Cited by 107Phytoestrogen effects and researchEffects and risks of endocrine disrupting chemicalsEstrogen and related hormone effects

Endocrine disruption by dietary phyto-oestrogens: impact on dimorphic sexual systems and behaviours

Open access
Patisaul, Heather B.·2017·Proceedings of the Nutrition Society

Abstract

A wide range of health benefits have been ascribed to soya intake including a lowered risk of osteoporosis, heart disease, breast cancer, and menopausal symptoms. Because it is a hormonally active diet, however, soya can also be endocrine disrupting, suggesting that intake has the potential to cause adverse health effects in certain circumstances, particularly when exposure occurs during development. Consequently, the question of whether or not soya phyto-oestrogens are beneficial or harmful to human health is neither straightforward nor universally applicable to all groups. Possible benefits and risks depend on age, health status, and even the presence or absence of specific gut microflora. As global consumption increases, greater awareness and consideration of the endocrine-disrupting properties of soya by nutrition specialists and other health practitioners is needed. Consumption by infants and small children is of particular concern because their hormone-sensitive organs, including the brain and reproductive system, are still undergoing sexual differentiation and maturation. Thus, their susceptibility to the endocrine-disrupting activities of soya phyto-oestrogens may be especially high. As oestrogen receptor partial agonists with molecular and cellular properties similar to anthropogenic endocrine disruptors such as bisphenol A, the soya phyto-oestrogens provide an interesting model for how attitudes about what is ‘synthetic’v. what is ‘natural,’ shapes understanding and perception of what it means for a compound to be endocrine disrupting and/or potentially harmful. This review describes the endocrine-disrupting properties of soya phyto-oestrogens with a focus on neuroendocrine development and behaviour.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1017/s0029665116000677

Cites

13 of 13 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Evidence of endocrine disrupting properties of GEN dates back decades, and soy is well recognized as a hormonally active food.

    “Evidence of the endocrine disrupting properties of GEN dates back decades, and soy is so well recognized as a hormonally active food, that it is frequently advertised and promoted as such (15, 111–115).”
  • There are some data showing endocrine disruption of AVP-related pathways and systems, including behaviors, by GEN.

    “but there are some data showing endocrine disruption of AVP-related pathways and systems, including behaviors (112).”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 196

  1. [1]Patisaul HB Jefferson W 2010 The pros and cons of phytoestrogens Front Neuroendocrinol 31 400 419 20347861 PMC3074428
  2. [3]Helferich WG Andrade JE Hoagland MS 2008 Phytoestrogens and breast cancer: a complex story Inflammopharmacology 16 219 226 18815740
  3. [4]Cederroth CR Auger J Zimmermann C 2010 Soy, phyto-oestrogens and male reproductive function: a review Int J Androl 33 304 316 19919579
  4. [5]Cederroth CR Zimmermann C Nef S 2012 Soy, phytoestrogens and their impact on reproductive health Mol Cell Endocrinol 355 192 200 22210487
  5. [6]Messina M 2010 A brief historical overview of the past two decades of soy and isoflavone research J Nutr 140 1350S 1354S 20484551
  6. [7]Whitten PL Kudo S Okubo KK 1997 Isoflavonoids Handbook of Plant and Fungal Toxicants 117 137 D’Mello JPF Boca Raton CRC Press
  7. [8]Kurzer MS Xu X 1997 Dietary phytoestrogens Annu Rev Nutr 17 353 381 9240932
  8. [9]Setchell KD 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 12468591
  9. [10]Setchell KD Brown NM Desai PB 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 12672914
  10. [11]Lampe J Karr S Hutchins A 1998 Urinary equol excretion with a soy challenge: influence of habitual diet PSEBM 217 335 339 9492344
  11. [12]Balk E Chung M Chew P 2005 Effects of soy on health outcomes Evid Rep Technol Assess (Summ) 126 1 8 PMC4781302 16194125
  12. [13]Jacobs A Wegewitz U Sommerfeld C 2009 Efficacy of isoflavones in relieving vasomotor menopausal symptoms – a systematic review Mol Nutr Food Res 53 1084 1097 19653225
  13. [15]Rozman KK Bhatia J Calafat AM 2006 NTP-CERHR expert panel report on the reproductive and developmental toxicity of genistein Birth Defects Res B Dev Reprod Toxicol 77 485 638 17186522 PMC2020434
  14. [16]National Toxicology Program 2008 NTP multigenerational reproductive study of Genistein (CAS no. 446-72-0) in Sprague–Dawley rats (Feed Study) Natl Toxicol Program Tech Rep Ser 1 266 18685713
