Cited by 397Nutritional Studies and DietColorectal Cancer Screening and DetectionMeat and Animal Product Quality

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Heme Iron from Meat and Risk of Colorectal Cancer: A Meta-analysis and a Review of the Mechanisms Involved

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Bastide, Nadia M., Pierre, Fabrice H.F., Corpet, Denis E.·2011·Cancer Prevention Research

DOI 10.1158/1940-6207.capr-10-0113

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Abstract

Red meat and processed meat intake is associated with a risk of colorectal cancer, a major cause of death in affluent countries. Epidemiological and experimental evidence supports the hypothesis that heme iron present in meat promotes colorectal cancer. This meta-analysis of prospective cohort studies of colon cancer reporting heme intake included 566,607 individuals and 4,734 cases of colon cancer. The relative risk of colon cancer was 1.18 (95% CI: 1.06-1.32) for subjects in the highest category of heme iron intake compared with those in the lowest category. Epidemiological data thus show a suggestive association between dietary heme and risk of colon cancer. The analysis of experimental studies in rats with chemically-induced colon cancer showed that dietary hemoglobin and red meat consistently promote aberrant crypt foci, a putative precancer lesion. The mechanism is not known, but heme iron has a catalytic effect on (i) the endogenous formation of carcinogenic N-nitroso compounds and (ii) the formation of cytotoxic and genotoxic aldehydes by lipoperoxidation. A review of evidence supporting these hypotheses suggests that both pathways are involved in heme iron toxicity.

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Quantifying heterogeneity in a meta‐analysis
Higgins, J. P. T., & Thompson, S. G. (2002) · Statistics in Medicine · doi:10.1002/sim.1186 · Cited by 36,763
Food, nutrition, physical activity, and the prevention of cancer: a global perspective
Marmot, M. G., Atinmo, T., Byers, T., Chen, J., Hirohata, T., Jackson, A., James, W., Kolonel, L. N., Kumanyika, S., Leitzmann, C., et al. (2008) · Choice Reviews Online · doi:10.5860/choice.45-5024 · Cited by 5,368
D IETARY F LAVONOIDS : Bioavailability, Metabolic Effects, and Safety
Ross, J. A., & Kasum, C. M. (2002) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.22.111401.144957 · Cited by 2,153
APC mutations occur early during colorectal tumorigenesis
Powell, S. M., Zilz, N. D., Beazer-barclay, Y. D., Bryan, T. M., Hamilton, S. R., Thibodeau, S. N., Vogelstein, B., & Kinzler, K. W. (1992) · Nature · doi:10.1038/359235a0 · Cited by 1,925
Oxyradicals and DNA damage
Marnett, L. J. (2000) · Carcinogenesis · doi:10.1093/carcin/21.3.361 · Cited by 1,922
Lipid peroxidation—DNA damage by malondialdehyde
Marnett, L. J. (1999) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(99)00010-x · Cited by 1,311
Role of N-nitroso compounds (NOC) and N-nitrosation in etiology of gastric, esophageal, nasopharyngeal and bladder cancer and contribution to cancer of known exposures to NOC
Mirvish, S. S. (1995) · Cancer Letters · doi:10.1016/0304-3835(95)03786-v · Cited by 916
Meat consumption and risk of colorectal cancer: A meta‐analysis of prospective studies
Larsson, S. C., & Wolk, A. (2006) · International Journal of Cancer · doi:10.1002/ijc.22170 · Cited by 663
Malondialdehyde, a Product of Lipid Peroxidation, Is Mutagenic in Human Cells
Niedernhofer, L. J., Daniels, J. S., Rouzer, C. A., Greene, R. E., & Marnett, L. J. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m212549200 · Cited by 586
Meat consumption and colorectal cancer risk: Dose‐response meta‐analysis of epidemiological studies
Norat, T., Lukanova, A., Ferrari, P., & Ríboli, E. (2001) · International Journal of Cancer · doi:10.1002/ijc.10126 · Cited by 510

Show all 76 references

Research works printed but not linked: 1

Nauss, 1983, Effect of alteration in the quality and quantity of dietary fat on DMH-induced colon tumorigenesis in rats, Cancer Res, 43, 4083

