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Endocrine-Disrupting Effects of Compounds in Danish Streams

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Abstract

Effluents from municipal wastewater-treatment plants and scattered dwellings, as well as runoff from agricultural fields, are sources of endocrine-disrupting compounds (EDCs) in the aquatic environment. The present study investigated the correlation between the occurrence of EDCs in nine Danish streams using passive samplers (polar organic integrative samplers and silicone membranes) and determined their possible biological effects as assessed by mammal cell cultures and the mussel (Unio tumidus). The passive samplers and mussels were exposed simultaneously at the study sites. The extracts from the passive samplers were used to measure the concentrations of EDCs and the biological effects on the estrogen (ER), androgen (AR), and aryl hydrocarbon (AhR)-receptor transactivation. Male mussels were investigated for biomarkers of endocrine effects, such as the levels of vitellogenin-like proteins measured as alkali-labile phosphate (ALP). EDC concentrations, hormone-receptor transactivation (ER, AR, AhR), and level of ALP were greater downstream of wastewater-treatment plants compared with upstream sites and sites supposed to be relatively nonimpacted by wastewater. Furthermore, there was a significant positive correlation between in vitro AhR transactivation and frequency of ALP of male mussels. We conclude that wastewater effluent is an important source of endocrine-disrupting effects in the aquatic environment and that the combination of biological effect measurements and chemical analyses based on passive sampling is useful in the assessment of the ecological state of the aquatic environment.

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References

  • Abarikwu SO, Pant AB, Farombi EO (2013) Effects of quercetin on mRNA expression of steroidogenesis genes in primary cultures of Leydig cells treated with atrazine. Toxicol In Vitro 27(2):700–707

    Article  CAS  Google Scholar 

  • Alvarez DA, Petty JD, Huckins JN, Jones-Lepp TL, Getting DT, Goddard JP, Manahan SE (2004) Development of a passive, in situ, integrative sampler for hydrophilic organic contaminants in aquatic environments. Environ Toxicol Chem 23(7):1640–1648

    Article  CAS  Google Scholar 

  • Andersen HR, Vinggaard AM, Rasmussen TH, Gjermandsen IM, Bonefeld-Jorgensen EC (2002) Effects of currently used pesticides in assays for estrogenicity, androgenicity, and aromatase activity in vitro. Toxicol Appl Pharmacol 179(1):1–12

    Article  CAS  Google Scholar 

  • Bauer ER, Meyer HH, Stahlschmidt-Allner P, Sauerwein H (1998) Application of an androgen receptor assay for the characterisation of the androgenic or antiandrogenic activity of various phenylurea herbicides and their derivatives. Analyst 123(12):2485–2487

    Article  CAS  Google Scholar 

  • Bonefeld-Jorgensen EC (2010) Biomonitoring in Greenland: human biomarkers of exposure and effects—a short review. Rural Remote Health 10(2):1362

    Google Scholar 

  • Bonefeld-Jorgensen EC, Long M, Hofmeister MV, Vinggaard AM (2007) Endocrine-disrupting potential of bisphenol A, bisphenol A dimethacrylate, 4-n-nonylphenol, and 4-n-octylphenol in vitro: new data and a brief review. Environ Health Perspect 115(Suppl 1):69–76. doi:10.1289/ehp.9368

    Article  Google Scholar 

  • Boutrup S, Fauser P, Thomsen M, Dahlöff I, Larsen MM, Strand J, Sortkjær O, Ellermann T, Rasmussen P, Jørgensen LF, Pedersen MW, Munk LM (2006) Miljøfremmede stoffer og tungmetaller i vandmiljøet. Tilstand og udvikling, 1998–2003. Faglig rapport fra DMU, nr. 585 Danamarks Miljøundersøgelser, Aarhus University, Denmark

  • Brack W, Segner H, Möder M, Schüürmann G (2000) Fixed-effect-level toxicity equivalents—a suitable parameter for assessing ethoxyresorufin-o-deethylase induction potency in complex environmental samples. Environ Toxicol Chem 19(10):2493–2501

