Skip to main content

Effects of Chemicals on Mammary Gland Development

  • Protocol
  • First Online:
Developmental and Reproductive Toxicology

Part of the book series: Methods in Pharmacology and Toxicology ((MIPT))

Abstract

The mammary gland is exceptionally a complex tissue. It is a sexually dimorphic organ in function, size, response to hormone signaling, and cellular structure. Unlike most organs, the mammary gland has several critical periods of growth and development after birth, and is only fully developed after a full-term pregnancy. Mammary gland development is dependent on complex endocrine signaling as well as paracrine and autocrine signaling between the stroma and parenchyma cells. Even outside of the critical windows of growth and development, the mammary gland is constantly changing with normal hormone fluctuations, most notably during the estrous/menstrual cycle. It is particularly sensitive to endocrine disrupting chemicals (EDCs). An EDC can affect both females and males, resulting in abnormal mammary gland development in adolescents. Later in life, EDCs can influence cancer outcomes. In adult females, alterations in mammary gland development can result in lactational impairment. This chapter describes the stages of development, the key hormone actions, and common EDCs and their effects on the mammary gland.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Brisken C, Park S, Vass T, Lydon JP, O'Malley BW, Weinberg RA (1998) A paracrine role for the epithelial progesterone receptor in mammary gland development. Proc Natl Acad Sci U S A 95(9):5076–5081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Hens JR, Wysolmerski JJ (2005) Key stages of mammary gland development: molecular mechanisms involved in the formation of the embryonic mammary gland. Breast Cancer Res 7(5):220–224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Maller O, Martinson H, Schedin P (2010) Extracellular matrix composition reveals complex and dynamic stromal-epithelial interactions in the mammary gland. J Mammary Gland Biol Neoplasia 15(3):301–318

    Article  PubMed  Google Scholar 

  4. Brisken C, O’Malley B (2010) Hormone action in the mammary gland. Cold Spring Harb Perspect Biol 2(12):a003178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Hennighausen L, Robinson GW (2001) Signaling pathways in mammary gland development. Dev Cell 1(4):467–475

    Article  CAS  PubMed  Google Scholar 

  6. Hovey RC, Trott JF, Vonderhaar BK (2002) Establishing a framework for the functional mammary gland: from endocrinology to morphology. J Mammary Gland Biol Neoplasia 7(1):17–38

    Article  PubMed  Google Scholar 

  7. Howard BA, Gusterson BA (2000) Human breast development. J Mammary Gland Biol Neoplasia 5(2):119–137

    Article  CAS  PubMed  Google Scholar 

  8. Rudel RA, Fenton SE, Ackerman JM, Euling SY, Makris SL (2011) Environmental exposures and mammary gland development: state of the science, public health implications, and research recommendations. Environ Health Perspect 119(8):1053–1061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Howlader N, Noone AM, Krapcho M, Miller D, Bishop K, Altekruse SF, Kosary CL, Yu M, Ruhl J, Tatalovich Z, Mariotto A, Lewis DR, Chen HS, Feuer EJ, Cronin KA (eds) (2016) SEER cancer statistics review, 1975–2013. National Cancer Institute, Bethesda, MD. http://seer.cancer.gov/csr/1975_2013/ (based on November 2015 SEER data submission)

    Google Scholar 

  10. American Cancer Society (ACS) (2016) Cancer facts and figures 2016. American Cancer Society, Atlanta

    Google Scholar 

  11. American Cancer Society (ACS) (2015) Breast cancer facts and figures 2015–2016. American Cancer Society, Inc., Atlanta

    Google Scholar 

  12. IBCERCC (2013) www.niehs.nih.gov/about/boards/ibcercc

  13. Macon MB, Fenton SE (2013) Endocrine disruptors and the breast: early life effects and later life disease. J Mammary Gland Biol Neoplasia 18(1):43–61

    Article  PubMed  PubMed Central  Google Scholar 

  14. Forman MR, Winn DM, Collman GW, Rizzo J, Birnbaum LS (2015) Environmental exposures, breast development and cancer risk: through the looking glass of breast cancer prevention. Reprod Toxicol 54:6–10

    Article  CAS  PubMed  Google Scholar 

  15. Drife JO (1986) Breast development in puberty. Ann N Y Acad Sci 464(1 Endocrinology):58–65

    Article  CAS  PubMed  Google Scholar 

  16. Russo J, Russo IH (2004) Development of the human breast. Maturitas 49(1):2–15

    Article  CAS  PubMed  Google Scholar 

  17. Jolicoeur F (2005) Intrauterine breast development and the mammary myoepithelial lineage. J Mammary Gland Biol Neoplasia 10(3):199–210

    Article  PubMed  Google Scholar 

  18. Robinson GW, Karpf ABC, Kratochwil K (1999) Regulation of mammary gland development by tissue interaction. J Mammary Gland Biol Neoplasia 4(1):9–19

    Article  CAS  PubMed  Google Scholar 

  19. Macias H, Hinck L (2012) Mammary gland development. Wiley Interdiscip Rev Dev Biol 1(4):533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Gusterson BA, Stein T (2012) Human breast development. Semin Cell Dev Biol 23(5):567

    Article  PubMed  Google Scholar 

  21. Hassiotou F, Geddes D (2013) Anatomy of the human mammary gland: current status of knowledge. Clin Anat 26(1):29–48

    Article  PubMed  Google Scholar 

  22. Javed A, Lteif A (2013) Development of the human breast. Semin Plast Surg 27(1):005–012

    Article  Google Scholar 

  23. Alexander JM, Campbell MJ (1997) Prevalence of inverted and non-protractile nipples in antenatal women who intend to breast-feed. Breast 6(2):72–78

    Article  Google Scholar 

  24. Montagna W, Yun JS (1972) The glands of montgomery. Br J Dermatol 86(2):126–133

    Article  CAS  PubMed  Google Scholar 

  25. Anbazhagan R, Bartek J, Monaghan P, Gusterson BA (1991) Growth and development of the human infant breast. Am J Anat 192(4):407–417

