Gut Microbial Metabolism of Plant Lignans: Influence on Human Health

Diet-Microbe Interactions in the Gut: Effects on Human Health and Disease

Volumn , Issue , 2015, Pages 103-117

  Yoder, Seth C ^a   Lancaster, Samuel M ^b   Hullar, Meredith A J ^a   Lampe, Johanna W ^a  

^a USA   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Chronic disease; Enterodiol; Enterolactone; Gut microbiota; Humans; Lignans

Indexed keywords

EID: 84942090869     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-0-12-407825-3.00007-1     Document Type: Chapter

References (123)

1. Ayres D., Loike J. Lignans: Chemical, Biological and Clinical Properties 1990, Cambridge University Press, Cambridge.
2. Umezawa T. Diversity in lignan biosynthesis. Phytochem Rev 2003, 2:371-390.
3. Hearon W.M., MacGregor W.S. The naturally occurring lignans. Chemical Rev 1955, 55:957-1068.
4. Pan J.-Y., Chen S.-L., Yang M.-H., Wu J., Sinkkonen J., Zou K. An update on lignans: natural products and synthesis. Nat Prod Rep 2009, 26:1251-1292.
5. Gang D.R., Dinkova-Kostova A.T., Davin L.B., Lewis N.G. Phylogenetic links in plant defense systems: lignans, isoflavonoids, and their reductases. Phytochemicals for Pest Control 1997, 59-89. American Chemical Society, Washington, DC. P.A. Hedin, R.M. Hollingworth, E.P. Masler, J. Miyamoto (Eds.).
6. Mäki-Arvela P., Holmbom B., Salmi T., Murzin D.Y. Recent progress in synthesis of fine and specialty chemicals from wood and other biomass by heterogeneous catalytic processes. Catal Rev 2007, 49:197-340.
7. Holmbom B., Eckerman C., Eklund P., et al. Knots in trees - a new rich source of lignans. Phytochem Rev 2003, 2:331-340.
8. Cesarino I., Araújo P., Domingues Júnior A.P., Mazzafera P. An overview of lignin metabolism and its effect on biomass recalcitrance. Braz J Bot 2012, 35:303-311.
9. Davin L.B., Jourdes M., Patten A.M., Kim K.-W., Vassão D.G., Lewis N.G. Dissection of lignin macromolecular configuration and assembly: comparison to related biochemical processes in allyl/propenyl phenol and lignan biosynthesis. Nat Prod Rep 2008, 25:1015-1090.
10. Cunha W.R., Luis M., Sola R.C., et al. Lignans: chemical and biological properties. Phytochemicals - A Global Perspective of Their Role in Nutrition and Health 2012, 213-234. InTech, Rijeka, Croatia. V. Rao (Ed.).
11. Harmatha J., Dinan L. Biological activities of lignans and stilbenoids associated with plant-insect chemical interactions. Phytochem Rev 2003, 2:321-330.
12. Lewis N.G., Kato M.J., Lopes N., Davin L.B. Lignans: diversity, biosynthesis, and function. Chemistry of the Amazon 1995, 135-167. American Chemical Society, Washington, DC. P.R. Seidl, O.R. Gottlieb, M.A.C. Kaplan (Eds.).
13. Milder I.E.J., Arts I.C.W., Van de Putte B., Venema D.P., Hollman P.C.H. Lignan contents of Dutch plant foods: a database including lariciresinol, pinoresinol, secoisolariciresinol and matairesinol. Br J Nutr 2005, 93:393-402.
14. Smeds A.I., Eklund P.C., Willför S.M. Content, composition, and stereochemical characterisation of lignans in berries and seeds. Food Chem 2012, 134:1991-1998.
15. Smeds A.I., Eklund P.C., Sjöholm R.E., et al. Quantification of a broad spectrum of lignans in cereals, oilseeds, and nuts. J Agric Food Chem 2007, 55:1337-1346.
16. Peñalvo J.L., Haajanen K.M., Botting N., Adlercreutz H. Quantification of lignans in food using isotope dilution gas chromatography/mass spectrometry. J Agric Food Chem 2005, 53:9342-9347.