  15. [17]Whitten PL Patisaul HB 2001 Cross-species and inter-assay comparisons of phytoestrogen action Environ Health Perspect 109 5 23 11250801 PMC1240538
  16. [20]Diamanti-Kandarakis E Bourguignon JP Giudice LC 2009 Endocrine-disrupting chemicals: an Endocrine Society scientific statement Endocr Rev 30 293 342 19502515 PMC2726844
  17. [21]Waye A Trudeau VL 2011 Neuroendocrine disruption: more than hormones are upset J Toxicol Environ Health B Crit Rev 14 270 291 21790312 PMC3173749
  18. [22]Gore AC Patisaul HB 2010 Neuroendocrine disruption: historical roots, current progress, questions for the future Front Neuroendocrinol 31 395 399 20638407 PMC2964387
  19. [23]Bennetts HW Underwood EJ Shier FL 1946 A specific breeding problem of sheep on subterranean clover pastures in Western Australia Aust Vet J 22 2 21028682
  20. [25]Adams NR 1995 Detection of the effects of phytoestrogens on sheep and cattle J Anim Sci 73 1509 1515 7665383
  21. [26]Green CC Kelly AM 2009 Effects of the estrogen mimic genistein as a dietary component on sex differentiation and ethoxyresorufin-O-deethylase (EROD) activity in channel catfish (Ictalurus punctatus) Fish Physiol Biochem 35 377 384 18777198
  22. [27]Gontier-Latonnelle K Cravedi JP Laurentie M 2007 Disposition of genistein in rainbow trout (Oncorhynchus mykiss) and siberian sturgeon (Acipenser baeri) Gen Comp Endocrinol 150 298 308 17097654
  23. [28]Whitten PL Naftolin F 1991 Dietary plant estrogens: a biologically active background for estrogen action The New Biology of Steroid Hormones 74 155 167 Hochberg RB NF New York Raven Press
  24. [29]Leopold A Erwin M Oh J 1976 Phytoestrogens: adverse effects on reproduction in California quail Science 191 98 100 1246602
  25. [30]Setchell K Gosselin S Welsh M 1987 Dietary estrogens – a probable cause of infertility and liver disease in captive cheetahs Gastroenterology 93 225 233 3297906
  26. [31]Sassi-Messai S Gibert Y Bernard L 2009 The phytoestrogen genistein affects zebrafish development through two different pathways PLoS ONE 4 e4935 19319186 PMC2655710
  27. [32]Clotfelter ED Rodriguez AC 2006 Behavioral changes in fish exposed to phytoestrogens Environ Pollut 144 833 839 16584819
  28. [33]Tubbs C Hartig P Cardon M 2012 Activation of Southern White Rhinoceros (Ceratotherium simum simum) estrogen receptors by phytoestrogens: potential role in the reproductive failure of captive-born females? Endocrinology 153 1444 1452 22253418 PMC3281539
  29. [35]Divi RL Chang HC Doerge DR 1997 Anti-thyroid isoflavones from soybean: isolation, characterization, and mechanisms of action Biochem Pharmacol 54 1087 1096 9464451
  30. [37]Li J Teng X Wang W 2011 Effects of dietary soy intake on maternal thyroid functions and serum anti-thyroperoxidase antibody level during early pregnancy J Med Food 14 543 550 21314363
  31. [38]Hooper L Ryder JJ Kurzer MS 2009 Effects of soy protein and isoflavones on circulating hormone concentrations in pre- and post-menopausal women: a systematic review and meta-analysis Hum Reprod Update 15 423 440 19299447 PMC2691652
  32. [39]Chandrareddy A Muneyyirci-Delale O McFarlane SI 2008 Adverse effects of phytoestrogens on reproductive health: a report of three cases Complem Ther Clin Pract 14 132 135 18396257
  33. [40]Gore AC Chappell VA Fenton SE 2015 EDC-2: the endocrine society’s second scientific statement on endocrine-disrupting chemicals Endocr Rev 36 E1 E150 26544531 PMC4702494
  34. [41]Freni-Titulaer LLW Cordero JJF Haddock LL 1986 Premature thelarche in Puerto Rico. A search for environmental factors Am J Dis Child 140 1263 1267 3776944
  35. [42]Schoental R 1983 Precocious sexual development in Puerto Rico and oestrogenic mycotoxins (zearalenone) Lancet 1 537 6131246
  36. [43]Strom BL Schinnar R Ziegler EE 2001 Exposureto soy-based formula in infancy and endocrinological and reproductive outcomes in young adulthood JAMA 286 807 814 11497534
  37. [44]D’Aloisio AA Baird DD DeRoo LA 2009 Association of intrauterine and early life exposures with diagnosis of uterine leiomyomata by age 35 in the sister study Environ Health Perspect 118 375 381 PMC2854766 20194067
  38. [45]Bernbaum JC Umbach DM Ragan NB 2008 Pilot studies of estrogen-related physical findings in infants Environ Health Perspect 116 416 420 18335112 PMC2265048
  39. [46]Andres A Moore MB Linam LE 2015 Compared with feeding infants breast milk or cow-milk formula, soy formula feeding does not affect subsequent reproductive organ size at 5 years of age J Nutr 145 871 875 25761499
  40. [47]D’Aloisio AA DeRoo LA Baird DD 2013 Prenatal and infant exposures and age at menarche Epidemiology 24 277 284 23348069 PMC3563843
  41. [48]Adgent MA Daniels JL Rogan WJ 2012 Early-life soy exposure and age at menarche Paediatr Perinat Epidemiol 26 163 175 22324503 PMC3443957
