Plasma enterolactone and risk of colon and rectal cancer in a case-cohort study of Danish men and women

Cancer Causes and Control

Volumn 21, Issue 1, 2010, Pages 153-162

  Johnsen, Nina Føns ^a   Olsen, Anja ^a   Thomsen, Birthe Lykke Riegels ^a   Christensen, Jane ^a   Egeberg, Rikke ^a   Bach Knudsen, Knud Erik ^b   Loft, Steffen ^c   Overvad, Kim ^d   Tjønneland, Anne ^a  

^a INSTITUTE OF CANCER EPIDEMIOLOGY   (Denmark)

^b DANISH INSTITUTE OF AGRICULTURAL SCIENCES   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d AALBORG UNIVERSITY HOSPITAL   (Denmark)

Author keywords

Antibiotics; Cancer; Enterolactone; Lignans; Phytoestrogens

Indexed keywords

ANTIBIOTIC AGENT; ENTEROLACTONE; LIGNAN; NONSTEROID ANTIINFLAMMATORY AGENT; PHYTOESTROGEN;

ADULT; ARTICLE; BLOOD SAMPLING; CANCER RISK; COHORT ANALYSIS; COLORECTAL CANCER; CONTROLLED STUDY; DENMARK; DISEASE ASSOCIATION; FEMALE; FLUOROIMMUNOASSAY; FOOD FREQUENCY QUESTIONNAIRE; HORMONE SUBSTITUTION; HUMAN; LIFESTYLE; MAJOR CLINICAL STUDY; MALE; PLASMA; PRIORITY JOURNAL; QUESTIONNAIRE; RISK ASSESSMENT;

4-BUTYROLACTONE; CASE-CONTROL STUDIES; COHORT STUDIES; COLONIC NEOPLASMS; DENMARK; FEMALE; FOOD HABITS; HUMANS; LIFE STYLE; LIGNANS; MALE; MIDDLE AGED; PHYTOESTROGENS; RECTAL NEOPLASMS; RISK FACTORS;

EID: 74149090692     PISSN: 09575243     EISSN: 15737225     Source Type: Journal    
DOI: 10.1007/s10552-009-9445-5     Document Type: Article

References (65)

