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SRIF's Activities - Endocrine Disrupting Chemicals (EDCs)

EDCs comprise a diverse group of compounds displaying a broad array of molecular structures and physiochemical properties.  They include natural steroidal hormones such as 17b-estradiol, estrone and estriol, synthetic hormones such as 17a-ethinyl estradiol found in birth control formulations and many other industrial chemicals such as chlorinated pesticides, polychlorinated biphenyls phthalate esters and alkylphenols.

The endocrine system regulates development, growth, reproduction, and behavior through an intricate system of hormones (Richardson 2004). Exposure to various hormonally active compounds can result in decreased androgen production (demasculinization) or increased estrogen production (feminization) in the males of many aquatic species (Milnes, Bermudez et al. 2006)  As the fish endocrine system shares many similarities with those of higher vertebrates including humans, fish have been used to monitor exposure to EDCs in aquatic environments (Zeng, Shan et al. 2005). EDCs have been shown to affect the form and function of reproductive systems skewing male-female ratios in fish.

Vitellogenesis is a critical part of the reproductive process.  It involves the synthesis of a large molecular weight protein precursor, vitellogenin (VTG), in the liver. VTG transported through the blood circulation to the ovary is thus sequestered by growing oocytes and proteolytically cleaved into the major yolk protein components (Soverchia, Ruggeri et al. 2005). Effluent from sewage-treatment containing estrogenic disrupting chemicals, or mixtures of EDC chemicals, stimulates vitellogenin synthesis in male fish (Sumpter 1995). Elevated plasma levels of vitellogenin have been observed in male fish exposed to EDC concentrations as low as 1 to 10 nanograms per liter in aquatic environments.

EDCs disrupt gonadal differentiation and can result in the simultaneous presence of ovarian and testicular tissue in the same gonad creating a condition referred to as intersex (Milnes, Bermudez et al. 2006).  This intersex phenomenon of feminized males is characterized by the occurrence of oocytes scattered throughout the testis or within distinct regions of ovarian tissue that are well delineated from testicular tissue (Nolan, Jobling et al. 2001). 

Examples of wild fish populations exhibiting intersex gonads include flounder taken from Tokyo Bay (Hashimoto, Bessho et al. 2000); rainbow trout (Tyler and Routledge, 1998), gudgeon (Gobio gobio) (vanAerle, Nolan et al. 2001) collected from rivers in the UK polluted with estrogenic sewage treatment effluent; wild barbell from polluted portions of the Po River in Italy (Vigano, Arillo et al. 2001), and lake whitefish (Coregonus clupeaformis) collected from the St. Lawrence River in Quebec, Canada (Mikaelian, Lafontaine et al. 2001). 

Studies show that reproductive effects from anthropogenic 17b-estradiol are dependent of the time and concentration of exposures in zebrafish. Some of these effects are reversible while others are permanent and those that occur in early life stages are brought about by low concentrations (Brion, Tyler et al. 2004).  Fathead minnows (Pimephales promelas)  exposed to an environmentally relevant concentration of ethinylestradiol for short intervals in fish early life-stages showed vitellogenic and gonadal responses where 60% of the male fish studied had feminizing transformations (vanAerle, Pounds et al. 2002)

Endocrine disrupting chemicals can also substantially affect gamete production and fertility. General decreases in spermatogenesis and ejaculated sperm counts have been observed in several species, including goldfish treated with 17b-estradiol  (Schoenfuss, Levitt et al. 2002), adult zebrafish after 24 days of laboratory exposure to 17-b-ethynylestradiol (VandenBelt, Verheyen et al. 2001), adult Japanese medaka exposed to 4-tert-octylphenol (Gronen, Denslow et al. 1999), swordtails (Xiphophorus helleri) exposed to nonylphenol (Kwak, Bae et al. 2001), and adult and sexually developing juvenile guppies exposed to vinclozolin and p; p’-DDE (Baatrup and Junge 2001); (Bayley, Nielsen et al. 1999)). Van den Belt et al. (2002) noted that spermatogenesis recovered when fish were removed to clean water.
Endocrine hormones are correlated with the mating displays of guppies and the secretion of pheromones in goldfish, but various EDCs can alter the performance of these reproductive behaviors. In adult male guppies exposed to EDCs, the number of sexual displays directed toward females were significantly reduced (Baatrup and Junge 2001).

