Heme iron from meat and risk of colorectal cancer: a meta-analysis and a review of the mechanisms involved
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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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High red meat intake increases endogenous formation of N-nitroso compounds in the GI tract, which are associated with increased epithelial proliferation, oxidative stress, and iron-induced hypoxia signaling.
“A high red meat intake (rich in heme iron), increases endogenous formation of N-nitroso compounds in the gastrointestinal tract that are associated with increased epithelial proliferation, oxidative stress, and iron-induced hypoxia signaling (166–168).”
From Food Consumption and its Impact on Cardiovascular Disease: Importance of Solutions Focused on the Globalized Food System (2015) · cites this paper as [167]
Potential mechanisms linking unprocessed red meat with CVD include saturated fat, cholesterol, iron, phosphatidylcholine, carnitine, and cooking methods that increase heterocyclic amine content and N-nitroso compounds.
“Potential mechanisms linking unprocessed red meat with CVD include saturated fat, cholesterol, iron, phosphatidylcholine, and carnitine; and cooking methods (e.g., barbecuing), that increase heterocyclic amine content and N-nitroso compounds, also implicated in colorectal cancer (167).”
From Food Consumption and its Impact on Cardiovascular Disease: Importance of Solutions Focused on the Globalized Food System (2015) · cites this paper as [167]
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Involvement of a Non-Human Sialic Acid in Human Cancer
Samraj, A. N., Läubli, H., Varki, N., & Varki, A. (2014) · Frontiers in Oncology · doi:10.3389/fonc.2014.00033 · Cited by 196 · see citing works
“There have been several mechanisms proposed by which red meat consumption increases the risk of cancer including: (1) high-fat intake (96); (2) the production of heterocyclic amines and polycyclic aromatic hydrocarbons formed by high temperatures during grilling (97); (3) the presence of mutagenic N -nitroso compounds…”
BackgroundMechanisms Linking Colorectal Cancer to the Consumption of (Processed) Red Meat: A Review
Demeyer, D. I., Mertens, B., SMET, S. D., & Ulens, M. (2015) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2013.873886 · Cited by 193 · see citing works
“Due to the nitrate and nitrite present in the curing salt, heme iron occurs in its nitrosylated form in processed red meat (Bastide et al., 2011).”
BackgroundResultInfluentialInnovations for healthier processed meats
Toldrá, F., & Reig, M. (2011) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2011.08.007 · Cited by 193 · see citing works
Kabe, Y., Nakane, T., Koike, I., Yamamoto, T., Sugiura, Y., Harada, E., Sugase, K., Shimamura, T., Ohmura, M., Muraoka, K., et al. (2016) · Nature Communications · doi:10.1038/ncomms11030 · Cited by 190 · see citing works
Red meat and colorectal cancer
Aykan, N. F. (2015) · Oncology Reviews · doi:10.4081/oncol.2015.288 · Cited by 188 · see citing works
Colorectal carcinogenesis-update and perspectives
Raskov, H. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i48.18151 · Cited by 182 · see citing works
The role of red and processed meat in colorectal cancer development: a perspective
Oostindjer, M., Alexander, J., Amdam, G. V., Andersen, G., Bryan, N. S., Chen, D., Corpet, D. E., SMET, S. D., Dragsted, L. O., Haug, A., et al. (2014) · Meat Science · doi:10.1016/j.meatsci.2014.02.011 · Cited by 178 · see citing works
Abid, Z., Cross, A. J., & Sinha, R. R. (2014) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.113.071597 · Cited by 165 · see citing works
Meat subtypes and their association with colorectal cancer: Systematic review and meta‐analysis
Carr, P. R., Walter, V., Brenner, H., & Hoffmeister, M. (2015) · International Journal of Cancer · doi:10.1002/ijc.29423 · Cited by 157 · see citing works
“A meta-analysis which compared the highest versus lowest category of heme iron consumption found an 18% increased risk of colon cancer with higher intake of heme iron.(8) Our meta-analysis supports these results since we found a 24% increased risk of colon cancer with beef consumption, which has a higher heme iron con…”
BackgroundResultLeu, R. K. L., Winter, J. M., Christophersen, C. T., Young, G. P., Humphreys, K. J., Hu, Y. C., Gratz, S. W., Miller, R. B., Topping, D. L., Bird, A. R., et al. (2015) · British Journal Of Nutrition · doi:10.1017/s0007114515001750 · Cited by 158 · see citing works
“and processed meat consumption and the risk of CRC((5)).”
