Breast Cancer Research and Treatment

, Volume 139, Issue 3, pp 801–809 | Cite as

Plasma enterolactone and breast cancer risk in the Nurses’ Health Study II

  • Jing Xie
  • Shelley S. Tworoger
  • Adrian A. Franke
  • Kathryn L. Terry
  • Megan S. Rice
  • Bernard A. Rosner
  • Walter C. Willett
  • Susan E. Hankinson
  • A. Heather EliassenEmail author


Lignans are plant-based phytoestrogens with both estrogenic and anti-estrogenic properties that may be important for breast carcinogenesis. Retrospective studies have observed decreased breast cancer risk associated with high circulating enterolactone concentrations, a biomarker of lignan intake, but results from prospective studies are conflicting. To prospectively examine this association, we measured plasma enterolactone levels in 802 breast cancer cases and 802 matched controls nested among predominantly premenopausal women in the Nurses’ Health Study II cohort. We used conditional logistic regression and polytomous logistic regression models, adjusting for known breast cancer risk factors, to calculate relative risks (RR) and 95 % confidence intervals (CI). Compared to women with enterolactone concentrations ≤4 nmol/L, the multivariate-adjusted RRs for breast cancer were 1.18 (95 % CI 0.86–1.62), 0.91 (95 % CI 0.66–1.25), and 0.96 (95 % CI 0.70–1.33) for women with enterolactone levels in the second to the fourth quartiles, respectively; P trend = 0.60. Results were similar across tumors defined by estrogen and progesterone receptor status. Among premenopausal women with follicular estradiol levels below the median (<47 pg/mL), women in the highest category of enterolactone levels had a 51 % lower breast cancer risk compared to those in the lowest category (95 % CI 0.27–0.91); P trend = 0.02. No association was observed among women with high-follicular estradiol levels (≥47 pg/mL), (comparable RR = 1.39, 95 % CI 0.73–2.65; P interaction = 0.02). We did not observe an overall association between plasma enterolactone and breast cancer risk in a large nested case–control study of US women. However, a significant inverse association was observed among premenopausal women with low-follicular estradiol levels, suggesting that enterolactone may be important in a low-estrogen environment. This should be confirmed in future studies.


Enterolactone Lignan Breast cancer Biomarker Prospective study Premenopausal 



This project was supported by the National Institutes of Health (NIH) R01 CA67272, R01 CA50385, and P30 CA71789. J.X. is supported by scholarships from Harvard University. M.S.R. is supported by the NIH T32 CA09001. The authors thank participants of the Nurses’ Health Study II for their longstanding contributions and support to this study. Laurie Custer, University of Hawai’i Cancer Center, is acknowledged for her skillful performance of the LCMS assay. The authors also thank 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.

Conflict of interest

The authors declare that they have no conflict of interest. The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; and preparation, review, or approval of the manuscript.

Supplementary material

10549_2013_2586_MOESM1_ESM.docx (15 kb)
Supplementary material 1 (DOCX 14 kb)