17. Blitz C.L., Murphy S.P., Au D.L.M. Adding lignan values to a food composition database. J Food Compos Anal 2007, 20:99-105.
18. Mazur W.M., Wähälä K., Rasku S., Salakka A., Hase T., Adlercreutz H. Lignan and isoflavonoid concentrations in tea and coffee. Br J Nutr 1998, 79:37-45.
19. Nurmi T., Heinonen S., Mazur W., Deyama T., Nishibe S., Adlercreutz H. Lignans in selected wines. Food Chem 2003, 83:303-309.
20. Borriello S.P., Setchell K.D., Axelson M., Lawson A.M. Production and metabolism of lignans by the human faecal flora. J Appl Bacteriol 1985, 58:37-43.
21. Setchell K.D.R., Adlercreutz H. The excretion of two new phenolic compounds (Compound 180/442 and Compound 180/410) during the human menstrual cycle and in pregnancy. J Steroid Biochem 1979, 11:xv-xvi.
22. Stitch S.R., Toumba J.K., Groen M.B., et al. Excretion, isolation and structure of a new phenolic constituent of female urine. Nature 1980, 287:738-740.
23. Axelson M., Sjövall J., Gustafsson B.E., Setchell K.D.R. Origin of lignans in mammals and identification of a precursor from plants. Nature 1982, 298:659-660.
24. Axelson M., Setchell K.D. The excretion of lignans in rats - evidence for an intestinal bacterial source for this new group of compounds. FEBS Lett 1981, 123:337-342.
25. Setchell K.D., Lawson A.M., Borriello S.P., et al. Lignan formation in man-microbial involvement and possible roles in relation to cancer. Lancet 1981, 2:4-7.
26. Clavel T., Doré J., Blaut M. Bioavailability of lignans in human subjects. Nutr Res Rev 2006, 19:187-196.
27. Lampe J.W., Atkinson C., Hullar M.A. Assessing exposure to lignans and their metabolites in humans. J AOAC Int 2006, 89:1174-1181.
28. Eeckhaut E., Struijs K., Possemiers S., Vincken J.-P., Keukeleire D.D., Verstraete W. Metabolism of the lignan macromolecule into enterolignans in the gastrointestinal lumen as determined in the simulator of the human intestinal microbial ecosystem. J Agric Food Chem 2008, 56:4806-4812.
29. Wang L.Q., Meselhy M.R., Li Y., Qin G.W., Hattori M. Human intestinal bacteria capable of transforming secoisolariciresinol diglucoside to mammalian lignans, enterodiol and enterolactone. Chem Pharm Bull 2000, 48:1606-1610.
30. Wang L. Mammalian phytoestrogens: enterodiol and enterolactone. J Chromatogr, B: Anal Technol Biomed Life Sci 2002, 777:289-309.
31. Landete J.M. Plant and mammalian lignans: a review of source, intake, metabolism, intestinal bacteria and health. Food Res Int 2012, 46:410-424.
32. Clavel T., Borrmann D., Braune A., Doré J., Blaut M. Occurrence and activity of human intestinal bacteria involved in the conversion of dietary lignans. Anaerobe 2006, 12:140-147.
33. Clavel T., Lippman R., Gavini F., Doré J., Blaut M. Clostridium saccharogumia sp. nov. and Lactonifactor longoviformis gen. nov., sp. nov., two novel human faecal bacteria involved in the conversion of the dietary phytoestrogen secoisolariciresinol diglucoside. Syst Appl Microbiol 2007, 30:16-26.
34. Clavel T., Henderson G., Engst W., Doré J., Blaut M. Phylogeny of human intestinal bacteria that activate the dietary lignan secoisolariciresinol diglucoside. FEMS Microbiol Ecol 2006, 55:471-478.
35. Roncaglia L., Amaretti A., Raimondi S., Leonardi A., Rossi M. Role of bifidobacteria in the activation of the lignan secoisolariciresinol diglucoside. Appl Microbiol Biotechnol 2011, 92:159-168.
