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Intakes of fat and micronutrients between ages 13 and 18 years and the incidence of proliferative benign breast disease

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Abstract

Purpose

Dietary exposures during adolescence may exert important effects on breast development and future breast cancer risk. This study evaluated the associations between high school intakes of fat and micronutrients and the incidence of proliferative benign breast disease (BBD), a marker of increased breast cancer risk.

Methods

29,480 women (mean age 43.3 years, range 33.6–52.9) completed a high school food frequency questionnaire in 1998 in the Nurses’ Health Study II. Between 1991 and 2001, 682 women (follow-up time: 259,828 person-years) were diagnosed with proliferative BBD whose biopsy slides were reviewed and confirmed by the study pathologists.

Results

In multivariate Cox proportional hazards models, high school intakes of total fat and types of fat were not associated with proliferative BBD. Women in the highest quintile of total retinol activity equivalents (RAEs), which incorporate retinol, α- and β-carotene, and β-cryptoxanthin intakes, had a 17 % lower risk of proliferative BBD than those in the lowest quintile [multivariate hazard ratio (HR) 95 % CI 0.83 (0.64, 1.07), p trend = 0.01]; however, additional adjustment for high school dietary factors (vitamin D, nuts, and fiber) rendered the association nonsignificant [0.99 (0.73, 1.34), p trend = 0.32]. Results were similar with additional adjustment for adult RAE intake. Intakes of vitamin E and individual carotenoids were not associated with proliferative BBD, although an inverse association cannot be ruled out.

Conclusions

In this study, adolescent fat and micronutrient intakes were not associated with risk of proliferative BBD.

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References

  1. Armstrong B, Doll R (1975) Environmental factors and cancer incidence and mortality in different countries with special reference to dietary practices. Int J Cancer 15:617–631

    Article  CAS  PubMed  Google Scholar 

  2. Boyd NF, Martin LJ, Noffel M, Lockwood GA, Trichler DL (1993) A meta-analysis of studies of dietary fat and breast cancer risk. Br J Cancer 68:627–636

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  3. Howe GR, Hirohata T, Hislop TG, Iscovich JM, Yuan JM, Katsouyanni K, Lubin F, Marubini E, Modan B, Rohan T et al (1990) Dietary factors and risk of breast cancer: combined analysis of 12 case–control studies. J Natl Cancer Inst 82:561–569

    Article  CAS  PubMed  Google Scholar 

  4. Michels KB, Mohllajee AP, Roset-Bahmanyar E, Beehler GP, Moysich KB (2007) Diet and breast cancer: a review of the prospective observational studies. Cancer 109:2712–2749

    Article  CAS  PubMed  Google Scholar 

  5. Smith-Warner SA, Spiegelman D, Adami HO, Beeson WL, van den Brandt PA, Folsom AR, Fraser GE, Freudenheim JL, Goldbohm RA, Graham S et al (2001) Types of dietary fat and breast cancer: a pooled analysis of cohort studies. Int J Cancer 92:767–774

    Article  CAS  PubMed  Google Scholar 

  6. Prentice RL, Caan B, Chlebowski RT, Patterson R, Kuller LH, Ockene JK, Margolis KL, Limacher MC, Manson JE, Parker LM et al (2006) Low-fat dietary pattern and risk of invasive breast cancer: the Women’s Health Initiative Randomized Controlled Dietary Modification Trial. JAMA 295:629–642

    Article  CAS  PubMed  Google Scholar 

  7. Martin LJ, Li Q, Melnichouk O, Greenberg C, Minkin S, Hislop G, Boyd NF (2011) A randomized trial of dietary intervention for breast cancer prevention. Cancer Res 71:123–133

    Article  CAS  PubMed  Google Scholar 

  8. Frei B (1994) Reactive oxygen species and antioxidant vitamins: mechanisms of action. Am J Med 97:5S–13S

    Article  CAS  PubMed  Google Scholar 

  9. McCall MR, Frei B (1999) Can antioxidant vitamins materially reduce oxidative damage in humans? Free Radic Biol Med 26:1034–1053

    Article  CAS  PubMed  Google Scholar 

  10. Blomhoff R (1994) Introduction: overview of vitamin A metabolism and function. In: Blomhoff R (ed) Vitamin A in health and disease. Marcel Dekker Inc, New York, pp 1–35

