Dietary Fat and Breast Cancer: Controversy and Biological Plausibility

  • David P. Rose
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 364)

Abstract

The influence which dietary fat may exert on the development of breast cancer continues to provoke heated debate.1-5 The association between fat consumption and mammary carcinogenesis in experimental animals was first described by Tannenbaum over 50 years ago6 and has been confirmed repeatedly since then.7-9 In addition to influencing the promotional stage of carcinogenesis, dietary fat also affects the growth of transplantable rodent mammary carcinomas10-12 and of human breast cancer cells when injected into athymic nude mice.13-17

Keywords

Obesity Migration Corn Estrogen Testosterone 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Willett, W.C., DJ. Hunter, M.J. Stampfer, G. Colditz, J.E. Manson, D. Spiegelman, B. Ros-ner, C.H. Hennekens, and F.E. Speizer, Dietary fat and fiber in relation to risk of breast cancer. An 8-year follow-up, JAMA 268:2037 (1992).PubMedCrossRefGoogle Scholar
  2. 2.
    Howe, G.R., High-fat diets and breast cancer risk. The epidemiologic evidence, JAMA 268:2080(1992).PubMedCrossRefGoogle Scholar
  3. 3.
    Boyd, N.F., Nutrition and breast cancer,J. Natl. Cancer Inst. 85:6 (1993).PubMedCrossRefGoogle Scholar
  4. 4.
    Whittemore, A.S. and B.E. Henderson, Dietary fat and breast cancer: where are we?, J. Natl. Cancer Inst. 85:762 (1993).PubMedCrossRefGoogle Scholar
  5. 5.
    Freedman, L.S., R.L. Prentice, C. Clifford, W. Harlan, M. Henderson, and J. Rossouw, Dietary fat and breast cancer: where we are, J. Natl. Cancer Inst. 85:764 (1993).CrossRefGoogle Scholar
  6. 6.
    Tannenbaum, A., The genesis and growth of tumors. III. Effects of a high fat diet, Cancer Res. 2:468 (1942).Google Scholar
  7. 7.
    Cohen, L.A., Dietary fat and mammary cancer, in: Diet, Nutrition and Cancer: A Critical Evaluation, Vol. 1 Macronutrients and Cancer, B.S. Reddy and L.A. Cohen, eds., CRC Press, Boca Raton (1986).Google Scholar
  8. 8.
    Welsch, C.W., Dietary fat, calories, and mammary gland tumorigenesis, in: Exercise, Calories, Fat, and Cancer, M.M. Jacobs, ed., Plenum Press, New York (1992).Google Scholar
  9. 9.
    Cave, W.T. Jr., Dietary fat effects on animal models of breast cancer, in: Diet and Breast Cancer, E.K. Weisburger, ed., Plenum Press, New York (1994).Google Scholar
  10. 10.
    Rao, G.A. and S. Abraham, Enhanced growth rate of transplanted mammary adenocarcinoma induced in C3H mice by dietary linoleate, J. Natl. Cancer Inst. 56:431 (1976).PubMedGoogle Scholar
  11. 11.
    Hillyard, L.A. and S. Abraham, Effect of dietary polyunsaturated fatty acids on growth of mammary adenocarcinomas in mice and rats, Cancer Res. 39:4430 (1979).PubMedGoogle Scholar
  12. 12.
    Karmali, R.A., J. Marsh, and C. Fuchs, Effect of omega-3 fatty acids on growth of a rat mammary tumor, J. Natl. Cancer Inst. 73:457 (1984).PubMedGoogle Scholar
  13. 13.
    Pritchard, G.A., D.L. Jones, and R.E. Mansel, Lipids in breast cancer, Br. J. Surg.76:1069 (1989).Google Scholar
  14. 14.
    Borgeson, C.E., L. Pardini, R.S. Pardini, and R.C. Reitz, Effects of dietary fish oil on human mammary carcinoma and on lipid-metabolizing enzymes, Lipids 24:290 (1989).PubMedCrossRefGoogle Scholar
  15. 15.