    CAS  Google Scholar 

  • Brack W, Klamer HJ, Lopez de Alda M, Barcelo D (2007) Effect-directed analysis of key toxicants in European river basins a review. Environ Sci Pollut Res Int 14(1):30–38

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Brown DJ, Clarke GC, van Benden RJ (1997) Halogenated aromatic hydrocarbon-binding proteins identified in several invertebrate marine species. Aquat Toxicol 37(1):71–78

    Article  CAS  Google Scholar 

  • Butler RA, Kelley ML, Powell WH, Hahn ME, Van Beneden RJ (2001) An aryl hydrocarbon receptor (AHR) homologue from the soft-shell clam, Mya arenaria: evidence that invertebrate AHR homologues lack 2,3,7,8-tetrachlorodibenzo-p-dioxin and beta-naphthoflavone binding. Gene 278(1–2):223–234

    Article  CAS  Google Scholar 

  • Chang HS, Choo KH, Lee B, Choi SJ (2009) The methods of identification, analysis, and removal of endocrine disrupting compounds (EDCs) in water. J Hazard Mater 172(1):1–12. doi:10.1016/j.jhazmat.2009.06.135

    Article  CAS  Google Scholar 

  • Chesman BS, Langston WJ (2006) Intersex in the clam Scrobicularia plana: a sign of endocrine disruption in estuaries? Biol Lett 2(3):420–422. doi:10.1098/rsbl.2006.0482

    Article  CAS  Google Scholar 

  • Cooper KR, Wintermyer M (2009) A critical review: 2,3,7,8-tetrachlorodibenzo-p-dioxin (2,3,7,8-TCDD) effects on gonad development in bivalve mollusks. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 27(4):226–245. doi:10.1080/10590500903310112

    Article  CAS  Google Scholar 

  • Danish EPA (2011) Pesticide statistics 2010. Information from EPA 5 (in Danish)

  • de Lafontaine Y, Gagne F, Blaise C, Costan G, Gagnon P, Chan HM (2000) Biomarkers in zebra mussels (Dreissena polymorpha) for the assessment and monitoring of water quality of the St Lawrence River (Canada). Aquat Toxicol 50(1–2):51–71

    Article  Google Scholar 

  • Delescluse C, Ledirac N, de Sousa G, Pralavorio M, Lesca P, Rahmani R (1998) Cytotoxic effects and induction of cytochromes P450 1A1/2 by insecticides, in hepatic or epidermal cells: Binding capability to the Ah receptor. Toxicol Lett 96–97:33–39

    Article  Google Scholar 

  • Eldridge JC, Stevens JT, Breckenridge CB (2008) Atrazine interaction with estrogen expression systems. Rev Environ Contam Toxicol 196:147–160

    CAS  Google Scholar 

  • Engwall M, Broman D, Ishaq R, Näf C, Zebühr Y, Brunström B (1999) Toxic potencies of lipophilic extracts from sediments and settling particulate matter (SPM) collected in a PCB-contaminated river system. Environ Toxicol Chem 15(2):213–222

    Article  Google Scholar 

  • Felding G, Mogensen BB, Sørensen JA, Hansen AC (1997) Surface run-off of pesticides from farmland to streams and lakes. Bekæmpelsesmiddelforskning fra Miljøstyrelsen, vol 29, p 76

  • Flammarion P, Brion F, Babut M, Garric J, Migeon B, Noury P, Thybaud E (2000) Induction of fish vitellogenin and alterations in testicular structure: preliminary results of estrogenic effects in chub (Leuciscus cephalus). Ecotoxicology 9:127–135

    Article  CAS  Google Scholar 

  • Gagne F, Blaise C, Pellerin J, Pelletier E, Strand J (2006) Health status of Mya arenaria bivalves collected from contaminated sites in Canada (Saguenay Fjord) and Denmark (Odense Fjord) during their reproductive period. Ecotoxicol Environ Saf 64(3):348–361. doi:10.1016/j.ecoenv.2005.04.007