Many natural and synthetic EDCs are continuously released in the aquatic environment when sewage treatment plants (STPs) are unsuccessful in completely removing them (Ternes, Stumpf et al. 1999).  Other EDCs enter the environment from agricultural runoff from fields treated with manure as fertilizer (Pedersen, Soliman et al. 2005). The removal of EDCs from STP effluent is very complex and currently not well understood (Servos, Bennie et al. 2005).  STPs systems designed for nitrification and denitrification may appreciably eliminate natural and synthetic estrogens (Andersen, Siegrist et al. 2003). However, storm events frequently overwhelm STPs and untreated sewage is often released into surface waters.  Furthermore, municipal effluents may contain a wide variety of other industrial and domestic EDCs such as alkylphenols, bisphenol-A, as well as many pharmaceuticals.  The environmental impact of the complex mixtures in effluents remains poorly understood.(Servos, Bennie et al. 2005)

Recent studies show the potential for EDCs to be easily distributed in the environment and their physicochemical properties can enable them to accumulate in river sediments (Kuster, Alda et al. 2004)  Recent data suggest that hormones in readily measured quantities can be transported considerable distances from the source of pollution.  Significant levels of estrogens were detected over a 100-km section of the Lower Jordan River below a major sewage treatment facility (Barel-Cohen, Shore et al. 2006).  Detectable levels of estrogens were observed downstream from an STP effluent discharge near Bordeaux, France along the Jalle d’Eysines River (Labadie and Budzinski 2005).  The effects of EDCs on fish and wildlife have been well-documented (Milnes, Bermudez et al. 2006).  Environmental impacts may be profound at levels as low as ~1 ng l-1 in aquatic species (Hansen, Dizer et al. 1998).
Many municipalities utilize surface water as a source of drinking water.  Drinking water supplies downstream from effluent discharges containing EDCs clearly raises concerns over the removal of these compounds by common drinking water treatment processes.  Conventional treatment regimes may have low removal of many EDC.  Therefore, knowledge of source concentrations is essential for devising efficient drinking water treatment to avoid drinking water contamination by EDCs.  Ozonation, activated carbon, and bank filtration have shown potential for removing EDCs (Richardson 2004) (Westerhoff, Yoon et al. 2005).

Selected References

Andersen, H., H. Siegrist, et al. (2003). "Fate of Estrogens in a Municipal Sewage Treatment Plant." Environmental Science and Technology 37(18): 4021-4026.
           
Baatrup, E. and M. Junge (2001). "Antiandrogenic Pesticides Disrupt Sexual Characteristics in the Adult Male Guppy (Poecilia reticulata)." Environmental Health Perspectives 109(10): 1063-1070.
           
Barel-Cohen, K., L. S. Shore, et al. (2006). "Monitoring of natural and synthetic hormones in a polluted river." Journal of Environmental Management 78: 16-23.
           
Bayley, M., M. Junge, et al. (2002). "Exposure of juvenile guppies to three antiandrogens causes demasculinization and a reduced sperm count in adult males." Aquatic Toxicology 56: 227-239.
           
Bayley, M., J. R. Nielsen, et al. (1999). "Guppy Sexual Behavior as an Effect Biomarker of Estrogen Mimics." Ecotoxicology and Environmental Safety 43: 68-73.
           
Brion, F., C. R. Tyler, et al. (2004). "Impacts of 17 beta -estradiol, including environmentally relevant concentrations, on reproduction after exposure during embryo-larval-, juvenile- and adult-life stages in zebrafish (Danio rerio)." Aquatic Toxicology 68(3): 193-217.
           
