Breast Cancer Research and Treatment

, Volume 134, Issue 2, pp 479–493

Fruits, vegetables and breast cancer risk: a systematic review and meta-analysis of prospective studies

  • D. Aune
  • D. S. M. Chan
  • A. R. Vieira
  • D. A. Navarro Rosenblatt
  • R. Vieira
  • D. C. Greenwood
  • T. Norat
Review

Abstract

Evidence for an association between fruit and vegetable intake and breast cancer risk is inconclusive. To clarify the association, we conducted a systematic review and meta-analysis of the evidence from prospective studies. We searched PubMed for prospective studies of fruit and vegetable intake and breast cancer risk until April 30, 2011. We included fifteen prospective studies that reported relative risk estimates and 95 % confidence intervals (CIs) of breast cancer associated with fruit and vegetable intake. Random effects models were used to estimate summary relative risks. The summary relative risk (RR) for the highest versus the lowest intake was 0.89 (95 % CI: 0.80–0.99, I2 = 0 %) for fruits and vegetables combined, 0.92 (95 % CI: 0.86–0.98, I2 = 9 %) for fruits, and 0.99 (95 % CI: 0.92–1.06, I2 = 20 %) for vegetables. In dose–response analyses, the summary RR per 200 g/day was 0.96 (95 % CI: 0.93–1.00, I2 = 2 %) for fruits and vegetables combined, 0.94 (95 % CI: 0.89–1.00, I2 = 39 %) for fruits, and 1.00 (95 % CI: 0.95–1.06, I2 = 17 %) for vegetables. In this meta-analysis of prospective studies, high intake of fruits, and fruits and vegetables combined, but not vegetables, is associated with a weak reduction in risk of breast cancer.

