What level of estrogenic activity determined by in vitro assays in municipal waste waters can be considered as safe?

Environment International

Volumn 64, Issue , 2014, Pages 98-109

  Jarošová, Barbora ^a   Bláha, Luděk ^a   Giesy, John P ^b   Hilscherová, Klára ^a  

^a MASARYK UNIVERSITY   (Czech Republic)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Environmental risk assessment; Estrogen; In vitro assay; Threshold; Waste water treatment plant

Indexed keywords

BIOASSAY; RISK ASSESSMENT; RIVERS; WASTEWATER;

ENVIRONMENTAL RISK ASSESSMENT; ESTROGEN; IN-VITRO ASSAYS; MUNICIPAL WASTEWATERS; PREDICTED NO-EFFECT CONCENTRATIONS; RELATIVE CONTRIBUTION; THRESHOLD; WASTEWATER TREATMENT PLANTS;

EFFLUENTS;

ESTRADIOL; ESTRIOL; ESTROGEN; ESTRONE; ETHINYLESTRADIOL; STEROID;

BIOASSAY; CONCENTRATION (COMPOSITION); DILUTION; EFFLUENT; ENVIRONMENTAL RISK; ESTROGENIC COMPOUND; RISK ASSESSMENT; WASTE TREATMENT; WASTEWATER; WATER TREATMENT;

BIOASSAY; CONCENTRATION (PARAMETERS); EFFLUENT; ESTROGEN ACTIVITY; IN VITRO STUDY; IN VIVO STUDY; PREDICTOR VARIABLE; PRIORITY JOURNAL; REVIEW; RISK ASSESSMENT; SAFE CONCENTRATION OF ESTROGENIC EQUIVALENT; WASTE WATER TREATMENT PLANT; WATER ANALYSIS; WATER QUALITY;

ENVIRONMENTAL RISK ASSESSMENT; ESTROGEN; IN VITRO ASSAY; THRESHOLD; WASTE WATER TREATMENT PLANT;

ANIMALS; BIOLOGICAL ASSAY; ENVIRONMENTAL MONITORING; ESTRENES; ESTROGENS; HUMANS; RIVERS; WASTE WATER; WATER POLLUTANTS, CHEMICAL; WATER QUALITY;

EID: 84891365760     PISSN: 01604120     EISSN: 18736750     Source Type: Journal    
DOI: 10.1016/j.envint.2013.12.009     Document Type: Review

References (82)

