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Breast cancer risk accumulation starts early: prevention must also

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Abstract

Nearly one in four breast cancers is diagnosed before the age of 50, and many early-stage premalignant lesions are present but not yet diagnosed. Therefore, we review evidence to support the strategy that breast cancer prevention efforts must begin early in life. This study follows the literature review methods and format. Exposures during childhood and adolescence affect a woman’s long-term risk of breast cancer, but have received far less research attention than exposures that occur later in life. Breast tissue undergoes rapid cellular proliferation between menarche and first full-term pregnancy, and risk accumulates rapidly until the terminal differentiation that accompanies first pregnancy. Evidence on childhood diet and growth in height, and adolescent alcohol intake, among other adolescent factors is related to breast cancer risk and risk of premalignant proliferative benign lesions. Breast cancer prevention efforts will have the greatest effect when initiated at an early age and continued over a lifetime. Gaps in knowledge are identified and deserve increase attention to inform prevention.

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References

  1. Brinton LA, Sherman ME, Carreon JD, Anderson WF (2008) Recent trends in breast cancer among younger women in the United States. J Natl Cancer Inst 100(22):1643–1648. doi:10.1093/jnci/djn344

    Article  PubMed Central  PubMed  Google Scholar 

  2. Mahabir S, Aagaard K, Anderson LM, Herceg Z, Hiatt RA, Hoover RN, Linet MS, Medina D, Potischman N, Tretli S, Trichopoulos D, Troisi R (2012) Challenges and opportunities in research on early-life events/exposures and cancer development later in life. Cancer Causes Control 23(6):983–990. doi:10.1007/s10552-012-9962-5

    Article  PubMed  Google Scholar 

  3. London SJ, Connolly JL, Schnitt SJ, Colditz GA (1992) A prospective study of benign breast disease and the risk of breast cancer. JAMA 267(7):941–944

    Article  CAS  PubMed  Google Scholar 

  4. Weinberg RA (ed) (2007) Multi-step tumorigenesis. In: The biology of cancer. Garland Science, Taylor & Francis Group, LLC, pp 399–462

  5. Hartmann LC, Sellers TA, Frost MH, Lingle WL, Degnim AC, Ghosh K, Vierkant RA, Maloney SD, Pankratz VS, Hillman DW, Suman VJ, Johnson J, Blake C, Tlsty T, Vachon CM, Melton LJ 3rd, Visscher DW (2005) Benign breast disease and the risk of breast cancer. N Engl J Med 353(3):229–237

    Article  CAS  PubMed  Google Scholar 

  6. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61(2):69–90. doi:10.3322/caac.20107

    Article  PubMed  Google Scholar 

  7. SEER Cancer Statistics Review (1975–2010) (Based on November 2012 SEER data submission, posted to the SEER web site, 2013). National Cancer Institute, Bethesda, MD

  8. Ziegler RG, Hoover RN, Pike MC, Hildesheim A, Nomura AMY, West DW, Wu-Williams AH, Kolonel LN, Horn-Ross PL, Rosenthal JF, Hyer MB (1993) Migration patterns and breast cancer risk in Asian-American women. J Natl Cancer Inst 85:1819–1827

    Article  CAS  PubMed  Google Scholar 

  9. Althuis MD, Dozier JM, Anderson WF, Devesa SS, Brinton LA (2005) Global trends in breast cancer incidence and mortality 1973–1997. Int J Epidemiol 34(2):405–412. doi:10.1093/ije/dyh414

    Article  PubMed  Google Scholar 

  10. Jung YS, Na KY, Kim KS, Ahn SH, Lee SJ, Park HK, Cho YU (2011) Nation-wide Korean breast cancer data from 2008 using the breast cancer registration program. J Breast Cancer 14(3):229–236. doi:10.4048/jbc.2011.14.3.229

    Article  PubMed Central  PubMed  Google Scholar 

  11. Leung GM, Thach TQ, Lam TH, Hedley AJ, Foo W, Fielding R, Yip PS, Lau EM, Wong CM (2002) Trends in breast cancer incidence in Hong Kong between 1973 and 1999: an age-period-cohort analysis. Br J Cancer 87(9):982–988. doi:10.1038/sj.bjc.6600583

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Colditz G, Rosner B (2000) Cumulative risk of breast cancer to age 70 years according to risk factor status: data from the Nurses’ Health Study. Am J Epidemiol 152(10):950–964

    Article  CAS  PubMed  Google Scholar 

  13. Collaborative Group on Hormonal Factors in Breast Cancer (2001) Familial breast cancer: collaborative reanalysis of individual data from 52 epidemiological studies including 58, 209 women with breast cancer and 101, 986 women without the disease. Lancet 358(9291):1389–1399. doi:10.1016/S0140-6736(01)06524-2

    Article  Google Scholar 

  14. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans (2012) Personal habits and indoor combustions. Volume 100 E. A review of human carcinogens, vol 100. IARC Monogr Eval Carcinog Risks Hum, vol Pt E

  15. Land CE, Tokunaga M, Koyama K, Soda M, Preston DL, Nishimori I, Tokuoka S (2003) Incidence of female breast cancer among atomic bomb survivors, Hiroshima and Nagasaki, 1950–1990. Radiat Res 160(6):707–717

