Biological effects and bioaccumulation of steroidal and phenolic endocrine disrupting chemicals in high-back crucian carp exposed to wastewater treatment plant effluents

Environmental Pollution

Volumn 162, Issue , 2012, Pages 325-331

  Liu, Jingliang ^a   Wang, Renmin ^a   Huang, Bin ^a   Lin, Chan ^a   Zhou, Jiali ^a   Pan, Xuejun ^a  

^a KUNMING UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Bioaccumulation; Endocrine disrupting chemicals; High back crucian carp; Vitellogenin; Wastewater treatment plant

Indexed keywords

ADVERSE EFFECT; BIOCONCENTRATION FACTOR; BIOLOGICAL EFFECTS; CRUCIAN CARP; ENDOCRINE DISRUPTING CHEMICALS; FISH MUSCLES; GONADOSOMATIC INDEX; HEPATOSOMATIC INDICES; PHENOLIC ENDOCRINE; PLASMA VITELLOGENIN; TIME-DEPENDENT; VITELLOGENIN; WASTEWATER TREATMENT PLANT; WASTEWATER TREATMENT PLANT EFFLUENT; WASTEWATER TREATMENT PLANTS; WWTP EFFLUENT;

BIOACCUMULATION; BIOCHEMISTRY; BIOLOGICAL WATER TREATMENT; CHEMICALS; CHEMICALS REMOVAL (WATER TREATMENT); FISH; LIPIDS; MUSCLE; PHENOLS; RECLAMATION; SEWAGE PUMPING PLANTS; WASTEWATER; WASTEWATER TREATMENT; WATER TREATMENT PLANTS;

EFFLUENTS;

ENDOCRINE DISRUPTOR; LAKE WATER; PHENOL DERIVATIVE; STEROID; VITELLOGENIN;

BIOACCUMULATION; EFFLUENT; ENDOCRINE DISRUPTOR; PHENOL; PHENOLIC COMPOUND; STEROID; WASTEWATER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTHROPOMETRIC PARAMETERS; ARTICLE; BIOACCUMULATION; CHINA; CONTROLLED STUDY; EFFLUENT; GOLDFISH; GONADOSOMATIC INDEX; HEPATOSOMATIC INDEX; LIVER METABOLISM; MUSCLE; NONHUMAN; WASTE WATER TREATMENT PLANT; WATER SAMPLING;

ANIMALS; CARPS; ENDOCRINE DISRUPTORS; PHENOLS; SEWAGE; STEROIDS; VITELLOGENINS; WATER POLLUTANTS, CHEMICAL;

CARASSIUS; CARASSIUS AURATUS;

EID: 83655169773     PISSN: 02697491     EISSN: 18736424     Source Type: Journal    
DOI: 10.1016/j.envpol.2011.11.036     Document Type: Article

References (72)