  1. 1.
    Key T, Appleby P, Barnes I, Reeves G (2002) Endogenous sex hormones and breast cancer in postmenopausal women: reanalysis of nine prospective studies. J Natl Cancer Inst 94:606–616PubMedCrossRefGoogle Scholar
  2. 2.
    Breast cancer and hormone replacement therapy: collaborative reanalysis of data from 51 epidemiological studies of 52,705 women with breast cancer and 108,411 women without breast cancer (1997). Lancet 350 (9084):1047–1059Google Scholar
  3. 3.
    Eliassen AH, Missmer SA, Tworoger SS, Spiegelman D, Barbieri RL, Dowsett M, Hankinson SE (2006) Endogenous steroid hormone concentrations and risk of breast cancer among premenopausal women. J Natl Cancer Inst 98(19):1406–1415PubMedCrossRefGoogle Scholar
  4. 4.
    Kaaks R, Berrino F, Key T, Rinaldi S, Dossus L, Biessy C, Secreto G, Amiano P, Bingham S, Boeing H, de Mesquita HBB, Chang-Claude J, Clavel-Chapelon F, Fournier A, van Gils CH, Gonzalez CA, Gurrea AB, Critselis E, Khaw KT, Krogh V, Lahmann PH, Nagel G, Olsen A, Onland-Moret NC, Overvad K, Palli D, Panico S, Peeters P, Quirós JR, Roddam A, Thiebaut A, Tjønneland A, Chirlaque MD, Trichopoulou A, Trichopoulos D, Tumino R, Vineis P, Norat T, Ferrari P, Slimani N, Riboli E (2005) Serum sex steroids in premenopausal women and breast cancer risk within the European prospective investigation into cancer and nutrition (EPIC). J Natl Cancer Inst 97(10):755–765PubMedCrossRefGoogle Scholar
  5. 5.
    Walker K, Bratton DJ, Frost C (2011) Premenopausal endogenous oestrogen levels and breast cancer risk: a meta-analysis. Br J Cancer 105(9):1451–1457PubMedCrossRefGoogle Scholar
  6. 6.
    Fortner R, Eliassen AH, Spiegelman D, Willett W, Barbieri R, Hankinson S (2013) Premenopausal endogenous steroid hormones and breast cancer risk: results from the Nurses’ Health Study II. Breast Cancer Res 15(2):R19PubMedCrossRefGoogle Scholar
  7. 7.
    Setchell KDR, Borriello SP, Gordon H, Lawson AM, Harkness R, Morgan DML, Kirk DN, Adlercreutz H, Anderson LC, Axelson M (1981) Lignan formation in man—microbial involvement and possible roles in relation to cancer. Lancet 318(8236):4–7CrossRefGoogle Scholar
  8. 8.
    Johnsen NF, Hausner H, Olsen A, Tetens I, Christensen J, Knudsen KEB, Overvad K, Tjønneland A (2004) Intake of whole grains and vegetables determines the plasma enterolactone concentration of Danish women. J Nutr 134(10):2691–2697PubMedGoogle Scholar
  9. 9.
    Nurmi T, Mursu J, Peñalvo JL, Poulsen HE, Voutilainen S (2010) Dietary intake and urinary excretion of lignans in Finnish men. Br J Nutr 103:677–685PubMedCrossRefGoogle Scholar
  10. 10.
    Adlercreutz H (2007) Lignans and human health. Crit Rev Clin Lab Sci 44(5–6):483–525PubMedCrossRefGoogle Scholar
  11. 11.
    Horner NK, Kristal AR, Prunty J, Skor HE, Potter JD, Lampe JW (2002) Dietary determinants of plasma enterolactone. Cancer Epidemiol Biomark Prev 11(1):121–126Google Scholar
  12. 12.
    Rowland IR, Wiseman H, Sanders TAB, Adlercreutz H, Bowey EA (2000) Interindividual variation in metabolism of soy isoflavones and lignans: influence of habitual diet on equol production by the gut microflora. Nutr Cancer 36(1):27–32PubMedCrossRefGoogle Scholar
  13. 13.
    Wang L-Q (2002) Mammalian phytoestrogens: enterodiol and enterolactone. J Chromatogr B 777(1–2):289–309CrossRefGoogle Scholar
  14. 14.
    Welshons WV, Murphy CS, Koch R, Calaf G, Jordan VC (1987) Stimulation of breast cancer cells in vitro by the environmental estrogen enterolactone and the phytoestrogen equol. Breast Cancer Res Treat 10(2):169–175. doi: 10.1007/bf01810580 PubMedCrossRefGoogle Scholar
