Skip to main content
Erschienen in: European Journal of Nutrition 3/2016

06.05.2015 | Original Contribution

Urinary phytoestrogens and cancer, cardiovascular, and all-cause mortality in the continuous National Health and Nutrition Examination Survey

verfasst von: Michael K. Reger, Terrell W. Zollinger, Ziyue Liu, Josette Jones, Jianjun Zhang

Erschienen in: European Journal of Nutrition | Ausgabe 3/2016

Einloggen, um Zugang zu erhalten

Abstract

Purpose

Experimental studies suggest that phytoestrogen intake alters cancer and cardiovascular risk. This study investigated the associations of urinary phytoestrogens with total cancer (n = 79), cardiovascular (n = 108), and all-cause (n = 290) mortality among 5179 participants in the continuous National Health and Nutrition Examination Survey (1999–2004).

Methods

Urinary phytoestrogens were measured using high-performance liquid chromatography with tandem mass spectrometric detection. Survival analysis was performed to evaluate hazard ratios (HRs) and 95 % confidence intervals (CIs) for each of the three outcomes in relation to urinary phytoestrogens.

Results

After adjustment for confounders, higher urinary concentrations of total enterolignans were associated with a reduced risk of death from cardiovascular disease (HR for tertile 3 vs. tertile 1 0.48; 95 % CI 0.24, 0.97), whereas higher urinary concentrations of total isoflavones (HR for tertile 3 vs. tertile 1 2.14; 95 % CI 1.03, 4.47) and daidzein (HR for tertile 3 vs. tertile 1 2.05; 95 % CI 1.02, 4.11) were associated with an increased risk. A reduction in all-cause mortality was observed for elevated urinary concentrations of total enterolignans (HR for tertile 3 vs. tertile 1 0.65; 95 % CI 0.43, 0.96) and enterolactone (HR for tertile 3 vs. tertile 1 0.65; 95 % CI 0.44, 0.97).