36. Jin J.-S., Hattori M. Human intestinal bacterium, strain END-2 is responsible for demethylation as well as lactonization during plant lignan metabolism. Biol Pharm Bull 2010, 33:1443-1447.
37. Xie L.-H., Akao T., Hamasaki K., Deyama T., Hattori M. Biotransformation of pinoresinol diglucoside to mammalian lignans by human intestinal microflora, and isolation of Enterococcus faecalis strain PDG-1 responsible for the transformation of (+)-pinoresinol to (+)-lariciresinol. Chem Pharm Bull 2003, 51:508-515.
38. Jin J.-S., Kakiuchi N., Hattori M. Enantioselective oxidation of enterodiol to enterolactone by human intestinal bacteria. Biol Pharm Bull 2007, 30:2204-2206.
39. Jin J.-S., Zhao Y.-F., Nakamura N., et al. Enantioselective dehydroxylation of enterodiol and enterolactone precursors by human intestinal bacteria. Biol Pharm Bull 2007, 30:2113-2119.
40. Liu C., Finegold S.M., Song Y., Lawson P.A. Reclassification of Clostridium coccoides, Ruminococcus hansenii, Ruminococcus hydrogenotrophicus, Ruminococcus luti, Ruminococcus productus and Ruminococcus schinkii as Blautia coccoides gen. nov., comb. nov., Blautia hansenii comb. nov., Blautia hydroge. Int J Syst Evol Microbiol 2008, 58:1896-1902.
41. Coulman K.D., Liu Z., Hum W.Q., Michaelides J., Thompson L.U. Whole sesame seed is as rich a source of mammalian lignan precursors as whole flaxseed. Nutr Cancer 2005, 52:156-165.
42. Peñalvo J.L., Heinonen S.-M., Aura A.-M., Adlercreutz H. Dietary sesamin is converted to enterolactone in humans. J Nutr 2005, 135:1056-1062.
43. Jan K.-C., Hwang L.S., Ho C.-T. Biotransformation of sesaminol triglucoside to mammalian lignans by intestinal microbiota. J Agric Food Chem 2009, 57:6101-6106.
44. Liu Z., Saarinen N.M., Thompson L.U. Sesamin is one of the major precursors of mammalian lignans in sesame seed (Sesamum indicum) as observed in vitro and in rats. J Nutr 2006, 136:906-912.
45. Zhu X., Zhang X., Sun Y., et al. Purification and fermentation in vitro of sesaminol triglucoside from sesame cake by human intestinal microbiota. J Agric Food Chem 2013, 61:1868-1877.
46. Saarinen N.M., Smeds A.I., Peñalvo J.L., Nurmi T., Adlercreutz H., Mäkelä S. Flaxseed ingestion alters ratio of enterolactone enantiomers in human serum. J Nutr Metab 2010, http://dx.doi.org/10.1155/2010/403076.
47. Jin J.-S., Hattori M. Further studies on a human intestinal bacterium Ruminococcus sp. END-1 for transformation of plant lignans to mammalian lignans. J Agric Food Chem 2009, 57:7537-7542.
48. Jin J.-S., Tobo T., Chung M.-H., Ma C., Hattori M. Transformation of trachelogenin, an aglycone of tracheloside from safflower seeds, to phytoestrogenic (-)-enterolactone by human intestinal bacteria. Food Chem 2012, 134:74-80.
49. Adlercreutz H. Lignans and human health. Crit Rev Clin Lab Sci 2007, 44:483-525.
50. Buck K., Zaineddin A.K., Vrieling A., Linseisen J., Chang-Claude J. Meta-analyses of lignans and enterolignans in relation to breast cancer risk. Am J Clin Nutr 2010, 92:141-153.
51. Cardoso Carraro J.C., Dantas MI de S, Espeschit A.C.R., Martino H.S.D., Ribeiro S.M.R. Flaxseed and human health: reviewing benefits and adverse effects. Food Rev Int 2012, 28:203-230.
52. Cassidy A., Hanley B., Lamuela-Raventos R.M. Isoflavones, lignans and stilbenes - origins, metabolism and potential importance to human health. J Sci Food Agric 2000, 80:1044-1062.
