The association between urinary phytoestrogen excretion and components of the metabolic syndrome in NHANES

European Journal of Nutrition

Volumn 53, Issue 6, 2014, Pages 1371-1381

  Struja, Tristan ^a   Richard, Aline ^a   Linseisen, Jakob ^b   Eichholzer, Monika ^a   Rohrmann, Sabine ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

Isoflavones; Lignans; Metabolic syndrome; NHANES; Phytoestrogens

Indexed keywords

ENTEROLACTONE; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; ISOFLAVONE; ISOFLAVONE DERIVATIVE; LIGNAN; PHYTOESTROGEN; TRIACYLGLYCEROL; GLUCOSE BLOOD LEVEL;

ADULT; ARTICLE; BLOOD PRESSURE; CARDIOVASCULAR RISK; CHOLESTEROL BLOOD LEVEL; CLINICAL EXAMINATION; CROSS-SECTIONAL STUDY; FEMALE; GEOMETRY; GLUCOSE BLOOD LEVEL; HUMAN; MAJOR CLINICAL STUDY; MALE; METABOLIC SYNDROME X; OUTCOME ASSESSMENT; TRIACYLGLYCEROL BLOOD LEVEL; URINARY EXCRETION; URINE LEVEL; WAIST CIRCUMFERENCE; BLOOD; BODY MASS; CARDIOVASCULAR DISEASES; COMPLICATION; DRUG EFFECTS; METABOLISM; MIDDLE AGED; NUTRITION; RISK FACTOR; URINE;

ADULT; BLOOD GLUCOSE; BLOOD PRESSURE; BODY MASS INDEX; CARDIOVASCULAR DISEASES; CHOLESTEROL, HDL; CROSS-SECTIONAL STUDIES; FEMALE; HUMANS; ISOFLAVONES; MALE; METABOLIC SYNDROME X; MIDDLE AGED; NUTRITION SURVEYS; PHYTOESTROGENS; RISK FACTORS; TRIGLYCERIDES; WAIST CIRCUMFERENCE;

EID: 84906936648     PISSN: 14366207     EISSN: 14366215     Source Type: Journal    
DOI: 10.1007/s00394-013-0639-y     Document Type: Article

References (69)

