Meat and meat-related compounds and risk of prostate cancer in a large prospective cohort study in the United States
Open accessAbstract
The authors examined associations between meat consumption (type, cooking method, and related mutagens), heme iron, nitrite/nitrate, and prostate cancer in a cohort of 175,343 US men aged 50-71 years. During 9 years of follow-up (1995-2003), they ascertained 10,313 prostate cancer cases (1,102 advanced) and 419 fatal cases. Hazard ratios comparing the fifth intake quintile with the first revealed elevated risks associated with red and processed meat for total (red meat: hazard ratio (HR) = 1.12, 95% confidence interval (CI): 1.04, 1.21; processed meat: HR = 1.07, 95% CI: 1.00, 1.14) and advanced (red meat: HR = 1.31, 95% CI: 1.05, 1.65; processed meat: HR = 1.32, 95% CI: 1.08, 1.61) prostate cancer. Heme iron, barbecued/grilled meat, and benzo[a]pyrene were all positively associated with total (HR = 1.09 (95% CI: 1.02, 1.17), HR = 1.11 (95% CI: 1.03, 1.19), and HR = 1.09 (95% CI: 1.00, 1.18), respectively) and advanced (HR = 1.28 (95% CI: 1.03, 1.58), HR = 1.36 (95% CI: 1.10, 1.69), and HR = 1.28 (95% CI: 1.00, 1.65), respectively) disease. Nitrite (HR = 1.24, 95% CI: 1.02, 1.51) and nitrate (HR = 1.31, 95% CI: 1.07, 1.61) intakes were associated with advanced prostate cancer. There were no clear associations for fatal prostate cancer. Red and processed meat may be positively associated with prostate cancer via mechanisms involving heme iron, nitrite/nitrate, grilling/barbecuing, and benzo[a]pyrene.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Nitrites in combination with dietary amines or amides, such as in red and cured meats, have been linked to stomach and several other cancers.
“Indeed, nitrites in combination with dietary amines or amides, such as in red and cured meats, have been linked to stomach and several other cancers[155,157,160,163–166].”
From Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health (2017) · cites this paper as [165]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
(2016) · Springer eBooks · doi:10.1007/978-3-319-40618-3 · Cited by 17,280 · see citing works
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 5,365 · see citing works
Self-citationTotal energy intake: implications for epidemiologic analyses.
WILLETT, W., & STAMPFER, M. J. (1986) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a114366 · Cited by 2,751 · see citing works
RE: “TOTAL ENERGY INTAKE: IMPLICATIONS FOR EPIDEMIOLOGIC ANALYSES”
Palmgren, J., & Kushi, L. H. (1991) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a115841 · Cited by 2,712 · see citing works
Cancers of the prostate and breast among Japanese and white immigrants in Los Angeles County
Shimizu, H., Ross, R., Bernstein, L., Yatani, R., Henderson, B. E., & Mack, T. (1991) · British Journal of Cancer · doi:10.1038/bjc.1991.210 · Cited by 890 · see citing works
(1980) · Environmental Pollution Series A Ecological and Biological · doi:10.1016/0143-1471(80)90144-0 · Cited by 633 · see citing works
Design and Serendipity in Establishing a Large Cohort with Wide Dietary Intake Distributions
Schatzkin, A. G., Subar, A. F., Thompson, F. E., Harlan, L. C., Tangrea, J. A., Hollenbeck, A. R., Hurwitz, P. E., Coyle, L. M., Schussler, N., Michaud, D. S., et al. (2001) · American Journal of Epidemiology · doi:10.1093/aje/154.12.1119 · Cited by 611 · see citing works
Self-citationAnalysis of 200 food items for benzo[a]pyrene and estimation of its intake in an epidemiologic study
Kazerouni, N., Sinha, R. R., Hsu, C.-H., Greenberg, A., & Rothman, N. (2001) · Food and Chemical Toxicology · doi:10.1016/s0278-6915(00)00158-7 · Cited by 532 · see citing works