    Article  CAS  PubMed  Google Scholar 

  16. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, Johnson KC, Kotchen JM, Ockene J (2002) Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women’s Health Initiative randomized controlled trial. JAMA 288(3):321–333

    Article  CAS  PubMed  Google Scholar 

  17. Collaborative Group on Hormonal Factors in Breast Cancer (1996) Breast cancer and hormonal contraceptives: collaborative reanalysis of individual data on 53 297 women with breast cancer and 100 239 women without breast cancer from 54 epidemiological studies. Lancet 347(9017):1713–1727

    Article  Google Scholar 

  18. International Agency for Research on Cancer (2002) Weight control and physical activity, vol 6. IARC handbook on cancer prevention. International Agency for Research on Cancer, Lyon

    Google Scholar 

  19. Baer HJ, Tworoger SS, Hankinson SE, Willett WC (2010) Body fatness at young ages and risk of breast cancer throughout life. Am J Epidemiol 171(11):1183–1194. doi:10.1093/aje/kwq045

    Article  PubMed Central  PubMed  Google Scholar 

  20. Network Cancer Genome Atlas (2012) Comprehensive molecular portraits of human breast tumours. Nature 490(7418):61–70. doi:10.1038/nature11412

    Article  CAS  Google Scholar 

  21. Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge O, Pergamenschikov A, Williams C, Zhu SX, Lonning PE, Borresen-Dale AL, Brown PO, Botstein D (2000) Molecular portraits of human breast tumours. Nature 406(6797):747–752. doi:10.1038/35021093

    Article  CAS  PubMed  Google Scholar 

  22. Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van de Rijn M, Jeffrey SS, Thorsen T, Quist H, Matese JC, Brown PO, Botstein D, Lonning PE, Borresen-Dale AL (2001) Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 98(19):10869–10874. doi:10.1073/pnas.191367098

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Millikan RC, Newman B, Tse CK, Moorman PG, Conway K, Dressler LG, Smith LV, Labbok MH, Geradts J, Bensen JT, Jackson S, Nyante S, Livasy C, Carey L, Earp HS, Perou CM (2008) Epidemiology of basal-like breast cancer. Breast Cancer Res Treat 109(1):123–139. doi:10.1007/s10549-007-9632-6

    Article  PubMed Central  PubMed  Google Scholar 

  24. Tamimi RM, Colditz GA, Hazra A, Baer HJ, Hankinson SE, Rosner B, Marotti J, Connolly JL, Schnitt SJ, Collins LC (2011) Traditional breast cancer risk factors in relation to molecular subtypes of breast cancer. Breast Cancer Res Treat. doi:10.1007/s10549-011-1702-0

  25. Yang XR, Chang-Claude J, Goode EL, Couch FJ, Nevanlinna H, Milne RL, Gaudet M, Schmidt MK, Broeks A, Cox A, Fasching PA, Hein R, Spurdle AB, Blows F, Driver K, Flesch-Janys D, Heinz J, Sinn P, Vrieling A, Heikkinen T, Aittomaki K, Heikkila P, Blomqvist C, Lissowska J, Peplonska B, Chanock S, Figueroa J, Brinton L, Hall P, Czene K, Humphreys K, Darabi H, Liu J, Van ‘t Veer LJ, van Leeuwen FE, Andrulis IL, Glendon G, Knight JA, Mulligan AM, O’Malley FP, Weerasooriya N, John EM, Beckmann MW, Hartmann A, Weihbrecht SB, Wachter DL, Jud SM, Loehberg CR, Baglietto L, English DR, Giles GG, McLean CA, Severi G, Lambrechts D, Vandorpe T, Weltens C, Paridaens R, Smeets A, Neven P, Wildiers H, Wang X, Olson JE, Cafourek V, Fredericksen Z, Kosel M, Vachon C, Cramp HE, Connley D, Cross SS, Balasubramanian SP, Reed MW, Dork T, Bremer M, Meyer A, Karstens JH, Ay A, Park-Simon TW, Hillemanns P, Arias Perez JI, Menendez Rodriguez P, Zamora P, Benitez J, Ko YD, Fischer HP, Hamann U, Pesch B, Bruning T, Justenhoven C, Brauch H, Eccles DM, Tapper WJ, Gerty SM, Sawyer EJ, Tomlinson IP, Jones A, Kerin M, Miller N, McInerney N, Anton-Culver H, Ziogas A, Shen CY, Hsiung CN, Wu PE, Yang SL, Yu JC, Chen ST, Hsu GC, Haiman CA, Henderson BE, Le Marchand L, Kolonel LN, Lindblom A, Margolin S, Jakubowska A, Lubinski J, Huzarski T, Byrski T, Gorski B, Gronwald J, Hooning MJ, Hollestelle A, van den Ouweland AM, Jager A, Kriege M, Tilanus-Linthorst MM, Collee M, Wang-Gohrke S, Pylkas K, Jukkola-Vuorinen A, Mononen K, Grip M, Hirvikoski P, Winqvist R, Mannermaa A, Kosma VM, Kauppinen J, Kataja V, Auvinen P, Soini Y, Sironen R, Bojesen SE, Orsted DD, Kaur-Knudsen D, Flyger H, Nordestgaard BG, Holland H, Chenevix-Trench G, Manoukian S, Barile M, Radice P, Hankinson SE, Hunter DJ, Tamimi R, Sangrajrang S, Brennan P, McKay J, Odefrey F, Gaborieau V, Devilee P, Huijts PE, Tollenaar RA, Seynaeve C, Dite GS, Apicella C, Hopper JL, Hammet F, Tsimiklis H, Smith LD, Southey MC, Humphreys MK, Easton D, Pharoah P, Sherman ME, Garcia-Closas M (2011) Associations of breast cancer risk factors with tumor subtypes: a pooled analysis from the Breast Cancer Association Consortium studies. J Natl Cancer Inst 103 (3):250–263. doi:10.1093/jnci/djq526