InfluentialDietary Fat and Cancer—Which Is Good, Which Is Bad, and the Body of Evidence
Bojková, B., Winklewski, P. J., & Wszędybył-Winklewska, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21114114 · Cited by 158 · see citing works
Alisson-Silva, F., Kawanishi, K., & Varki, A. (2016) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2016.07.002 · Cited by 156 · see citing works
“intake of “white meat” as chicken did not induce the generation of the same carcinogenic compounds (Bastide et al., 2011; Cross et al., 2003).”
InfluentialReview of the association between meat consumption and risk of colorectal cancer
Kim, E., Coelho, D., & Blachier, F. (2013) · Nutrition Research · doi:10.1016/j.nutres.2013.07.018 · Cited by 155 · see citing works
“[99] Bastide NM, Pierre FH, Corpet DE.”
BackgroundXue, X., Taylor, M. J., Anderson, E. R., Hao, C., Qu, A., Greenson, J. K., Zimmermann, E. M., Gonzalez, F. J., & Shah, Y. M. (2012) · Cancer Research · doi:10.1158/0008-5472.can-11-3836 · Cited by 146 · see citing works
“Increase in local iron levels have been implicated in the progression colon carcinogenesis (19-25), and the present data demonstrate the increase in tumor iron exacerbated cell proliferation and was critical in colon tumor formation”
BackgroundDiallo, A., Deschasaux, M., Latino‐Martel, P., Herçberg, S., Galan, P., Fassier, P., Allès, B., Guéraud, F., Pierre, F. H., & Touvier, M. (2017) · International Journal of Cancer · doi:10.1002/ijc.31046 · Cited by 147 · see citing works
“Potential carcinogens include heme iron, nitrates and nitrites and mutagenic compounds such as neoformed products generated in red meats and processed meat (heterocyclic amines, polycyclic aromatic hydrocarbons, N-nitroso compounds.(3,5,6) However, these procarcinogens may also be involved in more systemic mechanisms,…”
BackgroundBernstein, A. M., Song, M., Zhang, X., Pan, A., Wang, M., Fuchs, C. S., Le, N. T., Chan, A. T., Willett, W. C., Ogino, S., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0135959 · Cited by 143 · see citing works
Comparison of carnivore, omnivore, and herbivore mammalian genomes with a new leopard assembly
Kim, S., Cho, Y. S., Kim, H., Chung, O., Kim, H., Jho, S., Seomun, H., Kim, J., Bang, W. Y., Kim, C., et al. (2016) · Genome biology · doi:10.1186/s13059-016-1071-4 · Cited by 140 · see citing works
“We interpret this result as a dietary adaptation for high meat consumption that is associated with an increased risk of cancer in humans [46], and that the heme-related reactive oxygen species (ROS) in meat cause DNA damage and disrupt normal cell proliferation [47, 48].”
BackgroundColorectal cancer risk and nitrate exposure through drinking water and diet
Espejo‐Herrera, N., Gràcia‐Lavedan, E., Boldo, E., Aragonés, N., Pérez‐Gómez, B., Pollán, M., Molina, A. J., Fernández‐Villa, T., Martín, V., Vecchia, C. L., et al. (2016) · International Journal of Cancer · doi:10.1002/ijc.30083 · Cited by 136 · see citing works
“Information on heme iron intake was not available in this study, but should be accounted to evaluate the interaction with red meat in future analysis.(39) In contrast, inverse associations were found in groups of high vitamin E or fiber intake.”
BackgroundGut Microbes, Diet, and Cancer
Hullar, M. A. J., Burnett‐Hartman, A. N., & Lampe, J. W. (2013) · Cancer treatment and research · doi:10.1007/978-3-642-38007-5_22 · Cited by 135 · see citing works
Blachier, F., Beaumont, M., Andriamihaja, M., Davila, A., Lan, A., Grauso, M., Armand, L., Benamouzig, R., & Tomé, D. (2017) · American Journal Of Pathology · doi:10.1016/j.ajpath.2016.11.015 · Cited by 131 · see citing works
“These heme characteristics may explain the positive association between the heme intake and the risk of colorectal cancer risk.(65) However, not all epidemiological studies found correlation between dietary heme consumption and colorectal cancer incidence,(66) challenging this concept and suggesting that heme may syne…”
BackgroundColon Carcinogenesis: The Interplay Between Diet and Gut Microbiota
Loke, Y. L., Chew, M. T., Ngeow, Y. F., Lim, W. W.-D., & Peh, S. C. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.603086 · Cited by 129 · see citing works
“Heme Iron Red meat but not white meat, is associated with an elevated risk of CRC, and this has been linked to heme iron (Cross et al., 2010; Bastide et al., 2011; Oostindjer et al., 2014).”
