Intake of Meat Mutagens and Risk of Prostate Cancer in a Cohort of U.S. Health Professionals

Background: Evidence relating heterocyclic aromatic amines (HCA), associated with high-temperature cooking methods, to prostate cancer risk is inconsistent. Methods: In a large U.S. cohort study, intakes of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP), 2-amino-3,8-dimethylimidazo[4,5-f]quinoxaline (MeIQx), and 2-amino-3,4,8-trimethylimidazo[4,5-f]quinoxaline (DiMeIQx) and a meat-derived mutagenicity (MDM) index were assessed using a cooking method questionnaire administered in 1996. Until 2010, 2,770 prostate cancer cases were observed among 26,030 participants. Results: Intake of PhIP from red meat was statistically significantly associated with total prostate cancer risk (top vs. bottom quintile HR, 1.18; 95% confidence intervals; CI, 1.03–1.35), but not other HCAs (MeIQx, 1.12; 0.98–1.27, PhIP from white meat, 1.08; 0.95–1.22, DiMeIQx, 1.09; 0.97–1.21) or MDM (1.13; 1.00–1.28). For high-grade (Gleason sum 7 with pattern 4+3 and Gleason sum 8–10, n = 483 cases) and advanced cancers (n = 281), we only observed positive associations for PhIP from red meat (top vs. bottom quintile: high grade: HR, 1.44; 95% CI, 1.04–1.98, Ptrend = 0.03; advanced: HR, 1.50; 95% CI, 0.99–2.26; Ptrend = 0.12), but associations for advanced cancers did not reach statistical significance. Observed associations remained similar after adjustment for total, unprocessed, or processed red meat intake. Conclusion: Observed positive associations between PhIP intake from red meat and prostate cancer, particularly high-grade and possibly also advanced prostate cancer, need to be confirmed in other studies. Impact: Results do not provide strong evidence that HCAs increase risk of prostate cancers. Cancer Epidemiol Biomarkers Prev; 24(10); 1557–63. ©2015 AACR.

[1]  M. Torres-Ramos,et al.  Multiple Molecular and Cellular Mechanisms of Action of Lycopene in Cancer Inhibition , 2013, Evidence-based complementary and alternative medicine : eCAM.

[2]  J. Clements,et al.  The Potential Role of Lycopene for the Prevention and Therapy of Prostate Cancer: From Molecular Mechanisms to Clinical Evidence , 2013, International journal of molecular sciences.

[3]  S. Ingles,et al.  Red meat and poultry, cooking practices, genetic susceptibility and risk of prostate cancer: results from a multiethnic case-control study. , 2012, Carcinogenesis.

[4]  Guang-xun Li,et al.  Dietary Carcinogen 2-Amino-1-Methyl-6-Phenylimidazo[4,5-b]Pyridine–Induced Prostate Carcinogenesis in CYP1A-Humanized Mice , 2012, Cancer Prevention Research.

[5]  J. Witte,et al.  Impact of Meat Consumption, Preparation, and Mutagens on Aggressive Prostate Cancer , 2011, PloS one.

[6]  R. Sinha,et al.  Meat Consumption, Cooking Practices, Meat Mutagens, and Risk of Prostate Cancer , 2011, Nutrition and cancer.

[7]  Dominik D Alexander,et al.  A review and meta-analysis of prospective studies of red and processed meat intake and prostate cancer , 2010, Nutrition journal.

[8]  B. Henderson,et al.  Well-Done Meat Consumption, NAT1 and NAT2 Acetylator Genotypes and Prostate Cancer Risk: The Multiethnic Cohort study , 2010, Cancer Epidemiology, Biomarkers & Prevention.

[9]  S. Rohrmann,et al.  Intake of heterocyclic aromatic amines and the risk of prostate cancer in the EPIC-Heidelberg cohort , 2010, Cancer Causes & Control.

[10]  R. Sinha,et al.  Meat and meat-related compounds and risk of prostate cancer in a large prospective cohort study in the United States. , 2009, American journal of epidemiology.

[11]  R. Sinha,et al.  Meat and Meat Mutagens and Risk of Prostate Cancer in the Agricultural Health Study , 2008, Cancer Epidemiology Biomarkers & Prevention.

