Disruption of blastocyst implantation by triclosan in mice: Impacts of repeated and acute doses and combination with bisphenol-A

Reproductive Toxicology

Volumn 34, Issue 4, 2012, Pages 607-613

  Crawford, Brent R ^a   deCatanzaro, Denys ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Bisphenol A; Blastocyst; BPA; Estrogens; Implantation; Pregnancy; Triclosan

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ESTRADIOL; TRICLOSAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; GESTATION PERIOD; GESTATIONAL AGE; LITTER SIZE; MOUSE; NIDATION; NONHUMAN; REPRODUCTIVE TOXICITY; SURVIVAL; WEANING;

ANIMALS; ANIMALS, OUTBRED STRAINS; ANTI-INFECTIVE AGENTS, LOCAL; BENZHYDRYL COMPOUNDS; DRUG SYNERGISM; EMBRYO IMPLANTATION; ESTROGENS, NON-STEROIDAL; FEMALE; GESTATIONAL AGE; MATERNAL-FETAL EXCHANGE; MICE; PHENOLS; PREGNANCY; TRICLOSAN;

MUS;

EID: 84867740282     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2012.09.008     Document Type: Article

References (75)

1. Rodricks J.V., Swenberg J.A., Borzelleca J.F., Maronpot R.R., Shipp A.M. Triclosan: a critical review of the experimental data and development of margins of safety for consumer products. Critical Reviews in Toxicology 2010, 40:422-484.
2. Fang J., Stingley R.L., Beland F.A., Harrouk W., Lumpkins D.L., Howard P. Occurrence, efficacy, metabolism, and toxicity of triclosan. Journal of Environmental Science and Health Part C 2010, 28:147-151.
3. Dann A.B., Hontela A. Triclosan: environmental exposure, toxicity and mechanisms of action. Journal of Applied Toxicology 2011, 31:285-311.
4. Bedoux G., Roig B., Thomas O., Dupont V., Le Bot B. Occurrence and toxicity of antimicrobial triclosan and by-products in the environment. Environmental Science and Pollution Research 2012, 19:1044-1065.
5. Moss T., Howes D., Williams F.M. Percutaneous penetration and dermal metabolism of triclosan (2,4,4'-trichloro-2'-hydroxydiphenyl ether). Food and Chemical Toxicology 2000, 38:361-370.
6. Queckenberg C., Meins J., Wachall B., Doroshyenko O., Tomalik-Scharte D., Bastian B., et al. Absorption, pharmacokinetics, and safety of triclosan after dermal administration. Antimicrobial Agents and Chemotherapy 2010, 54:570-572.
7. Sandborgh-Eglund G., Adolfsson-Erici M., Odham G., Ekstrand J. Pharmacokinetics of triclosan following oral ingestion in humans. Journal of Toxicology and Environment Health 2006, 69:1861-1873.
8. Rotroff D.M., Wetmore B.A., Dix D.J., Ferguson S.S., Clewell H.J., Houck K.A., et al. Incorporating human dosimetry and exposure into high-throughput in vitro toxicity screening. Toxicological Sciences 2010, 117:348-358.
9. Allmyr M., Adolfsson-Erici M., McLachlan M.S., Sandborgh-Englund G. Triclosan in plasma and milk from Swedish nursing mothers and their exposure via personal care products. Science of the Total Environment 2006, 372:87-93.
10. Dirtu A.C., Roosens L., Geens T., Gheorghe A., Neels H., Covaci A. Simultaneous determination of bisphenol A, triclosan, and tetrabromobisphenol A in human serum using solid-phase extraction and gas chromatography-electron capture negative-ionization mass spectrometry. Analytical and Bioanalytical Chemistry 2008, 391:1175-1181.
11. Dayan A.D. Risk assessment of triclosan [irgasan] in human breast milk. Food and Chemical Toxicology 2007, 45:125-129.
12. Azzouz A., Jurado-Sánchez B., Souhail B., Ballesteros E. Simultaneous determination of 20 pharmacologically active substances in cow's milk, goat's milk, and human breast milk by gas chromatography-mass spectrometry. Journal of Agricultural and Food Chemistry 2011, 59:5125-5132.
13. Toms L.L., Allmyr M., Mueller J.F., Adolfsson-Erici M., McLachlan M., Murby J., et al. Triclosan in individual human milk samples from Australia. Chemosphere 2011, 85:1682-1686.
14. Calafat A.M., Ye X., Wong L., Reidy J.A., Needham L.L. Urinary concentrations of triclosan in the U.S. population: 2003-2004. Environmental Health Perspectives 2008, 116:303-307.
15. Geens T., Neels H., Covaci A. Sensitive and selective method for the determination of bisphenol-A and triclosan in serum and urine as pentafluorobenzoate-derivatives using GC-ECNI/MS. Journal of Chromatography B 2009, 877:4042-4046.