1. Aerni H.R., Kobler B., Rutishauser B.V., Wettstein F.E., Fischer R., Giger W., et al. Combined biological and chemical assessment of estrogenic activities in wastewater treatment plant effluents. Anal Bioanal Chem 2004, 378(3):688-696.
2. Anderson P.D., Johnson A.C., Pfeiffer D., Caldwell D.J., Hannah R., Mastrocco F., et al. Endocrine disruption due to estrogens derived from humans predicted to be low in the majority of U.S. surface waters. Environ Toxicol Chem 2012, 31(6):1407-1415.
3. Avbersek M., Zegura B., Filipic M., Heath E. Integration of GC-MSD and ER-Calux (R) assay into a single protocol for determining steroid estrogens in environmental samples. Sci Total Environ 2011, 409(23):5069-5075.
4. Balaguer P., Fenet H., Georget V., Comunale F., Terouanne B., Gilbin R., et al. Reporter cell lines to monitor steroid and antisteroid potential of environmental samples. Ecotoxicology 2000, 9(1-2):105-114.
5. Baronti C., Curini R., D'Ascenzo G., Di Corcia A., Gentili A., Samperi R. Monitoring natural and synthetic estrogens at activated sludge sewage treatment plants and in a receiving river water. Environ Sci Technol 2000, 34(24):5059-5066.
6. Bermudez D.S., Gray L.E., Wilson V.S. Modelling defined mixtures of environmental oestrogens found in domestic animal and sewage treatment effluents using an in vitro oestrogen-mediated transcriptional activation assay (T47D-KBluc). Int J Androl 2012, 35(3):397-406.
7. Bjorkblom C., Salste L., Katsiadaki I., Wiklund T., Kronberg L. Detection of estrogenic activity in municipal wastewater effluent using primary cell cultures from three-spined stickleback and chemical analysis. Chemosphere 2008, 73(7):1064-1070.
8. Bolong N., Ismail A.F., Salim M.R., Matsuura T. A review of the effects of emerging contaminants in wastewater and options for their removal. Desalination 2009, 239(1-3):229-246.
9. Breinholt V., Larsen J.C. Detection of weak estrogenic flavonoids using a recombinant yeast strain and a modified MCF7 cell proliferation assay. Chem Res Toxicol 1998, 11(6):622-629.
10. Caldwell D.J., Mastrocco F., Anderson P.D., Lange R., Sumpter J.P. Predicted-no-effect concentrations for the steroid estrogens estrone, 17 beta-estradiol, estriol, and 17 alpha-ethinylestradiol. Environ Toxicol Chem 2012, 31(6):1396-1406.
11. Cargouet M., Perdiz D., Mouatassim-Souali A., Tamisier-Karolak S., Levi Y. Assessment of river contamination by estrogenic compounds in Paris area (France). Sci Total Environ 2004, 324(1-3):55-66.
12. Clara M., Kreuzinger N., Strenn B., Gans O., Kroiss H. The solids retention time-a suitable design parameter to evaluate the capacity of wastewater treatment plants to remove micropollutants. Water Res 2005, 39(1):97-106.
13. Demirpence E., Duchesne M.J., Badia E., Gagne D., Pons M. Mvln cells-a bioluminescent Mcf-7-derived cell-line to study the modulation of estrogenic activity. J Steroid Biochem Mol Biol 1993, 46(3):355-364.
14. Desbrow C., Routledge E.J., Brighty G.C., Sumpter J.P., Waldock M. Identification of estrogenic chemicals in STW effluent. 1. Chemical fractionation and in vitro biological screening. Environ Sci Technol 1998, 32:1549-1558.
15. Drewes J.E., Hemming J., Ladenburger S.J., Schauer J., Sonzogni W. An assessment of endocrine disrupting activity changes during wastewater treatment through the use of bioassays and chemical measurements. Water Environ Res 2005, 77(1):12-23.
16. Environment Agency Proposed Predicted-No-Effect-Concentrations (PNECs) for Natural and Synthetic Steroid Oestrogens in Surface Waters. P2-T04/1 2004, R&D Technical Report, Bristol, UK.
17. European Commission Analytical methods relevant to the European Commission's 2012 proposal on Priority Substances under the Water Framework Directive 2012, JRC Scientific and Policy Report, Ispra, Italy. 10.2788/51497.
18. Fernandez M.P., Ikonomou M.G., Buchanan I. An assessment of estrogenic organic contaminants in Canadian wastewaters. Sci Total Environ 2007, 373(1):250-269.
19. Furuichi T., Kannan K., Giesy J.P., Masunaga S. Contribution of known endocrine disrupting substances to the estrogenic activity in Tama River water samples from Japan using instrumental analysis and in vitro reporter gene assay. Water Res 2004, 38(20):4491-4501.
20. Gardner M., Comber S., Scrimshaw M.D., Cartmell E., Lester J., Ellor B. The significance of hazardous chemicals in wastewater treatment works effluents. Sci Total Environ 2012, 437:363-372.