    Gonzalez, M.J., R.A. Schemmel, J.I. Gray, L. Dugan Jr., L.G. Sheffield, and C.W. Welsch, Effect of dietary fat on growth of MCF-7 and MDA-MB-231 human breast carcinomas in athymic nude mice: relationship between carcinoma growth and lipid peroxidation product levels, Carcinogenesis 12:1231 (1991).PubMedCrossRefGoogle Scholar
  16. 16.
    Rose, D.P., J.M. Connolly, and C.L. Meschter, Effect of dietary fat on human breast cancer growth and lung metastasis in nude mice, J. Natl. Cancer Inst. 83:1491 (1991).PubMedCrossRefGoogle Scholar
  17. 17.
    Rose, D.P., M.A. Hatala, J.M. Connolly, and J. Rayburn, Effects of diets containing different levels of linoleic acid on human breast cancer growth and lung metastasis in nude mice, Cancer Res. 53:4686 (1993).PubMedGoogle Scholar
  18. 18.
    Armstrong, B. and R. Doll, Environmental factors and cancer incidence and mortality in different countries, with special reference to dietary practices, Int. J. Cancer 15:617 (1975).PubMedCrossRefGoogle Scholar
  19. 19.
    Hems, G., The contributions of diet and childbearing to breast cancer rates, Br. J. Cancer 37:974 (1978).PubMedCrossRefGoogle Scholar
  20. 20.
    Rose, D.P., A.P. Boyar, and E.L. Wynder, International comparisons of mortality rates for cancer of the breast, ovary, prostate, and colon, and per capita food consumption, Cancer 58:2363 (1986).PubMedCrossRefGoogle Scholar
  21. 21.
    Prentice, R.L. and L. Sheppard, Dietary fat and cancer: consistency of the epidemiologic data, and disease prevention that may follow from a practical reduction in fat consumption, Cancer Causes Control 1:81 (1990).PubMedCrossRefGoogle Scholar
  22. 22.
    Sasaki, S., M. Horacsek, and H. Kesteloot, An ecological study of the relationship between dietary fat intake and breast cancer mortality, Prev. Med. 22:187 (1993).PubMedCrossRefGoogle Scholar
  23. 23.
    Hirayama, T., Epidemiology of breast cancer with special reference to the role of diet, Prev. Med. 7:173 (1978).PubMedCrossRefGoogle Scholar
  24. 24.
    Howe, G.R., T. Hirohata, T.G. Hislop, J.M. Iscovich, J.-M. Yuan, K. Katsouyanni, F. Lubin, E. Marubini, B. Modan, T. Rohan, P. Toniolo, and Y. Shunzhang, Dietary factors and risk of breast cancer: Combined analysis of 12 case-control studies, J. Natl. Cancer Inst. 82:561 (1990).PubMedCrossRefGoogle Scholar
  25. 25.
    Howe, G.R., C.M. Friedenreich, M. Jain, and A.B. Miller, A cohort study of fat intake and risk of breast cancer, J. Natl. Cancer Inst. 83:336 (1991).PubMedCrossRefGoogle Scholar
  26. 26.
    Chlebowski, R.T., Dietary fat intake reduction for patients with resected breast cancer, in: Diet and Breast Cancer, E.K. Weisburger, ed., Plenum Press, New York (1994).Google Scholar
  27. 27.
    Rose, D.P. and J.M. Connolly, Effects of dietary omega-3 fatty acids on human breast cancer growth and metastases in nude mice, J. Natl. Cancer Inst. 85:1743 (1993).PubMedCrossRefGoogle Scholar
  28. 28.
    Rose, D.P., J.M. Connolly, and X.-H. Liu, Dietary fatty acids and human breast cancer cell growth, invasion, and metastasis, in: Diet and Breast Cancer, E.K. Weisburger, ed., Plenum Press, New York (1994).Google Scholar
  29. 29.
    Hursting, S.D., M. Thornquist, and M.M. Henderson, types of diet fat and the incidence of cancer at five sites, Prev. Med. 19:242 (1990).PubMedCrossRefGoogle Scholar
  30. 30.
    Jurkowski, J.J. and W.T. Cave Jr., Dietary effects of menhaden oil on the growth and membrane lipid composition of rat mammary tumors, J. Natl. Cancer Inst. 74:1145 (1985).PubMedGoogle Scholar
  31. 31.
