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Epidemiology of Endocrine-Related Risk Factors for Breast Cancer

  • Leslie Bernstein
Article

Abstract

Ovarian and other hormones are major determinants of breast cancer risk. Particularly important is the accumulative exposure of the breast to circulating levels of the ovarian hormones estradiol and progesterone. A number of breast cancer risk factors can be understood in light of how they affect women's hormone profiles. Age is a marker for the onset and cessation of ovarian activity. Racial differences in hormone profiles correlate with breast cancer incidence patterns. Age at menarche not only serves as the chronological indicator of the onset of ovarian activity, but as a predictor of ovulatory frequency during adolescence and hormone levels in young adults, and has a long-lasting influence on risk. Age at menopause, another established breast cancer risk factor, marks the cessation of ovarian activity. Pregnancy history and lactation experience also are hormonal markers of breast cancer risk. Postmenopausal obesity, which is associated with higher levels of estrogen following cessation of ovarian activity, increases breast cancer risk, whereas physical activity, which can limit menstrual function, reduces risk. A relatively recent area of investigation is prenatal exposures like preeclampsia and low birth weight; both may be associated with lower in utero exposure to estrogen and also may predict lower breast cancer risk as an adult. Improved understanding of these exposures and their potential interactions with breast cancer susceptibility genes may, in the future, improve our prospects for breast cancer prevention.

breast cancer risk factors ovarian hormones incidence 

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REFERENCES

  1. 1.
    D.M. Parkin, S.L. Whelan, J. Ferlay, L. Raymond, and J. E. Young (eds.) (1997). Cancer Incidence in Five Continents, Vol.7, IARCScientific Publications No. 143, International Agency forResearch on Cancer, Lyon, France.Google Scholar
  2. 2.
    C.C. Boring, T.S. Squires, and T. Tong (1993). Cancer Statistics 1993. CA: Cancer J.Clin. 43: 7–26.Google Scholar
  3. 3.
    B.E. Henderson and H.S. Feigelson (2000). Hormonal carcino-genesis. Carcinogenesis 21: 427–433.PubMedGoogle Scholar
  4. 4.
    J. Waterhouse, C. Muir, K. Shanmugaratnam, and J.E. Powell(1982). Cancer Incidence in Five Continents, Vol. 4, IARC ScientificPublications No. 42, International Agency for Researchon Cancer, Lyon, France.Google Scholar
  5. 5.
    D.M. Parkin, C.S. Muir, S.L. Whelan, Y.T. Gao, J. Ferlay,and J. Powell (eds.) (1992). Cancer Incidence in Five Continents, IARCScientific Publications No. 120, International Agency forResearch on Cancer, Lyon, France.Google Scholar
  6. 6.
    B.A. Miller, L.N. Kolonel, L. Bernstein, J.L. Young Jr, G.M. Swanson, D. West, C.R. Key, J.M. Liff, C.S. Glover, and G.A. Alexander (eds.) (1996). Racial/Ethnic Patterns of Cancerin the United States 1988–1992I, NIH Pub. No. 96–4104, NationalCancer Institute, Bethesda, MD.Google Scholar
  7. 7.
    L. A.G. Ries, M.P. Eisner, C.L. Kosary, B.F. Hankey,B.A. Miller, L. Clegg, and B.K. Edwards (eds.) (2001). SEERCancer Statistics Review, 1973–1998, National Cancer Institute,Bethesda, MD.Google Scholar
  8. 8.
    S. Preston-Martin, M.C. Pike, R.K. Ross, P.A. Jones, and B.E. Henderson (1990). Increased cell division as a cause of humancancer. Cancer Res. 50: 7415–7421.PubMedGoogle Scholar
  9. 9.
    I.A. Mustafa and K.I. Bland (1998). Physiologic effects ofsteroid hormones and postmenopausal hormone replacement on the female breast and breast cancer risk. Ann.Surg. 228: 638–651.PubMedGoogle Scholar
  10. 10.
    B.E. Henderson, R.K. Ross, H.L. Judd, M.D. Krailo, and M.C. Pike (1985). Do regular ovulatory cycles increase breastcancer risk? Cancer 56: 1206–1208.PubMedGoogle Scholar
  11. 11.