    Article  CAS  Google Scholar 

  • Garrison PM, Tullis K, Aarts JM, Brouwer A, Giesy JP, Denison MS (1996) Species-specific recombinant cell lines as bioassay systems for the detection of 2,3,7,8-tetrachlorodibenzo-p-dioxin-like chemicals. Fundam Appl Toxicol Off J Soc Toxicol 30(2):194–203

    Article  CAS  Google Scholar 

  • Ghisari M, Bonefeld-Jorgensen EC (2009) Effects of plasticizers and their mixtures on estrogen receptor and thyroid hormone functions. Toxicol Lett 189(1):67–77. doi:10.1016/j.toxlet.2009.05.004

    Article  CAS  Google Scholar 

  • Hamers T, Leonards PE, Legler J, Vethaak AD, Schipper CA (2010) Toxicity profiling: an integrated effect-based tool for site-specific sediment quality assessment. Integr Environ Assess Manag 6(4):761–773. doi:10.1002/ieam.75

    Article  CAS  Google Scholar 

  • Hamers T, Legler J, Blaha L, Hylland K, Marigomez I, Schipper CA, Segner H, Vethaak AD, Witters H, de Zwart D, Leonards PE (2013) Expert opinion on toxicity profiling–report from a NORMAN expert group meeting. Integr Environ Assess Manag 9(2):185–191. doi:10.1002/ieam.1395

    Article  Google Scholar 

  • Hecker M, Tyler CR, Hoffmann M, Maddix S, Karbe L (2002) Plasma biomarkers in fish provide evidence for endocrine modulation in the Elbe River, Germany. Environ Sci Technol 36(11):2311–2321

    Article  CAS  Google Scholar 

  • Ishihara A, Rahman FB, Leelawatwattana L, Prapunpoj P, Yamauchi K (2009) In vitro thyroid hormone-disrupting activity in effluents and surface waters in Thailand. Environ Toxicol Chem 28(3):586–594. doi:10.1897/08-120.1

    Article  CAS  Google Scholar 

  • Jobling S, Nolan M, Tyler CR, Brighty G, Sumpter JP (1998) Widespread sexual disruption in wild fish. Environ Sci Technol 32:2498–2506

    Article  CAS  Google Scholar 

  • Kharat I, Saatcioglu F (1996) Antiestrogenic effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin are mediated by direct transcriptional interference with the liganded estrogen receptor. Cross-talk between aryl hydrocarbon- and estrogen-mediated signaling. J Biol Chem 271(18):10533–10537

    Article  CAS  Google Scholar 

  • Kjaerstad MB, Taxvig C, Nellemann C, Vinggaard AM, Andersen HR (2010) Endocrine disrupting effects in vitro of conazole antifungals used as pesticides and pharmaceuticals. Reprod Toxicol 30(4):573–582

    Article  CAS  Google Scholar 

  • Kjeldsen LS, Bonefeld-Jorgensen EC (2013) Perfluorinated compounds affect the function of sex hormone receptors. Environ Sci Pollut Res Int. doi:10.1007/s11356-013-1753-3

  • Kjeldsen LS, Ghisari M, Bonefeld-Jorgensen EC (2013) Currently used pesticides and their mixtures affect the function of sex hormone receptors and aromatase enzyme activity. Toxicol Appl Pharmacol 272(2):453–464. doi:10.1016/j.taap

    Google Scholar 

  • Kjølholt J, Stuer-Lauridsen F, Høibye L, Halling-Sørensen B, Ingerslev F, Bach K, Hansen M, Hansen N, Køppen B, Bjerregaard P, Frost B (2006) Survey of Estrogenic Activity in the Danish Aquatic Environment Part B. Environmental Project No. 1007, Danish Ministry of Environment

  • Kolodziej EP, Gray JL, Sedlak DL (2003) Quantification of steroid hormones with pheromonal properties in municipal wastewater effluent. Environ Toxicol Chem 22(11):2622–2629

