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Breast Cancer Research and Treatment

, Volume 170, Issue 3, pp 613–622 | Cite as

An estrogen-related lifestyle score is associated with risk of postmenopausal breast cancer in the PLCO cohort

  • Mark A. Guinter
  • Alexander C. McLain
  • Anwar T. Merchant
  • Dale P. Sandler
  • Susan E. Steck
Epidemiology

Abstract

Purpose

Healthy or unhealthy lifestyle behaviors are often adopted together. We aimed to investigate the combined effect of estrogen-related lifestyle factors on postmenopausal breast cancer risk.

Methods

Data from 27,153 women enrolled in the Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial were used. We created an estrogen-related lifestyle score (ERLS) by incorporating a previously developed measure of estrogenic diet, alcohol intake, body mass index (BMI), and physical activity. The scores ranged from 0 to 6 with alcohol and BMI accounting for higher weights than the other factors. To evaluate the preventive possibilities of a low estrogen-related lifestyle and to be consistent with other published lifestyle scores, higher scores were set to correspond with potentially lower estrogenic lifestyle. The association between the ERLS and incident breast cancer was examined using Cox proportional hazards models.

Results

Participants with an ERLS of 4 or ≥ 5 had a 23% (HR 0.77; 95% CI 0.67–0.89) and 34% (HR 0.66; 95% CI 0.56–0.78) lower risk of breast cancer, respectively, compared to those with an ERLS ≤ 2 after multivariable adjustment. Estimates were similar when restricting to invasive cases or estrogen receptor-positive subtypes. No single lifestyle component appeared to drive the association.

Conclusions

Our findings suggest that the combined effect of a lifestyle characterized by a low estrogenic diet, low alcohol consumption, low body weight, and high levels of physical activity are associated with a reduction in postmenopausal breast cancer risk, possibly through an influence on estrogen metabolism.

Keywords

Breast cancer Lifestyle score Estrogen metabolism Behavior Epidemiology Prospective cohort study 

Abbreviations

2/16

Ratio of 2- to 16-hydroxylated estrogen metabolites

AICR

American Institute for Cancer Research

BMI

Body mass index

CI

Confidence interval

CUP

Continuous Update Project

DQX

Dietary questionnaire

E2

Estradiol

EM

Estrogen metabolites

EPIC

European Prospective Investigation into Cancer and Nutrition

ER

Estrogen receptor

ERDP

Estrogen-related dietary pattern

ERLS

Estrogen-related lifestyle score

HR

Hazard ratio

OR

Odds ratio

PA

Physical activity

PMH

Postmenopausal hormone

PR

Progesterone receptor

PLCO

Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial

SD

Standard deviation

USDA

United States Department of Agriculture

WCRF

World Cancer Research Fund

Notes

Acknowledgements

This work was made possible in part by Grant Number T32-GM081740 from NIH-NIGMS. DPS is supported by the Intramural Research Program of the NIH, National Institute of Environmental Health Sciences (Z01 ES-044005 l). Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the NIGMS or NIH.

Compliance with ethical standards

Conflict of interest

The authors do not declare any conflicts of interest.

Supplementary material

10549_2018_4784_MOESM1_ESM.docx (28 kb)
Supplementary material 1 (DOCX 28 kb)
10549_2018_4784_MOESM2_ESM.docx (12 kb)
Supplementary material 2 (DOCX 11 kb)