Self-citationA Prospective Study of Red and Processed Meat Intake in Relation to Cancer Risk
Cross, A. J., Leitzmann, M. F., Gail, M. H., Hollenbeck, A. R., Schatzkin, A. G., & Sinha, R. R. (2007) · PLoS Medicine · doi:10.1371/journal.pmed.0040325 · Cited by 476 · see citing works
Self-citationMeat‐related mutagens/carcinogens in the etiology of colorectal cancer
Cross, A. J., & Sinha, R. R. (2004) · Environmental and Molecular Mutagenesis · doi:10.1002/em.20030 · Cited by 439 · see citing works
Self-citationShirai, T., Sano, M. E. B., Tamano, S., Takahashi, S., Hirose, M., Futakuchi, M., Hasegawa, R., Imaida, K., Matsumoto, K., Wakabayashi, K., et al. (1997) · PubMed · Cited by 392 · see citing works
(2003) · PubMed · Cited by 381 · see citing works
Overview of carcinogenic heterocyclic amines
Sügimura, T. (1997) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(97)00045-6 · Cited by 331 · see citing works
Sinha, R. R., Rothman, N., Salmon, C. P., Knize, M. G., Brown, E. D., Swanson, C. A., Rhodes, D., Rossi, S. C., Felton, J. S., & Levander, O. A. (1998) · Food and Chemical Toxicology · doi:10.1016/s0278-6915(97)00162-2 · Cited by 284 · see citing works
Self-citationA comparison of the tumors induced by coal tar and benzo[a]pyrene in a 2-year bioassay
Culp, S. (1998) · Carcinogenesis · doi:10.1093/carcin/19.1.117 · Cited by 284 · see citing works
Total Heme and Non‐heme Iron in Raw and Cooked Meats
Lombardi‐Boccia, G., Martínez, B., & Aguzzi, A. (2002) · Journal of Food Science · doi:10.1111/j.1365-2621.2002.tb08715.x · Cited by 255 · see citing works
Diet: Fat, Meat, and Prostate Cancer
Kolonel, L. N. (2001) · Epidemiologic Reviews · doi:10.1093/oxfordjournals.epirev.a000798 · Cited by 239 · see citing works
Cook, L. S., Goldoft, M., SCHWARTZ, S. M., et al. (1999) · The Journal of Urology · doi:10.1016/s0022-5347(01)62086-x · Cited by 235 · see citing works
Dose-dependent effect of dietary meat on endogenous colonic N-nitrosation
Hughes, R. (2001) · Carcinogenesis · doi:10.1093/carcin/22.1.199 · Cited by 234 · see citing works
Adamson, R. H., Thorgeirsson, U. P., Snyderwine, E. G., et al. (1990) · Japanese Journal of Cancer Research · doi:10.1111/j.1349-7006.1990.tb02500.x · Cited by 229 · see citing works
Sinha, R. R., Knize, M. G., Salmon, C. P., Brown, E. D., Rhodes, D., Felton, J. S., Levander, O. A., & Rothman, N. (1998) · Food and Chemical Toxicology · doi:10.1016/s0278-6915(97)00159-2 · Cited by 226 · see citing works
Self-citationLewin, M., Bailey, N., Bandaletova, T., Bowman, R., Cross, A. J., Pollock, J. R. A., Shuker, D. E. G., & Bingham, S. A. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-2237 · Cited by 219 · see citing works
Self-citationA prospective study on intake of animal products and risk of prostate cancer
Michaud, D. S., Bälter, K. A., Rimm, E. B., Stampfer, M. J., Willett, W. C., & Giovannucci, E. L. (2001) · Cancer Causes & Control · doi:10.1023/a:1011256201044 · Cited by 218 · see citing works
Thompson, F. E., Kipnis, V., Midthune, D., Freedman, L. S., Carroll, R. J., Subar, A. F., Brown, C. C., Butcher, M. S., Mouw, T., Leitzmann, M., et al. (2008) · Public Health Nutrition · doi:10.1017/s1368980007000419 · Cited by 209 · see citing works
Self-citationHeme and Chlorophyll Intake and Risk of Colorectal Cancer in the Netherlands Cohort Study
Balder, H. F., Vogel, J., Jansen, M. C. J. F., Weijenberg, M. P., van den Brandt, P. A., Westenbrink, S., van der Meer, R., & Goldbohm, R. A. (2006) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-05-0772 · Cited by 205 · see citing works
Knize, M. G., Salmon, C. P., Pais, P., & Felton, J. S. (1999) · Advances in experimental medicine and biology · doi:10.1007/978-1-4615-4853-9_12 · Cited by 200 · see citing works
A Prospective Study of Meat and Meat Mutagens and Prostate Cancer Risk
Cross, A. J., Peters, U., Kirsh, V. A., Andriole, G. L., Reding, D. J., Hayes, R. B., & Sinha, R. R. (2005) · Cancer Research · doi:10.1158/0008-5472.can-05-2191 · Cited by 196 · see citing works
Self-citationAllen, N. E., Key, T. J., Appleby, P. N., et al. (2008) · British Journal of Cancer · doi:10.1038/sj.bjc.6604331 · Cited by 195 · see citing works
Chemistry and biology of N-nitroso compounds
(1992) · International Journal of Biochemistry · doi:10.1016/0020-711x(92)90297-e · Cited by 187 · see citing works
Tappel, A. L. (2006) · Medical Hypotheses · doi:10.1016/j.mehy.2006.08.025 · Cited by 184 · see citing works
Heterocyclic Amine Content of Cooked Meat and Risk of Prostate Cancer
Norrish, A. E., Ferguson, L. R., Knize, M. G., et al. (1999) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/91.23.2038 · Cited by 178 · see citing works
Calculating dietary iron bioavailability: Refinement and computerization
Monsen, E. R., & Balintfy, J. L. (1982) · Journal of the American Dietetic Association · doi:10.1016/s0002-8223(21)08469-8 · Cited by 178 · see citing works
Animal products, calcium and protein and prostate cancer risk in the Netherlands Cohort Study
Schuurman, A. G., van den Brandt, P. A., Dorant, E., et al. (1999) · British Journal of Cancer · doi:10.1038/sj.bjc.6690472 · Cited by 175 · see citing works
An epidemiologic approach to studying heterocyclic amines
Sinha, R. R. (2002) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(02)00166-5 · Cited by 173 · see citing works
Self-citationSinha, R. R., Gustafson, D., Kulldorff, M., et al. (2000) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/92.16.1352 · Cited by 171 · see citing works
Self-citationDagnelie, P. C., Schuurman, A. G., Goldbohm, R. A., et al. (2004) · British Journal of Urology · doi:10.1111/j.1464-410x.2004.04795.x · Cited by 164 · see citing works
Foods, nutrients and prostate cancer: a case–control study in Uruguay
Deneo‐Pellegrini, H., Stéfani, E. D., Ronco, Á. L., & Mendilaharsu, M. (1999) · British Journal of Cancer · doi:10.1038/sj.bjc.6690396 · Cited by 152 · see citing works
Heterocyclic amine content in fast-food meat products
Knize, M. G., Sinha, R. R., Rothman, N., Brown, E. D., Salmon, C. P., Levander, O. A., Cunningham, P. L., & Felton, J. S. (1995) · Food and Chemical Toxicology · doi:10.1016/0278-6915(95)00025-w · Cited by 150 · see citing works
Self-citationA case-control study of cancer of the prostate in Somerset and east Devon
Ewings, P., & Bowie, C. (1996) · British Journal of Cancer · doi:10.1038/bjc.1996.418 · Cited by 149 · see citing works
Carcinogenicity in rats of a mutagenic compound, 2-amino-3,8-dimethylimidazo[4,5-f]quinoxaline
Kato, T., Ohgaki, H., Hasegawa, H., et al. (1988) · Carcinogenesis · doi:10.1093/carcin/9.1.71 · Cited by 142 · see citing works
Fat and meat intake and prostate cancer risk: The multiethnic cohort study
Park, S., Murphy, S. P., Wilkens, L. R., Henderson, B. E., & Kolonel, L. N. (2007) · International Journal of Cancer · doi:10.1002/ijc.22805 · Cited by 131 · see citing works
Meat and dairy consumption and subsequent risk of prostate cancer in a US cohort study
Rohrmann, S., Platz, E. A., Kavanaugh, C. J., Thuita, L. W., Hoffman, S. C., & Helzlsouer, K. J. (2006) · Cancer Causes & Control · doi:10.1007/s10552-006-0082-y · Cited by 122 · see citing works
Heme and Nonheme Iron Content of Animal Products Commonly Consumed in Thailand
Kongkachuichai, R., Napatthalung, P., & Charoensiri, R. (2002) · Journal of Food Composition and Analysis · doi:10.1006/jfca.2002.1080 · Cited by 120 · see citing works