    Article  CAS  Google Scholar 

  • Kruger T, Long M, Bonefeld-Jorgensen EC (2008) Plastic components affect the activation of the aryl hydrocarbon and the androgen receptor. Toxicology 246(2–3):112–123

    Article  Google Scholar 

  • Krüger T, Hjelmborg PS, Jönsson BAG, Hagmar L, Giwercman A, Manicardi G-C, Bizzaro D, Spanò M, Rignell-Hydbom A, Pedersen HS, Toft G, Bonde JP, Bonefeld-Jorgensen EC (2007) Xeno-androgenic activity in serum differs across European and Inuit populations. Environ Health Perspect 115(Suppl 1):21–27

    Article  Google Scholar 

  • Kusk KO, Kruger T, Long M, Taxvig C, Lykkesfeldt AE, Frederiksen H, Andersson AM, Andersen HR, Hansen KM, Nellemann C, Bonefeld-Jorgensen EC (2011) Endocrine potency of wastewater: contents of endocrine disrupting chemicals and effects measured by in vivo and in vitro assays. Environ Toxicol Chem 30(2):413–426. doi:10.1002/etc.385

    Article  CAS  Google Scholar 

  • Lafont R, Mathieu M (2007) Steroids in aquatic invertebrates. Ecotoxicology 16(1):109–130. doi:10.1007/s10646-006-0113-1

    Article  CAS  Google Scholar 

  • Larsen MM, Allan I, Næs K, Nyberg E, Hoydal K (2009) Evaluation of Passive Samplers for the Monitoring of Contaminants in Sediment and Water: Monitoring of POPs and PCBs in International Monitoring Programmes. TemaNord 2009:563, p 81. ISBN 978-92-893-1914-0

  • Li J, Ma M, Wang Z (2010) In vitro profiling of endocrine disrupting effects of phenols. Toxicol In Vitro 24(1):201–207

    Article  CAS  Google Scholar 

  • Lima D, Reis-Henriques MA, Silva R, Santos AI, Castro LF, Santos MM (2011) Tributyltin-induced imposex in marine gastropods involves tissue-specific modulation of the retinoid X receptor. Aquat Toxicol 101(1):221–227. doi:10.1016/j.aquatox.2010.09.022

    Article  CAS  Google Scholar 

  • Long M, Laier P, Vinggaard AM, Andersen HR, Lynggaard J, Bonefeld-Jorgensen EC (2003) Effects of currently used pesticides in the AhR-CALUX assay: comparison between the human TV101L and the rat H4IIE cell line. Toxicology 194(1–2):77–93

    Article  CAS  Google Scholar 

  • Long M, Andersen BS, Lindh CH, Hagmar L, Giwercman A, Manicardi GC, Bizzaro D, Spano M, Toft G, Pedersen HS, Zvyezday V, Bonde JP, Bonefeld-Jorgensen EC (2006) Dioxin-like activities in serum across European and Inuit populations. Environ Health 5:14

    Article  Google Scholar 

  • Long M, Ghisari M, Bonefeld-Jorgensen EC (2013) Effects of perfluoroalkyl acids on the function of the thyroid hormone and the aryl hydrocarbon receptor. Environ Sci Pollut Res Int. doi:10.1007/s11356-013-1628-7

  • Lye CM, Frid CLJ, Gill ME, McCormick D (1997) Abnormalities in the reproductive health of flounder platichthys flesus exposed to effluent from a sewage treatment works. Marine Poll Bul 34(1):34–41

    Article  CAS  Google Scholar 

  • Ma M, Li J, Wang Z (2005) Assessing the detoxication efficiencies of wastewater treatment processes using a battery of bioassays/biomarkers. Arch Environ Contam Toxicol 49(4):480–487. doi:10.1007/s00244-004-0204-z

    Article  CAS  Google Scholar 

  • MacLeod SL, McClure EL, Wong CS (2007) Laboratory calibration and field deployment of the polar organic chemical integrative sampler for pharmaceuticals and personal care products in wastewater and surface water. Environ Toxicol Chem 26(12):2517–2529. doi:10.1897/07-238.1