    Google Scholar 

  11. Kelley DS, Bendich A (1996) Essential nutrients and immunologic functions. Am J Clin Nutr 63:994S–996S

    CAS  PubMed  Google Scholar 

  12. Fulan H, Changxing J, Baina WY, Wencui Z, Chunqing L, Fan W, Dandan L, Dianjun S, Tong W, Da P, Yashuang Z (2011) Retinol, vitamins A, C, and E and breast cancer risk: a meta-analysis and meta-regression. Cancer Causes Control 22:1383–1396

    Article  PubMed  Google Scholar 

  13. Hu F, Wang Yi B, Zhang W, Liang J, Lin C, Li D, Wang F, Pang D, Zhao Y (2012) Carotenoids and breast cancer risk: a meta-analysis and meta-regression. Breast Cancer Res Treat 131:239–253

    Article  CAS  PubMed  Google Scholar 

  14. Zhang X, Spiegelman D, Baglietto L, Bernstein L, Boggs DA, van den Brandt PA, Buring JE, Gapstur SM, Giles GG, Giovannucci E et al (2012) Carotenoid intakes and risk of breast cancer defined by estrogen receptor and progesterone receptor status: a pooled analysis of 18 prospective cohort studies. Am J Clin Nutr 95:713–725

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Eliassen AH, Hendrickson SJ, Brinton LA, Buring JE, Campos H, Dai Q, Dorgan JF, Franke AA, Gao YT, Goodman MT et al (2012) Circulating carotenoids and risk of breast cancer: pooled analysis of eight prospective studies. J Natl Cancer Inst 104:1905–1916

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Aune D, Chan DS, Vieira AR, Navarro Rosenblatt DA, Vieira R, Greenwood DC, Norat T (2012) Dietary compared with blood concentrations of carotenoids and breast cancer risk: a systematic review and meta-analysis of prospective studies. Am J Clin Nutr 96:356–373

    Article  CAS  PubMed  Google Scholar 

  17. Schnitt SJ, Connolly JL (2004) Pathology of benign breast disorders. In: Harris JR, Lippman ME, Morrow M, Osborne CK (eds) Diseases of the breast, 3rd edn. Lippincott Williams and Wilkins, Philadelphia, pp 77–99

    Google Scholar 

  18. Rohan TE, Cook MG, Potter JD, McMichael AJ (1990) A case–control study of diet and benign proliferative epithelial disorders of the breast. Cancer Res 50:3176–3181

    CAS  PubMed  Google Scholar 

  19. Hislop TG, Band PR, Deschamps M, Ng V, Coldman AJ, Worth AJ, Labo T (1990) Diet and histologic types of benign breast disease defined by subsequent risk of breast cancer. Am J Epidemiol 131:263–270

    CAS  PubMed  Google Scholar 

  20. Lubin F, Wax Y, Ron E, Black M, Chetrit A, Rosen N, Alfandary E, Modan B (1989) Nutritional factors associated with benign breast disease etiology: a case–control study. Am J Clin Nutr 50:551–556

    CAS  PubMed  Google Scholar 

  21. Webb PM, Byrne C, Schnitt SJ, Connolly JL, Jacobs TW, Baer HJ, Willett WC, Colditz GA (2004) A prospective study of diet and benign breast disease. Cancer Epidemiol Biomarkers Prev 13:1106–1113

    PubMed  Google Scholar 

  22. Rohan TE, Jain M, Miller AB (1998) A case-cohort study of diet and risk of benign proliferative epithelial disorders of the breast (Canada). Cancer Causes Control 9:19–27

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  24. Buell P (1973) Changing incidence of breast cancer in Japanese–American women. J Natl Cancer Inst 51:1479–1483

    CAS  PubMed  Google Scholar 

  25. 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 4:567–571

    CAS  PubMed  Google Scholar 

  26. Ziegler RG, Hoover RN, Pike MC, Hildesheim A, Nomura AM, 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 

  27. Frazier AL, Ryan CT, Rockett H, Willett WC, Colditz GA (2003) Adolescent diet and risk of breast cancer. Breast Cancer Res 5:R59–R64

    Article  PubMed Central  PubMed  Google Scholar 

  28. Frazier AL, Li L, Cho E, Willett WC, Colditz GA (2004) Adolescent diet and risk of breast cancer. Cancer Causes Control 15:73–82

    Article  PubMed  Google Scholar 

  29. Baer HJ, Schnitt SJ, Connolly JL, Byrne C, Cho E, Willett WC, Colditz GA (2003) Adolescent diet and incidence of proliferative benign breast disease. Cancer Epidemiol Biomarkers Prev 12:1159–1167

    PubMed  Google Scholar 

  30. Colditz GA, Manson JE, Hankinson SE (1997) The Nurses’ Health Study: 20-year contribution to the understanding of health among women. J Womens Health 6:49–62