References

  1. 1.
    Siegel RL, Miller KD, Jemal A (2017) Cancer statistics, 2017. CA Cancer J Clin 67:7–30.  https://doi.org/10.3322/caac.21387 CrossRefPubMedGoogle Scholar
  2. 2.
    American Cancer Society (2015) Breast cancer facts & figures 2015-2016. American Cancer Society, AtlantaGoogle Scholar
  3. 3.
    World Cancer Research Fund/American Institute for Cancer Research (2007) Food, nutrition, physical activity, and the prevention of cancer: a global perspective. World Cancer Research Fund/American Institute for Cancer Research, Washington, DCGoogle Scholar
  4. 4.
    Continuous Update Project Report (2017) Diet, nutrition, physical activity and breast cancerGoogle Scholar
  5. 5.
    Brennan SF, Cantwell MM, Cardwell CR, Velentzis LS, Woodside JV (2010) Dietary patterns and breast cancer risk: a systematic review and meta-analysis. Am J Clin Nutr 91:1294–1302.  https://doi.org/10.3945/ajcn.2009.28796 CrossRefPubMedGoogle Scholar
  6. 6.
    Mourouti N, Kontogianni MD, Papavagelis C, Panagiotakos DB (2015) Diet and breast cancer: a systematic review. Int J Food Sci Nutr 66:1–42.  https://doi.org/10.3109/09637486.2014.950207 CrossRefPubMedGoogle Scholar
  7. 7.
    Stampfer MJ, Hu FB, Manson JE, Rimm EB, Willett WC (2000) Primary prevention of coronary heart disease in women through diet and lifestyle. N Engl J Med 343:16–22.  https://doi.org/10.1056/NEJM200007063430103 CrossRefPubMedGoogle Scholar
  8. 8.
    Romaguera D, Vergnaud A-C, Peeters PH, van Gils CH, Chan DS, Ferrari P et al (2012) Is concordance with World Cancer Research Fund/American Institute for Cancer Research guidelines for cancer prevention related to subsequent risk of cancer? Results from the EPIC study. Am J Clin Nutr 96:150–163.  https://doi.org/10.3945/ajcn.111.031674 CrossRefPubMedGoogle Scholar
  9. 9.
    Sánchez-Zamorano LM, Flores-Luna L, Ángeles-Llerenas A, Romieu I, Lazcano-Ponce E, Miranda-Hernández H et al (2011) Healthy lifestyle on the risk of breast cancer. Cancer Epidemiol Prev Biomarkers 20(5):912–922CrossRefGoogle Scholar
  10. 10.
    McKenzie F, Ferrari P, Freisling H, Chajès V, Rinaldi S, de Batlle J et al (2015) Healthy lifestyle and risk of breast cancer among postmenopausal women in the European Prospective Investigation into Cancer and Nutrition cohort study. Int J Cancer 136:2640–2648.  https://doi.org/10.1002/ijc.29315 CrossRefPubMedGoogle Scholar
  11. 11.
    McKenzie F, Ellison-Loschmann L, Jeffreys M, Firestone R, Pearce N, Romieu I (2014) Healthy lifestyle and risk of breast cancer for indigenous and non-indigenous women in New Zealand: a case control study. BMC Cancer 14:12.  https://doi.org/10.1186/1471-2407-14-12 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    McKenzie F, Biessy C, Ferrari P, Freisling H, Rinaldi S, Chajès V et al (2016) Healthy lifestyle and risk of cancer in the European Prospective Investigation into Cancer and Nutrition Cohort Study. Medicine (Baltimore) 95:e2850.  https://doi.org/10.1097/MD.0000000000002850 CrossRefGoogle Scholar
  13. 13.
    Romaguera D, Gracia-Lavedan E, Molinuevo A, de Batlle J, Mendez M, Moreno V et al (2017) Adherence to nutrition-based cancer prevention guidelines and breast, prostate and colorectal cancer risk in the MCC-Spain case-control study. Int J Cancer 141:83–93.  https://doi.org/10.1002/ijc.30722 CrossRefPubMedGoogle Scholar
  14. 14.