1. H.R. Aerni, B. Kobler, B.V. Rutishauser, F.E. Wettstein, R. Fischer, W. Giger, A. Hungerbuhler, M.D. Marazuela, A. Peter, R. Schonenberger, A.C. Vogeli, M.J.F. Suter, and R.I.L. Eggen Combined biological and chemical assessment of estrogenic activities in wastewater treatment plant effluents Analytical and Bioanalytical Chemistry 378 2004 688 696 (Pubitemid 40877760)
2. S. Aguayo, M.J. Munoz, A. de la Torre, J. Roset, E. de la Pena, and M. Carballo Identification of organic compounds and ecotoxicological assessment of sewage treatment plants (STP) effluents Environmental Science & Technology 328 2004 69 81 (Pubitemid 38798188)
3. M. Ahel, and W. Giger Partitioning of alkylphenols and alkylphenol polyethoxylates between water and organic solvents Chemosphere 26 1993 1471 1478 (Pubitemid 23169115)
4. A.M. Al-Ansari, A. Saleem, L.E. Kimpe, J.P. Sherry, M.E. McMaster, V.L. Trudeau, and J.M. Blais Bioaccumulation of the pharmaceutical 17 alpha-ethinylestradiol in shorthead redhorse suckers (Moxostoma macrolepidotum) from the St. Clair River, Canada Environmental Pollution 158 2010 2566 2571
5. J. Albaiges, A. Farran, M. Soler, A. Gallifa, and P. Martin Accumulation and distribution of biogenic and pollutant hydrocarbons, PCBs and DDT in tissues of Western Mediterranean fishes Marine Environmental Research 22 1987 1 18 (Pubitemid 17116980)
6. J.A. Arnot, and F.A.P.C. Gobas A review of bioconcentration factor (BCF) and bioaccumulation factor (BAF) assessments for organic chemicals in aquatic organisms Environmental Reviews 14 2006 257 297 (Pubitemid 46276957)
7. M.L. Ballesteros, M. Gonzalez, D.A. Wunderlin, M.A. Bistoni, and K.S.B. Miglioranza Uptake, tissue distribution and metabolism of the insecticide endosulfan in Jenynsia multidentata (Anablepidae, Cyprinodontiformes) Environmental Pollution 159 2011 1709 1714
8. L.B. Barber, K.E. Lee, D.L. Swackhamer, and H.L. Schoenfuss 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 Aquatic Toxicology 82 2007 36 46 (Pubitemid 46441499)
9. A. Belfroid, M. van Velzen, B. van der Horst, and D. Vethaak Occurrence of bisphenol A in surface water and uptake in fish: evaluation of field measurements Chemosphere 49 2002 97 103 (Pubitemid 34976604)
10. G. Bertanza, R. Pedrazzani, M. Dal Grande, M. Papa, V. Zambarda, C. Montani, N. Steimberg, G. Mazzoleni, and D. Di Lorenzo Effect of biological and chemical oxidation on the removal of estrogenic compounds (NP and BPA) from wastewater: an integrated assessment procedure Water Research 45 2011 2473 2484
11. M.A. Blackburn, S.J. Kirby, and M.J. Waldock Concentrations of alkyphenol polyethoxylates entering UK estuaries Marine Pollution Bulletin 38 1999 109 118 (Pubitemid 29092451)
12. O. Braga, G.A. Smythe, A.I. Schafer, and A.J. Feitz Fate of steroid estrogens in Australian inland and coastal wastewater treatment plants Environmental Science & Technology 39 2005 3351 3358 (Pubitemid 40638279)
13. J.V. Brian, C.A. Harris, M. Scholze, A. Kortenkamp, P. Booy, M. Lamoree, G. Pojana, N. Jonkers, A. Marcomini, and J.P. Sumpter Evidence of estrogenic mixture effects on the reproductive performance of fish Environmental Science & Technology 41 2007 337 344 (Pubitemid 46047863)
14. M. Carballa, F. Omil, J.M. Lema, M. Llompart, C. Garcia-Jares, I. Rodriguez, M. Gomez, and T. Ternes Behavior of pharmaceuticals, cosmetics and hormones in a sewage treatment plant Water Research 38 2004 2918 2926 (Pubitemid 38829583)
