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Red meat, poultry, and fish intake and breast cancer risk among Hispanic and Non-Hispanic white women: The Breast Cancer Health Disparities Study

Abstract

Purpose

There is suggestive but limited evidence for a relationship between meat intake and breast cancer (BC) risk. Few studies included Hispanic women. We investigated the association between meats and fish intake and BC risk among Hispanic and NHW women.

Methods

The study included NHW (1,982 cases and 2,218 controls) and the US Hispanics (1,777 cases and 2,218 controls) from two population-based case–control studies. Analyses considered menopausal status and percent Native American ancestry. We estimated pooled ORs combining harmonized data from both studies, and study- and race-/ethnicity-specific ORs that were combined using fixed or random effects models, depending on heterogeneity levels.

Results

When comparing highest versus lowest tertile of intake, among NHW we observed an association between tuna intake and BC risk (pooled OR 1.25; 95 % CI 1.05–1.50; trend p = 0.006). Among Hispanics, we observed an association between BC risk and processed meat intake (pooled OR 1.42; 95 % CI 1.18–1.71; trend p < 0.001), and between white meat (OR 0.80; 95 % CI 0.67–0.95; trend p = 0.01) and BC risk, driven by poultry. All these findings were supported by meta-analysis using fixed or random effect models and were restricted to estrogen receptor-positive tumors. Processed meats and poultry were not associated with BC risk among NHW women; red meat and fish were not associated with BC risk in either race/ethnic groups.

Conclusions

Our results suggest the presence of ethnic differences in associations between meat and BC risk that may contribute to BC disparities.

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References

  1. 1.

    Howlader N, Noone A, Krapcho M et al (2014) SEER Cancer Statistics Review, 1975–2011, National Cancer Institute. Bethesda, MD, http://seer.cancer.gov/csr/1975_2011/, based on November 2013 SEER data submission, posted to the SEER web site, April 2014

  2. 2.

    Sweeney C, Baumgartner KB, Byers T et al (2008) Reproductive history in relation to breast cancer risk among Hispanic and non-Hispanic white women. Cancer Causes Control 19:391–401. doi:10.1007/s10552-007-9098-1

    Article  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Siegel R, Naishadham D, Jemal A (2012) Cancer statistics for Hispanics/Latinos, 2012. CA Cancer J Clin 62:283–298. doi:10.3322/caac.21153

    Article  PubMed  Google Scholar 

  4. 4.

    John EM, Phipps AI, Davis A, Koo J (2005) Migration history, acculturation, and breast cancer risk in Hispanic women. Cancer Epidemiol Biomark Prev 14:2905–2913. doi:10.1158/1055-9965.EPI-05-0483

    Article  Google Scholar 

  5. 5.

    Chlebowski RT, Chen Z, Anderson GL et al (2005) Ethnicity and breast cancer: factors influencing differences in incidence and outcome. J Natl Cancer Inst 97:439–448. doi:10.1093/jnci/dji064

    Article  PubMed  Google Scholar 

  6. 6.

    Ziegler RG, Hoover RN, Pike MC et al (1993) Migration patterns and breast cancer risk in Asian-American women. JNCI J Natl Cancer Inst 85:1819–1827. doi:10.1093/jnci/85.22.1819

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    Fejerman L, John EM, Huntsman S et al (2008) Genetic ancestry and risk of breast cancer among U.S. Latinas. Cancer Res 68:9723–9728. doi:10.1158/0008-5472.CAN-08-2039

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. 8.

    Fejerman L, Romieu I, John EM et al (2010) European ancestry is positively associated with breast cancer risk in Mexican women. Cancer Epidemiol Biomark Prev 19:1074–1082. doi:10.1158/1055-9965.EPI-09-1193

    Article  Google Scholar 

  9. 9.

    Fejerman L, Chen GK, Eng C et al (2012) Admixture mapping identifies a locus on 6q25 associated with breast cancer risk in US Latinas. Hum Mol Genet 21:1907–1917. doi:10.1093/hmg/ddr617

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Fejerman L, Ahmadiyeh N, Hu D et al (2014) Genome-wide association study of breast cancer in Latinas identifies novel protective variants on 6q25. Nat Commun 5:5260. doi:10.1038/ncomms6260

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. 11.