21. Gutendorf B., Westendorf J. Comparison of an array of in vitro assays for the assessment of the estrogenic potential of natural and synthetic estrogens, phytoestrogens and xenoestrogens. Toxicology 2001, 166(1-2):79-89.
22. Hannah R., D'Aco V.J., Anderson P.D., Buzby M.E., Caldwell D.J., Cunningham V.L., et al. Exposure assessment of 17 alpha-ethinylestradiol in surface waters of the United States and Europe. Environ Toxicol Chem 2009, 28(12):2725-2732.
23. Harris C.A., Hamilton P.B., Runnalls T.J., Vinciotti V., Henshaw A., Hodgson D., et al. The consequences of feminization in breeding groups of wild fish. Environ Health Perspect 2011, 119:306-311.
24. Hilscherova K., Machala M., Kannan K., Blankenship A.L., Giesy J.P. Cell bioassays for detection of aryl hydrocarbon (AhR) and estrogen receptor (ER) mediated activity in environmental samples. Environ Sci Pollut Res 2000, 7(3):159-171.
25. Houtman C.J., Van Oostveen A.M., Brouwer A., Lamoree M.H., Legler J. Identification of estrogenic compounds in fish bile using bioassay-directed fractionation. Environ Sci Technol 2004, 38(23):6415-6423.
26. Jarosova B., Blaha L., Vrana B., Randak T., Grabic R., Giesy J.P., et al. Changes in concentrations of hydrophilic organic contaminants and of endocrine-disrupting potential downstream of small communities located adjacent to headwaters. Environ Int 2012, 45:22-31.
27. Jin S., Yang F., Liao T., Hui Y., Xu Y. Seasonal variations of estrogenic compounds and their estrogenicities in influent and effluent from a municipal sewage treatment plant in China. Environ Toxicol Chem 2008, 27(1):146-153.
28. Jobling S., Williams R., Johnson A., Taylor A., Gross-Sorokin M., Nolan M., et al. Predicted exposures to steroid estrogens in UK rivers correlate with widespread sexual disruption in wild fish populations. Environ Health Perspect 2006, 114:32-39.
29. Johnson A., Jurgens M. Endocrine active industrial chemicals: release and occurrence in the environment. Pure Appl Chem 2003, 75(11-12):1895-1904.
30. Johnson A.C., Sumpter J.P. Removal of endocrine-disrupting chemicals in activated sludge treatment works. Environ Sci Technol 2001, 35(24):4697-4703.
31. Johnson A.C., Belfroid A., Di Corcia A. Estimating steroid oestrogen inputs into activated sludge treatment works and observations on their removal from the effluent. Sci Total Environ 2000, 256(2-3):163-173.
32. Johnson A.C., Aerni H.R., Gerritsen A., Gibert M., Giger W., Hylland K., et al. Comparing steroid estrogen, and nonylphenol content across a range of European sewage plants with different treatment and management practices. Water Res 2005, 39(1):47-58.
33. Jurgens M.D., Holthaus K.I.E., Johnson A.C., Smith J.J.L., Hetheridge M., Williams R.J. The potential for estradiol and ethinylestradiol degradation in English rivers. Environ Toxicol Chem 2002, 21(3):480-488.
34. Kawanishi M., Takamura-Enya T., Ermawati R., Shimohara C., Sakamoto M., Matsukawa K., et al. Detection of genistein as an estrogenic contaminant of river water in Osaka. Environ Sci Technol 2004, 38(23):6424-6429.
35. Khanal S.K., Xie B., Thompson M.L., Sung S.W., Ong S.K., Van Leeuwen J. Fate, transport, and biodegradation of natural estrogens in the environment and engineered systems. Environ Sci Technol 2006, 40(21):6537-6546.
36. Kinnberg K. Evaluation of in vitro assays for determination of estrogenic activity in the environment 2003, Danish Environmental Protection Agency, Danish Ministry of the Environment.
37. Kiparissis Y., Hughes R., Metcalfe C., Ternes T. Identification of the isoflavonoid genistein in bleached kraft mill effluent. Environ Sci Technol 2001, 35(12):2423-2427.
38. Kirk L.A., Tyler C.R., Lye C.M., Sumpter J.P. Changes in estrogenic and androgenic activities at different stages of treatment in wastewater treatment works. Environ Toxicol Chem 2002, 21(5):972-979.
39. 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 US streams, 1999-2000: a national reconnaissance. Environ Sci Technol 2002, 36(6):1202-1211.
40. Korner W., Bolz U., Sussmuth W., Hiller G., Schuller W., Hanf V., et al. Input/output balance of estrogenic active compounds in a major municipal sewage plant in Germany. Chemosphere 2000, 40(9-11):1131-1142.
41. Korner W., Spengler P., Bolz U., Schuller W., Hanf V., Metzger J.W. Substances with estrogenic activity in effluents of sewage treatment plants in southwestern Germany. 2. Biological analysis. Environ Toxicol Chem 2001, 20(10):2142-2151.
42. Labadie P., Budzinski H. Determination of steroidal hormone profiles along the Jalle d'Eysines River (near Bordeaux, France). Environ Sci Technol 2005, 39(14):5113-5120.
