Cancer Causes & Control

, Volume 21, Issue 7, pp 1033–1046 | Cite as

Intake of fiber and nuts during adolescence and incidence of proliferative benign breast disease

  • Xuefen Su
  • Rulla M. Tamimi
  • Laura C. Collins
  • Heather J. Baer
  • Eunyoung Cho
  • Laura Sampson
  • Walter C. Willett
  • Stuart J. Schnitt
  • James L. Connolly
  • Bernard A. Rosner
  • Graham A. Colditz
Original paper

Abstract

Objective

We examined the association between adolescent fiber intake and proliferative BBD, a marker of increased breast cancer risk, in the Nurses’ Health Study II.

Methods

Among 29,480 women who completed a high school diet questionnaire in 1998, 682 proliferative BBD cases were identified and confirmed by centralized pathology review between 1991 and 2001. Multivariate-adjusted Cox proportional hazards regression was used to estimate hazard ratios (HRs) and 95% confidence intervals (CIs).

Results

Women in the highest quintile of adolescent fiber intake had a 25% lower risk of proliferative BBD (multivariate HR (95% CI): 0.75 (0.59, 0.96), p-trend = 0.01) than women in the lowest quintile. High school intake of nuts was also related to significantly reduced BBD risk. Women consuming ≥2 servings of nuts/week had a 36% lower risk (multivariate HR (95% CI): 0.64 (0.48, 0.85), p-trend < 0.01) than women consuming <1 serving/month. Results were essentially the same when the analysis was restricted to prospective cases (n = 142) diagnosed after return of the high school diet questionnaire.

Conclusions

These findings support the hypothesis that dietary intake of fiber and nuts during adolescence influences subsequent risk of breast disease and may suggest a viable means for breast cancer prevention.