Cai, Y., G. Jiang, et al. (2003). "Multiwalled Carbon Nanotubes as a Solid-Phase Extraction Adsorbent for the Determination of Bisphenol A, 4-n-Nonylphenol, and 4-tert-Octylphenol." Analytical Chemistry 75: 2519-2521.
           
Carpinteiro, J., J. B. Quintana, et al. (2004). "Applicability of solid-phase microextraction followed by on-fibersilylation for the determination of estrogens in water samples by gas chromatography–tandem mass spectrometry." Journal of Chromatography A 1056: 179-185.
           
Crain, D. A., J. L.J. Guillette, et al. (1997). "Alterations in steroidogenesis in alligators (Alligator mississippiensis) exposed naturally and experimentally to environmental contaminants." Environmental Health Perspectives 105(5): 528-533.
           
Famiglini, G., P. Palma, et al. (2005). "Determination of Endocrine Disrupting Compounds in Marine Water by Nanoliquid Chromatography/Direct-Electron Ionization Mass Spectrometry." Analytical Chemistry 77(7654-7661).
           
Ferguson, P., P. Lee, et al. (2001). "Determination of Steroid Estrogens in Wastewater
by Immunoaffinity Extraction Coupled with
HPLC-Electrospray-MS." Analytical Chemistry 73: 3890-3895.
           
Gronen, S., N. Denslow, et al. (1999). "Serum vitellogenin levels and reproductive impairment of male Japanese Medaka (Oryzias latipes) exposed to 4-tert-octylphenol." Environmental Health Perspectives 107(5): 385-390.
           
Hansen, P.-D., H. Dizer, et al. (1998). "Vitellogenin - a biomarker for endocrine
disruptors." Trends in Analytical Chemistry 17(7): 448-451.
           
Hashimoto, S., H. Bessho, et al. (2000). "Elevated serum vitellogenin levels and gonadal abnormalities in wild male flounder (Pleuronectes yokohamae) from Tokyo Bay, Japan." Marine Environmental Research 49: 37-53.
           
Hayes, T., K. Haston, et al. (2003). "Atrazine-Induced Hermaphroditism at 0.1 ppb in American Leopard Frogs (Rana pipiens): Laboratory and Field Evidence." Environmental Health Perspectives 111(4): 568-575.
           
Hernando, M. D., M. Mezcua, et al. (2004). "Comparative study of analytical methods involving gas chromatography–mass spectrometry after derivatization and gas chromatography–tandem mass spectrometry for the determination of
selected endocrine disrupting compounds in wastewaters." Journal of Chromatography A 1047: 129-135.
           
Jeannot, R., H. Sabik, et al. (2002). "D etermination of endocrine-disrupting compounds in environmental samples using gas and liquid chromatography with mass spectrometry." Journal of Chromatography A 974: 143-159.
           
Kang, I. J., H. Yokota, et al. (2003). "Effects of 4-nonylphenol on reproduction of Japanese medaka, Oryzias latipes." Environmental Toxicology and Chemistry 22(10): 2438-2345.
           
Koester, C. J. (2005). "Trends in Environmental Analysis." Analytical Chemistry 77: 3737-3754.
           
Kolpin, D. W., E. T. Furlong, et al. (2002). "Pharmaceuticals, Hormones, and Other Wastewater Contaminants in U.S. Streams 1999-2000: A National Reconnaissance." Environmental Science and Technology 36: 1202-1211.
           
Kuster, M., M. J. L. d. Alda, et al. (2004). "Analysis and distribution of estrogens and progestogens in sewage sludge, soils and sediments." Trends in Analytical Chemistry 23(10-11): 790-798.
           
Kwak, H. I., M. O. Bae, et al. (2001). "Effects of nonylphenol, bisphenol A, and their mixture on the viviparous swordtail fish (Xiphophorus helleri)." Environmental Toxicology and Chemistry 20(4): 787-795.
           
Labadie, P. and H. Budzinski (2005). "Determination of Steroidal Hormone Profiles along the Jalle d’Eysines River (near Bordeaux, France)." Environmental Science and Technology 39(14): 5112-5120.
           