15. C.F. Chang, and M.R. Chen Fluctuation in sex steroids and sexbinding protein during the development and annual cycle of the male common carp (Cyprinus carpio) Comparative Biochemistry and Physiology. Part A 97 1990 565 568
16. C. Desbrow, E.J. Routledge, G.C. Brighty, J.P. Sumpter, and M. Waldock Identification of estrogenic chemicals in STW effluent. 1. Chemical fractionation and in vitro biological screening Environmental Science & Technology 32 1998 1549 1558 (Pubitemid 28265342)
17. M.S. Diniz, I. Peres, I. Magalhaes-Antoine, J. Falla, and J.C. Pihan Estrogenic effects in crucian carp (Carassius carassius) exposed to treated sewage effluent Ecotoxicology and Environmental Safety 62 2005 427 435 (Pubitemid 41427147)
18. M.S. Diniz, I. Peres, and J.C. Pihan Comparative study of the estrogenic responses of mirror carp (Cyprinus carpio) exposed to treated municipal sewage effluent (Lisbon) during two periods in different seasons Science of the Total Environment 349 2005 129 139 (Pubitemid 41421070)
19. K.A. Fenlon, A.C. Johnson, C.R. Tyler, and E.M. Hill Gas-liquid chromatography-tandem mass spectrometry methodology for the quantitation of estrogenic contaminants in bile of fish exposed to wastewater treatment works effluents and from wild populations Journal of Chromatography A 1217 2010 112 118
20. A.L. Filby, J.A. Shears, B.E. Drage, J.H. Churchley, and C.R. Tyler Effects of advanced treatments of wastewater effluents on estrogenic and reproductive health impacts in fish Environmental Science & Technology 44 2010 4348 4354
21. L.C. Folmar, N.D. Denslow, K. Kroll, E.F. Orlando, J. Enblom, J. Marcino, C. Metcalfe, and L.J. Guillette Altered serum sex steroids and vitellogenin induction in walleye (Stizostedion vitreum) collected near a metropolitan sewage treatment plant Archives of Environmental Contamination and Toxicology 40 2001 392 398 (Pubitemid 32488560)
22. R. Gibson, M.D. Smith, C.J. Spary, C.R. Tyler, and E.M. Hill Mixtures of estrogenic contaminants in bile of fish exposed to wastewater treatment works effluents Environmental Science & Technology 39 2005 2461 2471 (Pubitemid 40570267)
23. J.P. Giesy, E.M. Snyder, K.M. Nichols, S.A. Snyder, S.A. Villalobos, P.D. Jones, and S.D. Fitzgerald Examination of reproductive endpoints in goldfish (Carassius auratus) exposed in situ to municipal sewage treatment plant effluent discharges in Michigan, USA Environmental Toxicology and Chemistry 22 2003 2416 2431 (Pubitemid 37163171)
24. B. Huang, X.J. Pan, X. Wan, J.L. Liu, S.M. Zhao, P. Hu, and F.R. Li Simultaneous determination of steroid endocrine disrupting chemicals in water by solid phase extraction-derivatization-gas chromatographic-mass spectrometry Chinese Journal of Analytical Chemistry 39 2011 449 454
25. T.H. Hutchinson, G.T. Ankley, H. Segner, and C.R. Tyler Screening and testing for endocrine disruption in fish - biomarkers as "signposts," not "traffic lights," in risk assessment Environmental Health Perspectives 114 2006 106 114
26. S. Jobling, M. Nolan, C.R. Tyler, G. Brighty, and J.P. Sumpter Widespread sexual disruption in wild fish Environmental Science & Technology 32 1998 2498 2506 (Pubitemid 28420276)
27. A.C. Johnson, H.R. Aerni, A. Gerritsen, M. Gibert, W. Giger, K. Hylland, M. Jurgens, T. Nakari, A. Pickering, M.J.F. Suter, A. Svenson, and F.E. Wettstein Comparing steroid estrogen, and nonylphenol content across a range of European sewage plants with different treatment and management practices Water Research 39 2005 47 58 (Pubitemid 40017754)
28. D.E. Kime, J.P. Nash, and A.P. Scott Vitellogenesis as a biomarker of reproductive disruption by xenobiotics Aquaculture 177 1999 345 352 (Pubitemid 29305970)
