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Exposure, susceptibility, and breast cancer risk: A hypothesis regarding exogenous carcinogens, breast tissue development, and social gradients, including black/white differences, in breast cancer incidence

Breast Cancer Research and Treatment volume 13, pages 205–223 (1989)Cite this article

Summary

At present, known risk factors account for only one-third of breast cancer cases diagnosed in the United States. They explain an even smaller fraction of the ten-fold variation in international breast cancer incidence rates. The low population-attributable risk of these identified risk factors, plus the existence of phenomena that cannot be easily explained by current etiologic hypotheses (such as the higher rate of breast cancer among black as compared to white women under age 40 within the United States), suggests that unidentified risk factors contribute substantially to breast cancer causation. This paper summarizes evidence to propose that two socially-conditioned factors determine a society's breast cancer incidence and its social gradients in risk: 1) the extent of exposure to exogenous carcinogens, and 2) breast tissue susceptibility to these exposures. It is further hypothesized that breast tissue susceptibility is inversely related to breast tissue differentiation, and that socially-mediated reproductive patterns (involving both early-terminated and full-term pregnancies) affect susceptibility both by altering (via hormonally-mediated mechanisms) the number and ratio of undifferentiated and differentiated cells, and by stimulating the growth of initiated and transformed cells. This view is presented in contrast to hypotheses that propose exposure to endogenous hormones as the major determinant of breast cancer risk.

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Abbreviations

BBD:

Benign Breast Disease

DDE:

Dichlorodiphenyl Dichloroethene

ETP:

Early-Terminated Pregnancy

FETP:

First Early-Terminated Pregnancy

FFTP:

First Full-Term Pregnancy

FTP:

Full-Term Pregnancy

OC:

Oral Contraceptive

PCB:

Polychlorinated Biphenyl

RR:

Relative Risk

SES:

Socioeconomic Status

TDLU:

Terminal Ductal-Lobular Unit

References

  1. U.S. Department of Health and Human Services: SEER program: cancer incidence and mortality in the United States, 1973–1981. NIH Pub. No. 85-1837. National Cancer Institute, Bethesda, MD, 1984

    Google Scholar 

  2. U.S. Department of Health and Human Services, Division of Cancer Prevention and Control: 1986 Annual Cancer Statistics Review. NIH Pub. No. 87-2789. National Cancer Institute, Bethesda, MD, 1987

    Google Scholar 

  3. American Cancer Society: Cancer Facts and Figures — 1987. American Cancer Society, New York, 1987

    Google Scholar 

  4. Donn AC, Muir CS: Breast cancer epidemiology and risk factors. In: Khogali M, Omar YT, Gjorgov A, Ismail AS (eds) Cancer Prevention in Developing Countries. Pergamon Press, Oxford, 1986, pp 155–166

    Google Scholar 

  5. Kelsey JL, Berkowitz GS: Breast cancer epidemiology. Cancer Res 48: 5615–5623, 1988

    PubMed  Google Scholar 

  6. Kelsey JL, Hildreth NG: Breast and gynecological cancer epidemiology. CRC Press, Boca Raton FL, 1985

    Google Scholar 

  7. Vorherr H: Breast Cancer: Epidemiology, Endocrinology, Biochemistry and Pathobiology. Urban and Schwarzenberg, Baltimore MD, 1980

    Google Scholar 

  8. Henderson BE, Pike MC, Gray GE: The epidemiology of breast cancer. In: Hoogstraten B, McDivitt RW (eds) Breast Cancer. CRC Press, Boca Raton FL, 1981, pp 1–25

    Google Scholar 

  9. DeWaard F: Epidemiology of breast cancer: a review. Eur J Cancer Clin Oncol 119: 1671–1676, 1983

    Article  Google Scholar 

  10. Boyle P, Leake R: Progress in understanding breast cancer: epidemiological and biological interactions. Breast Cancer Res Treat 11: 91–112, 1988

    Article  PubMed  Google Scholar 

  11. MacMahon B, Cole P, Lin TM: Age at first birth and breast cancer risk. Bull Wld Hlth Org 43: 209–221, 1970

    Google Scholar 

  12. Trichopoulos D, Hsieh CC, MacMahon B, Lin T, Lowe CR, Mirra AP, Ravnihar B, Salber EJ, Valaoras VG, Yuasa S: Age at any birth and breast cancer risk. Int J Cancer 31: 701–704, 1983

    PubMed  Google Scholar 

  13. Goodwin PJ, Boyd NF: Critical appraisal of the evidence that dietary fat is related to breast cancer risk in humans. JNCI 79: 473–485, 1987

    PubMed  Google Scholar 

  14. Willett WC, Stampfer MJ, Colditz GA, Rosner BA, Hennekens CH, Speizer FE: Dietary fat and the risk of breast cancer. N Engl J Med 316: 22–28, 1987