    Carroll, K.K. and H.T. Khor, Effects of level and type of dietary fat on incidence of mammary tumors induced in female Sprague-Dawley rats by 7,12-dimethylbenz[a]anthracene, Lipids 6:415 (1971).PubMedCrossRefGoogle Scholar
  32. 32.
    Cohen, L.A., D.O. Thompson, Y. Maeura, K. Choi, M.E. Blank, and D.P. Rose, Dietary fat and mammary cancer. I. Promoting effects of different dietary fats on N-nitrosomethyl-urea-induced rat mammary tumorigenesis, J. Natl. Cancer Inst. 77:33 (1986).PubMedGoogle Scholar
  33. 33.
    Tinsley, I.J., J.A. Schmitz, and D.A. Pierce, Influence of dietary fatty acids on the incidence of mammary tumors in the C3H mouse, Cancer Res. 41:1460 (1981).PubMedGoogle Scholar
  34. 34.
    Wynder, E.L., Y. Fujita, R.E. Harris, T. Hirayama, and T. Hiyama, Comparative epidemiology of cancer between the United States and Japan. A second look, Cancer 67:746 (1991).PubMedCrossRefGoogle Scholar
  35. 35.
    Kamano, K., H. Okuyama, R. Konishi, and H. Nagasawa, Effects of a high-linoleate and a high α-linolenate diet on spontaneous mammary tumorigenesis in mice, Anticancer Res. 9:1903(1989).PubMedGoogle Scholar
  36. 36.
    Dupont, W.D. and D.L. Page, Risk factors for breast cancer in women with proliferative breast disease, N. Engl. J. Med. 312:146 (1985).PubMedCrossRefGoogle Scholar
  37. 37.
    Webber, W. and N. Boyd, A critique of the methodology of studies of benign breast disease and breast cancer risk, J. Natl. Cancer Inst. 77:397 (1986).PubMedGoogle Scholar
  38. 38.
    Carter, C.L., D.K. Carle, M.S. Micozzi, A. Schatzkin, and P.R. Taylor, A prospective study of the development of breast cancer in 16,692 women with benign breast disease, Am. J. Epidemiol 128:467 (1988).PubMedGoogle Scholar
  39. 39.
    Lubin, F., Y. Wax, E. Ron, M. Black, A. Chetrit, N. Rosen, E. Alfandary, and B. Modan, Nutritional factors associated with benign breast disease etiology: a case-control study, Am. J. Clin. Nutr. 50:551 (1989).PubMedGoogle Scholar
  40. 40.
    Hislop, T.G., P.R. Band, M. Deschamps, V. Ng, A.J. Coldman, AJ. Worth, and T. Labo, Diet and histologic types of benign breast disease defined by subsequent risk of breast cancer, Am. J. Epidemiol. 131:263 (1990).PubMedGoogle Scholar
  41. 41.
    Schnitt, S.J., A. Jimi, and M. Kojiro, The increasing prevalence of benign proliferative breast lesions in Japanese women, Cancer 71:2528 (1993).PubMedCrossRefGoogle Scholar
  42. 42.
    Wynder, E.L., D.P. Rose, and L.A. Cohen, Diet and breast cancer in causation and therapy, Cancer 58:1804 (1986).PubMedCrossRefGoogle Scholar
  43. 43.
    King, H. and F.B. Locke, Cancer mortality among Chinese in the United States, J. Natl. Cancer Inst. 65:1141 (1980).PubMedGoogle Scholar
  44. 44.
    Staszewski, J. and W. Haenszel, Cancer mortality among Polish born in the United States,J. Natl. Cancer Inst. 35:292 (1965).Google Scholar
  45. 45.
    Miller, A.B., A. Kelly, and N.W. Choi, A study of diet and breast cancer, Am. J. Epidemiol. 107:499 (1978).PubMedGoogle Scholar
  46. 46.
    Toniolo, P., E. Riboli, F. Protta, M. Charrel, and A.P.M. Cappa, Calorie-providing nutrients and risk of breast cancer, J. Natl. Cancer Inst. 81:278 (1989).PubMedCrossRefGoogle Scholar
  47. 47.
