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ESTROGENIC ACTIVITY IN FIVE UNITED KINGDOM RIVERS DETECTED BY MEASUREMENT OF VITELLOGENESIS IN CAGED MALE TROUT

1997; Wiley; Volume: 16; Issue: 3 Linguagem: Inglês

10.1897/1551-5028(1997)016 2.3.co;2

1552-8618

Jule E. Harries, David A. Sheahan, Susan Jobling, Peter Matthiessen, Paula Neall, John P. Sumpter, Tina Tylor, Nicholas Zaman,

Fish Biology and Ecology Studies

Environmental Toxicology and ChemistryVolume 16, Issue 3 p. 534-542 Environmental Toxicology Estrogenic activity in five United Kingdom rivers detected by measurement of vitellogenesis in caged male trout Jule E. Harries, Jule E. Harries Department of Biology and Biochemistry Brunel University, Uxbridge, Middlesex UB8 3PH UKSearch for more papers by this authorDavid A. Sheahan, David A. Sheahan Ministry of Agriculture, Fisheries, and Food, Directorate of Fisheries Research, Fisheries Laboratory, Remembrance Avenue, Burnham-on-Crouch, Essex CM0 8HA, UKSearch for more papers by this authorSusan Jobling, Susan Jobling Department of Biology and Biochemistry Brunel University, Uxbridge, Middlesex UB8 3PH UKSearch for more papers by this authorPeter Matthiessen, Corresponding Author Peter Matthiessen Ministry of Agriculture, Fisheries, and Food, Directorate of Fisheries Research, Fisheries Laboratory, Remembrance Avenue, Burnham-on-Crouch, Essex CM0 8HA, UKMinistry of Agriculture, Fisheries, and Food, Directorate of Fisheries Research, Fisheries Laboratory, Remembrance Avenue, Burnham-on-Crouch, Essex CM0 8HA, UKSearch for more papers by this authorPaula Neall, Paula Neall Ministry of Agriculture, Fisheries, and Food, Directorate of Fisheries Research, Fisheries Laboratory, Remembrance Avenue, Burnham-on-Crouch, Essex CM0 8HA, UKSearch for more papers by this authorJohn P. Sumpter, John P. Sumpter Department of Biology and Biochemistry Brunel University, Uxbridge, Middlesex UB8 3PH UKSearch for more papers by this authorTina Tylor, Tina Tylor Ministry of Agriculture, Fisheries, and Food, Directorate of Fisheries Research, Fisheries Laboratory, Remembrance Avenue, Burnham-on-Crouch, Essex CM0 8HA, UKSearch for more papers by this authorNicholas Zaman, Nicholas Zaman Ministry of Agriculture, Fisheries, and Food, Directorate of Fisheries Research, Fisheries Laboratory, Remembrance Avenue, Burnham-on-Crouch, Essex CM0 8HA, UKSearch for more papers by this author Jule E. Harries, Jule E. Harries Department of Biology and Biochemistry Brunel University, Uxbridge, Middlesex UB8 3PH UKSearch for more papers by this authorDavid A. Sheahan, David A. Sheahan Ministry of Agriculture, Fisheries, and Food, Directorate of Fisheries Research, Fisheries Laboratory, Remembrance Avenue, Burnham-on-Crouch, Essex CM0 8HA, UKSearch for more papers by this authorSusan Jobling, Susan Jobling Department of Biology and Biochemistry Brunel University, Uxbridge, Middlesex UB8 3PH UKSearch for more papers by this authorPeter Matthiessen, Corresponding Author Peter Matthiessen Ministry of Agriculture, Fisheries, and Food, Directorate of Fisheries Research, Fisheries Laboratory, Remembrance Avenue, Burnham-on-Crouch, Essex CM0 8HA, UKMinistry of Agriculture, Fisheries, and Food, Directorate of Fisheries Research, Fisheries Laboratory, Remembrance Avenue, Burnham-on-Crouch, Essex CM0 8HA, UKSearch for more papers by this authorPaula Neall, Paula Neall Ministry of Agriculture, Fisheries, and Food, Directorate of Fisheries Research, Fisheries Laboratory, Remembrance Avenue, Burnham-on-Crouch, Essex CM0 8HA, UKSearch for more papers by this authorJohn P. Sumpter, John P. Sumpter Department of Biology and Biochemistry Brunel