Skip to main content

Advertisement

SpringerLink
Log in

Lignan exposure: a worldwide perspective

  • Review
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Dietary lignans are phytoestrogens that are mostly found in plant-based foods, especially whole grains, seeds, nuts, legumes and vegetables. An accurate assessment of lignan exposure is crucial to evaluate their potential health benefits and to establish future recommendations and dietary guidelines. This narrative review aimed to (i) summarize the pros and the cons of the current main assessment methods for lignan exposure─i.e., dietary questionnaires, food composition tables and biomarkers, (ii) describe the individual lignans more consumed from a worldwide perspective, as well as their main food sources, (iii) determine the lignans concentrations in both urine and blood, and explore their heterogeneity among countries, and finally (iv) discuss the main determinants of lignan exposure.

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

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

24-HDR:

24-H dietary recall

END:

Enterodiol

ENL:

Enterolactone

EPIC:

European Prospective Investigation into Cancer and Nutrition

FFQ:

Food frequency questionnaire

LARI:

Lariciresinol

MATA:

Matairesinol

MEDI:

Medioresinol

PINO:

Pinoresinol

SECO:

Secoisolariciresinol

SYRI:

Syringaresinol

References

  1. Peterson J, Dwyer J, Adlercreutz H, Scalbert A, Jacques P, McCullough ML (2010) Dietary lignans: physiology and potential for cardiovascular disease risk reduction. Nutr Rev 68:571–603. https://doi.org/10.1017/S0007114515005012

    Article  CAS  PubMed  Google Scholar 

  2. Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH, van der Saag PT, van der Burg B, Gustafsson JA (1998) Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139:4252–4263

    CAS  PubMed  Google Scholar 

  3. Grosso G, Micek A, Godos J, Pajak A, Sciacca S, Galvano F, Giovannucci EL (2017) Dietary flavonoid and lignan intake and mortality in prospective cohort studies: systematic review and dose-response meta-analysis. Am J Epidemiol 185(12):1304–1316. https://doi.org/10.1093/aje/kww207

    Article  PubMed  Google Scholar 

  4. Touillaud MS, Thiébaut AC, Fournier A, Niravong M, Boutron-Ruault MC, Clavel-Chapelon F (2007) Dietary lignan intake and postmenopausal breast cancer risk by estrogen and progesterone receptor status. J Natl Cancer Inst 99(6):475–486. https://doi.org/10.1093/jnci/djk096

    Article  CAS  PubMed  Google Scholar 

  5. Buja A, Pierbon M, Lago L, Grotto G, Baldo V (2020) Breast cancer primary prevention and diet: an umbrella review. Int J Environ Res Public Health 17(13):4731. https://doi.org/10.3390/ijerph17134731

    Article  CAS  PubMed Central  Google Scholar 

  6. Ma ZP, Zhang ZF, Yang YF, Yang Y (2019) Sesamin promotes osteoblastic differentiation and protects rats from osteoporosis. Med Sci Monit 25:5312–5320. https://doi.org/10.12659/MSM.915529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Pruthi S, Qin R, Terstreip SA et al (2012) A phase III, randomized, placebo-controlled, double-blind trial of flaxseed for the treatment of hot flashes: North Central Cancer Treatment Group N08C7. Menopause 19(1):48–53. https://doi.org/10.1097/gme.0b013e318223b021

    Article  PubMed  PubMed Central  Google Scholar 

  8. Adlercreutz H (2007) Lignans and human health. Crit Rev Clin Lab Sci 44:483–525

    CAS  PubMed  Google Scholar 

  9. Zamora-Ros R, Knaze V, Rothwell JA et al (2016) Dietary polyphenol intake in Europe: the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Eur J Nutr 55:1359–1375. https://doi.org/10.1007/s00394-015-0950-x

    Article  CAS  PubMed  Google Scholar 

  10. Smeds AI, Eklund PC, Sjöholm RE, Willför SM, Nishibe S, Deyama T, Holmbom BR (2007) Quantification of a broad spectrum of lignans in cereals, oilseeds, and nuts. J Agric Food Chem 55:1337–1346

    CAS  PubMed  Google Scholar 

  11. Clavel T, Doré J, Blaut M (2006) Bioavailability of lignans in human subjects. Nutr Res Rev 19:187–196. https://doi.org/10.1017/S0954422407249704

    Article  CAS  PubMed  Google Scholar 

  12. Heinonen S, Nurmi T, Liukkonen K, Poutanen K, Wähälä 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 49:3178–3186

    CAS  PubMed  Google Scholar 

  13. Nurmi T, Voutilainen S, Nyyssönen K, Adlercreutz H, Salonen JT (2003) Liquid chromatography method for plant and mammalian lignans in human urine. J Chromatogr B Analyt Technol Biomed Life Sci 798:101–110

    CAS  PubMed  Google Scholar 

  14. Pérez-Jiménez J, Neveu V, Vos F, Scalbert A (2010) Systematic analysis of the content of 502 polyphenols in 452 foods and beverages: an application of the phenol-explorer database. J Agric Food Chem 58:4959–4969. https://doi.org/10.1021/jf100128b

    Article  CAS  PubMed  Google Scholar 

  15. Kuhnle GGC, Dell’Aquila C, Aspinall SM, Runswick SA, Mulligan AA, Bingham SA (2008) Phytoestrogen content of foods of animal origin: dairy products, eggs, meat, fish, and seafood. J Agric Food Chem 56:10099–10104. https://doi.org/10.1021/jf801344x

    Article  CAS  PubMed  Google Scholar 

  16. Zamora-Ros R, Rabassa M, Llorach R, González CA, Andres-Lacueva C (2012) Application of dietary phenolic biomarkers in epidemiology: past, present, and future. J Agric Food Chem 60:6648–6657. https://doi.org/10.1021/jf204742e

    Article  CAS  PubMed  Google Scholar 

  17. Neveu V, Perez-Jiménez J, Vos F, Crespy V, du Chaffaut L, Mennen L, Knox C, Eisner R, Cruz J, Wishart D, Scalbert A (2010) Phenol-Explorer: an online comprehensive database on polyphenol contents in foods. Database (Oxford) 2010:bap024. https://doi.org/10.1093/database/bap024

  18. Thompson LU, Boucher BA, Liu Z, Cotterchio M, Kreiger N (2006) Phytoestrogen content of foods consumed in Canada, including isoflavones, lignans, and coumestan. Nutr Cancer 54:184–201

