubMed Leuratti C, Watson MA, Deag EJ, et al. Detection of malondialdehyde DNA adducts in human colorectal mucosa: relationship with diet and the presence of adenomas. Cancer Epidemiol Biomarkers Prev. 2002;11:267–73.PubMed
26.
go back to reference Baradat M, Jouanin I, Dalleau S, et al. 4-Hydroxy-2(E)-nonenal metabolism differs in Apc(+/+) cells and in Apc(Min/+) cells: it may explain colon cancer promotion by heme iron. Chem Res Toxicol. 2011;24:1984–93.CrossRefPubMed Baradat M, Jouanin I, Dalleau S, et al. 4-Hydroxy-2(E)-nonenal metabolism differs in Apc(+/+) cells and in Apc(Min/+) cells: it may explain colon cancer promotion by heme iron. Chem Res Toxicol. 2011;24:1984–93.CrossRefPubMed
27.
28.
go back to reference Pierre F, Peiro G, Taché S, et al. New marker of colon cancer risk associated with heme intake: 1,4-dihydroxynonane mercapturic acid. Cancer Epidemiol Biomarkers Prev. 2006;15:2274–9.CrossRefPubMed Pierre F, Peiro G, Taché S, et al. New marker of colon cancer risk associated with heme intake: 1,4-dihydroxynonane mercapturic acid. Cancer Epidemiol Biomarkers Prev. 2006;15:2274–9.CrossRefPubMed
29.
go back to reference Baron CP, Andersen HJ. Myoglobin-induced lipid oxidation. A review. J Agric Food Chem. 2002;50:3887–97.CrossRefPubMed Baron CP, Andersen HJ. Myoglobin-induced lipid oxidation. A review. J Agric Food Chem. 2002;50:3887–97.CrossRefPubMed
30.
go back to reference Dietrich M, Block G, Pogoda JM, et al. A review: dietary and endogenously formed N-nitroso compounds and risk of childhood brain tumors. Cancer Causes Control. 2005;16:619–35.CrossRefPubMed Dietrich M, Block G, Pogoda JM, et al. A review: dietary and endogenously formed N-nitroso compounds and risk of childhood brain tumors. Cancer Causes Control. 2005;16:619–35.CrossRefPubMed
32.
go back to reference Dubrow R, Darefsky AS, Park Y, et al. Dietary components related to N-nitroso compound formation: a prospective study of adult glioma. Cancer Epidemiol Biomarkers Prev. 2010;19:1709–22.CrossRefPubMedPubMedCentral Dubrow R, Darefsky AS, Park Y, et al. Dietary components related to N-nitroso compound formation: a prospective study of adult glioma. Cancer Epidemiol Biomarkers Prev. 2010;19:1709–22.CrossRefPubMedPubMedCentral
33.
go back to reference Cross AJ, Sinha R. Meat-related mutagens/carcinogens in the etiology of colorectal cancer. Environ Mol Mutagen. 2004;44:44–55.CrossRefPubMed Cross AJ, Sinha R. Meat-related mutagens/carcinogens in the etiology of colorectal cancer. Environ Mol Mutagen. 2004;44:44–55.CrossRefPubMed
35.
go back to reference Zhu Y, Wang PP, Zhao J, et al. Dietary N-nitroso compounds and risk of colorectal cancer: a case-control study in Newfoundland and Labrador and Ontario, Canada. Br J Nutr. 2014;111:1109–17.CrossRefPubMed Zhu Y, Wang PP, Zhao J, et al. Dietary N-nitroso compounds and risk of colorectal cancer: a case-control study in Newfoundland and Labrador and Ontario, Canada. Br J Nutr. 2014;111:1109–17.CrossRefPubMed
36.
go back to reference Loh YH, Jakszyn P, Luben RN, et al. N-nitroso compounds and cancer incidence: the european prospective investigation into cancer and nutrition (EPIC)—Norfolk Study. Am J Clin Nutr. 2011;93:1053–61.CrossRefPubMed Loh YH, Jakszyn P, Luben RN, et al. N-nitroso compounds and cancer incidence: the european prospective investigation into cancer and nutrition (EPIC)—Norfolk Study. Am J Clin Nutr. 2011;93:1053–61.CrossRefPubMed
37.