Conclusions

Some urinary phytoestrogens were associated with cardiovascular and all-cause mortality in a representative sample of the US population. This is one of the first studies that used urinary phytoestrogens as biomarkers of their dietary intake to evaluate the effect of these bioactive compounds on the risk of death from cancer and cardiovascular disease.
Literatur
1.
Zurück zum Zitat Murphy SL, Xu J, Kochanek KD (2013) Deaths: final data for 2010. Centers for Disease Control and Prevention, Atlanta Murphy SL, Xu J, Kochanek KD (2013) Deaths: final data for 2010. Centers for Disease Control and Prevention, Atlanta
2.
Zurück zum Zitat World Health Organization (2013) The top 10 causes of death: Fact Sheet Number 310 World Health Organization (2013) The top 10 causes of death: Fact Sheet Number 310
3.
Zurück zum Zitat Latest world cancer statistics—Press release number 223 (2013) World Health Organization, Lyon Latest world cancer statistics—Press release number 223 (2013) World Health Organization, Lyon
4.
Zurück zum Zitat Kuhnle GG, Dell’Aquila C, Low YL, Kussmaul M, Bingham SA (2007) Extraction and quantification of phytoestrogens in foods using automated solid-phase extraction and LC/MS/MS. Anal Chem 79(23):9234–9239CrossRef Kuhnle GG, Dell’Aquila C, Low YL, Kussmaul M, Bingham SA (2007) Extraction and quantification of phytoestrogens in foods using automated solid-phase extraction and LC/MS/MS. Anal Chem 79(23):9234–9239CrossRef
5.
Zurück zum Zitat Horn-Ross PL, Barnes S, Lee M, Coward L, Mandel E, Koo K, John EM, Smith M (2000) Assessing phytoestrogen exposure in epidemiologic studies: development of a database (United States). Cancer Causes Control 11:299–302CrossRef Horn-Ross PL, Barnes S, Lee M, Coward L, Mandel E, Koo K, John EM, Smith M (2000) Assessing phytoestrogen exposure in epidemiologic studies: development of a database (United States). Cancer Causes Control 11:299–302CrossRef
6.
Zurück zum Zitat Adlercreutz H (2007) Lignans and human health. Crit Rev Clin Lab Sci 44:483–525CrossRef Adlercreutz H (2007) Lignans and human health. Crit Rev Clin Lab Sci 44:483–525CrossRef
7.
Zurück zum Zitat Thomas BF, Zeisel SH, Busby MG, Hill JM, Mitchell RA, Scheffler NM, Brown SS, Bloeden LT, Dix KJ, Jeffcoat AR (2001) Quantitative analysis of the principle soy isoflavones genistein, daidzein and glycitein, and their primary conjugated metabolites in human plasma and urine using reversed-phase high-performance liquid chromatography with ultraviolet detection. J Chromatogr B Biomed Sci Appl 760(2):191–205CrossRef Thomas BF, Zeisel SH, Busby MG, Hill JM, Mitchell RA, Scheffler NM, Brown SS, Bloeden LT, Dix KJ, Jeffcoat AR (2001) Quantitative analysis of the principle soy isoflavones genistein, daidzein and glycitein, and their primary conjugated metabolites in human plasma and urine using reversed-phase high-performance liquid chromatography with ultraviolet detection. J Chromatogr B Biomed Sci Appl 760(2):191–205CrossRef
8.
Zurück zum Zitat Griffiths K, Denis L, Turkes A, Morton MS (1998) Possible relationship between dietary factors and pathogenesis of prostate cancer. Int J Urol 5:195–213CrossRef Griffiths K, Denis L, Turkes A, Morton MS (1998) Possible relationship between dietary factors and pathogenesis of prostate cancer. Int J Urol 5:195–213CrossRef
9.
Zurück zum Zitat Rowland IR, Wiseman H, Sanders TA, 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 36:27–32CrossRef Rowland IR, Wiseman H, Sanders TA, 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 36:27–32CrossRef
10.
Zurück zum Zitat Akaza H, Miyanaga N, Takashima N, Naito S, Hirao Y, Tsukamoto T, Mori M (2002) Is daidzein non-metabolizer a high risk for prostate cancer? A case–controlled study of serum soybean isoflavone concentration. Jpn J Clin Oncol 32(8):296–300CrossRef Akaza H, Miyanaga N, Takashima N, Naito S, Hirao Y, Tsukamoto T, Mori M (2002) Is daidzein non-metabolizer a high risk for prostate cancer? A case–controlled study of serum soybean isoflavone concentration. Jpn J Clin Oncol 32(8):296–300CrossRef
11.
Zurück zum Zitat Lampe JW (2003) Isoflavonoid and lignan phytoestrogens as dietary biomarkers. J Nutr 133(Suppl):956S–964S Lampe JW (2003) Isoflavonoid and lignan phytoestrogens as dietary biomarkers. J Nutr 133(Suppl):956S–964S
