Abstract
Purpose
Research on the role of red meat and poultry consumption in breast carcinogenesis is inconclusive, but the evidence in African-American (AA) women is lacking. The association between consuming meat and breast cancer risk was examined in the Women’s Circle of Health Study involving 803 AA cases, 889 AA controls, 755 Caucasian cases, and 701 Caucasian controls.
Methods
Dietary information was collected using a Food Frequency Questionnaire. Odds ratios (OR) and 95 % confidence intervals (CI) were obtained from logistic regression models adjusting for potential covariates.
Results
Comparing the fourth versus the first quartiles, among Caucasian women, processed meat (OR = 1.48; 95 % CI 1.07–2.04), unprocessed red meat (OR = 1.40; 95 % CI 1.01–1.94), and poultry intakes (OR = 1.42; 95 % CI 1.01–1.99) increased breast cancer risk. Risk associated with poultry intake was more dominant in premenopausal women (OR = 2.33; 95 % CI 1.44–3.77) and for women with ER− tumors (OR = 2.55; 95 % CI 1.29–5.03) in the Caucasian group. Associations in AA women were mostly null except for a significant increased risk trend with processed meat consumption for ER+ tumors (OR = 1.36; 95 % CI 0.94–1.97, p trend = 0.04).
Conclusions
Overall, associations between breast cancer risk and consumption of red meat and poultry were of different magnitude in AA and Caucasian women, with further differences noted by menopausal and hormone receptor status in Caucasian women. This is the first study to examine racial differences in meat and breast cancer risk and represents some of the first evidence in AA women.
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References
American Cancer Society (2012) Cancer Facts and Figures 2012. http://www.cancer.org/acs/groups/content/@epidemiologysurveilance/documents/document/acspc-031941.pdf. American Cancer Society, Atlanta
American Cancer Society (2011) Cancer facts and figures for African Americans 2011–2012. American Cancer Society, Atlanta
Daniel CR, Cross AJ, Koebnick C, Sinha R (2011) Trends in meat consumption in the USA. Public Health Nutr 14:575–583
Alexander DD, Morimoto LM, Mink PJ, Cushing CA (2010) A review and meta-analysis of red and processed meat consumption and breast cancer. Nutr Res Rev 23:349–365
Bao PP, Shu XO, Zheng Y et al (2012) Fruit, vegetable, and animal food intake and breast cancer risk by hormone receptor status. Nutr Cancer 64:806–819
De Stefani E, Boffetta P, Ronco AL et al (2012) Processed meat consumption and risk of cancer: a multisite case-control study in Uruguay. Br J Cancer 107:1584–1588
World Cancer Research Fund/American Institute for Cancer Research (2008) The associations between food, nutrition and physical activity and the risk of breast cancer. WCRF/AICR systematic literature review continuous update report
World Cancer Research Fund International/American Institute for Cancer Research (2010) Continuous update project report summary. Food, nutrition, physical activity, and the prevention of breast cancer
Missmer SA, Smith-Warner SA, Spiegelman D et al (2002) Meat and dairy food consumption and breast cancer: a pooled analysis of cohort studies. Int J Epidemiol 31:78–85
Gonzalez CA, Riboli E (2010) Diet and cancer prevention: contributions from the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Eur J Cancer 46:2555–2562
Egeberg R, Olsen A, Autrup H et al (2008) Meat consumption, N-acetyl transferase 1 and 2 polymorphism and risk of breast cancer in Danish postmenopausal women. Eur J Cancer Prev 17:39–47
Taylor EF, Burley VJ, Greenwood DC, Cade JE (2007) Meat consumption and risk of breast cancer in the UK Women’s Cohort Study. Br J Cancer 96:1139–1146