University, Uxbridge, Middlesex UB8 3PH UKSearch for more papers by this authorTina Tylor, Tina Tylor Ministry of Agriculture, Fisheries, and Food, Directorate of Fisheries Research, Fisheries Laboratory, Remembrance Avenue, Burnham-on-Crouch, Essex CM0 8HA, UKSearch for more papers by this authorNicholas Zaman, Nicholas Zaman Ministry of Agriculture, Fisheries, and Food, Directorate of Fisheries Research, Fisheries Laboratory, Remembrance Avenue, Burnham-on-Crouch, Essex CM0 8HA, UKSearch for more papers by this author First published: 26 October 2009 https://doi.org/10.1002/etc.5620160320Citations: 441Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Abstract It was recently demonstrated that most, if not all, effluents of sewage-treatment works (STWs) in the United Kingdom are estrogenic to fish. As many STWs discharge into rivers, it is possible that some stretches of rivers downstream of where the effluent enters might also be estrogenic. To assess this possibility, the induction of vitellogenin synthesis in caged male trout placed at various distances downstream of the effluent entry point was used as a biomarker of estrogen exposure. Individual discharges into five rivers in England were studied. In four cases, fish placed in the neat effluent, or close to where it entered a river, showed very marked and rapid increases in their plasma vitellogenin concentrations, demonstrating that the effluent was estrogenic. In two of these four cases, none of the downstream sites were estrogenic, whereas in one of the four, fish placed at a site 1.5 km downstream did respond by synthesizing appreciable amounts of vitellogenin, although sites further downstream were not estrogenic. The situation in the fourth river was quite different; not only was the effluent extremely estrogenic (a maximum vitellogenin response in the mg/ml range was attained), but so were all the other study sites on the river, the last of which was 5 km downstream of where the effluent entered. This particular river receives trade effluent from wool-scouring mills, which contains much higher concentrations of alkylphenolic chemicals than any of the other discharges studied. It is suggested that these chemicals probably account for the estrogenic activity of this river. The final (fifth) river showed no estrogenic activity, not even in the neat effluent. This discharge comes from a very small STW, which receives no trade waste, and one or both of these factors may account for why the effluent (and hence the river) was not estrogenic. REFERENCES 1 J. A. McLachlan, ed, 1980. Estrogens in the Environment. Elsevier, North Holland, New York, NY USA. 2 J. A. McLachlan, ed, 1985. Estrogens in the Environment II— Influences on Development. Elsevier, North Holland, New York, NY, USA. 3 T. Colborn and C. Clement, eds, 1992. Chemically Induced Alterations in Sexual and Functional Development: The Wildlife–Human Connection, Vol. 21—Advances in Modern Environmental Toxicology. Princeton Scientific Publishing, Princeton, NJ, USA. 4 Fry, D. M. and C. K. Toone, 1981. DDT-induced feminization of gull embryos. Science 213: 922– 924. 5 Guillette, Jr., L. J., T. S. Gross, G. R. Masson, J. M. Matter, H. F. Percival and A. R. Woodward, 1994. Developmental abnormalities of the gonad and abnormal sex hormone concentrations in juvenile alligators from contaminated and control lakes in Florida. Environ. Health Perspect. 102: 680– 688. 6 Carlsen, E., A. Giwercman, N. Kieding and N. Skakkebæk, 1992. Evidence for decreasing quality of sperm during the past 50 years. BMJ 305: 609– 613. 7 Hileman, B., 1994. Environmental estrogens linked to reproductive abnormalities, cancer. Chem. Eng. News Jan 31: 19– 23. 