Skip to main content

Advertisement

SpringerLink
Log in

Healthy dietary patterns and risk of breast cancer by molecular subtype

  • Epidemiology
  • Published:
Breast Cancer Research and Treatment Aims and scope Submit manuscript

Abstract

We examined associations between dietary quality indices and breast cancer risk by molecular subtype among 100,643 women in the prospective Nurses’ Health Study (NHS) cohort, followed from 1984 to 2006. Dietary quality scores for the Alternative Healthy Eating Index (AHEI), alternate Mediterranean diet (aMED), and Dietary Approaches to Stop Hypertension (DASH) dietary patterns were calculated from semi-quantitative food frequency questionnaires collected every 2–4 years. Breast cancer molecular subtypes were defined according to estrogen receptor (ER), progesterone receptor, human epidermal growth factor 2 (HER2), cytokeratin 5/6 (CK5/6), and epidermal growth factor receptor status from immunostained tumor microarrays in combination with histologic grade. Cox proportional hazards models, adjusted for age and breast cancer risk factors, were used to estimate hazard ratios (HRs) and 95 % confidence intervals (CIs). Competing risk analyses were used to assess heterogeneity by subtype. We did not observe any significant associations between the AHEI or aMED dietary patterns and risk of breast cancer by molecular subtype. However, a significantly reduced risk of HER2-type breast cancer was observed among women in 5th versus 1st quintile of the DASH dietary pattern [n = 134 cases, Q5 vs. Q1 HR (95 % CI) = 0.44 (0.25–0.77)], and the inverse trend across quintiles was significant (p trend = 0.02). We did not observe any heterogeneity in associations between AHEI (p het = 0.25), aMED (p het = 0.71), and DASH (p het = 0.12) dietary patterns and breast cancer by subtype. Adherence to the AHEI, aMED, and DASH dietary patterns was not strongly associated with breast cancer molecular subtypes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M et al (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:E359–E386

    Article  CAS  PubMed  Google Scholar 

  2. Smith-Warner SA, Spiegelman D, Yaun SS, van den Brandt PA, Folsom AR, Goldbohm RA et al (1998) Alcohol and breast cancer in women: a pooled analysis of cohort studies. JAMA 279:535–540

    Article  CAS  PubMed  Google Scholar 

  3. Jung S, Spiegelman D, Baglietto L, Bernstein L, Boggs DA, van den Brandt PA et al (2013) Fruit and vegetable intake and risk of breast cancer by hormone receptor status. J Natl Cancer Inst 105:219–236

    Article  PubMed Central  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. van Gils CH, Peeters PH, Bueno-de-Mesquita HB, Boshuizen HC, Lahmann PH, Clavel-Chapelon F et al (2005) Consumption of vegetables and fruits and risk of breast cancer. JAMA 293:183–193

    Article  PubMed  Google Scholar 

  6. Hunter DJ, Spiegelman D, Adami HO, Beeson L, van den Brandt PA, Folsom AR et al (1996) Cohort studies of fat intake and the risk of breast cancer—a pooled analysis. N Engl J Med 334:356–361

    Article  CAS  PubMed  Google Scholar 

  7. Hu FB (2002) Dietary pattern analysis: a new direction in nutritional epidemiology. Curr Opin Lipidol 13:3–9

    Article  CAS  PubMed  Google Scholar 

  8. Adebamowo CA, Hu FB, Cho E, Spiegelman D, Holmes MD, Willett WC (2005) Dietary patterns and the risk of breast cancer. Ann Epidemiol 15:789–795

    Article  PubMed  Google Scholar 

  9. Fung TT, Hu FB, Holmes MD, Rosner BA, Hunter DJ, Colditz GA et al (2005) Dietary patterns and the risk of postmenopausal breast cancer. Int J Cancer 116:116–121

    Article  CAS  PubMed  Google Scholar 

  10. Mannisto S, Dixon LB, Balder HF, Virtanen MJ, Krogh V, Khani BR et al (2005) Dietary patterns and breast cancer risk: results from three cohort studies in the DIETSCAN project. Cancer Causes Control 16:725–733