    PubMed  Google Scholar 

  15. Rohan TE, McMichael AH, Baghurst PA: A population-based case-control study of diet and breast cancer in Australia. Am J Epidemiol 128: 478–489, 1988

    PubMed  Google Scholar 

  16. Le MG, Moulton LH, Hill C, Kramer A: Consumption of dairy products and alcohol in a case-control study of breast cancer. JNCI 77: 633–636, 1986

    PubMed  Google Scholar 

  17. La Vecchia C, Decari A, Francheschi S, Pampallona S, Togoni G: Alcohol consumption and the risk of breast cancer in women. JNCI 75: 61–65, 1985

    PubMed  Google Scholar 

  18. Harvey EB, Schairer C, Brinton LA, Hoover RN, Fraumeni JF Jr: Alcohol consumption and breast cancer. JNCI 78: 657–661, 1987

    PubMed  Google Scholar 

  19. Willett WC, Stampfer MJ, Colditz GA, Rosner BA, Hennekens CH, Speizer FE: Moderate alcohol consumption and the risk of breast cancer. N Engl J Med 316: 1174–1180, 1987

    PubMed  Google Scholar 

  20. Schatzkin A, Jones DY, Hoover RN, Philip PR, Brinton LA, Ziegler RG, Harvey EB, Carter CL, Licitra LM, Dufour MC, Larson DB: Alcohol consumption and breast cancer in the epidemiological follow-up study of the first National Health And Nutrition Examination Survey. N Engl J Med 316: 1169–1173, 1987

    PubMed  Google Scholar 

  21. O'Connell DL, Hulka BS, Chambless LE, Wilkinson WE, Deubner DC: Cigarette smoking, alcohol consumption and breast cancer risk. JNCI 78: 229–234, 1987

    PubMed  Google Scholar 

  22. Longnacker HP, Berlin JA, Orza JG, Chalmers TC: A meta-analysis of alcohol consumption in relation to risk of breast cancer. JAMA 260: 652–656, 1988

    Article  PubMed  Google Scholar 

  23. Webber W, Boyd N: A critique of the methodology of studies of benign breast disease and breast cancer risk. JNCI 77: 397–404, 1986

    PubMed  Google Scholar 

  24. Wang DY, Fentiman IS: Epidemiology and endocrinology of benign breast disease. Breast Cancer Res Treat 6: 5–36, 1985

    Article  PubMed  Google Scholar 

  25. Carter CL, Corle DK, Micozzi MS, Schatzkin A, Taylor PR: A prospective study of the development of breast cancer in 16,692 women with benign breast disease. Am J Epidemiol 128: 467–477, 1988

    PubMed  Google Scholar 

  26. McPherson K, Vessey MP, Neil A, Doll R, Jones L, Roberts M: Early oral contraceptive use and breast cancer: results of another case-control study. Br J Cancer 56: 653–661, 1987

    PubMed  Google Scholar 

  27. Hennekens CH, Speizer FE, Lipnick RJ, Rosner B, Bain C, Belanger C, Stampfer MJ, Willett W, Peto R: A casecontrol study of oral contraceptive use and breast cancer. JNCI 72: 39–42, 1984

    PubMed  Google Scholar 

  28. Meirik B, Lund E, Adami HO, Bergstrom R, Christoffersen T, Bergsjo P: Contraceptive use and breast cancer in young women. Lancet ii: 650–654, 1986

    Article  Google Scholar 

  29. Pike MC, Henderson BE, Casagrande JT, Rosario I, Gray GE: Oral contraceptive use and early abortion as risk factors for breast cancer in young women. Br J Cancer 43: 72–76, 1981

    PubMed  Google Scholar 

  30. Choi NW, Howe GR, Miller AB, Matthews V, Morgan RW, Munan L, Burch JD, Feather J, Jain M, Kelly A: An epidemiological study of breast cancer. Am J Epidemiol 107: 510–521, 1978

    PubMed  Google Scholar 

  31. Hadjimichael OC, Boyle CA, Meis JW: Abortion before first livebirth and risk of breast cancer. Br J Cancer 53: 281–284, 1986

    PubMed  Google Scholar 

  32. Ewertz M, Duffy SW: Risk of breast cancer in relation to reproductive factors in Denmark. Br J Cancer 58: 99–104, 1988

    PubMed  Google Scholar 

  33. Helmrich SP, Shapiro S, Rosenberg L, Kaufman DW, Slone D, Bain C, Miettinen OS, Stolley PD, Rosenshein NB, Knapp RC, Leavitt T Jr, Schottenfeld D, Engle RL Jr, Levy M: Risk factors for breast cancer. Am J Epidemiol 117: 35–45, 1983