Pala V, Krogh V, Berrino F et al (2009) Meat, eggs, dairy products, and risk of breast cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort. Am J Clin Nutr 90:602–612
World Cancer Research Fund/American Institute for Cancer Research (2007) Food, nutrition, physical activity, and the prevention of cancer: a global perspective. American Institute for Cancer Research, Washington DC
Smolinska K, Paluszkiewicz P (2010) Risk of colorectal cancer in relation to frequency and total amount of red meat consumption. Systematic review and meta-analysis. Arch Med Sci 6:605–610
Kushi LH, Doyle C, McCullough M et al (2012) American Cancer Society Guidelines on nutrition and physical activity for cancer prevention: reducing the risk of cancer with healthy food choices and physical activity. CA Cancer J Clin 62:30–67
Johnson CM, Wei C, Ensor JE et al (2013) Meta-analyses of colorectal cancer risk factors. Cancer Causes Control 24:1207–1222
Millikan RC, Newman B, Tse CK et al (2008) Epidemiology of basal-like breast cancer. Breast Cancer Res Treat 109:123–139
Agurs-Collins T, Dunn BK, Browne D, Johnson KA, Lubet R (2010) Epidemiology of health disparities in relation to the biology of estrogen receptor-negative breast cancer. Semin Oncol 37:384–401
Amend K, Hicks D, Ambrosone CB (2006) Breast cancer in African-American women: differences in tumor biology from European-American women. Cancer Res 66:8327–8330
Chandran U, Hirshfield KM, Bandera EV (2012) The role of anthropometric and nutritional factors on breast cancer risk in African-American women. Public Health Nutr 15:738–748
Wang Y, Beydoun MA, Caballero B, Gary TL, Lawrence R (2010) Trends and correlates in meat consumption patterns in the US adult population. Public Health Nutr 13:1333–1345
Bastide NM, Pierre FH, Corpet DE (2011) Heme iron from meat and risk of colorectal cancer: a meta-analysis and a review of the mechanisms involved. Cancer Prev Res (Phila) 4:177–184
Knize MG, Felton JS (2005) Formation and human risk of carcinogenic heterocyclic amines formed from natural precursors in meat. Nutr Rev 63:158–165
Sinha R, Rothman N, Brown ED et al (1995) High concentrations of the carcinogen 2-amino-1-methyl-6-phenylimidazo-[4,5-b]pyridine (PhIP) occur in chicken but are dependent on the cooking method. Cancer Res 55:4516–4519
Keating GA, Bogen KT (2004) Estimates of heterocyclic amine intake in the US population. J Chromatogr B Analyt Technol Biomed Life Sci 802:127–133
Bandera EV, Chandran U, Zirpoli G, McCann SE, Ciupak G, Ambrosone CB (2013) Rethinking sources of representative controls for the conduct of case-control studies in minority populations. BMC Med Res Methodol 13:71
Ambrosone CB, Ciupak GL, Bandera EV et al (2009) Conducting molecular epidemiological research in the age of HIPAA: a multi-institutional case-control study of breast cancer in African-American and European-American Women. J Oncol 2009:871250
Patterson RE, Kristal AR, Tinker LF, Carter RA, Bolton MP, Agurs-Collins T (1999) Measurement characteristics of the Women’s Health Initiative food frequency questionnaire. Ann Epidemiol 9:178–187
Kristal AR, Feng Z, Coates RJ, Oberman A, George V (1997) Associations of race/ethnicity, education, and dietary intervention with the validity and reliability of a food frequency questionnaire: the Women’s Health Trial Feasibility Study in Minority Populations. Am J Epidemiol 146:856–869
Willett WC (1998) Nutritional epidemiology, 2nd edn. Oxford University Press, New York
Ferrucci LM, Cross AJ, Graubard BI et al (2009) Intake of meat, meat mutagens, and iron and the risk of breast cancer in the prostate, lung, colorectal, and ovarian cancer screening trial. Br J Cancer 101:178–184