BackgroundInfluentialHoffman, R. M., & Gerber, M. (2013) · Nutrition Reviews · doi:10.1111/nure.12040 · Cited by 128 · see citing works
Latino‐Martel, P., Cottet, V., Druesne‐Pecollo, N., Pierre, F. H. F., Touillaud, M. S., Touvier, M., Vasson, M., Deschasaux, M., Merdy, J. L., Barrandon, É., et al. (2016) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2016.01.002 · Cited by 125 · see citing works
Turesky, R. J. (2018) · CHIMIA International Journal for Chemistry · doi:10.2533/chimia.2018.718 · Cited by 127 · see citing works
Kralik, G., Kralik, Z., Grčević, M., & Hanžek, D. (2018) · InTech eBooks · doi:10.5772/intechopen.72865 · Cited by 134 · see citing works
Mutagenesis by Microbe: the Role of the Microbiota in Shaping the Cancer Genome
Barrett, M., Hand, C. K., Shanahan, F., Murphy, T., & O’Toole, P. W. (2020) · Trends in Cancer · doi:10.1016/j.trecan.2020.01.019 · Cited by 108 · see citing works
Iron: An Essential Element of Cancer Metabolism
Hsu, M. Y., Mina, E., Roetto, A., & Porporato, P. E. (2020) · Cells · doi:10.3390/cells9122591 · Cited by 116 · see citing works
“The latter has been given particular attention in epidemiology, and high heme content in red meat was found to contribute to colorectal cancer [12,13].”
BackgroundSteppeler, C., Haugen, J., Rødbotten, R., & Kirkhus, B. (2015) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.5b04201 · Cited by 113 · see citing works
Red Meat and Colorectal Cancer: A Quantitative Update on the State of the Epidemiologic Science
Alexander, D. D., Weed, D. L., Miller, P. E., & Mohamed, M. A. (2015) · Journal of the American College of Nutrition · doi:10.1080/07315724.2014.992553 · Cited by 111 · see citing works
“In a recent review of heme iron from meat and CRC, a proposed mechanism of action was suggested whereby heme promotes ATNC (apparent total Nnitroso compounds) growth and lipid peroxidation production [66].”
BackgroundIron intake, body iron status, and risk of breast cancer: a systematic review and meta-analysis
Chang, V. C., Cotterchio, M., & Khoo, E. (2019) · BMC Cancer · doi:10.1186/s12885-019-5642-0 · Cited by 111 · see citing works
Fang, X., An, P., Wang, H., Wang, X., Shen, X., Li, X., Min, J., Liu, S., & Wang, F. (2014) · Nutrition Metabolism and Cardiovascular Diseases · doi:10.1016/j.numecd.2014.09.002 · Cited by 113 · see citing works
Food Processing and the Mediterranean Diet
Hoffman, R. M., & Gerber, M. (2015) · Nutrients · doi:10.3390/nu7095371 · Cited by 105 · see citing works
“Since this study, six prospective studies [193–198], three meta-analyses [199–201] and one analysis of pooled studies [202] have shown some inconsistencies in relation to processed meat which might be related to different processing methods of meat between countries.”