    CAS  PubMed  Google Scholar 

  19. Milder IEJ, Arts ICW, van de Putte B, Venema DP, Hollman PCH (2005) Lignan contents of Dutch plant foods: a database including lariciresinol, pinoresinol, secoisolariciresinol and matairesinol. Br J Nutr 93:393–402

    CAS  PubMed  Google Scholar 

  20. Kuhnle GGC, Dell’Aquila C, Aspinall SM, Runswick SA, Joosen AMCP, Mulligan AA, Binham SA (2009) Phytoestrogen content of fruits and vegetables commonly consumed in the UK based on LC–MS and 13C-labelled standards. Food Chem 116:542–554

    CAS  Google Scholar 

  21. Kuhnle GGC, Dell’Aquila C, Aspinall SM, Runswick SA, Mulligan AA, Bingham SA (2008) Phytoestrogen content of beverages, nuts, seeds, and oils. J Agric Food Chem 56:7311–7315. https://doi.org/10.1021/jf801534g

    Article  CAS  PubMed  Google Scholar 

  22. Kuhnle GGC, Dell’aquila C, Aspinall SM, Runswick SA, Mulligan AA, Bingham SA (2009) Phytoestrogen content of cereals and cereal-based foods consumed in the UK. Nutr Cancer 61:302–309. https://doi.org/10.1080/01635580802567141

    Article  CAS  PubMed  Google Scholar 

  23. Valsta LM, Kilkkinen A, Mazur W, Nurmi T, Lampi A-M, Ovaskainen M-L, Korhonen T, Adlercreutz H, Pietinen P (2003) Phyto-oestrogen database of foods and average intake in Finland. Br J Nutr 89(Suppl 1):S31–S38

    CAS  PubMed  Google Scholar 

  24. Illner A-K, Freisling H, Boeing H, Huybrechts I, Crispim SP, Slimani N (2012) Review and evaluation of innovative technologies for measuring diet in nutritional epidemiology. Int J Epidemiol 41:1187–1203. https://doi.org/10.1093/ije/dys105

    Article  PubMed  Google Scholar 

  25. Potischman N (2003) Biologic and methodologic issues for nutritional biomarkers. J Nutr 133(Suppl 3):875S-880S. https://doi.org/10.1093/jn/133.3.875S

    Article  CAS  PubMed  Google Scholar 

  26. Peeters PHM, Slimani N, van der Schouw YT et al (2007) Variations in plasma phytoestrogen concentrations in European adults. J Nutr 137:1294–1300

    CAS  PubMed  Google Scholar 

  27. Pérez-Jiménez J, Hubert J, Hooper L, Cassidy A, Manach C, Williamson G, Scalbert A (2010) Urinary metabolites as biomarkers of polyphenol intake in humans: a systematic review. Am J Clin Nutr 92:801–809. https://doi.org/10.3945/ajcn.2010.29924

    Article  CAS  PubMed  Google Scholar 

  28. French MR, Thompson LU, Hawker GA (2007) Validation of a phytoestrogen food frequency questionnaire with urinary concentrations of isoflavones and lignan in premenopausal women. J Am Coll Nutr 26(1):76–82. https://doi.org/10.1080/07315724.2007.10719588

    Article  CAS  PubMed  Google Scholar 

  29. Horn-Ross PL, Barnes S, Lee VS et al (2006) Reliability and validity of an assessment of usual phytoestrogen consumption (United States). Cancer Causes Control 17(1):85–93. https://doi.org/10.1007/s10552-005-0391-6

    Article  PubMed  Google Scholar 

  30. Milder IEJ, Kuijsten A, Arts ICW, Feskens EJM, Kampman E, Hollman PC, Van ’t Veer P (2007) Relation between plasma enterodiol and enterolactone and dietary intake of lignans in a Dutch endoscopy-based population. J Nutr 137:1266–1271

    CAS  PubMed  Google Scholar 

  31. Lin Y, Wolk A, Håkansson N, Peñalvo JL, Lagergren J, Adlercreutz H, Lu Y (2013) Validation of FFQ-based assessment of dietary lignans compared with serum enterolactone in Swedish women. Br J Nutr 109(10):1873–1880. https://doi.org/10.1017/S000711451200387X

    Article  CAS  PubMed  Google Scholar 

  32. Liggins J, Grimwood R, Bingham SA (2000) Extraction and quantification of lignan phytoestrogens in food and human samples. Anal Biochem 287(1):102–109. https://doi.org/10.1006/abio.2000.4811

    Article  CAS  PubMed  Google Scholar 

  33. Zamora-Ros R, Biessy C, Rothwell JA, Monge A, Lajous M, Scalbert A, López-Ridaura R, Romieu I (2018) Dietary polyphenol intake and their major food sources in the Mexican Teachers’ Cohort. Br J Nutr 120:353–360. https://doi.org/10.1017/S0007114518001381

    Article  CAS  PubMed  Google Scholar 

  34. Adriouch S, Kesse-Guyot E, Feuillet T, Touvier M, Olié V, Andreeva V, Hercberg S, Galan P, Fezeu LK (2018) Total and specific dietary polyphenol intakes and 6-year anthropometric changes in a middle-aged general population cohort. Int J Obes (Lond) 42:310–317. https://doi.org/10.1038/ijo.2017.227

    Article  CAS  Google Scholar 

  35. Meija L, Söderholm P, Samaletdin A, Ignace G, Siksna I, Joffe R, Lejnieks A, Lietuvietis V, Krams I, Adlercreutz H (2013) Dietary intake and major sources of plant lignans in Latvian men and women. Int J Food Sci Nutr 64:535–543. https://doi.org/10.3109/09637486.2013.765835

    Article  CAS  PubMed  Google Scholar 

  36. Wisnuwardani R, Henauw S, Androutsos O et al (2018) Estimated dietary intake of polyphenols in European adolescents: the HELENA study. Eur J Nutr 58:2345–2363. https://doi.org/10.1007/s00394-018-1787-x

    Article  CAS  PubMed  Google Scholar 

  37. Tetens I, Turrini A, Tapanainen H, Christensen T, Lampe JW, Fagt S, Håkansson N, Lundquist A, Hallund J, Valsta LM (2013) Dietary intake and main sources of plant lignans in five European countries. Food Nutr Res. https://doi.org/10.3402/fnr.v57i0.19805