  42. [49]Frye CA Bo E Calamandrei G 2012 Endocrine disrupters: a review of some sources, effects, and mechanisms of actions on behaviour and neuroendocrine systems J Neuroendocrinol 24 144 159 21951193 PMC3245362
  43. [50]Patisaul HB Adewale HB 2009 Long-term effects of environmental endocrine disruptors on reproductive physiology and behavior Front Behav Neurosci 3 10 19587848 PMC2706654
  44. [51]Mahmoud AM Yang W Bosland MC 2014 Soy isoflavones and prostate cancer: a review of molecular mechanisms J Steroid Biochem Mol Biol 140 116 132 24373791 PMC3962012
  45. [52]Kuiper GGJM Lemmen JG Carlsson B 1998 Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor β Endocrinology 139 4252 4263 9751507
  46. [53]Pfitscher A Reiter E Jungbauer A 2008 Receptor binding and transactivation activities of red clover isoflavones and their metabolites J Steroid Biochem Mol Biol 112 87 94 18809497
  47. [54]Casanova M You L Gaido K 1999 Developmental effects of dietary phytoestrogens in Sprague–Dawley rats and interactions of genistein and daidzein with rat estrogen receptors alpha and beta in vitro Toxicol Sci 51 236 244 10543025
  48. [55]Kuiper GGJM Carlsson B Grandien K 1997 Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors α and β Endocrinology 138 863 870 9048584
  49. [56]Rappaport SM Smith MT 2010 Epidemiology. Environment and disease risks Science 330 460 461 20966241 PMC4841276
  50. [57]Cao J Patisaul HB 2013 Sex specific expression of estrogen receptors alpha and beta and kiss1 in the postnatal rat amygdala J Comp Neurol 521 465 478 22791648 PMC3492514
  51. [58]Cao J Patisaul HB 2011 Sexually dimorphic expression of hypothalamic estrogen receptors alpha and beta and kiss1 in neonatal male and female rats J Comp Neurol 519 2954 2977 21484804 PMC3874381
  52. [59]Schwarz JM Nugent BM McCarthy MM 2010 Developmental and hormone-induced epigenetic changes to estrogen and progesterone receptor genes in brain are dynamic across the life span Endocrinology 151 4871 4881 20702577 PMC2946142
  53. [60]Shughrue P Lane M Scrimo P 1998 Comparative distribution of estrogen receptor-α (ERα) and β (ERβ) mRNA in the rat pituitary, gonad, and reproductive tract Steroids 63 498 504 9800279
  54. [62]Koehler KF Helguero LA Haldosen LA 2005 Reflections on the discovery and significance of estrogen receptor beta Endocr Rev 26 465 478 15857973
  55. [63]Drummond A Fuller P 2009 The importance of ER {beta} signalling in ovarian function J Endocrinol 205 15 23 20019181
  56. [65]Rissman EF 2008 Roles of oestrogen receptors alpha and beta in behavioural neuroendocrinology: beyond Yin/Yang J Neuroendocrinol 20 873 879 18601711 PMC2667101
  57. [66]Simerly RB 2002 Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain Annu Rev Neurosci 25 507 536 12052919
  58. [67]Wright CL Schwarz JS Dean SL 2010 Cellular mechanisms of estradiol-mediated sexual differentiation of the brain Trend Endocrinol Metab 21 553 561 PMC2941875 20813326
  59. [68]Jia M Dahlman-Wright K Gustafsson JA 2015 Estrogen receptor alpha and beta in health and disease Best Pract Res Clin Endocrinol Metab 29 557 568 26303083
  60. [70]Handa RJ Weiser MJ Zuloaga DG 2009 A role for the androgen metabolite, 5alpha-androstane-3beta,17beta-diol, in modulating oestrogen receptor beta-mediated regulation of hormonal stress reactivity J Neuroendocrinol 21 351 358 19207807 PMC2727750
  61. [71]Acevedo-Rodriguez A Mani SK Handa RJ 2015 Oxytocin and estrogen receptor beta in the brain: an overview Front Endocrinol (Lausanne) 6 160 26528239 PMC4606117
  62. [72]Zhang JQ Cai WQ de Zhou S 2002 Distribution and differences of estrogen receptor beta immunoreactivity in the brain of adult male and female rats Brain Res 935 73 80 12062475
  63. [73]Fan X Xu H Warner M 2010 ERbeta in CNS: new roles in development and function Prog Brain Res 181 233 250 20478441
  64. [74]Kushner PJ Agard DA Greene GL 2000 Estrogen receptor pathways to AP-1 J Steroid Biochem Mol Biol 74 311 317 11162939
  65. [75]Levin ER 2009 Membrane oestrogen receptor alpha signalling to cell functions J Physiol 587 5019 5023 19687123 PMC2790244
  66. [76]Micevych P Kuo J Christensen A 2009 Physiology of membrane oestrogen receptor signalling in reproduction J Neuroendocrinol 21 249 256 19207814 PMC2667562
  67. [77]Vasudevan N Pfaff DW 2008 Non-genomic actions of estrogens and their interaction with genomic actions in the brain Front Neuroendocrinol 29 238 257 18083219
  68. [78]Kow LM Pfaff DW 2016 Rapid estrogen actions on ion channels: a survey in search for mechanisms Steroids 111 46 53 26939826 PMC4929851
  69. [79]Belcher SM Zsarnovszky A 2001 Estrogenic actions in the brain: estrogen, phytoestrogens, and rapid intracellular signaling mechanisms J Pharmacol Exp Ther 299 408 414 11602649