1. NM Saarinen A Smeds SI Makela, et al. 2002 Structural determinants of plant lignans for the formation of enterolactone in vivo J Chromatogr B Analyt Technol Biomed Life Sci 777 311 319 10.1016/S1570-0232(02)00339-2 1:CAS:528:DC%2BD38Xos1Wrurs%3D 12270222 (Pubitemid 35257879)
2. W Mazur 1998 Phytoestrogen content in foods Baillieres Clin Endocrinol Metab 12 729 742 10.1016/S0950-351X(98)80013-X 1:STN:280:DyaK1Mzht1yitA%3D%3D 10384822 (Pubitemid 29261280)
3. W Mazur H Adlercreutz 1998 Natural and anthropogenic environmental oestrogens: the scientific basis for risk assessment Pure Appl Chem 70 1759 1776 10.1351/pac199870091759 1:CAS:528:DyaK1MXhtVWlsrk%3D
4. M Axelson KD Setchell 1981 The excretion of lignans in rats-evidence for an intestinal bacterial source for this new group of compounds FEBS Lett 123 337 342 10.1016/0014-5793(81)80322-5 1:CAS:528:DyaL3MXktl2ks70%3D 6262113
5. SR Stitch JK Toumba MB Groen, et al. 1980 Excretion, isolation and structure of a new phenolic constituent of female urine Nature 287 738 740 10.1038/287738a0 1:CAS:528:DyaL3MXhvV2ju7s%3D 7432490 (Pubitemid 11216455)
6. PD Nesbitt Y Lam LU Thompson 1999 Human metabolism of mammalian lignan precursors in raw and processed flaxseed Am J Clin Nutr 69 549 555 1:CAS:528:DyaK1MXhslWntrw%3D 10075344
7. IR Rowland H Wiseman TA Sanders H Adlercreutz EA Bowey 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 10.1207/S15327914NC3601-5 1:CAS:528:DC%2BD3cXjtF2msrY%3D 10798213
8. H Adlercreutz 2002 Phyto-oestrogens and cancer Lancet Oncol 3 364 373 10.1016/S1470-2045(02)00777-5 12107024 (Pubitemid 34661986)
9. A Kilkkinen P Pietinen T Klaukka J Virtamo P Korhonen H Adlercreutz 2002 Use of oral antimicrobials decreases serum enterolactone concentration Am J Epidemiol 155 472 477 10.1093/aje/155.5.472 11867359 (Pubitemid 34174159)
10. KD Setchell AM Lawson FL Mitchell H Adlercreutz DN Kirk M Axelson 1980 Lignans in man and in animal species Nature 287 740 742 10.1038/287740a0 1:CAS:528:DyaL3MXhvV2ju7g%3D 6253812 (Pubitemid 11216456)
11. H Adlercretutz R Heikkinen M Woods T Fotsis JT Dwyer BR Goldin 1982 Excretion of the lignans enterolactone and enterodiol and of equol in omnivorous and vegetarian postmenopausal women and in women with breast cancer Lancet 11 1295 1298 10.1016/S0140-6736(82)91507-0
12. SO Mueller S Simon K Chae M Metzler KS Korach 2004 Phytoestrogens and their human metabolites show distinct agonistic and antagonistic properties on estrogen receptor alpha (ERalpha) and ERbeta in human cells Toxicol Sci 80 14 25 10.1093/toxsci/kfh147 1:CAS:528:DC%2BD2cXkvVSrs7g%3D 15084758 (Pubitemid 38967392)
13. P Penttinen J Jaehrling AE Damdimopoulos, et al. 2007 Diet-derived polyphenol metabolite enterolactone is a tissue-specific estrogen receptor activator Endocrinology 148 4875 4886 10.1210/en.2007-0289 1:CAS:528: DC%2BD2sXhtFWls7nJ 17628008 (Pubitemid 47481543)
14. DD Kitts YV Yuan AN Wijewickreme LU Thompson 1999 Antioxidant activity of the flaxseed lignan secoisolariciresinol diglucoside and its mammalian lignan metabolites enterodiol and enterolactone Moll Cell Biochem 202 91 100 10.1023/A:1007022329660 1:CAS:528:DC%2BD3cXhsFGjurk%3D
15. HB Niemeyer M Metzler 2003 Differences in the antioxidant capacity of plant and mammalian lignans J Food Eng 56 255 256 10.1016/S0260-8774(02)00263-7 (Pubitemid 35384658)
16. K Prasad 2000 Antioxidant activity of secoisolariciresinol diglucoside-derived metabolites, secoisolariciresinol, enterodiol, and enterolactone Int J Angiol 9 220 225 10.1007/BF01623898 11062311