    Article  PubMed  PubMed Central  Google Scholar 

  38. Grosso G, Stepaniak U, Topor-Mądry R, Szafraniec K, Pająk A (2014) Estimated dietary intake and major food sources of polyphenols in the Polish arm of the HAPIEE study. Nutrition 30:1398–1403. https://doi.org/10.1016/j.nut.2014.04.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Witkowska AM, Zujko ME, Waśkiewicz A, Terlikowska KM, Piotrowski W (2015) Comparison of various databases for estimation of dietary polyphenol intake in the population of polish adults. Nutrients 7:9299–9308. https://doi.org/10.3390/nu7115464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Russo GI, Di Mauro M, Regis F, Reale G, Campisi D, Marranzano M, Lo Giudice A, Solinas T, Madonia M, Cimino S, Morgia G (2018) Association between dietary phytoestrogens intakes and prostate cancer risk in Sicily. Aging Male 21:48–54. https://doi.org/10.1080/13685538.2017.1365834

    Article  CAS  PubMed  Google Scholar 

  41. Plumb J, Pigat S, Bompola F, Cushen M, Pinchen H, Nørby E, Astley S, Lyons J, Kiely M, Finglas P (2017) eBASIS (bioactive substances in food information systems) and bioactive intakes: major updates of the bioactive compound composition and beneficial bioeffects database and the development of a probabilistic model to assess intakes in Europe. Nutrients 9:E320. https://doi.org/10.3390/nu9040320

    Article  PubMed  Google Scholar 

  42. Carmichael SL, Cogswell ME, Ma C, Gonzalez-Feliciano A, Olney RS, Correa A, Shaw GM (2013) Hypospadias and maternal intake of phytoestrogens. Am J Epidemiol 178:434–440. https://doi.org/10.1093/aje/kws591

    Article  PubMed  PubMed Central  Google Scholar 

  43. Fink BN, Steck SE, Wolff MS, Kabat GC, Gammon MD (2006) Construction of a flavonoid database for assessing intake in a population-based sample of women on Long Island, New York. Nutr Cancer 56:57–66

    CAS  PubMed  Google Scholar 

  44. Cotterchio M, Boucher BA, Manno M, Gallinger S, Okey A, Harper P (2006) Dietary phytoestrogen intake is associated with reduced colorectal cancer risk. J Nutr 136:3046–3053

    CAS  PubMed  Google Scholar 

  45. Morisset A-S, Lemieux S, Veilleux A, Bergeron J, John Weisnagel S, Tchernof A (2009) Impact of a lignan-rich diet on adiposity and insulin sensitivity in post-menopausal women. Br J Nutr 102:195–200. https://doi.org/10.1017/S0007114508162092

    Article  CAS  PubMed  Google Scholar 

  46. Hernández-Ramírez RU, Galván-Portillo MV, Ward MH, Agudo A, González CA, Oñate-Ocaña LF, Herrera-Goepfert R, Palma-Coca O, López-Carrillo L (2009) Dietary intake of polyphenols, nitrate and nitrite and gastric cancer risk in Mexico City. Int J Cancer 125:1424–1430. https://doi.org/10.1002/ijc.24454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Nascimento-Souza MA, de Paiva PG, Pérez-Jiménez J, do Carmo Castro Franceschini S, Ribeiro AQ, (2018) Estimated dietary intake and major food sources of polyphenols in elderly of Viçosa, Brazil: a population-based study. Eur J Nutr 57:617–627. https://doi.org/10.1007/s00394-016-1348-0

    Article  CAS  PubMed  Google Scholar 

  48. Miranda AM, Steluti J, Fisberg RM, Marchioni DM (2016) Association between polyphenol intake and hypertension in adults and older adults: a population-based study in Brazil. PLoS ONE 11:e0165791. https://doi.org/10.1371/journal.pone.0165791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Miranda AM, Steluti J, Fisberg RM, Marchioni DM (2016) Dietary intake and food contributors of polyphenols in adults and elderly adults of Sao Paulo: a population-based study. Br J Nutr 115:1061–1670. https://doi.org/10.1017/S0007114515005061

    Article  CAS  PubMed  Google Scholar 

  50. Lahmann PH, Hughes MC, Ibiebele TI, Mulligan AA, Kuhnle GGC, Webb PM (2012) Estimated intake of dietary phyto-oestrogens in Australian women and evaluation of correlates of phyto-oestrogen intake. J Nutr Sci 1:e11. https://doi.org/10.1017/jns.2012.11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Hanna KL, O’Neill S, Lyons-Wall PM (2010) Intake of isoflavone and lignan phytoestrogens and associated demographic and lifestyle factors in older Australian women. Asia Pac J Clin Nutr 19:540–549

    CAS  PubMed  Google Scholar 

  52. Sohrab G, Hosseinpour-Niazi S, Hejazi J, Yuzbashian E, Mirmiran P, Azizi F (2013) Dietary polyphenols and metabolic syndrome among Iranian adults. Int J Food Sci Nutr 64:661–667. https://doi.org/10.3109/09637486.2013.787397

    Article  CAS  PubMed  Google Scholar 

  53. Sohrab G, Ebrahimof S, Hosseinpour-Niazi S, Yuzbashian E, Mirmiran P, Azizi F (2018) Association of dietary intakes of total polyphenol and its subclasses with the risk of metabolic syndrome: tehran lipid and glucose study. Metab Syndr Relat Disord 16:274–281. https://doi.org/10.1089/met.2017.0140

    Article  CAS  PubMed  Google Scholar 

  54. Jang J-H, Yoon J-Y, Cho S-H (2007) Intake of dietary phytoestrogen and indices of antioxidant and bone metabolism of pre- and post-menopausal Korean women. Nutr Res Pract 1:305–312. https://doi.org/10.4162/nrp.2007.1.4.30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Suzuki R, Rylander-Rudqvist T, Saji S, Bergkvist L, Adlercreutz H, Wolk A (2008) Dietary lignans and postmenopausal breast cancer risk by oestrogen receptor status: a prospective cohort study of Swedish women. Br J Cancer 98:636–640. https://doi.org/10.1038/sj.bjc.6604175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Peñalvo JL, Moreno-Franco B, Ribas-Barba L, Serra-Majem L (2012) Determinants of dietary lignan intake in a representative sample of young Spaniards: association with lower obesity prevalence among boys but not girls. Eur J Clin Nutr 66:795–798. https://doi.org/10.1038/ejcn.2012.45