    Article  CAS  PubMed  Google Scholar 

  26. Marshall WA, Tanner JM (1969) Variations in pattern of pubertal changes in girls. Arch Dis Child 44(235):291–303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Neville MC, McFadden TB, Forsyth I (2002) Hormonal regulation of mammary differentiation and milk secretion. J Mammary Gland Biol Neoplasia 7(1):49–66

    Article  PubMed  Google Scholar 

  28. Anderson E, Clarke RB (2004) Steroid receptors and cell cycle in normal mammary epithelium. J Mammary Gland Biol Neoplasia 9(1):3–13

    Article  PubMed  Google Scholar 

  29. Visvader JE (2009) Keeping abreast of the mammary epithelial hierarchy and breast tumorigenesis. Genes Dev 23(22):2563–2577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Russo J, Lynch H, Russo IH (2001) Mammary gland architecture as a determining factor in the susceptibility of the human breast to cancer. Breast J 7(5):278–291

    Article  CAS  PubMed  Google Scholar 

  31. Beesley R, Johnson J (2008) Glob. libr. women’s med

    Google Scholar 

  32. Davis B, Fenton S (2013) Mammary gland. In: Haschek WM, Rousseaux CG, Wallig MA (eds) Haschek and Rousseaux’s handbook of toxicologic pathology, vol 3. Elsevier Academic Press, New York, NY, pp 2665–2694

    Chapter  Google Scholar 

  33. Lamote I, Meyer E, Massart-Leën AM, Burvenich C (2004) Sex steroids and growth factors in the regulation of mammary gland proliferation, differentiation, and involution, vol 69. Elsevier Inc., United States

    Google Scholar 

  34. Taylor D, Pearce CL, Hovanessian-Larsen L, Downey S, Spicer DV, Bartow S et al (2009) Progesterone and estrogen receptors in pregnant and premenopausal non-pregnant normal human breast. Breast Cancer Res Treat 118(1):161–168

    Article  CAS  PubMed  Google Scholar 

  35. Russo J, Russo IH (2014) Techniques and methodological approaches in breast cancer research, vol 1. Springer, New York, NY

    Book  Google Scholar 

  36. Cowin P, Wysolmerski J (2010) Molecular mechanisms guiding embryonic mammary gland development. Cold Spring Harb Perspect Biol 2(6):a003251–a003251

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Robinson GW, Hennighausen L (1997) Inhibins and activins regulate mammary epithelial cell differentiation through mesenchymal-epithelial interactions. Development 124(14):2701

    CAS  PubMed  Google Scholar 

  38. Hatsell S, Rowlands T, Hiremath M, Cowin P (2003) β-catenin and tcfs in mammary development and cancer. J Mammary Gland Biol Neoplasia 8(2):145–158

    Article  PubMed  Google Scholar 

  39. Lindvall C, Bu W, Williams BO, Li Y (2007) Wnt signaling, stem cells, and the cellular origin of breast cancer. Stem Cell Rev 3(2):157–168

    Article  CAS  PubMed  Google Scholar 

  40. Osin PP, Anbazhagan R, Bartkova J, Nathan B, Gusterson BA (1998) Breast development gives insights into breast disease. Histopathology 33(3):275–283

    Article  CAS  PubMed  Google Scholar 

  41. Gallego MI, Binart N, Robinson GW, Okagaki R, Coschigano KT, Perry J, Kopchick JJ, Oka T, Kelly PA, Hennighausen L (2001) Prolactin, growth hormone, and epidermal growth factor activate Stat5 in different compartments of mammary tissue and exert different and overlapping developmental effects. Dev Biol 229(1):163–175

    Article  CAS  PubMed  Google Scholar 

  42. Feldman M, Ruan W, Tappin I, Wieczorek R, Kleinberg D (1999) The effect of GH on estrogen receptor expression in the rat mammary gland. J Endocrinol 163(3):515–522

    Article  CAS  PubMed  Google Scholar 

  43. Ciarloni L, Mallepell S, Brisken C (2007) Amphiregulin is an essential mediator of estrogen receptor α function in mammary gland development. Proc Natl Acad Sci U S A 104(13):5455–5460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. McBryan J, Howlin J, Napoletano S, Martin F (2008) Amphiregulin: role in mammary gland development and breast cancer. J Mammary Gland Biol Neoplasia 13(2):159–169

    Article  PubMed  Google Scholar 

  45. Obr AE, Edwards DP (2012) The biology of progesterone receptor in the normal mammary gland and in breast cancer. Mol Cell Endocrinol 357(1–2):4–17

    Article  CAS  PubMed  Google Scholar 

  46. Aupperlee MD, Leipprandt JR, Bennett JM, Schwartz RC, Haslam SZ (2013) Amphiregulin mediates progesterone-induced mammary ductal development during puberty. Breast Cancer Res 15(3):R44

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Beleut M, Rajaram RD, Caikovski M, Ayyanan A, Germano D, Choi Y et al (2010) Two distinct mechanisms underlie progesterone-induced proliferation in the mammary gland. Proc Natl Acad Sci U S A 107(7):2989–2994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Forsyth IA, Wallis M (2002) Growth hormone and prolactin – molecular and functional evolution. J Mammary Gland Biol Neoplasia 7(3):291–312

    Article  PubMed  Google Scholar 

  49. Monks J (2007) TGFβ as a potential mediator of progesterone action in the mammary gland of pregnancy. J Mammary Gland Biol Neoplasia 12(4):249–257

    Article  PubMed  Google Scholar 

  50. Navarrete MAH, Maier CM, Falzoni R, de Azevedo Quadros LG, Lima GR, Baracat EC, Nazário ACP (2005) Assessment of the proliferative, apoptotic and cellular renovation indices of the human mammary epithelium during the follicular and luteal phases of the menstrual cycle. Breast Cancer Res 7(3):R306–R313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Oakes SR, Rogers RL, Naylor MJ, Ormandy CJ (2008) Prolactin regulation of mammary gland development. J Mammary Gland Biol Neoplasia 13(1):13–28