    U. Goebelsmann and D. Mishell (1979). The menstrual cycle. In D. Mishell and V. Davajan (eds.), Reproductive Endocrinology,Infertility and Contraception, FA Davis, Philadelphia, PA, pp. 67–89.Google Scholar
  12. 12.
    M.C. Pike, D.V. Spicer, L. Dahmoush, and M.F. Press (1993). Estrogens, progestogens, normal breast cell proliferation, andbreast cancer risk. Epidemiol.Rev. 15: 17–35.PubMedGoogle Scholar
  13. 13.
    L. Bernstein and R.K. Ross (1993). Hormones and breast cancer. Epidemiol.Rev. 15: 48–65.PubMedGoogle Scholar
  14. 14.
    T. Key (1999). Serum estradiol and breast cancer risk. Endocrine-Rel.Cancer 6: 175–180.Google Scholar
  15. 15.
    H.V. Thomas, G.K. Reeves, and T.J. Key (1997). Endogenousestrogen and postmenopausal breast cancer: Aquantitative review. Cancer Causes Control 8: 922–928.PubMedGoogle Scholar
  16. 16.
    S.E. Hankinson, W.C. Willett, J.E. Manson, G.A. Colditz, D.A. Hunter, D. Spiegelman, R.L. Barbieri, and F.E. Speizer(1998). Plasma sex steroid hormone levels and risk of breastcancer in postmenopausal women. J.Natl.Cancer Inst. 90: 1292–1299.PubMedGoogle Scholar
  17. 17.
    T. Zeginiadou, A.H. Kortsaris, S. Koliais, and O. Antonoglou(1998). Sex hormone binding globulin inhibits strongly the up-takeof estradiol by human breast carcinoma cells via a depri-vativemechanism. Cancer Biochem.Biophys. 16: 253–263.PubMedGoogle Scholar
  18. 18.
    J.F. Dorgan, C. Longcope, H.E. Stephenson, R.T. Falk,R. Miller, C. Franz, L. Kahle, W.S. Campbell, J.A. Tantrea, and A. Schatzkin (1996). Relation of prediagnostic serum estrogenand androgen levels to breast cancer risk. Cancer EpidemiolBiomark.Prev. 5: 533–539.Google Scholar
  19. 19.
    D.C. Anderson (1974). Sex-hormone-binding globulin. Clin.Endocrinol. 3: 69–96.Google Scholar
  20. 20.
    L.E. Nachtigall, U. Raju, S. Banerjee, L. Wan, and M. Levitz(2000). Serum estradiol-binding profiles in postmenopausalwomen undergoing three common estrogen replacement ther-apies:Associations with sex hormone-binding globulin, estra-diol,and estrone levels. Menopause 7: 243–250.PubMedGoogle Scholar
  21. 21.
    E.S. Knochenhauer, L.R. Boots, H.D. Potter, and R. Azziz(1998). Differential binding of estradiol and testosterone toSHBG. Relation to circulating estradiol levels. J.Reprod.Med. 43:665–670.PubMedGoogle Scholar
  22. 22.
    J.M. Cline, G. Soderqvist, E. von Schoultz, L. Skoog, and B. von Schoultz (1996). Effects of hormone replacement therapy onthe mammary gland of surgically postmenopausal macaques. Am.J.Obstet.Gynecol. 174: 93–100.PubMedGoogle Scholar
  23. 23.
    C. Schairer, C. Byrne, P.M. Keyl, L.A. Brinton, S.R. Sturgeon, and R.N. Hoover (1994). Menopausal estrogen and estrogen–progestin replacement therapy and risk of breast cancer (United States). Cancer Causes Control 5: 491–500.PubMedGoogle Scholar
  24. 24.
    R.K. Ross, A. Paganini-Hill, P.C. Wan, and M.C. Pike (2000). Effect of hormone replacement therapy on breast cancer risk:Estrogen versus estrogen plus progestin. J.Natl.Cancer Ins. 92: 328–332.Google Scholar
  25. 25.