    Article  CAS  PubMed  Google Scholar 

  57. 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 133:1830–1833

    CAS  PubMed  Google Scholar 

  58. Pounis G, Di Castelnuovo A, Bonaccio M, Costanzo S, Persichillo M, Krogh V, Donati MB, de Gaetano G, Iacoviello L (2016) Flavonoid and lignan intake in a Mediterranean population: proposal for a holistic approach in polyphenol dietary analysis, the Moli-sani Study. Eur J Clin Nutr 70:338–345. https://doi.org/10.1038/ejcn.2015.178

    Article  CAS  PubMed  Google Scholar 

  59. Horn-Ross PL, John EM, Canchola AJ, Stewart SL, Lee MM (2003) Phytoestrogen intake and endometrial cancer risk. J Natl Cancer Inst 95:1158–1164

    CAS  PubMed  Google Scholar 

  60. Schabath MB, Hernandez LM, Wu X, Pillow PC, Spitz MR (2005) Dietary phytoestrogens and lung cancer risk. JAMA 294:1493–1504

    CAS  PubMed  Google Scholar 

  61. Milder IE, Feskens EJ, Arts IC, Bueno de Mesquita HB, Hollman PC, Kromhout D (2005) Intake of the plant lignans secoisolariciresinol, matairesinol, lariciresinol, and pinoresinol in Dutch men and women. J Nutr 135:1202–1207

    CAS  PubMed  Google Scholar 

  62. Hedelin M, Löf M, Andersson TM-L, Adlercreutz H, Weiderpass E (2011) Dietary phytoestrogens and the risk of ovarian cancer in the women’s lifestyle and health cohort study. Cancer Epidemiol Biomark Prev 20:308–317. https://doi.org/10.1158/1055-9965.EPI-10-0752

    Article  CAS  Google Scholar 

  63. Hedelin M, Löf M, Sandin S, Adami H-O, Weiderpass E (2016) Prospective study of dietary phytoestrogen intake and the risk of colorectal cancer. Nutr Cancer 68:388–395. https://doi.org/10.1080/01635581.2016.1152380

    Article  CAS  PubMed  Google Scholar 

  64. Rybak ME, Sternberg MR, Pfeiffer CM (2013) Sociodemographic and lifestyle variables are compound- and class-specific correlates of urine phytoestrogen concentrations in the U.S. population. J Nutr 143:986S-994S. https://doi.org/10.3945/jn.112.172981

    Article  CAS  PubMed  Google Scholar 

  65. Uehar M, Arai Y, Watanabe S, Adlercreutz H (2000) Comparison of plasma and urinary phytoestrogens in Japanese and Finnish women by time-resolved fluoroimmunoassay. BioFactors 12:217–225

    CAS  PubMed  Google Scholar 

  66. Liu W, Tanabe M, Harada KH, Koizumi A (2013) Levels of urinary isoflavones and lignan polyphenols in Japanese women. Environ Health Prev Med 18:394–400. https://doi.org/10.1007/s12199-013-0338-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Xu C, Liu Q, Zhang Q, Gu A, Jiang Z-Y (2015) Urinary enterolactone is associated with obesity and metabolic alteration in men in the US National Health and Nutrition Examination Survey 2001–10. Br J Nutr 113:683–690. https://doi.org/10.1017/S0007114514004115

    Article  CAS  PubMed  Google Scholar 

  68. Perez-Cornago A, Appleby PN, Boeing H et al (2018) Circulating isoflavone and lignan concentrations and prostate cancer risk: a meta-analysis of individual participant data from seven prospective studies including 2,828 cases and 5,593 controls. Int J Cancer 143:2677–2686. https://doi.org/10.1002/ijc.31640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Kuijsten A, Buijsman MN, Arts IC, Mulder PP, Hollman PC (2005) A validated method for the quantification of enterodiol and enterolactone in plasma using isotope dilution liquid chromatography with tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 822:178–184

    CAS  PubMed  Google Scholar 

  70. Krogholm KS, Bysted A, Brantsæter AL, Jakobsen J, Rasmussen SE, Kristoffersen L, Toft U (2012) Evaluation of flavonoids and enterolactone in overnight urine as intake biomarkers of fruits, vegetables and beverages in the Inter99 cohort study using the method of triads. Br J Nutr 108:1904–1912. https://doi.org/10.1017/S0007114512000104

    Article  CAS  PubMed  Google Scholar 

  71. Zamora-Ros R, Achaintre D, Rothwell JA et al (2016) Urinary excretions of 34 dietary polyphenols and their associations with lifestyle factors in the EPIC cohort study. Sci Rep 6:26905. https://doi.org/10.1038/srep26905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Ward H, Chapelais G, Kuhnle GG, Luben R, Khaw K-T, Bingham S (2008) Lack of prospective associations between plasma and urinary phytoestrogens and risk of prostate or colorectal cancer in the European Prospective into Cancer-Norfolk study. Cancer Epidemiol Biomark Prev 17:2891–2894. https://doi.org/10.1158/1055-9965.EPI-08-0335

    Article  CAS  Google Scholar 

  73. Low Y-L, Taylor JI, Grace PB, Dowsett M, Scollen S, Dunning AM, Mulligan AA, Welch AA, Luben RN, Khaw KT, Day NE, Wareham NJ, Bingham SA (2005) Phytoestrogen exposure correlation with plasma estradiol in postmenopausal women in European Prospective Investigation of Cancer and Nutrition-Norfolk may involve diet-gene interactions. Cancer Epidemiol Biomark Prev 14:213–220

    CAS  Google Scholar 

  74. Grace PB, Taylor JI, Low Y-L, Luben RN, Mulligan AA, Botting NP, Dowsett M, Welch AA, Khaw KT, 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 Biomark Prev 13:698–708

    CAS  Google Scholar 

  75. Low Y-L, Taylor JI, Grace PB, Dowsett M, Folkerd E, Doody D, Dunning AM, Scollen S, Mulligan AA, Welch AA, Luben RN, Khaw KT, Day NE, Wareham NJ, Bingham SA (2005) Polymorphisms in the CYP19 gene may affect the positive correlations between serum and urine phytoestrogen metabolites and plasma androgen concentrations in men. J Nutr 135:2680–2686

    CAS  PubMed  Google Scholar 

  76. Durazzo A, Carcea M, Adlercreutz H et al (2014) Effects of consumption of whole grain foods rich in lignans in healthy postmenopausal women with moderate serum cholesterol: a pilot study. Int J Food Sci Nutr 65:637–645. https://doi.org/10.3109/09637486.2014.893283