    Article  PubMed  Google Scholar 

  52. Harris J, Stanford PM, Sutherland K, Oakes SR, Naylor MJ, Robertson FG, Blazek KD, Kazlauskas M, Hilton HN, Wittlin S, Alexander WS, Lindeman GJ, Visvader JE, Ormandy CJ (2006) Socs2 and Elf5 mediate prolactin-induced mammary gland development. Mol Endocrinol 20(5):1177–1187

    Article  CAS  PubMed  Google Scholar 

  53. Knight CH, Peaker M, Wilde CJ (1998) Local control of mammary development and function. Rev Reprod 3(2):104–112. doi:10.1530/revreprod/3.2.104

    Article  CAS  PubMed  Google Scholar 

  54. Allan GJ, Beattie J, Flint DJ (2004) The role of IGFBP-5 in mammary gland development and involution. Domest Anim Endocrinol 27(3):257–266

    Article  CAS  PubMed  Google Scholar 

  55. Baxter FO, Neoh K, Tevendale MC (2007) The beginning of the end: death signaling in early involution. J Mammary Gland Biol Neoplasia 12(1):3–13

    Article  PubMed  Google Scholar 

  56. Sutherland KD, Lindeman GJ, Visvader JE (2007) The molecular culprits underlying precocious mammary gland involution. J Mammary Gland Biol Neoplasia 12(1):15–23

    Article  PubMed  Google Scholar 

  57. Barash I (2006) Stat5 in the mammary gland: controlling normal development and cancer. J Cell Physiol 209(2):305–313

    Article  CAS  PubMed  Google Scholar 

  58. Watson C (2006) Key stages in mammary gland development – involution: apoptosis and tissue remodelling that convert the mammary gland from milk factory to a quiescent organ. Breast Cancer Res 8(2):203

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Furth PA (1999) Mammary gland involution and apoptosis of mammary epithelial cells. J Mammary Gland Biol Neoplasia 4(2):123–127

    Article  CAS  PubMed  Google Scholar 

  60. Zinser GM, Welsh J (2004) Accelerated mammary gland development during pregnancy and delayed postlactational involution in vitamin D3 receptor null mice. Mol Endocrinol 18(9):2208–2223

    Article  CAS  PubMed  Google Scholar 

  61. Tonner E, Allan G, Flint D (2000) Hormonal control of plasmin and tissue-type plasminogen activator activity in rat milk during involution of the mammary gland. J Endocrinol 167(2):265–273

    Article  CAS  PubMed  Google Scholar 

  62. Hughes K, Wickenden JA, Allen JE, Watson CJ (2012) Conditional deletion of Stat3 in mammary epithelium impairs the acute phase response and modulates immune cell numbers during post-lactational regression. J Pathol 227(1):106–117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Mandrup KR, Hass U, Christiansen S, Boberg J (2012) Perinatal ethinyl oestradiol alters mammary gland development in male and female Wistar rats. Int J Androl 35(3):385–396

    Article  CAS  PubMed  Google Scholar 

  64. de Assis S, Warri AM, Cruz I, Laja O, Tian Y, Zhang B, Wang Y, Huang TH, Hilakivi-Clarke L (2012) High-fat or ethinyl-oestradiol intake during pregnancy increases mammary cancer risk in several generations of offspring. Nat Commun 3:1053

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. Wingo PA, Lee NC, Ory HW, Beral V, Peterson HB, Rhodes P (1993) Age-specific differences in the relationship between oral contraceptive use and breast cancer. Cancer 71(S4):1506–1517

    Article  CAS  PubMed  Google Scholar 

  66. Hilakivi-Clarke L, Wärri A, Bouker KB, Zhang X, Cook KL, Jin L, Zwart A, Nguyen N, Hu R, Cruz MI, de Assis S, Wang X, Xuan J, Wang Y, Wehrenberg B, Clarke R (2017) Effects of in utero exposure to ethinyl estradiol on tamoxifen resistance and breast cancer recurrence in a preclinical model. J Natl Cancer Inst 109(1.) p.djw188

    Google Scholar 

  67. American Cancer Society (ACS) (2015) Menopausal hormone therapy and cancer risk. American Cancer Society, Inc., Atlanta

    Google Scholar 

  68. NTP National Toxicology Program (2011) Diethylstilbestrol. 12th Report on Carcinogens 12:159–161

    Google Scholar 

  69. IARC (2012) Diethylstilbestrol. A review of human carcinogens. IARC Monogr Eval Carcinog Risks Hum 100A:175–218

    Google Scholar 

  70. 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(2):134

    Article  CAS  PubMed  Google Scholar 

  71. Palmer JR, Wise LA, Hatch EE, Troisi R, Titus-Ernstoff L, Strohsnitter W, Kaufman R, Herbst AL, Noller KL, Hyer M, Hoover RN (2006) Prenatal diethylstilbestrol exposure and risk of breast cancer. Cancer Epidemiol Biomarkers Prev 15(8):1509–1514

    Article  CAS  PubMed  Google Scholar 

  72. Hovey RC, Asai-Sato M, Warri A, Terry-Koroma B, Colyn N, Ginsburg E, Vonderhaar BK (2005) Effects of neonatal exposure to diethylstilbestrol, tamoxifen, and toremifene on the BALB/c mouse mammary gland. Biol Reprod 72(2):423–435

    Article  CAS  PubMed  Google Scholar 

  73. NTP National Toxicology Program (2008) Toxicology and carcinogenesis studies of genistein (cas no. 446-72-0) in Sprague-Dawley rats (feed study). National Toxicology Program Technical Report Series, vol (545), p 1

    Google Scholar 

  74. Strom BL, Schinnar R, Ziegler EE, Barnhart KT, Sammel MD, Macones GA, Stallings VA, Drulis JM, Nelson SE, Hanson SA (2001) Exposure to soy-based formula in infancy and endocrinological and reproductive outcomes in young adulthood. JAMA 286(7):807–814