    PubMed  Google Scholar 

  34. Kvale G, Heuch I, Eide GE: A prospective study of reproductive factors and breast cancer. I. Parity. Am J Epidemiol 126: 831–841, 1987

    PubMed  Google Scholar 

  35. Kvale G, Heuch I: A prospective study of reproductive factors and breast cancer. II. Age at first and last birth. Am J Epidemiol 126: 842–850, 1987

    PubMed  Google Scholar 

  36. McTiernan A, Thomas DB: Evidence for a protective effect of lactation on risk of breast cancer in young women: results from a case-control study. Am J Epidemiol 124: 353–358, 1986

    PubMed  Google Scholar 

  37. Willett W, Stampfer MJ, Bain C, Lipnick R, Speizer FE, Rosner B, Cramer D, Hennekens CH: Cigarette smoking, relative weight and menopause. Am J Epidemiol 117: 651–658, 1983

    PubMed  Google Scholar 

  38. Green A, Willett WC, Colditz GA, Stampfer MJ, Bain C, Rosner B, Hennekens C, Speizer FE: Use of permanent hair dyes and risk of breast cancer. JNCI 79: 253–257, 1987

    PubMed  Google Scholar 

  39. Schairer C, Brinton LA, Hoover RN: Methylxanthines and breast cancer. Int J Cancer 46: 469–473, 1987

    Google Scholar 

  40. Korenman S: Reproductive endocrinology and breast cancer in women. In: Pike MC, Siiteri PK, Welsch C (eds) Banbury Report 8. Hormones and Breast Cancer. Cold Spring Harbor Laboratory, Cold Spring Harbor NY, 1981, pp 71–83

    Google Scholar 

  41. Musey VG, Collins DC, Musey PI, Martino-Saltzman D, Preedy JRK: Long-term effects of a first pregnancy on the secretion of prolactin. N Engl J Med 316: 229–234, 1987

    PubMed  Google Scholar 

  42. Brinton LA, Hoover R, Fraumini JF Jr: Interaction of familial and hormonal risk factors for breast cancer. JNCI 69: 817–822, 1982

    PubMed  Google Scholar 

  43. Henderson BE, Ross RK, Pike MC, Casagrande JT: Endogenous hormones as a major factor in human cancer. Cancer Res 42: 3232–3239, 1982

    PubMed  Google Scholar 

  44. Pike MC, Krailo MD, Henderson BE, Casagrande JT, Hoel DG: ‘Hormonal’ risk factors, ‘breast tissue age’, and the age-incidence of breast cancer. Nature 303: 767–770, 1983

    Article  PubMed  Google Scholar 

  45. Weisberger JH, Williams GM: Carcinogen testing: Current problems and new approaches. Science 214: 401–407, 1981

    PubMed  Google Scholar 

  46. Wysowski DK, Comstock GW, Helsing KJ, Lau HL: Sex hormone levels in serum in relation to the development of breast cancer. Am J Epidemiol 124: 791–799, 1987

    Google Scholar 

  47. Myers F, Brown JB, Morrison AS, MacMahon B: Endogenous sex hormones, prolactin and breast cancer in premenopausal women. JNCI 77: 613–616, 1986

    PubMed  Google Scholar 

  48. Siiteri PK, Simberg N, Murai J: Estrogens and breast cancer. Ann NY Acad Sci 464: 100–105, 1986

    PubMed  Google Scholar 

  49. Cole P, Cramer D, Yen S, Paffenbarger R, MacMahon B, Brown J: Estrogen profiles of premenopausal women with breast cancer risk. Cancer Res 38: 745–748, 1978

    PubMed  Google Scholar 

  50. MacMahon B, Cole P, Brown JB, Paffenbarger R, Trichopoulos D, Yen S: Urine estrogens, frequency of ovulation, and breast cancer risk: a case-control study in premenopausal women. JNCI 70: 247–250, 1982

    Google Scholar 

  51. Ernster VL, Wrensch MR, Petrakis NL, King EB, Miike R, Murai J, Godson WH III, Siiteri PK: Benign and malignant breast disease: initial study results of serum and breast fluid analyses of endogenous estrogens. JNCI 79: 949–960, 1987

    PubMed  Google Scholar 

  52. Fishman J, Fukushima D, O'Connor J, Rosenfeld RS, Lynch HT, Lynch JF, Guirgis H, Maloney K: Plasma hormone profiles of young women at risk for familial breast cancer. Cancer Res 38: 4006–4011, 1978

    PubMed  Google Scholar 

  53. Yu MC, Gerkins VR, Henderson BE, Brown JB, Pike MC: Elevated levels of prolactin in nulliparous women. Br J Cancer 43: 826–831, 1981

    PubMed  Google Scholar 

  54. Hill P, Wynder EL, Helman P, Hickman R, Rona G, Kuno K: Plasma hormone levels in different ethnic populations of women. Cancer Res 36: 2297–2301, 1976