    Article  CAS  PubMed  Google Scholar 

  77. Travis RC, Spencer EA, Allen NE et al (2009) Plasma phyto-oestrogens and prostate cancer in the European prospective investigation into cancer and nutrition. Br J Cancer 100:1817–1823. https://doi.org/10.1038/sj.bjc.6605073

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Simon GA, Fletcher HM, Golden K, McFarlane-Anderson ND (2015) Urinary isoflavone and lignan phytoestrogen levels and risk of uterine fibroid in Jamaican women. Maturitas 82:170–175. https://doi.org/10.1016/j.maturitas.2015.06.041

    Article  CAS  PubMed  Google Scholar 

  79. 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 Biomark Prev 7:885–889

    CAS  Google Scholar 

  80. Valentín-Blasini L, Blount BC, Caudill SP, Needham LL (2003) Urinary and serum concentrations of seven phytoestrogens in a human reference population subset. J Expo Anal Environ Epidemiol 13:276–282

    PubMed  Google Scholar 

  81. Xie J, Tworoger SS, Franke AA, Terry KL, Rice MS, Rosner BA, Willett WC, Hankinson SE, Eliassen AH (2013) Plasma enterolactone and breast cancer risk in the nurses’ health study II. Breast Cancer Res Treat 139:801–809. https://doi.org/10.1007/s10549-013-2586-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Talaei M, Lee BL, Ong CN, van Dam RM, Yuan JM, Koh WP, Pan A (2016) Urine phyto-oestrogen metabolites are not significantly associated with risk of type 2 diabetes: the Singapore Chinese health study. Br J Nutr 115:1607–1615. https://doi.org/10.1017/S0007114516000581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Kunisue T, Tanabe S, Isobe T, Aldous KM, Kannan K (2010) Profiles of phytoestrogens in human urine from several Asian countries. J Agric Food Chem 58:9838–9846. https://doi.org/10.1021/jf102253j

    Article  CAS  PubMed  Google Scholar 

  84. Liu J, Mi S, Du L, Li X, Li P, Jia K, Zhao J, Zhang H, Zhao W, Gao Y (2018) The associations between plasma phytoestrogens concentration and metabolic syndrome risks in Chinese population. PLoS ONE 13:e0194639. https://doi.org/10.1371/journal.pone.0194639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Morton MS, Chan PS, Cheng C, Blacklock N, Matos-Ferreira A, Abranches-Monteiro L, Correia R, Lloyd S, Griffiths K (1997) Lignans and isoflavonoids in plasma and prostatic fluid in men: samples from Portugal, Hong Kong, and the United Kingdom. Prostate 32:122–128

    CAS  PubMed  Google Scholar 

  86. Ko K-P, Yeo Y, Yoon J-H, Kim C-S, Tokudome S, Ngoan LT, Koriyama C, Lim YK, Chang SH, Shin HR, Kang D, Park SK, Kang CH, Yoo KY (2018) Plasma phytoestrogens concentration and risk of colorectal cancer in two different Asian populations. Clin Nutr 37:1675–1682. https://doi.org/10.1016/j.clnu.2017.07.014

    Article  CAS  PubMed  Google Scholar 

  87. Morton MS, Arisaka O, Miyake N, Morgan LD, Evans BA (2002) Phytoestrogen concentrations in serum from Japanese men and women over forty years of age. J Nutr 132:3168–3171

    CAS  PubMed  Google Scholar 

  88. Johnsen NF, Hausner H, Olsen A, Tetens I, Christensen J, Knudsen KE, Overvad K, Tjønneland A (2004) Intake of whole grains and vegetables determines the plasma enterolactone concentration of Danish women. J Nutr 134:2691–2697. https://doi.org/10.1093/jn/134.10.2691

    Article  CAS  PubMed  Google Scholar 

  89. Micek A, Godos J, Brzostek T et al (2021) Dietary phytoestrogens and biomarkers of their intake in relation to cancer survival and recurrence: a comprehensive systematic review with meta-analysis. Nutr Rev 79(1):42–65. https://doi.org/10.1093/nutrit/nuaa043

    Article  PubMed  Google Scholar 

  90. Nurmi T, Mursu J, Peñalvo JL, Poulsen HE, Voutilainen S (2010) Dietary intake and urinary excretion of lignans in Finnish men. Br J Nutr 103:677–685. https://doi.org/10.1017/S0007114509992261

    Article  CAS  PubMed  Google Scholar 

  91. Hedelin M, Klint A, Chang ET, Bellocco R, Johansson J-E, Andersson SO, Heinonen SM, Adlercreutz H, Adami HO, Grönberg H, Bälter KA (2006) Dietary phytoestrogen, serum enterolactone and risk of prostate cancer: the cancer prostate Sweden study (Sweden). Cancer Causes Control 17:169–180

    PubMed  Google Scholar 

  92. Bhakta D, dos Santos SI, Higgins C, Sevak L, Kassam-Khamis T, Mangtani P, Adlercreutz H, McMichael A (2005) A semiquantitative food frequency questionnaire is a valid indicator of the usual intake of phytoestrogens by south Asian women in the UK relative to multiple 24-h dietary recalls and multiple plasma samples. J Nutr 135:116–123

    CAS  PubMed  Google Scholar 

  93. Bhakta D, Higgins CD, Sevak L, Mangtani P, Adlercreutz H, McMichael AJ, dos Santos SI (2006) Phyto-oestrogen intake and plasma concentrations in South Asian and native British women resident in England. Br J Nutr 95:1150–1158

    CAS  PubMed  Google Scholar 

  94. Mulligan AA, Kuhnle GG, Lentjes MA, van Scheltinga V, Powell NA, McTaggart A, Bhaniani A, Khaw KT (2013) Intakes and sources of isoflavones, lignans, enterolignans, coumestrol and soya-containing foods in the Norfolk arm of the European Prospective Investigation into Cancer and Nutrition (EPIC-Norfolk), from 7 d food diaries, using a newly updated database. Public Health Nutr 16:1454–1462. https://doi.org/10.1017/S1368980012003904

    Article  PubMed  Google Scholar 

  95. Witkowska AM, Waśkiewicz A, Zujko ME, Szcześniewska D, Stepaniak U, Pająk A, Drygas W (2018) Are total and individual dietary lignans related to cardiovascular disease and its risk factors in postmenopausal Women? A nationwide study. Nutrients 10:865. https://doi.org/10.3390/nu10070865

    Article  CAS  PubMed Central  Google Scholar 

  96. Linseisen J, Piller R, Hermann S, Chang-Claude J (2004) Dietary phytoestrogen intake and premenopausal breast cancer risk in a German case-control study. Int J Cancer 110:284–290