    Article  CAS  PubMed  Google Scholar 

  75. Spagnuolo C, Russo GL, Orhan IE, Habtemariam S, Daglia M, Sureda A, Nabavi SF, Devi KP, Loizzo MR, Tundis R, Nabavi SM (2015) Genistein and cancer: current status, challenges, and future directions. Adv Nutr 6(4):408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Lamartiniere CA, Zhang JX, Cotroneo MS (1998) Genistein studies in rats: potential for breast cancer prevention and reproductive and developmental toxicity. American Society for Clinical Nutrition, Inc., United States

    Google Scholar 

  77. Hilakivi-Clarke L, Onojafe I, Raygada M, Cho E, Skaar T, Russo I, Clarke R (1999) Prepubertal exposure to zearalenone or genistein reduces mammary tumorigenesis. Br J Cancer 80(11):1682–1688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Delclos KB, Bucci TJ, Lomax LG, Latendresse JR, Warbritton A, Weis CC, Newbold RR (2001) Effects of dietary genistein exposure during development on male and female CD (Sprague-Dawley) rats. Reprod Toxicol 15(6):647–663

    Article  CAS  PubMed  Google Scholar 

  79. Cabanes A, Wang M, Olivo S, DeAssis S, Gustafsson J, Khan G, Hilakivi-Clarke L (2004) Prepubertal estradiol and genistein exposures up-regulate BRCA1 mRNA and reduce mammary tumorigenesis. Carcinogenesis 25(5):741–748

    Article  CAS  PubMed  Google Scholar 

  80. Caëtano B, Le Corre L, Chalabi N, Delort L, Bignon Y, Bernard-Gallon DJ (2006) Soya phytonutrients act on a panel of genes implicated with BRCA1 and BRCA2 oncosuppressors in human breast cell lines. Br J Nutr 95(2):406

    Article  PubMed  CAS  Google Scholar 

  81. Hilakivi-Clarke L, Cho E, Clarke R (1998) Maternal genistein exposure mimics the effects of estrogen on mammary gland development in female mouse offspring. Oncol Rep 5(3):609–616

    CAS  PubMed  Google Scholar 

  82. Hilakivi-Clarke L, Cho E, Cabanes A, DeAssis S, Olivo S, Helferich W, Lippman MC, Clarke R (2002) Dietary modulation of pregnancy estrogen levels and breast cancer risk among female rat offspring. Clin Cancer Res 8(11):3601–3610

    CAS  PubMed  Google Scholar 

  83. Foster WG, Younglai EV, Boutross-Tadross O, Hughes CL, Wade MG (2004) Mammary gland morphology in Sprague-Dawley rats following treatment with an organochlorine mixture in utero and neonatal genistein. Toxicol Sci 77(1):91–100

    Article  CAS  PubMed  Google Scholar 

  84. Latendresse JR, Bucci TJ, Olson G, Mellick P, Weis CC, Thorn B, Newbold RR, Delclos KB (2009) Genistein and ethinyl estradiol dietary exposure in multigenerational and chronic studies induce similar proliferative lesions in mammary gland of male Sprague–Dawley rats. Reprod Toxicol 28(3):342–353

    Article  CAS  PubMed  Google Scholar 

  85. vom Saal FS, Nagel SC, Coe BL, Angle BM, Taylor JA (2012) The estrogenic endocrine disrupting chemical bisphenol A (BPA) and obesity. Mol Cell Endocrinol 354(1–2):74–84

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Voelkel W, Colnot T, Csanady G, Filser J, Dekant W (2002) Metabolism and kinetics of bisphenol A in humans at low doses following oral administration. Chem Res Toxicol 15(10):1281–1287

    Article  CAS  Google Scholar 

  87. Durando M, Kass L, Piva J, Sonnenschein C, Soto AM, Luque EH, Muñoz-de-Toro M (2007) Prenatal bisphenol A exposure induces preneoplastic lesions in the mammary gland in Wistar rats. Environ Health Perspect 115(1):80–86

    Article  CAS  PubMed  Google Scholar 

  88. Markey CM, Luque EH, de Toro MM, Sonnenschein C, Soto AM (2001) In utero exposure to bisphenol A alters the development and tissue organization of the mouse mammary gland. Biol Reprod 65(4):1215–1223

    Article  CAS  PubMed  Google Scholar 

  89. Muñoz-de-Toro M, Markey CM, Wadia PR, Luque EH, Rubin BS, Sonnenschein C, Soto AM (2005) Perinatal exposure to bisphenol-A alters peripubertal mammary gland development in mice. Endocrinology 146(9):4138–4147

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  90. Murray TJ, Maffini MV, Ucci AA, Sonnenschein C, Soto AM (2007) Induction of mammary gland ductal hyperplasias and carcinoma in situ following fetal bisphenol A exposure. Reprod Toxicol 23(3):383–390

    Article  CAS  PubMed  Google Scholar 

  91. Vandenberg LN, Maffini MV, Schaeberle CM, Ucci AA, Sonnenschein C, Rubin BS, Soto AM (2008) Perinatal exposure to the xenoestrogen bisphenol-A induces mammary intraductal hyperplasias in adult CD-1 mice. Reprod Toxicol 26(3):210–219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Shelby MD (2008) NTP-CERHR monograph on the potential human reproductive and developmental effects of bisphenol A. NTP CERHR MON (22):v-v

    Google Scholar 

  93. Acevedo N, Davis B, Schaeberle CM, Sonnenschein C, Soto AM (2013) Perinatally administered bisphenol a as a potential mammary gland carcinogen in rats. Environ Health Perspect 121(9):1040–1046

    PubMed  PubMed Central  Google Scholar 

  94. Mandrup K, Boberg J, Isling LK, Christiansen S, Hass U (2016) Low-dose effects of bisphenol A on mammary gland development in rats. Andrology 4(4):673–683

    Article  CAS  PubMed  Google Scholar 

  95. NTP National Toxicology Program (2008) NTP-CERHR monograph on the potential human reproductive and developmental effects of bisphenol A. RTP, NC 27709

    Google Scholar 

  96. FDA (2016) Bisphenol A (BPA): use in food contact application. http://www.fda.gov/newsevents/publichealthfocus/ucm064437.htm