    J.M. Grodin, P.K. Siiteri, and P.C. MacDonald (1973). Sourceof estrogen prouction in postmenopausal women. J.Clin.En-docrinol.Metab. 36: 207–214.Google Scholar
  26. 26.
    M.Lippman, G. Bolan, and K. Huff (1976). The effects of andro-gensand antiandrogens on hormone-responsive human breastcancer in long-term tissue culture. Cancer Res. 36: 4610–4618.PubMedGoogle Scholar
  27. 27.
    P. Hill, L. Garbaczewski, and F. Kasumi (1985). Plasma testos-teroneand breast cancer. Eur.J.Clin.Oncol. 21: 1265–1266.Google Scholar
  28. 28.
    B.R. Goldin, H. Adlercreutz, S.L. Gorbach, M.N. Woods, J.T. Dwyer, T. Conlon, E. Bohn, and S.N. Gershoff (1986). Therelationship between estrogen levels and diets of CaucasianAmerican and Oriental immigrant women. Am.J.Clin.Nutr. 44: 945–953.PubMedGoogle Scholar
  29. 29.
    T. J.A. Key, J. Chen, D.Y. Wang, M.C. Pike, and J. Boreham(1990). Sex hormones in women in rural China and in Britain. Br.J.Cancer 62: 631–636.PubMedGoogle Scholar
  30. 30.
    H. Shimizu, R.K. Ross, L. Bernstein, M.C. Pike, and B.E. Henderson (1990). Serum estrogen levels in postmenopausalwomen: Comparison of US whites and Japanese in Japan. Br.J.Cancer 62: 451-4.PubMedGoogle Scholar
  31. 31.
    D.K. Wysowski, G.W. Comstock, K.J. Helsing, and H. L. Lau (1987). Sex hormone levels in serum in relation to thedevelopment of breast cancer. Am.J.Epidemiol. 125: 791–799.PubMedGoogle Scholar
  32. 32.
    K.J. Helzlsouer, A.J. Alberg, T.L. Bush, C. Longcope, G.B. Gordon, and G.W. Comstock (1994). A prospective study of endogenous hormones and breast cancer. Cancer Detect.Prev. 18: 79–85.PubMedGoogle Scholar
  33. 33.
    P. Ebeling and V.A. Koivisto (1994). Physiological importanceof dehydroepiandrosterone. Lancet 343: 1479–1481.PubMedGoogle Scholar
  34. 34.
    A.G. Schwartz (1979). Inhibition of spontaneous breast cancerformation in female C3H (Avy/a) mice by long-term treatmentwith dehydroepiandrosterone. Cancer Res. 39: 1129–1132.PubMedGoogle Scholar
  35. 35.
    J. H.H. Thijssen, J. Poortman, and F. Schwarz (1975). Andro-gensin postmenopausal breast cancer: Excretion, productionand interaction with estrogens. J.Steroid Biochem. 6: 729–734.PubMedGoogle Scholar
  36. 36.
    B.K. Vonderhaar (1987). Prolactin transport, function, and re-ceptorsin mammary gland development and differentiation.In M. Neville and C. Daniels (eds.), The Mammary GlandDevelopment, Regulation and Function, Plenum, New York, pp. 383–438.Google Scholar
  37. 37.
    B.K. Vonderhaar (1999). Prolactin involvement in breastcancer. Endocrine-Rel.Cancer 6: 389–404.Google Scholar
  38. 38.
    C.W. Welsch and H. Nagasawa (1977). Prolactin and murinemammary tumorigenesis: A review. Cancer Res. 37: 951–963.PubMedGoogle Scholar
  39. 39.
    S.E. Hankinson, W.C. Willett, D.S. Michaud, J.E. Manson, G.A. Colditz, C. Longcope, B. Rosner, and F.E. Speizer (1999). Plasma prolactin levels and subsequent risk of breast cancer inpostmenopausal women. J.Natl.Cancer Inst. 91: 629–634.PubMedGoogle Scholar
  40. 40.