  26. Page DL, Dupont WD, Rogers LW, Rados MS (1985) Atypical hyperplastic lesions of the female breast. A long-term follow-up study. Cancer 55(11):2698–2708

    Article  CAS  PubMed  Google Scholar 

  27. Dupont WD, Page DL (1985) Risk factors for breast cancer in women with proliferative breast disease. N Engl J Med 312(3):146–151

    Article  CAS  PubMed  Google Scholar 

  28. Santen RJ, Mansel R (2005) Benign breast disorders. N Engl J Med 353(3):275–285. doi:10.1056/NEJMra035692

    Article  CAS  PubMed  Google Scholar 

  29. Dupont WD, Parl FF, Hartmann WH, Brinton LA, Winfield AC, Worrell JA, Schuyler PA, Plummer WD (1993) Breast cancer risk associated with proliferative breast disease and atypical hyperplasia. Cancer 71(4):1258–1265

    Article  CAS  PubMed  Google Scholar 

  30. Collins LC, Achacoso NA, Nekhlyudov L, Fletcher SW, Haque R, Quesenberry CP Jr, Alshak NS, Puligandla B, Brodsky GL, Schnitt SJ, Habel LA (2007) Clinical and pathologic features of ductal carcinoma in situ associated with the presence of flat epithelial atypia: an analysis of 543 patients. Mod Pathol 20(11):1149–1155. doi:10.1038/modpathol.3800949

    Article  PubMed  Google Scholar 

  31. Bombonati A, Sgroi DC (2011) The molecular pathology of breast cancer progression. J Pathol 223(2):307–317. doi:10.1002/path.2808

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Schnitt SJ, Collins LC (2010) Pathology of Benign Breast Disorders. In: Harris JR, Lippman ME, Morrow M, Osborne CK (eds) Diseases of the breast, 4th edn. Lippincott Williams & Wilkins, Philadelphia

    Google Scholar 

  33. Cole P, Mark Elwood J, Kaplan SD (1978) Incidence rates and risk factors of benign breast neoplasms. Am J Epidemiol 108(2):112–120

    CAS  PubMed  Google Scholar 

  34. Baer HJ, Schnitt SJ, Connolly JL, Byrne C, Willett WC, Rosner B, Colditz GA (2005) Early life factors and incidence of proliferative benign breast disease. Cancer Epidemiol Biomarkers Prev 14(12):2889–2897. doi:10.1158/1055-9965.EPI-05-0525

    Article  PubMed  Google Scholar 

  35. Berkey CS, Willett WC, Frazier AL, Rosner B, Tamimi RM, Colditz GA (2011) Prospective study of growth and development in older girls and risk of benign breast disease in young women. Cancer 117(8):1612–1620. doi:10.1002/cncr.25692

    Article  PubMed  Google Scholar 

  36. Berkey CS, Willett WC, Frazier AL, Rosner B, Tamimi RM, Rockett HR, Colditz GA (2010) Prospective study of adolescent alcohol consumption and risk of benign breast disease in young women. Pediatrics 125(5):e1081–e1087. doi:10.1542/peds.2009-2347

    Article  PubMed Central  PubMed  Google Scholar 

  37. Liu Y, Tamimi RM, Berkey CS, Willett WC, Collins LC, Schnitt SJ, Connolly JL, Colditz GA (2012) Intakes of alcohol and folate during adolescence and risk of proliferative benign breast disease. Pediatrics 129(5):e1192–e1198. doi:10.1542/peds.2011-2601

    Article  PubMed Central  PubMed  Google Scholar 

  38. Berkey CS, Willett WC, Tamimi RM, Rosner B, Frazier AL, Colditz GA (2013) Vegetable protein and vegetable fat intakes in pre-adolescent and adolescent girls, and risk for benign breast disease in young women. Breast Cancer Res Treat. doi:10.1007/s10549-013-2686-8

  39. Su X, Tamimi RM, Collins LC, Baer HJ, Cho E, Sampson L, Willett WC, Schnitt SJ, Connolly JL, Rosner BA, Colditz GA (2010) Intake of fiber and nuts during adolescence and incidence of proliferative benign breast disease. Cancer Causes Control 21(7):1033–1046. doi:10.1007/s10552-010-9532-7

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  40. Boeke CE, Tamimi RM, Berkey CS, Colditz GA, Eliassen AH, Malspeis S, Willett WC, Frazier AL (2014) Adolescent carotenoid intake and benign breast disease. Pediatrics. doi:10.1542/peds.2013-3844

  41. Berkey CS, Frazier AL, Gardner JD, Colditz GA (1999) Adolescence and breast carcinoma risk. Cancer 85(11):2400–2409

    Article  CAS  PubMed  Google Scholar 

  42. Rosner B, Colditz GA, Willett WC (1994) Reproductive risk factors in a prospective study of breast cancer: the Nurses’ Health Study. Am J Epidemiol 139(8):819–835