Keywords

Fruits Vegetables Breast cancer Systematic review Meta-analysis 

References

  1. 1.
    Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127:2893–2917PubMedCrossRefGoogle Scholar
  2. 2.
    Chia KS, Reilly M, Tan CS et al (2005) Profound changes in breast cancer incidence may reflect changes into a Westernized lifestyle: a comparative population-based study in Singapore and Sweden. Int J Cancer 113:302–306PubMedCrossRefGoogle Scholar
  3. 3.
    Leung GM, Thach TQ, Lam TH et al (2002) Trends in breast cancer incidence in Hong Kong between 1973 and 1999: an age–period–cohort analysis. Br J Cancer 87:982–988PubMedCrossRefGoogle Scholar
  4. 4.
    Kolonel LN (1980) Cancer patterns of four ethnic groups in Hawaii. J Natl Cancer Inst 65:1127–1139PubMedGoogle Scholar
  5. 5.
    Ziegler RG, Hoover RN, Pike MC et al (1993) Migration patterns and breast cancer risk in Asian-American women. J Natl Cancer Inst 85:1819–1827PubMedCrossRefGoogle Scholar
  6. 6.
    World Cancer Research Fund/American Institute for Cancer Research Food, Nutrition, Physical Activity and the Prevention of Cancer: a Global Perspective (2007). AICR, WashingtonGoogle Scholar
  7. 7.
    Maskarinec G, Morimoto Y, Takata Y, Murphy SP, Stanczyk FZ (2006) Alcohol and dietary fibre intakes affect circulating sex hormones among premenopausal women. Public Health Nutr 9:875–881PubMedCrossRefGoogle Scholar
  8. 8.
    Steinmetz KA, Potter JD (1991) Vegetables, fruit, and cancer. II. Mechanisms. Cancer Causes Control 2:427–442PubMedCrossRefGoogle Scholar
  9. 9.
    Vainio H, Weiderpass E (2006) Fruit and vegetables in cancer prevention. Nutr Cancer 54:111–142PubMedCrossRefGoogle Scholar
  10. 10.
    Shibata A, Paganini-Hill A, Ross RK, Henderson BE (1992) Intake of vegetables, fruits, beta-carotene, vitamin C and vitamin supplements and cancer incidence among the elderly: a prospective study. Br J Cancer 66:673–679PubMedCrossRefGoogle Scholar
  11. 11.
    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 4:29–37PubMedCrossRefGoogle Scholar
  12. 12.
    Byrne C, Ursin G, Ziegler RG (1996) A comparison of food habit and food frequency data as predictors of breast cancer in the NHANES I/NHEFS cohort. J Nutr 126:2757–2764PubMedGoogle Scholar
  13. 13.
    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 75:149–155PubMedCrossRefGoogle Scholar
  14. 14.
    Zhang S, Hunter DJ, Forman MR et al (1999) Dietary carotenoids and vitamins A, C, and E and risk of breast cancer. J Natl Cancer Inst 91:547–556PubMedCrossRefGoogle Scholar
  15. 15.
    Key TJ, Sharp GB, Appleby PN et al (1999) Soya foods and breast cancer risk: a prospective study in Hiroshima and Nagasaki, Japan. Br J Cancer 81:1248–1256PubMedCrossRefGoogle Scholar
  16. 16.
    Olsen A, Tjonneland A, Thomsen BL et al (2003) Fruits and vegetables intake differentially affects estrogen receptor negative and positive breast cancer incidence rates. J Nutr 133:2342–2347PubMedGoogle Scholar
  17. 17.
    van Gils CH, Peeters PH, Bueno-de-Mesquita HB et al (2005) Consumption of vegetables and fruits and risk of breast cancer. JAMA 293:183–193PubMedCrossRefGoogle Scholar
  18. 18.
    Sonestedt E, Borgquist S, Ericson U et al (2008) Plant foods and oestrogen receptor alpha- and beta-defined breast cancer: observations from the Malmo Diet and Cancer cohort. Carcinogenesis 29:2203–2209PubMedCrossRefGoogle Scholar
  19. 19.
    Jayalekshmi P, Varughese SC, Kalavathi et al (2009) A nested case-control study of female breast cancer in Karunagappally cohort in Kerala, India. Asian Pac J Cancer Prev 10:241–246PubMedGoogle Scholar
  20. 20.
    Butler LM, Wu AH, Wang R, Koh WP, Yuan JM, Yu MC (2010) A vegetable-fruit-soy dietary pattern protects against breast cancer among postmenopausal Singapore Chinese women. Am J Clin Nutr 91:1013–1019PubMedCrossRefGoogle Scholar
  21. 21.
    Boggs DA, Palmer JR, Wise LA et al (2010) Fruit and vegetable intake in relation to risk of breast cancer in the Black Women’s Health Study. Am J Epidemiol 172:1268–1279PubMedCrossRefGoogle Scholar
  22. 22.
    Brasky TM, Lampe JW, Potter JD, Patterson RE, White E (2010) Specialty supplements and breast cancer risk in the VITamins And Lifestyle (VITAL) Cohort. Cancer Epidemiol Biomarkers Prev 19:1696–1708PubMedCrossRefGoogle Scholar
  23. 23.
    Lof M, Sandin S, Lagiou P, Trichopoulos D, Adami HO, Weiderpass E (2011) Fruit and vegetable intake and risk of cancer in the Swedish women’s lifestyle and health cohort. Cancer Causes Control 22:283–289PubMedCrossRefGoogle Scholar
  24. 24.
    George SM, Park Y, Leitzmann MF et al (2009) Fruit and vegetable intake and risk of cancer: a prospective cohort study. Am J Clin Nutr 89:347–353PubMedCrossRefGoogle Scholar
  25. 25.
    Gandini S, Merzenich H, Robertson C, Boyle P (2000) Meta-analysis of studies on breast cancer risk and diet: the role of fruit and vegetable consumption and the intake of associated micronutrients. Eur J Cancer 36:636–646PubMedCrossRefGoogle Scholar
  26. 26.
    Riboli E, Norat T (2003) Epidemiologic evidence of the protective effect of fruit and vegetables on cancer risk. Am J Clin Nutr 78:559S–569SPubMedGoogle Scholar
  27. 27.
    Michels KB, Mohllajee AP, Roset-Bahmanyar E, Beehler GP, Moysich KB (2007) Diet and breast cancer: a review of the prospective observational studies. Cancer 109:2712–2749PubMedCrossRefGoogle Scholar
  28. 28.
    Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 339:b2535PubMedCrossRefGoogle Scholar
  29. 29.
    Key TJ, Thorogood M, Appleby PN, Burr ML (1996) Dietary habits and mortality in 11,000 vegetarians and health conscious people: results of a 17 year follow up. BMJ 313:775–779PubMedCrossRefGoogle Scholar
  30. 30.
    Appleby PN, Key TJ, Burr ML, Thorogood M (2002) Mortality and fresh fruit consumption. IARC Sci Publ 156:131–133PubMedGoogle Scholar
  31. 31.
    Sauvaget C, Nagano J, Hayashi M, Spencer E, Shimizu Y, Allen N (2003) Vegetables and fruit intake and cancer mortality in the Hiroshima/Nagasaki Life Span Study. Br J Cancer 88:689–694PubMedCrossRefGoogle Scholar
  32. 32.
    Maynard M, Gunnell D, Emmett P, Frankel S, Davey SG (2003) Fruit, vegetables, and antioxidants in childhood and risk of adult cancer: the Boyd Orr cohort. J Epidemiol Community Health 57:218–225PubMedCrossRefGoogle Scholar
  33. 33.
    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 90:122–127PubMedCrossRefGoogle Scholar
  34. 34.
    Mattisson I, Wirfalt E, Wallstrom P, Gullberg B, Olsson H, Berglund G (2004) High fat and alcohol intakes are risk factors of postmenopausal breast cancer: a prospective study from the Malmo diet and cancer cohort. Int J Cancer 110:589–597PubMedCrossRefGoogle Scholar
  35. 35.
    Fung TT, Hu FB, Holmes MD et al (2005) Dietary patterns and the risk of postmenopausal breast cancer. Int J Cancer 116:116–121PubMedCrossRefGoogle Scholar
  36. 36.
    Ravn-Haren G, Olsen A, Tjonneland A et al (2006) Associations between GPX1 Pro198Leu polymorphism, erythrocyte GPX activity, alcohol consumption and breast cancer risk in a prospective cohort study. Carcinogenesis 27:820–825PubMedCrossRefGoogle Scholar
  37. 37.
    Sonestedt E, Gullberg B, Wirfalt E (2007) Both food habit change in the past and obesity status may influence the association between dietary factors and postmenopausal breast cancer. Public Health Nutr 10:769–779PubMedCrossRefGoogle Scholar
  38. 38.
    Trichopoulou A, Bamia C, Lagiou P, Trichopoulos D (2010) Conformity to traditional Mediterranean diet and breast cancer risk in the Greek EPIC (European Prospective Investigation into Cancer and Nutrition) cohort. Am J Clin Nutr 92:620–625PubMedCrossRefGoogle Scholar
  39. 39.
    Frazier AL, Li L, Cho E, Willett WC, Colditz GA (2004) Adolescent diet and risk of breast cancer. Cancer Causes Control 15:73–82PubMedCrossRefGoogle Scholar
  40. 40.
    DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7:177–188PubMedCrossRefGoogle Scholar
  41. 41.
    Greenland S, Longnecker MP (1992) Methods for trend estimation from summarized dose-response data, with applications to meta-analysis. Am J Epidemiol 135:1301–1309PubMedGoogle Scholar
  42. 42.
    Bandera EV, Kushi LH, Moore DF, Gifkins DM, McCullough ML (2007) Fruits and vegetables and endometrial cancer risk: a systematic literature review and meta-analysis. Nutr Cancer 58:6–21PubMedCrossRefGoogle Scholar
  43. 43.
    Royston P (2000) A strategy for modelling the effect of a continuous covariate in medicine and epidemiology. Stat Med 19:1831–1847PubMedCrossRefGoogle Scholar
  44. 44.
    Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558PubMedCrossRefGoogle Scholar
  45. 45.
    Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634Google Scholar
  46. 46.
    Smith-Warner SA, Spiegelman D, Yaun SS et al (2001) Intake of fruits and vegetables and risk of breast cancer: a pooled analysis of cohort studies. JAMA 285:769–776PubMedCrossRefGoogle Scholar
  47. 47.
    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 74:1125–1131PubMedCrossRefGoogle Scholar
  48. 48.
    Toniolo P, Van Kappel AL, Akhmedkhanov A et al (2001) Serum carotenoids and breast cancer. Am J Epidemiol 153:1142–1147PubMedCrossRefGoogle Scholar
  49. 49.
    Sato R, Helzlsouer KJ, Alberg AJ, Hoffman SC, Norkus EP, Comstock GW (2002) Prospective study of carotenoids, tocopherols, and retinoid concentrations and the risk of breast cancer. Cancer Epidemiol Biomarkers Prev 11:451–457PubMedGoogle Scholar
  50. 50.
    Tamimi RM, Hankinson SE, Campos H et al (2005) Plasma carotenoids, retinol, and tocopherols and risk of breast cancer. Am J Epidemiol 161:153–160PubMedCrossRefGoogle Scholar
  51. 51.
    Fowke JH, Chung FL, Jin F et al (2003) Urinary isothiocyanate levels, brassica, and human breast cancer. Cancer Res 63:3980–3986PubMedGoogle Scholar
  52. 52.
    He K, Hu FB, Colditz GA, Manson JE, Willett WC, Liu S (2004) Changes in intake of fruits and vegetables in relation to risk of obesity and weight gain among middle-aged women. Int J Obes Relat Metab Disord 28:1569–1574PubMedCrossRefGoogle Scholar
  53. 53.
    Aune D, Lau R, Chan DS et al (2011) Nonlinear reduction in risk for colorectal cancer by fruit and vegetable intake based on meta-analysis of prospective studies. Gastroenterology 141:106–118PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC. 2012

Authors and Affiliations

  • D. Aune
    • 1
  • D. S. M. Chan
    • 1
  • A. R. Vieira
    • 1
  • D. A. Navarro Rosenblatt
    • 1
  • R. Vieira
    • 1
  • D. C. Greenwood
    • 2
  • T. Norat
    • 1
  1. 1.Department of Epidemiology and Biostatistics, School of Public HealthImperial College LondonLondonUK
  2. 2.Biostatistics Unit, Centre for Epidemiology and BiostatisticsUniversity of LeedsLeedsUK

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