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Wu, T., Sonoda, S., & Liu, H. (2019) · Nutrition & Dietetics · doi:10.1111/1747-0080.12555 · Cited by 13
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Zhang, X., Ma, J., Wu, K., Chan, A. T., Fuchs, C. S., & Giovannucci, E. L. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039319 · Cited by 13
“[31] Heme iron, mainly found in animal foods, has been shown to have cytotoxic effects in rats [32] and to increase formation of endogenous intestinal N-nitroso compounds, [33] established human carcinogens.”
Background
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Gender and plasma iron biomarkers, but not HFE gene mutations, increase the risk of colorectal cancer and polyps
Castiella, A., Múgica, F., Zapata, E., Zubiaurre, L., Iribarren, A., Juan, M., Alzate, L., Gil, I., Urdapilleta, G., Otazua, P., et al. (2015) · Tumor Biology · doi:10.1007/s13277-015-3406-2 · Cited by 12
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Dahham, S. S., & Majid, A. M. S. A. (2016) · Journal of Applied Pharmaceutical Science · doi:10.7324/japs.2016.60935 · Cited by 12
“Thus, heme iron may promote the initiation of tumor cells by influencing the cytoplasmic and nuclear signal transduction pathways (Bastide et al. , 2011; Sosa et al. , 2013).”
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“These products typically contain high levels of saturated fat, sodium, and preservatives such as nitrites and nitrates, which promote the formation of N-nitroso compounds (NOCs), potent carcinogens that are particularly implicated in colorectal cancer (115).”
Protein intake and cancer: an umbrella review of systematic reviews for the evidence-based guideline of the German Nutrition Society
Kuhn, T. E., Kalotai, N., Amini, A. M., Haardt, J., Lehmann, A. C., Schmidt, A., Buyken, A. E., Egert, S., Ellinger, S., Kroke, A., et al. (2024) · European Journal of Nutrition · doi:10.1007/s00394-024-03380-4 · Cited by 12
“…formed during the preparation such as heterocyclic amines, polycyclic aromatic hydrocarbons, as well as nitrate and N-nitroso-compounds, have been suggested here as underlying mechanisms for the observed positive associations between red and processed meat and prostate cancer risk [70, 71].”
Background
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Onali, T., Slabá, H., Jian, C., Koivumäki, T., Päivärinta, E., Marttinen, M., Määttänen, M., Salonen, A., & Pajari, A. (2025) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2025.109906 · Cited by 11
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Background
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Background
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Background
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“protect the colon mucosa against hemin-induced cytotoxicity/genotoxicity (Bastide et al., 2011).”
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“…to the dual and versatile nature of iron, meat products provide on the one hand a highly nutritional value, but excessive consumption on the other hand promotes the development of non-communicable diseases such as cancer or diabetes and comorbidities such as cardiovascular diseases [12 – 14].”
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Seok, J., Kim, D. H., Kim, H. J., Jo, H. H., Kim, E. Y., Jeong, J., Park, Y. S., Lee, S. H., Kim, D. J., Nam, S.-Y., et al. (2022) · Journal of Veterinary Science · doi:10.4142/jvs.22097 · Cited by 10
“Epidemiological support the concept that heme iron intake significantly increases the risk of colon cancer [4].”
Background
The effect of iron and zinc supplementation and discontinuation of this practice on iron and zinc level in tissues in rats fed deficient diets
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Background
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Background
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Surya, R., Surya, E., Nugroho, D., Romulo, A., Kamal, N., Rahayu, W. P., Benchawattananon, R., & Oh, J.-S. (2023) · Journal of Ethnic Foods · doi:10.1186/s42779-023-00176-5 · Cited by 9
“In addition, calcium and chlorophyll havs also been shown to prevent early colorectal carcinogenesis in heme-fed animal models through heme-trapping mechanism [41].”
Background
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“The hypothesis of a contribution of lipid peroxides to the carcinogenesis of colorectal cancer is widely supported in the literature [5, 10].”
Background
Source-specific nitrate and nitrite intake and association with colorectal cancer in the Danish Diet, Cancer and Health Cohort