    B.E. Henderson, M.C. Pike, L. Bernstein, and R.K. Ross(1996). Breast cancer. In D. Schottenfeld and J. Fraumeni Jr. (eds.), Cancer Epidemiology and Prevention, 2nd edn., W.B. Saunders, New York, pp. 1022–1039.Google Scholar
  41. 41.
    B.E. Henderson, M.C. Pike, and J.T. Casagrande (1981). Breastcancer and the oestrogen window hypothesis. Lancet 2: 363–364.Google Scholar
  42. 42.
    D. Apter and R. Vihko (1983). Early menarche, a risk factor forbreast cancer, indicates early onset of ovulatory cycles. J.Clin.Endocrinol.Metab. 57: 82–86.PubMedGoogle Scholar
  43. 43.
    R. Vihko and D.J. Apter (1984). Endocrine characteristics ofadolescent menstrual cycles: Impact of early menarche. SteroidBiochem. 20: 231–236.Google Scholar
  44. 44.
    D. Apter, M. Reinila, and R. Vihko (1989). Some endocrinecharacteristics of early menarche, a risk factor for breast cancerare preserved into adulthood. In t.J.Cancer 44: 783–787.Google Scholar
  45. 45.
    D. Trichopoulos, B. MacMahon, and P. Cole (1972). Themenopause and breast cancer risk. J.Natl.Cancer Inst. 48: 605–613.PubMedGoogle Scholar
  46. 46.
    L.A. Brinton, C. Schairer, R.N. Hoover, and J.F. Fraumeni(1988). Menstrual factors and risk of breast cancer. Cancer Investig. 6: 245–254.Google Scholar
  47. 47.
    B. MacMahon, P. Cole, M.T. Lin, C.R. Lowe, A.P. Mirra,B. Ravnihar, E.J. Salber, V.G. Valaoras, and S. Yuasa (1970). Age at first birth and cancer of the breast. A summary of aninternational study. Bull.W.H.O. 43: 209–221.PubMedGoogle Scholar
  48. 48.
    J.M. Yuan, M.C. Yu, R.K. Ross, Y.T. Gao, and B.E. Henderson(1988). Risk factors for breast cancer in Chinese women inShanghai. Cancer Res. 48: 1949–1953.PubMedGoogle Scholar
  49. 49.
    P. Bruzzi, E. Negri, C. La Vecchia, A. Decarli, D. Palli, F. Parazzini, and M.R. Del Turco (1988). Short term increasein risk of breast cancer after full term pregnancy. Br.Med.J. 297: 1096–1098.Google Scholar
  50. 50.
    L. Bernstein, R.H. Depue, R.K. Ross, H.L. Judd, M.C. Pike,and B.E. Henderson (1986). Higher maternal levels of freeestradiol in first compared to second pregnancy: A study ofearly gestational differences. J.Natl.Cancer Inst. 75: 1035–1039.Google Scholar
  51. 51.
    S.M. Enger, R.K. Ross, H. B. E, and L. Bernstein (1997). Breastfeeding history, pregnancy experience and risk of breast cancer. Br.J.Cancer 76: 118–123.PubMedGoogle Scholar
  52. 52.
    R.H. Depue, L. Bernstein, R.K. Ross, H.L. Judd, M.C. Pike,and B.E. Henderson (1987). Hyperemesis gravidarum in rela-tionto estradiol levels, pregnancy outcome, and other maternal. factors: A sero-epidemiologic study. Am.J.Obstet.Gynecol. 156: 1137–1141.PubMedGoogle Scholar
  53. 53.
    L. Bernstein, M.C. Pike, R.K. Ross, H.L. Judd, J.B. Brown, and B.E. Henderson (1985). Estrogen and sex hormone-bindingglobulin levels in nulliparous and parous women. J.Natl.CancerInst. 74: 741–745.Google Scholar
  54. 54.
    V.C. Musey, D.C. Collins, P.I. Musey, D. Martino-Saltzman,and J.R. Preedy (1987). Long-term effect of a first preg-nancyon the secretion of prolactin. New Engl.J.Med. 316: 229–234.PubMedGoogle Scholar
  55. 55.