go back to reference Jakszyn P, Gonzalez CA. Nitrosamine and related food intake and gastric and oesophageal cancer risk: a systematic review of the epidemiological evidence. World J Gastroenterol. 2006;12:4296–303.CrossRefPubMedPubMedCentral Jakszyn P, Gonzalez CA. Nitrosamine and related food intake and gastric and oesophageal cancer risk: a systematic review of the epidemiological evidence. World J Gastroenterol. 2006;12:4296–303.CrossRefPubMedPubMedCentral
38.
go back to reference Knekt P, Järvinen R, Dich J, Hakulinen T. Risk of colorectal and other gastro-intestinal cancers after exposure to nitrate, nitrite and N-nitroso compounds: a follow-up study. Int J Cancer. 1999;80:852–6.CrossRefPubMed Knekt P, Järvinen R, Dich J, Hakulinen T. Risk of colorectal and other gastro-intestinal cancers after exposure to nitrate, nitrite and N-nitroso compounds: a follow-up study. Int J Cancer. 1999;80:852–6.CrossRefPubMed
39.
go back to reference Honikel KO. The use and control of nitrate and nitrite for the processing of meat products. Meat Sci. 2008;78:68–76.CrossRefPubMed Honikel KO. The use and control of nitrate and nitrite for the processing of meat products. Meat Sci. 2008;78:68–76.CrossRefPubMed
41.
42.
go back to reference Silvester KR, Bingham SA, Pollock JR, et al. Effect of meat and resistant starch on fecal excretion of apparent N-nitroso compounds and ammonia from the human large bowel. Nutr Cancer. 1997;29:13–23.CrossRefPubMed Silvester KR, Bingham SA, Pollock JR, et al. Effect of meat and resistant starch on fecal excretion of apparent N-nitroso compounds and ammonia from the human large bowel. Nutr Cancer. 1997;29:13–23.CrossRefPubMed
43.
go back to reference Bingham SA, Pignatelli B, Pollock JR, et al. Does increased endogenous formation of N-nitroso compounds in the human colon explain the association between red meat and colon cancer? Carcinogenesis. 1996;17:515–23.CrossRefPubMed Bingham SA, Pignatelli B, Pollock JR, et al. Does increased endogenous formation of N-nitroso compounds in the human colon explain the association between red meat and colon cancer? Carcinogenesis. 1996;17:515–23.CrossRefPubMed
44.
go back to reference Cross AJ, Pollock JR, Bingham SA. Haem, not protein or inorganic iron, is responsible for endogenous intestinal N-nitrosation arising from red meat. Cancer Res. 2003;63:2358–60.PubMed Cross AJ, Pollock JR, Bingham SA. Haem, not protein or inorganic iron, is responsible for endogenous intestinal N-nitrosation arising from red meat. Cancer Res. 2003;63:2358–60.PubMed
45.
go back to reference Richardson G, Benjamin N. Potential therapeutic uses for S-nitrosothiols. Clin Sci (Lond). 2002;102:99–105.CrossRef Richardson G, Benjamin N. Potential therapeutic uses for S-nitrosothiols. Clin Sci (Lond). 2002;102:99–105.CrossRef
46.
go back to reference Kuhnle GG, Bingham SA. Dietary meat, endogenous nitrosation and colorectal cancer. Biochem Soc Trans. 2007;35:1355–7.CrossRefPubMed Kuhnle GG, Bingham SA. Dietary meat, endogenous nitrosation and colorectal cancer. Biochem Soc Trans. 2007;35:1355–7.CrossRefPubMed
47.
go back to reference Pegg RB, Shahidi F. Possible substitutes for nitrite, in nitrite curing of meat: the N-nitrosamine problem and nitrite alternatives. Food & Nutrition Press, Inc., Trumbull, 2004. doi:10.1002/9780470385081.ch9. Pegg RB, Shahidi F. Possible substitutes for nitrite, in nitrite curing of meat: the N-nitrosamine problem and nitrite alternatives. Food & Nutrition Press, Inc., Trumbull, 2004. doi:10.​1002/​9780470385081.​ch9.
48.
go back to reference Ijssennagger N, de Wit N, Müller M, et al. Dietary heme-mediated PPARα activation does not affect the heme-induced epithelial hyperproliferation and hyperplasia in mouse colon. PLoS One. 2012;7:e43260.CrossRefPubMedPubMedCentral Ijssennagger N, de Wit N, Müller M, et al. Dietary heme-mediated PPARα activation does not affect the heme-induced epithelial hyperproliferation and hyperplasia in mouse colon. PLoS One. 2012;7:e43260.CrossRefPubMedPubMedCentral
49.
go back to reference Ijssennagger N, Rijnierse A, de Wit NJ, et al. Dietary heme induces acute oxidative stress, but delayed cytotoxicity and compensatory hyperproliferation in mouse colon. Carcinogenesis. 2013;34:1628–35.CrossRefPubMed Ijssennagger N, Rijnierse A, de Wit NJ, et al. Dietary heme induces acute oxidative stress, but delayed cytotoxicity and compensatory hyperproliferation in mouse colon. Carcinogenesis. 2013;34:1628–35.CrossRefPubMed
50.
go back to reference Chou HH, Takematsu H, Diaz S, et al. A mutation in human CMP-sialic acid hydroxylase occurred after the Homo-Pan divergence. Proc Natl Acad Sci USA. 1998;95:11751–6.CrossRefPubMedPubMedCentral Chou HH, Takematsu H, Diaz S, et al. A mutation in human CMP-sialic acid hydroxylase occurred after the Homo-Pan divergence. Proc Natl Acad Sci USA. 1998;95:11751–6.CrossRefPubMedPubMedCentral
51.
go back to reference Samraj AN, Pearce OM, Läubli H, et al. A red meat-derived glycan promotes inflammation and cancer progression. Proc Natl Acad Sci USA. 2015;112:542–7.CrossRefPubMed Samraj AN, Pearce OM, Läubli H, et al. A red meat-derived glycan promotes inflammation and cancer progression. Proc Natl Acad Sci USA. 2015;112:542–7.CrossRefPubMed
52.
go back to reference Lombardi-Boccia G, Martinez-Dominguez B, Aguzzi A. Total heme and non-heme iron in raw and cooked meats. J Food Sci. 2002;67:1738–41.CrossRef Lombardi-Boccia G, Martinez-Dominguez B, Aguzzi A. Total heme and non-heme iron in raw and cooked meats. J Food Sci. 2002;67:1738–41.CrossRef
54.
go back to reference Alaejos MS, Afonso AM. Factors that affect the content of heterocyclic aromatic amines in foods. Compr Rev Food Sci Food Saf. 2011;10:52–108.CrossRef Alaejos MS, Afonso AM. Factors that affect the content of heterocyclic aromatic amines in foods. Compr Rev Food Sci Food Saf. 2011;10:52–108.CrossRef
55.
go back to reference Puangsombat K, Gadgil P, Houser TA, et al. Occurrence of heterocyclic amines in cooked meat products. Meat Sci. 2012;90:739–46.CrossRefPubMed Puangsombat K, Gadgil P, Houser TA, et al. Occurrence of heterocyclic amines in cooked meat products. Meat Sci. 2012;90:739–46.CrossRefPubMed
56.
go back to reference Helmus DS, Thompson CL, Zelenskiy S, et al. Red meat-derived heterocyclic amines increase risk of colon cancer: a population-based case–control study. Nutr Cancer. 2013;65:1141–50.CrossRefPubMedPubMedCentral Helmus DS, Thompson CL, Zelenskiy S, et al. Red meat-derived heterocyclic amines increase risk of colon cancer: a population-based case–control study. Nutr Cancer. 2013;65:1141–50.CrossRefPubMedPubMedCentral
57.