    PubMed  Google Scholar 

  55. MacMahon B, Trichopoulos D, Brown J, Andersen AP, Cole P, DeWaard F, Kauraniemi T, Polychronopoulou A, Ravnihar B, Stormby N, Westland K: Age at menarche, urine estrogens and breast cancer risk. Int J Cancer 30: 427–431, 1982

    PubMed  Google Scholar 

  56. Sukumar S, Carney WP, Barbacid M: Independent molecular pathways in initiation and loss of hormone responsiveness of breast carcinoma. Science 240: 524–526, 1988

    PubMed  Google Scholar 

  57. Van Zwieten MJ: The Rat as an Animal Model in Breast Cancer Research. Martinus Nijhoff, Boston MA, 1984

    Google Scholar 

  58. Welsch CW, Nagasawa H: Prolactin and murine mammary tumorigenesis: a review. Cancer Res 37: 951–963, 1977

    PubMed  Google Scholar 

  59. Berg JW: Clinical importance of risk factors for breast cancer. Cancer 53: 589–591, 1984

    Google Scholar 

  60. Seidman H, Stellman SD, Mushinski MH: A different perspective on breast cancer risk factors: some implications of nonattributable risk. CA-A 32: 301–313, 1982

    Google Scholar 

  61. Nomura AMY, Lee J, Kolonel LN, Hirohata T: Breast cancer incidence in two populations with different levels of risk for the disease. Am J Epidemiol 119: 496–502, 1984

    PubMed  Google Scholar 

  62. Dorn HF: Illness from cancer in the United States. Public Health Reports 59(2): 33–35, (3): 65–67, (4): 97–115, 1944

    Google Scholar 

  63. Dorn HF, Cutler SJ: Morbidity from cancer in the United States: Part I — Variation in incidence by age, sex, race, marital status, and geographic region. U.S. Dept. of Health, Education, and Welfare Public Health Monograph No. 29. U.S. Government Printing Office, Washington DC, 1959

    Google Scholar 

  64. Cutler SJ, Young JL Jr: Third national cancer survey: incidence data. U.S. Government Printing Office, Washington DC, 1975

    Google Scholar 

  65. Gray GE, Henderson BE, Pike MC: Changing ratio of breast cancer incidence rates with age of black females compares with white females in the United States. JNCI 64: 461–463, 1980

    PubMed  Google Scholar 

  66. White E, Daling JR, Norsted TL, Chu J: Rising incidence of breast cancer among young women in Washington state. JNCI 79: 239–243, 1987

    PubMed  Google Scholar 

  67. Austin H, Cole P, Wynder E: Breast cancer in black american women. Int J Cancer 24: 541–544, 1979

    PubMed  Google Scholar 

  68. Schatzkin A, Palmer JR, Rosenberg L, Helmrich SP, Miller DR, Kaufman DW, Lesko SM, Shapiro S: Risk factors for breast cancer in black women. JNCI 78: 213–217, 1987

    PubMed  Google Scholar 

  69. Devesa SS, Diamond EL: Association of breast cancer and cervical cancer incidence with income and education among whites and blacks. JNCI 65: 515–528, 1980

    PubMed  Google Scholar 

  70. U.S. Department of Health and Human Services: Report of the Secretary's task force on black and minority health, vol. 3: Cancer. U.S. Government Printing Office, Washington DC, 1986

    Google Scholar 

  71. Kumanyika S, Helitzer DL: Nutritional status and dietary patterns of racial minorities. In: U.S. Department of Health and Human Services, ed. Report of the Secretary's task force on black and minority health, vol. 2: Crosscutting issues in minority health. U.S. Government Printing Office, Washington DC, 1985, pp 118–190

    Google Scholar 

  72. Cronin FJ, Krebs-Smith SM, Wyse BW, Light L: Characterizing food usage by demographic variables. J Am Dietet Assoc 81: 661–673, 1982

    Google Scholar 

  73. Patterson BH, Block G: Food choices and cancer guidelines. Am J Public Health 78: 282–286, 1988

    PubMed  Google Scholar 

  74. White E: Projected changes in breast cancer incidence due to a trend toward delayed childbearing. Am J Public Health 77: 495–497, 1987

    PubMed  Google Scholar 

  75. U.S. Bureau of the Census: The social and economic status of the black population in the United States: An historical view, 1790–1978. Current Population Reports, Special Studies, Series P-23, No. 80. U.S. Government Printing Office, Washington DC, 1980

    Google Scholar 

  76. Hayes CD: Risking the future: adolescent sexuality, pregnancy and childbearing, Vol. I. National Academy Press, Washington DC, 1987