    CAS  PubMed  Google Scholar 

  97. Boker LK, Van der Schouw YT, De Kleijn MJ, Jacques PF, Grobbee DE, Peeters PH (2002) Intake of dietary phytoestrogens by Dutch women. J Nutr 132:1319–1328

    CAS  PubMed  Google Scholar 

  98. Milder IE, Feskens EJ, Arts IC, Bueno-de-Mesquita HB, Hollman PC, Kromhout D (2006) Intakes of 4 dietary lignans and cause-specific and all-cause mortality in the Zutphen elderly study. Am J Clin Nutr 84:400–405

    CAS  PubMed  Google Scholar 

  99. Pérez-Jiménez J, Fezeu L, Touvier M, Arnault N, Manach C, Hercberg S, Galan P, Scalbert A (2011) Dietary intake of 337 polyphenols in French adults. Am J Clin Nutr 93:1220–1228. https://doi.org/10.3945/ajcn.110.007096

    Article  CAS  PubMed  Google Scholar 

  100. Lefèvre-Arbogast S, Gaudout D, Bensalem J, Letenneur L, Dartigues JF, Hejblum BP, Féart C, Delcourt C, Samieri C (2019) Pattern of polyphenol intake and the long-term risk of dementia in older persons. Neurology 90:e1979–e1988. https://doi.org/10.1212/WNL.0000000000005607

    Article  CAS  Google Scholar 

  101. Pellegrini N, Valtueña S, Ardigò D, Brighenti F, Franzini L, Del Rio D, Scazzina F, Piatti PM, Zavaroni I (2010) Intake of the plant lignans matairesinol, secoisolariciresinol, pinoresinol, and lariciresinol in relation to vascular inflammation and endothelial dysfunction in middle age-elderly men and post-menopausal women living in Northern Italy. Nutr Metab Cardiovasc Dis 20:64–71. https://doi.org/10.1016/j.numecd.2009.02.003

    Article  CAS  PubMed  Google Scholar 

  102. Godos J, Marventano S, Mistretta A, Galvano F, Grosso G (2017) Dietary sources of polyphenols in the mediterranean healthy eating, aging and lifestyle (MEAL) study cohort. Int J Food Sci Nutr 68:750–756. https://doi.org/10.1080/09637486.2017.1285870

    Article  CAS  PubMed  Google Scholar 

  103. Godos J, Bergante S, Satriano A, Pluchinotta FR, Marranzano M (2018) Dietary phytoestrogen intake is inversely associated with hypertension in a cohort of adults living in the mediterranean area. Molecules 23:E368. https://doi.org/10.3390/molecules23020368

    Article  CAS  PubMed  Google Scholar 

  104. González S, Fernández M, Cuervo A, Lasheras C (2014) Dietary intake of polyphenols and major food sources in an institutionalised elderly population. J Hum Nutr Diet 27:176–183. https://doi.org/10.1111/jhn.12058

    Article  PubMed  Google Scholar 

  105. Zamora-Ros R, Not C, Guinó E, Luján-Barroso L, García RM, Biondo S, Salazar R, Moreno V (2013) Association between habitual dietary flavonoid and lignan intake and colorectal cancer in a Spanish case–control study (the Bellvitge Colorectal Cancer Study). Cancer Causes Control 24:549–557. https://doi.org/10.1007/s10552-012-9992-z

    Article  PubMed  Google Scholar 

  106. Tresserra-Rimbau A, Medina-Remón A, Pérez-Jiménez J (2013) Dietary intake and major food sources of polyphenols in a Spanish population at high cardiovascular risk: the PREDIMED study. Nutr Metab Cardiovasc Dis 23:953–959. https://doi.org/10.1016/j.numecd.2012.10.008

    Article  CAS  PubMed  Google Scholar 

  107. Mendonça RD, Carvalho NC, Martin-Moreno JM, Pimenta AM, Lopes ACS, Gea A, Martinez-Gonzalez MA, Bes-Rastrollo M (2019) Total polyphenol intake, polyphenol subtypes and incidence of cardiovascular disease: the SUN cohort study. Nutr Metab Cardiovasc Dis 29:69–78. https://doi.org/10.1016/j.numecd.2018.09.012

    Article  CAS  PubMed  Google Scholar 

  108. Petrick JL, Steck SE, Bradshaw PT, Chow W-H, Engel LS, He K, Risch HA, Vaughan TL, Gammon MD (2015) Dietary flavonoid intake and Barrett’s esophagus in western Washington State. Ann Epidemiol 25:730–735. https://doi.org/10.1016/j.annepidem.2015.05.010

    Article  PubMed  PubMed Central  Google Scholar 

  109. Petrick JL, Steck SE, Bradshaw PT, Trivers KF, Abrahamson PE, Engel LS, He K, Chow WH, Mayne ST, Risch HA, Vaughan TL, Gammon MD (2015) Dietary intake of flavonoids and oesophageal and gastric cancer: incidence and survival in the United States of America (USA). Br J Cancer 112:1291–1300. https://doi.org/10.1038/bjc.2015.25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Williams AM, Bonner M, Ochs-Balcom HM, Hwang H, Morrison C, McCann SE (2015) Dietary lignan intake and androgen receptor expression in breast tumors. Cancer Causes Control 26:311–317. https://doi.org/10.1007/s10552-014-0504-1

    Article  PubMed  Google Scholar 

  111. Waetjen LE, Leung K, Crawford SL, Huang M-H, Gold EB, Greendale GA (2013) The relationship between dietary phytoestrogens and development of urinary incontinence in midlife women. Menopause 20:428–436. https://doi.org/10.1097/gme.0b013e3182703c9c

    Article  PubMed  PubMed Central  Google Scholar 

  112. Bandera EV, King M, Chandran U, Paddock LE, Rodriguez-Rodriguez L, Olson SH (2011) Phytoestrogen consumption from foods and supplements and epithelial ovarian cancer risk: a population-based case control study. BMC Womens Health 11:40. https://doi.org/10.1186/1472-6874-11-40

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Chang ET, Canchola AJ, Clarke CA, Lu Y, West DW, Bernstein L, Wang SS, Horn-Ross PL (2011) Dietary phytocompounds and risk of lymphoid malignancies in the California Teachers Study cohort. Cancer Causes Control 22:237–249. https://doi.org/10.1007/s10552-010-9692-5

    Article  PubMed  Google Scholar 

  114. 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 122:229–235. https://doi.org/10.1007/s10549-009-0681-x