16. Kim K., Park H., Yang W., Lee J.H. Urinary concentrations of bisphenol A and triclosan and associations with demographic factors in the Korean population. Environmental Research 2011, 111:1280-1285.
17. Geens T., Neels H., Covaci A. Distribution of bisphenol-A, triclosan and n-nonylphenol in human adipose tissue, liver and brain. Chemosphere 2012, 87:796-802.
18. McAvoy D.C., Schatowitz B., Jacob M., Hauk A., Eckhoff W.S. Measurement of triclosan in wastewater treatment systems. Environmental Toxicology and Chemistry 2002, 21:1323-1329.
19. Lishman L., Smyth S.A., Sarafin K., Kleywegt S., Tioto J., Peart T., et al. Occurrence and reductions of pharmaceuticals and personal care products and estrogens by municipal wastewater treatment plants in Ontario, Canada. Science of the Total Environment 2006, 367:544-558.
20. Coogan M.A., La Point T.W. Snail bioaccumulation of triclocarban, triclosan, and methyltriclosan in a North Texas, USA, stream affected by wastewater treatment plant runoff. Environmental Toxicology and Chemistry 2008, 27:1788-1793.
21. Ying G., Kookana R.S. Triclosan in wastewaters and biosolids from Australian wastewater treatment plants. Environment International 2007, 33:199-205.
22. Kumar K.S., Priya S.M., Peck A.M., Sajwan K.S. Mass loadings of triclosan and triclocarbon from four wastewater treatment plants to three rivers and landfills in Savannah, Georgia, USA. Archives of Environment Contamination and Toxicology 2010, 58:275-285.
23. Kolpin D.W., Furlong E.T., Meyer M.T., Thurman E.M., Zaugg S.D., Barber L.B., et al. Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999-2000: a national reconnaissance. Environmental Science and Technology 2002, 36:1202-1211.
24. Li X., Ying G., Su H., Yang X., Wang L. Simultaneous determination and assessment of 4-nonylphenol, bisphenol A and triclosan in tap water, bottled water and baby bottles. Environment International 2010, 36:557-562.
25. Foran C.M., Bennett E.R., Benson W.H. Developmental evaluation of a potential non-steroidal estrogen: triclosan. Marine Environment Research 2000, 50:153-156.
26. Ishibashi H., Matsumura N., Hirano M., Matsuoka M., Shiratsuchi H., Ishibashi Y., et al. Effects of triclosan on the early life stages and reproduction of medaka Oryzias latipes and induction of hepatic vitellogenin. Aquatic Toxicology 2004, 67:167-179.
27. Raut S.A., Angus R.A. Triclosan has endocrine-disrupting effects in male western mosquitofish, Gambusia affinis. Environmental Toxicology and Chemistry 2010, 29:1287-1291.
28. Kumar V., Chakraborty A., Kural M.R., Roy P. Alteration of testicular steroidogenesis and histopathology of reproductive system in male rats treated with triclosan. Reproductive Toxicology 2009, 27:177-185.
29. Zorilla L.M., Gibson E.K., Jeffay S.C., Crofton K.M., Setzer W.R., Cooper R.L., et al. The effects of triclosan on puberty and thyroid hormones in male Wistar rats. Toxicological Sciences 2009, 107:56-64.
30. Jung E., An B., Choi K., Jeung E. Potential estrogenic activity of triclosan in the uterus of immature rats and rat pituitary GH3 cells. Toxicology Letters 2012, 208:142-148.
31. Rodríguez P.E.A., Sanchez M.S. Maternal exposure to triclosan impairs thyroid homeostasis and female pubertal development in Wistar rat offspring. Journal of Toxicology and Environmental Health Part A 2010, 73:1678-1688.
32. Stoker T.E., Gibson E.K., Zorilla L.M. Triclosan exposure modulates estrogen-dependent responses in the female Wistar rat. Toxicological Sciences 2010, 117:45-53.
33. Roblero L.S., Garavagno A.C. Effect of oestradiol-17β and progesterone on oviductal transport and early development of mouse embryos. Journal of Reproduction and Fertility 1979, 57:91-95.
34. Paria B.C., Huet-Hudson Y.M., Dey S.K. Blastocyst's state of activity determines the window of implantation in the receptive mouse uterus. Proceedings of the National Academy of Sciences 1993, 90:10159-10162.
35. Potter S.W., Gaza G., Morris J.E. Estradiol induces E-cadherin degradation in mouse uterine epithelium during the estrous cycle and early pregnancy. Journal of Cellular Physiology 1996, 169:1-14.
36. Wang H., Dey S.K. Roadmap to embryo implantation: clues from mouse models. Nature Reviews Genetics 2006, 7:185-199.