Lambropoulou, D. A. and T. A. Albanis (2004). "Sensitive trace enrichment of environmental andiandrogen vinclozolin from natural waters and sediment samples using hollow-fiber liquid-phase microextraction." Journal of Chromatography A 1061: 11-18.
           
MD-DNR (2006). Maryland's Surf Your Watershed - Watershed Profile for the Anacostia River, Maryland Department of Natural Resources.
           
Meng, Z., W. Chen, et al. (2006). "Removal of Estrogenic Pollutants from Contaminated Water Using Molecularly Imprinted Polymers."
           
Mikaelian, I., Y. D. Lafontaine, et al. (2001). "Health of lake whitefish (Coregonus clupeaformis) with elevated tissue levels of environmental contaminants." Environmental Toxicology and Chemistry 21(3): 532-541.
           
Milnes, M. R., D. S. Bermudez, et al. (2006). "Contaminant-induced feminization and demasculinization of nonmammalian vertebrate males in aquatic environments." Environmental Research 100: 3-17.
           
Mitani, K., M. Fujioka, et al. (2005). "Fully automated analysis of estrogens in environmental waters by in-tube solid-phase microextraction coupled with liquid chromatography–tandem mass spectrometry." Journal of Chromatography A 1081: 218-224.
           
Nolan, M., S. Jobling, et al. (2001). "A histological description of intersexuality in the roach." Journal of Fish Biology 58(1): 160-176.
           
Palace, V. P., R. E. Evans, et al. (2002). "Induction of vitellogenin and histological effects in wild fathead minnows from a lake experimentally treated with the synthetic estrogen, ethynylestradiol." Water Quality Research Journal of Canada 37(3): 637-350.
           
Pedersen, J. A., M. Soliman, et al. (2005). "Human Pharmaceuticals, Hormones, and Personal Care Product Ingredients in Runoff from Agricultural Fields Irrigated withTreated Wastewater." Journal of Agricultural and Food Chemistry 53: 1625-1632.
           
Rajapakse, N., E. Silva, et al. (2004). "Deviation from Additivity with Estrogenic Mixtures Containing 4-Nonylphenol and 4-tert-Octylphenol Detected in the E-SCREEN Assay." Environmental Science and Technology 38: 6343-6352.
           
Richardson, S. D. (2002). "Environmental Mass Spectrometry: Emerging Contaminants and Current Issues." Analytical Chemistry 74: 2719-2742.
           
Richardson, S. D. (2004). "Environmental Mass Spectrometry: Emerging
Contaminants and Current Issues." Analytical Chemistry 76: 3337-3364.
           
Richardson, S. D. and T. A. Ternes (2005). "Water Analysis: Emerging Contaminants and
Current Issues." Analytical Chemistry 77: 3807-3838.
           
Schoenfuss, H. L., J. T. Levitt, et al. (2002). "Ten-week exposure to treated sewage discharge has relatively minor, variable effects on reproductive behavior and sperm production in goldfish." Environmental Toxicology and Chemistry 21(10): 2185-2190.
           
Servos, M. R., D. T. Bennie, et al. (2005). "Distribution of estrogens,17b-estradiol and estrone, in Canadian municipal wastewater treatment plants." Science of the Total Environment 336: 155-170.
           
Shareef, A., C. J. Parnis, et al. (2004). "Suitability of N,O-bis(trimethylsilyl)trifluoroacetamide and N-(tert-butyldimethylsilyl)-N-methyltrifluoroacetamide as derivatization reagents for the determination of the estrogens estrone and 17-ethinylestradiol by gas chromatography–mass spectrometry." Journal of Chromatography A 1026: 295-300.
           
Silva, E., N. Rajapakse, et al. (2002). "Something from “Nothing” - Eight Weak Estrogenic Chemicals Combined at Concentrations below NOECs Produce Significant Mixture Effects." Environmental Science and Technology 36: 1751-1756.
           