    Article  CAS  PubMed  Google Scholar 

  31. 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 21:1033–1046

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Trumbo P, Yates AA, Schlicker S, Poos M (2001) Dietary reference intakes: vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc. J Am Diet Assoc 101:294–301

    Article  CAS  PubMed  Google Scholar 

  33. 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 161:89–97

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  35. Willett W, Stampfer M (1998) Implications of total energy intake for epidemiologic analyses. In: Willett W (ed) Nutritional Epidemiology, 2nd edn. Oxford University Press, New York, pp 273–301

    Chapter  Google Scholar 

  36. 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 134:783–791

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. Therneau TM (1997) Extending the Cox Model. In: Lin DY, Fleming TR (eds) Proceedings of the first seattle symposium in biostatistics: survival Analysis. Springer, New York, pp 51–84

    Chapter  Google Scholar 

  38. 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 133:e1292-e1298

  39. 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 141:299–306

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  40. Nagel G, Linseisen J, van Gils CH, Peeters PH, Boutron-Ruault MC, Clavel-Chapelon F, Romieu I, Tjønneland A, Olsen A, Roswall N (2010) Dietary β-carotene, vitamin C and E intake and breast cancer risk in the European Prospective Investigation into Cancer and Nutrition (EPIC). Breast Cancer Res Treat 119:753–765

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank the participants and staff of the Nurses’ Health Study II for their valuable contributions as well as the following state cancer registries for their help: AL, AZ, AR, CA, CO, CT, DE, FL, GA, ID, IL, IN, IA, KY, LA, ME, MD, MA, MI, NE, NH, NJ, NY, NC, ND, OH, OK, OR, PA, RI, SC, TN, TX, VA, WA, WY. In addition, this study was approved by the Connecticut Department of Public Health (DPH) Human Investigations Committee. Certain data used in this publication were obtained from the DPH. This work was supported by the Breast Cancer Research Foundation and the National Institutes of Health (Grant Nos. UM1 CA176726, CA 050385, CA 046475). Caroline Boeke was funded by T32 CA 09001. Graham Colditz was supported by an American Cancer Society Clinical Research Professorship and by the Breast Cancer Research Foundation.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. School of Public Health and Primary Care, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong, People’s Republic of China

    Xuefen Su

  2. CUHK Shenzhen Research Institute, Shenzhen, People’s Republic of China

    Xuefen Su

  3. Channing Division of Network Medicine, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, 181 Longwood Avenue, 3rd Floor, Boston, MA, 02115, USA

    Caroline E. Boeke, Walter C. Willett, Bernard Rosner & Rulla M. Tamimi

  4. Department of Epidemiology, Harvard School of Public Health, 677 Huntington Avenue, Boston, MA, 02114, USA

    Caroline E. Boeke, Heather J. Baer, Walter C. Willett, Bernard Rosner & Rulla M. Tamimi

  5. Department of Pathology, Harvard Medical School and Beth Israel Deaconess Medical Center, 330 Brookline Avenue, Boston, MA, 02215, USA

    Laura C. Collins, Stuart J. Schnitt & James L. Connolly

  6. Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA

    Heather J. Baer, Walter C. Willett, Bernard Rosner & Rulla M. Tamimi

  7. Department of Nutrition, Harvard School of Public Health, Boston, MA, USA

    Walter C. Willett

  8. Department of Biostatistics, Harvard School of Public Health, Boston, MA, USA

    Bernard Rosner

  9. Alvin J. Siteman Cancer Center and Department of Surgery, Washington University School of Medicine, 660 S Euclid Avenue, St Louis, MO, 63110, USA

    Graham A. Colditz

Authors
  1. Xuefen Su
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  2. Caroline E. Boeke
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  3. Laura C. Collins
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  4. Heather J. Baer
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  7. James L. Connolly
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  8. Bernard Rosner
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  9. Graham A. Colditz
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  10. Rulla M. Tamimi
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Corresponding author

Correspondence to Caroline E. Boeke.

Additional information

Graham A. Colditz and Rulla M. Tamimi have contributed equally to this manuscript and should be considered co-senior authors.

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Su, X., Boeke, C.E., Collins, L.C. et al. Intakes of fat and micronutrients between ages 13 and 18 years and the incidence of proliferative benign breast disease. Cancer Causes Control 26, 79–90 (2015). https://doi.org/10.1007/s10552-014-0484-1

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  • DOI: https://doi.org/10.1007/s10552-014-0484-1

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