  70. [80]Thomas P Dong J 2006 Binding and activation of the seven-transmembrane estrogen receptor GPR30 by environmental estrogens: a potential novel mechanism of endocrine disruption J Steroid Biochem Mol Biol 102 175 179 17088055
  71. [81]Barton M 2016 Not lost in translation: emerging clinical importance of the G protein-coupled estrogen receptor GPER Steroids 111 37 45 26921679
  72. [82]Shanle EK Xu W 2011 Endocrine disrupting chemicals targeting estrogen receptor signaling: identification and mechanisms of action Chem Res Toxicol 24 6 19 21053929 PMC3119362
  73. [83]Li Y Tollefsbol TO 2010 Impact on DNA methylation in cancer prevention and therapy by bioactive dietary components Curr Med Chem 17 2141 2151 20423306 PMC2904405
  74. [84]Labinskyy N Csiszar A Veress G 2006 Vascular dysfunction in aging: potential effects of resveratrol, an anti-inflammatory phytoestrogen Curr Med Chem 13 989 996 16611080 PMC2228263
  75. [85]Franke AA Custer LJ 1994 High-performance liquid chromatographic assay of isoflavonoids and coumestrol from human urine J Chromatogr B Biomed Appl 662 47 60 7894693
  76. [86]Patel S Zhou C Rattan S 2015 Effects of endocrine-disrupting chemicals on the ovary Biol Reprod 93 20 26063868 PMC6366440
  77. [87]Piasecka-Srader J Kolomycka A Nynca A 2014 Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin and phytoestrogen genistein on the activity and the presence of steroi-dogenic enzyme proteins in cultured granulosa cells of pigs Anim Reprod Sci 148 171 181 25022331
  78. [88]Tagawa N Kubota S Kobayashi Y 2015 Genistein inhibits glucocorticoid amplification in adipose tissue by suppression of 11beta-hydroxysteroid dehydrogenase type 1 Steroids 93 77 86 25447798
  79. [89]Taves MD Plumb AW Sandkam BA 2015 Steroid profiling reveals widespread local regulation of glucocorticoid levels during mouse development Endocrinology 156 511 522 25406014
  80. [90]Remage-Healey L London SE Schlinger BA 2010 Birdsong and the neural production of steroids J Chem Neuroanat 39 72 81 19589382 PMC2821977
  81. [91]Fokidis HB Adomat HH Kharmate G 2015 Regulation of local steroidogenesis in the brain and in prostate cancer: lessons learned from interdisciplinary collaboration Front Neuroendocrinol 36 108 129 25223867
  82. [92]Pino AM Valladares LE Palma MA 2000 Dietary isoflavones affect sex hormone-binding globulin levels in postmenopausal women J Clin Endocrinol Metab 85 2797 2800 10946884
  83. [93]Low YL Dunning AM Dowsett M 2006 Implications of gene-environment interaction in studies of gene variants in breast cancer: an example of dietary isoflavones and the D356N polymorphism in the sex hormone-binding globulin gene Cancer Res 66 8980 8983 16982738
  84. [94]Tanaka M Fujimoto K Chihara Y 2009 Isoflavone supplements stimulated the production of serum equol and decreased the serum dihydrotestosterone levels in healthy male volunteers Prostate Cancer Prostatic Dis 12 247 252 19597532 PMC2834330
  85. [95]Maskarinec G Williams AE Inouye JS 2002 A randomized isoflavone intervention among premenopausal women Cancer Epidemiol Biomarkers Prev 11 195 201 11867507
  86. [96]Wu AH Stanczyk FZ Hendrich S 2000 Effects of soy foods on ovarian function in premenopausal women Br J Cancer 82 1879 1886 10839307 PMC2363237
  87. [97]Atkinson C Newton KM Stanczyk FZ 2008 Daidzein-metabolizing phenotypes in relation to serum hormones and sex hormone binding globulin, and urinary estrogen metabolites in premenopausal women in the United States Cancer Causes Control 19 1085 1093 18478336
  88. [98]Jackson RL Greiwe JS Schwen RJ 2011 Emerging evidence of the health benefits of S-equol, an estrogen receptor beta agonist Nutr Rev 69 432 448 21790611
  89. [99]Xia Y Chen M Zhu P 2013 Urinary phytoestrogen levels related to idiopathic male infertility in Chinese men Environ Int 59 161 167 23820060
  90. [100]Mumford SL Kim S Chen Z 2015 Urinary phytoestrogens are associated with subtle indicators of semen quality among male partners of couples desiring pregnancy J Nutr 145 2535 2541 26423741 PMC4620723
  91. [101]Patisaul HB Luskin JR Wilson ME 2004 A soy supplement and tamoxifen inhibit sexual behavior in female rats Horm Behav 45 270 277 15053943
  92. [102]Patisaul HB Dindo M Whitten PL 2001 Soy isoflavone supplements antagonize reproductive behavior and ERα- and ERβ-dependent gene expression in the brain Endocrinology 142 2946 2952 11416015
  93. [103]Patisaul HB Melby M Whitten PL 2002 Genistein affects ERβ-but not ERα-dependent gene expression in the hypothalamus Endocrinology 143 2189 2197 12021182
  94. [104]Martinez J Lewi JE 2008 An unusual case of gynecomastia associated with soy product consumption Endocr Pract 14 415 418 18558591
  95. [105]Kotsopoulos D Dalais FS Liang YL 2000 The effects of soy protein containing phytoestrogens on menopausal symptoms in postmenopausal women Climacteric 3 161 167 11910617