  15. 15.
    Mousavi Y, Adlercreutz H (1992) Enterolactone and estradiol inhibit each other’s proliferative effect on MCF-7 breast cancer cells in culture. J Steroid Biochem Mol Biol 41(3–8):615–619PubMedCrossRefGoogle Scholar
  16. 16.
    Bergman Jungeström M, Thompson LU, Dabrosin C (2007) Flaxseed and its lignans inhibit estradiol-induced growth, angiogenesis, and secretion of vascular endothelial growth factor in human breast cancer xenografts in vivo. Clin Cancer Res 13(3):1061–1067PubMedCrossRefGoogle Scholar
  17. 17.
    Martin P, Horwitz K, Ryan D, McGuire W (1978) Phytoestrogen interaction with estrogen receptors in human breast cancer cells. Endocrinology 103(5):1860–1867. doi: 10.1210/endo-103-5-1860 PubMedCrossRefGoogle Scholar
  18. 18.
    Adlercreutz H, Bannwart C, Wahala K, Makela T, Brunow G, Hase T, Arosemena P, Kellis JJ, Vickery L (1993) Inhibition of human aromatase by mammalian lignans and isoflavonoid phytoestrogens. J Steroid Biochem Mol Biol 44(2):147–153PubMedCrossRefGoogle Scholar
  19. 19.
    Brooks JD, Thompson LU (2005) Mammalian lignans and genistein decrease the activities of aromatase and 17β-hydroxysteroid dehydrogenase in MCF-7 cells. J Steroid Biochem Mol Biol 94(5):461–467PubMedCrossRefGoogle Scholar
  20. 20.
    Siiteri PK (1987) Adipose tissue as a source of hormones. Am J Clin Nutr 45(1):277–282PubMedGoogle Scholar
  21. 21.
    Prasad K (2000) Antioxidant activity of secoisolariciresinol diglucoside-derived metabolites, secoisolariciresinol, enterodiol, and enterolactone. Int J Angiol 9(4):220–225PubMedCrossRefGoogle Scholar
  22. 22.
    Carreau C, Flouriot G, Bennetau-Pelissero C, Potier M (2008) Enterodiol and enterolactone, two major diet-derived polyphenol metabolites have different impact on ERα transcriptional activation in human breast cancer cells. J Steroid Biochem Mol Biol 110(1–2):176–185PubMedCrossRefGoogle Scholar
  23. 23.
    Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH, Van der Saag PT, van der Burg B, Gustafsson J (1998) Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139:4252–4263PubMedCrossRefGoogle Scholar
  24. 24.
    Penttinen P, Jaehrling J, Damdimopoulos AE, Inzunza J, Lemmen JG, van der Saag P, Pettersson K, Gauglitz G, Mäkelä S, Pongratz I (2007) Diet-derived polyphenol metabolite enterolactone is a tissue-specific estrogen receptor activator. Endocrinology 148(10):4875–4886PubMedCrossRefGoogle Scholar
  25. 25.
    Buck K, Zaineddin AK, Vrieling A, Linseisen J, Chang-Claude J (2010) Meta-analyses of lignans and enterolignans in relation to breast cancer risk. Am J Clin Nutr 92(1):141–153PubMedCrossRefGoogle Scholar
  26. 26.
    Ingram D, Sanders K, Kolybaba M, Lopez D (1997) Case–control study of phyto-oestrogens and breast cancer. Lancet 350(9083):990–994PubMedCrossRefGoogle Scholar
  27. 27.
    Dai Q, Franke AA, Jin F, Shu X-O, Hebert JR, Custer LJ, Cheng J, Gao Y-T, Zheng W (2002) Urinary excretion of phytoestrogens and risk of breast cancer among Chinese women in Shanghai. Cancer Epidemiol Biomarkers Prev 11(9):815–821PubMedGoogle Scholar
  28. 28.
    Pietinen P, Stumpf K, Mannisto S, Kataja V, Uusitupa M, Adlercreutz H (2001) Serum enterolactone and risk of breast cancer: a case–control study in eastern Finland. Cancer Epidemiol Biomarkers Prev 10:339–344PubMedGoogle Scholar
  29. 29.
    Zaineddin AK, Vrieling A, Buck K, Becker S, Linseisen J, Flesch-Janys D, Kaaks R, Chang-Claude J (2012) Serum enterolactone and postmenopausal breast cancer risk by estrogen, progesterone and herceptin 2 receptor status. Int J Cancer 130(6):1401–1410PubMedCrossRefGoogle Scholar