12.
Zurück zum Zitat Ohno S, Nakajima Y, Inoue K, Nakazawa H, Nakajin S (2003) Genistein administration decreases serum corticosterone and testosterone levels in rats. Life Sci 74:733–742CrossRef Ohno S, Nakajima Y, Inoue K, Nakazawa H, Nakajin S (2003) Genistein administration decreases serum corticosterone and testosterone levels in rats. Life Sci 74:733–742CrossRef
13.
Zurück zum Zitat Matori H, Umar S, Nadadur RD, Sharma S, Partow-Navid R, Afkhami M, Amjedi M, Eghbali M (2012) Genistein, a soy phytoestrogen, reverses severe pulmonary hypertension and prevents right heart failure in rats. Hypertension 60(2):425–430CrossRef Matori H, Umar S, Nadadur RD, Sharma S, Partow-Navid R, Afkhami M, Amjedi M, Eghbali M (2012) Genistein, a soy phytoestrogen, reverses severe pulmonary hypertension and prevents right heart failure in rats. Hypertension 60(2):425–430CrossRef
14.
Zurück zum Zitat Shi L, Ryan HH, Jones E, Simas TA, Lichenstein AH, Sun Q, Hayman LL (2014) Urinary isoflavone concentrations are inversely associated with cardiometabolic risk markers in pregnant U.S. women. J Nutr 144(3):344–351CrossRef Shi L, Ryan HH, Jones E, Simas TA, Lichenstein AH, Sun Q, Hayman LL (2014) Urinary isoflavone concentrations are inversely associated with cardiometabolic risk markers in pregnant U.S. women. J Nutr 144(3):344–351CrossRef
15.
Zurück zum Zitat Nicastro HL, Mondul AM, Rohrmann S, Platz EA (2013) Associations between urinary soy isoflavonoids and two inflammatory markers in the United States in 2005-2008. Cancer Causes Control 24(6):1185–1196CrossRef Nicastro HL, Mondul AM, Rohrmann S, Platz EA (2013) Associations between urinary soy isoflavonoids and two inflammatory markers in the United States in 2005-2008. Cancer Causes Control 24(6):1185–1196CrossRef
16.
Zurück zum Zitat Branham WA, Dial SL, Moland CL, Hass BS, Blair RM, Fang H, Shi L, Tong W, Perkins RG, Sheehan DM (2002) Phytoestrogens and mycoestrogens bind to the rat uterine estrogen receptor. J Nutr 132(4):658–664 Branham WA, Dial SL, Moland CL, Hass BS, Blair RM, Fang H, Shi L, Tong W, Perkins RG, Sheehan DM (2002) Phytoestrogens and mycoestrogens bind to the rat uterine estrogen receptor. J Nutr 132(4):658–664
17.
Zurück zum Zitat Holzbeierlein JM, McIntosh J, Thrasher JB (2005) The role of soy phytoestrogens in prostate cancer. Curr Opin Urol 15:17–22CrossRef Holzbeierlein JM, McIntosh J, Thrasher JB (2005) The role of soy phytoestrogens in prostate cancer. Curr Opin Urol 15:17–22CrossRef
18.
Zurück zum Zitat Magee PJ, Rowland IR (2004) Phytoestrogens, their mechanism of action: current evidence for a role in breast and prostate cancer. Br J Nutr 91:513–531CrossRef Magee PJ, Rowland IR (2004) Phytoestrogens, their mechanism of action: current evidence for a role in breast and prostate cancer. Br J Nutr 91:513–531CrossRef
19.
Zurück zum Zitat Kuipper 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(10):4252–4263 Kuipper 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(10):4252–4263
20.
Zurück zum Zitat Onozawa M, Fukuda K, Ohtani M, Akaza H, Sugimura T, Wakabayashi K (1998) Effects of soybean isoflavones on cell growth and apoptosis of the human prostatic cancer cell link LNCaP. Jpn J Clin Oncol 28:360–363CrossRef Onozawa M, Fukuda K, Ohtani M, Akaza H, Sugimura T, Wakabayashi K (1998) Effects of soybean isoflavones on cell growth and apoptosis of the human prostatic cancer cell link LNCaP. Jpn J Clin Oncol 28:360–363CrossRef
21.
Zurück zum Zitat Turner JV, Agatonovic-Kustrin S, Glass BD (2007) Molecular aspects of phytoestrogen selective binding at estrogen receptors. J Pharm Sci 96(8):1879–1885CrossRef Turner JV, Agatonovic-Kustrin S, Glass BD (2007) Molecular aspects of phytoestrogen selective binding at estrogen receptors. J Pharm Sci 96(8):1879–1885CrossRef
22.
Zurück zum Zitat Weber KS, Setchell KD, Stocco DM, Lephart ED (2001) Dietary soy-phytoestrogens decrease testosterone levels and prostate weight without altering LH, prostate 5-alpha-reductase or testicular steroidogenic acute regulatory peptide levels in adult male Sprague-Dawley rats. J Endocrinol 170(3):591–599CrossRef Weber KS, Setchell KD, Stocco DM, Lephart ED (2001) Dietary soy-phytoestrogens decrease testosterone levels and prostate weight without altering LH, prostate 5-alpha-reductase or testicular steroidogenic acute regulatory peptide levels in adult male Sprague-Dawley rats. J Endocrinol 170(3):591–599CrossRef