Keywords

Adolescent diet Fiber Nuts Proliferative BBD 

References

  1. 1.
    Stewart BW, Kleihues P (2003) World cancer report. International Agency for Research on Cancer, Lyon, France; [cited 9 Dec 2008]. Available from: http://www.iarc.fr/en/Publications/PDFs-online/World-Cancer-Report
  2. 2.
    Ziegler RG, Hoover RN, Pike MC et al (1993) Migration patterns and breast cancer risk in Asian-American women. J Natl Cancer Inst 85:1819–1927CrossRefPubMedGoogle Scholar
  3. 3.
    Buell P (1973) Changing incidence of breast cancer in Japanese-American women. J Natl Cancer Inst 51:1479–1483PubMedGoogle Scholar
  4. 4.
    Cohen LA, Zhao Z, Zang EA, Wynn TT, Simi B, Rivenson A (1996) Wheat bran and psyllium diets: effects on N-methylnitrosourea-induced mammary tumorigenesis in F344 rats. J Natl Cancer Inst 88:899–907CrossRefPubMedGoogle Scholar
  5. 5.
    Howe GR, Hirohata T, Hislop TG et al (1990) Dietary factors and risk of breast cancer: combined analysis of 12 case-control studies. J Natl Cancer Inst 82:561–569CrossRefPubMedGoogle Scholar
  6. 6.
    Baghurst PA, Rohan TE (1994) High-fiber diets and reduced risk of breast cancer. Int J Cancer 56:173–176CrossRefPubMedGoogle Scholar
  7. 7.
    De Stefani E, Correa P, Ronco A, Mendilaharsu M, Guidobono M, Deneo-Pellegrini H (1997) Dietary fiber and risk of breast cancer: a case-control study in Uruguay. Nutr Cancer 28:14–19CrossRefPubMedGoogle Scholar
  8. 8.
    Freudenheim JL, Marshall JR, Vena JE et al (1996) Premenopausal breast cancer risk and intake of vegetables, fruits, and related nutrients. J Natl Cancer Inst 88:340–348CrossRefPubMedGoogle Scholar
  9. 9.
    Yuan JM, Wang QS, Ross RK, Henderson BE, Yu MC (1995) Diet and breast cancer in Shanghai and Tianjin, China. Br J Cancer 71:1353–1358PubMedGoogle Scholar
  10. 10.
    Cade JE, Burley VJ, Greenwood DC, UK Women’s Cohort Study Steering Group (2007) Dietary fibre and risk of breast cancer in the UK Women’s Cohort Study. Int J Epidemiol 36:431–438CrossRefPubMedGoogle Scholar
  11. 11.
    Park Y, Brinton LA, Subar AF, Hollenbeck A, Schatzkin A (2009) Dietary fiber intake and risk of breast cancer in postmenopausal women: the National Institutes of Health-AARP Diet and Health Study. Am J Clin Nutr 90:664–671CrossRefPubMedGoogle Scholar
  12. 12.
    Cho E, Spiegelman D, Hunter DJ, Chen W, Colditz GA, Willett WC (2003) Premenopausal dietary carbohydrate, glycemic index, glycemic load, and fiber in relation to risk of breast cancer. Cancer Epidemiol Biomarkers Prev 12:1153–1158PubMedGoogle Scholar
  13. 13.
    Giles GG, Simpson JA, English DR et al (2006) Dietary carbohydrate, fibre, glycaemic index, glycaemic load and the risk of postmenopausal breast cancer. Int J Cancer 118:1843–1847CrossRefPubMedGoogle Scholar
  14. 14.
    Graham S, Zielezny M, Marshall J et al (1992) Diet in the epidemiology of postmenopausal breast cancer in the New York State Cohort. Am J Epidemiol 136:1327–1337PubMedGoogle Scholar
  15. 15.
    Holmes MD, Liu S, Hankinson SE, Colditz GA, Hunter DJ, Willett WC (2004) Dietary carbohydrates, fiber, and breast cancer risk. Am J Epidemiol 159:732–739CrossRefPubMedGoogle Scholar
  16. 16.
    Horn-Ross PL, Hoggatt KJ, West DW et al (2002) Recent diet and breast cancer risk: the California Teachers Study (USA). Cancer Causes Control 13:407–415CrossRefPubMedGoogle Scholar
  17. 17.
    Jarvinen R, Knekt P, Seppanen R, Teppo L (1997) Diet and breast cancer risk in a cohort of Finnish women. Cancer Lett 114:251–253CrossRefPubMedGoogle Scholar
  18. 18.
    Maruti SS, Lampe JW, Potter JD, Ready A, White E (2008) A prospective study of bowel motility and related factors on breast cancer risk. Cancer Epidemiol Biomark Prev 17:1746–1750CrossRefGoogle Scholar