  97. EFSA. European Food Safety Authority (2015) Scientific opinion on bisphenol A (2015). https://www.efsa.europa.eu/sites/default/files/corporate_publications/files/factsheetbpa150121.pdf

  98. Vandenberg LN, Prins GS (2016) Clarity in the face of confusion: new studies tip the scales on bisphenol A(BPA). Andrology 4:561–564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Bhargava HN, Leonard PA (1996) Triclosan: applications and safety. Am J Infect Control 24:209–218

    Article  CAS  PubMed  Google Scholar 

  100. Halden RU, Paull DH (2005) Co-occurrence of triclocarban and triclosan in U.S. water resources. Environ Sci Technol 39(6):1420–1426

    Article  CAS  PubMed  Google Scholar 

  101. Sandborgh-Englund G, Adolfsson-Erici M, Odham G, Ekstrand J (2006) Pharmacokinetics of triclosan following oral ingestion in humans. J Toxicol Environ Health A 69:1861–1873

    Article  CAS  PubMed  Google Scholar 

  102. Adolfsson-Erici M, Pettersson M, Parkkonen J, Sturve J (2002) Triclosan, a commonly used bactericide found in human milk and in the aquatic environment in Sweden. Chemosphere 46:1485–1489

    Article  CAS  PubMed  Google Scholar 

  103. Calafat XY, Wong L, Reidy JA, Needham LL (2008) Urinary concentrations of triclosan in the U.S. population: 2003–2004 Antonia M. Environ Health Perspect 116(3):303–307

    Article  CAS  PubMed  Google Scholar 

  104. Allmyr M, Adolfsson-Erici M, McLachlan MS, Sandborgh Englund G (2006) Triclosan in plasma and milk from Swedish nursing mothers and their exposure via personal care products. Sci Total Environ 372:87–93

    Article  CAS  PubMed  Google Scholar 

  105. Crofton KM, Paul KB, Devito MJ, Hedge JM (2007) Short-term in vivo exposure to the water contaminant triclosan: evidence for disruption of thyroxine. Environ Toxicol Pharmacol 24(2):194–197

    Article  CAS  PubMed  Google Scholar 

  106. Gee RH, Charles A, Taylor N, Darbre PD (2008) Oestrogenic and androgenic activity of triclosan in breast cancer cells. J Appl Toxicol 28:78–91

    Article  CAS  PubMed  Google Scholar 

  107. Stoker TE, Gibson EK, Zorrilla LM (2010) Triclosan exposure modulates estrogen-dependent responses in the female Wistar rat. Toxicol Sci 117(1):45–53

    Article  CAS  PubMed  Google Scholar 

  108. Darbre PD, Charles AK (2010) Environmental oestrogens and breast cancer: evidence for combined involvement of dietary, household and cosmetic xenoestrogens. Anticancer Res 30(3):815

    CAS  PubMed  Google Scholar 

  109. Dinwiddie MT, Terry PD, Chen J (2014) Recent evidence regarding triclosan and cancer risk. Int J Environ Res Public Health 11(2):2209–2209

    Article  PubMed  PubMed Central  Google Scholar 

  110. http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm378542.htm

  111. http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm517478.htm

  112. US EPA (2000) Reregistration eligibility decision (RED) vinclozolin. Office of Prevention, Pesticides and Toxic Substances. US Environmental Protection Agency

    Google Scholar 

  113. Kelce WR, Monosson E, Gamcsik MP, Laws SC, Gray LEJ (1994) Environmental hormone disruptors: evidence that vinclozolin developmental toxicity is mediated by antiandrogenic metabolites. Toxicol Appl Pharmacol 126:276–285

    Article  CAS  PubMed  Google Scholar 

  114. Monosson E, Kelce WR, Lambright C, Ostby J, Gray LE Jr (1999) Peripubertal exposure to the antiandrogenic fungicide, vinclozolin, delays puberty, inhibits the development of androgen-dependent tissues, and alters androgen receptor function in the male rat. Toxicol Ind Health 15:65–79

    Article  CAS  PubMed  Google Scholar 

  115. Gray LE Jr, Ostby J, Furr J, Wolf CJ, Lambright C, Parks L, Veeramachaneni DN, Wilson V, Price M, Hotchkiss A, Orlando E, Guillette L (2001) Effects of environmental antiandrogens on reproductive development in experimental animals. Hum Reprod 7:248–264

    Article  CAS  Google Scholar 

  116. Christiansen S, Scholze M, Dalgaard M, Vinggaard AM, Axelstad M, Kortenkamp A, Hass U (2009) Synergistic disruption of external male sex organ development by a mixture of four antiandrogens. Environ Health Perspect 117:1839–1846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Yeh S, Hu YC, Wang P, Xie C, Xu Q, Tsai M, Dong Z, Wang R, Lee T, Chang C (2003) Abnormal mammary gland development and growth retardation in female mice and MCF7 breast cancer cells lacking androgen receptor. J Exp Med 198:1899–1908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Irigaray P, Newby JA, Clapp R, Hardell L, Howard V, Montagnier L, Epstein S, Belpomme D (2007) Lifestyle-related factors and environmental agents causing cancer: an overview. Biomed Pharmacother 61:640–658

    Article  CAS  PubMed  Google Scholar 

  119. Guerrero-Bosagna C, Settles M, Lucker BJ, Skinner MK (2010) Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome. PLoS One 5:e13100

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  120. Anway MD, Cupp AS, Uzumcu M, Skinner MK (2005) Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308:1466–1469

    Article  CAS  PubMed  Google Scholar 

  121. Anway MD, Leathers C, Skinner MK (2006) Endocrine disruptor vinclozolin induced epigenetic transgenerational adult-onset disease. Endocrinology 147(12):5515–5523

    Article  CAS  PubMed  Google Scholar 

  122. El Sheikh Saad H, Meduri G, Phrakonkham P, Bergès R, Vacher S, Djallali M, Auger J, Canivenc-Lavier MC, Perrot-Applanat M (2011) Abnormal peripubertal development of the rat mammary gland following exposure in utero and during lactation to a mixture of genistein and the food contaminant vinclozolin. Reprod Toxicol 32(1):15–25