23.
Zurück zum Zitat 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 98:388–396CrossRef 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 98:388–396CrossRef
24.
Zurück zum Zitat Hedelin M, Klint A, Chang ET, Bellocco R, Johansson JE, Andersson SO, Heinonen SM, Adlercreutz H, Adami HO, Gronberg H, Balter KA (2006) Dietary phytoestrogen, serum enterolactone and risk of prostate cancer: the cancer prostate Sweden study. Cancer Causes Control 17:169–180CrossRef Hedelin M, Klint A, Chang ET, Bellocco R, Johansson JE, Andersson SO, Heinonen SM, Adlercreutz H, Adami HO, Gronberg H, Balter KA (2006) Dietary phytoestrogen, serum enterolactone and risk of prostate cancer: the cancer prostate Sweden study. Cancer Causes Control 17:169–180CrossRef
25.
Zurück zum Zitat Ziegler RG (2004) Phytoestrogens and breast cancer. Am J Clin Nutr 79(2):183–184 Ziegler RG (2004) Phytoestrogens and breast cancer. Am J Clin Nutr 79(2):183–184
26.
Zurück zum Zitat Horn-Ross PL, John EM, Lee M, Stewart SL, Koo J, Sakoda LC, Shiau AC, Goldstein J, Davis P, Perez-Stable EJ (2001) Phytoestrogen consumption and breast cancer risk in a multiethnic population. Am J Epidemiol 154(5):434–441CrossRef Horn-Ross PL, John EM, Lee M, Stewart SL, Koo J, Sakoda LC, Shiau AC, Goldstein J, Davis P, Perez-Stable EJ (2001) Phytoestrogen consumption and breast cancer risk in a multiethnic population. Am J Epidemiol 154(5):434–441CrossRef
27.
Zurück zum Zitat van der Schouw YT, Kreijkamp-Kaspers S, Peeters PHM, Keinan-Boker L, Rimm EB, Grobbee DE (2005) Cardiovascular disease in women: prospective study on usual dietary phytoestrogen intake and cardiovascular disease risk in western women. Circulation 111(4):465–471CrossRef van der Schouw YT, Kreijkamp-Kaspers S, Peeters PHM, Keinan-Boker L, Rimm EB, Grobbee DE (2005) Cardiovascular disease in women: prospective study on usual dietary phytoestrogen intake and cardiovascular disease risk in western women. Circulation 111(4):465–471CrossRef
28.
Zurück zum Zitat Lissin LW, Cooke JP (2000) Phytoestrogens and cardiovascular health. J Am Coll Cardiol 35(6):1403–1410CrossRef Lissin LW, Cooke JP (2000) Phytoestrogens and cardiovascular health. J Am Coll Cardiol 35(6):1403–1410CrossRef
29.
Zurück zum Zitat Adlercreutz H (2002) Phyto-oestrogens and cancer. Lancet Oncol 3:364–373CrossRef Adlercreutz H (2002) Phyto-oestrogens and cancer. Lancet Oncol 3:364–373CrossRef
30.
Zurück zum Zitat Anderson LN, Cotterchio M, Boucher BA, Kreiger N (2013) 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 132:1683–1692CrossRef Anderson LN, Cotterchio M, Boucher BA, Kreiger N (2013) 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 132:1683–1692CrossRef
31.
Zurück zum Zitat van der Schouw YT, Kreijkamp-Kaspers S, Peeters PH, Keinan-Boker L, Rimm EB, Grobbee DE (2005) Prospective study on usual dietary phytoestrogen intake and cardiovascular disease risk in western women. Circulation 111:465–471CrossRef van der Schouw YT, Kreijkamp-Kaspers S, Peeters PH, Keinan-Boker L, Rimm EB, Grobbee DE (2005) Prospective study on usual dietary phytoestrogen intake and cardiovascular disease risk in western women. Circulation 111:465–471CrossRef
32.
Zurück zum Zitat Seow A, Shi CY, Franke AA, Hankin JH, Lee HP, Yu MC (1998) Isoflavonoid levels in spot urine are associated with frequency of dietary soy intake in a population-based sample of middle aged and older Chinese in Singapore. Cancer Epidemiol Biomarkers Prev 7:135–140 Seow A, Shi CY, Franke AA, Hankin JH, Lee HP, Yu MC (1998) Isoflavonoid levels in spot urine are associated with frequency of dietary soy intake in a population-based sample of middle aged and older Chinese in Singapore. Cancer Epidemiol Biomarkers Prev 7:135–140
33.
Zurück zum Zitat 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):76–82CrossRef 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):76–82CrossRef
34.