29. K.M. Lai, M.D. Scrimshaw, and J.N. Lester Prediction of the bioaccumulation factors and body burden of natural and synthetic estrogens in aquatic organisms in the river systems Science of the Total Environment 289 2002 159 168 (Pubitemid 34311792)
30. A. Lange, G.C. Paull, P.B. Hamilton, T. Iguchi, and C.R. Tyler Implications of persistent exposure to treated wastewater effluent for breeding in wild roach (Rutilus rutilus) populations Environmental Science & Technology 45 2011 1673 1679
31. D.G.J. Larsson, M. Adolfsson-Erici, J. Parkkonen, M. Pettersson, A.H. Berg, P.E. Olsson, and L. Forlin Ethinyloestradiol - an undesired fish contraceptive? Aquatic Toxicology 45 1999 91 97 (Pubitemid 29112824)
32. K.E. Liney, S. Jobling, J.A. Shears, P. Simpson, and C.R. Tyler Assessing the sensitivity of different life stages for sexual disruption in roach (Rutilus rutilus) exposed to effluents from wastewater treatment works Environmental Health Perspectives 113 2005 1299 1307 (Pubitemid 41511983)
33. J.L. Liu, X.J. Pan, B. Huang, K. Fang, Y. Wang, and J.P. Gao An improved method for simultaneous analysis of steroid and phenolic endocrine disrupting chemicals in biological samples International Journal of Environmental Analytical Chemistry 2011 10.1080/03067319.2010.510604
34. J.L. Liu, R.M. Wang, B. Huang, C. Lin, Y. Wang, and X.J. Pan Distribution and bioaccumulation of steroidal and phenolic endocrine disrupting chemicals in wild fish species from Dianchi Lake, China Environmental Pollution 159 2011 2815 2822
35. C.M. Lye, C.L.J. Frid, M.E. Gill, D.W. Cooper, and D.M. Jones Estrogenic alkylphenols in fish tissues, sediments, and waters from the UK Tyne and Tees estuaries Environmental Science & Technology 33 1999 1009 1014 (Pubitemid 29169165)
36. D. Mackay, and A. Fraser Bioaccumulation of persistent organic chemicals: mechanisms and models Environmental Pollution 110 2000 375 391 (Pubitemid 30624195)
37. L. Mita, M. Bianco, E. Viggiano, F. Zollo, U. Bencivenga, V. Sica, G. Monaco, M. Portaccio, N. Diano, A. Colonna, M. Lepore, P. Canciglia, and D.G. Mita Bisphenol A content in fish caught in two different sites of the Tyrrhenian Sea (Italy) Chemosphere 82 2011 405 410
38. C.L. Mitchelmore, and C.P. Rice Correlations of nonylphenol-ethoxylates and nonylphenol with biomarkers of reproductive function in carp (Cyprinus carpio) from the Cuyahoga River Science of the Total Environment 371 2006 391 401 (Pubitemid 44755086)
39. N. Nakada, T. Tanishima, H. Shinohara, K. Kiri, and H. Takada Pharmaceutical chemicals and endocrine disrupters in municipal wastewater in Tokyo and their removal during activated sludge treatment Water Research 40 2006 3297 3303 (Pubitemid 44332504)
40. P.M. Ondarza, M. Gonzalez, G. Fillmann, and K.S.B. Miglioranza Polybrominated diphenyl ethers and organochlorine compound levels in brown trout (Salmo trutta) from Andean Patagonia, Argentina Chemosphere 83 2011 1597 1602
41. M. Petrovic, M. Sole, M.J.L. de Alda, and D. Barcelo Endocrine disruptors in sewage treatment plants, receiving river waters, and sediments: Integration of chemical analysis and biological effects on feral carp Environmental Toxicology and Chemistry 21 2002 2146 2156
42. P. Pothitou, and D. Voutsa Endocrine disrupting compounds in municipal and industrial wastewater treatment plants in Northern Greece Chemosphere 73 2008 1716 1723
43. C.E. Purdom, P.A. Hardiman, V.J. Bye, N.C. Eno, C. Tyler, and J.P. Sumpter Estrogenic effects of effluents from sewage treatment works Chemistry and Ecology 8 1994 275 285