  19. 19.
    Mattisson I, Wirfalt E, Johansson U, Gullberg B, Olsson H, Berglund G (2004) Intakes of plant foods, fibre and fat and risk of breast cancer—a prospective study in the Malmo Diet and Cancer cohort. Br J Cancer 90:122–127CrossRefPubMedGoogle Scholar
  20. 20.
    Rohan TE, Howe GR, Friedenreich CM, Jain M, Miller AB (1993) Dietary fiber, vitamins A, C, and E, and risk of breast cancer: a cohort study. Cancer Causes Control 4:29–37CrossRefPubMedGoogle Scholar
  21. 21.
    Sonestedt E, Borgquist S, Ericson U et al (2008) Plant foods and oestrogen receptor α- and β-defined breast cancer: observations from the Malmo Diet and Cancer cohort. Carcinogenesis 29:2203–2209CrossRefPubMedGoogle Scholar
  22. 22.
    Suzuki R, Rylander-Rudqvist T, Ye W, Saji S, Adlercreutz H, Wolk A (2008) Dietary fiber intake and risk of postmenopausal breast cancer defined by estrogen and progesterone receptor status—a prospective cohort study among Swedish women. Int J Cancer 122:403–412CrossRefPubMedGoogle Scholar
  23. 23.
    Terry P, Jain M, Miller AB, Howe GR, Rohan TE (2002) No association among total dietary fiber, fiber fractions, and risk of breast cancer. Cancer Epidemiol Biomarkers Prev 11:1507–1508PubMedGoogle Scholar
  24. 24.
    Verhoeven DT, Assen N, Goldbohm RA et al (1997) Vitamins C and E, retinol, beta- carotene and dietary fibre in relation to breast cancer risk: a prospective cohort study. Br J Cancer 75:149–155PubMedGoogle Scholar
  25. 25.
    Wen W, Shu XO, Li H et al (2009) Dietary carbohydrates, fiber, and breast cancer risk in Chinese women. Am J Clin Nutr 89:283–289CrossRefPubMedGoogle Scholar
  26. 26.
    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 & Wilkins, Philadelphia, pp 77–99Google Scholar
  27. 27.
    Li W, Ray RM, Lampe JW et al (2005) Dietary and other risk factors in women having fibrocystic breast conditions with and without concurrent breast cancer: a nested case-control study in Shanghai, China. Int J Cancer 115:981–993CrossRefPubMedGoogle Scholar
  28. 28.
    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 9:19–27CrossRefPubMedGoogle Scholar
  29. 29.
    Wu C, Ray RM, Lin MG et al (2004) A case-control study of risk factors for fibrocystic breast conditions: Shanghai Nutrition and Breast Disease Study, China, 1995–2000. Am J Epidemiol 160:945–960CrossRefPubMedGoogle Scholar
  30. 30.
    Baghurst PA, Rohan TE (1995) Dietary fiber and risk of benign proliferative epithelial disorders of the breast. Int J Cancer 63:481–485CrossRefPubMedGoogle Scholar
  31. 31.
    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 50:3176–3181PubMedGoogle Scholar
  32. 32.
    Webb PM, Byrne C, Schnitt SJ et al (2004) A prospective study of diet and benign breast disease. Cancer Epidemiol Biomarkers Prev 13:1106–1113PubMedGoogle Scholar
  33. 33.
    Russo J, Tay LK, Russo IH (1982) Differentiation of the mammary gland and susceptibility to carcinogenesis. Breast Cancer Res Treat 2:5–73CrossRefPubMedGoogle Scholar
  34. 34.
    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 4:567–571PubMedGoogle Scholar
  35. 35.
    Land CE, Tokunaga M, Koyama K et al (2003) Incidence of female breast cancer among atomic bomb survivors, Hiroshima and Nagasaki, 1950–1990. Radiat Res 160:707–717CrossRefPubMedGoogle Scholar
  36. 36.
    Tretli S, Gaard M (1996) Lifestyle changes during adolescence and risk of breast cancer: an ecologic study of the effect of World War II in Norway. Cancer Causes Control 7:507–512CrossRefPubMedGoogle Scholar
  37. 37.
    Frazier AL, Li L, Cho E, Willett WC, Colditz GA (2004) Adolescent diet and risk of breast cancer. Cancer Causes Control 15:73–82CrossRefPubMedGoogle Scholar