    Hislop, T.G., AJ. Coldman, and J.M. Elwood, Childhood and recent eating patterns and risk of breast cancer, Cancer Detect. Prev. 9:47 (1986).PubMedGoogle Scholar
  48. 48.
    Rohan, T.E., A.J. McMichael, and P.A. Baghurst, A population-based case-control study of diet and breast cancer in Australia, Am. J. Epidemiol. 128:478 (1988).PubMedGoogle Scholar
  49. 49.
    Lubin, F., Y.K. Wax, and B. Modan, Role of fat, animal protein and dietary fiber in breast cancer etiology: A case-control study, J. Natl. Cancer Inst. 77:605 (1986).PubMedGoogle Scholar
  50. 50.
    Hirohata, T., A. Nomura, J.H. Hankin, L.N. Kolonel, and J. Lee, An epidemiologic study on the association between diet and breast cancer, J. Natl. Cancer Inst. 78:595 (1987).PubMedGoogle Scholar
  51. 51.
    Iscovich, J., G.R. Howe, and J.M. Kaldor, A case-control study of breast cancer in Argentina, Int. J. Cancer 44:770 (1989).PubMedCrossRefGoogle Scholar
  52. 52.
    Katsouyanni, K., D. Trichopoulos, P. Boyle, E. Xirouchaki, A. Trichopoulou, B. Lisseos, S. Vasilaros, and B. MacMahon, Diet and breast cancer: a case-control study in Greece, Int. J. Cancer 38:815 (1986).PubMedCrossRefGoogle Scholar
  53. 53.
    Willett, W.C., MJ. Stampfer, G.A. Colditz, B.A. Rosner, C.H. Hennekens, and F.E. Speizer, Dietary fat and the risk of breast cancer, N. Engl. J. Med. 316:22 (1987).PubMedCrossRefGoogle Scholar
  54. 54.
    Wynder, E.L., E. Taioli, and D.P. Rose, Breast cancer—the optimal diet, in: Exercise, Calories, Fat, and Cancer, M.M. Jacobs, ed., Plenum Press, New York (1992).Google Scholar
  55. 55.
    Prentice, R.L., F. Kakar, S. Hursting, L. Sheppard, R. Klein, and L.H. Kushi, Aspects of the rationale for the Women’s Health Trial, J. Natl. Cancer Inst. 80:802 (1988).PubMedCrossRefGoogle Scholar
  56. 56.
    Cohen, L.A., K. Choi, J.H. Weisburger, and D.P. Rose, Effect of varying proportions of dietary fat on the development of N-nitrosomethylurea-induced rat mammary tumors, Anticancer Res. 6:215 (1986).PubMedGoogle Scholar
  57. 57.
    Rose, D.P., Diet, hormones, and cancer, Annu. Rev. Public Health 14:1 (1993).PubMedCrossRefGoogle Scholar
  58. 58.
    Jones, D.Y., A. Schatzkin, S.B. Green, G. Block, L.A. Brinton, R.G. Ziegler, R. Hoover, and P.R. Taylor, Dietary fat and breast cancer in the National Health and Nutrition Examination Survey. I. Epidemiologie Follow-up Study, J. Natl. Cancer Inst. 79:465 (1987).PubMedGoogle Scholar
  59. 59.
    Graham, S., M. Zielezny, J. Marshall, R. Priore, J. Freudenheim, J. Brasure, B. Haughey, P. Nasca, and M. Zdeb, Diet in the epidemiology of postmenopausal breast cancer in the New York State cohort, Am. J. Epidemiol. 136:1327 (1992).PubMedGoogle Scholar
  60. 60.
    van den Brandt, P.A., P. van’t Veer, R.A. Goldbohm, E. Dorant, A. Volovics, R.J.J. Hermus, and F. Sturmans}, A prospective cohort study on dietary fat and the risk of postmenopausal breast cancer, Cancer Res. 53:75 (1993).PubMedGoogle Scholar
  61. 61.
    Howe, G.R., Dietary fat and cancer: Response, J. Natl. Cancer Inst. 83:1035 (1991).Google Scholar
  62. 62.