Genkinger JM, Makambi KH, Palmer JR, Rosenberg L, Adams-Campbell LL (2013) Consumption of dairy and meat in relation to breast cancer risk in the Black Women’s Health Study. Cancer Causes Control 24:675–684
Williams CD, Satia JA, Adair LS et al (2009) Dietary patterns, food groups, and rectal cancer risk in Whites and African-Americans. Cancer Epidemiol Biomarkers Prev 18:1552–1561
Satia JA, Tseng M, Galanko JA, Martin C, Sandler RS (2009) Dietary patterns and colon cancer risk in Whites and African Americans in the North Carolina Colon Cancer Study. Nutr Cancer 61:179–193
Cho E, Chen WY, Hunter DJ et al (2006) Red meat intake and risk of breast cancer among premenopausal women. Arch Intern Med 166:2253–2259
Taylor VH, Misra M, Mukherjee SD (2009) Is red meat intake a risk factor for breast cancer among premenopausal women? Breast Cancer Res Treat 117:1–8
Hu J, La Vecchia C, DesMeules M, Negri E, Mery L (2008) Meat and fish consumption and cancer in Canada. Nutr Cancer 60:313–324
United States Department of Agriculture (2010) What is the relationship between the intake of animal protein products and breast cancer? USDA Nutrition Evidence Analysis Library. In: Library UNEA (ed)
Linos E, Willett WC, Cho E, Colditz G, Frazier LA (2008) Red meat consumption during adolescence among premenopausal women and risk of breast cancer. Cancer Epidemiol Biomarkers Prev 17:2146–2151
International Agency for Research on Cancer (2011) Agents classified by the IARC Monographs. In: http://monographs.iarc.fr/ENG/Classification/index.php. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans: IARC
Santarelli RL, Pierre F, Corpet DE (2008) Processed meat and colorectal cancer: a review of epidemiologic and experimental evidence. Nutr Cancer 60:131–144
Zheng W, Gustafson DR, Sinha R et al (1998) Well-done meat intake and the risk of breast cancer. J Natl Cancer Inst 90:1724–1729
Fu Z, Deming SL, Fair AM et al (2011) Well-done meat intake and meat-derived mutagen exposures in relation to breast cancer risk: the Nashville Breast Health Study. Breast Cancer Res Treat 129:919–928
Yang S, Leff MG, McTague D et al (1998) Multistate surveillance for food-handling, preparation, and consumption behaviors associated with foodborne diseases: 1995 and 1996 BRFSS food-safety questions. MMWR CDC Surveill Summ 47:33–57
Zheng W, Lee SA (2009) Well-done meat intake, heterocyclic amine exposure, and cancer risk. Nutr Cancer 61:437–446
Zheng W, Wen WQ, Gustafson DR, Gross M, Cerhan JR, Folsom AR (2002) GSTM1 and GSTT1 polymorphisms and postmenopausal breast cancer risk. Breast Cancer Res Treat 74:9–16
Rebbeck TR (1997) Molecular epidemiology of the human glutathione S-transferase genotypes GSTM1 and GSTT1 in cancer susceptibility. Cancer Epidemiol Biomarkers Prev 6:733–743
Qiu C, Shan L, Yu M, Snyderwine EG (2005) Steroid hormone receptor expression and proliferation in rat mammary gland carcinomas induced by 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine. Carcinogenesis 26:763–769
Lauber SN, Ali S, Gooderham NJ (2004) The cooked food derived carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b] pyridine is a potent oestrogen: a mechanistic basis for its tissue-specific carcinogenicity. Carcinogenesis 25:2509–2517
Liehr JG, Jones JS (2001) Role of iron in estrogen-induced cancer. Curr Med Chem 8:839–849
Rohrmann S, Lukas Jung SU, Linseisen J, Pfau W (2009) Dietary intake of meat and meat-derived heterocyclic aromatic amines and their correlation with DNA adducts in female breast tissue. Mutagenesis 24:127–132
Brinkman MT, Baglietto L, Krishnan K et al (2010) Consumption of animal products, their nutrient components and postmenopausal circulating steroid hormone concentrations. Eur J Clin Nutr 64:176–183
McTiernan A, Wu L, Chen C et al (2006) Relation of BMI and physical activity to sex hormones in postmenopausal women. Obesity (Silver Spring) 14:1662–1677