43. Labadie P., Budzinski H. Development of an analytical procedure for determination of selected estrogens and progestagens in water samples. Anal Bioanal Chem 2005, 381(6):1199-1205.
44. Lagana A., Bacaloni A., De Leva I., Faberi A., Fago G., Marino A. Analytical methodologies for determining the occurrence of endocrine disrupting chemicals in sewage treatment plants and natural waters. Anal Chim Acta 2004, 501(1):79-88.
45. Legler J., Zeinstra L.M., Schuitemaker F., Lanser P.H., Bogerd J., Brouwer A., et al. Comparison of in vivo and in vitro reporter gene assays for short-term screening of estrogenic activity. Environ Sci Technol 2002, 36(20):4410-4415.
46. Leusch F.D.L., Chapman H.F., Korner W., Gooneratne S.R., Tremblay L.A. Efficacy of an advanced sewage treatment plant in southeast Queensland, Australia, to remove estrogenic chemicals. Environ Sci Technol 2005, 39(15):5781-5786.
47. Leusch F.D.L., van den Heuvel M.R., Chapman H.F., Gooneratne S.R., Eriksson A.M.E., Tremblay L.A. Development of methods for extraction and in vitro quantification of estrogenic and androgenic activity of wastewater samples. Comp Biochem Physiol C Toxicol Pharmacol 2006, 143(1):117-126.
48. Leusch F.D.L., De Jager C., Levi Y., Lim R., Puijker L., Sacher F., et al. Comparison of five in vitro bioassays to measure estrogenic activity in environmental waters. Environ Sci Technol 2010, 44(10):3853-3860.
49. Liu Z.H., Kanjo Y., Mizutani S. Removal mechanisms for endocrine disrupting compounds (EDCs) in wastewater treatment-physical means, biodegradation, and chemical advanced oxidation: a review. Sci Total Environ 2009, 407(2):731-748.
50. Liu Z.H., Kanjo Y., Mizutani S. A review of phytoestrogens: their occurrence and fate in the environment. Water Res 2010, 44(2):567-577.
51. Miege C., Choubert J.M., Ribeiro L., Eusebe M., Coquery M. Fate of pharmaceuticals and personal care products in wastewater treatment plants-conception of a database and first results. Environ Pollut 2009, 157(5):1721-1726.
52. Muller M., Rabenoelina F., Balaguer P., Patureau D., Lemenach K., Budzinski H., et al. Chemical and biological analysis of endocrine-disrupting hormones and estrogenic activity in an advanced sewage treatment plant. Environ Toxicol Chem 2008, 27(8):1649-1658.
53. Murk A.J., Legler J., van Lipzig M.M.H., Meerman J.H.N., Belfroid A.C., Spenkelink A., et al. Detection of estrogenic potency in wastewater and surface water with three in vitro bioassays. Environ Toxicol Chem 2002, 21(1):16-23.
54. Nadzialek S., Vanparys C., Van der Heiden E., Michaux C., Brose F., Scippo M.-L., et al. Understanding the gap between the estrogenicity of an effluent and its real impact into the wild. Sci Total Environ 2010, 408(4):812-821.
55. Nakada N., Nyunoya H., Nakamura M., Hara A., Iguchi T., Takada H. Identification of estrogenic compounds in wastewater effluent. Environ Toxicol Chem 2004, 23(12):2807-2815.
56. Nishihara T., Nishikawa J., Kanayama T., Dakeyama F., Saito K., Imagawa M., et al. Estrogenic activities of 517 chemicals by yeast two-hybrid assay. J Health Sci 2000, 46(4):282-298.
57. Pawlowski S., Ternes T., Bonerz M., Kluczka T., Van der Burg B., Nau H., et al. Combined in situ and in vitro assessment of the estrogenic activity of sewage and surface water samples. Toxicol Sci 2003, 75(1):57-65.
58. Pawlowski S., Ternes T.A., Bonerz M., Rastall A.C., Erdinger L., Braunbeck T. 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 2004, 18(1):129-138.
59. Petrovic M., Eljarrat E., de Alda M.J.L., Barcelo D. Endocrine disrupting compounds and other emerging contaminants in the environment: a survey on new monitoring strategies and occurrence data. Anal Bioanal Chem 2004, 378(3):549-562.
60. Pothitou P., Voutsa D. Endocrine disrupting compounds in municipal and industrial wastewater treatment plants in Northern Greece. Chemosphere 2008, 73(11):1716-1723.
61. Preuss T.G., Gurer-Orhan H., Meerman J., Ratte H.T. Some nonylphenol isomers show antiestrogenic potency in the MVLN cell assay. Toxicol in Vitro 2010, 24:129-134.
62. Purdom C.E., Hardiman P.A., Bye V.V.J., Eno N.C., Tyler C.R., Sumpter J.P. Estrogenic effects of effluents from sewage treatment works. Chem Ecol 1994, 8(4):275-285.
63. Routledge E.J., Sumpter J.P. Estrogenic activity of surfactants and some of their degradation products assessed using a recombinant yeast screen. Environ Toxicol Chem 1996, 15(3):241-248.