1. Danaei G, Finucane MM, Lu Y et al (2011) National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2.7 million participants. Lancet 378(9785):31-40. doi:10.1016/S0140-6736(11)60679-X
2. World Health Organization WHO Diabetes. http://www.who.int/mediacentre/ factsheets/fs312/en/index.html. Accessed 27 Nov 2012
3. Starcke S, Vollmer G (2006) Is there an estrogenic component in the metabolic syndrome? Genes Nutr 1(3-4):177-188. doi:10.1007/BF02829967
4. Saarinen NM, Bingham C, Lorenzetti S et al (2006) Tools to evaluate estrogenic potency of dietary phytoestrogens: a consensus paper from the EU Thematic Network "Phytohealth" (QLKI-2002-2453). Genes Nutr 1(3-4):143-158. doi:10.1007/BF02829964
5. French MR, Thompson LU, Hawker GA (2007) Validation of a phytoestrogen food frequency questionnaire with urinary concentrations of isoflavones and lignan metabolites in premenopausal women. J Am Coll Nutr 26(1):76-82 (Pubitemid 46411399)
6. Frankenfeld CL, Patterson RE, Kalhorn TF et al (2002) Validation of a soy food frequency questionnaire with plasma concentrations of isoflavones in US adults. J Am Diet Assoc 102(10):1407-1413 (Pubitemid 40450308)
7. Cornwell T (2004) Dietary phytoestrogens and health. Phytochemistry 65(8):995-1016. doi:10.1016/j.phytochem.2004.03.005
8. Bar-El DS, Reifen R (2010) Soy as an endocrine disruptor: cause for caution? J Pediatr Endocrinol Metab 23(9):855-861
9. Cederroth CR, Nef S (2009) Soy, phytoestrogens and metabolism: a review. Mol Cell Endocrinol 304(1-2):30-42. doi:10.1016/j.mce.2009.02.027
10. Chun OK, Chung SJ, Song WO (2009) Urinary isoflavones and their metabolites validate the dietary isoflavone intakes in US adults. J Am Diet Assoc 109(2):245-254. doi:10.1016/j.jada.2008.10.055
11. Frankenfeld CL (2011) Dairy consumption is a significant correlate of urinary equol concentration in a representative sample of US adults. Am J Clin Nutr 93(5):1109-1116. doi:10.3945/ajcn.111.011825
12. Buck K, Zaineddin AK, Vrieling A et al (2010) Meta-analyses of lignans and enterolignans in relation to breast cancer risk. Am J Clin Nutr 92(1):141-153. doi:10.3945/ajcn.2009.28573
13. Hwang YW, Kim SY, Jee SH et al (2009) Soy food consumption and risk of prostate cancer: a meta-analysis of observational studies. Nutr Cancer 61(5):598-606. doi:10.1080/01635580902825639
14. Guthrie JR, Ball M, Murkies A et al (2000) Dietary phytoestrogen intake in mid-life Australian-born women: relationship to health variables. Climacteric 3(4):254-261 (Pubitemid 32165443)
15. Jayagopal V, Albertazzi P, Kilpatrick ES et al (2002) Beneficial effects of soy phytoestrogen intake in postmenopausal women with type 2 diabetes. Diabetes Care 25(10):1709-1714 (Pubitemid 41071075)
16. Greany KA, Nettleton JA, Wangen KE et al (2004) Probiotic consumption does not enhance the cholesterol-lowering effect of soy in postmenopausal women. J Nutr 134(12):3277-3283 (Pubitemid 39602998)
17. Cheng S, Shaw N, Tsai K et al (2004) The hypoglycemic effects of soy isoflavones on postmenopausal women. J Womens Health (Larchmt) 13(10):1080-1086. doi:10.1089/jwh.2004.13.1080
18. Anderson JW, Hoie LH (2005) Weight loss and lipid changes with low-energy diets: comparator study of milk-based versus soy-based liquid meal replacement interventions. J Am Coll Nutr 24(3):210-216 (Pubitemid 41201964)
19. Li Z, Hong K, Saltsman P et al (2005) Long-term efficacy of soy-based meal replacements vs an individualized diet plan in obese type II DM patients: relative effects on weight loss, metabolic parameters, and C-reactive protein. Eur J Clin Nutr 59(3): 411-418. doi:10.1038/sj.ejcn.1602089 (Pubitemid 40403296)
20. Anderson JW, Fuller J, Patterson K et al (2007) Soy compared to casein meal replacement shakes with energy-restricted diets for obese women: randomized controlled trial. Metabolism 56(2): 280-288. doi:10.1016/j.metabol.2006.10.013 (Pubitemid 46074076)
21. FDA (1999) CFR - Code of Federal Regulations title 21. http://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfcfr/CFRSearch.cfm?fr=101.82. Accessed 01 Oct 2012
22. Canada Go, Canada H, Health Products and Food Branch, Natural Health Products Directorate (2009) Technical report to summarize the scientific rationale for the natural health products directorate's new guidance on the regulation of soy isoflavone products - health Canada. http://www.hc-sc.gc.ca/ dhp-mps/prodnatur/legislation/docs/rapport-tech-report-soya-eng.php#b. Accessed 01 Oct 2012
23. Bhupathy P, Haines CD, Leinwand LA (2010) Influence of sex hormones and phytoestrogens on heart disease in men and women. Womens Health (Lond Engl) 6(1):77-95. doi:10.2217/whe.09.80