    Article  PubMed  CAS  Google Scholar 

  123. El Sheikh Saad H, Toullec A, Vacher S, Pocard M, Bieche I, Perrot-Applanat M (2013) In utero and lactational exposure to vinclozolin and genistein induces genomic changes in the rat mammary gland. J Endocrinol 216(2):245–263

    Article  PubMed  CAS  Google Scholar 

  124. Knower KC, To, S. Q, Leung YK, Ho SM, Clyne CD (2014) Endocrine disruption of the epigenome: a breast cancer link. Endocr Relat Cancer 21:T33–T55

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Rudel RA, Ackerman JM, Attfield KR, Brody JG (2014) New exposure biomarkers as tools for breast cancer epidemiology, biomonitoring, and prevention: a systematic approach based on animal evidence. National Institute of Environmental Health Sciences, United States

    Google Scholar 

  126. Emond C, DeVito M, Warner M, Eskenazi B, Mocarelli P, Birnbaum LS (2016) An assessment of dioxin exposure across gestation and lactation using a PBPK model and new data from seveso. Environ Int 92–93:23–32

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  127. Bruner-Tran KL, Gnecco J, Ding T, Glore DR, Pensabene V, Osteen KG (2016) Exposure to the environmental endocrine disruptor TCDD and human reproductive dysfunction: translating lessons from murine models. Reprod Toxicol 68:59–71

    Article  PubMed  CAS  Google Scholar 

  128. Safe SH (1995) Modulation of gene expression and endocrine response pathways by 2,3,7,8-tetrachlorodibenzo-p-dioxin and related compounds. Pharmacol Ther 67(2):247–281

    Article  CAS  PubMed  Google Scholar 

  129. Rogers JM, Denison MS (2002) Analysis of the antiestrogenic activity of 2,3,7,8-tetrachlorodibenzo-p-dioxin in human ovarian carcinoma BG-1 cells. Mol Pharmacol 61(6):1393–1403

    Article  CAS  PubMed  Google Scholar 

  130. Brown N, Manzolillo P, Zhang J, Wang J, Lamartiniere C (1998) Prenatal TCDD and predisposition to mammary cancer in the rat. Carcinogenesis 19(9):1623–1629

    Article  CAS  PubMed  Google Scholar 

  131. Fenton S, Hamm J, Birnbaum L, Youngblood G (2002) Persistent abnormalities in the rat mammary gland following gestational and lactational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Toxicol Sci 67(1):63–74

    Article  CAS  PubMed  Google Scholar 

  132. Vorderstrasse BA, Fenton SE, Bohn AA, Cundiff JA, Lawrence B (2004) A novel effect of dioxin: exposure during pregnancy severely impairs mammary gland differentiation. Toxicol Sci 78(2):248–257

    Article  CAS  PubMed  Google Scholar 

  133. Lew BJ, Collins LL, O’Reilly MA, Lawrence BP (2009) Activation of the aryl hydrocarbon receptor during different critical windows in pregnancy alters mammary epithelial cell proliferation and differentiation. Toxicol Sci 111(1):151–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Warner M, Mocarelli P, Samuels S, Needham L, Brambilla P, Eskenazi B (2011) Dioxin exposure and cancer risk in the seveso women’s health study. Environ Health Perspect 119(12):1700–1705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Warner M, Eskenazi B, Mocarelli P, Gerthoux PM, Samuels S, Needham L, Patterson D, Brambilla P (2002) Serum dioxin concentrations and breast cancer risk in the seveso women’s health study. Environ Health Perspect 110(7):625–628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Leijs MM, Koppe JG, Olie K, Aalderen WMC v, Voogt P d, Vulsma T, Westra M, ten Tusscher GW (2008) Delayed initiation of breast development in girls with higher prenatal dioxin exposure; a longitudinal cohort study. Chemosphere 73(6):999–1004

    Article  CAS  PubMed  Google Scholar 

  137. Pup LD, Mantovani A, Cavaliere C, Facchini G, Luce A, Sperlongano P, Caraglia M, Berretta M (2016) Carcinogenetic mechanisms of endocrine disruptors in female cancers (review). Oncol Rep 36(2):603–612

    PubMed  PubMed Central  Google Scholar 

  138. IARC (1993) Monographs on the Evaluation of the carcinogenic risk of chemicals to humans. Beryllium, cadmium, mercury, and exposures in the glass manufacturing industry. International Agency for Research on Cancer, Lyon, France

    Google Scholar 

  139. Garcia-Morales P, Saceda M, Kenney N, Kim N, Salomon DS, Gottardis MM, Solomon HB, Sholler PF, Jordan VC, Martin MB (1994) Effect of cadmium on estrogen receptor levels and estrogen-induced responses in human breast cancer cells. J Biol Chem 269(24):16896

    CAS  PubMed  Google Scholar 

  140. Martin MB, Reiter R, Trock B, Paik S, Lirio AA, Kenney N, Stoica A, Foss C, Chepko G, Singh B, Hilakivi-Clarke L, Clarke R, Sholler PF, Johnson MD (2003) Cadmium mimics the in vivo effects of estrogen in the uterus and mammary gland. Nat Med 9(8):1081–1084

    Article  PubMed  CAS  Google Scholar 

  141. Davis J, Khan G, Martin MB, Hilakivi-Clarke L (2013) Effects of maternal dietary exposure to cadmium during pregnancy on mammary cancer risk among female offspring. J Carcinog 12(1):11–11

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  142. Öhrvik H, Yoshioka M, Oskarsson A, Tallkvist J, Sveriges lantbruksuniversitet (2006) Cadmium-induced disturbances in lactating mammary glands of mice. Toxicol Lett 164(3):207–213

    Article  PubMed  CAS  Google Scholar 

  143. Fenga C (2016) Occupational exposure and risk of breast cancer. Biomed Rep 4(3):282–292

    PubMed  PubMed Central  Google Scholar 

  144. Lin J, Zhang F, Lei Y (2016) Dietary intake and urinary level of cadmium and breast cancer risk: a meta-analysis. Cancer Epidemiol 42:101–107