    CAS  PubMed  Google Scholar 

  43. Li CI, Malone KE, Daling JR, Potter JD, Bernstein L, Marchbanks PA, Strom BL, Simon MS, Press MF, Ursin G, Burkman RT, Folger SG, Norman S, McDonald JA, Spirtas R (2008) Timing of menarche and first full-term birth in relation to breast cancer risk. Am J Epidemiol 167(2):230–239. doi:10.1093/aje/kwm271

    Article  PubMed Central  PubMed  Google Scholar 

  44. Pike MC, Krailo MD, Henderson BE, Casagrande JT, Hoel DG (1983) ‘Hormonal’ risk factors, ‘breast tissue age’ and the age-incidence of breast cancer. Nature 303(5920):767–770

    Article  CAS  PubMed  Google Scholar 

  45. Rosner B, Colditz GA (1996) Nurses’ health study: log-incidence mathematical model of breast cancer incidence. J Natl Cancer Inst 88(6):359–364

    Article  CAS  PubMed  Google Scholar 

  46. Colditz GA, Frazier AL (1995) Models of breast cancer show that risk is set by events of early life: prevention efforts must shift focus. Cancer Epidemiol Biomarkers Prev 4(5):567–571

    CAS  PubMed  Google Scholar 

  47. Medina D (2005) Mammary developmental fate and breast cancer risk. Endocr Relat Cancer 12(3):483–495. doi:10.1677/erc.1.00804

    Article  CAS  PubMed  Google Scholar 

  48. Medina D (2013) Pregnancy protection of breast cancer: new insights reveal unanswered questions. Breast Cancer Res 15(3):103. doi:10.1186/bcr3414

    CAS  PubMed Central  PubMed  Google Scholar 

  49. Meier-Abt F, Milani E, Roloff T, Brinkhaus H, Duss S, Meyer DS, Klebba I, Balwierz PJ, van Nimwegen E, Bentires-Alj M (2013) Parity induces differentiation and reduces Wnt/Notch signaling ratio and proliferation potential of basal stem/progenitor cells isolated from mouse mammary epithelium. Breast Cancer Res 15(2):R36. doi:10.1186/bcr3419

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  50. Medina D, Kittrell FS (2003) p53 function is required for hormone-mediated protection of mouse mammary tumorigenesis. Cancer Res 63(19):6140–6143

    CAS  PubMed  Google Scholar 

  51. Choudhury S, Almendro V, Merino VF, Wu Z, Maruyama R, Su Y, Martins FC, Fackler MJ, Bessarabova M, Kowalczyk A, Conway T, Beresford-Smith B, Macintyre G, Cheng YK, Lopez-Bujanda Z, Kaspi A, Hu R, Robens J, Nikolskaya T, Haakensen VD, Schnitt SJ, Argani P, Ethington G, Panos L, Grant M, Clark J, Herlihy W, Lin SJ, Chew G, Thompson EW, Greene-Colozzi A, Richardson AL, Rosson GD, Pike M, Garber JE, Nikolsky Y, Blum JL, Au A, Hwang ES, Tamimi RM, Michor F, Haviv I, Liu XS, Sukumar S, Polyak K (2013) Molecular profiling of human mammary gland links breast cancer risk to a p27(+) cell population with progenitor characteristics. Cell Stem Cell 13(1):117–130. doi:10.1016/j.stem.2013.05.004

    Article  CAS  PubMed  Google Scholar 

  52. Bernstein L, Pike MC, Ross RK, Judd HL, Brown JB, Henderson BE (1985) Estrogen and sex hormone-binding globulin levels in nulliparous and parous women. J Natl Cancer Inst 74(4):741–745

    CAS  PubMed  Google Scholar 

  53. Musey VC, Collins DC, Musey PI, Martino-Saltzman D, Preedy JR (1987) Long-term effect of a first pregnancy on the secretion of prolactin. N Engl J Med 316(5):229–234. doi:10.1056/NEJM198701293160501

    Article  CAS  PubMed  Google Scholar 

  54. van den Brandt PA, Spiegelman D, Yaun SS, Adami HO, Beeson L, Folson AR, Fraser G, Goldbohm RA, Graham S, Kushi L, Marshall JR, Miller AB, Rohan T, Smith-Warner SA, Speizer FE, Willett WC, Wolk A, Hunter DJ (2000) Pooled analysis of prospective cohort studies on height, weight, and breast cancer risk. Am J Epidemiol 152:514–527

    Article  PubMed  Google Scholar 

  55. Amadou A, Ferrari P, Muwonge R, Moskal A, Biessy C, Romieu I, Hainaut P (2013) Overweight, obesity and risk of premenopausal breast cancer according to ethnicity: a systematic review and dose-response meta-analysis. Obes Rev. doi:10.1111/obr.12028

  56. Fuemmeler BF, Pendzich MK, Tercyak KP (2009) Weight, dietary behavior, and physical activity in childhood and adolescence: implications for adult cancer risk. Obes Facts 2(3):179–186. doi:10.1159/000220605

    Article  PubMed Central  PubMed  Google Scholar 

  57. Must A, Phillips SM, Naumova EN, Blum M, Harris S, Dawson-Hughes B, Rand WM (2002) Recall of early menstrual history and menarcheal body size: after 30 years, how well do women remember? Am J Epidemiol 155(7):672–679