    D.Y. Wang, B. L. de Stavola, R.D. Bulbrook, D.S. Allen, H.G. Kwa, A.A. Verstraeten, J.W. Moore, I.S. Fentiman, J.L. Hayward, and I.H. Gravelle (1988). The permanent effect ofreproductive events on blood prolactin levels and its relationto breast cancer risk: A population study of postmenopausalwomen. Eur.J.Cancer Clin.Oncol. 24: 1225–1231.PubMedGoogle Scholar
  56. 56.
    J.W. Moore, T. J.A. Key, R.D. Bulbrook, G.M. Clark,D.S. Allen, D.Y. Wang, and M.C. Pike (1987). Sex hormonebinding globulin and risk factors for breast cancer in a popu-lationof normal women who had never used exogenous sexhormones. Br.J.Cancer 56: 661–666.PubMedGoogle Scholar
  57. 57.
    P.A. Wingo, K. Newsome, J.S. Marks, E.E. Calle, and S.L. Parker (1997). The risk of breast cancer following sponta-neousand induced abortion. Cancer Causes Control 8: 93–108.PubMedGoogle Scholar
  58. 58.
    P.A. Newcomb, B.E. Storer, M.P. Longnecker, R. Mittendorf,E.R. Greenberg, R.W. Clapp, K.P. Burke, W.C. Willett, and B. MacMahon (1994). Lactation and a reduced risk of pre-menopausalbreast cancer. New Engl.J.Med. 330: 81–86.PubMedGoogle Scholar
  59. 59.
    S.M. Enger, R.K. Ross, A. Paganini-Hill, and L. Bernstein(1998). Breastfeeding experience and breast cancer risk amongpostmenopausal women. Cancer Epidemiol.Biomark.Prev. 7: 365–369.Google Scholar
  60. 60.
    D.J. Hunter and W.C. Willett (1993). Diet, body size, and breastcancer. Epidemiol.Rev. 15: 110–132.PubMedGoogle Scholar
  61. 61.
    Z. Huang, S.E. Hankinson, G.A. Colditz, M.J. Stampfer,D.J. Hunter, J.E. Manson, C.H. Hennekens, B. Rosner,F.E. Speizer, and W.C. Willett (1997). Dual effects of weightand weight gain on breast cancer risk. J.Am.Med.Assoc. 278: 1407–1411.Google Scholar
  62. 62.
    P.K. Siiteri and P.C. MacDonald (1973). Role of extraglan-dularestrogen in human endocrinology. In S.R. Geiger, E.B. Astwood, and R.O. Greep (eds.), Handbook of Physiology, American Physiological Society, Washington, DC, pp. 615–629.Google Scholar
  63. 63.
    T. J.A. Key and M.C. Pike (1988a). The dose–effect relationship between “unopposed” oestrogens and endometrial mitoticrate: Its central role in explaining and predicting endometrial cancer risk. Br.J.Cancer 57: 205–212.PubMedGoogle Scholar
  64. 64.
    G. Ursin, M.P. Longnecker, R.W. Haile, and S. Greenland(1995). A meta-analysis of body mass index and risk of pre-menopausalbreast cancer. Epidemiology 6: 137–141.PubMedGoogle Scholar
  65. 65.
    M.C. Pike (1990). Reducing cancer risk in women throughlifestyle-mediated changes in hormone levels. Cancer Detect.Prev. 14: 595–607.PubMedGoogle Scholar
  66. 66.
    L. Bernstein and B.E. Henderson (1996). Exogenous hormones. In D. Schottenfeld and J. Fraumeni Jr. (eds.), Cancer Epidemiology and Prevention, 2nd edn., W.B. Saunders, New York, pp. 462–488.Google Scholar
  67. 67.
    L. Bernstein, M.C. Pike, M. Krailo, and B.E. Henderson (1990). Update of the Los Angeles study of oral contraceptives andbreast cancer: 1981 and 1983. In R. Mann (ed.), Oral Contra-ceptivesand Breast Cancer, Parthenon, Park Ridge, NJ, pp. 169–180.Google Scholar
  68. 68.