    Rose, D.P., Dietary fiber and breast cancer, Nutr. Cancer 13:1 (1990).PubMedCrossRefGoogle Scholar
  63. 63.
    Knekt, P., D. Albanes, R. Seppänen, A. Aromaa, R. Järviven, L. Hyvönen, L. Teppo, and E. Pukkala, Dietary fat and risk of breast cancer, Am. J. Clin. Nutr. 52:903 (1990).PubMedGoogle Scholar
  64. 64.
    Wynder, E.L. and S.D. Stellman, The “over-exposed” control group, Am. J. Epidemiol. 135:459 (1992).PubMedGoogle Scholar
  65. 65.
    Wynder, E.L. and L.A. Cohen, A rationale for dietary intervention in the treatment of postmenopausal breast cancer patients, Nutr. Cancer 3:195 (1982).PubMedCrossRefGoogle Scholar
  66. 66.
    Chlebowski, R.T., D.P. Rose, I.M. Buzzard, G.L. Blackburn, W. Insull Jr., M. Grosvenor, R. Elashoff, and E.L. Wynder, Adjuvant dietary fat intake reduction in postmenopausal breast cancer patient management, Breast Cancer Res. Treat. 20:73 (1992).PubMedCrossRefGoogle Scholar
  67. 67.
    Cohen, L.A., D.P. Rose, and E.L. Wynder, A rationale for dietary intervention in postmenopausal breast cancer patients: An update, Nutr. Cancer 19:1 (1993).PubMedCrossRefGoogle Scholar
  68. 68.
    Wynder, E.L., T. Kajitani, J. Kuno, J.C. Lucas, and A. DePalo, A comparison of survival rates between American and Japanese patients with breast cancer, Surg. Gynecol. Obstet. 117:196(1963).PubMedGoogle Scholar
  69. 69.
    Sakamoto, G., H. Sugano, and W.H. Hartman, Comparative clinicopathological study of breast cancer among Japanese and American females, Jpn. J. Cancer 25:161 (1979).Google Scholar
  70. 70.
    Dickson, R.B. and M.E. Lippman, Estrogenic regulation of growth and polypeptide growth factor secretion in human breast carcinoma, Endocr. Rev. 8:29 (1987).PubMedCrossRefGoogle Scholar
  71. 71.
    Henderson, B.E., R. Ross, and L. Bernstein, Estrogens as a cause of human cancer: The Richard and Hilda Rosenthal Foundation Award Lecture, Cancer Res. 48:246 (1988).PubMedGoogle Scholar
  72. 72.
    Litherland, S. and M. Jackson, Antiestrogens in the management of hormone-dependent breast cancer, Cancer Treat. Rev. 15:183 (1987).CrossRefGoogle Scholar
  73. 73.
    Kelsey, J.L. and G.S. Berkowitz, Breast cancer epidemiology, Cancer Res. 48:5615 (1988).PubMedGoogle Scholar
  74. 74.
    Adami, H.-O., E.D.B. Johansson, J. Vegelius, and A. Victor, Serum concentrations of es-trone, androstenedione, testosterone and sex-hormone-binding globulin in postmenopausal women with breast cancer and in age-matched controls, Ups. J. Med. Sci. 84:259 (1979).PubMedCrossRefGoogle Scholar
  75. 75.
    Moore, J.W., G.M.G. Clark, R.D. Bulbrook, J.L. Hayward, J.T. Murai, G.L. Hammond, and P.K. Siiteri, Serum concentrations of total and non-protein-bound oestradiol in patients with breast cancer and in normal controls, Int. J. Cancer 29:17 (1982).PubMedCrossRefGoogle Scholar
  76. 76.
    Jones, L.A., D.M. Ota, G.A. Jackson, P.M. Jackson, K. Kemp, D.E. Anderson, S.K. McCamant, and D.H. Bauman, Bioavailability of estradiol as a marker for breast cancer risk assessment, Cancer Res. 47:5224 (1987).PubMedGoogle Scholar
  77. 77.