    Article  CAS  PubMed  Google Scholar 

  58. Must A, Willett WC, Dietz WH (1993) Remote recall of childhood height, weight, and body build by elderly subjects. Am J Epidemiol 138(1):56–64

    CAS  PubMed  Google Scholar 

  59. Baer HJ, Tworoger SS, Hankinson SE, Willett WC (2010) Body fatness at young ages and risk of breast cancer throughout life. Am J Epidemiol 171(11):1183–1194. doi:10.1093/aje/kwq045

    Article  PubMed Central  PubMed  Google Scholar 

  60. Hankinson SE, Colditz GA, Hunter DJ, Manson JE, Willett WC, Stampfer MJ, Longcope C, Speizer FE (1995) Reproductive factors and family history of breast cancer in relation to plasma estrogen and prolactin levels in postmenopausal women in the Nurses’ Health Study (United States). Cancer Causes Control 6(3):217–224

    Article  CAS  PubMed  Google Scholar 

  61. Su X, Hankinson SE, Clevenger CV, Eliassen AH, Tworoger SS (2009) Energy balance, early life body size, and plasma prolactin levels in postmenopausal women. Cancer Causes Control 20(2):253–262. doi:10.1007/s10552-008-9240-8

    Article  PubMed Central  PubMed  Google Scholar 

  62. Schernhammer ES, Tworoger SS, Eliassen AH, Missmer SA, Holly JM, Pollak MN, Hankinson SE (2007) Body shape throughout life and correlations with IGFs and GH. Endocr Relat Cancer 14(3):721–732. doi:10.1677/ERC-06-0080

    Article  CAS  PubMed  Google Scholar 

  63. Poole EM, Tworoger SS, Hankinson SE, Schernhammer ES, Pollak MN, Baer HJ (2011) Body size in early life and adult levels of insulin-like growth factor 1 and insulin-like growth factor binding protein 3. Am J Epidemiol 174(6):642–651. doi:10.1093/aje/kwr123

    Article  PubMed Central  PubMed  Google Scholar 

  64. Rice MS, Bertrand KA, Lajous M, Tamimi RM, Torres-Mejia G, Biessy C, Lopez-Ridaura R, Romieu I (2013) Body size throughout the life course and mammographic density in Mexican women. Breast Cancer Res Treat 138(2):601–610. doi:10.1007/s10549-013-2463-8

    Article  PubMed Central  PubMed  Google Scholar 

  65. Andersen ZJ, Baker JL, Bihrmann K, Vejborg I, Sorensen TI, Lynge E (2014) Birth weight, childhood body mass index, and height in relation to mammographic density and breast cancer: a register-based cohort study. Breast Cancer Res 16(1):R4. doi:10.1186/bcr3596

    Article  PubMed Central  PubMed  Google Scholar 

  66. Preston-Martin S, Pike MC, Ross RK, Jones PA, Henderson BE (1990) Increased cell division as a cause of human cancer. Cancer Res 50:7415–7421

    CAS  PubMed  Google Scholar 

  67. Berkey CS, Gardner JD, Frazier AL, Colditz GA (2000) Relation of childhood diet and body size to menarche and adolescent growth in girls. Am J Epidemiol 152(5):446–452

    Article  CAS  PubMed  Google Scholar 

  68. Ahlgren M, Melbye M, Wohlfahrt J, Sorensen TI (2004) Growth patterns and the risk of breast cancer in women. N Engl J Med 351(16):1619–1626. doi:10.1056/NEJMoa040576

    Article  CAS  PubMed  Google Scholar 

  69. De Stavola BL, dos Santos Silva I, McCormack V, Hardy RJ, Kuh DJ, Wadsworth ME (2004) Childhood growth and breast cancer. Am J Epidemiol 159(7):671–682

    Article  PubMed  Google Scholar 

  70. Kaplowitz PB, Slora EJ, Wasserman RC, Pedlow SE, Herman-Giddens ME (2001) Earlier onset of puberty in girls: relation to increased body mass index and race. Pediatrics 108(2):347–353

    Article  CAS  PubMed  Google Scholar 

  71. De Leonibus C, Marcovecchio ML, Chiavaroli V, de Giorgis T, Chiarelli F, Mohn A (2013) Timing of puberty and physical growth in obese children: a longitudinal study in boys and girls. Pediatr Obe. doi:10.1111/j.2047-6310.2013.00176.x

    Google Scholar 

  72. Berkey CS, Colditz GA, Rockett HR, Frazier AL, Willett WC (2009) Dairy consumption and female height growth: prospective cohort study. Cancer Epidemiol Biomarkers Prev 18(6):1881–1887. doi:10.1158/1055-9965.EPI-08-1163

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  73. Berkey CS, Willett WC, Tamimi RM, Rosner B, Frazier AL, Colditz GA (2013) Dairy intakes in older girls and risk of benign breast disease in young women. Cancer Epidemiol Biomarkers Prev 22(4):670–674. doi:10.1158/1055-9965.EPI-12-1133

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  74. Group Collaborative, in Breast C (2012) Menarche, menopause, and breast cancer risk: individual participant meta-analysis, including 118 964 women with breast cancer from 117 epidemiological studies. Lancet Oncol 13(11):1141–1151. doi:10.1016/S1470-2045(12)70425-4