37. Ma W., Song H., Das S.K., Paria B.C., Dey S.K. Estrogen is a critical determinant that specifies the duration of the window of uterine receptivity for implantation. Proceedings of the National Academy of Sciences 2003, 100:2963-2968.
38. Valbuena D., Martin J., de Pablo J.L., Remohi J., Pellicer A., Simon C. Increasing levels of estradiol are deleterious to embryonic implantation because they directly affect the embryo. Fertility and Sterility 2001, 76:962-968.
39. Burdick H.O., Whitney R. Acceleration of the rate of passage of fertilized ova through the fallopian tubes of mice by massive injections of an estrogenic substance. Endocrinology 1937, 21:637-643.
40. deCatanzaro D., Beaton E.A., Khan A., Vella E. Urinary oestradiol and testosterone levels from novel male mice approach values sufficient to disrupt early pregnancy in nearby inseminated females. Reproduction 2006, 32:309-317.
41. deCatanzaro D., MacNiven E., Ricciuti F. Comparison of the adverse effects of adrenal and ovarian steroids on early pregnancy in mice. Psychoneuroendocrinology 1991, 16:525-536.
42. deCatanzaro D., Baptista M.A.S., Vella E. Administration of minute quantities of 17β-estradiol on the nasal area terminates early pregnancy in inseminated female mice. Pharmacology Biochemistry and Behavior 2001, 69:503-509.
43. Berger R.G., Hancock T., deCatanzaro D. Influence of oral and subcutaneous bisphenol-A on intrauterine implantation of fertilized ova in inseminated female mice. Reproductive Toxicology 2007, 23:138-144.
44. Berger R.G., Shaw J., deCatanzaro D. Impact of acute bisphenol-A exposure upon intrauterine implantation of fertilized ova and urinary levels of progesterone and 17β-estradiol. Reproductive Toxicology 2008, 26:94-99.
45. Berger R.G., Foster W.G., deCatanzaro D. Bisphenol-A exposure during the period of blastocyst implantation alters uterine morphology and perturbs measures of estrogen and progesterone receptor expression in mice. Reproductive Toxicology 2010, 30:393-400.
46. Paul K.B., Hedge J.M., DeVito M.J., Crofton K.M. Developmental triclosan exposure decreases maternal and neonatal thyroxine in rats. Environmental Toxicology and Chemistry 2010, 29:2840-2844.
47. Kortenkamp A. Ten years of mixing cocktails: a review of combination effects of endocrine-disrupting chemicals. Environmental Health Perspectives 2007, 115:98-105.
48. Rajapakse N., Silva E., Kortenkamp A. Combining xenoestrogens at levels below individual no-observed-effect concentrations dramatically enhances steroid hormone action. Environmental Health Perspectives 2002, 110:917-921.
49. Silva E., Rajapakse N., Kortenkamp A. Something from nothing-eight weak estrogenic chemicals combined at concentrations below NOECs produce significant mixture effects. Environmental Science and Technology 2002, 36:1751-1756.
50. Silva E., Rajapakse N., Scholze M., Backhaus T., Ermler S., Kortenkamp A. Joint effects of heterogeneous estrogenic chemicals in the E-Screen-exploring the applicability of concentration addition. Toxicological Sciences 2011, 122:383-394.
51. Charles G.D., Gennings C., Tornesi B., Kan H.L., Zacharewski T.R., Gollapudi B.B., et al. Analysis of the interaction of phytoestrogens and synthetic chemicals: an in vitro/in vivo comparison. Toxicology and Applied Pharmacology 2007, 218:280-288.
52. Thorpe K.L., Hutchinson T.H., Hetheridge M.J., Scholze M., Sumpter J.P., Tyler C.R. Assessing the biological potency of binary mixtures of environmental estrogens using vitellogenin induction in juvenile rainbow trout (Oncorhynchus mykiss). Environmental Science and Technology 2001, 35:2476-2481.
53. Brian J.V., Harris C.A., Scholze M., Backhaus T., Booy P., Lamoree M., et al. Accurate prediction of the response of freshwater fish to a mixture of estrogenic chemicals. Environmental Health Perspectives 2005, 113:721-728.
54. Brian J.V., Harris C.A., Scholze M., Kortenkamp A., Booy P., Lamoree M., et al. Evidence of estrogenic mixture effects on the reproductive performance of fish. Environmental Science and Technology 2007, 41:337-344.
55. Jin S., Yang F., Liao T., Hui Y., Wen S., Xu Y. Enhanced effects by mixtures of three estrogenic compounds at environmentally relevant levels on development of Chinese rare minnow (Gobiocypris rarus). Environmental Toxicology and Pharmacology 2012, 33:277-283.
