Advertisement

Breast Cancer Research and Treatment

, Volume 128, Issue 3, pp 883–889 | Cite as

Prediagnostic plasma enterolactone levels and mortality among women with breast cancer

  • Anja OlsenEmail author
  • Jane Christensen
  • Knud Erik Bach Knudsen
  • Nina Føns Johnsen
  • Kim Overvad
  • Anne Tjønneland
Epidemiology

Abstract

Experimental and epidemiological studies have suggested that the phytoestrogen enterolactone is associated to biological mechanisms that may have positive effects on breast cancer development. In a recent study based on American breast cancer patients, high intakes of lignans, the precursor of enterolactone, was found related to lower mortality. The aim of this study was, for the first time, to evaluate if prediagnostic plasma levels of enterolactone were associated to mortality in women diagnosed with breast cancer. Among 24,697 postmenopausal women included into a Danish cohort between 1993 and 1997, 424 developed breast cancer before December 31, 2000. Enterolactone levels were measured in baseline blood samples and related to mortality by Cox proportional hazard models. During a median of 10 years after breast cancer diagnosis, 111 women died (80 from breast cancer). When comparing women with enterolactone levels above the median (>20.5 nmol/l) to those with lower levels, decreased hazard rates (HR) were seen for both all-cause mortality (HR: 0.47; 95% confidence interval: 0.32–0.68) and breast cancer mortality (HR: 0.56; 95% confidence interval: 0.36–0.87). Higher prediagnostic plasma levels of enterolactone were found related to lower mortality among breast cancer patients.

Keywords

Breast cancer mortality All-cause mortality Plasma enterolactone Cohort study Survival 

Notes

Acknowledgments

This work was supported by The Danish Cancer Society; and NordForsk (the Nordic Centres of Excellence HELGA and SysDiet). Neither of the funding agencies had any influence on design and conduct of the study; collection, management, analysis, and interpretation of the data; or preparation, review, or approval of the manuscript.