53. Cornwell T., Cohick W., Raskin I. Dietary phytoestrogens and health. Phytochemistry 2004, 65:995-1016.
54. Gikas P.D., Mokbel K. Phytoestrogens and the risk of breast cancer: a review of the literature. Int J Fertil Women's Med 2005, 50:250-258.
55. Peterson J., Dwyer J., Adlercreutz H., Scalbert A., Jacques P., McCullough M.L. Dietary lignans: physiology and potential for cardiovascular disease risk reduction. Nutr Rev 2010, 68:571-603.
56. Bedell S., Nachtigall M., Naftolin F. The pros and cons of plant estrogens for menopause. J Steroid Biochem Mol Biol 2014, 139:225-236.
57. Velentzis L.S., Cantwell M.M., Cardwell C., Keshtgar M.R., Leathem A.J., Woodside J.V. Lignans and breast cancer risk in pre- and post-menopausal women: meta-analyses of observational studies. Br J Cancer 2009, 100:1492-1498.
58. Touré A., Xueming X. Flaxseed lignans: source, biosynthesis, metabolism, antioxidant activity, bio-active components, and health benefits. Compr Rev Food Sci Food Saf 2010, 9:261-269.
59. Webb A.L., McCullough M.L. Dietary lignans: potential role in cancer prevention. Nutr Cancer 2005, 51:117-131.
60. McCann M.J., Gill C.I.R., McGlynn H., Rowland I.R. Role of mammalian lignans in the prevention and treatment of prostate cancer. Nutr Cancer 2005, 52:1-14.
61. Saarinen N.M., Tuominen J., Pylkkänen L., Santti R. Assessment of information to substantiate a health claim on the prevention of prostate cancer by lignans. Nutrients 2010, 2:99-115.
62. Heinonen S., Nurmi T., Liukkonen K., et al. In vitro metabolism of plant lignans: new precursors of mammalian lignans enterolactone and enterodiol. J Agric Food Chem 2001, 49:3178-3186.
63. Aehle E., Müller U., Eklund P.C., Willför S.M., Sippl W., Dräger B. Lignans as food constituents with estrogen and antiestrogen activity. Phytochemistry 2011, 72:2396-2405.
64. Kurzer M.S., Xu X. Dietary phytoestrogens. Annu Rev Nutr 1997, 17:353-381.
65. Mueller S.O., Simon S., Chae K., Metzler M., Korach K.S. Phytoestrogens and their human metabolites show distinct agonistic and antagonistic properties on estrogen receptor alpha (ERalpha) and ERbeta in human cells. Toxicol Sci 2004, 80:14-25.
66. Adolphe J.L., Whiting S.J., Juurlink B.H.J., Thorpe L.U., Alcorn J. Health effects with consumption of the flax lignan secoisolariciresinol diglucoside. Br J Nutr 2010, 103:929-938.
67. Penttinen P., Jaehrling J., Damdimopoulos A.E., et al. Diet-derived polyphenol metabolite enterolactone is a tissue-specific estrogen receptor activator. Endocrinology 2007, 148:4875-4886.
68. Saleem M., Kim H.J., Ali M.S., Lee Y.S. An update on bioactive plant lignans. Nat Prod Rep 2005, 22:696-716.
69. Lof M., Weiderpass E. Epidemiologic evidence suggests that dietary phytoestrogen intake is associated with reduced risk of breast, endometrial, and prostate cancers. Nutr Res 2006, 26:609-619.
70. Zeleniuch-Jacquotte A., Lundin E., Micheli A., et al. Circulating enterolactone and risk of endometrial cancer. Int J Cancer 2006, 119:2376-2381.
71. Bandera E.V., Williams M.G., Sima C., et al. Phytoestrogen consumption and endometrial cancer risk: a population-based case-control study in New Jersey. Cancer Causes Control 2009, 20:1117-1127.
72. Zamora-Ros R., Agudo A., Luján-Barroso L., et al. Dietary flavonoid and lignan intake and gastric adenocarcinoma risk in the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Am J Clin Nutr 2012, 96:1398-1408.