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To what extent does the nitrosation of meat proteins influence their digestibility?
Théron, L., Chambon, C., Sayd, T., Pomélie, D. D. L., Santé-Lhoutellier, V., & Gatellier, P. (2018) · Food Research International · doi:10.1016/j.foodres.2018.06.071 · Cited by 9
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Background
Milk and Conjugated Linoleic Acid
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Background
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Background
Associations of red and processed meat with survival among patients with cancers of the upper aerodigestive tract and lung
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“Heme-iron may promote formation of some of these carcinogenic compounds and aldehydes, damaging cells and DNA [32].”
Background
Red Meat and Health
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Micronutrients: A Double-Edged Sword in Microbe-Induced Gastric Carcinogenesis
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Reeves, A., McEvoy, M., MacDonald‐Wicks, L. K., Barker, D., Attia, J., Hodge, A. M., & Patterson, A. J. (2017) · Nutrients · doi:10.3390/nu9050515 · Cited by 6
“A meta-analysis investigating haem iron from meat and the colorectal cancer risk from prospective cohort studies concluded there was a statistically significant association between haem iron and the development of colorectal cancer [35].”
Background
Feasibility of addition of polyphenol-rich vegetable extracts in whole cooked products: Benefits and drawbacks
Barbieri, G., Bergamaschi, M., Franceschini, M., & Barbieri, G. (2018) · Meat Science · doi:10.1016/j.meatsci.2018.01.010 · Cited by 6
Impact on Longevity of Genetic Cardiovascular Risk and Lifestyle including Red Meat Consumption
da Silva, A. P., Costa, M. D. C., Aguiar, L., Matos, A., Gil, Â., Clara, J. G., Polónia, J. J., & Bicho, M. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/1305413 · Cited by 6
“The risk associated with this consumption (Table 1) has been neglected in longevity studies, but it is important that it be deepened because red meat increases heme-iron levels, inducing lipid peroxidation products, generating an inflammatory process and endogenous formation of abnormal NO radical derivatives as nitra…”
Background
Adverse effect after cessation of rats' unjustified iron or iron and zinc supplementation on hematological parameters but not ferritin concentration
Kałuża, J., & Madej, D. (2014) · Clinical Nutrition · doi:10.1016/j.clnu.2013.12.016 · Cited by 6
Alimentation et cancer colorectal
Lafay, L., & Ancellin, R. (2015) · Cahiers de Nutrition et de Diététique · doi:10.1016/j.cnd.2015.03.005 · Cited by 7
The Iron y of Tumor-Induced Inflammation
Greten, F. R. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.08.025 · Cited by 5
“Heme iron has been suggested to have a catalytic effect on the endogenous formation of carcinogenic N-nitroso compounds and the formation of cytotoxic and genotoxic aldehydes by lipid peroxidation, thus increasing mutational load in intestinal epithelia (Bastide et al., 2011).”
Background
Toxigenic gut bacteria, diet and colon carcinogenesis
Keenan, J. I., & Frizelle, F. (2019) · Journal of the Royal Society of New Zealand · doi:10.1080/03036758.2019.1695636 · Cited by 6
“Diets high in red meat are also positively associated with increased risk of CRC (Cross et al. 2010; Bastide et al. 2011; Aune et al. 2013), an association that appears to be largely independent of dietary fat content (Sesink et al.”
Background
Daily berry consumption attenuates β-catenin signalling and genotoxicity in colon carcinoma cells exposed to faecal water from healthy volunteers in a clinical trial
Slabá, H., Määttänen, M., Marttinen, M., Lapinkero, V., Päivärinta, E., & Pajari, A. (2023) · Journal of Functional Foods · doi:10.1016/j.jff.2023.105440 · Cited by 5
Iron supplementation in young iron-deficient females causes gastrointestinal redox imbalance: protective effect of a fermented nutraceutical.
BERTUCCELLI, G., Marotta, F., Zerbinati, N., Cabeca, A., He, F., Jain, S., Lorenzetti, A., Yadav, H., Milazzo, M., Calabrese, F., et al. (2014) · PubMed · Cited by 5
Dietary hemin promotes colonic preneoplastic lesions and DNA damage but not tumor development in a medium-term model of colon carcinogenesis in rats
de Moura, N. A., Caetano, B. F. R., Bidinotto, L. T., Rodrigues, M. A. M., & Barbisan, L. F. (2019) · Mutation Research/Genetic Toxicology and Environmental Mutagenesis · doi:10.1016/j.mrgentox.2019.07.006 · Cited by 5
Lack of Protective Effects of Zinc Gluconate against Rat Colon Carcinogenesis
da Silva, F. R. M., Dias, M. C., Barbisan, L. F., & Rodrigues, M. A. M. (2013) · Nutrition and Cancer · doi:10.1080/01635581.2013.775317 · Cited by 5