  30. 30.
    Piller R, Chang-Claude J, Linseisen J (2006) Plasma enterolactone and genistein and the risk of premenopausal breast cancer. Eur J Cancer Prev 15:225–232PubMedCrossRefGoogle Scholar
  31. 31.
    den Tonkelaar I, Keinan-Boker L, Van’t Veer P, Arts CJM, Adlercreutz H, Thijssen JHH, Peeters PHM (2001) Urinary phytoestrogens and postmenopausal breast cancer risk. Cancer Epidemiol Biomarkers Prev 10(3):223–228Google Scholar
  32. 32.
    Hultén K, Winkvist A, Lenner P, Johansson R, Adlercreutz H, Hallmans G (2002) An incident case-referent study on plasma enterolactone and breast cancer risk. Eur J Nutr 41(4):168–176PubMedCrossRefGoogle Scholar
  33. 33.
    Olsen A, Knudsen KEB, Thomsen BL, Loft S, Stripp C, Overvad K, Møller S, Tjønneland A (2004) Plasma enterolactone and breast cancer incidence by estrogen receptor status. Cancer Epidemiol Biomarkers Prev 13(12):2084–2089PubMedGoogle Scholar
  34. 34.
    Kilkkinen A, Virtamo J, Vartiainen E, Sankila R, Virtanen MJ, Adlercreutz H, Pietinen P (2004) Serum enterolactone concentration is not associated with breast cancer risk in a nested case–control study. Int J Cancer 108(2):277–280PubMedCrossRefGoogle Scholar
  35. 35.
    Verheus M, van Gils CH, Keinan-Boker L, Grace PB, Bingham SA, Peeters PHM (2007) Plasma phytoestrogens and subsequent breast cancer risk. J Clin Oncol 25(6):648–655PubMedCrossRefGoogle Scholar
  36. 36.
    Ward H, Chapelais G, Kuhnle G, Luben R, Khaw K-T, Bingham S (2008) Breast cancer risk in relation to urinary and serum biomarkers of phytoestrogen exposure in the European Prospective into Cancer-Norfolk cohort study. Breast Cancer Res 10(2):R32PubMedCrossRefGoogle Scholar
  37. 37.
    Sonestedt E, Borgquist S, Ericson U, Gullberg B, Olsson H, Adlercreutz H, Landberg G, Wirfält E (2008) Enterolactone is differently associated with estrogen receptor β-negative and positive breast cancer in a Swedish nested case–control study. Cancer Epidemiol Biomarkers Prev 17(11):3241–3251PubMedCrossRefGoogle Scholar
  38. 38.
    Goodman MT, Shvetsov YB, Wilkens LR, Franke AA, Le Marchand L, Kakazu KK, Nomura AMY, Henderson BE, Kolonel LN (2009) Urinary phytoestrogen excretion and postmenopausal breast cancer risk: the multiethnic cohort study. Cancer Prev Res 2(10):887–894CrossRefGoogle Scholar
  39. 39.
    Zeleniuch-Jacquotte A, Adlercreutz H, Shore R, Koenig K, Kato I, Arslan A, Toniolo P (2004) Circulating enterolactone and risk of breast cancer: a prospective study in New York. Br J Cancer 91:99–105PubMedCrossRefGoogle Scholar
  40. 40.
    Boccardo F, Lunardi G, Guglielmini P, Parodi M, Murialdo R, Schettini G, Rubagotti A (2004) Serum enterolactone levels and the risk of breast cancer in women with palpable cysts. Eur J Cancer 40:84–89PubMedCrossRefGoogle Scholar
  41. 41.
    Grace PB, Taylor JI, Low Y-L, Luben RN, Mulligan AA, Botting NP, Dowsett M, Welch AA, Khaw K-T, Wareham NJ, Day NE, Bingham SA (2004) Phytoestrogen concentrations in serum and spot urine as biomarkers for dietary phytoestrogen intake and their relation to breast cancer risk in European prospective investigation of cancer and nutrition-norfolk. Cancer Epidemiol Biomarkers Prev 13(5):698–708PubMedGoogle Scholar
  42. 42.
    Stampfer MJ, Willett WC, Speizer FE, Dysert DC, Lipnick R, Rosner B, Hennekens CH (1984) Test of the National Death Index. Am J Epidemiol 119(5):837–839PubMedGoogle Scholar
  43. 43.