ResultSustainable ruminant production to help feed the planet
Pulina, G., Francesconi, A. H. D., Stefanon, B., Sevi, A., Calamari, L., Lacetera, N., DELL’ORTO, V., Pilla, F., Ajmone‐Marsan, P., Mele, M. L., et al. (2016) · Italian Journal of Animal Science · doi:10.1080/1828051x.2016.1260500 · Cited by 106 · see citing works
“…of nitrates and nitrites in processed meat and, finally, the polycyclic aromatic compounds (PHCs) that are formed during the cooking of red meat (Bastide et al. 2011) The main concern about Fe-heme regards its tendency to promote the production of heterocyclic amines in the intestine, which, in…”
BackgroundInfluentialColorectal cancer and medicinal plants: Principle findings from recent studies
Benarba, B., & Pandiella, A. (2018) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2018.08.006 · Cited by 97 · see citing works
Association Between Red and Processed Meat Intake and Mortality Among Colorectal Cancer Survivors
McCullough, M. L., Gapstur, S. M., Shah, R. A., Jacobs, E. J., & Campbell, P. T. (2013) · Journal of Clinical Oncology · doi:10.1200/jco.2013.49.1126 · Cited by 97 · see citing works
Cascella, M., Bimonte, S., Barbieri, A., Vecchio, V. D., Caliendo, D., Schiavone, V., Fusco, R., Granata, V., Arra, C., & Cuomo, A. (2018) · Infectious Agents and Cancer · doi:10.1186/s13027-018-0174-9 · Cited by 96 · see citing works
Animal Proteins as Important Contributors to a Healthy Human Diet
Elmadfa, I., & Meyer, A. L. (2016) · Annual Review of Animal Biosciences · doi:10.1146/annurev-animal-022516-022943 · Cited by 102 · see citing works
Pierre, F. H. F., Martin, O. C. B., Santarelli, R. L., Taché, S., Naud, N., Guéraud, F., Audebert, M., Dupuy, J., Meunier, N., Attaix, D., et al. (2013) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.113.061069 · Cited by 95 · see citing works
“Nitrosation and heme iron hypotheses have received most experimental support (3).”
BackgroundHever, J., & Cronise, R. J. (2017) · Europe PMC (PubMed Central) · doi:10.11909/j.issn.1671-5411.2017.05.012 · Cited by 94 · see citing works
Plant-Based Diets: A Physician’s Guide
Hever, J. (2016) · The Permanente Journal · doi:10.7812/tpp/15-082 · Cited by 89 · see citing works
Meng, Y., Sun, J., Yu, J. Q., Wang, C., & Su, J. (2018) · Biological Trace Element Research · doi:10.1007/s12011-018-1474-z · Cited by 87 · see citing works
Intestinal Iron Homeostasis and Colon Tumorigenesis
Xue, X., & Shah, Y. M. (2013) · Nutrients · doi:10.3390/nu5072333 · Cited by 83 · see citing works
“Furthermore, heme iron from red meat could also promote colon carcinogenesis through its catalytic effects on the formation of carcinogenic N-nitroso compounds or cytotoxic and genotoxic secondary lipid oxidation products, such as 4-hydroxy-2(E)-nonenal (HNE) [52–54].”
BackgroundGeneral Aspects of Metal Ions as Signaling Agents in Health and Disease
Krzywoszyńska, K., Witkowska, D., Świa̧tek-Kozłowska, J., Szebesczyk, A., & Kozłowski, H. (2020) · Biomolecules · doi:10.3390/biom10101417 · Cited by 82 · see citing works
Time trends of colorectal cancer incidence and associated lifestyle factors in South Korea
Khil, H., Kim, S., Hong, S., Gil, H., Cheon, E., Lee, D. H., Kim, Y. A., & Keum, N. (2021) · Scientific Reports · doi:10.1038/s41598-021-81877-2 · Cited by 82 · see citing works
Nogacka, A. M., Gómez‐Martín, M., Suárez, A., González‐Bernardo, Ó., Reyes‐Gavilán, C. G. D. L., & González, S. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20082051 · Cited by 81 · see citing works
“In this regard, haem iron, in addition to being related to the production of NOCs at the intestinal level, has been associated with the generation of aldehydes with cytotoxic and genotoxic properties [42].”