    Article  PubMed  Google Scholar 

  11. Schulz M, Hoffmann K, Weikert C, Nothlings U, Schulze MB, Boeing H (2008) Identification of a dietary pattern characterized by high-fat food choices associated with increased risk of breast cancer: the European Prospective Investigation into Cancer and Nutrition [EPIC]-Potsdam Study. Br J Nutr 100:942–946

    Article  CAS  PubMed  Google Scholar 

  12. Sieri S, Krogh V, Pala V, Muti P, Micheli A, Evangelista A et al (2004) Dietary patterns and risk of breast cancer in the ORDET cohort. Cancer Epidemiol Biomarkers Prev 13:567–572

    PubMed  Google Scholar 

  13. Terry P, Suzuki R, Hu FB, Wolk A (2001) A prospective study of major dietary patterns and the risk of breast cancer. Cancer Epidemiol Biomarkers Prev 10:1281–1285

    CAS  PubMed  Google Scholar 

  14. Link LB, Canchola AJ, Bernstein L, Clarke CA, Stram DO, Ursin G et al (2013) Dietary patterns and breast cancer risk in the California Teachers Study cohort. Am J Clin Nutr 98:1524–1532

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Sant M, Allemani C, Sieri S, Krogh V, Menard S, Tagliabue E et al (2007) Salad vegetables dietary pattern protects against HER-2-positive breast cancer: a prospective Italian study. Int J Cancer 121:911–914

    Article  CAS  PubMed  Google Scholar 

  16. Velie EM, Schairer C, Flood A, He JP, Khattree R, Schatzkin A (2005) Empirically derived dietary patterns and risk of postmenopausal breast cancer in a large prospective cohort study. Am J Clin Nutr 82:1308–1319

    CAS  PubMed  Google Scholar 

  17. Cui X, Dai Q, Tseng M, Shu XO, Gao YT, Zheng W (2007) Dietary patterns and breast cancer risk in the shanghai breast cancer study. Cancer Epidemiol Biomarkers Prev 16:1443–1448

    Article  CAS  PubMed  Google Scholar 

  18. Edefonti V, Decarli A, La Vecchia C, Bosetti C, Randi G, Franceschi S et al (2008) Nutrient dietary patterns and the risk of breast and ovarian cancers. Int J Cancer 122:609–613

    Article  CAS  PubMed  Google Scholar 

  19. Franceschi S, Favero A, La Vecchia C, Negri E, Dal Maso L, Salvini S et al (1995) Influence of food groups and food diversity on breast cancer risk in Italy. Int J Cancer 63:785–789

    Article  CAS  PubMed  Google Scholar 

  20. Karimi Z, Jessri M, Houshiar-Rad A, Mirzaei HR, Rashidkhani B (2014) Dietary patterns and breast cancer risk among women. Public Health Nutr 17:1098–1106

    Article  PubMed  Google Scholar 

  21. Hirose K, Matsuo K, Iwata H, Tajima K (2007) Dietary patterns and the risk of breast cancer in Japanese women. Cancer Sci 98:1431–1438

    Article  CAS  PubMed  Google Scholar 

  22. McCann SE, McCann WE, Hong CC, Marshall JR, Edge SB, Trevisan M et al (2007) Dietary patterns related to glycemic index and load and risk of premenopausal and postmenopausal breast cancer in the Western New York Exposure and Breast Cancer Study. Am J Clin Nutr 86:465–471

    PubMed Central  CAS  PubMed  Google Scholar 

  23. Murtaugh MA, Sweeney C, Giuliano AR, Herrick JS, Hines L, Byers T et al (2008) Diet patterns and breast cancer risk in Hispanic and non-Hispanic white women: the Four-Corners Breast Cancer Study. Am J Clin Nutr 87:978–984

    PubMed Central  CAS  PubMed  Google Scholar 

  24. Ronco AL, De Stefani E, Boffetta P, Deneo-Pellegrini H, Acosta G, Mendilaharsu M (2006) Food patterns and risk of breast cancer: a factor analysis study in Uruguay. Int J Cancer 119:1672–1678

    Article  CAS  PubMed  Google Scholar 

  25. Fung TT, Hu FB, McCullough ML, Newby PK, Willett WC, Holmes MD (2006) Diet quality is associated with the risk of estrogen receptor-negative breast cancer in postmenopausal women. J Nutr 136:466–472