56. Tinwell H., Ashby J. Sensitivity of the immature rat uterotrophic assay to mixtures of estrogens. Environmental Health Perspectives 2005, 112:575-582.
57. Shaw J., deCatanzaro D. Estrogenicity of parabens revisited: Impact of parabens on early pregnancy and an uterotrophic assay in mice. Reproductive Toxicology 2009, 28:26-31.
58. deCatanzaro D., MacNiven E. Psychogenic pregnancy disruptions in mammals. Neuroscience and Biobehavioral Reviews 1992, 16:43-53.
59. Xiao S., Diao H., Smith M.A., Song X., Ye X. Preimplantation exposure to bisphenol A (BPA) affects embryo transport, preimplantation embryo development, and uterine receptivity in mice. Reproductive Toxicology 2011, 32:434-441.
60. Diamanti-Kandarakis E., Bourguignon J-P., Giudice L.C., Hauser R., Prins G.S., Soto A.M., et al. Endocrine-disrupting chemicals: an endocrine society scientific statement. Endocrine Reviews 2009, 30:293-342.
61. Kuiper G.G.J.M., Lemmen J.G., Carlsson B., Corton J.C., Safe S.H., van der Saag P.T., et al. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor β. Endocrinology 1998, 139:4252-4263.
62. Laws S.C., Carey S.A., Ferrell J.M., Bodman G.J., Cooper R.L. Estrogenic activity of octylphenol, nonylphenol, bisphenol A and methoxychlor in rats. Toxicological Sciences 2000, 54:154-167.
63. Okada H., Tokunaga T., Liu X., Takayanagi S., Matsushima A., Shimohigashi Y. Direct evidence revealing structural elements essential for the high binding ability of bisphenol A to human estrogen-related receptor-γ. Environmental Health Perspectives 2008, 116:32-38.
64. Nativelle-Serpentini C., Richard S., Séralini G.E., Sourdaine P. Aromatase activity modulation by lindane and bisphenol-A in human placental JEG-3 and transfected kidney E293 cells. Toxicology In Vitro 2003, 17:413-422.
65. Lee H.J., Chattopadhyay S., Gong E.Y., Ahn R.S., Lee K. Antiandrogenic effects of bisphenol A and nonylphenol on the function of androgen receptor. Toxicological Sciences 2003, 75:40-46.
66. Christen V., Crettaz P., Oberli-Schrammli A., Fent K. Some flame retardants and the antimicrobials triclosan and triclocarban enhance the androgenic activity in vitro. Chemosphere 2010, 81:1245-1252.
67. Chen J., Ahn K.C., Gee N.A., Gee S.J., Hammock B.D., Lasley B.L. Antiandrogenic properties of parabens and other phenolic containing small molecules in personal care products. Toxicology and Applied Pharmacology 2007, 221:278-284.
68. Ahn K.C., Zhao B., Chen J., Cherednichenko G., Sanmarti E., Denison M.S., et al. In vitro biologic activities of the antimicrobials triclocarban, its analogs, and triclosan in bioassay screens: receptor-based bioassay screens. Environmental Health Perspectives 2008, 116:203-210.
69. Gee R.H., Charles A., Taylor N., Darbe P.D. Oestrogenic and androgenic activity of triclosan in breast cancer cells. Journal of Applied Toxicology 2008, 28:78-91.
70. Forgacs A.L., Ding Q., Jaremba R.G., Huhtaniemi I.T., Rahman N.A., Zacharewski T.R. BLTK1 murine leydig cells: a novel steroidogenic model for evaluating the effects of reproductive and developmental toxicants. Toxicological Sciences 2012, 127:391-402.
71. Henry ND, Fair PA. Comparison of in vitro cytotoxicity, estrogenicity and anti-estrogenicity of triclosan, perfluorooctane sulfonate and perfluorooctanoic acid. Journal of Applied Toxicology, in press. doi:10.1002/jat.1736.
72. James M.O., Li W., Summerlot D.P., Rowland-Faux L., Wood C.E. Triclosan is a potent inhibitor of estradiol and estrone sulfonation in sheep placenta. Environment International 2010, 36:942-949.
73. Muir C., Vella E., Pisani N., deCatanzaro D. Enzyme immunoassay of 17β-estradiol, estrone conjugates, and testosterone in urinary and fecal samples from male and female mice. Hormone and Metabolic Research 2001, 33:653-658.
74. Guzzo A.C., Jheon J., Imtiaz F., deCatanzaro D. Oestradiol transmission from males to females in the context of the Bruce and Vandenbergh effects in mice (Mus musculus). Reproduction 2012, 143:539-548.
75. Ehrlich S., Williams P.L., Missmer S.A., Flaws J.A., Berry K.F., Calafat A.M., et al. Urinary bisphenol A concentrations and implantation failure among women undergoing in vitro fertilization. Environmental Health Perspectives 2012, 120:978-983.