    Article  PubMed  Google Scholar 

  145. Filgo AJ, Quist EM, Hoenerhoff MJ, Brix AE, Kissling GE, Fenton SE (2015) Perfluorooctanoic acid (PFOA)–induced liver lesions in two strains of mice following developmental exposures: PPARα is not required. Toxicol Pathol 43(4):558–568

    Article  CAS  PubMed  Google Scholar 

  146. Olsen GW, Burris JM, Ehresman DJ, Froehlich JW, Seacat AM, Butenhoff JL, Zobel LR (2007) Half-life of serum elimination of perfluorooctanesulfonate, perfluorohexanesulfonate, and perfluorooctanoate in retired fluorochemical production workers. Environ Health Perspect 115(9):1298–1305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Lau C (2012) Perfluorinated compounds. Springer Basel, Basel, pp 47–86

    Google Scholar 

  148. Yang C, Tan YS, Harkema JR, Haslam SZ (2009) Differential effects of peripubertal exposure to perfluorooctanoic acid on mammary gland development in C57Bl/6 and Balb/c mouse strains. Reprod Toxicol 27(3):299–306

    Article  CAS  PubMed  Google Scholar 

  149. Macon MB, Villanueva LR, Tatum-Gibbs K, Zehr RD, Strynar MJ, Stanko JP, White SS, Helfant L, Fenton SE (2011) Prenatal perfluorooctanoic acid exposure in CD-1 mice: low-dose developmental effects and internal dosimetry. Toxicol Sci 122(1):134–145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. White SS, Stanko JP, Kato K, Calafat AM, Hines EP, Fenton SE (2011) Gestational and chronic low-dose PFOA exposures and mammary gland growth and differentiation in three generations of CD-1 mice. Environ Health Perspect 119(8):1070–1076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Tucker DK, Macon MB, Strynar MJ, Dagnino S, Andersen E, Fenton SE (2015) The mammary gland is a sensitive pubertal target in CD-1 and C57Bl/6 mice following perinatal perfluorooctanoic acid (PFOA) exposure. Reprodu Toxicol 54:26–36

    Article  CAS  Google Scholar 

  152. Zhao Y, Tan YS, Haslam SZ, Yang C (2010) Perfluorooctanoic acid effects on steroid hormone and growth factor levels mediate stimulation of peripubertal mammary gland development in C57BL/6 mice. Toxicol Sci 115(1):214–224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Bonefeld-Jorgensen EC, Long M, Bossi R, Ayotte P, Asmund G, Krüger T, Ghisari M, Mulvad G, Kern P, Nzulumiki P, Dewailly E (2011) Perfluorinated compounds are related to breast cancer risk in greenlandic inuit: a case control study. Environ Health 10(1):88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. US EPA (2016) Drinking water health advisory for perfluorooctanoic acid (PFOA). Office of Water. US Environmental Protection Agency

    Google Scholar 

  155. IARC (2016) Monograph on the evaluation of carcinogenic risk to humans: some chemicals used as solvents and in polymer manufacture. International Agency for Research on Cancer, Lyon, France

    Google Scholar 

  156. IARC (1999) Monograph on the evaluation of carcinogenic risk to humans: occupational exposure in insecticide application and some Pesticides. International Agency for Research on Cancer, Lyon, France

    Google Scholar 

  157. Cooper RL, Laws SC, Das PC, Narotsky MG, Goldman JM, Tyrey EL, Stoker TE (2007) Atrazine and reproductive function: mode and mechanism of action studies. Birth Defects Res B Dev Reprod Toxicol 80(2):98–112

    Article  CAS  PubMed  Google Scholar 

  158. Rayner JL, Wood C, Fenton SE (2004) Exposure parameters necessary for delayed puberty and mammary gland development in Long–Evans rats exposed in utero to atrazine. Toxicol Appl Pharmacol 195(1):23–34

    Article  CAS  PubMed  Google Scholar 

  159. Rayner JL, Enoch RR, Fenton SE (2005) Adverse effects of prenatal exposure to atrazine during a critical period of mammary gland growth. Toxicol Sci 87(1):255–266

    Article  CAS  PubMed  Google Scholar 

  160. Wetzel L, Luempert LI, Breckenridge C, Tisdel M, Stevens J, Thakur A, Extrom P, Eldridge J (1994) Chronic effects of atrazine on estrus and mammary tumor formation in female Sprague-Dawley and Fischer 344 rats. J Toxicol Environ Health 43(2):169–182

    Article  CAS  PubMed  Google Scholar 

  161. Wirbisky SE, Freeman JL (2015) Atrazine exposure and reproductive dysfunction through the hypothalamus-pituitary-gonadal (HPG) axis. Toxics 3(4):414–450

    Article  PubMed  PubMed Central  Google Scholar 

  162. US EPA (2003) Memorandum. Review of atrazine cancer epidemiology, DP Barcode D2950200, chemical #080803. Office of Prevention, Pesticides and Toxic Substances. US Environmental Protection Agency

    Google Scholar 

  163. Rayner JL, Fenton SE (2011) Atrazine: an environmental endocrine disruptor that alters mammary gland development and tumor susceptibility. Springer New York, New York, NY, pp 167–183

    Google Scholar 

  164. Knudson AG (1996) Hereditary cancer: two hits revisited. J Cancer Res Clin Oncol 122(3):135–140

    Article  CAS  PubMed  Google Scholar 

  165. NTP (National Toxicology Program) (2016) Report on carcinogens, 14th edn. U.S. Department of Health and Human Services, Public Health Service, Research Triangle Park, NC. http://ntp.niehs.nih.gov/go/roc14/

    Google Scholar 

  166. Nguyen D, Oketch-Rabah H, Illa-Bochaca I, Geyer F, Reis-Filho J, Mao J, Ravani S, Zavadil J, Borowsky A, Jerry D, Dunphy K, Seo J, Haslam S, Medina D, Barcellos-Hoff M (2011) Radiation acts on the microenvironment to affect breast carcinogenesis by distinct mechanisms that decrease cancer latency and affect tumor type. Cancer Cell 19(5):640–651