go back to reference Kampman E, Slattery ML, Bigler J, et al. Meat consumption, genetic susceptibility, and colon cancer risk: a United States multicenter case–control study. Cancer Epidemiol Biomark Prev. 1999;8:15–24. Kampman E, Slattery ML, Bigler J, et al. Meat consumption, genetic susceptibility, and colon cancer risk: a United States multicenter case–control study. Cancer Epidemiol Biomark Prev. 1999;8:15–24.
58.
go back to reference Butler LM, Sinha R, Millikan RC, et al. Heterocyclic amines, meat intake, and association with colon cancer in a population-based study. Am J Epidemiol. 2003;157:434–45.CrossRefPubMed Butler LM, Sinha R, Millikan RC, et al. Heterocyclic amines, meat intake, and association with colon cancer in a population-based study. Am J Epidemiol. 2003;157:434–45.CrossRefPubMed
59.
go back to reference Nöthlings U, Yamamoto JF, Wilkens LR, et al. Meat and heterocyclic amine intake, smoking, NAT1 and NAT2 polymorphisms, and colorectal cancer risk in the multiethnic cohort study. Cancer Epidemiol Biomark Prev. 2009;18:2098–106.CrossRef Nöthlings U, Yamamoto JF, Wilkens LR, et al. Meat and heterocyclic amine intake, smoking, NAT1 and NAT2 polymorphisms, and colorectal cancer risk in the multiethnic cohort study. Cancer Epidemiol Biomark Prev. 2009;18:2098–106.CrossRef
60.
go back to reference Tiemersma EW, Voskuil DW, Bunschoten A, et al. Risk of colorectal adenomas in relation to meat consumption, meat preparation, and genetic susceptibility in a Dutch population. Cancer Causes Control. 2004;15:225–36.CrossRefPubMed Tiemersma EW, Voskuil DW, Bunschoten A, et al. Risk of colorectal adenomas in relation to meat consumption, meat preparation, and genetic susceptibility in a Dutch population. Cancer Causes Control. 2004;15:225–36.CrossRefPubMed
61.
go back to reference Cross AJ, Ferrucci LM, Risch A, et al. A large prospective study of meat consumption and colorectal cancer risk: an investigation of potential mechanisms underlying this association. Cancer Res. 2010;70:2406–14.CrossRefPubMedPubMedCentral Cross AJ, Ferrucci LM, Risch A, et al. A large prospective study of meat consumption and colorectal cancer risk: an investigation of potential mechanisms underlying this association. Cancer Res. 2010;70:2406–14.CrossRefPubMedPubMedCentral
62.
63.
go back to reference Kassie F, Lhoste EF, Bruneau A, et al. Effect of intestinal microfloras from vegetarians and meat eaters on the genotoxicity of 2-amino-3-methylimidazo[4,5-f]quinoline, a carcinogenic heterocyclic amine. J Chromatogr B Analyt Technol Biomed Life Sci. 2004;802:211–5.CrossRefPubMed Kassie F, Lhoste EF, Bruneau A, et al. Effect of intestinal microfloras from vegetarians and meat eaters on the genotoxicity of 2-amino-3-methylimidazo[4,5-f]quinoline, a carcinogenic heterocyclic amine. J Chromatogr B Analyt Technol Biomed Life Sci. 2004;802:211–5.CrossRefPubMed
64.
go back to reference Schwab CE, Huber WW, Parzefall W, et al. Search for compounds that inhibit the genotoxic and carcinogenic effects of heterocyclic aromatic amines. Crit Rev Toxicol. 2000;30:1–69.CrossRefPubMed Schwab CE, Huber WW, Parzefall W, et al. Search for compounds that inhibit the genotoxic and carcinogenic effects of heterocyclic aromatic amines. Crit Rev Toxicol. 2000;30:1–69.CrossRefPubMed
65.