    CAS  PubMed  Google Scholar 

  26. Nkondjock A, Ghadirian P (2007) Diet quality and BRCA-associated breast cancer risk. Breast Cancer Res Treat 103:361–369

    Article  CAS  PubMed  Google Scholar 

  27. Castello A, Pollan M, Buijsse B, Ruiz A, Casas AM, Baena-Canada JM et al (2014) Spanish Mediterranean diet and other dietary patterns and breast cancer risk: case–control EpiGEICAM study. Br J Cancer 111:1454–1462

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  28. Albuquerque RC, Baltar VT, Marchioni DM (2014) Breast cancer and dietary patterns: a systematic review. Nutr Rev 72:1–17

    Article  PubMed  Google Scholar 

  29. Couto E, Sandin S, Lof M, Ursin G, Adami HO, Weiderpass E (2013) Mediterranean dietary pattern and risk of breast cancer. PLoS ONE 8:e55374

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Mourouti N, Kontogianni MD, Papavagelis C, Plytzanopoulou P, Vassilakou T, Malamos N et al (2014) Adherence to the Mediterranean diet is associated with lower likelihood of breast cancer: a case–control study. Nutr Cancer 66:810–817

    Article  CAS  PubMed  Google Scholar 

  31. Mourouti N, Papavagelis C, Plytzanopoulou P, Kontogianni M, Vassilakou T, Malamos N et al (2014) Dietary patterns and breast cancer: a case–control study in women. Eur J Nutr 54:609–617

    Article  PubMed  Google Scholar 

  32. Tamimi RM, Colditz GA, Hazra A, Baer HJ, Hankinson SE, Rosner B et al (2012) Traditional breast cancer risk factors in relation to molecular subtypes of breast cancer. Breast Cancer Res Treat 131:159–167

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  33. Perou CM, Jeffrey SS, van de Rijn M, Rees CA, Eisen MB, Ross DT et al (1999) Distinctive gene expression patterns in human mammary epithelial cells and breast cancers. Proc Natl Acad Sci USA 96:9212–9217

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H et al (2001) Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 98:10869–10874

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. Sorlie T, Tibshirani R, Parker J, Hastie T, Marron JS, Nobel A et al (2003) Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci USA 100:8418–8423

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. Brenton JD, Carey LA, Ahmed AA, Caldas C (2005) Molecular classification and molecular forecasting of breast cancer: ready for clinical application? J Clin Oncol 23:7350–7360

    Article  CAS  PubMed  Google Scholar 

  37. Willett WC, Sampson L, Stampfer MJ, Rosner B, Bain C, Witschi J et al (1985) Reproducibility and validity of a semiquantitative food frequency questionnaire. Am J Epidemiol 122:51–65

    CAS  PubMed  Google Scholar 

  38. Feskanich D, Rimm EB, Giovannucci EL, Colditz GA, Stampfer MJ, Litin LB et al (1993) Reproducibility and validity of food intake measurements from a semiquantitative food frequency questionnaire. J Am Diet Assoc 93:790–796

    Article  CAS  PubMed  Google Scholar 

  39. Chiuve SE, Fung TT, Rimm EB, Hu FB, McCullough ML, Wang M et al (2012) Alternative dietary indices both strongly predict risk of chronic disease. J Nutr 142:1009–1018

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  40. Trichopoulou A, Costacou T, Bamia C, Trichopoulos D (2003) Adherence to a Mediterranean diet and survival in a Greek population. N Engl J Med 348:2599–2608

    Article  PubMed  Google Scholar 

  41. Trichopoulou A, Kouris-Blazos A, Wahlqvist ML, Gnardellis C, Lagiou P, Polychronopoulos E et al (1995) Diet and overall survival in elderly people. BMJ 311:1457–1460

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  42. Fung TT, McCullough ML, Newby PK, Manson JE, Meigs JB, Rifai N et al (2005) Diet-quality scores and plasma concentrations of markers of inflammation and endothelial dysfunction. Am J Clin Nutr 82:163–173