References

  1. 1.
    Ferlay J, Bray F, Pisani P, Parkin DM (2004) GLOBOCAN 2002: cancer incidence, mortality and prevalence worldwide. IARC CancerBase No. 5, version 2.0. IARC Press, LyonGoogle Scholar
  2. 2.
    Patterson RE, Cadmus LA, Emond JA, Pierce JP (2010) Physical activity, diet, adiposity and female breast cancer prognosis: a review of the epidemiologic literature. Maturitas 66(1):5–15PubMedCrossRefGoogle Scholar
  3. 3.
    Kellen E, Vansant G, Christiaens MR, Neven P, Van LE (2009) Lifestyle changes and breast cancer prognosis: a review. Breast Cancer Res Treat 114:13–22PubMedCrossRefGoogle Scholar
  4. 4.
    Cornwell T, Cohick W, Raskin I (2004) Dietary phytoestrogens and health. Phytochemistry 65:995–1016PubMedCrossRefGoogle Scholar
  5. 5.
    Mazur W (1998) Phytoestrogen content in foods. Baillieres Clin Endocrinol Metab 12:729–742PubMedCrossRefGoogle Scholar
  6. 6.
    Peeters PH, Slimani N, van der Schouw YT, Grace PB, Navarro C, Tjonneland A, Olsen A, Clavel-Chapelon F, Touillaud M, Boutron-Ruault MC, Jenab M, Kaaks R, Linseisen J, Trichopoulou A, Trichopoulos D, Dilis V, Boeing H, Weikert C, Overvad K, Pala V, Palli D, Panico S, Tumino R, Vineis P, Bueno-de-Mesquita HB, van Gils CH, Skeie G, Jakszyn P, Hallmans G, Berglund G, Key TJ, Travis R, Riboli E, Bingham SA (2007) Variations in plasma phytoestrogen concentrations in European adults. J Nutr 137:1294–1300PubMedGoogle Scholar
  7. 7.
    Kilkkinen A, Stumpf K, Pietinen P, Valsta LM, Tapanainen H, Adlercreutz H (2001) Determinants of serum enterolactone concentration. Am J Clin Nutr 73:1094–1100PubMedGoogle Scholar
  8. 8.
    Wang L, Chen J, Thompson LU (2005) The inhibitory effect of flaxseed on the growth and metastasis of estrogen receptor negative human breast cancer xenograftsis attributed to both its lignan and oil components. Int J Cancer 116:793–798PubMedCrossRefGoogle Scholar
  9. 9.
    Chen J, Wang L, Thompson LU (2006) Flaxseed and its components reduce metastasis after surgical excision of solid human breast tumor in nude mice. Cancer Lett 234:168–175PubMedCrossRefGoogle Scholar
  10. 10.
    Brooks JD, Thompson LU (2005) Mammalian lignans and genistein decrease the activities of aromatase and 17beta-hydroxysteroid dehydrogenase in MCF-7 cells. J Steroid Biochem Mol Biol 94:461–467PubMedCrossRefGoogle Scholar
  11. 11.
    Hutchins AM, Martini MC, Olson BA, Thomas W, Slavin JL (2001) Flaxseed consumption influences endogenous hormone concentrations in postmenopausal women. Nutr Cancer 39:58–65PubMedCrossRefGoogle Scholar
  12. 12.
    Boccardo F, Puntoni M, Guglielmini P, Rubagotti A (2006) Enterolactone as a risk factor for breast cancer: a review of the published evidence. Clin Chim Acta 365:58–67PubMedCrossRefGoogle Scholar
  13. 13.
    McCann SE, Thompson LU, Nie J, Dorn J, Trevisan M, Shields PG, Ambrosone CB, Edge SB, Li HF, Kasprzak C, Freudenheim JL (2010) Dietary lignan intakes in relation to survival among women with breast cancer: the Western New York Exposures and Breast Cancer (WEB) Study. Breast Cancer Res Treat 122:229–235PubMedCrossRefGoogle Scholar
  14. 14.
    Kaaks RJ (1997) Biochemical markers as additional measurements in studies of the accuracy of dietary questionnaire measurements: conceptual issues. Am J Clin Nutr 65:1232S–1239SPubMedGoogle Scholar
  15. 15.
    Tjonneland A, Olsen A, Boll K, Stripp C, Christensen J, Engholm G, Overvad K (2007) Study design, exposure variables, and socioeconomic determinants of participation in diet, cancer and health: a population-based prospective cohort study of 57, 053 men and women in Denmark. Scand J Public Health 35:432–441PubMedCrossRefGoogle Scholar
  16. 16.
    Storm HH, Michelsen EV, Clemmensen IH, Pihl J (1997) The Danish Cancer Registry–history, content, quality and use. Dan Med Bull 44:535–539PubMedGoogle Scholar
  17. 17.
    Fischerman K, Mouridsen HT (1988) Danish Breast Cancer Cooperative Group (DBCG). Structure and results of the organization. Acta Oncol 27:593–596PubMedCrossRefGoogle Scholar
  18. 18.
    Stumpf K, Uehara M, Nurmi T, Adlercreutz H (2000) Changes in the time-resolved fluoroimmunoassay of plasma enterolactone. Anal Biochem 284:153–157PubMedCrossRefGoogle Scholar
  19. 19.
    Uehara M, Lapcik O, Hampl R, Al Maharik N, Makela T, Wahala K, Mikola H, Adlercreutz H (2000) Rapid analysis of phytoestrogens in human urine by time-resolved fluoroimmunoassay. J Steroid Biochem Mol Biol 72:273–282PubMedCrossRefGoogle Scholar
  20. 20.
    Heinonen S, Nurmi T, Liukkonen K, Poutanen K, Wahala K, Deyama T, Nishibe S, Adlercreutz H (2001) In vitro metabolism of plant lignans: new precursors of mammalian lignans enterolactone and enterodiol. J Agric Food Chem 49:3178–3186PubMedCrossRefGoogle Scholar
  21. 21.
    Adlercreutz H (2002) Phytoestrogens and breast cancer. J Steroid Biochem Mol Biol 83:113–118PubMedCrossRefGoogle Scholar
  22. 22.
    Zeleniuch-Jacquotte A, Adlercreutz H, Akhmedkhanov A, Toniolo P (1998) Reliability of serum measurements of lignans and isoflavonoid phytoestrogens over a two-year period. Cancer Epidemiol Biomarkers Prev 7:885–889PubMedGoogle Scholar
  23. 23.
    Nieto FJ, Coresh J (1996) Adjusting survival curves for confounders: a review and a new method. Am J Epidemiol 143:1059–1068PubMedCrossRefGoogle Scholar
  24. 24.
    Olsen A, Knudsen KE, Thomsen BL, Loft S, Stripp C, Overvad K, Moller S, Tjonneland A (2004) Plasma enterolactone and breast cancer incidence by estrogen receptor status. Cancer Epidemiol Biomarkers Prev 13:2084–2089PubMedGoogle Scholar
  25. 25.
    Kilkkinen A, Valsta LM, Virtamo J, Stumpf K, Adlercreutz H, Pietinen P (2003) Intake of lignans is associated with serum enterolactone concentration in Finnish men and women. J Nutr 133:1830–1833PubMedGoogle Scholar
  26. 26.
    Adlercreutz H (2007) Lignans and human health. Crit Rev Clin Lab Sci 44:483–525PubMedCrossRefGoogle Scholar
  27. 27.
    Johnsen NF, Hausner H, Olsen A, Tetens I, Christensen J, Knudsen KE, Overvad K, Tjonneland A (2004) Intake of whole grains and vegetables determines the plasma enterolactone concentration of Danish women. J Nutr 134:2691–2697PubMedGoogle Scholar
  28. 28.
    Slavin JL, Jacobs D, Marquart L, Wiemer K (2001) The role of whole grains in disease prevention. J Am Diet Assoc 101:780–785PubMedCrossRefGoogle Scholar
  29. 29.
    Jacobs DR Jr, Gallaher DD (2004) Whole grain intake and cardiovascular disease: a review. Curr Atheroscler Rep 6:415–423PubMedCrossRefGoogle Scholar
  30. 30.
    Fardet A (2010) New hypotheses for the health-protective mechanisms of whole-grain cereals: what is beyond fibre? Nutr Res Rev 23:65–134PubMedCrossRefGoogle Scholar
  31. 31.
    Milder IE, Kuijsten A, Arts IC, Feskens EJ, Kampman E, Hollman PC, Van V (2007) Relation between plasma enterodiol and enterolactone and dietary intake of lignans in a Dutch endoscopy-based population. J Nutr 137:1266–1271PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC. 2011

Authors and Affiliations

  • Anja Olsen
    • 1
    Email author
  • Jane Christensen
    • 1
  • Knud Erik Bach Knudsen
    • 2
  • Nina Føns Johnsen
    • 1
  • Kim Overvad
    • 3
    • 4
  • Anne Tjønneland
    • 1
  1. 1.Institute of Cancer Epidemiology, Danish Cancer SocietyCopenhagen ODenmark
  2. 2.Department of Animal Health and Bioscience, Faculty of Agricultural SciencesAarhus UniversityTjeleDenmark
  3. 3.Department of EpidemiologySchool of Public Health, Aarhus UniversityAarhusDenmark
  4. 4.Department of CardiologyAalborg Hospital, Aarhus University HospitalAalborgDenmark

Personalised recommendations