24. Peñalvo JL, López-Romero P (2012) Urinary enterolignan concentrations are positively associated with serum HDL cholesterol and negatively associated with serum triglycerides in U.S. adults. J Nutr 142(4):751-756. doi:10.3945/jn.111.150516
25. NHANES CNCfHS (2012, March 30) NHANES-continuous NHANES web tutorial - survey design factors. http://www.cdc.gov/nchs/tutorials/NHANES/SurveyDesign/ intro.htm. Accessed 01 Oct 2012
26. NHANES CNCfHS (2012, Aug 30) NHANES - NHANES participants homepage. http://www.cdc.gov/nchs/nhanes/participant.htm. Accessed 01 Oct 2012
27. NHANES CNCfHS (2012, Jan) NHANES 1999-2000: PHPYPA urinary phthalates data documentation, codebook, and frequencies. http://www.cdc.gov/nchs/nhanes/ nhanes1999-2000/PHPYPA.htm. Accessed 01 Oct 2012
28. NHANES CNCfHS (2012, Jan) NHANES 2001-2002: urinary phthalates, phytoestrogens and PAHs data documentation, codebook, and frequencies. http://www.cdc.gov/nchs/nhanes/nhanes2001-2002/PHPYPA-B.htm. Accessed 01 Oct 2012
29. NHANES CNCfHS (2009, Aug) NHANES 2003-2004: urinary phytoestrogens data documentation, codebook, and frequencies. http://www.cdc.gov/nchs/nhanes/ nhanes2003-2004/L06PHY-C.htm. Accessed 01 Oct 2012
30. NHANES CNCfHS (2010, May 14) NHANES - NHANES 1999-2000 - lab methods. http://www.cdc.gov/nchs/nhanes/nhanes1999-2000/lab-methods-99-00.htm. Accessed 01 Oct 2012
31. Barnes S, Coward L, Kirk M et al (1998) HPLC - mass spectrometry analysis of isoflavones. Proc Soc Exp Biol Med 217(3):254-262
32. NHANES CNCfHS (2010, May 14) NHANES - NHANES 2003-2004 - lab methods. http://www.cdc.gov/nchs/nhanes/nhanes2003-2004/lab-methods-03-04.htm. Accessed 01 Oct 2012
33. Westgard JO (2003) Internal quality control: planning and implementation strategies. Ann Clin Biochem 40(6):593-611. doi:10.1258/000456303770367199
34. NHANES CNCfHS (2008, May) NHANES 2003-2004 triglycerides and LDL-cholesterol. http://www.cdc.gov/nchs/nhanes/nhanes2003-2004/L13AM-C.htm
35. Friedewald WT, Levy RI, Fredrickson DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18(6):499-502
36. Grundy SM (2005) Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart,Lung, and Blood Institute scientific statement. Circulation 112(17):2735-2752. doi:10.1161/CIRCULATIONAHA.105.169404
37. de Kleijn MJJ, van der Schouw YT, Wilson PWF et al (2002) Dietary intake of phytoestrogens is associated with a favorable metabolic cardiovascular risk profile in postmenopausal U.S. women: the Framingham study. J Nutr 132(2):276-282 (Pubitemid 34135607)
38. Cornish SM, Chilibeck PD, Paus-Jennsen L et al (2009) A randomized controlled trial of the effects of flaxseed lignan complex on metabolic syndrome composite score and bone mineral in older adults. Appl Physiol Nutr Metab 34(2):89-98. doi:10.1139/H08-142
39. Yang G, Shu XO, Jin F et al (2004) Soyfood consumption and risk of glycosuria: a cross-sectional study within the Shanghai Women's Health Study. Eur J Clin Nutr 58(4):615-620. doi:10.1038/sj.ejcn.1601855 (Pubitemid 38500131)
40. Goodman-Gruen D, Kritz-Silverstein D (2001) Usual dietary isoflavone intake is associated with cardiovascular disease risk factors in postmenopausal women. J Nutr 131(4):1202-1206 (Pubitemid 32275100)
41. Kuijsten A, Arts ICW, Vree TB et al (2005) Pharmacokinetics of enterolignans in healthy men and women consuming a single dose of secoisolariciresinol diglucoside. J Nutr 135(4):795-801 (Pubitemid 40464107)
42. Setchell KDR, Faughnan MS, Avades T et al (2003) Comparing the pharmacokinetics of daidzein and genistein with the use of 13C-labeled tracers in premenopausal women. Am J Clin Nutr 77(2):411-419 (Pubitemid 36133385)
43. Bloedon LT, Jeffcoat AR, Lopaczynski W et al (2002) Safety and pharmacokinetics of purified soy isoflavones: single-dose administration to postmenopausal women. Am J Clin Nutr 76(5):1126-1137 (Pubitemid 35244688)
44. Nielsen ILF, Williamson G (2007) Review of the factors affecting bioavailability of soy isoflavones in humans. Nutr Cancer 57(1):1-10. doi:10.1080/01635580701267677 (Pubitemid 46871564)
45. Valentín-Blasini L, Blount BC, Caudill SP et al (2003) Urinary and serum concentrations of seven phytoestrogens in a human reference population subset. J Expo Anal Environ Epidemiol 13(4):276-282. doi:10.1038/sj.jea.7500278 (Pubitemid 36999366)
46. Dixon RA (2004) Phytoestrogens. Annu Rev Plant Biol 55(1):225-261. doi:10.1146/annurev.arplant.55.031903.141729
47. Merritt JC (2004) Metabolic syndrome: soybean foods and serum lipids. J Natl Med Assoc 96(8):1032-1041
48. Pan A, Yu D, Demark-Wahnefried W et al (2009) Meta-analysis of the effects of flaxseed interventions on blood lipids. Am J Clin Nutr 90(2):288-297. doi:10.3945/ajcn.2009.27469