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Osborne G, Rudel R, Schwarzman M (2015) Evaluating chemical effects on mammary gland development: a critical need in disease prevention. Reprod Toxicol 54:148–155

    Article  CAS  PubMed  Google Scholar 

  168. Vandenberg LN, Schaeberleb CM, Rubinb BS, Sonnenscheinb C, Soto AM (2013) The male mammary gland: a target for the xenoestrogen bisphenol A. Reprod Toxicol 37:15–23

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Diamanti-Kandarakis E, Jean-Pierre Bourguignon J-E, Gore AC (2009) Endocrine-disrupting chemicals: an endocrine society scientific statement. Endocr Rev 30(4):293–342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Pinter A, Torok G, Borzsonyi M, Surjan A, Calk M, Kelecsenvi Z, Kocsis Z (1990) Long-term carcinogenicity bioassay of the herbicide atrazine in F344 rats. Neoplasma 37(5):533–544

    CAS  PubMed  Google Scholar 

  171. Brown NM, Lamartiniere CA (1995) Xenoestrogens alter mammary gland differentiation and cell proliferation in the rat. Environ Health Perspect 103:708–713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Jenkins S, Rowell C, Wang J, Lamartiniere CA (2007) Prenatal TCDD exposure predisposes for mammary cancer in rats. Reprod Toxicol 23:391–396

    Article  CAS  PubMed  Google Scholar 

  173. Radisky DC, Hartmann LC (2009) Mammary involution and breast cancer risk: transgenic models and clinical studies. J Mammary Gland Biol Neoplasia 14:181–191

    Article  PubMed  PubMed Central  Google Scholar 

  174. Simpkins JW, Swenberg JA, Weiss N, Brusick D, Eldridge JC, Stevens JT, Handa RJ, Hovey RC, Plant TM, Pastoor TP, Breckenridge CB (2011) Atrazine and breast cancer: a framework assessment of the toxicological and epidemiological evidence. Toxicol Sci 123(2):441–459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. IARC (International Agency for Research on Cancer) (1997) Polychlorinated dibenzo-para-dioxins and polychlorinated dibenzofurans. IARC Monogr Eval Carcinog Risks Hum 69

    Google Scholar 

  176. Steenland K, Bertazzi P, Baccarelli A, Kogevinas M (2004) Dioxin revisited: developments since the 1997 IARC classification of dioxin as a human carcinogen. Environ Health Perspect 112(13):1265–1268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Boffetta P, Mundt KA, Adami HO, Cole P, Mandel JS (2011) TCDD and cancer: a critical review of epidemiologic studies. Crit Rev Toxicol 41(7):622–636. (review)

    Article  PubMed  PubMed Central  Google Scholar 

  178. Herbst AL, Ulfelder H, Poskanzer DC (1971) Adenocarcinoma of the vagina: Association of Maternal Stilbestrol Therapy with tumor appearance in young women. N Engl J Med 284(16):878–881

    Article  CAS  PubMed  Google Scholar 

  179. Bromer JG, Zhou Y, Taylor MB, Doherty L, Taylor HS (2010) Bisphenol-A exposure in utero leads to epigenetic alterations in the developmental programming of uterine estrogen response. FASEB J 24(7):2273–2280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Bromer JG, Wu J, Zhou Y, Taylor HS (2009) Hypermethylation of homeobox A10 by in utero diethylstilbestrol exposure: an epigenetic mechanism for altered developmental programming. Endocrinology 150(7):3376–3382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  181. Haynes BA, Mookadam F (2009) Male gynecomastia. Mayo Clin Proc 84(8):672–672

    Article  PubMed  PubMed Central  Google Scholar 

  182. Felner EL, White PC (2000) Prepubertal gynecomastia: indirect exposure to estrogen cream. Pediatrics 105(4):e55–E55

    Article  CAS  PubMed  Google Scholar 

  183. Henley DV, Lipson N, Korach KS, Bloch CA (2007) Prepubertal gynecomastia linked to lavender and tea tree oils. N Engl J Med 356(5):479–485

    Article  CAS  PubMed  Google Scholar 

  184. Thayer KA, Foster PM (2007) Workgroup Report: National Toxicology Program Workshop on hormonally induced reproductive tumors: relevance of rodent bioassays. Environ Health Perspect 115(9):1351–1356

    Article  PubMed  PubMed Central  Google Scholar 

  185. Rudel RA, Attfield KR, Schifano JN, Brody JG (2007) Chemicals causing mammary gland tumors in animals signal new directions for epidemiology, chemicals testing, and risk assessment for breast cancer prevention. Cancer 109:2635–2666

    Article  CAS  PubMed  Google Scholar 

  186. Cohn BA, Wolff MS, Cirillo PM, Sholtz RI (2007) DDT and breast cancer in young women: new data on the significance of age at exposure. Environ Health Perspect 115(10):1406–1414

    CAS  PubMed  PubMed Central  Google Scholar 

  187. Ly D, Forman D, Ferlay J, Brinton LA, Cook MB (2013) An international comparison of male and female breast cancer incidence rates. Int J Cancer 132(8):1918–1926

    Article  CAS  PubMed  Google Scholar 

  188. Skinner MK (2007) Endocrine disruptors and epigenetic transgenerational disease etiology. Pediatr Res 61:48R–50R

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Adam J. Filgo .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer Science+Business Media New York

About this protocol

Cite this protocol

Filgo, A.J., Faqi, A.S. (2017). Effects of Chemicals on Mammary Gland Development. In: Faqi, A. (eds) Developmental and Reproductive Toxicology. Methods in Pharmacology and Toxicology. Humana Press, New York, NY. https://doi.org/10.1007/7653_2017_69

Download citation

  • DOI: https://doi.org/10.1007/7653_2017_69

  • Published:

  • Publisher Name: Humana Press, New York, NY

  • Print ISBN: 978-1-4939-7206-7

  • Online ISBN: 978-1-4939-7208-1

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics