Metabolism of isoflavones, lignans and prenylflavonoids by intestinal bacteria: Producer phenotyping and relation with intestinal community

FEMS Microbiology Ecology

Volumn 61, Issue 2, 2007, Pages 372-383

  Possemiers, Sam ^a   Bolca, Selin ^a   Eeckhaut, Ellen ^a   Depypere, Herman ^b   Verstraete, Willy ^a  

^a GHENT UNIVERSITY   (Belgium)

^b GHENT UNIVERSITY HOSPITAL   (Belgium)

Author keywords

Intestinal bacteria; Isoflavones; Lignans; Methanogens; Prenylflavonoids; Sulfate reducing bacteria

Indexed keywords

8 PRENYLNARINGENIN; DAIDZEIN; ENTERODIOL; ENTEROLACTONE; EQUOL; ISOFLAVONE; ISOXANTHOHUMOL; LIGNAN; O NORANGOLENSIN; PHYTOESTROGEN; UNCLASSIFIED DRUG;

ESTROGENIC COMPOUND; METABOLISM; METHANOGENIC BACTERIUM; ORGANIC COMPOUND; PHENOTYPE; SULFATE-REDUCING BACTERIUM;

ADULT; AGED; ARTICLE; BACTERIAL COUNT; BACTERIAL METABOLISM; CLOSTRIDIUM; CLOSTRIDIUM COCCOIDES; CORRELATION ANALYSIS; EUBACTERIUM; EUBACTERIUM RECTALE; FEMALE; HUMAN; INTESTINE FLORA; METHANOGEN; MICROBIAL ACTIVITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL;

BACTERIA; CLOSTRIDIUM; COLONY COUNT, MICROBIAL; EUBACTERIUM; FECES; FLAVONOIDS; HUMANS; INTESTINES; ISOFLAVONES; LIGNANS; PHENOTYPE; PHYTOESTROGENS;

BACTERIA (MICROORGANISMS); CLOSTRIDIUM COCCOIDES; EUBACTERIUM RECTALE;

EID: 34447532076     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2007.00330.x     Document Type: Article

References (90)

1. Agradi E, Vegeto E, Sozzi A, Fico G, Regondi S Tome F (2006) Traditional healthy Mediterranean diet: estrogenic activity of plants used as food and flavoring agents. Phytother Res 20 : 670 675.
2. Akaza H, Miyanaga N, Takashima N et al 2004) Comparisons of percent equol producers between prostate cancer patients and controls: case-controlled studies of isoflavones in Japanese, Korean and American residents. Jpn J Clin Oncol 34 : 86 89.
3. Altman DG (1991) Practical statistics for medical research. Chapman & Hall, London.
4. Arai Y, Uehara M, Sato Y, Kimira M, Eboshida A, Adlercreutz H Watanabe S (2000) Comparison of isoflavones among dietary intake, plasma concentration and urinary excretion for accurate estimation of phytoestrogen intake. J Epidemiol 10 : 127 135.
5. Atkinson C, Berman S, Humbert O Lampe JW (2004) In vitro incubation of human feces with daidzein and antibiotics suggests interindividual differences in the bacteria responsible for equol production. J Nutr 134 : 596 599.
6. Atkinson C, Frankenfeld CL Lampe JW (2005) Gut bacterial metabolism of the soy isoflavone daidzein: exploring the relevance to human health. Exp Biol Med 230 : 155 170.
7. Atkinson C, Lampe JW, Scholes D, Chen C, Wahala K Schwartz SM (2006) Lignan and isoflavone excretion in relation to uterine fibroids: a case-control study of young to middle-aged women in the United States. Am J Clin Nutr 84 : 587 593.
8. Bennets HW, Underwood EJ Shier FL (1946) A specific breeding problem of sheep on subterranean clover pastures in Western Australia. Aust Vet J 22 : 2 12.
9. Berg JO, Nord CE Wadstrom T (1978) Formation of glycosidases in batch and continuous cultures of Bacteroides fragilis. Appl Environ Microbiol 35 : 269 273.
10. Blair RM, Appt SE, Franke AA Clarkson TB (2003) Treatment with antibiotics reduces plasma equol concentration in cynomolgus monkeys (Macaca fascicularis). J Nutr 133 : 2262 2267.
11. Blakesmith SJ, Lyons-Wall PM, Joannou GE, Petocz P Samman S (2005) Urinary isoflavonoid excretion is inversely associated with the ratio of protein to dietary fibre intake in young women. Eur J Clin Nutr 59 : 284 290.
12. Boker LK, Van der Schouw YT, De Kleijn MJJ, Jacques PF, Grobbee DE Peeters PHM (2002) Intake of dietary phytoestrogens by Dutch women. J Nutr 132 : 1319 1328.
13. Boon N, Top EM, Verstraete W Siciliano SD (2003) Bioaugmentation as a tool to protect the structure and function of an activated-sludge microbial community against a 3-chloroaniline shock load. Appl Environ Microbiol 69 : 1511 1520.
14. Borriello SP, Setchell KDR, Axelson M Lawson AM (1985) Production and metabolism of lignans by the human fecal flora. J Appl Bacteriol 58 : 37 43.
15. Bowey E, Adlercreutz H Rowland I (2003) Metabolism of isoflavones and lignans by the gut microflora: a study in germ-free and human flora associated rats. Food Chem Toxicol 41 : 631 636.
16. Chen AM Rogan WJ (2004) Isoflavones in soy infant formula: a review of evidence for endocrine and other activity in infants. Ann Rev Nutr 24 : 33 54.
17. Clavel T, Fallani M, Lepage P et al 2005a) Isoflavones and functional foods alter the dominant intestinal microbiota in postmenopausal women. J Nutr 135 : 2786 2792.
18. Clavel T, Henderson G, Alpert CA, Philippe C, Rigottier-Gois L, Dore J Blaut M (2005b) Intestinal bacterial communities that produce active estrogen-like compounds enterodiol and enterolactone in humans. Appl Environ Microbiol 71 : 6077 6085.
19. Coldham NG Sauer MJ (2001) Identification, quantitation and biological activity of phytoestrogens in a dietary supplement for breast enhancement. Food Chem Toxicol 39 : 1211 1224.
20. Cornwell T, Cohick W Raskin I (2004) Dietary phytoestrogens and health. Phytochemistry 65 : 995 1016.
21. Cummings JH Englyst HN (1987) Fermentation in the human large intestine and the available substrates. Am J Clin Nutr 45 : 1243 1255.
22. Cunnane SC, Hamadeh MJ, Liede AC, Thompson LU, Wolever TMS Jenkins DJA (1995) Nutritional attributes of traditional flaxseed in healthy-young adults. Am J Clin Nutr 61 : 62 68.
23. Decroos K, Vanhemmens S, Cattoir S, Boon N Verstraete W (2005) Isolation and characterisation of an equol-producing mixed microbial culture from a human faecal sample and its activity under gastrointestinal conditions. Arch Microbiol 183 : 45 55.
24. Duncan AM, Merz-Demlow BE, Xu X, Phipps WR Kurzer MS (2000) Premenopausal equol excretors show plasma hormone profiles associated with lowered risk of breast cancer. Cancer Epidemiol Biomarkers Prev 9 : 581 586.
25. El Oufir L, Flourie B, desVarannes SB, Barry JL, Cloarec D, Bornet F Galmiche JP (1996) Relations between transit time, fermentation products, and hydrogen consuming flora in healthy humans. Gut 38 : 870 877.
26. Fernandes J, Wolever TMS Rao AV (1998) Increased serum cholesterol in healthy human methane producers is confounded by age. J Nutr 128 : 1349 1354.
27. Fernandes J, Rao AV Wolever TMS (2000) Different substrates and methane producing status affect short-chain fatty acid profiles produced by in vitro fermentation of human feces. J Nutr 130 : 1932 1936.
28. Florin THJ, Zhu G, Kirk KM Martin NG (2000) Shared and unique environmental factors determine the ecology of methanogens in humans and rats. Am J Gastroenterol 95 : 2872 2879.
29. Gibson GR (1990) Physiology and ecology of the sulphate-reducing bacteria. J Appl Bacteriol 69 : 769 797.
30. Gibson GR, Cummings JH Macfarlane GT (1988a) Competition for hydrogen between sulfate reducing bacteria and methanogenic bacteria from the human large intestine. J Appl Bacteriol 65 : 241 247.
31. Gibson GR, Macfarlane GT Cummings JH (1988b) Occurrence of sulfate reducing bacteria in human feces and the relationship of dissimilatory sulfate reduction to methanogenesis in the large gut. J Appl Bacteriol 65 : 103 111.
32. Gibson GR, Macfarlane GT Cummings JH (1993) Sulfate reducing bacteria and hydrogen metabolism in the human large intestine. Gut 34 : 437 439.
33. Hales BA, Edwards C, Ritchie DA, Hall G, Pickup RW Saunders JR (1996) Isolation and identification of methanogen-specific DNA from blanket bog feat by PCR amplification and sequence analysis. Appl Environ Microbiol 62 : 668 675.
34. Heinonen S, Wahala K Adlercreutz H (1999) Identification of isoflavone metabolites dihydrodaidzein, dihydrogenistein, 6′-OH-O-DMA, and cis-4-OH-equol in human urine by gas chromatography-mass spectroscopy using authentic reference compounds. Anal Biochem 274 : 211 219.
35. Hoey L, Rowland IR, Lloyd AS, Clarke DB Wiseman H (2004) Influence of soya-based infant formula consumption on isoflavone and gut microflora metabolite concentrations in urine and on faecal microflora composition and metabolic activity in infants and children. Br J Nutr 91 : 607 616.
36. Hutchins AM, Slavin JL Lampe JW (1995) Urinary isoflavonoid phytoestrogen and lignan excretion after consumption of fermented and unfermented soy products. J Am Diet Assoc 95 : 545 551.
37. Hutchins AM, Martini MC, Olson BA, Thomas W Slavin JL (2000) Flaxseed influences urinary lignan excretion in a dose-dependent manner in postmenopausal women. Cancer Epidemiol Biomarkers Prev 9 : 1113 1118.
38. Joannou GE, Kelly GE, Reeder AY, Waring M Nelson C (1995) A urinary profile study of dietary phytoestrogens - the identification and mode of metabolism of new isoflavonoids. J Steroid Biochem Mol Biol 54 : 167 184.
39. Johnsson P, Kamal-Eldin A, Lundgren LN Aman P (2000) HPLC method for analysis of secoisolariciresinol diglucoside in flaxseeds. J Agric Food Chem 48 : 5216 5219.
40. Kelly GE, Nelson C, Waring MA, Joannou GE Reeder AY (1993) Metabolites of dietary (soya) isoflavones in human urine. Clin Chim Acta 223 : 9 22.
41. 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 : 122 128.
42. Kelly GE, Joannou GE, Reeder AY, Nelson C Waring MA (1995) The variable metabolic response to dietary isoflavones in humans. Proc Soc Exp Biol Med 208 : 40 43.
43. Lampe JW, Karr SC, Hutchins AM Slavin JL (1998) Urinary equol excretion with a soy challenge: influence of habitual diet. Proc Soc Exp Biol Med 217 : 335 339.
44. Lampe JW, Atkinson C Hullar MAJ (2006) Assessing exposure to lignans and their metabolites in humans. J AOAC Int 89 : 1174 1181.