Sohoni, P., C. R. Tyler, et al. (2001). "Reproductive Effects of Long-Term Exposure to Bisphenol A in the Fathead Minnow (Pimephales promelas)." Environmental Science and Technology 35: 2917-2925.
           
Soverchia, L., B. Ruggeri, et al. (2005). "Modulation of vitellogenin synthesis through estrogen receptor beta-1 in goldfish (Carassius auratus) juveniles exposed to 17-b estradiol and nonylphenol." Toxicology and Applied Pharmacology 209: 236-243.
           
Sumpter, J. P. (1995). Feminized responses in fish to environmental e
estrogens. International Congress of Toxicology, 2-6 Jul1995, Seattle, WA (USA).
           
Suzuki, T., K. Ide, et al. (2001). "Classification of Environmental Estrogens by Physicochemical Properties Using Principal Component Analysis and Hierarchical Cluster Analysis." J. Chem. Inf. Comput. Sci, 41: 718-726.
           
Suzuki, T., Y. Nakagawa, et al. (2004). "Environmental Fate of Bisphenol A and Its Biological Metabolites in River Water and Their Xeno-estrogenic Activity." Environmental Science and Technology 38: 2389-2396.
           
Ternes, T. A., H. Andersen, et al. (2002). "Determination of Estrogens in Sludge and Sediments by Liquid Extraction and GC/MS/MS." Analytical Chemistry 74: 3498-3504.
           
Ternes, T. A., U. M. Stumpf, et al. (1999). "Behavior and occurrence of estrogens in municipal sewage treatment plants } I. Investigations in Germany, Canada and Brazil." The Science of the Total Environment 225: 81-90.
           
Thorpe, K., R. Benstead, et al. (2003). "Reproductive effects of exposure to oestrone in the fathead minnow." Fish Physiology and Biochemistry 28(1-4): 451.
           
Tsuda, T., A. Takino, et al. (2001). "Evaluation of 4-Nonylphenols and 4-tert-Octylphenol Contamination of Fish and Rivers by Laboratory Accumulation and Excretion Experiments." Wat. Res 35(7): 1786-1792.
           
vanAerle, R., M. Nolan, et al. (2001). "Sexual disruption in a second species of wild cyprinid fish (the gudgeon, Gobio gobio) in United Kingdom freshwaters." Environmental Toxicology and Chemistry 20(12): 2841-2847.
           
vanAerle, R., N. Pounds, et al. (2002). "Window of sensitivity for the estrogenic effects of ethinylestradiol in early life-stages of fathead minnow, Pimephales promelas." Ecotoxicology 11(6): 423-434.
           
VandenBelt, K., R. Verheyen, et al. (2001). "Reproductive Effects of Ethynylestradiol and 4t-Octylphenol on the Zebrafish (Danio rerio)." Archives of Environmental Contamination and Toxicology 41: 458-467.
           
Vigano, L., A. Arillo, et al. (2001). "First observation of intersex cyprinids in the Po River, Italy." The Science of the Total Environment 269: 189-194.
           
Waters (2003). Oasis SPE Method for Endocrine Disruptors. Oasis SPE Product Application. Milford, MA, Waters Corporation.
           
Westerhoff, P., Y. Yoon, et al. (2005). "Fate of Endocrine-Disruptor, Pharmaceutical, and Personal Care Product Chemicals during Simulated Drinking Water Treatment Processes." Environmental Science and Technology 39: 6649-6663.
           
Yokota, H., Y. Tsuruda, et al. (2000). "Effect of bisphenol A on the early life stage in Japanese medaka (Oryzias latipes)." Environmental Toxicology and Chemistry 19(7): 1925-1930.
           
Zeng, Z., T. Shan, et al. (2005). "Development of Estrogen-Responsive Transgenic Medaka for Environmental Monitoring of Endocrine Disrupters." Environmental Science and Technology 39: 9001-9008.
           
Zhang, L., I. A. Khan, et al. (2002). "Characterization of the estrogenic response to genistein in Japanese medaka (Oryzias latipes)." Comparative Biochemistry and Physiology Part C 132: 203-211.
           


 

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