64. Routledge E.J., Sheahan D., Desbrow C., Brighty G.C., Waldock M., Sumpter J.P. Identification of estrogenic chemicals in STW effluent. 2. In vivo responses in trout and roach. Environ Sci Technol 1998, 32(11):1559-1565.
65. Rutishauser B.V., Pesonen M., Escher B.I., Ackermann G.E., Aerni H.R., Suter M.J.F., et al. Comparative analysis of estrogenic activity in sewage treatment plant effluents involving three in vitro assays and chemical analysis of steroids. Environ Toxicol Chem 2004, 23(4):857-864.
66. Sheahan D.A., Brighty G.C., Daniel M., Jobling S., Harries J.E., Hurst M.R., et al. Reduction in the estrogenic activity of a treated sewage effluent discharge to an English river as a result of a decrease in the concentration of industrially derived surfactants. Environ Toxicol Chem 2002, 21(3):515-519.
67. Snyder S.A., Villeneuve D.L., Snyder E.M., Giesy J.P. Identification and quantification of estrogen receptor agonists in wastewater effluents. Environ Sci Technol 2001, 35(18):3620-3625.
68. Sole M., de Alda M.J.L., Castillo M., Porte C., Ladegaard-Pedersen K., Barcelo D. Estrogenicity determination in sewage treatment plants and surface waters from the Catalonian area (NE Spain). Environ Sci Technol 2000, 34(24):5076-5083.
69. Sonneveld E., Riteco J.A.C., Jansen H.J., Pieterse B., Brouwer A., Schoonen W.G., et al. Comparison of in vitro and in vivo screening models for androgenic and estrogenic activities. Toxicol Sci 2006, 89(1):173-187.
70. Soto A.M., Lin T.M., Justicia H., Silvia R.M., Sonnenschein C. An "in culture" bioassay to assess the estrogenicity of xenobiotics (E-SCREEN). J Clean Technol Environ Toxicol Occup Med 1998, 7(3):331-343.
71. Sumpter J.P., Johnson A.C. 10th Anniversary Perspective: reflections on endocrine disruption in the aquatic environment: from known knowns to unknown unknowns (and many things in between). J Environ Monit 2008, 10(12):1476-1485.
72. Sumpter J.P., Johnson A.C., Williams R.J., Kortenkamp A., Scholze M. Modeling effects of mixtures of endocrine disrupting chemicals at the river catchment scale. Environ Sci Technol 2006, 40(17):5478-5489.
73. Svenson A., Allard A.S., Ek M. Removal of estrogenicity in Swedish municipal sewage treatment plants. Water Res 2003, 37(18):4433-4443.
74. Thomas K.V., Dye C., Schlabach M., Langford K.H. Source to sink tracking of selected human pharmaceuticals from two Oslo city hospitals and a wastewater treatment works. J Environ Monit 2007, 9(12):1410-1418.
75. Thorpe K.L., Gross-Sorokin M., Johnson I., Brighty G., Tyler C.R. An assessment of the model of concentration addition for predicting the estrogenic activity of chemical mixtures in wastewater treatment works effluents. Environ Health Perspect 2006, 114:90-97.
76. Van den Belt K., Berckmans P., Vangenechten C., Verheyen R., Witters H. Comparative study on the in vitro in vivo estrogenic potencies of 17 beta-estradiol, estrone, 17 alpha-ethynylestradiol and nonylphenol. Aquat Toxicol 2004, 66(2):183-195.
77. Van der Burg B., Winter R., Weimer M., Berckmans P., Suzuki G., Gijsbers L., et al. Optimization and prevalidation of the in vitro ER alpha CALUX method to test estrogenic and antiestrogenic activity of compounds. Reprod Toxicol 2010, 30(1):73-80.
78. Vermeirssen E.L.M., Korner O., Schonenberger R., Suter M.J.F., Burkhardt-Holm P. Characterization of environmental estrogens in river water using a three pronged approach: active and passive water sampling and the analysis of accumulated estrogens in the bile of caged fish. Environ Sci Technol 2005, 39(21):8191-8198.
79. Vethaak A.D., Lahr J., Schrap S.M., Belfroid A.C., Rijs G.B.J., Gerritsen A., et al. An integrated assessment of estrogenic contamination and biological effects in the aquatic environment of The Netherlands. Chemosphere 2005, 59:511-524.
80. Wehmas L.C., Cavallin J.E., Durhan E.J., Kahl M.D., Martinovic D., Mayasich J., et al. Screening Complex Effluents for Estrogenic Activity with the T47d-Kbluc Cell Bioassay: Assay Optimization and Comparison with in Vivo Responses in Fish. Environ Toxicol Chem 2011, 30(2):439-445.
81. Wilson V.S., Bobseine K., Gray L.E. Development and characterization of a cell line that stably expresses an estrogen-responsive luciferase reporter for the detection of estrogen receptor agonist and antagonists. Toxicol Sci 2004, 81(1):69-77.
82. Ye X., Guo X.S., Cui X., Zhang X., Zhang H., Wang M.K., et al. Occurrence and removal of endocrine-disrupting chemicals in wastewater treatment plants in the Three Gorges Reservoir area, Chongqing, China. J Environ Monit 2012, 14(8):2204-2211.