    Article  CAS  PubMed  Google Scholar 

  115. Mervish NA, Teitelbaum SL, Pajak A, Windham GC, Pinney SM, Kushi LH, Biro FM, Wolff MS (2017) Peripubertal dietary flavonol and lignan intake and age at menarche in a longitudinal cohort of girls. Pediatr Res 82:201–208. https://doi.org/10.1038/pr.2017.34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. van der Schouw YT, Sampson L, Willett WC, Rimm EB (2005) The usual intake of lignans but not that of isoflavones may be related to cardiovascular risk factors in U.S. men. J Nutr 135:260–266

    PubMed  Google Scholar 

  117. Horn-Ross PL, Hoggatt KJ, Lee MM (2002) Phytoestrogens and thyroid cancer risk: the San Francisco Bay Area thyroid cancer study. Cancer Epidemiol Prev Biomark 11:43–49

    CAS  Google Scholar 

  118. McCann SE, Freudenheim JL, Marshall JR, Graham S (2003) Risk of human ovarian cancer is related to dietary intake of selected nutrients, phytochemicals and food groups. J Nutr 133:1937–1942

    CAS  PubMed  Google Scholar 

  119. de Kleijn MJ, van der Schouw YT, Wilson PW, Adlercreutz H, Mazur W, Grobbee DE, Jacques PF (2001) Intake of dietary phytoestrogens is low in postmenopausal women in the United States: the Framingham study. J Nutr 131:1826–1832

    PubMed  Google Scholar 

  120. Chávez-Suárez KM, Ortega-Vélez MI, Valenzuela-Quintanar AI et al (2017) Phytoestrogen concentrations in human urine as biomarkers for dietary phytoestrogen intake in Mexican women. Nutrients 9:E1078. https://doi.org/10.3390/nu9101078

    Article  CAS  PubMed  Google Scholar 

  121. Park S-Y, Wilkens LR, Franke AA, Le Marchand L, Kakazu KK, Goodman MT, Murphy SP, Henderson BE, Kolonel LN (2009) Urinary phytoestrogen excretion and prostate cancer risk: a nested case–control study in the Multiethnic Cohort. Br J Cancer 101:185–191. https://doi.org/10.1038/sj.bjc.6605137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Hu Y, Song Y, Franke AA, Hu FB, van Dam RM, Sun Q (2015) A prospective investigation of the association between urinary excretion of dietary lignan metabolites and weight change in US women. Am J Epidemiol 182:503–511. https://doi.org/10.1093/aje/kwv091

    Article  PubMed  PubMed Central  Google Scholar 

  123. Reger MK, Zollinger TW, Liu Z, Jones J, Zhang J (2017) Association between urinary phytoestrogens and C-reactive protein in the continuous national health and nutrition examination survey. J Am Coll Nutr 36:434–441. https://doi.org/10.1080/07315724.2017.1318722

    Article  CAS  PubMed  Google Scholar 

  124. Martínez Steele E, Monteiro CA (2017) Association between dietary share of ultra-processed foods and urinary concentrations of phytoestrogens in the US. Nutrients 9:E209. https://doi.org/10.3390/nu9030209

    Article  PubMed  Google Scholar 

  125. Adlercreutz H, Fotsis T, Heikkinen R, Dwyer JT, Woods M, Goldin BR, Gorbach SL (1982) Excretion of the lignans enterolactone and enterodiol and of equol in omnivorous and vegetarian postmenopausal women and in women with breast cancer. Lancet 2:1295–1299

    CAS  PubMed  Google Scholar 

  126. Miles FL, Navarro SL, Schwarz Y, Gu H, Djukovic D, Randolph TW, Shojaie A, Kratz M, Hullar MAJ, Lampe PD, Neuhouser ML, Raftery D, Lampe JW (2017) Plasma metabolite abundances are associated with urinary enterolactone excretion in healthy participants on controlled diets. Food Funct 8:3209–3218. https://doi.org/10.1039/c7fo00684e

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Reger MK, Zollinger TW, Liu Z, Jones J, Zhang J (2016) Urinary phytoestrogens and cancer, cardiovascular, and all-cause mortality in the continuous National Health and Nutrition Examination Survey. Eur J Nutr 55:1029–1040. https://doi.org/10.1007/s00394-015-0917-y

    Article  CAS  PubMed  Google Scholar 

  128. Eichholzer M, Richard A, Nicastro HL, Platz EA, Linseisen J, Rohrmann S (2014) Urinary lignans and inflammatory markers in the US National Health and Nutrition Examination Survey (NHANES) 1999–2004 and 2005–2008. Cancer Causes Control 25:395–403. https://doi.org/10.1007/s10552-014-0340-3

    Article  PubMed  PubMed Central  Google Scholar 

  129. Valentín-Blasini L, Sadowski MA, Walden D, Caltabiano L, Needham LL, Barr DB (2005) Urinary phytoestrogen concentrations in the U.S. population (1999–2000). J Expo Anal Environ Epidemiol 15:509–523

    PubMed  Google Scholar 

  130. Sun Q, Wedick NM, Pan A, Townsend MK, Cassidy A, Franke AA, Rimm EB, Hu FB, van Dam RM (2014) Gut microbiota metabolites of dietary lignans and risk of type 2 diabetes: a prospective investigation in two cohorts of U.S. women. Diabetes Care 37:1287–1295. https://doi.org/10.2337/dc13-2513

    Article  PubMed  PubMed Central  Google Scholar 

  131. Levine LD, Kim K, Purdue-Smithe A, Sundaram R, Schisterman EF, Connell M, Devilbiss EA, Alkhalaf Z, Radoc JG, Buck Louis GM, Mumford SL (2019) Urinary phytoestrogens and relationship to menstrual cycle length and variability among healthy, eumenorrheic women. J Endocr Soc 4:bvz003. https://doi.org/10.1210/jendso/bvz003

  132. Stumpf K, Pietinen P, Puska P, Adlercreutz H (2000) Changes in serum enterolactone, genistein, and daidzein in a dietary intervention study in Finland. Cancer Epidemiol Biomark Prev 9:1369–1372

    CAS  Google Scholar 

  133. Pietinen P, Stumpf K, Männistö S, Kataja V, Uusitupa M, Adlercreutz H (2001) Serum enterolactone and risk of breast cancer: a case-control study in eastern Finland. Cancer Epidemiol Biomark Prev 10:339–344