Red meat vs. white meat: A comparative analysis of histological characteristics, nutritional profiles, and health implications
Zhang, H., Gan, M., Wu, Q., Dan, H., Chen, L., Niu, L., Zhao, Y., Wang, Y., Zhu, L., & Shen, L. (2025) · Food Chemistry X · doi:10.1016/j.fochx.2025.103211 · Cited by 5
Effects of meat-based, meat-based with α-tocopherol, and pesco-vegetarian diets on biomarkers associated with colorectal cancer risk: a randomized behavioral intervention trial
Dinu, M., Ristori, S., Pagliai, G., Lotti, S., Meriggi, N., Nerini, A., Chevolleau, S., Bowman, J., Caderni, G., Colombini, B., et al. (2025) · Scientific Reports · doi:10.1038/s41598-025-31410-6 · Cited by 5
“…markers capture complementary pathways: lipid peroxidation as indices of heme-driven oxidative injury 32,33 ; SCFAs and bile acids for microbial/epithelial homeostasis and oxidative stress/DNA damage 34–37 ; and iron/inflammatory indices relevant to red-meat exposure and carcinogenesis 8,38–40 .”
Influential
Characterization of diet-linked amino acid pool influence on Fusobacterium spp. growth and metabolism
Robinson, A. V., Vancuren, S. J., Marcone, M. F., & Allen‐Vercoe, E. (2025) · mSphere · doi:10.1128/msphere.00789-24 · Cited by 4
“It has been proposed that N -nitroso compounds resulting from heme iron and/or nitrate metabolism (7) could cause a mutagenic signature in CRC (8).”
Carcinogenicity of food additives: A review
Qadir, A. M., & Salih, D. J. (2025) · European Food Science and Engineering · doi:10.55147/efse.1607021 · Cited by 5
Systematic Analysis of the Differential Effects of Red Meat on Colorectal Cancer Risks: A Meta-Analytic Approach
Woon, J. Y., Vidanapathirana, G. U., Lam, A. K.-Y., & Gopalan, V. (2025) · Journal of Gastrointestinal Cancer · doi:10.1007/s12029-025-01247-3 · Cited by 5
“This correlation also supports the hypothesized role of heme iron in CRC carcinogenesis through NOC formation and lipid peroxidation [62].”
Meat Consumption in Relation to Colorectal Cancer Incidence in Anatomical Subsites in the National Institutes of Health-AARP Diet and Health Study
Zouiouich, S., Wahl, D. H., Liao, L. M., Graubard, B. I., Hong, H. G., Loftfield, E., & Sinha, R. R. (2025) · Current Developments in Nutrition · doi:10.1016/j.cdnut.2025.107540 · Cited by 4
The Importance of Poultry Meat in Medicine: A Review
Jilo, S. A., & Hasan, L. A. (2022) · Journal of World s Poultry Research · doi:10.36380/jwpr.2022.28 · Cited by 6
Calcium-rich dairy matrix protects better than mineral calcium against colonic luminal haem-induced alterations in male rats
Olier, M., Naud, N., Fouché, E., Tondereau, V., Ahn, I., Leconte, N., Blas-Y-Estrada, F., Garric, G., Héliès‐Toussaint, C., Harel-Oger, M., et al. (2024) · npj Science of Food · doi:10.1038/s41538-024-00273-y · Cited by 4
Hemoglobin levels in red blood cells and risk of colorectal cancer: A causal investigation based on Mendelian randomization
Shen, J., Qin, X., Zeng, X. G., Xiao, H., & Lai, S. (2024) · Medicine · doi:10.1097/md.0000000000040562 · Cited by 4
“[22,23] Iron deficiency anemia is prevalent in CRC patients, with studies indicating that female gender, right-sided colon tumors, and larger tumors are risk factors for this condition.”
The association between animal protein, plant protein, and their substitution with bladder cancer risk: a pooled analysis of 10 cohort studies
Beigrezaei, S., Dianatinasab, M., Salehi‐Abargouei, A., Fararouei, M., Akbari-Beni, A., Brinkman, M. T., White, E., Weiderpass, E., Calvez‐Kelm, F. L., Gunter, M. J., et al. (2024) · European Journal of Nutrition · doi:10.1007/s00394-024-03551-3 · Cited by 5
Meat and Cancer Evidence for and Against
Sødring, M. S., Oostindjer, M., Dragsted, L. O., Haug, A., Paulsen, J. E., & Egelandsdal, B. (2017) · Elsevier eBooks · doi:10.1016/b978-0-08-100593-4.00020-5 · Cited by 4
Colorectal Carcinoma and Emerging Targeted Therapies.
Khanal, N., Upadhyay, S., & Silberstein, P. T. (2015) · Europe PMC (PubMed Central) · Cited by 4
Consommation de charcuteries et risque de cancer colorectal : état des lieux et définition d’une prévention nutritionnelle
Pierre, F. (2019) · Cahiers de Nutrition et de Diététique · doi:10.1016/s0007-9960(20)30011-0 · Cited by 4
Free radical-mediated acetaldehyde formation by model reactions of dietary components: effects of meat, wine, cooking oil and coffee
Kasai, H., & Kawai, K. (2021) · Genes and Environment · doi:10.1186/s41021-021-00201-6 · Cited by 4
“In relation to red meat intake, N-nitroso compounds, such as N-nitroso-glucosylglycine, and aldehydic compounds, such as 4-hydroxy-2nonenal and malonaldehyde, generated by heme-induced lipid peroxidation, have been suggested as possible carcinogenesis mechanisms [15], but the role of AcAld has not been described so fa…”