  96. [106]Lephart ED Setchell KD Handa RJ 2004 Behavioral effects of endocrine-disrupting substances: phytoestrogens Ilar J 45 443 454 15454683
  97. [107]Thomas AJ Ismail R Taylor-Swanson L 2014 Effects of isoflavones and amino acid therapies for hot flashes and co-occurring symptoms during the menopausal transition and early postmenopause: a systematic review Maturitas 78 263 276 24951101 PMC4120238
  98. [109]Patisaul HB 2005 Phytoestrogen action in the adult and developing brain J Neuroendocrinol 17 57 64 15720476
  99. [110]Patisaul HB Sullivan AW Radford ME 2012 Anxiogenic effects of developmental bisphenol a exposure are associated with gene expression changes in the juvenile rat amygdala and mitigated by soy PLoS ONE 7 e43890 22957036 PMC3434201
  100. [112]Hartley DE Edwards JE Spiller CE 2003 The soya isoflavone content of rat diet can increase anxiety and stress hormone release in the male rat Psychopharmacology (Berl) 167 46 53 12618915
  101. [113]Scallet AC Wofford M Meredith JC 2003 Dietary exposure to genistein increases vasopressin but does not alter beta-endorphin in the rat hypothalamus Toxicol Sci 72 296 300 12660364
  102. [114]Hrabovszky E Kallo I Hajszan T 1998 Expression of estrogen receptor-beta messenger ribonucleic acid in oxytocin and vasopressin neurons of the rat supraoptic and paraventricular nuclei Endocrinology 139 2600 2604 9564876
  103. [116]Patisaul HB Scordalakes EM Young LJ 2003 Oxytocin, but not oxytocin receptor, is regulated by oestrogen receptor beta in the female mouse hypothalamus J Neuroendocrinol 15 787 793 12834440
  104. [117]Nomura M McKenna E Korach K 2002 Estrogen receptor-β regulates transcript levels for oxytocin and arginine vasopressin in the hypothalamic paraventricular nucleus of male mice Mol Brain Res 109 84 94 12531518
  105. [118]Pfaff D 1999 Drive Cambridge, MASS MIT Press
  106. [119]Lephart ED West T Weber KS 2002 Neurobehavioral effects of dietary soy phytoestrogens Neurotoxicol Teratol 24 5 16 11836067
  107. [120]Lephart ED Setchell KD Lund TD 2005 Phytoestrogens: hormonal action and brain plasticity Brain Res Bull 65 193 198 15811581
  108. [121]Patisaul HB Polston EK 2008 Influence of endocrine active compounds on the developing rodent brain Brain Res Rev 57 352 362 17822772
  109. [122]Newbold RR 2008 Prenatal exposure to diethylstilbestrol (DES) Fertil Steril 89 e55 e56 18308064
  110. [123]Gorski RA 1963 Modification of ovulatory mechanisms by postnatal administration of estrogen to the rat Am J Physiol 205 842 844 5896305
  111. [124]Gorski RA 1985 Sexual dimorphisms of the brain J Anim Sci 61, Suppl 3 38 61 3908433
  112. [125]Lindzey J Korach KS 1997 Developmental and physiological effects of estrogen receptor gene disruption in mice Trends Endocrinol Metab 8 137 145 18406799
  113. [127]Reed CE Fenton SE 2013 Exposure to diethylstilbestrol during sensitive life stages: a legacy of heritable health effects Birth Defects Res C Embryo Today 99 134 146 23897597 PMC3817964
  114. [128]Newbold RR 2004 Lessons learned from perinatal exposure to diethylstilbestrol Toxicol Appl Pharmacol 199 142 150 15313586
  115. [129]Aksglaede L Sorensen K Petersen JH 2009 Recent decline in age at breast development: the Copenhagen Puberty Study Pediatrics 123 e932 e939 19403485
  116. [131]Mouritsen A Aksglaede L Sorensen K 2010 Hypothesis: exposure to endocrine-disrupting chemicals may interfere with timing of puberty Int J Androl 33 346 359 20487042
  117. [132]Zawatski W Lee MM 2013 Male pubertal development: are endocrine-disrupting compounds shifting the norms? J Endocrinol 218 R1 R12 23709001
  118. [133]Swan SH Elkin EP Fenster L 2000 The question of declining sperm density revisited: an analysis of 101 studies published 1934–1996 Environ Health Perspect 108 961 966 11049816 PMC1240129
  119. [134]Hauser R 2006 The environment and male fertility: recent research on emerging chemicals and semen quality Semin Reprod Med 24 156 167 16804814
  120. [135]Joensen UN Jorgensen N Rajpert-De Meyts E 2008 Testicular dysgenesis syndrome and Leydig cell function Basic Clin Pharmacol Toxicol 102 155 161 18226069
  121. [136]North K Golding J 2000 A maternal vegetarian diet in pregnancy is associated with hypospadias. The ALSPAC Study Team. Avon Longitudinal Study of Pregnancy and Childhood BJU Int 85 107 113 10619956
  122. [137]Skakkebaek NE Rajpert-De Meyts E Main KM 2001 Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects Hum Reprod 16 972 978 11331648
  123. [138]Fisher JS 2004 Environmental anti-androgens and male reproductive health: focus on phthalates and testicular dysgenesis syndrome Reproduction 127 305 315 15016950
  124. [139]Massart F Parrino R Seppia P 2006 How do environmental estrogen disruptors induce precocious puberty? Minerva Pediatr 58 247 254 16832329