73. Cotterchio M., Boucher B.A., Manno M., Gallinger S., Okey A., Harper P. Dietary phytoestrogen intake is associated with reduced colorectal cancer risk. J Nutr 2006, 136:3046-3053.
74. Kuijsten A., Arts I.C.W., Hollman P.C.H., van't Veer P., Kampman E. Plasma enterolignans are associated with lower colorectal adenoma risk. Cancer Epidemiol Biomarkers Prev 2006, 15:1132-1136.
75. Johnsen N.F., Olsen A., Thomsen B.L.R., et al. Plasma enterolactone and risk of colon and rectal cancer in a case-cohort study of Danish men and women. Cancer Causes & Control 2010, 21:153-162.
76. Buck K., Zaineddin A.K., Vrieling A., et al. Estimated enterolignans, lignan-rich foods, and fibre in relation to survival after postmenopausal breast cancer. Br J Cancer 2011, 105:1151-1157.
77. Guglielmini P., Rubagotti A., Boccardo F. Serum enterolactone levels and mortality outcome in women with early breast cancer: a retrospective cohort study. Breast Cancer Res Treat 2012, 132:661-668.
78. Anderson L.N., Cotterchio M., Boucher B.A., Kreiger N. Phytoestrogen intake from foods, during adolescence and adulthood, and risk of breast cancer by estrogen and progesterone receptor tumor subgroup among Ontario women. Int J Cancer 2013, 132:1683-1692.
79. McCann S.E., Hootman K.C., Weaver A.M., et al. Dietary intakes of total and specific lignans are associated with clinical breast tumor characteristics. J Nutr 2012, 142:91-98.
80. Truan J.S., Chen J.-M., Thompson L.U. Comparative effects of sesame seed lignan and flaxseed lignan in reducing the growth of human breast tumors (MCF-7) at high levels of circulating estrogen in athymic mice. Nutr Cancer 2012, 64:65-71.
81. Mabrok H.B., Klopfleisch R., Ghanem K.Z., Clavel T., Blaut M., Loh G. Lignan transformation by gut bacteria lowers tumor burden in a gnotobiotic rat model of breast cancer. Carcinogenesis 2012, 33:203-208.
82. McCann M.J., Rowland I.R., Roy N.C. Anti-proliferative effects of physiological concentrations of enterolactone in models of prostate tumourigenesis. Mol Nutr Food Res 2013, 57:212-224.
83. Ward H.A., Kuhnle G.G.C. Phytoestrogen consumption and association with breast, prostate and colorectal cancer in EPIC Norfolk. Arch Biochem Biophys 2010, 501:170-175.
84. Jackson M.D., McFarlane-Anderson N.D., Simon G.A., Bennett F.I., Walker S.P. Urinary phytoestrogens and risk of prostate cancer in Jamaican men. Cancer Causes Control 2010, 21:2249-2257.
85. Ward H.A., Kuhnle G.G.C., Mulligan A.A., Lentjes M.A.H., Luben R.N., Khaw K. Breast, colorectal, and prostate cancer risk in the European Prospective Investigation into Cancer and Nutrition-Norfolk in relation to phytoestrogen intake derived from an improved database. Am J Clin Nutr 2010, 91:440-448.
86. Kuhnle G.G.C., Dell'Aquila C., Aspinall S.M., Runswick S.A., Mulligan A.A., Bingham S.A. Phytoestrogen content of foods of animal origin: dairy products, eggs, meat, fish, and seafood. J Agric Food Chem 2008, 56:10099-10104.
87. Peñalvo J.L., López-Romero P. Urinary enterolignan concentrations are positively associated with serum HDL cholesterol and negatively associated with serum triglycerides in U.S. adults. J Nutr 2012, 142:751-756.
88. Pietrofesa R., Turowski J., Tyagi S., et al. Radiation mitigating properties of the lignan component in flaxseed. BMC Cancer 2013, 13:179.
89. Sonestedt E., Wirfält E. Enterolactone and breast cancer: methodological issues may contribute to conflicting results in observational studies. Nutr Res 2010, 30:667-677.