44. T.P. Rodgers-Gray, S. Jobling, C. Kelly, S. Morris, G. Brighty, M.J. Waldock, J.P. Sumpter, and C.R. Tyler Exposure of juvenile roach (Rutilus rutilus) to treated sewage effluent induces dose-dependent and persistent disruption in gonadal duct development Environmental Science & Technology 35 2001 462 470 (Pubitemid 32125951)
45. T.P. Rodgers-Gray, S. Jobling, S. Morris, C. Kelly, S. Kirby, A. Janbakhsh, J.E. Harries, M.J. Waldock, J.P. Sumpter, and C.R. Tyler Long-term temporal changes in the estrogenic composition of treated sewage effluent and its biological effects on fish Environmental Science & Technology 34 2000 1521 1528 (Pubitemid 30217479)
46. E.J. Routledge, D. Sheahan, C. Desbrow, G.C. Brighty, M. Waldock, and J.P. Sumpter Identification of estrogenic chemicals in STW effluent. 2. In vivo responses in trout and roach Environmental Science & Technology 32 1998 1559 1565 (Pubitemid 28265343)
47. V. Samaras, N. Thomaidis, A. Stasinakis, and T. Lekkas An analytical method for the simultaneous trace determination of acidic pharmaceuticals and phenolic endocrine disrupting chemicals in wastewater and sewage sludge by gas chromatography-mass spectrometry Analytical and Bioanalytical Chemistry 399 2011 2549 2561
48. S. Schubert, A. Peter, R. Burki, R. Schonenberger, M.J.F. Suter, H. Segner, and P. Burkhardt-Holm Sensitivity of brown trout reproduction to long-term estrogenic exposure Aquatic Toxicology 90 2008 65 72
49. P.B. Singh, and V. Singh Bioaccumulation of hexachlorocyclohexane, dichlorodiphenyltrichloroethane, and estradiol-17 beta in catfish and carp during the pre-monsoon season in India Fish Physiology and Biochemistry 34 2008 25 36 (Pubitemid 351330652)
50. M. Sole, D. Raldua, D. Barcelo, and C. Porte Long-term exposure effects in vitellogenin, sex hormones, and biotransformation enzymes in female carp in relation to a sewage treatment works Ecotoxicology and Environmental Safety 56 2003 373 380 (Pubitemid 37324096)
51. A. Sousa, R. Schonenberger, N. Jonkers, M.J.F. Suter, S. Tanabe, and C.M. Barroso Chemical and biological characterization of estrogenicity in effluents from WWTPs in Ria de Aveiro (NW Portugal) Archives of Environmental Contamination and Toxicology 58 2010 1 8
52. A.S. Stasinakis, G. Gatidou, D. Mamais, N.S. Thomaidis, and T.D. Lekkas Occurrence and fate of endocrine disrupters in Greek sewage treatment plants Water Research 42 2008 1796 1804 (Pubitemid 351380618)
53. Q.F. Sun, S.B. Deng, J. Huang, G. Shen, and G. Yu Contributors to estrogenic activity in wastewater from a large wastewater treatment plant in Beijing, China Environmental Toxicology and Pharmacology 25 2008 20 26 (Pubitemid 350198997)
54. Y. Suzuki, and T. Maruyama Fate of natural estrogens in batch mixing experiments using municipal sewage and activated sludge Water Research 40 2006 1061 1069 (Pubitemid 43287917)
55. A. Svenson, A.S. Allard, and M. Ek Removal of estrogenicity in Swedish municipal sewage treatment plants Water Research 37 2003 4433 4443 (Pubitemid 37152432)
56. B.L.L. Tan, D.W. Hawker, J.F. Mueller, F.D.L. Leusch, L.A. Tremblay, and H.F. Chapman Modelling of the fate of selected endocrine disruptors in a municipal wastewater treatment plant in South East Queensland, Australia Chemosphere 69 2007 644 654 (Pubitemid 47331587)
57. B.L.L. Tan, D.W. Hawker, J.F. Muller, F.D.L. Leusch, L.A. Tremblay, and H.F. Chapman Comprehensive study of endocrine disrupting compounds using grab and passive sampling at selected wastewater treatment plants in South East Queensland, Australia Environment International 33 2007 654 669 (Pubitemid 46776881)