  125. [140]Fowler PA Bellingham M Sinclair KD 2012 Impact of endocrine-disrupting compounds (EDCs) on female reproductive health Mol Cell Endocrinol 355 231 239 22061620
  126. [141]West MC Anderson L McClure N 2005 Dietary oestrogens and male fertility potential Hum Fertil (Camb) 8 197 207 16234205
  127. [142]Jefferson WN Newbold RR 2000 Potential endocrine-modulating effects of various phytoestrogens in the diet Nutrition 16 658 662 10906588
  128. [143]Patisaul HB Mabrey N Adewale HB 2014 Soy but not bisphenol A (BPA) induces hallmarks of polycystic ovary syndrome (PCOS) and related metabolic co-morbidities in rats Reprod Toxicol 49C 209 218 PMC4366357 25242113
  129. [144]Jefferson WN Padilla-Banks E Newbold RR 2005 Adverse effects on female development and reproduction in CD-1 mice following neonatal exposure to the phytoestrogen genistein at environmentally relevant doses Biol Reprod 73 798 806 15930323
  130. [145]Jefferson WN Padilla-Banks E Goulding EH 2009 Neonatal exposure to genistein disrupts ability of female mouse reproductive tract to support preimplantation embryo development and implantation Biol Reprod 80 425 431 19005167 PMC2677916
  131. [146]Cederroth CR Auger J Zimmermann C 2009 Soy, phyto-oestrogens and male reproductive function: a review Int J Androl 33 304 316 19919579
  132. [147]Tan KA Walker M Morris K 2006 Infant feeding with soy formula milk: effects on puberty progression, reproductive function and testicular cell numbers in marmoset monkeys in adulthood Hum Reprod 21 896 904 16476680
  133. [148]Sharpe RM Martin B Morris K 2002 Infant feeding with soy formula milk: effects on the testis and on blood testosterone levels in marmoset monkeys during the period of neonatal testicular activity Hum Reprod 17 1692 1703 12093826
  134. [149]Eustache F Mondon F Canivenc-Lavier MC 2009 Chronic dietary exposure to a low-dose mixture of genistein and vinclozolin modifies the reproductive axis, testis transcriptome, and fertility Environ Health Perspect 117 1272 1279 19672408 PMC2721872
  135. [150]Delclos KB Bucci TJ Lomax LG 2001 Effects of dietary genistein exposure during development on male and female CD (Sprague–Dawley) rats Reprod Toxicol 15 647 663 11738518
  136. [151]Delclos KB Newbold R 2007 NTP Toxicity Report of Reproductive Dose Range-Finding Study of Genistein (CAS No. 446-72-0) Administered in Feed to Sprague–Dawley Rats Toxicity Report Series 1-C2 18685712
  137. [152]Boberg J Mandrup KR Jacobsen PR 2013 Endocrine disrupting effects in rats perinatally exposed to a dietary relevant mixture of phytoestrogens Reprod Toxicol 40 41 51 23770295
  138. [153]Rudel RA Fenton SE Ackerman JM 2011 Environmental exposures and mammary gland development: state of the science, public health implications, and research recommendations Environ Health Perspect 119 1053 1061 21697028 PMC3237346
  139. [154]Fenton SE 2006 Endocrine-disrupting compounds and mammary gland development: early exposure and later life consequences Endocrinology 147 S18 S24 16690811
  140. [155]Rebuli ME Patisaul HB 2015 Assessment of sex specific endocrine disrupting effects in the prenatal and pre-pubertal rodent brain J Steroid Biochem Mol Biol 160 148 159 26307491 PMC4762757
  141. [156]Cooke B Hegstrom C Villeneuve L 1998 Sexual differentiation of the vertebrate brain: principles and mechanisms Front Neuroendocrinol 19 323 362 9799588
  142. [157]Ahmed EI Zehr JL Schulz KM 2008 Pubertal hormones modulate the addition of new cells to sexually dimorphic brain regions Nat Neurosci 11 995 997 19160494 PMC2772186
  143. [158]Sisk CL 2016 Hormone-dependent adolescent organization of socio-sexual behaviors in mammals Curr Opin Neurobiol 38 63 68 26963894 PMC4921305
  144. [159]Doerge DR Churchwell MI Chang HC 2001 Placental transfer of the soy isoflavone genistein following dietary and gavage administration to Sprague Dawley rats Reprod Toxicol 15 105 110 11297868
  145. [160]Doerge DR Twaddle NC Churchwell MI 2006 Lactational transfer of the soy isoflavone, genistein, in Sprague–Dawley rats consuming dietary genistein Reprod Toxicol 21 307 312 16257506
  146. [161]Chang HC Churchwell MI Delclos KB 2000 Mass spectrometric determination of genistein tissue distribution in diet-exposed Sprague–Dawley rats J Nutr 130 1963 1970 10917909
  147. [162]Gorski RA Gordon JH Shryne JE 1978 Evidence for a morphological sex difference within the medial pre-optic area of the rat brain Brain Res 143 333 346 656937
  148. [163]Shughrue PL Lane MV Merchenthaler I 1997 Comparative distribution of estrogen receptor α and β mRNA intherat central nervous system J Comp Neurol 388 507 525 9388012
  149. [164]Patchev AV Gotz F Rohde W 2004 Differential role of estrogen receptor isoforms in sex-specific brain organization FASEB J 18 1568 1570 15289439