    World Cancer Research Fund/American Institute for Cancer Research (2010) Continuous update project report. Food, nutrition, physical activity, and the prevention of breast cancer

  12. 12.

    Romieu I (2011) Diet and breast cancer. Salud Publica Mex 53:430–439

    PubMed  Google Scholar 

  13. 13.

    Huang X (2003) Iron overload and its association with cancer risk in humans: evidence for iron as a carcinogenic metal. Mutat Res 533:153–171

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Andersson AM, Skakkebaek NE (1999) Exposure to exogenous estrogens in food: possible impact on human development and health. Eur J Endocrinol 140:477–485. doi:10.1530/eje.0.1400477

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Felton JS, Knize MG, Wu RW et al (2007) Mutagenic potency of food-derived heterocyclic amines. Mutat Res 616:90–94. doi:10.1016/j.mrfmmm.2006.11.010

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    Rothman N, Poirier MC, Baser ME et al (1990) Formation of polycyclic aromatic hydrocarbon-DNA adducts in peripheral white blood cells during consumption of charcoal-broiled beef. Carcinogenesis 11:1241–1243. doi:10.1093/carcin/11.7.1241

    CAS  Article  PubMed  Google Scholar 

  17. 17.

    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. doi:10.1017/S0954422410000235

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    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. doi:10.1093/ije/31.1.78

    Article  PubMed  Google Scholar 

  19. 19.

    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. doi:10.1007/s10549-009-0441-y

    Article  PubMed  Google Scholar 

  20. 20.

    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. doi:10.1097/CEJ.0b013e32809b4cdd

    CAS  Article  PubMed  Google Scholar 

  21. 21.

    Lee H, Wang Q, Yang F et al (2012) SULT1A1 Arg213His polymorphism, smoked meat, and breast cancer risk: a case–control study and meta-analysis. DNA Cell Biol 31:688–699. doi:10.1089/dna.2011.1403

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Slattery ML, John EM, Torres-Mejia G et al (2012) Genetic variation in genes involved in hormones, inflammation and energetic factors and breast cancer risk in an admixed population. Carcinogenesis 33:1512–1521. doi:10.1093/carcin/bgs163

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Slattery ML, Sweeney C, Edwards S et al (2007) Body size, weight change, fat distribution and breast cancer risk in Hispanic and non-Hispanic white women. Breast Cancer Res Treat 102:85–101. doi:10.1007/s10549-006-9292-y

    Article  PubMed  Google Scholar 

  24. 24.

    McDonald A, Van Horn L, Slattery M et al (1991) The CARDIA dietary history: development, implementation, and evaluation. J Am Diet Assoc 91:1104–1112

    CAS  PubMed  Google Scholar 

  25. 25.

    Slattery ML, Caan BJ, Duncan D et al (1994) A computerized diet history questionnaire for epidemiologic studies. J Am Diet Assoc 94:761–766

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    John EM, Horn-Ross PL, Koo J (2003) Lifetime physical activity and breast cancer risk in a multiethnic population: the San Francisco Bay area breast cancer study. Cancer Epidemiol Biomark Prev 12:1143–1152

    Google Scholar 

  27. 27.

    Horn-Ross PL, John EM, Lee M et al (2001) Phytoestrogen consumption and breast cancer risk in a multiethnic population: the Bay Area Breast Cancer Study. Am J Epidemiol 154:434–441

    CAS  Article  PubMed  Google Scholar 

  28. 28.

    Willett WC, Howe GR, Kushi LH (1997) Adjustment for total energy intake in epidemiologic studies. Am J Clin Nutr 65:1220S–1228S (discussion 1229S–1231S)

    CAS  PubMed  Google Scholar 

  29. 29.

    DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7:177–188

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    Higgins JPT, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558. doi:10.1002/sim.1186

    Article  PubMed  Google Scholar 

  31. 31.

    Zheng J, Hu X, Zhao Y et al (2013) Intake of fish and marine n-3 polyunsaturated fatty acids and risk of breast cancer: meta-analysis of data from 21 independent prospective cohort studies. BMJ 346:f3706. doi:10.1136/bmj.f3706

    Article  PubMed  Google Scholar 

  32. 32.