  38. 38.
    Frazier AL, Ryan CT, Rockett H, Willett WC, Colditz GA (2003) Adolescent diet and risk of breast cancer. Breast Cancer Res 5:R59–R64CrossRefGoogle Scholar
  39. 39.
    Hislop TG, Coldman AJ, Elwood JM, Brauer G, Kan L (1986) Childhood and recent eating patterns and risk of breast cancer. Cancer Detect Prev 9:47–58PubMedGoogle Scholar
  40. 40.
    Potischman N, Weiss HA, Swanson CA et al (1998) Diet during adolescence and risk of breast cancer among young women. J Natl Cancer Inst 90:226–233CrossRefPubMedGoogle Scholar
  41. 41.
    Pryor M, Slattery ML, Robison LM, Egger M (1989) Adolescent diet and breast cancer in Utah. Cancer Res 49:2161–2167PubMedGoogle Scholar
  42. 42.
    Baer HJ, Schnitt SJ, Connolly JL et al (2003) Adolescent diet and incidence of proliferative benign breast disease. Cancer Epidemiol Biomarkers Prev 12:1159–1167PubMedGoogle Scholar
  43. 43.
    Colditz GA, Manson JE, Hankinson SE (1997) The Nurses’ Health Study: 20-year contribution to the understanding of health among women. J Womens Health 6:49–62CrossRefPubMedGoogle Scholar
  44. 44.
    Maruti SS, Feskanich D, Colditz GA et al (2005) Adult recall of adolescent diet: reproducibility and comparison with maternal reporting. Am J Epidemiol 161:89–97CrossRefPubMedGoogle Scholar
  45. 45.
    Dupont WD, Page DL (1985) Risk factors for breast cancer in women with proliferative breast disease. N Engl J Med 312:146–151PubMedCrossRefGoogle Scholar
  46. 46.
    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 273–301Google Scholar
  47. 47.
    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 51–84Google Scholar
  48. 48.
    Cohen LA (1999) Dietary fiber and breast cancer. Anticancer Res 19:3685–3688PubMedGoogle Scholar
  49. 49.
    Gerber M (1998) Fibre and breast cancer. Eur J Cancer Prev 7:S63–S67CrossRefPubMedGoogle Scholar
  50. 50.
    Goldin BR, Adlercreutz H, Gorbach SL et al (1982) Estrogen excretion patterns and plasma levels in vegetarian and omnivorous women. N Engl J Med 307:1542–1547PubMedCrossRefGoogle Scholar
  51. 51.
    Gorbach SL (1984) Estrogens, breast cancer, and intestinal flora. Rev Infect Dis 6:S85–S90PubMedGoogle Scholar
  52. 52.
    Rose DP (1990) Dietary fiber and breast cancer. Nutr Cancer 13:1–8CrossRefPubMedGoogle Scholar
  53. 53.
    Shultz TD, Howie BJ (1986) In vitro binding of steroid hormones by natural and purified fibers. Nutr Cancer 8:141–147CrossRefPubMedGoogle Scholar
  54. 54.
    Adlercreutz H (2007) Lignans and human health. Crit Rev Clin Lab Sci 44:483–525CrossRefPubMedGoogle Scholar
  55. 55.
    Adlercreutz H, Fotsis T, Bannwart C et al (1986) Determination of urinary lignans and phytoestrogen metabolites, potential antiestrogens and anticarcinogens, in urine of women on various habitual diets. J Steroid Biochem 25:791–797CrossRefPubMedGoogle Scholar
  56. 56.
    Adlercreutz H, Mousavi Y, Clark J et al (1992) Dietary phytoestrogens and cancer: in vitro and in vivo studies. J Steroid Biochem Mol Biol 41:331–337CrossRefPubMedGoogle Scholar
  57. 57.
    Linko AM, Juntunen KS, Mykkanen HM, Adlercreutz H (2005) Whole-grain rye bread consumption by women correlates with plasma alkylresorcinols and increases their concentration compared with low-fiber wheat bread. J Nutr 135:580–583PubMedGoogle Scholar
  58. 58.
    Adlercreutz H, Bannwart C, Wahala K et al (1993) Inhibition of human aromatase by mammalian lignans and isoflavonoid phytoestrogens. J Steroid Biochem Mol Biol 44:147–153CrossRefPubMedGoogle Scholar
  59. 59.