[12]  S. Rohrmann,et al.  Intake of heterocyclic aromatic amines from meat in the European Prospective Investigation into Cancer and Nutrition (EPIC)-Heidelberg cohort , 2007, British Journal of Nutrition.

[13]  A. D. De Marzo,et al.  The dietary charred meat carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine acts as both a tumor initiator and promoter in the rat ventral prostate. , 2007, Cancer research.

[14]  Ulrike Peters,et al.  A prospective study of meat and meat mutagens and prostate cancer risk. , 2005, Cancer research.

[15]  R. Sinha,et al.  Development of a food frequency questionnaire module and databases for compounds in cooked and processed meats. , 2005, Molecular nutrition & food research.

[16]  G. Haas,et al.  Heterocyclic amines and genotype of N-acetyltransferases as risk factors for prostate cancer , 2005, Prostate Cancer and Prostatic Diseases.

[17]  E. Rimm,et al.  A prospective study on intake of animal products and risk of prostate cancer , 2001, Cancer Causes & Control.

[18]  V. Fogliano,et al.  Influence of antioxidants in virgin olive oil on the formation of heterocyclic amines in fried beefburgers. , 2003, Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association.

[19]  A. Clifford,et al.  Effect of Dietary Constituents With Chemopreventive Potential on Adduct Formation of a Low Dose of the Heterocyclic Amines PhIP and IQ and Phase II Hepatic Enzymes , 2003, Nutrition and cancer.

[20]  P. Walsh A prospective study on the intake of animal products and risk of prostate cancer. , 2002, The Journal of urology.

[21]  K. Skog,et al.  Problems associated with the determination of heterocyclic amines in cooked foods and human exposure. , 2002, Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association.

[22]  N Rothman,et al.  Dietary intake of heterocyclic amines, meat-derived mutagenic activity, and risk of colorectal adenomas. , 2001, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[23]  J. Jakobsen,et al.  Dose-response effects of lycopene on selected drug-metabolizing and antioxidant enzymes in the rat. , 2000, Cancer letters.

[24]  L R Ferguson,et al.  Heterocyclic amine content of cooked meat and risk of prostate cancer. , 1999, Journal of the National Cancer Institute.

[25]  G. Haas,et al.  N-Acetyltransferase expression and DNA binding of N-hydroxyheterocyclic amines in human prostate epithelium. , 1999, Carcinogenesis.

[26]  M. Jägerstad,et al.  Carcinogenic heterocyclic amines in model systems and cooked foods: a review on formation, occurrence and intake. , 1998, Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association.

[27]  W. Willett,et al.  Predictors of dietary heterocyclic amine intake in three prospective cohorts. , 1998, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[28]  T. Sugimura,et al.  Overview of carcinogenic heterocyclic amines. , 1997, Mutation research.

[29]  S. Thorgeirsson,et al.  Metabolism of food-derived heterocyclic amines in nonhuman primates. , 1997, Mutation research.

[30]  M. Knize,et al.  Effects of marinating on heterocyclic amine carcinogen formation in grilled chicken. , 1997, Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association.

[31]  W. Stahl,et al.  Lycopene: a biologically important carotenoid for humans? , 1996, Archives of biochemistry and biophysics.

[32]  G. Steineck,et al.  Effect of cooking temperature on the formation of heterocyclic amines in fried meat products and pan residues. , 1995, Carcinogenesis.

[33]  N Ito,et al.  Carcinogenicity of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in rats: dose-response studies. , 1995, Princess Takamatsu symposia.

[34]  M. Jägerstad,et al.  Effects of edible oils and fatty acids on the formation of mutagenic heterocyclic amines in a model system. , 1993, Carcinogenesis.

[35]  G A Colditz,et al.  Reproducibility and validity of an expanded self-administered semiquantitative food frequency questionnaire among male health professionals. , 1992, American journal of epidemiology.

[36]  G. Gross,et al.  Quantitation of mutagenic/carcinogenic heterocyclic aromatic amines in food products. , 1992, Journal of chromatography.

[37]  M. Jägerstad,et al.  Formation of heterocyclic amines using model systems. , 1991, Mutation research.

[38]  M. Singer,et al.  Nutritional Epidemiology , 2020, Definitions.