    Genkinger JM, Makambi KH, Palmer JR et al (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. doi:10.1007/s10552-013-0146-8

    Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Kiyabu GY, Inoue M, Saito E et al (2015) Fish, n-3 polyunsaturated fatty acids and n-6 polyunsaturated fatty acids intake and breast cancer risk: the Japan Public Health Center-based prospective study. Int J Cancer. doi:10.1002/ijc.29672

    PubMed  Google Scholar 

  34. 34.

    Stripp C, Overvad K, Christensen J et al (2003) Fish intake is positively associated with breast cancer incidence rate. J Nutr 133:3664–3669

    CAS  PubMed  Google Scholar 

  35. 35.

    Bessaoud F, Daurès J-P, Gerber M (2008) Dietary factors and breast cancer risk: a case control study among a population in Southern France. Nutr Cancer 60:177–187. doi:10.1080/01635580701649651

    Article  PubMed  Google Scholar 

  36. 36.

    Hermann S, Linseisen J, Chang-Claude J (2002) Nutrition and breast cancer risk by age 50: a population-based case–control study in Germany. Nutr Cancer 44:23–34. doi:10.1207/S15327914NC441_4

    Article  PubMed  Google Scholar 

  37. 37.

    Hu J, La Vecchia C, DesMeules M et al (2008) Meat and fish consumption and cancer in Canada. Nutr Cancer 60:313–324. doi:10.1080/01635580701759724

    Article  PubMed  Google Scholar 

  38. 38.

    Kim J, Lim S-Y, Shin A et al (2009) Fatty fish and fish omega-3 fatty acid intakes decrease the breast cancer risk: a case–control study. BMC Cancer 9:216. doi:10.1186/1471-2407-9-216

    Article  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Ambrosone CB, Freudenheim JL, Sinha R et al (1998) Breast cancer risk, meat consumption and N-acetyltransferase (NAT2) genetic polymorphisms. Int J Cancer 75:825–830

    CAS  Article  PubMed  Google Scholar 

  40. 40.

    Bao P-P, Shu X-O, Zheng Y et al (2012) Fruit, vegetable, and animal food intake and breast cancer risk by hormone receptor status. Nutr Cancer 64:806–819. doi:10.1080/01635581.2012.707277

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. 41.

    Larsson SC, Kumlin M, Ingelman-Sundberg M, Wolk A (2004) Dietary long-chain n-3 fatty acids for the prevention of cancer: a review of potential mechanisms. Am J Clin Nutr 79:935–945

    CAS  PubMed  Google Scholar 

  42. 42.

    Domingo JL, Bocio A, Falcó G, Llobet JM (2007) Benefits and risks of fish consumption part I. A quantitative analysis of the intake of omega-3 fatty acids and chemical contaminants. Toxicology 230:219–226. doi:10.1016/j.tox.2006.11.054

    CAS  Article  PubMed  Google Scholar 

  43. 43.

    Byrne C, Divekar SD, Storchan GB et al (2013) Metals and breast cancer. J Mammary Gland Biol Neoplasia 18:63–73. doi:10.1007/s10911-013-9273-9

    Article  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Sidhu KS (2003) Health benefits and potential risks related to consumption of fish or fish oil. Regul Toxicol Pharmacol 38:336–344. doi:10.1016/j.yrtph.2003.07.002

    CAS  Article  PubMed  Google Scholar 

  45. 45.

    Burger J, Gochfeld M (2004) Mercury in canned tuna: white versus light and temporal variation. Environ Res 96:239–249. doi:10.1016/j.envres.2003.12.001

    CAS  Article  PubMed  Google Scholar 

  46. 46.

    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. doi:10.1038/sj.bjc.6603689

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. 47.

    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. doi:10.3945/ajcn.2008.27173

    CAS  Article  PubMed  Google Scholar 

  48. 48.

    Pouchieu C, Deschasaux M, Hercberg S et al (2014) Prospective association between red and processed meat intakes and breast cancer risk: modulation by an antioxidant supplementation in the SU.VI.MAX randomized controlled trial. Int J Epidemiol 43:1583–1592. doi:10.1093/ije/dyu134

    Article  PubMed  Google Scholar 

  49. 49.