    CAS  PubMed  Google Scholar 

  43. United States Department of Health and Human Services NIoH, National Heart Lung, and Blood Institute (2006) Your guide to lowering your blood pressure with DASH. http://www.nhlbi.nih.gov/health/resources/heart/hbp-dash-index. Accessed 15 Sep 2015

  44. Sacks FM (1995) Dietary approaches to stop hypertension. Ann Epidemiol 5:502

    Article  CAS  PubMed  Google Scholar 

  45. Fung TT, Chiuve SE, McCullough ML, Rexrode KM, Logroscino G, Hu FB (2008) Adherence to a DASH-style diet and risk of coronary heart disease and stroke in women. Arch Intern Med 168:713–720

    Article  PubMed  Google Scholar 

  46. Tamimi RM, Baer HJ, Marotti J, Galan M, Galaburda L, Fu Y et al (2008) Comparison of molecular phenotypes of ductal carcinoma in situ and invasive breast cancer. Breast Cancer Res 10:R67

    Article  PubMed Central  PubMed  Google Scholar 

  47. Collins LC, Marotti JD, Baer HJ, Tamimi RM (2008) Comparison of estrogen receptor results from pathology reports with results from central laboratory testing. J Natl Cancer Inst 100:218–221

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  48. Collins LC, Botero ML, Schnitt SJ (2005) Bimodal frequency distribution of estrogen receptor immunohistochemical staining results in breast cancer: an analysis of 825 cases. Am J Clin Pathol 123:16–20

    Article  PubMed  Google Scholar 

  49. Nielsen TO, Hsu FD, Jensen K, Cheang M, Karaca G, Hu Z et al (2004) Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. Clin Cancer Res 10:5367–5374

    Article  CAS  PubMed  Google Scholar 

  50. Abd El-Rehim DM, Ball G, Pinder SE, Rakha E, Paish C, Robertson JF et al (2005) High-throughput protein expression analysis using tissue microarray technology of a large well-characterised series identifies biologically distinct classes of breast cancer confirming recent cDNA expression analyses. Int J Cancer 116:340–350

    Article  CAS  PubMed  Google Scholar 

  51. Abd El-Rehim DM, Pinder SE, Paish CE, Bell J, Blamey RW, Robertson JF et al (2004) Expression of luminal and basal cytokeratins in human breast carcinoma. J Pathol. 203:661–671

    Article  PubMed  Google Scholar 

  52. van de Rijn M, Perou CM, Tibshirani R, Haas P, Kallioniemi O, Kononen J et al (2002) Expression of cytokeratins 17 and 5 identifies a group of breast carcinomas with poor clinical outcome. Am J Pathol 161:1991–1996

    Article  PubMed Central  PubMed  Google Scholar 

  53. Millikan RC, Newman B, Tse CK, Moorman PG, Conway K, Dressler LG et al (2008) Epidemiology of basal-like breast cancer. Breast Cancer Res Treat 109:123–139

    Article  PubMed Central  PubMed  Google Scholar 

  54. Yang XR, Sherman ME, Rimm DL, Lissowska J, Brinton LA, Peplonska B et al (2007) Differences in risk factors for breast cancer molecular subtypes in a population-based study. Cancer Epidemiol Biomarkers Prev. 16:439–443

    Article  CAS  PubMed  Google Scholar 

  55. Lunn M, McNeil D (1995) Applying Cox regression to competing risks. Biometrics 51:524–532

    Article  CAS  PubMed  Google Scholar 

  56. Fung TT, Chiuve SE, Willett WC, Hankinson SE, Hu FB, Holmes MD (2013) Intake of specific fruits and vegetables in relation to risk of estrogen receptor-negative breast cancer among postmenopausal women. Breast Cancer Res Treat 138:925–930

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  57. Fung TT, Hu FB, Barbieri RL, Willett WC, Hankinson SE (2007) Dietary patterns, the Alternate Healthy Eating Index and plasma sex hormone concentrations in postmenopausal women. Int J Cancer 121:803–809

    Article  CAS  PubMed  Google Scholar 

  58. Smith-Warner SA, Spiegelman D, Yaun SS, Adami HO, Beeson WL, van den Brandt PA et al (2001) Intake of fruits and vegetables and risk of breast cancer: a pooled analysis of cohort studies. JAMA 285:769–776