  150. [166]Scallet AC Divine RL Newbold RR 2004 Increased volume of the calbindin D28k-labeled sexually dimorphic hypothalamus in genistein and nonylphenol-treated male rats1 Toxicol Sci 82 570 576 15456915
  151. [167]Lewis RW Brooks N Milburn GM 2003 The effects of the phytoestrogen genistein on the postnatal development of the rat Toxicol Sci 71 74 83 12520077
  152. [168]Patisaul HB Fortino AE Polston EK 2007 Differential disruption of nuclear volume and neuronal phenotype in the preoptic area by neonatal exposure to genistein and bisphenol-A Neurotoxicology 28 1 12 17109964
  153. [169]Faber KA Hughes CL Jr 1993 Dose-response characteristics of neonatal exposure to genistein on pituitary responsiveness to gonadotropin releasing hormone and volume of the sexually dimorphic nucleus of the preoptic area (SDN-POA) in postpubertal castrated female rats Reprod Toxicol 7 35 39 8448414
  154. [170]Masutomi N Shibutani M Takagi H 2003 Impact of dietary exposure to methoxychlor, genistein, or diisononyl phthalate during the perinatal period on the development of the rat endocrine/reproductive systems in later life Toxicology 192 149 170 14580783
  155. [171]Davis EC Shryne JE Gorski RA 1996 Structural sexual dimorphisms in the anteroventral periventricular nucleus of the rat hypothalamus are sensitive to gonadal steroids perinatally, but develop peripubertally Neuroendocrinology 63 142 148 9053778
  156. [172]Cooke B Hegstrom CD Villeneuve LS 1998 Sexual differentiation of the vertebrate brain: principles and mechanisms Front Neuroendocrinol 19 323 362 9799588
  157. [173]Gorski RA Mennin SP Kubo K 1975 The neural and hormonal bases of the reproductive cycle of the rat Adv Exp Med Biol 54 115 153 1092141
  158. [174]Elkind-Hirsch K King JC Gerall AA 1981 The luteinizing hormone-releasing hormone (LHRH) system in normal and estrogenized neonatal rats Brain Res Bull 7 645 654 7034869
  159. [175]Semaan SJ Kauffman AS 2010 Sexual differentiation and development of forebrain reproductive circuits Curr Opin Neurobiol 20 424 431 20471241 PMC2937059
  160. [176]Grumbach MM 2002 The neuroendocrinology of human puberty revisited Horm Res 57, Suppl 2 2 14 12065920
  161. [177]McCarthy MM Wright CL Schwarz JM 2009 New tricks by an old dogma: mechanisms of the Organizational/Activational Hypothesis of steroid-mediated sexual differentiation of brain and behavior Horm Behav 55 655 665 19682425 PMC2742630
  162. [178]Schwarz JM McCarthy MM 2008 Cellular mechanisms of estradiol-mediated masculinization of the brain J Steroid Biochem Mol Biol 109 300 306 18430566 PMC2493288
  163. [179]Bateman HL Patisaul HB 2008 Disrupted female reproductive physiology following neonatal exposure to phytoestrogens or estrogen specific ligands is associated with decreased GnRH activation and kisspeptin fiber density in the hypothalamus Neurotoxicology 29 988 997 18656497 PMC2647326
  164. [180]Patisaul HB Todd KL Mickens JA 2009 Impact of neonatal exposure to the ERα agonist PPT, bisphenol-a or phytoestrogens on hypothalamic kisspeptin fiber density in male and female rats Neurotoxicology 3 10 PMC3691558 19442818
  165. [181]Bateman HL Patisaul HB 2008 Disrupted female reproductive physiology following neonatal exposure to phytoestrogens or estrogen specific ligands is associated with decreased GnRH activation and kisspeptin fiber density in the hypothalamus Neurotoxicology 29 988 997 18656497 PMC2647326
  166. [182]Oakley AE Clifton DK Steiner RA 2009 Kisspeptin signaling in the brain Endocr Rev 30 713 743 19770291 PMC2761114
  167. [183]Piet R de Croft S Liu X 2015 Electrical properties of kisspeptin neurons and their regulation of GnRH neurons Front Neuroendocrinol 36 15 27 24907402
  168. [184]Patisaul HB 2013 Effects of environmental endocrine disruptors and phytoestrogens on the kisspeptin system Adv Exp Med Biol 784 455 479 23550019
  169. [185]Badger TM Ronis MJ Hakkak R 2002 The health consequences of early soy consumption J Nutr 132 559S 565S 11880593
  170. [186]Forsyth BW McCarthy PL Leventhal JM 1985 Problems of early infancy, formula changes, and mothers’ beliefs about their infants J Pediatr 106 1012 1017 3998939
  171. [187]Barrett JR 2006 The science of soy: what do we really know? Environ Health Perspect 114 A352 A358 16759972 PMC1480510
  172. [188]Bhatia J Greer F 2008 Use of soy protein-based formulas in infant feeding Pediatrics 121 1062 1068 18450914
  173. [189]Badger TM Gilchrist JM Pivik RT 2009 The health implications of soy infant formula Am J Clin Nutr 89 1668S 1672S 19357221
  174. [190]Barrett JR 2002 Soy and children’s health: a formula for trouble Environ Health Perspect 110 A294 A296 12055058 PMC1240881
  175. [191]Goldman LR Newbold R Swan SH 2001 Exposure to soy-based formula in infancy JAMA 286 2402 2403 11712933