17. N Danbara T Yuri M Tsujita-Kyutoku R Tsukamoto N Uehara A Tsubura 2005 Enterolactone induces apoptosis and inhibits growth of Colo 201 human colon cancer cells both in vitro and in vivo Anticancer Res 25 2269 2276 1:CAS:528:DC%2BD2MXmtl2gsrw%3D 16158974
18. Y Mousavi H Adlercreutz 1992 Enterolactone and estradiol inhibit each other's proliferative effect on MCF-7 breast cancer cells in culture J Steroid Biochem Mol Biol 41 615 619 10.1016/0960-0760(92)90393-W 1:CAS:528: DyaK38XktVWitLc%3D 1562532
19. JD Brooks LU Thompson 2005 Mammalian lignans and genistein decrease the activities of aromatase and 17beta-hydroxysteroid dehydrogenase in MCF-7 cells J Steroid Biochem Mol Biol 94 461 467 10.1016/j.jsbmb.2005.02.002 1:CAS:528:DC%2BD2MXjvVKktrg%3D 15876411 (Pubitemid 40616407)
20. MK Sung M Lautens LU Thompson 1998 Mammalian lignans inhibit the growth of estrogen-independent human colon tumor cells Anticancer Res 18 1405 1408 1:CAS:528:DyaK1cXltF2ks7o%3D 9673348
21. PA Konstantinopoulos A Kominea G Vandoros, et al. 2003 Oestrogen receptor beta (ERbeta) is abundantly expressed in normal colonic mucosa, but declines in colon adenocarcinoma paralleling the tumour's dedifferentiation Eur J Cancer 39 1251 1258 10.1016/S0959-8049(03)00239-9 1:CAS:528:DC%2BD3sXjvFeluro%3D 12763213 (Pubitemid 36579196)
22. O Wada-Hiraike M Warner JA Gustafsson 2006 New developments in oestrogen signalling in colonic epithelium Biochem Soc Trans 34 1114 1116 10.1042/BST0341114 1:CAS:528:DC%2BD28XhtFKgtLfN 17073763 (Pubitemid 46772912)
23. F Castiglione A Taddei DR Degl'Innocenti, et al. 2008 Expression of estrogen receptor beta in colon cancer progression Diagn Mol Pathol 17 231 236 10.1097/PDM.0b013e3181656d67 1:CAS:528:DC%2BD1cXhsVajtLzK 19034156
24. N Jassam SM Bell V Speirs P Quirke 2005 Loss of expression of oestrogen receptor beta in colon cancer and its association with Dukes' staging Oncol Rep 14 17 21 1:CAS:528:DC%2BD2MXmt1ChtLs%3D 15944762
25. LQ Xie JP Yu HS Luo 2004 Expression of estrogen receptor beta in human colorectal cancer World J Gastroenterol 10 214 217 1:CAS:528: DC%2BD2cXhsVOrsrY%3D 14716825
26. N Hebert-Croteau 1998 A meta-analysis of hormone replacement therapy and colon cancer in women Cancer Epidemiol Biomarkers Prev 7 653 659 1:CAS:528:DyaK1cXls1Sjt74%3D 9718216
27. HD Nelson LL Humphrey P Nygren SM Teutsch JD Allan 2002 Postmenopausal hormone replacement therapy: scientific review JAMA 288 872 881 10.1001/jama.288.7.872 1:CAS:528:DC%2BD38Xmt1yitL8%3D 12186605
28. A Kuijsten PC Hollman HC Boshuizen, et al. 2008 Plasma enterolignan concentrations and colorectal cancer risk in a nested case-control study Am J Epidemiol 167 734 742 10.1093/aje/kwm349 18192676
29. H Ward G Chapelais GG Kuhnle R Luben KT Khaw S Bingham 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 Biomarkers Prev 17 2891 2894 10.1158/1055-9965.EPI-08- 0335 1:CAS:528:DC%2BD1cXht1egt7nN 18843034
30. A Tjonneland A Olsen K Boll, et al. 2007 Study design, exposure variables, and socioeconomic determinants of participation in Diet, Cancer and Health: a population-based prospective cohort study of 57,053 men and women in Denmark Scand J Public Health 35 432 441 10.1080/14034940601047986 17786808 (Pubitemid 47386794)
31. K Overvad A Tjonneland J Haraldsdottir M Ewertz OM Jensen 1991 Development of a semiquantitative food frequency questionnaire to assess food, energy and nutrient intake in Denmark Int J Epidemiol 20 900 905 10.1093/ije/20.4.900 1:STN:280:DyaK387pt12ntA%3D%3D 1800428