    Google Scholar 

  77. Krieger N: Rising incidence of breast cancer (letter). JNCI 80: 2, 1988

    PubMed  Google Scholar 

  78. Ventura SJ, Taffel SM, Mosher WD: Estimates of pregnancies and pregnancy rates for the United States, 1976–85. Am J Public Health 78: 504–511, 1988

    Google Scholar 

  79. O'Hare WP: Black demographic trends in the 1980s. Milbank Memorial Fund Quarterly 65 (Suppl 1): 35–55, 1987

    Google Scholar 

  80. U.S. Bureau of the Census: Statistical Abstract of the United States: 1985 (105th edition). U.S. Government Printing Office, Washington DC, 1984, p 63

    Google Scholar 

  81. Cairns J: Mutation selection and the natural history of cancer. Nature 255: 197–200, 1975

    Article  PubMed  Google Scholar 

  82. Russo J, Tay LK, Russo IH: Differentiation of the mammary gland and susceptibility to carcinogenesis. Breast Cancer Res Treat 2: 5–73, 1982

    Article  PubMed  Google Scholar 

  83. Russo J, Calaf G, Roi L, Russo IH: Influence of age and gland topography on cell kinetics of normal human breast tissue. JNCI 78: 413–418, 1987

    PubMed  Google Scholar 

  84. Potten CS, Watson RJ, Williams GT, Tickle S, Roberts SA, Harris M, Howell A: The effect of age and menstrual cycle upon proliferative activity of the normal human breast. Br J Cancer 58: 163–170, 1988

    PubMed  Google Scholar 

  85. Albanes D, Winick M: Are cell number and cell proliferation risk factors for cancer? JNCI 80: 772–775, 1988

    PubMed  Google Scholar 

  86. Susser M, Watson W, Hopper K: Sociology in Medicine, 3rd edition. Oxford University Press, New York, 1985, pp 3–27

    Google Scholar 

  87. Doyal L: The Political Economy of Health. South End Press, Boston MA, 1979

    Google Scholar 

  88. Sander D: The Struggle for Health: Medicine and the Politics of Underdevelopment. MacMillan Publishers, London, 1985

    Google Scholar 

  89. Beardsley EH: A History of Neglect: Health Care for Blacks and Millworkers in the Twentieth-century South. University of Tennessee Press, Knoxville TN, 1987

    Google Scholar 

  90. Krieger N, Basset M: The health of black folk: disease, class and ideology in science. Monthly Review 38: 74–85, 1986

    Google Scholar 

  91. Drife JO: Breast development in puberty. Ann NY Acad Sci 464: 58–65, 1986

    PubMed  Google Scholar 

  92. Knight CH, Peaker M: Development of the mammary gland. J Reprod Fert 65: 521–536, 1982

    Google Scholar 

  93. Furnival CM: Function of the normal breast: physiology and endocrine control. In: Forbes JF (ed) Breast Disease. Churchill Livingston, Edinburgh, 1986, pp 1–19

    Google Scholar 

  94. Anderson TJ, Ferguson DJP, Raab GM: Cell turnover in the ‘resting’ human breast: influence of parity, contraceptive pill, age and laterally. Br J Cancer 46: 376–382, 1982

    PubMed  Google Scholar 

  95. Wellings SR, Jensen HM, Marcum RG: An atlas of sub-gross pathology of the human breast with special reference to possible precancerous lesions. JNCI 55: 231–243, 1975

    PubMed  Google Scholar 

  96. Azzopardi JG: Problems in Breast Pathology. WB Saunders, London, 1977

    Google Scholar 

  97. Taylor-Papadimitriou J, Lanne EG, Chang SE: Cell lineages and interactions in neoplastic expression in the human breast. In: Rich MA, Hager JC, Furmanski P (eds) Understanding Breast Cancer. Marcel Dekker, New York, 1983, pp 215–246

    Google Scholar 

  98. Squartini F, Bistorchi M, Sarnelli R, Basolo F: Early pathologic changes in experimental and human breast cancer: facts and comments. Ann NY Acad Sci 464: 231–261, 1986

    PubMed  Google Scholar 

  99. Moolgavkar SH, Day SE, Stevens RG: Two-stage model of carcinogenesis: Epidemiology of breast cancer in females. JNCI 65: 559–569, 1980

    PubMed  Google Scholar 

  100. Chavkin W: Introduction. In: Chavkin W (ed) Double Exposure: Women's Health Hazards on the Job and at Home. Monthly Review Press, New York, 1984, pp 1–13

    Google Scholar 

  101. Tokunga M, Tokuaka S, Lind CE: Breast cancer in atomic bomb survivors. Gann 32: 167–177, 1986

    Google Scholar 

  102. Boice JD Jr, Manson RR: Breast cancer in women after repeated fluoroscopic examinations of the chest. JNCI 59: 823–832, 1977