  176. [192]Setchell KDR Zimmer-Nechemias L Cai J 1997 Exposure of infants to phyto-oestrogens from soy-based infant formula Lancet 350 23 27 9217716
  177. [193]Tuohy PG 2003 Soy infant formula and phytoestrogens J Paediatr Child Health 39 401 405 12919490
  178. [194]Zoppi G Guandalini S 1999 The story of soy formula feeding in infants: a road paved with good intentions J Pediatr Gastroenterol Nutr 28 541 543 10328136
  179. [195]Chen A Rogan WJ 2004 Isoflavones in soy infant formula: a review of evidence for endocrine and other activity in infants Annu Rev Nutr 24 33 54 15189112
  180. [196]Franke AA Custer LJ Tanaka Y 1998 Isoflavones in human breast milk and other biological fluids Am J Clin Nutr 68 1466S 1473S 9848518
  181. [197]Messina M Nagata C Wu AH 2006 Estimated Asian adult soy protein and isoflavone intakes Nutr Cancer 55 1 12 16965235
  182. [198]Mortensen A Kulling SE Schwartz H 2009 Analytical and compositional aspects of isoflavones in food and their biological effects Mol Nutr Food Res 53, Suppl 2 S266 S309 19774555
  183. [199]Chun OK Chung SJ Song WO 2007 Estimated dietary flavonoid intake and major food sources of U.S. adults J Nutr 137 1244 1252 17449588
  184. [200]Chun OK Chung SJ Song WO 2009 Urinary isoflavones and their metabolites validate the dietary isoflavone intakes in US adults J Am Diet Assoc 109 245 254 19167951
  185. [201]Horn-Ross PL Barnes S Lee VS 2006 Reliability and validity of an assessment of usual phytoestrogen consumption (United States) Cancer Causes Control 17 85 93 16411057
  186. [205]Thomas JM Lutz SF 2001 Soy protein lowers fat and saturated fat in school lunch beef and pork entrees J Am Diet Assoc 101 461 463 11320954
  187. [207]Setchell KD Brown NM Desai P 2001 Bioavailability of pure isoflavones in healthy humans and analysis of commercial soy isoflavone supplements J Nutr 131 1362S 1375S 11285356
  188. [208]Piotrowska E Jakobkiewicz-Banecka J Wegrzyn G 2009 Different amounts of isoflavones in various commercially available soy extracts in the light of gene expression-targeted isoflavone therapy Phytother Res 24, Suppl 1 S109 113 19610046
  189. [209]Cao Y Calafat AM Doerge DR 2009 Isoflavones in urine, saliva, and blood of infants: data from a pilot study on the estrogenic activity of soy formula J Expo Sci Environ Epidemiol 19 223 234 18665197 PMC2630504
  190. [210]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 7722188
  191. [211]Markiewicz L Garey J Adlercreutz H 1993 In vitro bioassays of non-steroidal phytoestrogens J Steroid Biochem Mol Biol 45 399 405 8499347
  192. [212]Rolwand I Wiseman H Sanders T 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 10798213
  193. [213]Verkasalo PK Appleby PN Allen NE 2001 Soya intake and plasma concentrations of daidzein and genistein: validity of dietary assessment among eighty British women (Oxford arm of the European Prospective Investigation into Cancer and Nutrition) Br J Nutr 86 415 421 11570994
  194. [214]Adlercreutz H Yamada T Wahala K 1999 Maternal and neonatal phytoestrogens in Japanese women during birth Am J Obstet Gynecol 180 737 743 10076156
  195. [215]Winter JSD Hughes IA Reyes FI 1976 Pituitary–gonadal relations in infancy: patterns of serum gonadal steroid concentrations in man from birth to two years of age J Clin Endocrinol Metab 42 679 686 1262442
  196. [216]Setchell KD Zimmer-Nechemias L Cai J 1998 Isoflavone content of infant formulas and the metabolic fate of these phytoestrogens in early life Am J Clin Nutr 68 1453S 9848516

Cited by

Sorted by citations

Authors
Patisaul, H. B.
Affiliations
North Carolina State University (US)
Corresponding author
Patisaul, Heather B.
Venue
Proceedings of the Nutrition Society
Published
2016-07-08
Volume
76
Issue
2
Pages
130-144
ISSN
  • 0029-6651 (ISSN-L)
  • 1475-2719
OpenAlex
W2463686992
Cited by
107
References
13
Citations by year
2026: 9 · 2025: 10 · 2024: 10 · 2023: 11 · 2022: 14 · 2021: 20 · 2020: 11 · 2019: 12 · 2018: 5 · 2017: 3 · 2016: 2
FWCI
1.15
Type
journal article
Language
en
Open access
Locations
  • Proceedings of The Nutrition Society (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • North Carolina State University
  • National Institute of Environmental Health Sciences (R21ES021233)
Topics
  • Health Sciences › Medicine › Pathology and Forensic Medicine › Phytoestrogen effects and research
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
Keywords
endocrine disruption, phytoestrogens, soybean, sexual differentiation, sexual behavior, neuroendocrine development, gut microbiota, bisphenol A
MeSH terms
Bisphenol A Compounds, Animals, Benzhydryl Compounds, Diet, Disease Models, Animal, Humans, Isoflavones, Neurosecretory Systems, Phenols, Reproduction, Sexual Behavior, Sexual Behavior, Animal, Glycine max, Phytoestrogens, Endocrine Disruptors

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review