8 Raloff, J., 1994. The gender benders: Are environmental "hormones" emasculating wildlife? Sci. News 145: 24– 27. 9 Raloff, J., 1994. That feminine touch: Are men suffering from prenatal or childhood exposures to "hormonal" toxicants? Sci. News 145: 56– 58. 10 Stone, R., 1994. Environmental estrogens stir debate. Science 265: 308– 310. 11 Soto, A. M., K. L. Chung and C. Sonnenschein, 1994. The pesticides endosulfan, toxaphene and dieldrin have estrogenic effects on human estrogen-sensitive cells. Environ. Health Perspect. 102: 380– 385. 12 Kelce, W. R., C. R. Stone, S. C. Laws, L. E. Gray, J. A. Kemppainen and E. M. Wilson, 1995. Persistent DDT metabolite p,p'-DDE is a potent androgen receptor antagonist. Nature 375: 581– 585. 13 Safe, S. H., 1995. Environmental and dietary estrogens and human health: Is there a problem? Environ. Health Perspect. 103: 346– 351. 14 Ginsberg, J., S. Okolo, G. Prelevic and P. Hardiman, 1994. Residence in the London area and sperm density. Lancet 343: 230. 15 Sharpe, R. M. and N. E. Skakkebæk, 1993. Are oestrogens involved in falling sperm counts and disorders of the male reproductive tract? Lancet 341: 1392– 1395. 16 Soto, A. M., H. Justicia, J. W. Wray and C. Sonnenschein, 1991. p-Nonylphenol: An estrogenic xenobiotic released from "modified" polystyrene. Environ. Health Perspect. 92: 167– 173. 17 Krishnan, A. V., P. Stathis, S. F. Permuth, L. Tokes and D. Feldman, 1993. Bisphenol-A: An estrogenic substance is released from polycarbonate flasks during autoclaving. Endocrinology 132: 2279– 2286. 18 Hertz, R., 1985. The estrogen problem—Retrospect and prospect. In J. A. McLachlan, ed., Estrogens in the Environment II—Influences on Development. Elsevier, North Holland, New York, NY, USA, pp. 1– 11. 19 Soto, A. M., T.-M. Lin, H. Justicia, R. M. Silvia and C. Sonnenschein, 1992. An "in culture" bioassay to assess the estrogenicity of xenobiotics (E-Screen). In T. Colburn and C. Clement, eds., Chemically Induced Alterations in Sexual and Functional Development: The Wildlife–Human Connection, Vol. 21—Ad-vances in Modern Environmental Toxicology. Princeton Scientific Publishing, Princeton, NJ, USA, pp. 295– 309. 20 Jobling, S. and J. P. Sumpter, 1993. Detergent components in sewage effluent are weakly oestrogenic to fish: An in vitro study using rainbow trout (Oncorhynchus mykiss) hepatocytes. Aquat. Toxicol. 27: 361– 372. 21 White, R., S. Jobling, S. A. Hoare, J. P. Sumpter and M. G. Parker, 1994. Environmentally persistent alkylphenolic compounds are estrogenic. Endocrinology 135: 175– 182. 22 Routledge, E. J. and J. P. Sumpter, 1996. Estrogenic activity of surfactants and some of their degradation products assessed using a recombinant yeast screen. Environ. Toxicol. Chem. 15: 241– 248. 23 Jobling, S., T. Reynolds, R. White, M. G. Parker and J. P. Sumpter, 1995. A variety of environmentally persistent chemicals, including some phthalate plasticizers, are weakly estrogenic. Environ. Health Perspect. 103: 582– 587. 24 Purdom, C. E., P. A. Hardiman, V. J. Bye, N. C. Eno, C. R. Tyler and J. P. Sumpter, 1994. Estrogenic effects of effluents from sewage treatment works. Chem. Ecol. 8: 275– 285. 25 Harries, J. E., D. A. Sheahan, S. Jobling, P. Matthiessen, P. Neall, E. J. Routledge, R. Rycroft, J. P. Sumpter and T. Tylor, 1996. A survey of estrogenic activity in U.K. inland waters. Environ. Toxicol. Chem. 15: 1993– 2002. 26 Le Guellec, K., K. Lawless, Y. Valotaire, M. Kress and M. Tenniswood, 1988. Vitellogenin gene expression in male rainbow trout (Salmo gairdneri). Gen. Comp. Endocrinol. 71: 359– 371. 