    PubMed  Google Scholar 

  103. Buell PL: Changing incidence of breast cancer in Japanese-American women. JNCI 51: 1479–1483, 1973

    PubMed  Google Scholar 

  104. Staszweski J, Haenzel WM: Cancer mortality among the Polish-born in the United States. JNCI 35: 291–297, 1965

    PubMed  Google Scholar 

  105. Newell GR, Mills PK: Cancer rates in Hispanic women related to social and economic factors. In: Stellman SD (ed) Women and Cancer. Harrington Park Press, New York, 1987, pp 23–35

    Google Scholar 

  106. Petrakis NL: Physiologic, biochemical, and cytological aspects of nipple aspirate fluid. Breast Cancer Res Treat 8: 7–19, 1986

    Article  PubMed  Google Scholar 

  107. Rizk SL, Sky-Peck HH: Comparison between concentration of trace elements in normal and neoplastic human breast tissue. Cancer Res 44: 5390–5394, 1984

    PubMed  Google Scholar 

  108. Rogan WJ, Bagniewska A, Domstra T: Current concepts: pollutants in breast milk. N Engl J Med 302: 1450–1453, 1980

    PubMed  Google Scholar 

  109. Rogan WJ, Gladen BC, McKinney JD, Carreras N, Hardy P, Thullen J, Tingelstad J, Tully M: Polychlorinated biphenyls (PCBs) and dichloroethane (DDE) in human milk: effects of maternal factors and previous lactation. Am J Public Health 76: 172–177, 1986

    PubMed  Google Scholar 

  110. Wynder EL, Brous IJ, Hirayama T: A study of the epidemiology of breast cancer. Cancer 13: 559–601, 1960

    PubMed  Google Scholar 

  111. Valaoras VG, Trichopoulos D, Polychronopoulou A: Lactation and reproductive histories of breast cancer patients in Greater Athens, 1965–67. Int J Cancer 4: 350–363, 1969

    PubMed  Google Scholar 

  112. Yuasa S, MacMahon B: Lactation and reproductive histories of breast cancer patients in Tokyo, Japan. Bull Wld Hlth Org 42: 195–204, 1970

    Google Scholar 

  113. Mirra AP, Cole P, MacMahon B: Breast cancer in an area of high parity: Sao Paolo, Brazil. Cancer Res 31: 77–83, 1971

    PubMed  Google Scholar 

  114. Brinton LA, Hoover R, Fraumeni JF Jr: Reproductive factors in the aetiology of breast cancer. Br J Cancer 47: 757–762, 1983

    PubMed  Google Scholar 

  115. Rosenberg L, Palmer JR, Kaufman DWS, Strom BL, Schottenfeld D, Shapiro S: Breast cancer in relation to the occurrence and time of induced and spontaneous abortion. Am J Epidemiol 127: 981–989, 1988

    PubMed  Google Scholar 

  116. Kaufman DW, Miller DR, Rosenberg L, Helmrich SP, Stolley P, Schottenfeld D, Shapiro S: Noncontraceptive estrogen use and the risk of breast cancer. JAMA 252: 63–67, 1984

    Article  PubMed  Google Scholar 

  117. Buring JE, Hennekens CH, Lipnick RJ, Willett W, Stampfer MR, Rosner B, Peto R, Speizer FE: A prospective cohort study of postmenopausal hormone use and risk of breast cancer in US women. Am J Epidemiol 125: 939–947, 1987

    PubMed  Google Scholar 

  118. Vessey MP, McPherson K, Yeates D, Doll R: Oral contraceptive use and abortion before first term pregnancy in relation to breast cancer risk. Br J Cancer 43: 327–331, 1982

    Google Scholar 

  119. Clavel F, Benham ASE, Sitruk-Ware R, Mauvais-Jarvis P, Flamant P: Breast cancer and oral contraceptives: a review. Contraception 32: 553–569, 1985

    PubMed  Google Scholar 

  120. Stadel BV, Rubin GL, Webster LA, Schlesselman JJ, Wingo PA: Oral contraceptives and breast cancer in young women. Lancet ii: 970–973, 1985

    Article  Google Scholar 

  121. Paul C, Skegg DCG, Spears FGS, Kaldor JM: Oral contraceptives and breast cancer: a national study. Br Med J 293: 723–726, 1986

    Google Scholar 

  122. Schlesselman JJ, Stadel BV, Murray P, Lai S: Breast cancer risk in relation to type of estrogen contained in oral contraceptives. Contraception 36: 595–613, 1987

    Article  PubMed  Google Scholar 

  123. Skegg DCG: Potential for bias in case-control studies of oral contraceptives and breast cancer. Am J Epidemiol 127: 205–212, 1988

    PubMed  Google Scholar 

  124. Myers JS: Cell proliferation in normal human ducts, fibroadenomas, and other ductal hyperplasias measured by nuclear labeling with tritiated thymidine: effect of menstrual phase, age, and oral contraceptive hormones. Human Pathology 8: 67–81, 1987