BackgroundMeat intake and cancer risk: prospective analyses in UK Biobank
Knüppel, A., Papier, K., Fensom, G. K., Appleby, P. N., Schmidt, J. A., Tong, T. Y. N., Travis, R. C., Key, T. J., & Perez‐Cornago, A. (2020) · International Journal of Epidemiology · doi:10.1093/ije/dyaa142 · Cited by 81 · see citing works
Protective effects of yacon (Smallanthus sonchifolius) intake on experimental colon carcinogenesis
de Moura, N. A., Caetano, B. F. R., Sivieri, K., Urbano, L. H., Cabello, C., Rodrigues, M. A. M., & Barbisan, L. F. (2012) · Food and Chemical Toxicology · doi:10.1016/j.fct.2012.05.006 · Cited by 81 · see citing works
“Although its etiology is multifactorial and complex, it is generally accepted that the hereditary genetic component associated with dietary habits such as low intake of fibers, proteins, fruits and vegetables as well as diets with high red and processed meat and fat levels are among the greatest risk factors (Khan et…”
BackgroundDiscovery and Features of an Alkylating Signature in Colorectal Cancer
Gurjao, C., Zhong, R., Haruki, K., Li, Y. Y., Spurr, L. F., Lee-Six, H., Reardon, B. M., Ugai, T., Zhang, X., Cherniack, A. D., et al. (2021) · Cancer Discovery · doi:10.1158/2159-8290.cd-20-1656 · Cited by 79 · see citing works
“The suggested mechanism is mutagenesis through alkylating damage induced by N-nitroso-compounds (NOC), which are metabolic products of blood heme iron or meat nitrites/ nitrates (11).”
Iron Load Toxicity in Medicine: From Molecular and Cellular Aspects to Clinical Implications
Kontoghiorghes, G. J. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241612928 · Cited by 79 · see citing works
The role of oral iron in the treatment of adults with iron deficiency
Lo, J. O.-T., Benson, A. E., Martens, K. L., Hedges, M. A., McMurry, H. S., DeLoughery, T. G., Aslan, J. E., & Shatzel, J. J. (2022) · European Journal Of Haematology · doi:10.1111/ejh.13892 · Cited by 77 · see citing works
“associated with heme-iron have been previously raised, as red meat and processed meat consumption has been linked to the incidence of colon cancer in certain epidemiologic studies and in some preclinical studies using mouse models.(34) While there are not definitive studies on this topic, studies that parse out the so…”
ResultQiao, L., & Feng, Y. (2013) · Cancer Causes & Control · doi:10.1007/s10552-013-0197-x · Cited by 75 · see citing works
Ijssennagger, N., Rijnierse, A., de Wit, N. J. W., Jonker-Termont, D. S. M. L., Dekker, J. P., Müller, M. M., & van der Meer, R. (2011) · Gut · doi:10.1136/gutjnl-2011-300239 · Cited by 75 · see citing works
Dietary patterns and colorectal cancer: results from a Canadian population-based study
Chen, Z., Wang, P., Woodrow, J. R., Zhu, Y., Roebothan, B., McLaughlin, J. R., & Parfrey, P. S. (2015) · Nutrition Journal · doi:10.1186/1475-2891-14-8 · Cited by 76 · see citing works
“Another possible mechanism is that heme, sodium nitrate, nitrite and N-nitroso compounds, which were found in lots of red meat and processed meat, have been associated with higher CRC risk [32-35].”
BackgroundRombouts, C., Hemeryck, L., HECKE, T. V., SMET, S. D., Vos, W. H. D., & Vanhaecke, L. (2017) · Scientific Reports · doi:10.1038/srep42514 · Cited by 74 · see citing works
Iron in red meat–friend or foe
Czerwonka, M., & Tokarz, A. (2016) · Meat Science · doi:10.1016/j.meatsci.2016.09.012 · Cited by 80 · see citing works
Martin, O. C. B., Olier, M., Ellero‐Simatos, S., Naud, N., Dupuy, J., Laurence Therese, H. U. C., Taché, S., Graillot, V., Levêque, M., Bézirard, V., et al. (2019) · Microbiome · doi:10.1186/s40168-019-0685-7 · Cited by 72 · see citing works
“Several red meat components have been suspected to explain the link with colorectal cancer risk, including animal fat and proteins, heterocyclic amines, N-nitroso compounds, and haem iron [2, 3].”
BackgroundPham, N. M., Mizoue, T., Tanaka, K., Tsuji, I., Tamakoshi, A., Matsuo, K., Wakai, K., Nagata, C., Inoue, M., Tsugane, S., et al. (2014) · Japanese Journal of Clinical Oncology · doi:10.1093/jjco/hyu061 · Cited by 73 · see citing works
“Heme iron can also induce DNA damage (55), which is involved in carcinogenesis (56), and catalyze the formation of cytotoxic and genotoxic aldehydes (15).”