    Nomura SJO, Inoue-Choi M, Lazovich D, Robien K (2016) WCRF/AICR recommendation adherence and breast cancer incidence among postmenopausal women with and without non-modifiable risk factors. Int J Cancer 138:2602–2615.  https://doi.org/10.1002/ijc.29994 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Harris HR, Bergkvist L, Wolk A (2016) Adherence to the World Cancer Research Fund/American Institute for Cancer Research recommendations and breast cancer risk. Int J Cancer 138:2657–2664.  https://doi.org/10.1002/ijc.30015 CrossRefPubMedGoogle Scholar
  16. 16.
    Samavat H, Kurzer MS (2015) Estrogen metabolism and breast cancer. Cancer Lett 356:231–243.  https://doi.org/10.1016/j.canlet.2014.04.018 CrossRefPubMedGoogle Scholar
  17. 17.
    Hankinson SE, Willett WC, Manson JE, Hunter DJ, Colditz GA, Stampfer MJ et al (1995) Alcohol, height, and adiposity in relation to estrogen and prolactin levels in postmenopausal women. J Natl Cancer Inst 87:1297–1302.  https://doi.org/10.1093/JNCI/87.17.1297 CrossRefPubMedGoogle Scholar
  18. 18.
    Choudhury F, Bernstein L, Hodis HN, Stanczyk FZ, Mack WJ (2011) Physical activity and sex hormone levels in estradiol- and placebo-treated postmenopausal women. Menopause 18:1079–1086.  https://doi.org/10.1097/gme.0b013e318215f7bd CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Harris HR, Bergkvist L, Wolk A (2015) An estrogen-associated dietary pattern and breast cancer risk in the Swedish Mammography Cohort. Int J Cancer 137:2149–2154.  https://doi.org/10.1002/ijc.29586 CrossRefPubMedGoogle Scholar
  20. 20.
    Guinter MA, McLain AC, Merchant AT, Sandler DP, Steck SE (2018) A dietary pattern based on estrogen metabolism is associated with breast cancer risk in a prospective cohort of postmenopausal women. Int J Cancer.  https://doi.org/10.1002/ijc.31387 PubMedGoogle Scholar
  21. 21.
    Fung TT, Schulze MB, Hu FB, Hankinson SE, Holmes MD (2012) A dietary pattern derived to correlate with estrogens and risk of postmenopausal breast cancer. Breast Cancer Res Treat 132:1157–1162.  https://doi.org/10.1007/s10549-011-1942-z CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Prorok PC, Andriole GL, Bresalier RS, Buys SS, Chia D, Crawford ED et al (2000) Design of the Prostate, Lung, Colorectal and Ovarian (PLCO) Cancer Screening Trial. Control Clin Trials 21:273S–309SCrossRefPubMedGoogle Scholar
  23. 23.
    Fuhrman BJ, Schairer C, Gail MH, Boyd-Morin J, Xu X, Sue LY et al (2012) Estrogen metabolism and risk of breast cancer in postmenopausal women. J Natl Cancer Inst 104:326–339.  https://doi.org/10.1093/jnci/djr531 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Tippett KS, Cypel YS (1997) Design and operation: the continuing survey of food intakes by individuals and the diet and health knowledge survey 1994–96. National Food Survey Report. USDA-Agricultural Research Service, Maryland, p 96Google Scholar
  25. 25.
    US Department of Health and Human Services (2015) 2015–2020 dietary guidelines for Americans, 8th edn. US Department of Health and Human Services, Washington, DCGoogle Scholar
  26. 26.
    Hayes RB, Sigurdson A, Moore L, Peters U, Huang W-Y, Pinsky P et al (2005) Methods for etiologic and early marker investigations in the PLCO trial. Mutat Res 592:147–154.  https://doi.org/10.1016/j.mrfmmm.2005.06.013 CrossRefPubMedGoogle Scholar
  27. 27.
    Cox DR (1972) Regression models and life-tables. J R Stat Soc B 34:187–220.  https://doi.org/10.2307/2985181 Google Scholar
  28. 28.
    Schoenfeld D (1982) Partial residuals for the proportional hazards regression model. Biometrika 69:239–241.  https://doi.org/10.1093/biomet/69.1.239 CrossRefGoogle Scholar
  29. 29.