Zurück zum Zitat Maskarinec G, Singh S, Meng L, Franke AA (1998) Dietary soy intake and urinary isoflavone excretion among women from a multiethnic population. Cancer Epidemiol Biomarkers Prev 7(7):613–619 Maskarinec G, Singh S, Meng L, Franke AA (1998) Dietary soy intake and urinary isoflavone excretion among women from a multiethnic population. Cancer Epidemiol Biomarkers Prev 7(7):613–619
35.
Zurück zum Zitat Jaceldo-Siegl K, Fraser GE, Chan J, Franke A, Sabate J (2008) Validation of soy protein estimates from a food-frequency questionnaire with repeated 24-h recalls and isoflavonoid excretion in overnight urine in a western population with a wide range of soy intakes. Am J Clin Nutr 87(5):1422–1427 Jaceldo-Siegl K, Fraser GE, Chan J, Franke A, Sabate J (2008) Validation of soy protein estimates from a food-frequency questionnaire with repeated 24-h recalls and isoflavonoid excretion in overnight urine in a western population with a wide range of soy intakes. Am J Clin Nutr 87(5):1422–1427
36.
Zurück zum Zitat Lampe JW, Gustafson DR, Hutchins AM, Martini MC, Li S, Wahala K, Grandits GA, Potter JD, Slavin JL (1999) Urinary isoflavonoid and lignan excretion on a western diet: relation to soy, vegetable, and fruit intake. Cancer Epidemiol Biomarkers Prev 8:699–707 Lampe JW, Gustafson DR, Hutchins AM, Martini MC, Li S, Wahala K, Grandits GA, Potter JD, Slavin JL (1999) Urinary isoflavonoid and lignan excretion on a western diet: relation to soy, vegetable, and fruit intake. Cancer Epidemiol Biomarkers Prev 8:699–707
37.
Zurück zum Zitat NHANES (1999–2004) Public-use Linked Mortality Files (2006) (2013) National Health and Nutrition Examination Survey NHANES (1999–2004) Public-use Linked Mortality Files (2006) (2013) National Health and Nutrition Examination Survey
38.
Zurück zum Zitat NHANES 1999–2000 Public Data Release File Documentation (2000). US Department of Health and Human Services, Centers for Disease Control and Prevention, Hyattsville NHANES 1999–2000 Public Data Release File Documentation (2000). US Department of Health and Human Services, Centers for Disease Control and Prevention, Hyattsville
39.
Zurück zum Zitat Analytic and Reporting Guidelines: The National Health and Nutrition Examination Survey (NHANES) (2006) Centers for Disease Control and Prevention, Hyattsville Analytic and Reporting Guidelines: The National Health and Nutrition Examination Survey (NHANES) (2006) Centers for Disease Control and Prevention, Hyattsville
40.
Zurück zum Zitat Rybak ME, Parker DL, Pfeiffer CM (2008) Determination of urinary phytoestrogens by HPLC-MS/MS: a comparison of atmospheric pressure chemical ionization (APCI) and electrospray ionization (ESI). J Chromatogr B Analyt Technol Biomed Life Sci 861(1):145–150CrossRef Rybak ME, Parker DL, Pfeiffer CM (2008) Determination of urinary phytoestrogens by HPLC-MS/MS: a comparison of atmospheric pressure chemical ionization (APCI) and electrospray ionization (ESI). J Chromatogr B Analyt Technol Biomed Life Sci 861(1):145–150CrossRef
41.
Zurück zum Zitat Parker DL (2004) Division of laboratory sciences laboratory protocol: phytoestrogens. National Center for Health Statistics, Hyatsville Parker DL (2004) Division of laboratory sciences laboratory protocol: phytoestrogens. National Center for Health Statistics, Hyatsville
42.
Zurück zum Zitat National Health and Nutrition Examination Survey (1999-2004) Linked Mortality Files (2009) Office of Analysis and Epidemiology, Hyatsville National Health and Nutrition Examination Survey (1999-2004) Linked Mortality Files (2009) Office of Analysis and Epidemiology, Hyatsville
43.
Zurück zum Zitat Yu O, Eberg M, Benayoun S, Aprikian A, Barist G, Suissa S, Azoulay L (2014) Use of statins and the risk of death in patients with prostate cancer. J Clin Oncol 32(1):5–11CrossRef Yu O, Eberg M, Benayoun S, Aprikian A, Barist G, Suissa S, Azoulay L (2014) Use of statins and the risk of death in patients with prostate cancer. J Clin Oncol 32(1):5–11CrossRef
44.
Zurück zum Zitat Van Hemelrijck M, Holmberg L, Garmo M, Hammar N, Walldium G, Binda E, Lambe M, Jungner I (2011) Association between levels of c-reactive protein and leukocytes and cancer: three repeated measurements in the Swedish AMORIS study. Cancer Epidemiol Biomarkers Prev 20(3):428–438CrossRef Van Hemelrijck M, Holmberg L, Garmo M, Hammar N, Walldium G, Binda E, Lambe M, Jungner I (2011) Association between levels of c-reactive protein and leukocytes and cancer: three repeated measurements in the Swedish AMORIS study. Cancer Epidemiol Biomarkers Prev 20(3):428–438CrossRef