32. A Tjonneland K Overvad J Haraldsdottir S Bang M Ewertz OM Jensen 1991 Validation of a semiquantitative food frequency questionnaire developed in Denmark Int J Epidemiol 20 906 912 10.1093/ije/20.4.906 1:STN:280: DyaK387pt12ntQ%3D%3D 1800429
33. A Tjonneland J Haraldsdottir K Overvad C Stripp M Ewertz OM Jensen 1992 Influence of individually estimated portion size data on the validity of a semiquantitative food frequency questionnaire Int J Epidemiol 21 770 777 10.1093/ije/21.4.770 1:STN:280:DyaK38zpsVOlug%3D%3D 1521982
34. Lauritsen J (1998) Foodcalc 1.3
35. CJ Probert PM Emmett KW Heaton 1993 Intestinal transit time in the population calculated from self made observations of defecation J Epidemiol Community Health 47 331 333 10.1136/jech.47.4.331 1:STN:280: DyaK2c%2FksFCjsQ%3D%3D 8228773
36. D Gaist HT Sorensen J Hallas 1997 The Danish prescription registries Dan Med Bull 44 445 448 1:STN:280:DyaK1c%2FhslKlug%3D%3D 9377907
37. H Adlercreutz GJ Wang O Lapcik, et al. 1998 Time-resolved fluoroimmunoassay for plasma enterolactone Anal Biochem 265 208 215 10.1006/abio.1998.2886 1:CAS:528:DyaK1MXitVygtQ%3D%3D 9882394 (Pubitemid 29002063)
38. K Stumpf M Uehara T Nurmi H Adlercreutz 2000 Changes in the time-resolved fluoroimmunoassay of plasma enterolactone Anal Biochem 284 153 157 10.1006/abio.2000.4655 1:CAS:528:DC%2BD3cXlsVGqs7c%3D 10933868 (Pubitemid 30679123)
39. RL Prentice 1986 A case-cohort design for epidemiologic cohort studies and disease prevention trials Biometrika 73 1 11 10.1093/biomet/73.1.1
40. WE Barlow L Ichikawa D Rosner S Izumi 1999 Analysis of case-cohort designs J Clin Epidemiol 52 1165 1172 10.1016/S0895-4356(99)00102-X 1:STN:280:DC%2BD3c%2Fks1OntA%3D%3D 10580779 (Pubitemid 29535416)
41. DY Lin LJ Wei 1989 The robust inference for the cox proportional hazards model J Am Stat Assoc 84 1074 1078 10.2307/2290085
42. NF Johnsen H Hausner A Olsen, et al. 2004 Intake of whole grains and vegetables determines the plasma enterolactone concentration of Danish women J Nutr 134 2691 2697 1:CAS:528:DC%2BD2cXosV2jtbc%3D 15465768
43. NF Johnsen J Christensen BL Thomsen, et al. 2006 Physical activity and risk of colon cancer in a cohort of Danish middle-aged men and women Eur J Epidemiol 21 877 884 10.1007/s10654-006-9076-z 17160429 (Pubitemid 46197154)
44. NK Horner AR Kristal J Prunty HE Skor JD Potter JW Lampe 2002 Dietary determinants of plasma enterolactone Cancer Epidemiol Biomarkers Prev 11 121 126 1:CAS:528:DC%2BD38XhvFGiur4%3D 11815409
45. K Hulten A Winkvist P Lenner R Johansson H Adlercreutz G Hallmans 2002 An incident case-referent study on plasma enterolactone and breast cancer risk Eur J Nutr 41 168 176 10.1007/s00394-002-0373-3 1:CAS:528:DC%2BD38XosVSnurw%3D 12242585 (Pubitemid 36056326)
46. A Kilkkinen K Stumpf P Pietinen LM Valsta H Tapanainen H Adlercreutz 2001 Determinants of serum enterolactone concentration Am J Clin Nutr 73 1094 1100 1:CAS:528:DC%2BD3MXktlWhsrk%3D 11382665
47. JW Lampe DR Gustafson AM Hutchins, et al. 1999 Urinary isoflavonoid and lignan excretion on a Western diet: relation to soy, vegetable, and fruit intake Cancer Epidemiol Biomarkers Prev 8 699 707 1:CAS:528:DyaK1MXnslyqtr0%3D 10744130
48. IE Milder A Kuijsten IC Arts, et al. 2007 Relation between plasma enterodiol and enterolactone and dietary intake of lignans in a Dutch endoscopy-based population J Nutr 137 1266 1271 1:CAS:528:DC%2BD2sXkvV2ju7g%3D 17449591
49. E Sonestedt S Borgquist U Ericson, et al. 2008 Enterolactone is differently associated with estrogen receptor beta-negative and -positive breast cancer in a Swedish nested case-control study Cancer Epidemiol Biomarkers Prev 17 3241 3251 10.1158/1055-9965.EPI-08-0393 1:CAS:528:DC%2BD1cXhtlCkurzE 18990767