    Goldin BR, Woods MN, Spiegelman DL et al (1994) The effect of dietary fat and fiber on serum estrogen concentrations in premenopausal women under controlled dietary conditions. Cancer 74:1125–1131CrossRefPubMedGoogle Scholar
  60. 60.
    Rose DP, Goldman M, Connolly JM, Strong LE (1991) High-fiber diet reduces serum estrogen concentrations in premenopausal women. Am J Clin Nutr 54:520–525PubMedGoogle Scholar
  61. 61.
    Schaefer EJ, Lamon-Fava S, Spiegelman D et al (1995) Changes in plasma lipoprotein concentrations and composition in response to a low-fat, high-fiber diet are associated with changes in serum estrogen concentrations in premenopausal women. Metabolism 44:749–756CrossRefPubMedGoogle Scholar
  62. 62.
    Dorgan JF, Hunsberger SA, McMahon RP et al (2003) Diet and sex hormones in girls: findings from a randomized controlled clinical trial. J Natl Cancer Inst 95:132–141PubMedGoogle Scholar
  63. 63.
    Kris-Etherton PM, Yu-Poth S, Sabate J, Ratcliffe HE, Zhao G, Etherton TD (1999) Nuts and their bioactive constituents: effects on plasma lipids and other factors that affect disease risk. Am J Clin Nutr 70:504S–511SPubMedGoogle Scholar
  64. 64.
    Kris-Etherton PM, Hu F, Ros E, Sabate J (2008) The role of tree nuts and peanuts in the prevention of coronary heart disease: multiple potential mechanisms. J Nutr 138:1746S–1751SPubMedGoogle Scholar
  65. 65.
    Galvan-Portillo M, Torres-Sanchez L, Lopez-Carrillo L (2002) Dietary and reproductive factors associated with benign breast disease in Mexican women. Nutr Cancer 43:133–140CrossRefPubMedGoogle Scholar
  66. 66.
    Hislop TG, Band PR, Deschamps M et al (1990) Diet and histologic types of benign breast disease defined by subsequent risk of breast cancer. Am J Epidemiol 131:263–270PubMedGoogle Scholar
  67. 67.
    Ingram DM, Nottage E, Roberts T (1991) The role of diet in the development of breast cancer: a case-control study of patients with breast cancer, benign epithelial hyperplasia and fibrocystic disease of the breast. Br J Cancer 64:187–191PubMedGoogle Scholar
  68. 68.
    Cumming RG, Klineberg RJ (1994) A study of the reproducibility of long-term recall in the elderly. Epidemiology 5:116–119CrossRefPubMedGoogle Scholar
  69. 69.
    Frazier AL, Willett WC, Colditz GA (1995) Reproducibility of recall of adolescent diet: Nurses’ Health Study (United States). Cancer Causes Control 6:499–506CrossRefPubMedGoogle Scholar
  70. 70.
    Wolk A, Bergstrom R, Hansson LE, Nyren O (1997) Reliability of retrospective information on diet 20 years ago and consistency of independent measurements of remote adolescent diet. Nutr Cancer 29:234–241CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Xuefen Su
    • 1
    • 2
  • Rulla M. Tamimi
    • 1
    • 2
  • Laura C. Collins
    • 3
  • Heather J. Baer
    • 2
    • 4
  • Eunyoung Cho
    • 1
    • 5
  • Laura Sampson
    • 1
    • 5
  • Walter C. Willett
    • 1
    • 2
    • 5
  • Stuart J. Schnitt
    • 3
  • James L. Connolly
    • 3
  • Bernard A. Rosner
    • 1
    • 6
  • Graham A. Colditz
    • 2
    • 7
  1. 1.Channing Laboratory, Department of MedicineBrigham and Women’s Hospital and Harvard Medical SchoolBostonUSA
  2. 2.Department of EpidemiologyHarvard School of Public HealthBostonUSA
  3. 3.Department of PathologyHarvard Medical School and Beth Israel Deaconess Medical CenterBostonUSA
  4. 4.Division of General MedicineBrigham and Women’s Hospital and Harvard Medical SchoolBostonUSA
  5. 5.Department of NutritionHarvard School of Public HealthBostonUSA
  6. 6.Department of BiostatisticsHarvard School of Public HealthBostonUSA
  7. 7.Alvin J. Siteman Cancer Center and Department of SurgeryWashington University School of MedicineSt. LouisUSA

Personalised recommendations