45.
Zurück zum Zitat Ozasa K, Nakao M, Watanabe Y, Hayashi K, Miki T, Mikami K, Mori M, Sakauchi F, Washio M, Ito Y, Suzuki K, Wakai K, Tamakoshi A (2004) Serum phytoestrogens and prostate cancer risk in a nested case–control study among Japanese men. Cancer Sci 95(1):65–71CrossRef Ozasa K, Nakao M, Watanabe Y, Hayashi K, Miki T, Mikami K, Mori M, Sakauchi F, Washio M, Ito Y, Suzuki K, Wakai K, Tamakoshi A (2004) Serum phytoestrogens and prostate cancer risk in a nested case–control study among Japanese men. Cancer Sci 95(1):65–71CrossRef
46.
Zurück zum Zitat Kurahashi N, Iwasaki M, Inoue M, Sasazuki S, Tsugane S (2008) Plasma isoflavones and subsequent risk of prostate cancer in a nested case–control study: the Japan Public Health Center. J Clin Oncol 26:5923–5929CrossRef Kurahashi N, Iwasaki M, Inoue M, Sasazuki S, Tsugane S (2008) Plasma isoflavones and subsequent risk of prostate cancer in a nested case–control study: the Japan Public Health Center. J Clin Oncol 26:5923–5929CrossRef
47.
Zurück zum Zitat Verhaus M, van Gils CH, Keinan-Boker L, Grace PB, Bingham SA, Peeters PHM (2007) Plasma phytoestrogens and subsequent breast cancer risk. J Clin Oncol 25(6):648–655CrossRef Verhaus M, van Gils CH, Keinan-Boker L, Grace PB, Bingham SA, Peeters PHM (2007) Plasma phytoestrogens and subsequent breast cancer risk. J Clin Oncol 25(6):648–655CrossRef
48.
Zurück zum Zitat Bylund A, Zhang J-X, Bergh A, Damber JE, Widmark A, Johnsson A, Adlercreutz H, Aman P, Shepherd MJ, Hallmans G (2000) Rye bran and soy protein delay growth and increase apoptosis of human LNCaP prostate adenocarcinoma in nude mice. Prostate 42:304–314CrossRef Bylund A, Zhang J-X, Bergh A, Damber JE, Widmark A, Johnsson A, Adlercreutz H, Aman P, Shepherd MJ, Hallmans G (2000) Rye bran and soy protein delay growth and increase apoptosis of human LNCaP prostate adenocarcinoma in nude mice. Prostate 42:304–314CrossRef
49.
Zurück zum Zitat Goetzl MA, Van Veldhuizen PJ, Thrasher JB (2007) Effects of soy phytoestrogens on the prostate. Prostate Cancer Prostatic Dis 10:216–223CrossRef Goetzl MA, Van Veldhuizen PJ, Thrasher JB (2007) Effects of soy phytoestrogens on the prostate. Prostate Cancer Prostatic Dis 10:216–223CrossRef
50.
Zurück zum Zitat Rao CV, Wang C-X, Simi B, Lubet R, Kelloff G, Steele V, Reddy BS (1997) Enhancement of experimental colon cancer by genistein. Cancer Res 57:3717–3722 Rao CV, Wang C-X, Simi B, Lubet R, Kelloff G, Steele V, Reddy BS (1997) Enhancement of experimental colon cancer by genistein. Cancer Res 57:3717–3722
51.
Zurück zum Zitat Jackson MD, McFarlane-Anderson ND, Simon GA, Bennett FI, Walker SP (2010) Urinary phytoestrogens and risk of prostate cancer in Jamaican men. Cancer Causes Control 21(12):2249–2257CrossRef Jackson MD, McFarlane-Anderson ND, Simon GA, Bennett FI, Walker SP (2010) Urinary phytoestrogens and risk of prostate cancer in Jamaican men. Cancer Causes Control 21(12):2249–2257CrossRef
52.
Zurück zum Zitat Chen L-H, Fang J, Sun Z, Li H, Wu Y, Denmark-Wahnefried W, Lin X (2009) Enterolactone inhibits insulin-like growth factor-1 receptor signaling in human prostatic carcinoma PC-3 cells. J Nutr 139(4):653–659CrossRef Chen L-H, Fang J, Sun Z, Li H, Wu Y, Denmark-Wahnefried W, Lin X (2009) Enterolactone inhibits insulin-like growth factor-1 receptor signaling in human prostatic carcinoma PC-3 cells. J Nutr 139(4):653–659CrossRef
53.
Zurück zum Zitat Penalvo JL, Lopez-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):751–756CrossRef Penalvo JL, Lopez-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):751–756CrossRef
54.
Zurück zum Zitat 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(9196):2112–2115CrossRef 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(9196):2112–2115CrossRef
55.
Zurück zum Zitat 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(10):571–603CrossRef 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(10):571–603CrossRef
56.