    Article  Google Scholar 

  75. Shi L, Remer T, Buyken AE, Hartmann MF, Hoffmann P, Wudy SA (2010) Prepubertal urinary estrogen excretion and its relationship with pubertal timing. Am J Physiol Endocrinol Metab 299(6):E990–E997. doi:10.1152/ajpendo.00374.2010

    Article  CAS  PubMed  Google Scholar 

  76. Madigan MP, Troisi R, Potischman N, Dorgan JF, Brinton LA, Hoover RN (1998) Serum hormone levels in relation to reproductive and lifestyle factors in postmenopausal women (United States). Cancer Causes Control 9(2):199–207

    Article  CAS  PubMed  Google Scholar 

  77. Allred DC, Brown P, Medina D (2004) The origins of estrogen receptor alpha-positive and estrogen receptor alpha-negative human breast cancer. Breast Cancer Res 6(6):240–245. doi:10.1186/bcr938

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  78. Ma H, Bernstein L, Pike MC, Ursin G (2006) Reproductive factors and breast cancer risk according to joint estrogen and progesterone receptor status: a meta-analysis of epidemiological studies. Breast Cancer Res 8(4):R43. doi:10.1186/bcr1525

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  79. Ritte R, Lukanova A, Tjonneland A, Olsen A, Overvad K, Mesrine S, Fagherazzi G, Dossus L, Teucher B, Steindorf K, Boeing H, Aleksandrova K, Trichopoulou A, Lagiou P, Trichopoulos D, Palli D, Grioni S, Mattiello A, Tumino R, Sacerdote C, Quiros JR, Buckland G, Molina-Montes E, Chirlaque MD, Ardanaz E, Amiano P, Bueno-de-Mesquita B, van Duijnhoven F, van Gils CH, Peeters PH, Wareham N, Khaw KT, Key TJ, Travis RC, Krum-Hansen S, Gram IT, Lund E, Sund M, Andersson A, Romieu I, Rinaldi S, McCormack V, Riboli E, Kaaks R (2013) Height, age at menarche and risk of hormone receptor-positive and -negative breast cancer: a cohort study. Int J Cancer 132(11):2619–2629. doi:10.1002/ijc.27913

    Article  CAS  PubMed  Google Scholar 

  80. Setiawan VW, Monroe KR, Wilkens LR, Kolonel LN, Pike MC, Henderson BE (2009) Breast cancer risk factors defined by estrogen and progesterone receptor status: the multiethnic cohort study. Am J Epidemiol 169(10):1251–1259. doi:10.1093/aje/kwp036

    Article  PubMed Central  PubMed  Google Scholar 

  81. Silvera SA, Rohan TE (2008) Benign proliferative epithelial disorders of the breast: a review of the epidemiologic evidence. Breast Cancer Res Treat 110(3):397–409. doi:10.1007/s10549-007-9740-3

    Article  PubMed  Google Scholar 

  82. Tamimi RM, Rosner B, Colditz GA (2010) Evaluation of a breast cancer risk prediction model expanded to include category of prior benign breast disease lesion. Cancer 116(21):4944–4953. doi:10.1002/cncr.25386

    Article  PubMed Central  PubMed  Google Scholar 

  83. Wyshak G, Frisch RE (1982) Evidence for a secular trend in age of menarche. N Engl J Med 306(17):1033–1035. doi:10.1056/NEJM198204293061707

    Article  CAS  PubMed  Google Scholar 

  84. Morris DH, Jones ME, Schoemaker MJ, Ashworth A, Swerdlow AJ (2011) Secular trends in age at menarche in women in the UK born 1908–93: results from the Breakthrough Generations Study. Paediatr Perinat Epidemiol 25(4):394–400. doi:10.1111/j.1365-3016.2011.01202.x

    Article  PubMed  Google Scholar 

  85. Nichols HB, Trentham-Dietz A, Hampton JM, Titus-Ernstoff L, Egan KM, Willett WC, Newcomb PA (2006) From menarche to menopause: trends among US Women born from 1912 to 1969. Am J Epidemiol 164(10):1003–1011. doi:10.1093/aje/kwj282

    Article  PubMed  Google Scholar 

  86. Onland-Moret NC, Peeters PH, van Gils CH, Clavel-Chapelon F, Key T, Tjonneland A, Trichopoulou A, Kaaks R, Manjer J, Panico S, Palli D, Tehard B, Stoikidou M, Bueno-De-Mesquita HB, Boeing H, Overvad K, Lenner P, Quiros JR, Chirlaque MD, Miller AB, Khaw KT, Riboli E (2005) Age at menarche in relation to adult height: the EPIC study. Am J Epidemiol 162(7):623–632. doi:10.1093/aje/kwi260

    Article  CAS  PubMed  Google Scholar 

  87. McDowell MA, Brody DJ, Hughes JP (2007) Has age at menarche changed? Results from the National Health and Nutrition Examination Survey (NHANES) 1999–2004. J Adolesc Health 40(3):227–231. doi:10.1016/j.jadohealth.2006.10.002

    Article  PubMed  Google Scholar 

  88. Cho GJ, Park HT, Shin JH, Hur JY, Kim YT, Kim SH, Lee KW, Kim T (2010) Age at menarche in a Korean population: secular trends and influencing factors. Eur J Pediatr 169(1):89–94. doi:10.1007/s00431-009-0993-1