    CAS  Google Scholar 

  134. 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 354:2112–2115

    CAS  PubMed  Google Scholar 

  135. Kilkkinen A, Erlund I, Virtanen MJ, Alfthan G, Ariniemi K, Virtamo J (2006) Serum enterolactone concentration and the risk of coronary heart disease in a case-cohort study of Finnish male smokers. Am J Epidemiol 163:687–693

    PubMed  Google Scholar 

  136. Vanharanta M, Voutilainen S, Nurmi T, Kaikkonen J, Roberts LJ, Morrow JD, Adlercreutz H, Salonen JT (2002) Association between low serum enterolactone and increased plasma F2-isoprostanes, a measure of lipid peroxidation. Atherosclerosis 160:465–469

    CAS  PubMed  Google Scholar 

  137. Kilkkinen A, Stumpf K, Pietinen P, Valsta LM, Tapanainen H, Adlercreutz H (2001) Determinants of serum enterolactone concentration. Am J Clin Nutr 73:1094–1100

    CAS  PubMed  Google Scholar 

  138. Vanharanta M, Voutilainen S, Rissanen TH, Adlercreutz H, Salonen JT (2003) Risk of cardiovascular disease-related and all-cause death according to serum concentrations of enterolactone: Kuopio Ischaemic Heart Disease Risk Factor Study. Arch Intern Med 163:1099–1104

    CAS  PubMed  Google Scholar 

  139. Sonestedt E, Ivarsson MIL, Harlid S, Ericson U, Gullberg B, Carlson J, Olsson H, Adlercreutz H, Wirfält E (2009) The protective association of high plasma enterolactone with breast cancer is reasonably robust in women with polymorphisms in the estrogen receptor alpha and beta genes. J Nutr 139:993–1001. https://doi.org/10.3945/jn.108.101691

    Article  CAS  PubMed  Google Scholar 

  140. Stattin P, Bylund A, Biessy C, Kaaks R, Hallmans G, Adlercreutz H (2004) Prospective study of plasma enterolactone and prostate cancer risk (Sweden). Cancer Causes Control 15:1095–1102

    PubMed  Google Scholar 

  141. Lin Y, Wolk A, Håkansson N, Peñalvo JL, Lagergren J, Adlercreutz H, Lu Y (2013) Validation of FFQ-based assessment of dietary lignans compared with serum enterolactone in Swedish women. Br J Nutr 109:1873–1880. https://doi.org/10.1017/S000711451200387X

    Article  CAS  PubMed  Google Scholar 

  142. 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 41:168–176

    PubMed  Google Scholar 

  143. Aarestrup J, Kyrø C, Knudsen KEB, Weiderpass E, Christensen J, Kristensen M, Würtz AM, Johnsen NF, Overvad K, Tjønneland A, Olsen A (2013) Plasma enterolactone and incidence of endometrial cancer in a case-cohort study of Danish women. Br J Nutr 109:2269–2275. https://doi.org/10.1017/S0007114512004424

    Article  CAS  PubMed  Google Scholar 

  144. Eriksen AK, Kyrø C, Nørskov NP, Frederiksen K, Bach Knudsen K-E, Overvad K, Landberg R, Tjønneland A, Olsen A (2019) Pre-diagnostic plasma enterolactone concentrations are associated with lower mortality among individuals with type 2 diabetes: a case-cohort study in the Danish Diet, Cancer and Health cohort. Diabetologia 62:959–969. https://doi.org/10.1007/s00125-019-4854-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Verheus M, van Gils CH, Keinan-Boker L, Grace PB, Bingham SA, Peeters PH (2007) Plasma phytoestrogens and subsequent breast cancer risk. J Clin Oncol 25:648–655

    CAS  PubMed  Google Scholar 

  146. Heald CL, Ritchie MR, Bolton-Smith C, Morton MS, Alexander FE (2007) Phyto-oestrogens and risk of prostate cancer in Scottish men. Br J Nutr 98:388–396

    CAS  PubMed  Google Scholar 

  147. Piller R, Chang-Claude J, Linseisen J (2006) Plasma enterolactone and genistein and the risk of premenopausal breast cancer. Eur J Cancer Prev 15:225–232

    CAS  PubMed  Google Scholar 

  148. Horner NK, Kristal AR, Prunty J, Skor HE, Potter JD, Lampe JW (2002) Dietary determinants of plasma enterolactone. Cancer Epidemiol Biomark Prev 11:121–126

    CAS  Google Scholar 

  149. Ko KP, Yeo Y, Yoon JH et al (2018) Plasma phytoestrogens concentration and risk of colorectal cancer in two different Asian populations. Clin Nutr 37:1675–1682. https://doi.org/10.1016/j.clnu.2017.07.014

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This research was funded by the Instituto de Salud Carlos III through the grants CP15/00100 and PI18/00191 (Co-funded by the European Regional Development Fund. ERDF, a way to build Europe); and by La Marató de TV3 (project 201943-30). We thank CERCA Program/Generalitat de Catalunya for institutional support. LR-B, MF-N and RZ-R would like to thank the program were supported by the “PFIS” (FI20/00006), “Sara Borrell” (CD20/00036) and the “Miguel Servet” (CPII20/00009) programs from the Institute of Health Carlos III (Co-funded by the European Social Fund (ESF)—ESF investing in your future), respectively.

Author information

Authors and Affiliations

  1. Unit of Nutrition and Cancer, Cancer Epidemiology Research Program, Catalan Institute of Oncology, Bellvitge Biomedical Research Institute (IDIBELL), Av Gran Via 199-203, 08908, L’Hospitalet de Llobregat, Barcelona, Spain

    Lucia Rizzolo-Brime, Elida M. Caro-Garcia, Cynthia A. Alegre-Miranda & Raul Zamora-Ros

  2. Research and Development Unit, Parc Sanitari Sant Joan de Déu, Barcelona, Spain

    Mireia Felez-Nobrega

Authors
  1. Lucia Rizzolo-Brime
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elida M. Caro-Garcia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cynthia A. Alegre-Miranda
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mireia Felez-Nobrega
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Raul Zamora-Ros
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Raul Zamora-Ros.

Ethics declarations

Conflict of interest

The authors are not aware of any conflicts of interest.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 26 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rizzolo-Brime, L., Caro-Garcia, E.M., Alegre-Miranda, C.A. et al. Lignan exposure: a worldwide perspective. Eur J Nutr 61, 1143–1165 (2022). https://doi.org/10.1007/s00394-021-02736-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-021-02736-4

Keywords

Search

Navigation