90. Kuijsten A., Arts I.C.W., Vree T.B. Hollman PCH. Pharmacokinetics of enterolignans in healthy men and women consuming a single dose of secoisolariciresinol diglucoside. J Nutr 2005, 135:795-801.
91. Possemiers S., Bolca S., Eeckhaut E., Depypere H., Verstraete W. Metabolism of isoflavones, lignans and prenylflavonoids by intestinal bacteria: producer phenotyping and relation with intestinal community. FEMS Microbiol Ecol 2007, 61:372-383.
92. Lampe J.W., Chang J.-L. Interindividual differences in phytochemical metabolism and disposition. Semin Cancer Biol 2007, 17:347-353.
93. Setchell K., Adlercreutz H. Mammalian lignans and phytoestrogens. Recent studies on their formation, metabolism, and biological role in health and disease. Role of the Gut Flora in Toxicity and Cancer 1988, 316-345. Academic Press, London. I.R. Rowland (Ed.).
94. Adlercreutz H., Van der Wildt J., Kinzel J. Lignan and isoflavonoid conjugates in human urine. J Steroid Biochem Mol Biol 1995, 52:97-103.
95. Jansen G.H.E., Arts I.C.W., Nielen M.W.F., Müller M., Hollman P.C.H., Keijer J. Uptake and metabolism of enterolactone and enterodiol by human colon epithelial cells. Arch Biochem Biophys 2005, 435:74-82.
96. Jacobs E., Kulling S.E., Metzler M. Novel metabolites of the mammalian lignans enterolactone and enterodiol in human urine. J Steroid Biochem Mol Biol 1999, 68:211-218.
97. Okura T., Ibe M., Umegaki K., Shinozuka K., Yamada S. Effects of dietary ingredients on function and expression of P-Glycoprotein in human intestinal epithelial cells. Biol Pharm Bull 2010, 33:255-259.
98. Adlercreutz H., Fotsis T., Bannwart C., et al. Determination of urinary lignans and phytoestrogen metabolites, potential antiestrogens and anticarcinogens, in urine of women on various habitual diets. J Steroid Biochem 1986, 25:791-797.
99. Stumpf K., Pietinen P., Puska P., Adlercreutz H. Changes in serum enterolactone, genistein, and daidzein in a dietary intervention study in Finland. Cancer Epidemiol Biomarkers Prev 2000, 9:1369-1372.
100. Mazur W.M., Uehara M., Wähälä K., Adlercreutz H. Phyto-oestrogen content of berries, and plasma concentrations and urinary excretion of enterolactone after a single strawberry-meal in human subjects. Br J Nutr 2000, 83:381-387.
101. Kirkman L.M., Lampe J.W., Campbell D.R., Martini M.C., Slavin J.L. Urinary lignan and isoflavonoid excretion in men and women consuming vegetable and soy diets. Nutr Cancer 1995, 24:1-12.
102. Juntunen K.S., Mazur W.M., Liukkonen K.H., et al. Consumption of wholemeal rye bread increases serum concentrations and urinary excretion of enterolactone compared with consumption of white wheat bread in healthy Finnish men and women. Br J Nutr 2000, 84:839-846.
103. Vanharanta M., Mursu J., Nurmi T., et al. Phloem fortification in rye bread elevates serum enterolactone level. Eur J Clin Nutr 2002, 56:952-957.
104. McIntosh G.H., Noakes M., Royle P.J., Foster P.R. Whole-grain rye and wheat foods and markers of bowel health in overweight middle-aged men. Am J Clin Nutr 2003, 77:967-974.
105. Kristensen M.B., Hels O., Tetens I. No changes in serum enterolactone levels after eight weeks' intake of rye-bran products in healthy young men. Scandinavian Journal of Food & Nutrition 2005, 49:62-67.
106. Knust U., Spiegelhalder B., Strowitzki T., Owen R.W. Contribution of linseed intake to urine and serum enterolignan levels in German females: a randomised controlled intervention trial. Food Chem Toxicol 2006, 44:1057-1064.