50. M Vanharanta J Mursu T Nurmi, et al. 2002 Phloem fortification in rye bread elevates serum enterolactone level Eur J Clin Nutr 56 952 957 10.1038/sj.ejcn.1601510 1:CAS:528:DC%2BD38Xns1Gntb0%3D 12373614 (Pubitemid 35244170)
51. A Kuijsten IC Arts PC Hollman P van't Veer E Kampman 2006 Plasma enterolignans are associated with lower colorectal adenoma risk Cancer Epidemiol Biomarkers Prev 15 1132 1136 10.1158/1055-9965.EPI-05-0991 1:CAS:528: DC%2BD28Xls1ehsb8%3D 16775171
52. C Carreau G Flouriot C netau-Pelissero M Potier 2008 Enterodiol and enterolactone, two major diet-derived polyphenol metabolites have different impact on ERalpha transcriptional activation in human breast cancer cells J Steroid Biochem Mol Biol 110 176 185 10.1016/j.jsbmb.2008.03.032 1:CAS:528:DC%2BD1cXmvFeqsrk%3D 18457947
53. ME Martin M Haourigui C Pelissero C Benassayag EA Nunez 1996 Interactions between phytoestrogens and human sex steroid binding protein Life Sci 58 429 436 10.1016/0024-3205(95)02308-9 1:STN:280:DyaK287ntlahtw%3D%3D 8594308 (Pubitemid 26188083)
54. M Schottner D Gansser G Spiteller 1997 Lignans from the roots of Urtica dioica and their metabolites bind to human sex hormone binding globulin (SHBG) Planta Med 63 529 532 10.1055/s-2006-957756 1:STN:280:DyaK1c%2Fps1SrtA%3D%3D 9434605 (Pubitemid 28035448)
55. H Hausner NF Johnsen J Hallund I Tetens 2004 A single measurement is inadequate to estimate enterolactone levels in danish postmenopausal women due to large intraindividual variation J Nutr 134 1197 1200 1:CAS:528: DC%2BD2cXjvFGqu7k%3D 15113970
56. KE Bach Knudsen A Serena AK Kjaer, et al. 2003 Rye bread in the diet of pigs enhances the formation of enterolactone and increases its levels in plasma, urine and feces J Nutr 133 1368 1375 12730424
57. Souhami RL, Tannock I, Hohenberger P, Horiot J-C (2002) Oxford textbook of oncology. Oxford: Oxford University Press
58. A Sonnenberg AD Muller 1993 Constipation and cathartics as risk factors of colorectal cancer: a meta-analysis Pharmacology 47 Suppl 1 224 233 10.1159/000139862 8234434
59. LM Kirkman JW Lampe DR Campbell MC Martini JL Slavin 1995 Urinary lignan and isoflavonoid excretion in men and women consuming vegetable and soy diets Nutr Cancer 24 1 12 10.1080/01635589509514388 1:CAS:528:DyaK2MXnt12hsL4%3D 7491293
60. KW Heaton J Radvan H Cripps RA Mountford FE Braddon AO Hughes 1992 Defecation frequency and timing, and stool form in the general population: a prospective study Gut 33 818 824 10.1136/gut.33.6.818 1:STN:280: DyaK38zisVKmtw%3D%3D 1624166
61. CS Probert PM Emmett KW Heaton 1995 Some determinants of whole-gut transit time: a population-based study QJM 88 311 315 1:STN:280: DyaK2Mzhs1CltQ%3D%3D 7796084
62. MC Roberts RC Millikan JA Galanko C Martin RS Sandler 2003 Constipation, laxative use, and colon cancer in a North Carolina population Am J Gastroenterol 98 857 864 10.1111/j.1572-0241.2003.07386.x 12738468 (Pubitemid 36576314)
63. B Iacopetta 2002 Are there two sides to colorectal cancer? Int J Cancer 101 403 408 10.1002/ijc.10635 1:CAS:528:DC%2BD38Xnt1ehsrw%3D 12216066 (Pubitemid 35050679)
64. C Benassayag M Perrot-Applanat F Ferre 2002 Phytoestrogens as modulators of steroid action in target cells J Chromatogr B Analyt Technol Biomed Life Sci 777 233 248 10.1016/S1570-0232(02)00340-9 1:CAS:528:DC%2BD38Xos1Wrtbc%3D 12270216 (Pubitemid 35264607)
65. J Matthews JA Gustafsson 2003 Estrogen signaling: a subtle balance between ER alpha and ER beta Mol Interv 3 281 292 10.1124/mi.3.5.281 1:CAS:528:DC%2BD3sXnt12guro%3D 14993442