    G. Ursin, R.K. Ross, J. Sullivan-Halley, R. Hanisch, B.E. Henderson, and L. Bernstein (1998). Use of oral contracep-tivesand risk of breast cancer in young women. Breast CancerRes.Treat. 50: 175–184.Google Scholar
  69. 69.
    Collaborative Group on Hormonal Factors in Breast Cancer. (1996a). Breast cancer and hormonal contraceptives. Lancet 347: 1713–1727.Google Scholar
  70. 70.
    Collaborative Group on Hormonal Factors in Breast Cancer. (1996b). Breast cancer and hormonal contraceptives: Furtherresults. Contraception S 54: 1–106.Google Scholar
  71. 71.
    J.L. Stanford and D.B. Thomas (1993). Exogenous progestinsand breast cancer. Epidemiol.Rev. 15: 98–107.PubMedGoogle Scholar
  72. 72.
    M.C. Pike, L. Bernstein, and D.V. Spicer (1993). The re-lationshipof exogenous hormones to breast cancer risk. In J. Niederhuber (ed.), Current Therapy in Oncology, Mosby, St. Louis, MO, pp. 292–303.Google Scholar
  73. 73.
    T.J. Key and M.C. Pike (1988b). The role of oestrogens and pro-gestagensin the epidemiology and prevention of breast cancer. Eur.J.Cancer Clin.Oncol. 13: 29–43.Google Scholar
  74. 74.
    C. Magnusson, J.A. Baron, N. Correia, R. Bergstrom,H.O. Adami, and I. Persson (1999). Breast-cancer risk follow-inglong-term oestrogen-and oestrogen-progestin-replacementtherapy. In t.J.Cancer 81: 339–344.Google Scholar
  75. 75.
    C. Schairer, J. Lubin, R. Troisi, S. Sturgeon, L. Brinton, and R. Hoover (2000). Menopausal estrogen and estrogen–progestin replacement therapy and breast cancer risk. J.Am.Med.Assoc. 283: 485–491.Google Scholar
  76. 76.
    R.E. Frisch, A.V. Gotz-Welbergen, J.W. McArthur,T. Albright, J. Witschi, B. Bullen, J. Birnholz, and R.B. Reed(1981). Delayed menarche and amenorrhea of college athletesin relation to age of onset of training. J.Am.Med.Assoc. 246: 1559–1563.Google Scholar
  77. 77.
    B. Schwartz, D.C. Cumming, E. Riordan, M. Selye, S.S. Yen,and R.W. Rebar (1981). Exercise-associated amenorrhea: Adistinct entity? Am.J.Obstet.Gynecol. 141: 662–670.PubMedGoogle Scholar
  78. 78.
    M.M. Shangold and H.A. Levine (1982). The effect ofmarathon training upon menstrual function. Am.J.Obstet.Gynecol. 143: 862–869.PubMedGoogle Scholar
  79. 79.
    M.M. Shangold (1985). Exercise and amenorrhea. Sem.Re-prod Endocrinol. 3: 35–43.Google Scholar
  80. 80.
    E. Dale, D. Gerlach, and A.L. Wilhite (1979). Menstrual dys-functionin distance runners. Obstet.Gynecol. 54: 47–53.PubMedGoogle Scholar
  81. 81.
    K.M. Pirke, U. Schweiger, A. Broocks, R.J. Tuschl, and R.G. Laessle (1990). Luteinizing hormone and follicle stim-ulatinghormone secretion patterns in female athletes withand without menstrual disturbances. Clin.Endocrinol. 33: 345–353.Google Scholar
  82. 82.
    A. Broocks, K.M. Pirke, U. Schweiger, R.J. Tuschl,R.G. Laessle, T. Strowitzki, E. Horl, T. Horl, W. Haas, and D. Jeschke (1990). Cyclic ovarian function in recreational ath-letes. J.Appl.Physiol. 68: 2083–2086.PubMedGoogle Scholar
  83. 83.
    J.C. Prior, Y.M. Vigna, M.T. Schechter, and A.E. Burgess(1990). Spinal bone loss and ovulatory disturbances. New Engl.J.Med. 323: 1221–1227.PubMedGoogle Scholar
  84. 84.