go back to reference Alaejos MS, González 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 Addit Contam Part A Chem Anal Control Expo Risk Assess. 2008;25:2–24.CrossRefPubMed Alaejos MS, González 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 Addit Contam Part A Chem Anal Control Expo Risk Assess. 2008;25:2–24.CrossRefPubMed
67.
go back to reference Boffetta P, Jourenkova N, Gustavsson P. Cancer risk from occupational and environmental exposure to polycyclic aromatic hydrocarbons. Cancer Causes Control. 1997;8:444–72.CrossRefPubMed Boffetta P, Jourenkova N, Gustavsson P. Cancer risk from occupational and environmental exposure to polycyclic aromatic hydrocarbons. Cancer Causes Control. 1997;8:444–72.CrossRefPubMed
68.
go back to reference Dennis MJ, Massey RC, McWeeny DJ, et al. Analysis of polycyclic aromatic hydrocarbons in UK total diets. Food Chem Toxicol. 1983;21:569–74.CrossRefPubMed Dennis MJ, Massey RC, McWeeny DJ, et al. Analysis of polycyclic aromatic hydrocarbons in UK total diets. Food Chem Toxicol. 1983;21:569–74.CrossRefPubMed
69.
go back to reference Estensen RD, Jordan MM, Wiedmann TS, et al. Effect of chemopreventive agents on separate stages of progression of benzo[α]pyrene induced lung tumors in A/J mice. Carcinogenesis. 2004;25:197–201.CrossRefPubMed Estensen RD, Jordan MM, Wiedmann TS, et al. Effect of chemopreventive agents on separate stages of progression of benzo[α]pyrene induced lung tumors in A/J mice. Carcinogenesis. 2004;25:197–201.CrossRefPubMed
70.
go back to reference Yang SK, McCourt DW, Roller PP, et al. Enzymatic conversion of benzo(a)pyrene leading predominantly to the diol-epoxider-7, t-8-dihydroxy-t-9,10-oxy-7,8,9,10-tetrahydrobenzo(a)pyrene through a single enantiomer of r-7, t-8-dihydroxy-7,8-dihydrobenzo(a)pyrene. Proc Natl Acad Sci USA. 1976;73:2594–8.CrossRefPubMedPubMedCentral Yang SK, McCourt DW, Roller PP, et al. Enzymatic conversion of benzo(a)pyrene leading predominantly to the diol-epoxider-7, t-8-dihydroxy-t-9,10-oxy-7,8,9,10-tetrahydrobenzo(a)pyrene through a single enantiomer of r-7, t-8-dihydroxy-7,8-dihydrobenzo(a)pyrene. Proc Natl Acad Sci USA. 1976;73:2594–8.CrossRefPubMedPubMedCentral
71.
72.
go back to reference Diggs DL, Huderson AC, Harris KL, et al. Polycyclic aromatic hydrocarbons and digestive tract cancers: a perspective. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev. 2011;29:324–57.CrossRefPubMedPubMedCentral Diggs DL, Huderson AC, Harris KL, et al. Polycyclic aromatic hydrocarbons and digestive tract cancers: a perspective. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev. 2011;29:324–57.CrossRefPubMedPubMedCentral
73.
go back to reference Sinha R, Kulldorff M, Gunter MJ, et al. Dietary benzo[a]pyrene intake and risk of colorectal adenoma. Cancer Epidemiol Biomark Prev. 2005;14:2030–4.CrossRef Sinha R, Kulldorff M, Gunter MJ, et al. Dietary benzo[a]pyrene intake and risk of colorectal adenoma. Cancer Epidemiol Biomark Prev. 2005;14:2030–4.CrossRef
74.
go back to reference Gunter MJ, Probst-Hensch NM, Cortessis VK, et al. Meat intake, cooking-related mutagens and risk of colorectal adenoma in a sigmoidoscopy-based case-control study. Carcinogenesis. 2005;26:637–42.CrossRefPubMed Gunter MJ, Probst-Hensch NM, Cortessis VK, et al. Meat intake, cooking-related mutagens and risk of colorectal adenoma in a sigmoidoscopy-based case-control study. Carcinogenesis. 2005;26:637–42.CrossRefPubMed
75.
