Comparative biological effects and potency of 17α- and 17β-estradiol in fathead minnows.

17β-Estradiol is the most potent natural estrogen commonly found in anthropogenically altered environments and has been the focus of many toxicological laboratory studies. However, fewer aquatic toxicological data on the effects of 17α-estradiol, a diastereoisomer of 17β-estradiol, exists in the literature even though it has been found in the aquatic environment, sometimes at higher concentrations than 17β-estradiol. The central objective of this study was to determine how the anatomical, physiological, and behavioral effects of exposure to 17α-estradiol compare to the well-documented effects of 17β-estradiol exposures in aquatic vertebrates. A 21-day flow-through exposure of mature male and female fathead minnows to three concentrations each of 17α- and 17β-estradiol (averaged measured concentrations 27, 72, and 150 ng/L for 17α-estradiol, and 9, 20, and 44 ng/L for β-estradiol, respectively) yielded significant, concentration-dependent differences in plasma vitellogenin concentrations among estradiol-exposed males when compared to fish from an ethanol carrier control. Interstitial cell prominence in the testis of fish was elevated in all estradiol treatments. Aggressiveness of male fish to defend nest sites appeared depressed in many of the higher concentration estradiol treatments (albeit not significantly). No clear effects were observed in female fish. Based on plasma vitellogenin data, it appears that 17β-estradiol is 8-9 times more potent than 17α-estradiol and that the lowest observable effect concentration (LOEC) for 17α-estradiol in fathead minnows is greater than 25 ng/L and may be less than 75 ng/L.

[1]  Karen A Kidd,et al.  Collapse of a fish population after exposure to a synthetic estrogen , 2007, Proceedings of the National Academy of Sciences.

[2]  Gerald T Ankley,et al.  Temporal variation in the estrogenicity of a sewage treatment plant effluent and its biological significance. , 2008, Environmental science & technology.

[3]  C. A. Harris,et al.  Accurate Prediction of the Response of Freshwater Fish to a Mixture of Estrogenic Chemicals , 2005, Environmental health perspectives.

[4]  Heiko L Schoenfuss,et al.  Reproductive responses of male fathead minnows exposed to wastewater treatment plant effluent, effluent treated with XAD8 resin, and an environmentally relevant mixture of alkylphenol compounds. , 2007, Aquatic toxicology.

[5]  Roy S. Thompson,et al.  Adverse reproductive effects in male fathead minnows (Pimephales promelas) exposed to environmentally relevant concentrations of the natural oestrogens, oestradiol and oestrone , 1998 .

[6]  G. Ankley,et al.  Fathead minnow vitellogenin: Complementary DNA sequence and messenger RNA and protein expression after 17β‐estradiol treatment , 2000 .

[7]  C. Tyler,et al.  An Assessment of the Model of Concentration Addition for Predicting the Estrogenic Activity of Chemical Mixtures in Wastewater Treatment Works Effluents , 2005, Environmental health perspectives.

[8]  P. Sorensen,et al.  Ten‐week exposure to treated sewage discharge has relatively minor, variable effects on reproductive behavior and sperm production in goldfish , 2002, Environmental toxicology and chemistry.

[9]  K. Dimberg,et al.  Male goldfish reproductive behaviour and physiology are severely affected by exogenous exposure to 17beta-estradiol. , 2001, Aquatic toxicology.

[10]  Roy S. Thompson,et al.  Intermittent Exposure of Fish to Estradiol , 2000 .

[11]  J. McLachlan,et al.  Fathead minnow (Pimephales promelas) vitellogenin: purification, characterization and quantitative immunoassay for the detection of estrogenic compounds. , 1999, Comparative biochemistry and physiology. Part C, Pharmacology, toxicology & endocrinology.

[12]  Dalma Martinović,et al.  Environmental estrogens suppress hormones, behavior, and reproductive fitness in male fathead minnows , 2007, Environmental toxicology and chemistry.

[13]  R. J. Smith.  Seasonal changes in the histology of the gonads and dorsal skin of the fathead minnow, Pimephales promelas , 1978 .

[14]  John P. Sumpter,et al.  Widespread Sexual Disruption in Wild Fish , 1998 .

[15]  P. Bjerregaard,et al.  Vitellogenin induction by 17β-estradiol and 17α-ethinylestradiol in male zebrafish (Danio rerio) , 2002 .

[16]  J. Cairns,et al.  Aquatic toxicology. Part 2 , 1990 .

[17]  A. Biales,et al.  Assessing the effects of exposure timing on biomarker expression using 17beta-estradiol. , 2010, Aquatic toxicology.

[18]  L. Unger.  Nest defense by deceit in the fathead minnow, Pimephales promelas , 1983, Behavioral Ecology and Sociobiology.