    Rich-Edwards JW, Corsano KA, Stampfer MJ (1994) Test of the National Death Index and Equifax Nationwide Death Search. Am J Epidemiol 140(11):1016–1019PubMedGoogle Scholar
  44. 44.
    Tworoger SS, Sluss P, Hankinson SE (2006) Association between plasma prolactin concentrations and risk of breast cancer among predominately premenopausal women. Cancer Res 66(4):2476–2482PubMedCrossRefGoogle Scholar
  45. 45.
    Kotsopoulos J, Tworoger SS, Campos H, Chung F-L, Clevenger CV, Franke AA, Mantzoros CS, Ricchiuti V, Willett WC, Hankinson SE, Eliassen AH (2010) Reproducibility of plasma, red blood cell, and urine biomarkers among premenopausal and postmenopausal women from the nurses’ health studies. Cancer Epidemiol Biomarkers Prev 19(4):938–946PubMedCrossRefGoogle Scholar
  46. 46.
    Franke AA, Custer LJ, Wilkens LR, Le Marchand LL, Nomura AM, Goodman MT, Kolonel LN (2002) Liquid chromatographic-photodiode array mass spectrometric analysis of dietary phytoestrogens from human urine and blood. J Chromatogr B 777(1–2):45–59CrossRefGoogle Scholar
  47. 47.
    Rosner B (1983) Percentage points for a generalized ESD many-outlier procedure. Technometrics 25:165–172CrossRefGoogle Scholar
  48. 48.
    Marshall R, Chisholm E (1985) Hypothesis testing in the polychotomous logistic model with an application to detecting gastrointestinal cancer. Stat Med 4(3):337–344PubMedCrossRefGoogle Scholar
  49. 49.
    Aarestrup J, Kyrø C, Knudsen KEB, Weiderpass E, Christensen J, Kristensen M, Würtz AML, Johnsen NF, Overvad K, Tjønneland A, Olsen A (2012) Plasma enterolactone and incidence of endometrial cancer in a case-cohort study of Danish women. Br J Nutr, FirstView:1–7Google Scholar
  50. 50.
    Olsen A, Christensen J, Knudsen K, Johnsen N, Overvad K, Tjønneland A (2011) Prediagnostic plasma enterolactone levels and mortality among women with breast cancer. Breast Cancer Res Treat 128(3):883–889PubMedCrossRefGoogle Scholar
  51. 51.
    Zeleniuch-Jacquotte A, Lundin E, Micheli A, Koenig KL, Lenner P, Muti P, Shore RE, Johansson I, Krogh V, Lukanova A, Stattin P, Afanasyeva Y, Rinaldi S, Arslan AA, Kaaks R, Berrino F, Hallmans G, Toniolo P, Adlercreutz H (2006) Circulating enterolactone and risk of endometrial cancer. Int J Cancer 119(10):2376–2381PubMedCrossRefGoogle Scholar
  52. 52.
    Stattin P, Adlercreutz H, Tenkanen L, Jellum E, Lumme S, Hallmans G, Harvei S, Teppo L, Stumpf K, Luostarinen T, Lehtinen M, Dillner J, Hakama M (2002) Circulating enterolactone and prostate cancer risk: a Nordic nested case–control study. Int J Cancer 99(1):124–129PubMedCrossRefGoogle Scholar
  53. 53.
    Vanharanta M, Voutilainen S, Lakka TA, van der Lee M, Adlercreutz H, Salonen JT (1999) Risk of acute coronary events according to serum concentrations of enterolactone: a prospective population-based case–control study. Lancet 354(9196):2112–2115PubMedCrossRefGoogle Scholar
  54. 54.
    Lin Y, Wolk A, Håkansson N, Peñalvo JL, Lagergren J, Adlercreutz H, Lu Y (2012) Validation of FFQ-based assessment of dietary lignans compared with serum enterolactone in Swedish women. Br J Nutr, FirstView:1–8Google Scholar
  55. 55.
    Travis RC, Spencer EA, Allen NE, Appleby PN, Roddam AW, Overvad K, Johnsen NF, Olsen A, Kaaks R, Linseisen J, Boeing H, Nothlings U, Bueno-de-Mesquita HB, Ros MM, Sacerdote C, Palli D, Tumino R, Berrino F, Trichopoulou A, Dilis V, Trichopoulos D, Chirlaque MD, Ardanaz E, Larranaga N, Gonzalez C, Suarez LR, Sanchez MJ, Bingham S, Khaw KT, Hallmans G, Stattin P, Rinaldi S, Slimani N, Jenab M, Riboli E, Key TJ (2009) Plasma phyto-oestrogens and prostate cancer in the European Prospective Investigation into Cancer and Nutrition. Br J Cancer 100(11):1817–1823PubMedCrossRefGoogle Scholar