    Fung TT, Hu FB, Holmes MD et al (2005) Dietary patterns and the risk of postmenopausal breast cancer. Int J Cancer 116:116–121. doi:10.1002/ijc.20999

    CAS  Article  PubMed  Google Scholar 

  50. 50.

    van der Hel OL, Peeters PHM, Hein DW et al (2004) GSTM1 null genotype, red meat consumption and breast cancer risk (The Netherlands). Cancer Causes Control 15:295–303. doi:10.1023/B:CACO.0000024255.16305.f4

    Article  PubMed  Google Scholar 

  51. 51.

    Wu K, Sinha R, Holmes MD et al (2010) Meat mutagens and breast cancer in postmenopausal women–a cohort analysis. Cancer Epidemiol Biomark Prev 19:1301–1310. doi:10.1158/1055-9965.EPI-10-0002

    CAS  Article  Google Scholar 

  52. 52.

    Kabat GC, Cross AJ, Park Y et al (2009) Meat intake and meat preparation in relation to risk of postmenopausal breast cancer in the NIH-AARP diet and health study. Int J Cancer 124:2430–2435. doi:10.1002/ijc.24203

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. 53.

    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. doi:10.1038/sj.bjc.6605118

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Goodman MT, Nomura AM, Wilkens LR, Hankin J (1992) The association of diet, obesity, and breast cancer in Hawaii. Cancer Epidemiol Biomark Prev 1:269–275

    CAS  Google Scholar 

  55. 55.

    Steck SE, Gaudet MM, Eng SM et al (2007) Cooked meat and risk of breast cancer—lifetime versus recent dietary intake. Epidemiology 18:373–382. doi:10.1097/01.ede.0000259968.11151.06

    Article  PubMed  Google Scholar 

  56. 56.

    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. doi:10.1007/s10549-011-1538-7

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  57. 57.

    Mourouti N, Kontogianni MD, Papavagelis C et al (2015) Meat consumption and breast cancer: a case–control study in women. Meat Sci 100:195–201. doi:10.1016/j.meatsci.2014.10.019

    Article  PubMed  Google Scholar 

  58. 58.

    Chandran U, Zirpoli G, Ciupak G et al (2013) Racial disparities in red meat and poultry intake and breast cancer risk. Cancer Causes Control 24:2217–2229. doi:10.1007/s10552-013-0299-5

    Article  PubMed  PubMed Central  Google Scholar 

  59. 59.

    Guo J, Wei W, Zhan L (2015) Red and processed meat intake and risk of breast cancer: a meta-analysis of prospective studies. Breast Cancer Res Treat 151:191–198. doi:10.1007/s10549-015-3380-9

    CAS  Article  PubMed  Google Scholar 

  60. 60.

    Richardson S, Gerber M, Cenée S (1991) The role of fat, animal protein and some vitamin consumption in breast cancer: a case control study in southern France. Int J Cancer 48:1–9

    CAS  PubMed  Google Scholar 

  61. 61.

    Zhang C-X, Ho SC, Chen Y-M et al (2009) Meat and egg consumption and risk of breast cancer among Chinese women. Cancer Causes Control 20:1845–1853. doi:10.1007/s10552-009-9377-0

    CAS  Article  PubMed  Google Scholar 

  62. 62.

    Franceschi S, Favero A, La Vecchia C et al (1995) Influence of food groups and food diversity on breast cancer risk in Italy. Int J Cancer 63:785–789

    CAS  Article  PubMed  Google Scholar 

  63. 63.

    Engelman RW, Day NK, Good RA (1994) Calorie intake during mammary development influences cancer risk: lasting inhibition of C3H/HeOu mammary tumorigenesis by peripubertal calorie restriction. Cancer Res 54:5724–5730

    CAS  PubMed  Google Scholar 

  64. 64.

    Farvid MS, Cho E, Chen WY et al (2014) Dietary protein sources in early adulthood and breast cancer incidence: prospective cohort study. BMJ 348:g3437. doi:10.1136/bmj.g3437

    Article  PubMed  PubMed Central  Google Scholar 

  65. 65.