    L. Bernstein, R.K. Ross, R.A. Lobo, R. Hanisch, M.D. Krailo,and B.E. Henderson (1987). The effects of moderate physicalactivity on menstrual cycle patterns in adolescence: Implica-tionsfor breast cancer prevention. Br.J.Cancer 55: 681–685.PubMedGoogle Scholar
  85. 85.
    J.B. Russell, D. Mitchell, P.I. Musey, and D.C. Collins (1984). The relationship of exercise to anovulatory cycles in female ath-letes:Hormonal and physical characteristics. Obstet.Gynecol. 63: 452–456.PubMedGoogle Scholar
  86. 86.
    C.M. Friedenreich and T.E. Rohan (1995). Areview of physicalactivity and breast cancer. Epidemiology 6: 311–317.PubMedGoogle Scholar
  87. 87.
    A. McTiernan, C. Ulrich, S. Slate, and J. Potter (1998). Physi-calactivity and cancer etiology: Associations and mechanisms. Cancer Causes Control 9: 487–509.PubMedGoogle Scholar
  88. 88.
    L. Bernstein, B.E. Henderson, R. Hanisch, J. Sullivan-Halley,and R.K. Ross (1994). Physical exercise and reduced risk ofbreast cancer in young women. J.Natl.Cancer Inst. 86: 1403–1408.PubMedGoogle Scholar
  89. 89.
    C.L. Carpenter, R.K. Ross, A. Paganini-Hill, and L. Bernstein(1999). Lifetime exercise activity and breast cancer risk amongpost-menopausal women. Br.J.Cancer 80: 1852–1858.PubMedGoogle Scholar
  90. 90.
    G. Jasienska, I. Thune, and P.T. Ellison (2000). Energeticfactors, ovarian steroids and the risk of breast cancer. Eur.J.Cancer Prev. 9: 231–239.PubMedGoogle Scholar
  91. 91.
    J. Russo and I.H. Russo (1987). Development of the human mammary gland. In M. Neville and C. Daniel (eds.), The Mam-maryGland, Plenum, New York, pp. 67–93.Google Scholar
  92. 92.
    D. Trichopoulos (1990). Hypothesis: Does breast cancer origi-natein utero? Lancet 335: 939–940.PubMedGoogle Scholar
  93. 93.
    R. Anbazhagan and B.A. Gusterson (1994). Prenatal factorsmay influence predisposition to breast cancer. Eur.J.Cancer A 30: 1–3.Google Scholar
  94. 94.
    E. Petridou, K. Panagiotopoulou, K. Katsouyanni, E. Spanos,and D. Trichopoulos (1990). Tobacco smoking, pregnancy estrogens,and birth weight. Epidemiology 1: 247–250.PubMedGoogle Scholar
  95. 95.
    A. Ekbom, D. Trichopoulos, H.O. Adami, C.C. Hsieh, and S.J. Lan (1992). Evidence of prenatal influences on breastcancer risk. Lancet 340: 1015–1018.PubMedGoogle Scholar
  96. 96.
    K.B. Michels, D. Trichopoulos, J.B. Robins, B.A. Rosner,J.E. Manson, D.J. Hunter, G.A. Colditz, S.E. Hankinson,F.E. Speizer, and W.C. Willett (1996). Birthweight as a riskfactor for breast cancer. Lancet 348: 1542–1546.PubMedGoogle Scholar
  97. 97.
    A. Ekbom, C.C. Hsieh, L. Lipworth, H.O. Adami, and D. Trichopoulos (1997). Intrauterine environment and breastcancer risk in women: Apopulation-based study. J.Natl.CancerInst. 89: 71–76.Google Scholar
  98. 98.
    A. Shibata and A.Y. Minn (2000). Perinatal sex hormones and risk of breast and prostate cancers in adulthood. Epidemiol.Rev. 22: 239–248.PubMedGoogle Scholar

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© Plenum Publishing Corporation 2002

Authors and Affiliations

  • Leslie Bernstein
    • 1
  1. 1.Department of Preventive MedicineKeck School of Medicine of the University of Southern CaliforniaLos Angeles

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