BackgroundDietary heme iron and the risk of colorectal cancer with specific mutations in KRAS and APC
Gilsing, A. M. J., Fransen, F., de Kok, T. M. C. M., Goldbohm, A., Schouten, L. J., A, A. P. D. B., van Engeland, M., van den Brandt, P. A., de Goeij, A. F. P. M., & Weijenberg, M. P. (2013) · Carcinogenesis · doi:10.1093/carcin/bgt290 · Cited by 73 · see citing works
“A recently conducted meta-analysis of five prospective studies showed a consistent, though modest, increased risk of 18% comparing the highest to the lowest category of heme iron intake (11).”
BackgroundXu, X., Yu, E., Gao, X., Song, N., Liu, L., Wei, X., Zhang, W., & Fu, C. (2012) · International Journal of Cancer · doi:10.1002/ijc.27625 · Cited by 72 · see citing works
“Additionally, heme iron from red meat might be another potential risk factor for CRC development.(8) It has been established that most CRCs arise from colorectal adenoma (CRA) by a process referred to as the adenoma–carcinoma sequence.”
BackgroundWindey, K., Preter, V. D., Louat, T., Schuit, F. C., Herman, J., Vansant, G. A. A. M., & Verbeke, K. (2012) · PLoS ONE · doi:10.1371/journal.pone.0052387 · Cited by 72 · see citing works
“As high meat intake is not only associated with higher protein intake but also with a higher intake of fat [14], heterocyclic amines [18] and heme [19], it is extremely difficult to attribute the increased CRC and IBD risk to protein intake or fermentation.”
BackgroundChiavarini, M., Bertarelli, G., Minelli, L., & Fabiani, R. (2017) · Nutrients · doi:10.3390/nu9050514 · Cited by 70 · see citing works
“Meat is rich in heme iron which has been implicated in the colon carcinogenesis by promoting oxidative damage and nitrosilation [7].”
BackgroundMeat-Related Compounds and Colorectal Cancer Risk by Anatomical Subsite
Miller, P. E., Lazarus, P. J., Lesko, S. M., Cross, A. J., Sinha, R. R., Laio, J., Zhu, J., Harper, G. R., Muscat, J. E., & Hartman, T. J. (2013) · Nutrition and Cancer · doi:10.1080/01635581.2013.756534 · Cited by 67 · see citing works
“Several individual compounds have been suggested to explain the underlying mechanisms by which red and processed meat may increase the risk of colorectal cancer, including heme iron (8,9), heterocyclic amines (HCAs) (8,10), polycyclic aromatic hydrocarbons (PAHs) (11), and nitrites and nitrates (8,12).”
BackgroundZhong, Y., Zhu, Y., Li, Q., Wang, F., Ge, X., Zhou, G., & Miao, L. (2020) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqaa083 · Cited by 67 · see citing works
Lee, S. Y., Lee, D. Y., Kang, J. H., Kim, J. H., Jeong, J. W., Kim, H. W., Oh, D. H., Yoon, S. H., & Hur, S. J. (2022) · Food Research International · doi:10.1016/j.foodres.2022.111327 · Cited by 67 · see citing works
Joshi, A. D., Kim, A., Lewinger, J. P., Ulrich, C. M., Potter, J. D., Cotterchio, M., Marchand, L. L., & Stern, M. C. (2015) · Cancer Medicine · doi:10.1002/cam4.461 · Cited by 64 · see citing works
“A meta-analysis of prospective cohort studies reported evidence for a positive association between heme intake and CRC risk [8].”
BackgroundIs Timing Important? The Role of Diet and Lifestyle During Early Life on Colorectal Neoplasia
Nimptsch, K., & Wu, K. (2018) · Current Colorectal Cancer Reports · doi:10.1007/s11888-018-0396-7 · Cited by 63 · see citing works
Katidi, A., Xypolitaki, K., Vlassopoulos, A., & Kapsokefalou, M. (2023) · Nutrients · doi:10.3390/nu15020401 · Cited by 66 · see citing works
Parr, C. L., Hjartåker, A., Lund, E., & Veierød, M. B. (2013) · International Journal of Cancer · doi:10.1002/ijc.28101 · Cited by 62 · see citing works
Jeyakumar, A., Dissabandara, L., & Gopalan, V. (2016) · Journal of Gastroenterology · doi:10.1007/s00535-016-1294-x · Cited by 64 · see citing works
Bastide, N. M., Morois, S., Cadeau, C., Kangas, S. T., Serafini, M., Gusto, G., Dossus, L., Pierre, F. H. F., Clavel‐Chapelon, F., & Boutron‐Ruault, M. (2016) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-15-0724 · Cited by 60 · see citing works
“In processed red meat, heme iron is nitrosylated because curing salt contains nitrate or nitrite (5), and the International Agency for Research on Cancer recently classified processed red meat as a carcinogen (8).”