    Article  CAS  Google Scholar 

  • Matozzo V, Gagne F, Marin MG, Ricciardi F, Blaise C (2008) Vitellogenin as a biomarker of exposure to estrogenic compounds in aquatic invertebrates: a review. Environ Int 34(4):531–545. doi:10.1016/j.envint.2007.09.008

    Article  CAS  Google Scholar 

  • Matthews J, Gustafsson JA (2006) Estrogen receptor and aryl hydrocarbon receptor signaling pathways. Nucl Recept Signal 4:e016. doi:10.1621/nrs.04016

    Google Scholar 

  • Matthiessen P, Arnold D, Johnson AC, Pepper TJ, Pottinger TG, Pulman KG (2006) Contamination of headwater streams in the United Kingdom by oestrogenic hormones from livestock farms. Sci Total Environ 367(2–3):616–630. doi:10.1016/j.scitotenv.2006.02.007

    Article  CAS  Google Scholar 

  • Mazzella N, Dubernet JF, Delmas F (2007) Determination of kinetic and equilibrium regimes in the operation of polar organic chemical integrative samplers. Application to the passive sampling of the polar herbicides in aquatic environments. J Chromatogr A 1154(1–2):42–51. doi:10.1016/j.chroma.2007.03.087

    Article  CAS  Google Scholar 

  • McGinnis CL, Crivello JF (2011) Elucidating the mechanism of action of tributyltin (TBT) in zebrafish. Aquat Toxicol 103(1–2):25–31

    Article  CAS  Google Scholar 

  • Mnif W, Hassine AI, Bouaziz A, Bartegi A, Thomas O, Roig B (2011) Effect of endocrine disruptor pesticides: a review. Int J Environ Res Public Health 8(6):2265–2303. doi:10.3390/ijerph8062265

    Article  CAS  Google Scholar 

  • Mortensen AS, Arukwe A (2009) Effects of tributyltin (TBT) on in vitro hormonal and biotransformation responses in Atlantic salmon (Salmo salar). J Toxicol Environ Health A 72(3–4):209–218

    Article  CAS  Google Scholar 

  • Murata T, Yamauchi K (2008) 3,3′,5-Triiodo-l-thyronine-like activity in effluents from domestic sewage treatment plants detected by in vitro and in vivo bioassays. Toxicol Appl Pharmacol 226(3):309–317. doi:10.1016/j.taap.2007.09.003

    Article  CAS  Google Scholar 

  • Murphy KA, Quadro L, White LA (2007) The intersection between the aryl hydrocarbon receptor (AhR)- and retinoic acid-signaling pathways. Vitam Horm 75:33–67. doi:10.1016/s0083-6729(06)75002-6

    CAS  Google Scholar 

  • Olsen CM, Meussen-Elholm ET, Holme JA, Hongslo JK (2002) Brominated phenols: characterization of estrogen-like activity in the human breast cancer cell-line MCF-7. Toxicol Lett 129(1–2):55–63

    Article  CAS  Google Scholar 

  • Orton F, Rosivatz E, Scholze M, Kortenkamp A (2011) Widely used pesticides with previously unknown endocrine activity showed as in vitro antiandrogens. Environ Health Perspect 119(6):794–800

    CAS  Google Scholar 

  • Pawlowski S, Ternes TA, Bonerz M, Rastall AC, Erdinger L, Braunbeck T (2004) Estrogenicity of solid phase-extracted water samples from two municipal sewage treatment plant effluents and river Rhine water using the yeast estrogen screen. Toxicol In Vitro 18(1):129–138

    Article  CAS  Google Scholar 

  • Penza M, Jeremic M, Marrazzo E, Maggi A, Ciana P, Rando G et al (2011) The environmental chemical tributyltin chloride (TBT) shows both estrogenic and adipogenic activities in mice which might depend on the exposure dose. Toxicol Appl Pharmacol 255(1):65–75