49. Drewnowski A (2012) The economics of food choice behavior: why poverty and obesity are linked. Nestle Nutr Inst Workshop Ser 73:95-112. doi:10.1159/000341303
50. Heo M, Kim RS, Wylie-Rosett J et al (2011) Inverse association between fruit and vegetable intake and BMI even after controlling for demographic, socioeconomic and lifestyle factors. Obes Facts 4(6):449-455. doi:10.1159/000335279
51. Lutfiyya MN, Chang LF, Lipsky MS (2012) A cross-sectional study of US rural adults' consumption of fruits and vegetables: do they consume at least five servings daily? BMC Public Health 12:280. doi:10.1186/1471-2458-12-280
52. NHANES CNCfHS (2011-2014) NHANES 2011-2012. Asian oversampling. http://www.cdc.gov/nchs/nhanes/nhanes2011-2012/nhanes11-12.htm. Accessed 26 Nov 2012
53. Vergne S, Sauvant P, Lamothe V et al (2009) Influence of ethnic origin (Asian v. Caucasian) and background diet on the bioavailability of dietary isoflavones. Br J Nutr 102(11):1642. doi:10.1017/S0007114509990833
54. Kunisue T, Tanabe S, Isobe T et al (2010) Profiles of phytoestrogens in human urine from several Asian countries. J Agric Food Chem 58(17):9838-9846. doi:10.1021/jf102253j
55. Meeuwisse-Pasterkamp SH, van der Klauw MM, Wolffenbuttel BHR (2008) Type 2 diabetes mellitus: prevention of macrovascular complications. Expert Rev Cardiovasc Ther 6(3):323-341. doi:10.1586/14779072.6.3.323
56. Grundy SM (2004) Definition of metabolic syndrome: report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition. Circulation 109(3):433-438. doi:10.1161/01.CIR.0000111245.75752.C6
57. Cederroth CR, Vinciguerra M, Gjinovci A et al (2008) Dietary phytoestrogens activate AMP-activated protein kinase with improvement in lipid and glucose metabolism. Diabetes 57(5):1176-1185. doi:10.2337/db07-0630
58. Aoyama T, Fukui K, Nakamori T et al (2000) Effect of soy and milk whey protein isolates and their hydrolysates on weight reduction in genetically obese mice. Biosci Biotechnol Biochem 64(12):2594-2600
59. Choi MS, Jung UJ, Yeo J et al (2008) Genistein and daidzein prevent diabetes onset by elevating insulin level and altering hepatic gluconeogenic and lipogenic enzyme activities in nonobese diabetic (NOD) mice. Diabetes Metab Res Rev 24(1):74-81. doi:10.1002/dmrr.780 (Pubitemid 351176003)
60. Lee CC, Bloem CJ, Kasa-Vubu JZ et al (2012) Effect of oral phytoestrogen on androgenicity and insulin sensitivity in postmenopausal women. Diabetes Obes Metab 14(4):315-319. doi:10.1111/j.1463-1326.2011.01532.x
61. Marinangeli CPF, Jones PJH (2011) Whole and fractionated yellow pea flours reduce fasting insulin and insulin resistance in hypercholesterolaemic and overweight human subjects. Br J Nutr 105(1):110-117. doi:10.1017/ S0007114510003156
62. Hall WL, Vafeiadou K, Hallund J et al (2006) Soy-isoflavone-enriched foods and markers of lipid and glucose metabolism in postmenopausal women: interactions with genotype and equol production. Am J Clin Nutr 83(3):592-600 (Pubitemid 44699204)
63. Morisset A, Lemieux S, Veilleux A et al (2009) Impact of a lignan-rich diet on adiposity and insulin sensitivity in postmenopausal women. Br J Nutr 102(2):195-200. doi:10.1017/S0007114508162092
64. Rosero Arenas MA, Rosero Arenas E, Portaceli Armiñana MA et al (2008) Utilidad de los fitoestrógenos en la reducción de la presión arterial. Revisión sistemática y metaanálisis (Usefulness of phyto-oestrogens in reduction of blood pressure. Systematic review and meta-analysis). Aten Primaria 40(4):177-186 (Pubitemid 351534810)
65. Taddei S (2009) Blood pressure through aging and menopause. Climacteric 12(Suppl 1):36-40
66. Weggemans RM, Trautwein EA (2003) Relation between soy-associated isoflavones and LDL and HDL cholesterol concentrations in humans: a meta-analysis. Eur J Clin Nutr 57(8): 940-946. doi:10.1038/sj.ejcn.1601628 (Pubitemid 36987241)
67. McPherson R, Frohlich J, Fodor G et al (2006) Canadian Cardiovascular Society position statement-recommendations for the diagnosis and treatment of dyslipidemia and prevention of cardiovascular disease. Can J Cardiol 22(11):913-927 (Pubitemid 44596492)
68. Erberich LCN, Alcantara VM, Picheth G et al (2002) Hormone replacement therapy in postmenopausal women and its effects on plasma lipid levels. Clin Chem Lab Med 40(5):446-451. doi:10.1515/CCLM.2002.076 (Pubitemid 34700167)
69. Eisenberg DM, Kessler RC, Foster C et al (1993) Unconventional medicine in the United States. Prevalence, costs, and patterns of use. N Engl J Med 328(4):246-252. doi:10.1056/NEJM199301283280406 (Pubitemid 23035311)