Zurück zum Zitat Frankenfeld CL (2014) Cardiometabolic risk factors are associated with high urinary enterolactone concentration, independent of urinary enterodiol concentration and dietary fiber intake in adults. J Nutr 144(9):1446–1453CrossRef Frankenfeld CL (2014) Cardiometabolic risk factors are associated with high urinary enterolactone concentration, independent of urinary enterodiol concentration and dietary fiber intake in adults. J Nutr 144(9):1446–1453CrossRef
57.
Zurück zum Zitat 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(3):395–403CrossRef 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(3):395–403CrossRef
58.
Zurück zum Zitat Struja T, Richard A, Linseisen J, Eichholzer M, Rohrmann S (2014) The association between urinary phytoestrogen excretion and components of the metabolic syndrome in NHANES. Eur J Nutr 53(6):1371–1381CrossRef Struja T, Richard A, Linseisen J, Eichholzer M, Rohrmann S (2014) The association between urinary phytoestrogen excretion and components of the metabolic syndrome in NHANES. Eur J Nutr 53(6):1371–1381CrossRef
59.
Zurück zum Zitat Prasad K (2005) Hypocholesterolemic and antiantherosclerotic effect of flax lignan complex isolated from flaxseed. Atherosclerosis 179(2):269–275CrossRef Prasad K (2005) Hypocholesterolemic and antiantherosclerotic effect of flax lignan complex isolated from flaxseed. Atherosclerosis 179(2):269–275CrossRef
60.
Zurück zum Zitat Prasad K (2008) Regression of hypercholesterolemic atherosclerosis in rabbits by secoisolariciresinol diglucoside isolated from flaxseed. Atherosclerosis 197(1):34–42CrossRef Prasad K (2008) Regression of hypercholesterolemic atherosclerosis in rabbits by secoisolariciresinol diglucoside isolated from flaxseed. Atherosclerosis 197(1):34–42CrossRef
61.
Zurück zum Zitat Penumathsa SV, Koneru S, Thirunavukkarasu M, Zhan L, Prasad K, Maulik N (2007) Secoisolariciresinol diglucoside: relevance to angiogenesis and cardioprotection against ischemia-reperfusion injury. J Pharmacol Exp Ther 320(2):951–959CrossRef Penumathsa SV, Koneru S, Thirunavukkarasu M, Zhan L, Prasad K, Maulik N (2007) Secoisolariciresinol diglucoside: relevance to angiogenesis and cardioprotection against ischemia-reperfusion injury. J Pharmacol Exp Ther 320(2):951–959CrossRef
62.
Zurück zum Zitat Carmeliet P, Ng YS, Nuyens D, Theilmeier G, Brusselmans K, Cornelissen I, Ehler E, Kakkar VV, Stalmans I, Mattot V, Perriard JC, Dewerchin M, Flameng W, Nagy A, Lupu F, Moons L, Collen D, D’Amore PA, Shima DT (1999) Impaired myocardial angiogenesis and ischemic cardiomyopathy in mice lacking the vascular endothelial growth factor isoforms VEGF 164 and VEGF188. Nat Med 5(5):495–502CrossRef Carmeliet P, Ng YS, Nuyens D, Theilmeier G, Brusselmans K, Cornelissen I, Ehler E, Kakkar VV, Stalmans I, Mattot V, Perriard JC, Dewerchin M, Flameng W, Nagy A, Lupu F, Moons L, Collen D, D’Amore PA, Shima DT (1999) Impaired myocardial angiogenesis and ischemic cardiomyopathy in mice lacking the vascular endothelial growth factor isoforms VEGF 164 and VEGF188. Nat Med 5(5):495–502CrossRef
63.
Zurück zum Zitat Hodis HN, Mack WJ, Kono N, Azen SP, Shoupe D, Hwang-Levine J, Petitti D, Whitfield-Maxwell L, Yan M, Franke AA, Selzer RH (2011) Isoflavone soy protein supplementation and atherosclerosis progression in healthy postmenopausal women: a randomized controlled trial. Stroke 42:3168–3175CrossRef Hodis HN, Mack WJ, Kono N, Azen SP, Shoupe D, Hwang-Levine J, Petitti D, Whitfield-Maxwell L, Yan M, Franke AA, Selzer RH (2011) Isoflavone soy protein supplementation and atherosclerosis progression in healthy postmenopausal women: a randomized controlled trial. Stroke 42:3168–3175CrossRef
64.
Zurück zum Zitat Li S-H, Liu X-X, Bai Y-Y, Wang X-J, Sun K, Chen J-Z, Hui R-T (2010) Effect of oral supplementation on vascular endothelial function in postmenopausal women: a meta-analysis of randomized placebo-controlled trials. Am J Clin Nutr 91(2):480–486CrossRef Li S-H, Liu X-X, Bai Y-Y, Wang X-J, Sun K, Chen J-Z, Hui R-T (2010) Effect of oral supplementation on vascular endothelial function in postmenopausal women: a meta-analysis of randomized placebo-controlled trials. Am J Clin Nutr 91(2):480–486CrossRef
65.
Zurück zum Zitat 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(2):260–266 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(2):260–266