BackgroundResultInfluentialQamar, T. R., Syed, F., Nasir, M., Rehman, H., Zahid, M., Liu, R., & Iqbal, S. (2016) · Nutrients · doi:10.3390/nu8080465 · Cited by 59 · see citing works
“Being quite a complex process, many factors contribute to the onset of colon cancer and the major risk factors include family history, age, pre-carcinogens present in the food chain and environment [1,2], inflammatory bowel diseases, low intake of vegetables, fruits and fibers, high consumption of red meat and process…”
BackgroundHeme Iron Intake and Risk of Stroke
Kałuża, J., Wolk, A., & Larsson, S. C. (2013) · Stroke · doi:10.1161/strokeaha.112.679662 · Cited by 58 · see citing works
A prospective study of intakes of zinc and heme iron and colorectal cancer risk in men and women
Zhang, X., Giovannucci, E. L., Smith‐Warner, S. A., Wu, K., Fuchs, C. S., Pollak, M., Willett, W. C., & Ma, J. (2011) · Cancer Causes & Control · doi:10.1007/s10552-011-9839-z · Cited by 55 · see citing works
Lei, L., Zhang, J., Decker, E. A., & Zhang, G. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.665591 · Cited by 57 · see citing works
Iron metabolism in colorectal cancer: a balancing act
Estêvão, D., da Cruz-Ribeiro, M., Cardoso, A. P., Costa, Â. M., Oliveira, M. J., Duarte, T. L., & Cruz, T. (2023) · Cellular Oncology · doi:10.1007/s13402-023-00828-3 · Cited by 54 · see citing works
“Additionally, heme iron is a potential pro-oxidant capable of generating reactive oxygen species (ROS), acting as a nitrosating agent, and consequently, increasing lipid peroxidation and carcinogenic N-nitroso compounds [21, 33, 39].”
BackgroundWhat causes human cancer? Approaches from the chemistry of DNA damage
Kasai, H. (2016) · Genes and Environment · doi:10.1186/s41021-016-0046-8 · Cited by 52 · see citing works
“Based on epidemiological studies, a higher intake of heme iron is positively associated with colorectal cancer risk [46].”
BackgroundDiet and Lifestyle in Survivors of Colorectal Cancer
Lee, J., Jeon, J. Y., & Meyerhardt, J. A. (2014) · Hematology/Oncology Clinics of North America · doi:10.1016/j.hoc.2014.09.005 · Cited by 51 · see citing works
Diallo, A., Srour, B., Sellem, L., Deschasaux, M., Latino‐Martel, P., Herçberg, S., Galan, P., Fassier, P., Guéraud, F., Pierre, F. H. F., et al. (2018) · International Journal of Cancer · doi:10.1002/ijc.31593 · Cited by 53 · see citing works
“heterocyclic amines, polycyclic aromatic hydrocarbons, N-nitroso compounds.(10,11) However, the links between other animal products, notably dairies, and cancer risk are still unclear.”
BackgroundBaradat, M., Jouanin, I., Dalleau, S., Taché, S., Gieules, M., Debrauwer, L., Canlet, C., Laurence Therese, H. U. C., Dupuy, J., Pierre, F. H. F., et al. (2011) · Chemical Research in Toxicology · doi:10.1021/tx2003036 · Cited by 50 · see citing works
- Authors
- Bastide, N. M., Pierre, F. H. F., & Corpet, D. E.
- Affiliations
- École Nationale Vétérinaire de Toulouse (FR)
- Corresponding author
- Pierre, Fabrice H.F.
- Venue
- Cancer Prevention Research
- Published
- 2011-02-01
- Volume
- 4
- Issue
- 2
- Pages
- 177-184
- ISSN
- 1940-6207 (ISSN-L)
- 1940-6215
- 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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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
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