    Lunn M, McNeil D (1995) Applying cox regression to competing risks. Biometrics 51:524.  https://doi.org/10.2307/2532940 CrossRefPubMedGoogle Scholar
  30. 30.
    Hulka BS, Moorman PG (2001) Breast cancer: hormones and other risk factors. Maturitas 38:103–113CrossRefPubMedGoogle Scholar
  31. 31.
    Ziegler RG, Fuhrman BJ, Moore SC, Matthews CE (2015) Epidemiologic studies of estrogen metabolism and breast cancer. Steroids 99:67–75.  https://doi.org/10.1016/j.steroids.2015.02.015 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Albenberg LG, Wu GD (2014) Diet and the intestinal microbiome: associations, functions, and implications for health and disease. Gastroenterology 146:1564–1572.  https://doi.org/10.1053/j.gastro.2014.01.058 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Shapira I, Sultan K, Lee A, Taioli E (2013) Evolving concepts: how diet and the intestinal microbiome act as modulators of breast malignancy. ISRN Oncol 2013:1–10.  https://doi.org/10.1155/2013/693920 CrossRefGoogle Scholar
  34. 34.
    Gavaler JS, Van Thiel DH (1992) The association between moderate alcoholic beverage consumption and serum estradiol and testosterone levels in normal postmenopausal women: relationship to the literature. Alcohol Clin Exp Res 16:87–92CrossRefPubMedGoogle Scholar
  35. 35.
    Rose DP, Komninou D, Stephenson GD (2004) Obesity, adipocytokines, and insulin resistance in breast cancer. Obes Rev 5:153–165.  https://doi.org/10.1111/j.1467-789X.2004.00142.x CrossRefPubMedGoogle Scholar
  36. 36.
    Schmidt S, Monk JM, Robinson LE, Mourtzakis M (2015) The integrative role of leptin, oestrogen and the insulin family in obesity-associated breast cancer: potential effects of exercise. Obes Rev 16:473–487.  https://doi.org/10.1111/obr.12281 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Calder PC, Ahluwalia N, Brouns F, Buetler T, Clement K, Cunningham K et al (2011) Dietary factors and low-grade inflammation in relation to overweight and obesity. Br J Nutr 106(Suppl):S5–S78.  https://doi.org/10.1017/s0007114511005460 CrossRefPubMedGoogle Scholar
  38. 38.
    Barbaresko J, Koch M, Schulze MB, Nothlings U (2013) Dietary pattern analysis and biomarkers of low-grade inflammation: a systematic literature review. Nutr Rev 71:511–527.  https://doi.org/10.1111/nure.12035 CrossRefPubMedGoogle Scholar
  39. 39.
    Greenberg AS, Obin MS (2006) Obesity and the role of adipose tissue in inflammation and metabolism. Am J Clin Nutr 83:461S–465SCrossRefPubMedGoogle Scholar
  40. 40.
    O’Connor M-F, Irwin MR (2010) Links between behavioral factors and inflammation. Clin Pharmacol Ther 87:479–482.  https://doi.org/10.1038/clpt.2009.255 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Willett W (2012) Nutritional epidemiology. Oxford University Press, New York.  https://doi.org/10.1093/acprof:oso/9780199754038.001.0001
  42. 42.
    Lin CJ, DeRoo LA, Jacobs SR, Sandler DP (2012) Accuracy and reliability of self-reported weight and height in the Sister Study. Public Health Nutr 15:989–999.  https://doi.org/10.1017/S1368980011003193 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Behavioral and Epidemiology Research GroupAmerican Cancer SocietyAtlantaUSA
  2. 2.Department of Epidemiology and Biostatistics, Arnold School of Public HealthUniversity of South CarolinaColumbiaUSA
  3. 3.Epidemiology BranchNational Institute of Environmental Health Sciences, National Institutes of HealthResearch Triangle ParkUSA
  4. 4.Cancer Prevention and Control ProgramUniversity of South CarolinaColumbiaUSA

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