    Article  PubMed  Google Scholar 

  89. Karapanou O, Papadimitriou A (2010) Determinants of menarche. Reprod Biol Endocrinol 8:115. doi:10.1186/1477-7827-8-115

    Article  PubMed Central  PubMed  Google Scholar 

  90. Morris DH, Jones ME, Schoemaker MJ, Ashworth A, Swerdlow AJ (2010) Determinants of age at menarche in the UK: analyses from the Breakthrough Generations Study. Br J Cancer 103(11):1760–1764. doi:10.1038/sj.bjc.6605978

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  91. Lynch BM, Neilson HK, Friedenreich CM (2011) Physical activity and breast cancer prevention. In: Courneya KS, Friedenreich CM (eds) Physical activity and cancer. Spring, Berlin

    Google Scholar 

  92. Monninkhof EM, Elias SG, Vlems FA, van der Tweel I, Schuit AJ, Voskuil DW, van Leeuwen FE (2007) Physical activity and breast cancer: a systematic review. Epidemiology 18(1):137–157. doi:10.1097/01.ede.0000251167.75581.98

    Article  PubMed  Google Scholar 

  93. Peters TM, Moore SC, Gierach GL, Wareham NJ, Ekelund U, Hollenbeck AR, Schatzkin A, Leitzmann MF (2009) Intensity and timing of physical activity in relation to postmenopausal breast cancer risk: the prospective NIH-AARP diet and health study. BMC Cancer 9:349. doi:10.1186/1471-2407-9-349

    Article  PubMed Central  PubMed  Google Scholar 

  94. Maruti SS, Willett WC, Feskanich D, Rosner B, Colditz GA (2008) A prospective study of age-specific physical activity and premenopausal breast cancer. J Natl Cancer Inst 100:728–737

  95. Matthews CE, Shu XO, Jin F, Dai Q, Hebert JR, Ruan ZX, Gao YT, Zheng W (2001) Lifetime physical activity and breast cancer risk in the Shanghai Breast Cancer Study. Br J Cancer 84(7):994–1001. doi:10.1054/bjoc.2000.1671

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  96. Neilson HK, Friedenreich CM, Brockton NT, Millikan RC (2009) Physical activity and postmenopausal breast cancer: proposed biologic mechanisms and areas for future research. Cancer Epidemiol Biomarkers Prev 18(1):11–27. doi:10.1158/1055-9965.EPI-08-0756

    Article  CAS  PubMed  Google Scholar 

  97. Garland M, Hunter DJ, Colditz GA, Spiegelman DL, Manson JE, Stampfer MJ, Willett WC (1999) Alcohol consumption in relation to breast cancer risk in a cohort of United States women 25–42 years of age. Cancer Epidemiol Biomarkers Prev 8(11):1017–1021

    CAS  PubMed  Google Scholar 

  98. Horn-Ross PL, Canchola AJ, West DW, Stewart SL, Bernstein L, Deapen D, Pinder R, Ross RK, Anton-Culver H, Peel D, Ziogas A, Reynolds P, Wright W (2004) Patterns of alcohol consumption and breast cancer risk in the California Teachers Study cohort. Cancer Epidemiol Biomarkers Prev 13(3):405–411

    PubMed  Google Scholar 

  99. Liu Y, Colditz GA, Rosner B, Berkey CS, Collins LC, Schnitt SJ, Connolly JL, Chen WY, Willett WC, Tamimi RM (2013) Alcohol intake between menarche and first pregnancy: a prospective study of breast cancer risk. J Natl Cancer Inst 105(20):1571–1578. doi:10.1093/jnci/djt213

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  100. Cui Y, Page DL, Chlebowski RT, Beresford SA, Hendrix SL, Lane DS, Rohan TE (2007) Alcohol and folate consumption and risk of benign proliferative epithelial disorders of the breast. Int J Cancer 121(6):1346–1351. doi:10.1002/ijc.22861

    Article  CAS  PubMed  Google Scholar 

  101. Friedenreich C, Bryant H, Alexander F, Hugh J, Danyluk J, Page D (2000) Risk factors for benign proliferative breast disease. Int J Epidemiol 29(4):637–644

    Article  CAS  PubMed  Google Scholar 

  102. Rohan TE, Cook MG (1989) Alcohol consumption and risk of benign proliferative epithelial disorders of the breast in women. Int J Cancer 43(4):631–636

    Article  CAS  PubMed  Google Scholar 

  103. Berkey CS, Tamimi RM, Rosner B, Frazier AL, Colditz GA (2012) Young women with family history of breast cancer and their risk factors for benign breast disease. Cancer 118(11):2796–2803. doi:10.1002/cncr.26519

    Article  PubMed Central  PubMed  Google Scholar 

  104. Seitz HK, Pelucchi C, Bagnardi V, La Vecchia C (2012) Epidemiology and pathophysiology of alcohol and breast cancer: update 2012. Alcohol Alcohol 47(3):204–212. doi:10.1093/alcalc/ags011

    Article  PubMed  Google Scholar 

  105. Korde LA, Wu AH, Fears T, Nomura AM, West DW, Kolonel LN, Pike MC, Hoover RN, Ziegler RG (2009) Childhood soy intake and breast cancer risk in Asian American women. Cancer Epidemiol Biomarkers Prev 18(4):1050–1059. doi:10.1158/1055-9965.EPI-08-0405