  56. 56.
    Morton M, Arisaka O, Miyake N, Morgan L, Evans B (2002) Phytoestrogen concentrations in serum from Japanese men and women over forty years of age. J Nutr 132:3168–3171PubMedGoogle Scholar
  57. 57.
    Lampe JW, Martini MC, Kurzer MS, Adlercreutz H, Slavin JL (1994) Urinary lignan and isoflavonoid excretion in premenopausal women consuming flaxseed powder. Am J Clin Nutr 60(1):122–128PubMedGoogle Scholar
  58. 58.
    Boccardo F, Torrisi R, Zanardi S, Valenti G, Pensa F, De Franchis V, Barreca A, Ferraro P, Minuto F (1991) EGF in breast cyst fluid: relationships with intracystic androgens, estradiol and progesterone. Int J Cancer 47(4):523–526PubMedCrossRefGoogle Scholar
  59. 59.
    Navarrete M, Maier C, Falzoni R, Quadros L, Lima G, Baracat E, Nazario A (2005) Assessment of the proliferative, apoptotic and cellular renovation indices of the human mammary epithelium during the follicular and luteal phases of the menstrual cycle. Breast Cancer Res 7(3):R306–R313PubMedCrossRefGoogle Scholar
  60. 60.
    Ferguson D, Anderson T (1981) Morphological evaluation of cell turnover in relation to the menstrual cycle in the “resting” human breast. Br J Cancer 44(2):177–181PubMedCrossRefGoogle Scholar
  61. 61.
    Pike MC, Spicer DV, Dahmoush L, Press MF (1993) Estrogens, progestogens, normal breast cell proliferation, and breast cancer risk. Epidemiol Rev 15(1):17–30PubMedGoogle Scholar
  62. 62.
    Vasei M, Azarpira N, Talei A (2006) Status of estrogen and progesterone receptors in various phases of the menstrual cycle in breast cancer. Arch Iran Med 9(3):250–253PubMedGoogle Scholar
  63. 63.
    Karbowski B, Jackisch C, Deppe B, Schneider H (1999) Relationship of estrogen and progesterone receptors to the menstual cycle and menopausal status at the time of breast surgery. Zentralbl Gynakol 121(8):367–374PubMedGoogle Scholar
  64. 64.
    Khan SA, Yee KA, Kaplan C, Siddiqui JF (2002) Estrogen receptor α expression in normal human breast epithelium is consistent over time. Int J Cancer 102(4):334–337PubMedCrossRefGoogle Scholar
  65. 65.
    Grace P, Taylor J, Botting N, Fryatt T, Oldfield M, Al Maharik N, Bingham S (2003) Quantification of isoflavones and lignans in serum using isotope dilution liquid chromatography/tandem mass spectrometry. Rapid Commun Mass Spectrom 17:1350–1357PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Jing Xie
    • 1
    • 2
  • Shelley S. Tworoger
    • 1
    • 2
  • Adrian A. Franke
    • 3
  • Kathryn L. Terry
    • 2
    • 4
  • Megan S. Rice
    • 1
    • 2
  • Bernard A. Rosner
    • 1
    • 5
  • Walter C. Willett
    • 1
    • 2
    • 6
  • Susan E. Hankinson
    • 1
    • 2
    • 7
  • A. Heather Eliassen
    • 1
    • 2
    Email author
  1. 1.Channing Division of Network Medicine, Department of MedicineBrigham and Women’s Hospital and Harvard Medical SchoolBostonUSA
  2. 2.Department of EpidemiologyHarvard School of Public HealthBostonUSA
  3. 3.University of Hawaii Cancer CenterHonoluluUSA
  4. 4.Obstetrics and Gynecology Epidemiology Center, Department of Obstetrics and GynecologyBrigham and Women’s Hospital and Harvard Medical SchoolBostonUSA
  5. 5.Department of BiostatisticsHarvard School of Public HealthBostonUSA
  6. 6.Department of NutritionHarvard School of Public HealthBostonUSA
  7. 7.Division of Biostatistics and Epidemiology, School of Public Health and Health SciencesUniversity of MassachusettsAmherstUSA

Personalised recommendations