Rodríguez, C., McCullough, M. L., Mondul, A. M., Jacobs, E. J., Chao, A., Patel, A. V., Thun, M. J., & Calle, E. E. (2006) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-05-0614 · Cited by 117 · see citing works
Sinha, R. R., Cross, A. J., Curtin, J., Zimmerman, T. P., McNutt, S., Risch, A., & Holden, J. M. (2005) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.200500018 · Cited by 115 · see citing works
Self-citationMeat and Meat Mutagens and Risk of Prostate Cancer in the Agricultural Health Study
Koutros, S., Cross, A. J., Sandler, D. P., et al. (2008) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-07-0392 · Cited by 104 · see citing works
Self-citationPark, Y., Mitrou, P. N., Kipnis, V., Hollenbeck, A. R., Schatzkin, A. G., & Leitzmann, M. F. (2007) · American Journal of Epidemiology · doi:10.1093/aje/kwm268 · Cited by 97 · see citing works
Self-citationEvaluation of Methods Used in Meat Iron Analysis and Iron Content of Raw and Cooked Meats
Carpenter, C. E., & Clark, E. M. (1995) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf00055a014 · Cited by 95 · see citing works
Carcinogenicity of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in the rat
Ito, N., Hasegawa, R., Imaida, K., Tamano, S., Hagiwara, A., Hirose, M., & Shirai, T. (1997) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(97)00032-8 · Cited by 91 · see citing works
Tseng, M., Breslow, R. A., DeVellis, R. F., & Ziegler, R. G. (2004) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-03-0076 · Cited by 88 · see citing works
Heterocyclic Amine Content in Restaurant-Cooked Hamburgers, Steaks, Ribs, and Chicken
Knize, M. G., Sinha, R. R., Brown, E. D., et al. (1998) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf980639a · Cited by 87 · see citing works
Self-citationKettering award lecture. The role of marrow transplantation in the eradication of malignant disease
Thomas, E. D. (1982) · Cancer · doi:10.1002/1097-0142(19820515)49:10 · Cited by 72 · see citing works
Kabat, G. C., Cross, A. J., Park, Y., Schatzkin, A. G., Hollenbeck, A. R., Rohan, T. E., & Sinha, R. R. (2008) · International Journal of Cancer · doi:10.1002/ijc.24203 · Cited by 56 · see citing works
Self-citationIron and colorectal cancer risk in the α‐tocopherol, β‐carotene cancer prevention study
Cross, A. J., Gunter, M. J., Wood, R. J., Pietinen, P., Taylor, P. R., Virtamo, J. R. K., Albanes, D., & Sinha, R. R. (2006) · International Journal of Cancer · doi:10.1002/ijc.21780 · Cited by 54 · see citing works
Self-citationMultiethnic studies of diet, nutrition, and cancer in Hawaii.
Kolonel, L. N., Jh, H., & Nomura, A. M. (1985) · PubMed · Cited by 53 · see citing works
Shirai, T., Cui, L., Takahashi, S., Futakuchi, M., Asamoto, M., Kato, K., & Ito, N. (1999) · Cancer Letters · doi:10.1016/s0304-3835(99)00128-7 · Cited by 53 · see citing works
Knize, M. G., Sinha, R. R., Salmon, C. P., et al. (1996) · Journal of Muscle Foods · doi:10.1111/j.1745-4573.1996.tb00603.x · Cited by 39 · see citing works
Self-citationCarcinogenicities in mice and rats of IQ, MeIQ, and MeIQx.
Ohgaki, H., Hasegawa, H., Kato, T., Suenaga, M., Sato, S., Takayama, S., & Sugimura, T. (1985) · PubMed · Cited by 22 · see citing works
Cross, A., Pollock, J. R. A., & Bingham, S. (2002) · PubMed · Cited by 16 · see citing works
Self-citationAdamson, R. H. (1997) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(97)00018-3 · Cited by 3 · see citing works
Flagged first, then by citations
Research works printed but not linked: 4
- Knize MG, Sinha R, Salmon CP, et al. Formation of hetero- cyclic amine mutagens/carcinogens during cooking of muscle meat. J Muscle Foods. 1996;7(3):271-279.