    Article  CAS  PubMed  Google Scholar 

  59. Boggs DA, Palmer JR, Wise LA, Spiegelman D, Stampfer MJ, Adams-Campbell LL et al (2010) Fruit and vegetable intake in relation to risk of breast cancer in the Black Women’s Health Study. Am J Epidemiol 172:1268–1279

    Article  PubMed Central  PubMed  Google Scholar 

  60. Zhang X, Spiegelman D, Baglietto L, Bernstein L, Boggs DA, van den Brandt PA 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  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  62. Schwingshackl L, Hoffmann G (2014) Adherence to Mediterranean diet and risk of cancer: a systematic review and meta-analysis of observational studies. Int J Cancer 135:1884–1897

    Article  CAS  PubMed  Google Scholar 

  63. Schwingshackl L, Hoffmann G (2015) Diet quality as assessed by the healthy eating index, the alternate healthy eating index, the dietary approaches to stop hypertension score, and health outcomes: a systematic review and meta-analysis of cohort studies. J Acad Nutr Diet. 115(780–800):e5

    PubMed  Google Scholar 

  64. Bosire C, Stampfer MJ, Subar AF, Park Y, Kirkpatrick SI, Chiuve SE et al (2013) Index-based dietary patterns and the risk of prostate cancer in the NIH-AARP diet and health study. Am J Epidemiol 177:504–513

    Article  PubMed Central  PubMed  Google Scholar 

  65. Belin RJ, Greenland P, Allison M, Martin L, Shikany JM, Larson J et al (2011) Diet quality and the risk of cardiovascular disease: the Women’s Health Initiative [WHI]. Am J Clin Nutr 94:49–57

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  66. Farvid MS, Cho E, Chen WY, Eliassen AH, Willett WC (2015) Adolescent meat intake and breast cancer risk. Int J Cancer 136:1909–1920

    Article  CAS  PubMed  Google Scholar 

  67. 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 145:461–470

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  68. Linos E, Willett WC, Cho E, Frazier L (2010) Adolescent diet in relation to breast cancer risk among premenopausal women. Cancer Epidemiol Biomarkers Prev. 19:689–696

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by the NIH UM1 CA186107 (Meir Stampfer) and P01 CA087969 (Meir Stampfer). KA Hirko is supported by the R25 CA098566 and the T32 CA009001 training grants. We would like to thank the participants and staff of the Nurses’ Health Study 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, and WY. The authors assume full responsibility for analyses and interpretation of these data.

Author information

Authors and Affiliations

  1. Department of Epidemiology and Biostatistics, Michigan State University, 909 Fee Road, East Lansing, MI, 48824, USA

    Kelly A. Hirko

  2. Channing Division of Network Medicine, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, 909 Fee Road, Boston, MA, 02115, USA

    Walter C. Willett, Susan E. Hankinson, Bernard A. Rosner, Rulla M. Tamimi & A. Heather Eliassen

  3. Department of Epidemiology, Harvard T.H. Chan School of Public Health, 909 Fee Road, Boston, MA, USA

    Walter C. Willett, Susan E. Hankinson, Rulla M. Tamimi & A. Heather Eliassen

  4. Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, MA, USA

    Walter C. Willett

  5. Department of Biostatistics and Epidemiology, University of Massachusetts, Amherst, MA, USA

    Susan E. Hankinson

  6. Department of Pathology, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, MA, USA

    Andrew H. Beck

Authors
  1. Kelly A. Hirko
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Walter C. Willett
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Susan E. Hankinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bernard A. Rosner
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andrew H. Beck
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rulla M. Tamimi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. A. Heather Eliassen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kelly A. Hirko.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

The analysis presented here complies with current laws of the country in which they were performed.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 16 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hirko, K.A., Willett, W.C., Hankinson, S.E. et al. Healthy dietary patterns and risk of breast cancer by molecular subtype. Breast Cancer Res Treat 155, 579–588 (2016). https://doi.org/10.1007/s10549-016-3706-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10549-016-3706-2

Keywords

Search

Navigation