    Farvid MS, Cho E, Chen WY et al (2015) Adolescent meat intake and breast cancer risk. Int J Cancer 136:1909–1920. doi:10.1002/ijc.29218

    CAS  Article  PubMed  Google Scholar 

  66. 66.

    Batis C, Hernandez-Barrera L, Barquera S et al (2011) Food acculturation drives dietary differences among Mexicans, Mexican Americans, and Non-Hispanic Whites. J Nutr 141:1898–1906. doi:10.3945/jn.111.141473

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  67. 67.

    Dai Q, Shu X-O, Jin F et al (2002) Consumption of animal foods, cooking methods, and risk of breast cancer. Cancer Epidemiol Biomark Prev 11:801–808

    Google Scholar 

  68. 68.

    Daniel CR, Cross AJ, Graubard BI et al (2011) Prospective investigation of poultry and fish intake in relation to cancer risk. Cancer Prev Res 4:1903–1911. doi:10.1158/1940-6207.CAPR-11-0241

    Article  Google Scholar 

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Acknowledgments

The Breast Cancer Health Disparities Study was funded by Grant CA14002 from the National Cancer Institute to Dr. Slattery. The San Francisco Bay Area Breast Cancer Study was supported by Grants CA63446 and CA77305 from the National Cancer Institute, Grant DAMD17-96-1-6071 from the US Department of Defense, and Grant 7PB-0068 from the California Breast Cancer Research Program. The collection of cancer incidence data used in this study was supported by the California Department of Public Health as part of the statewide cancer reporting program mandated by California Health and Safety Code Section 103885; the National Cancer Institute’s Surveillance, Epidemiology and End Results Program under contract HHSN261201000036C awarded to the Cancer Prevention Institute of California; and the Centers for Disease Control and Prevention’s National Program of Cancer Registries, under agreement #1U58 DP000807-01 awarded to the Public Health Institute. The 4-Corners Breast Cancer Study was funded by Grants CA078682, CA078762, CA078552, and CA078802 from the National Cancer Institute. The research also was supported by the Utah Cancer Registry, which is funded by contract N01-PC-67000 from the National Cancer Institute, with additional support from the State of Utah Department of Health, the New Mexico Tumor Registry, and the Arizona and Colorado cancer registries, funded by the Centers for Disease Control and Prevention National Program of Cancer Registries and additional state support. The contents of this manuscript are solely the responsibility of the authors and do not necessarily represent the official view of the National Cancer Institute or endorsement by the State of California Department of Public Health, the National Cancer Institute, and the Centers for Disease Control and Prevention or their Contractors and Subcontractors. The Mexico Breast Cancer Study was funded by Consejo Nacional de Ciencia y Tecnología (CONACyT) (SALUD-2002-C01-7462). Mariana C. Stern received support from Grant RSF-09-020-01-CNE from the American Cancer Society, from award number 5P30 ES07048 from the National Institute of Environmental Health Sciences and award number P30CA014089 from the National Cancer Institute. Andre E. Kim received support from Grant 5T32 ES013678 from the National Institute of Environmental Health Sciences.

Author contributions

We would also like to acknowledge the contributions of the following individuals to the study: Sandra Edwards for data harmonization oversight; Jennifer Herrick for data management and data harmonization; Erica Wolff and Michael Hoffman for laboratory support; Jocelyn Koo for data management for the San Francisco Bay Area Breast Cancer Study; Dr. Tim Byers for his contribution to the 4-Corners Breast Cancer Study; and Dr. Josh Galanter for assistance in selection of AIMs markers.

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Correspondence to Mariana C. Stern.

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Martha L. Slattery and Mariana C. Stern: Co-senior authors.

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Kim, A.E., Lundgreen, A., Wolff, R.K. et al. Red meat, poultry, and fish intake and breast cancer risk among Hispanic and Non-Hispanic white women: The Breast Cancer Health Disparities Study. Cancer Causes Control 27, 527–543 (2016). https://doi.org/10.1007/s10552-016-0727-4

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Keywords

  • Breast cancer
  • Meat
  • Hispanics
  • Processed meat