- Cross AJ, Pollock JRA, Bingham SA. Increased endogenous N-nitrosation in the human colon: a response to red and white meat? [abstract]. Br J Cancer. 2000;83:81.
- Michaud DS, Midthune D, Hermansen S, et al. Comparison of cancer registry case ascertainment with SEER estimates and self-reporting in a subset of the NIH-AARP Diet and Health Study. J Registry Manag. 2005;32:70-77.
- Sugimura T. Mutagens, carcinogens, and tumor promoters in our daily food. Cancer. 1970;49(10):1970-1981.
Cited by
Sorted by citations
Trends in meat consumption in the USA
Daniel, C. R., Cross, A. J., Koebnick, C., & Sinha, R. (2011) · Public Health Nutrition · doi:10.1017/s1368980010002077 · Cited by 504 · see citing works
Self-citationKoch, C. D., Gladwin, M. T., Freeman, B. A., Lundberg, J. O., Weitzberg, E., & Morris, A. (2017) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.12.015 · Cited by 186 · 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
Chazelas, E., Pierre, F., Druesne-Pecollo, N., Esseddik, Y., Szabo de Edelenyi, F., Agaesse, C., De Sa, A., Lutchia, R., Gigandet, S., Srour, B., et al. (2022) · International Journal of Epidemiology · doi:10.1093/ije/dyac046 · Cited by 135 · see citing works
Nitrite and nitrate: cardiovascular risk–benefit and metabolic effect
Tang, Y., Jiang, H., & Bryan, N. S. (2011) · Current Opinion in Lipidology · doi:10.1097/mol.0b013e328341942c · Cited by 69 · see citing works
A “green” diet-based approach to cardiovascular health? Is inorganic nitrate the answer?
Rathod, K. S., Velmurugan, S., & Ahluwalia, A. (2016) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201500313 · Cited by 42 · see citing works
Zhou, J., Liu, H., Hu, L., Kagami, H., & Wang, S. (2024) · Medicine Plus · doi:10.1016/j.medp.2023.100003 · Cited by 17 · see citing works
- Authors
- Sinha, R., Park, Y., Graubard, B. I., Leitzmann, M. F., Hollenbeck, A., Schatzkin, A., & Cross, A. J.
- Affiliations
- National Cancer Institute (US)
- Corresponding author
- Sinha, R.
- Venue
- American Journal of Epidemiology
- Publisher
- Oxford University Press (OUP)
- Published
- 2009-10-06
- Volume
- 170
- Issue
- 9
- Pages
- 1165-1177
- ISSN
- 0002-9262 (ISSN-L)
- 1476-6256
- PMC
- PMC2781742
- OpenAlex
- W2098858441
- Cited by
- 181
- References
- 60
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 13 · 2023: 8 · 2022: 7 · 2021: 11 · 2020: 5 · 2019: 10 · 2018: 11 · 2017: 12 · 2016: 11 · 2015: 13 · 2014: 11 · 2013: 11 · 2012: 16
- FWCI
- 15.39
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- American Journal of Epidemiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- University of Regensburg Publication Server (University of Regensburg) (submittedVersion)
- Funders
- Universität Regensburg
- Division of Cancer Epidemiology and Genetics, National Cancer Institute
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Nutritional Studies and Diet
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Meat and Animal Product Quality
- Health Sciences › Medicine › Oncology › Cancer Risks and Factors
- Keywords
- prostate cancer, red meat, processed meat, heme iron, nitrite, nitrate, benzo[a]pyrene, cooking methods, food mutagens, advanced prostate cancer, fatal prostate cancer, cancer risk factors, men's health
- MeSH terms
- Aged, Benzo(a)pyrene, Cooking, Heme, Humans, Male, Meat, Middle Aged, Nitrates, Nitrites, Polycyclic Aromatic Hydrocarbons, Prospective Studies, Prostatic Neoplasms, United States
About these checks
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.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review