    Google Scholar 

  125. Hirohata T, Nomura AMY, Hankin JH, Kolonel LN, Lee J: An epidemiological study on the association between diet and breast cancer. JNCI 78: 595–600, 1987

    PubMed  Google Scholar 

  126. Malet C, Gompel A, Spritzer P, Kuttenn F, Mauvais-Jarvis P: Effect of estradiol and the synthetic progestin Promegestone (R5020) on the proliferation of human mammary cells in culture. Ann NY Acad Sci 464: 489–492, 1986

    Google Scholar 

  127. Thijssen JHH, Von Londeghem AJ, Poortman J: Uptake and concentration of steroid hormones in mammary tissues. Ann NY Acad Sci 464: 106–116, 1986

    PubMed  Google Scholar 

  128. Nagasawa H, Yanni R, Taniguchi M: Importance of mammary gland DNA synthesis in carcinogen-induced mammary tumorigenesis in rats. Cancer Res 36: 2225–2226, 1976

    Google Scholar 

  129. Russo J, Saby J, Isenberg WM, Russo IH: Pathogenesis of mammary carcinomas induced in rats by 7,12-dimethylben[a]anthracene. JNCI 59: 435–445, 1977

    Google Scholar 

  130. Russo IH, Russo J: Developmental stage of the rat mammary gland as determinant of its susceptibility to 7,12-dimethylbenz[a]anthracene. JNCI 61: 1439–1449, 1978

    PubMed  Google Scholar 

  131. Russo J, Russo IH: DNA labeling index and structure of the rat mammary gland as determinant of its susceptibility to carcinogenesis. JNCI 61: 1451–1459, 1978

    PubMed  Google Scholar 

  132. Russo J, Wilgood G, Russo IH: Susceptibility of the mammary gland to carcinogenesis. I. Differentiation of the mammary gland as determinant of tumor incidence and type of lesion. Am J Pathology 96: 721–733, 1979

    Google Scholar 

  133. Russo J, Russo IH: Susceptibility of the mammary gland to carcinogenesis. II. Pregnancy interruption as a risk factor in tumor incidence. Am J Pathology 100: 497–508, 1980

    Google Scholar 

  134. Russo J, Russo IH: Influence of differentiation and cell kinetics on the susceptibility of the rat mammary gland to carcinogenesis. Cancer Res 40: 2677–2687, 1980

    PubMed  Google Scholar 

  135. Dao TL, Back FG, Greiner JM: Mammary carcinogenesis by 3-methylcholanthracene. II. Inhibitory effect of pregnancy and lactation on tumor induction. JNCI 25: 991–1002, 1960

    PubMed  Google Scholar 

  136. Davies JE, Edmundson WF, Raffonelli A, Cassady JC, Morgade C: The role of social class in human pesticide pollution. Am J Epidemiol 96: 334–341, 1972

    PubMed  Google Scholar 

  137. Finklea J, Priester LE, Creason JP, Hauser T, Hinners T, Hammers DI: Polychlorinated biphenyl residues in human plasma expose a major urban pollution problem. Am J Public Health 62: 645–651, 1972

    PubMed  Google Scholar 

  138. American Cancer Society: Cancer in the economically disadvantaged. American Cancer Society, New York, 1986

    Google Scholar 

  139. Pollack S, Grozuczak J: Reagan, toxics and minorities. Urban Environment Conference, Washington DC, 1984

  140. Robinson JC: Racial inequality and the probability of occupation-related injury or illness. Milbank Memorial Fund Quarterly 62: 567–590, 1984

    Google Scholar 

  141. Lee C: Toxic wastes and race in the United States: a national report on the racial and social economic characteristics of communities with hazardous waste sites. United Church of Christ, New York, 1987

    Google Scholar 

  142. U.S. Dept. of Health and Human Services: Report of the Secretary's task force on black and minority health, vol. 1: Executive summary. [1985 0-487-673 (WL3)]. U.S. Government Printing Office, Washington DC, 1985

    Google Scholar 

  143. U.S. Dept. of Health and Human Services: Health status of minorities and low income groups. DHHS Pub. No. (HRSA) HRS-P-DV 85-1. U.S. Government Printing Office, Washington DC, 1985

    Google Scholar 

  144. Farley R: The quality of life for Black Americans twenty years after the civil rights revolution. Milbank Memorial Fund Quarterly 65 (Suppl 1): 9–34, 1987