[19]  John P. Sumpter,et al.  Estrogenic activity in five United Kingdom rivers detected by measurement of vitellogenesis in caged male trout , 1997 .

[20]  J. R. Nielsen,et al.  Guppy sexual behavior as an effect biomarker of estrogen mimics. , 1999, Ecotoxicology and environmental safety.

[21]  N. Stacey,et al.  A steroidal pheromone and spawning stimuli act via different neuroendocrine mechanisms to increase gonadotropin and milt volume in male goldfish Carassius auratus. , 1997, General and comparative endocrinology.

[22]  C. Bowman,et al.  Vitellogenin mRNA regulation and plasma clearance in male sheepshead minnows, (Cyprinodon variegatus) after cessation of exposure to 17 beta-estradiol and p-nonylphenol. , 2002, Aquatic toxicology.

[23]  D R Dietrich,et al.  Determination of vitellogenin kinetics in male fathead minnows (Pimephales promelas). , 2002, Toxicology letters.

[24]  T. Croley,et al.  Estrogenic potency of chemicals detected in sewage treatment plant effluents as determined by in vivo assays with Japanese medaka (Oryzias latipes) , 2001, Environmental toxicology and chemistry.

[25]  P. Wester,et al.  Effects of the estrogen agonist 17β‐estradiol and antagonist tamoxifen in a partial life‐cycle assay with zebrafish (Danio rerio) , 2007, Environmental toxicology and chemistry.

[26]  A. Wilkie,et al.  Determination of steroidal estrogens in flushed dairy manure wastewater by gas chromatography-mass spectrometry. , 2006, Journal of environmental quality.

[27]  L. A. Wagner,et al.  During development, 17alpha-estradiol is a potent estrogen and carcinogen. , 1997, Environmental health perspectives.

[28]  R. Suri,et al.  Presence of steroid hormones and antibiotics in surface water of agricultural, suburban and mixed-use areas , 2009, Environmental monitoring and assessment.

[29]  Thomas Heberer,et al.  Determination of estrogenic steroids in surface water and wastewater by liquid chromatography-electrospray tandem mass spectrometry. , 2005, Journal of separation science.

[30]  W. Horwitz,et al.  A Heuristic Derivation of the Horwitz Curve , 1997 .

[31]  N. Shappell,et al.  Estrogenicity and nutrient concentration of surface waters surrounding a large confinement dairy operation using best management practices for land application of animal wastes. , 2010, Environmental science & technology.

[32]  L. Barber,et al.  Larval exposure to environmentally relevant mixtures of alkylphenolethoxylates reduces reproductive competence in male fathead minnows. , 2006, Aquatic toxicology.

[33]  Melanie A Vrabel,et al.  Destruction of estrogens using Fe-TAML/peroxide catalysis. , 2008, Environmental science & technology.

[34]  J. Giesy,et al.  Effects of waterborne exposure of 17 β-estradiol on secondary sex characteristics and gonads of fathead minnows (Pimephales promelas) , 1999 .

[35]  W. E I Z H E N G.  Analysis of Steroid Hormones in a Typical Dairy Waste Disposal System , 2007 .

[36]  C. Tyler,et al.  Associations between altered vitellogenin concentrations and adverse health effects in fathead minnow (Pimephales promelas). , 2007, Aquatic toxicology.

[37]  L. Tremblay,et al.  Steroid estrogens, conjugated estrogens and estrogenic activity in farm dairy shed effluents. , 2010, Environmental pollution.

[38]  G. Brighty,et al.  Assessment of Feminization of Male Fish in English Rivers by the Environment Agency of England and Wales , 2005, Environmental health perspectives.

[39]  L. Barber,et al.  Impairment of the reproductive potential of male fathead minnows by environmentally relevant exposures to 4-nonylphenolf. , 2008, Aquatic toxicology.

[40]  M. Cabrera,et al.  17β-estradiol and testosterone in soil and runoff from grasslands amended with broiler litter , 2000 .

[41]  J. Sumpter,et al.  Estrogenic Effects of Effluents from Sewage Treatment Works , 1994 .

[42]  Charles R. Tyler,et al.  Long-Term Exposure to Environmental Concentrations of the Pharmaceutical Ethynylestradiol Causes Reproductive Failure in Fish , 2004, Environmental health perspectives.

[43]  M. White,et al.  Analysis of lagoon samples from different concentrated animal feeding operations for estrogens and estrogen conjugates. , 2007, Environmental science & technology.

[44]  C Sonnenschein,et al.  The E-SCREEN assay as a tool to identify estrogens: an update on estrogenic environmental pollutants. , 1995, Environmental health perspectives.