107. Lampe J.W., Martini M.C., Kurzer M.S., Adlercreutz H., Slavin J.L. Urinary lignan and isoflavonoid excretion in premenopausal women consuming flaxseed powder. Am J Clin Nutr 1994, 60:122-128.
108. Kurzer M.S., Lampe J.W., Martini M.C., Adlercreutz H. Fecal lignan and isoflavonoid excretion in premenopausal women consuming flaxseed powder. Cancer Epidemiol Biomarkers Prev 1995, 4:353-358.
109. Nesbitt P.D., Lam Y., Thompson L.U. Human metabolism of mammalian lignan precursors in raw and processed flaxseed. Am J Clin Nutr 1999, 69:549-555.
110. Kuijsten A., Arts I.C.W., van't Veer P., Hollman P.C.H. The relative bioavailability of enterolignans in humans is enhanced by milling and crushing of flaxseed. J Nutr 2005, 135:2812-2816.
111. Aura A.-M., Myllymäki O., Bailey M., Penalvo J.L., Adlercreutz H., Poutanen K. Interrelationships between carbohydrate type, phenolic acids and initial pH on in vitro conversion of enterolactone from rye lignans. Dietary Fibre: Components and Functions 2007, 235-245. Wageningen Academic Publishers, Wageningen, The Netherlands. H. Salovaara, F. Gates, M. Tenkanen (Eds.).
112. Adlercreutz H., Honjo H., Higashi A., et al. Urinary excretion of lignans and isoflavonoid phytoestrogens in Japanese men and women consuming a traditional Japanese diet. Am J Clin Nutr 1991, 54:1093-1100.
113. Horner N.K., Kristal A.R., Prunty J., Skor H.E., Potter J.D., Lampe J.W. Dietary determinants of plasma enterolactone. Cancer Epidemiol Biomarkers Prev 2002, 11:121-126.
114. Lampe J.W., Gustafson D.R., Hutchins A.M., et al. Urinary isoflavonoid and lignan excretion on a Western diet: relation to soy, vegetable, and fruit intake. Cancer Epidemiol Biomarkers Prev 1999, 8:699-707.
115. Milder I.E.J., Kuijsten A., Arts I.C.W., et al. Relation between plasma enterodiol and enterolactone and dietary intake of lignans in a Dutch endoscopy-based population. J Nutr 2007, 137:1266-1271.
116. Kilkkinen A., Stumpf K., Pietinen P., Valsta L.M., Tapanainen H., Adlercreutz H. Determinants of serum enterolactone concentration. Am J Clin Nutr 2001, 73:1094-1100.
117. Jacobs D.R., Pereira M.A., Stumpf K., Pins J.J., Adlercreutz H. Whole grain food intake elevates serum enterolactone. Br J Nutr 2002, 88:111-116.
118. Cunnane S.C., Hamadeh M.J., Liede A.C., Thompson L.U., Wolever T.M., Jenkins D.J. Nutritional attributes of traditional flaxseed in healthy young adults. Am J Clin Nutr 1995, 61:62-68.
119. Clavel T., Henderson G., Alpert C.-A., et al. Intestinal bacterial communities that produce active estrogen-like compounds enterodiol and enterolactone in humans. Appl Environ Microbiol 2005, 71:6077-6085.
120. Lampe J.W., Fredstrom S.B., Slavin J.L., Potter J.D. Sex differences in colonic function: a randomised trial. Gut 1993, 34:531-536.
121. Kilkkinen A., Pietinen P., Klaukka T., Virtamo J., Korhonen P., Adlercreutz H. Use of oral antimicrobials decreases serum enterolactone concentration. Am J Epidemiol 2002, 155:472-477.
122. Johnsen N.F., Hausner H., Olsen A., et al. Intake of whole grains and vegetables determines the plasma enterolactone concentration of Danish women. J Nutr 2004, 134:2691-2697.
123. Rybak M.E., Sternberg M.R., Pfeiffer C.M. Sociodemographic and lifestyle variables are compound- and class-specific correlates of urine phytoestrogen concentrations in the U.S. population. J Nutr 2013, 1-9.