    Google Scholar 

  145. Henshaw SK: Induced abortions: a worldwide perspective. Fam Plan Perspectives 18: 250–254, 1986

    Google Scholar 

  146. Potts M, Diggory P, Peel J: Abortion. Cambridge University Press, Cambridge, 1977

    Google Scholar 

  147. Epstein SS, Swartz JB: Fallacies of lifestyle cancer theories. Nature 289: 127–130, 1981

    Article  PubMed  Google Scholar 

  148. Beer AE, Billingham RE: Adipose tissue: a neglected factor in the aetiology of breast cancer? Lancet ii: 296, 1978

    Article  Google Scholar 

  149. Robinson WS: Ecological correlations and the behavior of individuals. Am Sociol Rev 15: 351–357, 1950

    Google Scholar 

  150. Alker HR Jr: A typology of ecologic fallacies. In: Doggan M, Rokkan S (eds) Social Ecology. MIT Press, Cambridge MA, 1969, pp 69–86

    Google Scholar 

  151. Stavraky KM: The role of ecologic analysis in studies of the etiology of disease: a discussion with reference to large bowel cancer. J Chron Dis 29: 435–444, 1976

    Article  PubMed  Google Scholar 

  152. Morgenstern H: Uses of ecologic analysis in epidemiologic research. Am J Public Health 72:1336–1344, 1982

    PubMed  Google Scholar 

  153. Selvin S: Two issues concerning the analysis of grouped data. Eur J Epidemiol 3: 284–287, 1987

    Article  PubMed  Google Scholar 

  154. Piantadosi S, Byar DP, Green SB: The ecological fallacy. Am J Epidemiol 127: 893–904, 1988

    PubMed  Google Scholar 

  155. Davis GA, Donaldson OF: Blacks in the United States: a geographic perspective. Houghton Mifflin, Boston MA, 1975

    Google Scholar 

  156. Jones J: Labor of Love, Labor of Sorrow: Black Women, Work and the Family from Slavery to the Present. Basic Books, New York, 1985

    Google Scholar 

  157. Rassin DK, Richardson CJ, Daranowski T, Nader TR, Guenther N, Bee DE, Brown JP: Incidence of breast feeding in a low socioeconomic group of mothers in the United States: ethnic patterns. Pediatrics 73: 132–137, 1984

    PubMed  Google Scholar 

  158. Young S, Kaufman M: Promoting breastfeeding in a migrant health center. Am J Public Health 78: 523–525, 1988

    PubMed  Google Scholar 

  159. Gebhard PH, Pomeroy WB, Martin CE, Christenson CV: Pregnancy birth and abortion. Harper & Bros., New York, 1958

    Google Scholar 

  160. Calderone MS: Abortion in the United States. Hoeber-Harper Books, New York, 1958

    Google Scholar 

  161. Henshaw SK, O'Reilly K: Characteristics of abortion patients in the United States, 1979 and 1980. Fam Plan Perspectives 15: 5–16, 1983

    Google Scholar 

  162. Henshaw SK, Binkin NH, Blaine E, Smith JC: A portrait of American women who obtain abortions. Fam Plan Perspectives 17: 90–96, 1985

    Google Scholar 

  163. Centers for Disease Control: Hysterectomy among women of reproductive age, United States, update for 1981–1982. In: CDC Surveillance Summaries 33 (No. 3SS), 1984, pp 1SS-6SS

    Google Scholar 

  164. Rose G: Sick individuals and sick populations. Int J Epidemiol 14: 32–38, 1985

    PubMed  Google Scholar 

  165. National Center for Health Statistics: Plan and operation of the Second National Health and Nutrition Examination Survey, 1976–1980. Vital and Health Statistics, Series 1, No. 15, DHHS Pub No. (PHS) 81-1317. U.S. Government Printing Office, Washington DC, 1981

    Google Scholar 

  166. Kannel WB, Castelli WP, McNamara P: Cigarette smoking and risk of coronary heart disease: epidemiologic clues to pathogenesis — The Framingham Study. National Cancer Institute Monograph No. 28. National Cancer Institute, Bethesda MD, 1968

    Google Scholar 

  167. Cairns J: The treatment of diseases and the war against cancer. Sci Am 253: 51–59, 1985

    PubMed  Google Scholar 

  168. Bailar JC III, Smith EM: Progress against cancer? N Engl J Med 314: 1226–1232, 1986

    PubMed  Google Scholar 

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  1. Epidemiology Program, Haviland 101, Dept. of Biomedical and Environmental Health Sciences, School of Public Health, University of California at Berkeley, 94720, Berkeley, CA, USA

    Nancy Krieger

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Krieger, N. Exposure, susceptibility, and breast cancer risk: A hypothesis regarding exogenous carcinogens, breast tissue development, and social gradients, including black/white differences, in breast cancer incidence. Breast Cancer Res Tr 13, 205–223 (1989). https://doi.org/10.1007/BF02106571

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Key words

  • abortion
  • breast neoplasms
  • race
  • risk factors
  • social class
  • susceptibility to carcinogens