Background
Anti-Oxidant, Pro-Oxidant and Anti-Inflammatory Effects of Unpolished Rice Relevant to Colorectal Cancer
Suwannalert, P., Payuhakrit, W., & Koomsang, T. (2016) · Europe PMC (PubMed Central) · doi:10.22034/apjcp.2016.17.12.5047 · Cited by 4
“MDA can react with DNA to form adducts with deoxyguanosine, deoxyadenosine and deoxycytidine (Bastide et al., 2011).”
Background
Differences in risk factor–colorectal adenoma associations according to non-steroidal anti-inflammatory drug use
Mujtaba, S., & Bostick, R. M. (2018) · European Journal of Gastroenterology & Hepatology · doi:10.1097/meg.0000000000001252 · Cited by 4
Measurement of thermophysical properties of binary system of (water + ascorbic acid) and ternary systems of (water + ascorbic acid + glycerol) and (water + ascorbic acid + d-sorbitol) at T = 293.15 K to 323.15 K and atmospheric pressure
Rostami, A., Kiani, F., Saraei, A. G., Koohyar, F., & Omran, M. M. (2019) · Journal of Molecular Liquids · doi:10.1016/j.molliq.2019.02.117 · Cited by 4
Analytical Tools for Assessing the Chemical Safety of Meat and Poultry
Toldrá, F., & Reig, M. (2012) · Springer eBooks · doi:10.1007/978-1-4614-4277-6 · Cited by 4
Stress oxydant et qualités nutritionnelles des produits animaux
Delosière, M., Damon, M., & Durand, D. (2013) · Cahiers de Nutrition et de Diététique · doi:10.1016/j.cnd.2013.04.006 · Cited by 4
Lack of Association between Red Meat Consumption and a Positive Fecal Immunochemical Colorectal Cancer Screening Test in Khon Kaen, Thailand: a Population- Based Randomized Controlled Trial
Pramual, P., Sarakarn, P., Kamsa‐ard, S., Jirapornkul, C., Maneenin, N., Thavondunstid, P., Juntarach, P., & Promthet, S. S. (2018) · Europe PMC (PubMed Central) · doi:10.22034/apjcp.2018.19.1.271 · Cited by 4
“Based on a meta-analysis, dietary hemoglobin and red meat consistently promote aberrant crypt foci (ACF), putative pre-cancer lesions (Bastide et al., 2011).”
Background
HUMAN NUTRITION | Meat and Human Diet: Facts and Myths
Santé-Lhoutellier, V. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-384731-7.00178-1 · Cited by 4
Convergent relaxation of molecular constraint in herbivores reveals the changing role of liver and kidney functions across mammalian dietsPreprint
Pollard, M. D., Meyer, W. K., & Puckett, E. E. (2024) · Genome Research · doi:10.1101/gr.278930.124 · Cited by 5
Cellular Senescence Triggered by Food and Environmental Genotoxins
Kaina, B., Tomicic, M. T., & Christmann, M. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27052389 · Cited by 3
“Although N-nitrosamines and heterocyclic amines are also formed during the preparation of fish and white, blood-poor meat (chicken and turkey), a correlation between meat consumption and colorectal cancer incidence has only been demonstrated for red meat [176,177].”
Metabolic Engineering of Microbial Cell Factories for Efficient Heme Biosynthesis: Advances, Challenges, and Future Perspectives
Cao, Z., Zhang, X., Li, S., Cao, W., Li, Y., & Lu, F. (2026) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.5c17284 · Cited by 3
The Relation of Lifestyle with Inflammation at the Time of Diagnosis in Patients with Colorectal Cancer
Gielen, A. H. C., Melenhorst, J., Breukink, S. O., Weijenberg, M. P., & Bours, M. J. L. (2023) · Cancers · doi:10.3390/cancers15174307 · Cited by 3
Temperature of Food and Drink Intake Matters
Wong, K. V. (2016) · Journal of Energy Resources Technology · doi:10.1115/1.4032624 · Cited by 3
Regulation and Consumer Interest in an Antioxidant-Enriched Ham Associated with Reduced Colorectal Cancer Risks
Marette, S., Guéraud, F., & Pierre, F. H. F. (2021) · Nutrients · doi:10.3390/nu13051542 · Cited by 3
“Notably, research has examined the effect of heterocyclic amines, N-nitroso compounds, and the ability of heme iron content to catalyze the oxidation of dietary lipids and the nitrosylation [6].”
Background
Role of Food Additives and Intestinal Microflora in Colorectal Cancer
Soni, V. K., Amit, A., Chandra, V., Singh, P. K., Singh, P. K., Singh, R. P., Patel, G. K., & Singh, R. P. (2022) · Springer eBooks · doi:10.1007/978-3-030-72702-4_14 · Cited by 3
Mechanistic Hypotheses on Colorectal Cancer and Red Meat Intake: A Review
Surya, R. (2020) · IOP Conference Series Earth and Environmental Science · doi:10.1088/1755-1315/426/1/012176 · Cited by 4
New Plausible Mechanism for Gastric and Colorectal Carcinogenesis: Free Radical-Mediated Acetaldehyde Generation in a Heme/Myoglobin–Linoleate–Ethanol Mixture
Kasai, H., & Kawai, K. (2021) · ACS Omega · doi:10.1021/acsomega.1c00614 · Cited by 3