    Article  CAS  Google Scholar 

  • Quinn B, Gagne F, Costello M, McKenzie C, Wilson J, Mothersill C (2004) The endocrine disrupting effect of municipal effluent on the zebra mussel (Dreissena polymorpha). Aquat Toxicol 66(3):279–292

    Article  CAS  Google Scholar 

  • Quinn B, Gagne F, Blaise C, Costello MJ, Wilson JG, Mothersill C (2006) Evaluation of the lethal and sub-lethal toxicity and potential endocrine disrupting effect of nonylphenol on the zebra mussel (Dreissena polymorpha). Comp Biochem Physiol C Toxicol Pharmacol 142(1–2):118–127. doi:10.1016/j.cbpc.2005.11.004

    Article  Google Scholar 

  • Quiros L, Cespedes R, Lacorte S, Viana P, Raldua D, Barcelo D, Pina B (2005) Detection and evaluation of endocrine-disruption activity in water samples from Portuguese rivers. Environ Toxicol Chem 24(2):389–395

    Article  CAS  Google Scholar 

  • Rucinski M, Ziolkowska A, Hochol A, Pucher A, Macchi C, Belloni AS et al (2006) Estradiol and resveratrol stimulating effect on osteocalcin, but not osteonectin and collagen-1alpha gene expression in primary culture of rat calvarial osteoblast-like cells. Int J Mol Med 18(4):565–570

    CAS  Google Scholar 

  • Rusina TP, Smedes F, Klanova J, Booij K, Holoubek I (2007) Polymer selection for passive sampling: a comparison of critical properties. Chemosphere 68(7):1344–1351. doi:10.1016/j.chemosphere.2007.01.025

    Article  CAS  Google Scholar 

  • Schiliro T, Pignata C, Fea E, Gilli G (2004) Toxicity and estrogenic activity of a wastewater treatment plant in Northern Italy. Arch Environ Contam Toxicol 47(4):456–462. doi:10.1007/s00244-003-0153-y

    Article  CAS  Google Scholar 

  • Sharan S, Nikhil K, Roy P (2013) Effects of low dose treatment of tributyltin on the regulation of estrogen receptor functions in MCF-7 cells. Toxicol Appl Pharmacol 269(2):176–186

    Article  CAS  Google Scholar 

  • Simon S, Mueller SO (2006) Human reporter gene assays: transcriptional activity of the androgen receptor is modulated by the cellular environment and promoter context. Toxicology 220(2–3):90–103. doi:10.1016/j.tox.2005.12.002

    Article  CAS  Google Scholar 

  • Stuer-Lauridsen F, Kjølholt J, Høibye L, Hinge-Christensen S, Ingerslev F, Hansen M, Andersen Krogh K, Andersen HR, Halling-Sørensen B, Hansen N, Køppen B, Bjerregaard P, Frost B (2005) Survey of estrogenic activity in the Danish aquatic environment. Environmental Project. no. 977, Danish Ministry of Environment

  • Styczen M, Wiberg-Larsen P, Aagaard A (2003) Tag pulsen på pesticiderne i vandmiljøet. Vand & Jord 10:84–87

    Google Scholar 

  • Takeuchi S, Iida M, Yabushita H, Matsuda T, Kojima H (2008) In vitro screening for aryl hydrocarbon receptor agonistic activity in 200 pesticides using a highly sensitive reporter cell line, DR-EcoScreen cells, and in vivo mouse liver cytochrome P450-1A induction by propanil, diuron and linuron. Chemosphere 74(1):155–165

    Article  CAS  Google Scholar 

  • Tollefsen KE, Finne EF, Romstad R, Sandberg C (2006) Effluents from oil production activities contain chemicals that interfere with normal function of intra- and extracellular estrogen binding proteins. Mar Environ Res 62(Suppl):S191–S194