    Article  CAS  PubMed  Google Scholar 

  106. Wu AH, Yu MC, Tseng CC, Pike MC (2008) Epidemiology of soy exposures and breast cancer risk. Br J Cancer 98(1):9–14. doi:10.1038/sj.bjc.6604145

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  107. Lee SA, Shu XO, Li H, Yang G, Cai H, Wen W, Ji BT, Gao J, Gao YT, Zheng W (2009) Adolescent and adult soy food intake and breast cancer risk: results from the Shanghai Women’s Health Study. Am J Clin Nutr 89(6):1920–1926. doi:10.3945/ajcn.2008.27361

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  108. Su X, Tamimi RM, Collins LC, Baer HJ, Cho E, Sampson L, Willett WC, Schnitt SJ, Connolly JL, Rosner BA, Colditz GA (2010) Intake of fiber and nuts during adolescence and incidence of proliferative benign breast disease. Cancer Causes Control 21(7):1033–1046. doi:10.1007/s10552-010-9532-7

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  109. Linos E, Willett WC, Cho E, Frazier L (2010) Adolescent diet in relation to breast cancer risk among premenopausal women. Cancer Epidemiol Biomarkers Prev 19(3):689–696. doi:10.1158/1055-9965.EPI-09-0802

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  110. Liu Y, Colditz GA, Cotterchio M, Boucher BA, Kreiger N (2014) Adolescent dietary fiber, vegetable fat, vegetable protein, and nut intakes and breast cancer risk. Breast Cancer Res Treat. doi:10.1007/s10549-014-2953-3

    PubMed Central  Google Scholar 

  111. de Beer H (2012) Dairy products and physical stature: a systematic review and meta-analysis of controlled trials. Econ Hum Biol 10(3):299–309. doi:10.1016/j.ehb.2011.08.003

    Article  PubMed  Google Scholar 

  112. Su X, Colditz GA, Collins LC, Baer HJ, Sampson LA, Willett WC, Berkey CS, Schnitt SJ, Connolly JL, Rosner BA, Tamimi RM (2012) Adolescent intakes of vitamin D and calcium and incidence of proliferative benign breast disease. Breast Cancer Res Treat 134(2):783–791. doi:10.1007/s10549-012-2091-8

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  113. Fund World Cancer Research (2010) Continuos update project. Keeping the science current. Breast cancer 2010 report. Continuos update project. American Institute for Cancer Research, Washington

    Google Scholar 

  114. Dwyer JT, Coleman KA (1997) Insights into dietary recall from a longitudinal study: accuracy over four decades. Am J Clin Nutr 65(4 Suppl):1153S–1158S

    CAS  PubMed  Google Scholar 

  115. Maruti SS, Feskanich D, Colditz GA, Frazier AL, Sampson LA, Michels KB, Hunter DJ, Spiegelman D, Willett WC (2005) Adult recall of adolescent diet: reproducibility and comparison with maternal reporting. Am J Epidemiol 161(1):89–97. doi:10.1093/aje/kwi019

    Article  PubMed Central  PubMed  Google Scholar 

  116. Maruti SS, Feskanich D, Rockett HR, Colditz GA, Sampson LA, Willett WC (2006) Validation of adolescent diet recalled by adults. Epidemiology 17(2):226–229. doi:10.1097/01.ede.0000198181.86685.49

    Article  PubMed  Google Scholar 

  117. Casey VA, Dwyer JT, Berkey CS, Coleman KA, Gardner J, Valadian I (1991) Long-term memory of body weight and past weight satisfaction: a longitudinal follow-up study. Am J Clin Nutr 53(6):1493–1498

    CAS  PubMed  Google Scholar 

  118. Must A, Willett WC, Dietz WH (1993) Remote recall of childhood height, weight, and body build by elderly subjects. Am J Epidemiol 138:56–64

    CAS  PubMed  Google Scholar 

  119. Interagency Breast Cancer and Environmental Research Coordinating Committee (2013) Breast cancer and the environment: prioritizing prevention. Interagency Breast Cancer and Environmental Research Coordinating Committee. National Institutes of Health, Bethesda, MD

  120. Rudel RA, Fenton SE, Ackerman JM, Euling SY, Makris SL (2011) Environmental exposures and mammary gland development: state of the science, public health implications, and research recommendations. Environ Health Perspect 119(8):1053–1061. doi:10.1289/ehp.1002864

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

GAC and KB are supported by the Foundation for Barnes-Jewish Hospital, St. Louis, Missouri. GAC and CSB are also supported by the Breast Cancer Research Foundation.

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Authors and Affiliations

  1. The Division of Public Health Sciences, Department of Surgery, Washington University School of Medicine, Campus Box 8109, 660 S. Euclid Avenue, St. Louis, MO, 63110, USA

    Graham A. Colditz & Kari Bohlke

  2. The Siteman Cancer Center, Barnes-Jewish Hospital, Washington University School of Medicine, St. Louis, MO, USA

    Graham A. Colditz & Kari Bohlke

  3. Channing Division of Network Medicine, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA

    Catherine S. Berkey

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  1. Graham A. Colditz
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Colditz, G.A., Bohlke, K. & Berkey, C.S. Breast cancer risk accumulation starts early: prevention must also. Breast Cancer Res Treat 145, 567–579 (2014). https://doi.org/10.1007/s10549-014-2993-8

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