66.
Zurück zum Zitat Kelly LA, O’Leary JJ, Seidlova-Wuttke D, Wuttke W, Norris LA (2010) Genistein alters coagulation gene expression in ovariectomised rats treated with phytoestrogens. Thromb Haemost 104:1250–1257CrossRef Kelly LA, O’Leary JJ, Seidlova-Wuttke D, Wuttke W, Norris LA (2010) Genistein alters coagulation gene expression in ovariectomised rats treated with phytoestrogens. Thromb Haemost 104:1250–1257CrossRef
67.
Zurück zum Zitat Liggins J, Mulligan A, Runswick S, Bingham SA (2002) Daidzein and genistein content of cereals. Eur J Clin Nutr 56:961–966CrossRef Liggins J, Mulligan A, Runswick S, Bingham SA (2002) Daidzein and genistein content of cereals. Eur J Clin Nutr 56:961–966CrossRef
68.
Zurück zum Zitat Liggins J, Bluck LJ, Runswick S, Atkinson C, Coward WA, Bingham SA (2000) Daidzein and genistein contents of vegetables. Br J Nutr 84:717–725 Liggins J, Bluck LJ, Runswick S, Atkinson C, Coward WA, Bingham SA (2000) Daidzein and genistein contents of vegetables. Br J Nutr 84:717–725
69.
Zurück zum Zitat Liggins J, Bluck LJ, Runswick S, Atkinson C, Coward WA, Bingham SA (2000) Daidzein and genistein content of fruits and nuts. J Nutr Biochem 11(6):326–331CrossRef Liggins J, Bluck LJ, Runswick S, Atkinson C, Coward WA, Bingham SA (2000) Daidzein and genistein content of fruits and nuts. J Nutr Biochem 11(6):326–331CrossRef
70.
Zurück zum Zitat Rowland I, Faughnan M, Hoey L, Wahala K, Williamson G, Cassidy A (2003) Bioavailability of phyto-oestrogens. Br J Nutr 89:S45–S58 Rowland I, Faughnan M, Hoey L, Wahala K, Williamson G, Cassidy A (2003) Bioavailability of phyto-oestrogens. Br J Nutr 89:S45–S58
71.
Zurück zum Zitat Bhaqwat S, Haytowitz DB, Holden JM (2008) USDA Database for the Isoflavone Content of Selected Foods, vol 2. Nutrient Data Laboratory, Beltsville Bhaqwat S, Haytowitz DB, Holden JM (2008) USDA Database for the Isoflavone Content of Selected Foods, vol 2. Nutrient Data Laboratory, Beltsville
72.
Zurück zum Zitat Park SY, 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(1):185–191CrossRef Park SY, 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(1):185–191CrossRef
73.
Zurück zum Zitat Atkinson C, Skor HE, Fitzgibbons ED, Scholes D, Chen C, Wahala K, Schwartz SM, Lampe JW (2002) Overnight urinary isoflavone excretion in a population of women living in the United States, and its relationship to isoflavone intake. Cancer Epidemiol Biomarkers Prev 11:253–260 Atkinson C, Skor HE, Fitzgibbons ED, Scholes D, Chen C, Wahala K, Schwartz SM, Lampe JW (2002) Overnight urinary isoflavone excretion in a population of women living in the United States, and its relationship to isoflavone intake. Cancer Epidemiol Biomarkers Prev 11:253–260
74.
Zurück zum Zitat Barr DB, Wilder LC, Caudill SP, Gonzalez AJ, Needham LL, Pirkle JL (2005) Urinary creatinine concentrations in the U.S. population: implications for urinary biologic monitoring measurements. Environ Health Perspect 113(2):192–200CrossRef Barr DB, Wilder LC, Caudill SP, Gonzalez AJ, Needham LL, Pirkle JL (2005) Urinary creatinine concentrations in the U.S. population: implications for urinary biologic monitoring measurements. Environ Health Perspect 113(2):192–200CrossRef
75.
Zurück zum Zitat Grace PB, Taylor JI, Low Y-L, Luben RN, Mulligan AA, Botting NP, Dowsett M, Welch AA, Khaw K-T, 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 Biomarkers Prev 13(5):698–708 Grace PB, Taylor JI, Low Y-L, Luben RN, Mulligan AA, Botting NP, Dowsett M, Welch AA, Khaw K-T, 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 Biomarkers Prev 13(5):698–708
Metadaten
Titel
Urinary phytoestrogens and cancer, cardiovascular, and all-cause mortality in the continuous National Health and Nutrition Examination Survey
verfasst von
Michael K. Reger
Terrell W. Zollinger
Ziyue Liu
Josette Jones
Jianjun Zhang
Publikationsdatum
06.05.2015
Verlag
Springer Berlin Heidelberg
Erschienen in
European Journal of Nutrition / Ausgabe 3/2016
Print ISSN: 1436-6207
Elektronische ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-015-0917-y

Weitere Artikel der Ausgabe 3/2016

European Journal of Nutrition 3/2016 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.