45. Levitt MD, Furne JK, Kuskowski M Ruddy J (2006) Stability of human methanogenic flora over 35 years and a review of insights obtained from breath methane measurements. Clin Gastroenterol Hepatol 4 : 123 129.
46. Lin C Miller TL (1998) Phylogenetic analysis of Methanobrevibacter isolated from feces of humans and other animals. Arch Microbiol 169 : 397 403.
47. MacGregor CA, Canney PA, Patterson G, McDonald R Paul J (2005) A randomised double-blind controlled trial of oral soy supplements versus placebo for treatment of menopausal symptoms in patients with early breast cancer. Eur J Cancer 41 : 708 714.
48. Magee PJ Rowland IR (2004) Phytoestrogens, their mechanism of action: current evidence for a role in breast and prostate cancer. Br J Nutr 91 : 513 531.
49. Marrian GF Haslewood GAD (1932) Equol, a new inactive phenol isolated from the ketohydroxyoestrin fraction of mares' urine. Biochem J 26 : 1227 1232.
50. Maubach J, Bracke ME, Heyerick A, Depypere HT, Serreyn RF, Mareel MM De Keukeleire D (2003) Quantitation of soy-derived phytoestrogens in human breast tissue and biological fluids by high-performance liquid chromatography. J Chromatogr B 784 : 137 144.
51. Mazur W Adlercreutz H (2000) Overview of naturally occurring endocrine-active substances in the human diet in relation to human health. Nutrition 16 : 654 658.
52. McKay LF, Eastwood MA Brydon WG (1985) Methane excretion in man - a study of breath, flatus, and feces. Gut 26 : 69 74.
53. Melcher EA, Levitt MD Slavin JL (1991) Methane production and bowel function parameters in healthy subjects on low-fiber and high-fiber diets. Nutr Cancer 16 : 85 92.
54. Messina M, Kucuk O Lampe JW (2006) An overview of the health effects of isoflavones with an emphasis on prostate cancer risk and prostate-specific antigen levels. J AOAC Int 89 : 1121 1134.
55. Milder IEJ, Arts ICW, van de Putte B, Venema DP Hollman PCH (2005a) Lignan contents of Dutch plant foods: a database including lariciresinol, pinoresinol, secoisolariciresinol and matairesinol. Br J Nutr 93 : 393 402.
56. Milder IEJ, Feskens EJM, Arts ICW, de Mesquita HBB, Hollman PCH Kromhout D (2005b) Intake of the plant lignans secoisolariciresinol, matairesinol, lariciresinol, and pinoresinol in Dutch men and women. J Nutr 135 : 1202 1207.
57. Miller LT Wolin MJ (1981) Fermentation by the human large intestine microbial community in an in vitro semicontinuous culture system. Appl Environ Microbiol 42 : 400 407.
58. Miller TL Wolin MJ (1983) Oxidation of hydrogen and reduction of methanol to methane is the sole energy source for a methanogen isolated from human feces. J Bacteriol 153 : 1051 1055.
59. Miller TL Wolin MJ (1986) Methanogens in human and animal intestinal tracts. Syst Appl Microbiol 7 : 223 229.
60. Milligan SR, Kalita JC, Heyerick A, Rong H, De Cooman L De Keukeleire D (1999) Identification of a potent phytoestrogen in hops (Humulus lupulus L.) and beer. J Clin Endocrinol Metab 84 : 2249 2252.
61. Nesbitt PD, Lam Y Thompson LU (1999) Human metabolism of mammalian lignan precursors in raw and processed flaxseed. Am J Clin Nutr 69 : 549 555.
62. Ososki AL Kennelly EJ (2003) Phytoestrogens: a review of the present state of research. Phytother Res 17 : 845 869.
63. Possemiers S, Heyerick A, Robbens V, De Keukeleire D Verstraete W (2005) Activation of proestrogens from hops (Humulus lupulus L.) by intestinal microbiota; conversion of isoxanthohumol into 8-prenylnaringenin. J Agric Food Chem 53 : 6281 6288.
64. Possemiers S, Bolca S, Grootaert C et al 2006) The prenylflavonoid isoxanthohumol from hops (Humulus lupulus L.) is activated into the potent phytoestrogen 8-prenylnaringenin in vitro and in the human intestine. J Nutr 136 : 1862 1867.
65. Raffaelli B, Hoikkala A, Leppala E Wahala K (2002) Enterolignans. J Chromatogr B 777 : 29 43.
66. Rasier G, Toppari J, Parent AS Bourguignon JP (2006) Female sexual maturation and reproduction after prepubertal exposure to estrogens and endocrine disrupting chemicals: a review of rodent and human data. Mol Cell Endocrinol 254 : 187 201.