58. K.L. Thorpe, R. Benstead, P. Eccles, G. Maack, T. Williams, and C.R. Tyler A practicable laboratory flow-through exposure system for assessing the health effects of effluents in fish Aquatic Toxicology 88 2008 164 172
59. K.L. Thorpe, R.I. Cummings, T.H. Hutchinson, M. Scholze, G. Brighty, J.P. Sumpter, and C.R. Tyler Relative potencies and combination effects of steroidal estrogens in fish Environmental Science & Technology 37 2003 1142 1149 (Pubitemid 36504981)
60. K.L. Thorpe, G. Maack, R. Benstead, and C.R. Tyler Estrogenic wastewater treatment works effluents reduce egg production in fish Environmental Science & Technology 43 2009 2976 2982
61. T. Tsuda, A. Takino, M. Kojima, H. Harada, K. Muraki, and M. Tsuji 4-Nonylphenols and 4- tert-octylphenol in water and fish from rivers flowing into Lake Biwa Chemosphere 41 2000 757 762
62. C.R. Tyler, C. Spary, R. Gibson, E.M. Santos, J. Shears, and E.M. Hill Accounting for differences in estrogenic responses in rainbow trout (Oncorhynchus mykiss: Salmonidae) and roach (Rutilus rutilus: Cyprinidae) exposed to effluents from wastewater treatment works Environmental Science & Technology 39 2005 2599 2607 (Pubitemid 40570285)
63. A.D. Vethaak, J. Lahr, S.M. Schrap, A.C. Belfroid, G.B.J. Rijs, A. Gerritsen, J. de Boer, A.S. Bulder, G.C.M. Grinwis, R.V. Kuiper, J. Legler, T.A.J. Murk, W. Peijnenburg, H.J.M. Verhaar, and P. de Voogt An integrated assessment of estrogenic contamination and biological effects in the aquatic environment of The Netherlands Chemosphere 59 2005 511 524
64. B. Wang, X. Wan, S.M. Zhao, Y. Wang, F. Yu, and X.J. Pan Analysis of six phenolic endocrine disrupting chemicals in surface water and sediment Chromatographia 74 2011 297 306
65. G. West Methods of assessing ovarian development in fishes - a review Australian Journal of Marine and Freshwater Research 41 1990 199 222
66. J. Xiao, T.M. Zou, Y.B. Chen, L. Chen, S.J. Liu, M. Tao, C. Zhang, R.R. Zhao, Y. Zhou, Y. Long, C.P. You, J.P. Yan, and Y. Liu Coexistence of diploid, triploid and tetraploid crucian carp (Carassius auratus) in natural waters BMC Genetics 12 2011 20
67. G.G. Ying, R.S. Kookana, A. Kumar, and M. Mortimer Occurrence and implications of estrogens and xenoestrogens in sewage effluents and receiving waters from South East Queensland Science of the Total Environment 407 2009 5147 5155
68. R.G. Zan Studies of sex chromosomes and C-banding karyotypes of two forms of Carassius auratus in Kunming Lake Acta Genetica Sinica 9 1982 32 39
69. J.M. Zha, Z.J. Wang, N. Wang, and C. Ingersoll Histological alternation and vitellogenin induction in adult rare minnow (Gobiocypris rarus) after exposure to ethynylestradiol and nonylphenol Chemosphere 66 2007 488 495 (Pubitemid 44791419)
70. H. Zhang, F.X. Kong, Y. Yu, X.L. Shi, M. Zhang, and H.E. Tian Assessing the combination effects of environmental estrogens in fish Ecotoxicology 19 2010 1476 1486
71. H.D. Zhou, X. Huang, X.L. Wang, X.H. Zhi, C.D. Yang, X.H. Wen, Q.H. Wang, H. Tsuno, and H. Tanaka Behaviour of selected endocrine-disrupting chemicals in three sewage treatment plants of Beijing, China Environmental Monitoring and Assessment 161 2010 107 121
72. L. Zhou, Y. Wang, and J.F. Gui Genetic evidence for gonochoristic reproduction in gynogenetic silver crucian carp (Carassius auratus gibelio bloch) as revealed by RAPD assays Journal of Molecular Evolution 51 2000 498 506