    Article  CAS  Google Scholar 

  • Tran DQ, Kow KY, McLachlan JA, Arnold SF (1996) The inhibition of estrogen receptor-mediated responses by chloro-S-triazine-derived compounds is dependent on estradiol concentration in yeast. Biochem Biophys Res Commun 227(1):140–146

    Article  CAS  Google Scholar 

  • Undeger U, Schlumpf M, Lichtensteiger W (2010) Effect of the herbicide pendimethalin on rat uterine weight and gene expression and in silico receptor binding analysis. Food Chem Toxicol 48(2):502–508

    Article  CAS  Google Scholar 

  • van Aerle R, Nolan TM, Jobling S, Christiansen LB, Sumpter JP, Tyler CR (2001) Sexual disruption in a second species of wild cyprinid fish (the gudgeon, Gobio gobio) in United Kingdom freshwaters. Environ Toxicol Chem 20(12):2841–2847

    Google Scholar 

  • Van der Linden SC, Heringa MB, Man HY, Sonneveld E, Puijker LM, Brouwer A, Van der Burg B (2008) Detection of multiple hormonal activities in wastewater effluents and surface water, using a panel of steroid receptor CALUX bioassays. Environ Sci Technol 42(15):5814–5820

    Article  Google Scholar 

  • Wilson VS, Bobseine K, Lambright CR, Gray LE Jr (2002) A novel cell line, MDA-kb2, that stably expresses an androgen- and glucocorticoid-responsive reporter for the detection of hormone receptor agonists and antagonists. Toxicol Sci 66(1):69–81

    Article  CAS  Google Scholar 

  • Witters HE, Vangenechten C, Berckmans P (2001) Detection of estrogenic activity in Flemish surface waters using an in vitro recombinant assay with yeast cells. Water Sci Technol 43(2):117–123

    CAS  Google Scholar 

  • Wold S (1995) Chemometrics: what do we mean with it, and what do we want from it? Chemom Intell Lab Syst 30:109–115

    Google Scholar 

  • Zha J, Wang Z, Schlenk D (2006) Effects of pentachlorophenol on the reproduction of Japanese medaka (Oryzias latipes). Chem Biol Interact 161(1):26–36

    Article  CAS  Google Scholar 

  • Zhang Z, Hibberd A, Zhou JL (2008) Analysis of emerging contaminants in sewage effluent and river water: comparison between spot and passive sampling. Anal Chim Acta 607(1):37–44. doi:10.1016/j.aca.2007.11.024

    Article  CAS  Google Scholar 

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Acknowledgments

For excellent technical assistance, we thank Charlotte Dahl Schiødt, Christel Christoffersen, and Inga Jensen, Department of Environmental Science, Aarhus University; Peter Koefoed and Dorte W. Jensen, Department of Bioscience, Aarhus University; and Dorte Olsson, Centre for Arctic Health, Unit of Cellular and Molecular Toxicology, Department of Public Health, Aarhus University. This study was supported by the Danish Environmental Protection Agency.

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  1. Unit of Cellular and Molecular Toxicology, Department of Public Health, Centre for Arctic Health, Aarhus University, BartholinsAllé 2, Building 1260, 8000, Århus C, Denmark

    Manhai Long, Tanja Krüger & Eva Cecilie Bonefeld-Jørgensen

  2. Department of Bioscience, Aarhus University, 4000, Roskilde, Denmark

    Jakob Strand, Pia Lassen, Martin M. Larsen & Peter Wiberg-Larsen

  3. Department of Environmental Science, Aarhus University, 4000, Roskilde, Denmark

    Pia Lassen & Rossana Bossi

  4. Department of Biological and Environmental Sciences, University of Gothenburg, 405 30, Göteborg, Sweden

    Ingela Dahllöf

  5. Department of Environmental Science, Aarhus University, 8600, Silkeborg, Denmark

    Peter Wiberg-Larsen

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Long, M., Strand, J., Lassen, P. et al. Endocrine-Disrupting Effects of Compounds in Danish Streams. Arch Environ Contam Toxicol 66, 1–18 (2014). https://doi.org/10.1007/s00244-013-9959-4

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