67. Rinttila T, Kassinen A, Malinen E, Krogius L Palva A (2004) Development of an extensive set of 16S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. J Appl Microbiol 97 : 1166 1177.
68. Robert C, Del'Homme C Bernalier-Donadille A (2001) Interspecies H2 transfer in cellulose degradation between fibrolytic bacteria and H2-utilizing microorganisms from the human colon. FEMS Microbiol Lett 205 : 209 214.
69. Rossiter RC Beck AB (1966) Physiological and ecological studies on the estrogenic isoflavones in subterranean clover (Trifolium subterraneum) I. Effects of temperature. Aust J Agric Res 17 : 29 37.
70. Rowland I, Wiseman H, Sanders T, Adlercreutz H Bowey E (1999) Metabolism of oestrogens and phytoestrogens: role of the gut microflora. Biochem Soc Trans 27 : 304 308.
71. 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 : 27 32.
72. Setchell KDR Adlercreutz H (1979) Excretion of 2 new phenolic compounds (compound 180-442 and compound 180-410) during the human menstrual cycle and in pregnancy. J Steroid Biochem Mol Biol 11 : R15 R16.
73. Setchell KDR Cole SJ (2006) Method of defining equol-producer status and its frequency among vegetarians. J Nutr 136 : 2188 2193.
74. Setchell KDR, Borriello SP, Hulme P, Kirk DN Axelson M (1984) Nonsteroidal estrogens of dietary origin - Possible roles in hormone-dependent disease. Am J Clin Nutr 40 : 569 578.
75. Setchell KDR, Lawson AM, Mitchell FL, Adlercreutz H, Kirk DN Axelson M (1980) Lignans in man and in animal species. Nature 287 : 740 742.
76. Setchell KDR, Brown NM Lydeking-Olsen E (2002) The clinical importance of the metabolite equol - A clue to the effectiveness of soy and its isoflavones. J Nutr 132 : 3577 3584.
77. Setchell KDR, Brown NM, Desai PB et al 2003) Bioavailability, disposition, and dose-response effects of soy isoflavones when consumed by healthy women at physiologically typical dietary intakes. J Nutr 133 : 1027 1035.
78. Sirtori CR, Arnoldi A Johnson SK (2005) Phytoestrogens: end of a tale? Ann Med 37 : 423 438.
79. Song KB, Atkinson C, Frankenfeld CL, Jokela T, Wahala K, Thomas WK Lampe JW (2006) Prevalence of daidzein-metabolizing phenotypes differs between Caucasian and Korean American women and girls. J Nutr 136 : 1347 1351.
80. Stephen AM, Wiggins HS, Englyst HN, Cole TJ, Wayman BJ Cummings JH (1986) The effect of age, sex and level of intake of dietary fiber from wheat on large bowel function in 30 healthy subjects. Br J Nutr 56 : 349 361.
81. Stevens JF, Taylor AW Deinzer ML (1999) Quantitative analysis of xanthohumol and related prenylflavonoids in hops and beer by liquid chromatography tandem mass spectrometry. J Chromatogr A 832 : 97 107.
82. Stitch SR, Toumba JK, Groen MB, Funke CW, Leemhuis J, Vink J Woods GF (1980) Excretion, isolation and structure of a new phenolic constituent of female urine. Nature 287 : 738 740.
83. Taylor AH Al-Azzawi F (2000) Immunolocalisation of oestrogen receptor beta in human tissues. J Mol Endocrinol 24 : 145 155.
84. Thompson LU, Robb P, Serraino M Cheung F (1991) Mammalian lignan production from various foods. Nutr Cancer 16 : 43 52.
85. Turner NJ, Thomson BM Shaw IC (2003) Bioactive isoflavones in functional foods: the importance of gut microflora on bioavailability. Nutr Rev 61 : 204 213.
86. Valsta LM, Kilkkinen A, Mazur W et al 2003) Phyto-oestrogen database of foods and average intake in Finland. Br J Nutr 89 : S31 S38.
87. Wang LQ (2002) Mammalian phytoestrogens: enterodiol and enterolactonee. J Chromatogr B 777 : 289 309.
88. Wang LQ, Meselhy MR, Li Y, Qin GW Hattori M (2000) Human intestinal bacteria capable of transforming secoisolariciresinol diglucoside to mammalian lignans, enterodiol and enterolactonee. Chem Pharm Bull 48 : 1606 1610.
89. Wathen CN (2006) Alternatives to hormone-replacement therapy: a multi-method study of women's experiences. Complement Ther Med 14 : 185 192.
90. Zhang CZ, Wang SX, Zhang Y, Chen JP Liang XM (2005) In vitro estrogenic activities of Chinese medicinal plants traditionally used for the management of menopausal symptoms. J Ethnopharmacol 98 : 295 300.