go back to reference Tabatabaei SM, Heyworth JS, Knuiman MW, et al. Dietary benzo[a]pyrene intake from meat and the risk of colorectal cancer. Cancer Epidemiol Biomark Prev. 2010;19:3182–4.CrossRef Tabatabaei SM, Heyworth JS, Knuiman MW, et al. Dietary benzo[a]pyrene intake from meat and the risk of colorectal cancer. Cancer Epidemiol Biomark Prev. 2010;19:3182–4.CrossRef
76.
go back to reference Ferrucci LM, Sinha R, Graubard BI, et al. Dietary meat intake in relation to colorectal adenoma in asymptomatic women. Am J Gastroenterol. 2009;104:1231–40.CrossRefPubMedPubMedCentral Ferrucci LM, Sinha R, Graubard BI, et al. Dietary meat intake in relation to colorectal adenoma in asymptomatic women. Am J Gastroenterol. 2009;104:1231–40.CrossRefPubMedPubMedCentral
77.
go back to reference Wurzelmann JI, Silver A, Schreinemachers DM, Sandler RS, Everson RB. Iron intake and the risk of colorectal cancer. Cancer Epidemiol Biomark Prev. 1996;5:503–7. Wurzelmann JI, Silver A, Schreinemachers DM, Sandler RS, Everson RB. Iron intake and the risk of colorectal cancer. Cancer Epidemiol Biomark Prev. 1996;5:503–7.
78.
go back to reference Calmels S, Ohshima H, Vincent P, Gounot AM, Bartsch H. Screening of microorganisms for nitrosation catalysis at pH 7 and kinetic studies on nitrosamine formation from secondary amines by E. coli strains. Carcinogenesis. 1985;6:911–5.CrossRefPubMed Calmels S, Ohshima H, Vincent P, Gounot AM, Bartsch H. Screening of microorganisms for nitrosation catalysis at pH 7 and kinetic studies on nitrosamine formation from secondary amines by E. coli strains. Carcinogenesis. 1985;6:911–5.CrossRefPubMed
79.
go back to reference Evans DF, Pye G, Bramley R, Clark AG, Dyson TJ, Hardcastle JD. Measurement of gastrointestinal pH profiles in normal ambulant human subjects. Gut. 1988;29:1035–41.CrossRefPubMedPubMedCentral Evans DF, Pye G, Bramley R, Clark AG, Dyson TJ, Hardcastle JD. Measurement of gastrointestinal pH profiles in normal ambulant human subjects. Gut. 1988;29:1035–41.CrossRefPubMedPubMedCentral
80.
go back to reference Povey AC, Hall CN, Badawi AF, Cooper DP, O’Connor PJ. Elevated levels of the pro-carcinogenic adduct, O(6)-methylguanine, in normal DNA from the cancer prone regions of the large bowel. Gut. 2000;47:362–5.CrossRefPubMedPubMedCentral Povey AC, Hall CN, Badawi AF, Cooper DP, O’Connor PJ. Elevated levels of the pro-carcinogenic adduct, O(6)-methylguanine, in normal DNA from the cancer prone regions of the large bowel. Gut. 2000;47:362–5.CrossRefPubMedPubMedCentral
Metadata
Title
A critical overview on the biological and molecular features of red and processed meat in colorectal carcinogenesis
Authors
Arunan Jeyakumar
Lakal Dissabandara
Vinod Gopalan
Publication date
01-04-2017
Publisher
Springer Japan
Published in
Journal of Gastroenterology / Issue 4/2017
Print ISSN: 0944-1174
Electronic ISSN: 1435-5922
DOI
https://doi.org/10.1007/s00535-016-1294-x

Other articles of this Issue 4/2017

Journal of Gastroenterology 4/2017 Go to the issue