    Ota, D.M., L.A. Jones, G.L. Jackson, P.M. Jackson, K. Kemp, and D. Bauman, Obesity, non-protein-bound estradiol levels, and distribution of estradiol in the sera of breast cancer patients, Cancer 57:558 (1986).PubMedCrossRefGoogle Scholar
  78. 78.
    Takatani, O., H. Kosano, T. Okumoto, K. Akamatsu, S. Tamakuma, and H. Hiraide, Distribution of estradiol and percentage of free testosterone in sera of Japanese women: preop-erative breast cancer patients and normal controls, J. Natl. Cancer Inst. 79:1199 (1987).PubMedGoogle Scholar
  79. 79.
    Shimizu, H., R.K. Ross, L. Bernstein, M.C. Pike, and B.E. Henderson, Serum oestrogen levels in postmenopausal women: comparison of American whites and Japanese in Japan, Br.J. Cancer 62:451 (1990).PubMedCrossRefGoogle Scholar
  80. 80.
    Key, T.J.A., J. Chen, D.Y. Wang, M.C. Pike, and J. Boreham, Sex hormones in women in rural China and in Britain, Br. J. Cancer 62:631 (1990).PubMedCrossRefGoogle Scholar
  81. 81.
    Wang, D.Y., T.J.A. Key, M.C. Pike, J. Boreham, and J. Chen, Serum hormone levels in British and rural Chinese females, Breast Cancer Res. Treat. 18:S41 (1991).PubMedCrossRefGoogle Scholar
  82. 82.
    Goldin, B.R. and S.L. Gorbach, Hormone studies and the diet and breast cancer connection, in: Diet and Breast Cancer, E.K. Weisburger, ed., Plenum Press, New York (1994).Google Scholar
  83. 83.
    Rose, D.P., A.P. Boyar, C. Cohen, and L.E. Strong, Effect of a low-fat diet on hormone levels in women with cystic breast disease. I. Serum steroids and gonadotropins, J. Natl. Cancer Inst. 78:623 (1987).PubMedGoogle Scholar
  84. 84.
    Rose, D.P., J.M. Connolly, R.T. Chlebowski, I.M. Buzzard, and E.L. Wynder, The effects of a low-fat dietary intervention and tamoxifen adjuvant therapy on the serum estrogen and sex hormone-binding globulin concentrations of postmenopausal breast cancer patients, Breast Cancer Res. Treat. 27:253 (1993).PubMedCrossRefGoogle Scholar
  85. 85.
    Prentice, R.L., Dietary fat reduction as a hypothesis for the prevention of postmenopausal breast cancer, and a discussion of hypothesis testing research strategies, in: Diet and Breast Cancer, E.K. Weisburger, ed., Plenum Press, New York (1994).Google Scholar
  86. 86.
    Early Breast Cancer Trialists’ Collaborative Group, Systemic treatment of early breast cancer by hormonal, cytotoxic, or immune therapy: 133 randomised trials involving 31,000 recurrences and 24,000 deaths among 75,000 women, Lancet 339:71 (1992).Google Scholar
  87. 87.
    Nayfield, S.G., J.E. Korp, L.G. Ford, F.A. Dorr, and B.S. Kramer, Potential role of tamoxifen in prevention of breast cancer, J. Natl. Cancer Inst. 83:1450 (1991).PubMedCrossRefGoogle Scholar
  88. 88.
    Jordan, V.C., Chemosuppression of breast cancer with long-term tamoxifen therapy, Prev. Med. 20:3 (1991).PubMedCrossRefGoogle Scholar
  89. 89.
    Adlercreutz, H., H. Honjo, A. Higashi, T. Fotsis, E. Hämäläinen, T. Hasegawa, and H. Okada, Urinary excretion of lignans and isoflavonoid phytoestrogens in Japanese men and women consuming a traditional Japanese diet, Am. J. Clin. Nutr. 54:1093 (1991).PubMedGoogle Scholar
  90. 90.
    Rose, D.R, Dietary fiber, phytoestrogens, and breast cancer, Nutrition 8:47 (1992).PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1994

Authors and Affiliations

  • David P. Rose
    • 1
  1. 1.Division of Nutrition and EndocrinologyAmerican Health FoundationValhallaUSA

Personalised recommendations