Authors: Bastide, N. M., Pierre, F. H. F., & Corpet, D. E.
Affiliations: École Nationale Vétérinaire de Toulouse (FR)
Corresponding author: Pierre, Fabrice H.F.
ORCID: Pierre, Fabrice H.F.
Corpet, Denis E.
Venue: Cancer Prevention Research
Publisher: American Association for Cancer Research (AACR)
Published: 2011-02-01
Volume: 4
Issue: 2
Pages: 177-184
ISSN: 1940-6207 (ISSN-L)
1940-6215
DOI: 10.1158/1940-6207.capr-10-0113
OpenAlex: W2106489922
Cited by: 397
References: 76
Citations by year: 2026: 22 · 2025: 24 · 2024: 18 · 2023: 23 · 2022: 18 · 2021: 24 · 2020: 29 · 2019: 28 · 2018: 29 · 2017: 23 · 2016: 45 · 2015: 31 · 2014: 25 · 2013: 31 · 2012: 19
FWCI: 3.97
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Cancer Prevention Research (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion, other-oa)
Funders: Institut National de la Santé et de la Recherche Médicale
Topics: Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Nutritional Studies and Diet
Health Sciences › Medicine › Oncology › Colorectal Cancer Screening and Detection
Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Meat and Animal Product Quality
Keywords: heme iron, red meat, processed meat, colorectal cancer, colon cancer, aberrant crypt foci, N-nitroso compounds, lipid peroxidation, aldehydes, carcinogenesis mechanisms, hemoglobin
MeSH terms: Animals, Heme, Humans, Meat Products, Review Literature as Topic, Colorectal Neoplasms, Iron, Dietary, Rats

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Heme Iron from Meat and Risk of Colorectal Cancer: A Meta-analysis and a Review of the Mechanisms Involved

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