Perks CM, Holly JM (2011) Hormonal mechanisms underlying the relationship between obesity and breast cancer. Endocrinol Metab Clin North Am 40:485–507
Andersson AM, Skakkebaek NE (1999) Exposure to exogenous estrogens in food: possible impact on human development and health. Eur J Endocrinol 140:477–485
Vieira FG, Di Pietro PF, Boaventura BC et al (2011) Factors associated with oxidative stress in women with breast cancer. Nutr Hosp 26:528–536
Felton JS, Knize MG, Wood C et al (1984) Isolation and characterization of new mutagens from fried ground beef. Carcinogenesis 5:95–102
Felton JS, Knize MG, Shen NH, Andresen BD, Bjeldanes LF, Hatch FT (1986) Identification of the mutagens in cooked beef. Environ Health Perspect 67:17–24
Wang Y, Chen X (2011) How much of racial/ethnic disparities in dietary intakes, exercise, and weight status can be explained y nutrition- and health related psychological factors and socioeconomic status among US adults? J Am Diet Assoc 111:1904–1911
Newby PK, Noel SE, Grant R, Judd S, Shikany JM, Ard J (2012) Race and region have independent and synergistic effects on dietary intakes in black and white women. Nutr J 11:25
Hartge P (2006) Participation in population studies. Epidemiology 17:252–254
Acknowledgments
This work was funded by National Cancer Institute (P01 CA151135, R01 CA100598, K22 CA138563, and P30CA072720), US Army Medical Research and Material Command (DAMD-17-01-1-0334), the Breast Cancer Research Foundation, and a gift from the Philip L. Hubbell family. The New Jersey State Cancer Registry is supported by the National Program of Cancer Registries of the Centers for Disease Control and Prevention under cooperative agreement 1US58DP003931-01 awarded to the New Jersey Department of Health. The collection of New Jersey cancer incidence data is also supported by the Surveillance, Epidemiology, and End Results Program of the National Cancer Institute under contract N01PC-2010-00027 and the State of New Jersey. The funding agents played no role in design, in the collection, analysis, and interpretation of data, in the writing of the manuscript, or in the decision to submit the manuscript for publication. We thank the colleagues, physicians, and clinical staff in New York and New Jersey who facilitated identification and enrollment of cases into the study: Kandace Amend (i3 Drug Safety), Helena Furberg (Memorial Sloan-Kettering Cancer Center), Thomas Rohan and Joseph Sparano (Albert Einstein College of Medicine), Paul Tartter and Alison Estabrook (St. Luke’s Roosevelt Hospital), James Reilly (Kings County Hospital Center), Benjamin Pace, George Raptis, and Christina Weltz (Mount Sinai School of Medicine), Maria Castaldi (Jacob Medical Center), Sheldon Feldman (New York-Presbyterian), and Margaret Kemeny (Queens Hospital Center). We also thank our research personnel at the Rutgers Cancer Institute of New Jersey, Roswell Park Cancer Institute, Mount Sinai School of Medicine, Rutgers School of Public Health, and the New Jersey State Cancer Registry, as well as our African-American breast cancer advocates and community partners, and all the women who generously donated their time to participate in the study.
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The authors declare that they have no conflict of interest.
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Chandran, U., Zirpoli, G., Ciupak, G. et al. Racial disparities in red meat and poultry intake and breast cancer risk. Cancer Causes Control 24, 2217–2229 (2013). https://doi.org/10.1007/s10552-013-0299-5
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DOI: https://doi.org/10.1007/s10552-013-0299-5