27 Sheahan, D. A., D. Bucke, P. Matthiessen, J. P. Sumpter, M. F. Kirby, P. Neall and M. Waldock, 1994. The effects of low levels of 17α-ethynylestradiol upon plasma vitellogenin levels in male and female rainbow trout Oncorhynchus mykiss (Walbaum) held at two acclimation temperatures. In R. Müller and R. Lloyd, eds., Sublethal and Chronic Effects of Pollutants on Freshwater Fish. Fishing News Books, Oxford, UK, pp. 99– 112. 28 Bagenal, T., 1978. Methods for Assessment of Fish Production in Fresh Waters, 3rd ed. IBP Handbook 3. Blackwell, Oxford, UK. 29 Sumpter, J. P., 1985. The purification, radioimmunoassay and plasma levels of vitellogenin from the rainbow trout Salmo gairdneri. In B. Lofts and W. H. Holmes, eds., Trends in Comparative Endocrinology. Hong Kong University Press, Hong Kong, pp. 355– 357. 30 Blackburn, M. A. and M. J. Waldock, 1995. Concentrations of alkylphenols in rivers and estuaries in England and Wales. Water Res. 29: 1623– 1629. 31 Van Bohemen, C. G., J. E. D. Lambert, H. J. T. Goos and P. G. W. J. van Oordt, 1982. Estrone and estradiol participation during exogenous vitellogenesis in the female rainbow trout, Salmo gairdneri. Gen. Comp. Endocrinol. 44: 94– 107. 32 Scott, A. P. and J. P. Sumpter, 1983. A comparison of the female reproductive cycles of autumn-spawning and winter-spawning strains of rainbow trout (Salmo gairdneri Richardson). Gen. Comp. Endocrinol. 52: 79– 85. 33 Harries, J. E., S. Jobling, P. Matthiessen, D. A. Sheahan and J. P. Sumpter, 1995. Effects of trace organics on fish—Phase II. PECD 7/7/384 and 7/7/381. Report FR/D 0022. U.K. Department of the Environment, Foundation for Water Research, Marlow, UK. 34 Rathner, M. and M. Sonneborn, 1979. Biologisch wirksame östrogene in trink- und abwasser. Forum Städte-Hygiene 30: 45– 49. 35 Waggott, A., 1981. Trace organic substances in the River Lee. In W. J. Cooper, ed., Chemistry in Water Reuse. Ann Arbor Science, Ann Arbor, MI, USA, pp. 55– 99. 36 Aherne, G. W., J. English and V. Marks, 1985. The role of immunoassay in the analysis of microcontaminants in water samples. Ecotoxicol. Environ. Saf. 9: 79– 83. 37 Jobling, S., D. Sheahan, J. A. Osborne, P. Matthiessen and J. P. Sumpter, 1996. Inhibition of testicular growth in rainbow trout (Oncorhynchus mykiss) exposed to estrogenic alkylphenolic chemicals. Environ. Toxicol. Chem. 15: 194– 202. 38 Richtler, H. J. and J. Knaut, 1988. World prospects for surfactants. Proceedings, Second World Surfactant Congress, Paris, France, May 24–27, pp. 3– 58. 39 Ahel, M., W. Giger and C. Schaffner, 1994. Behaviour of alkylphenol polyethoxylate surfactants in the aquatic environment, 2—Occurrence and transformation in rivers. Water Res. 28: 1143– 1152. 40 Naylor, C. G., 1992. Environmental fate of alkylphenol ethoxylates. Proceedings, Soap/Cosmetics/Chem. Specialties USA, August 27–31, p. 72. 41 Clark, L. B., R. T. Rosen, T. G. Hartman, J. B. Louis, I. H. Suffet, R. L. Leppincott and J. D. Rosen, 1992. Determination of alkylphenol ethoxylates and their acetic acid derivatives in drinking water by particle beam liquid chromatography/mass spectrometry. Int. J. Environ. Anal. Chem. 47: 167– 180. 42 U.K. Department of the Environment. 1993. Uses, fate and entry to the environment of nonylphenol ethoxylates. Final report. London, UK. 43 Shaw, T., 1994. Agricultural chemicals in raw wool and the wool textile industry. J. Instit. Water Environ. Manage. 8: 287– 290. 44 Singh, P. B. and D. E. Kime, 1995. Impact of γ-hexachlorocyclohexane on the in vitro production of steroids from endogenous and exogenous precursors in the spermiating roach, Rutilus rutilus. Aquat. Toxicol. 31: 231– 240. 45 Walsh, G. E. and L. H. Bahner, 1980. Toxicity of textile mill effluents to freshwater and estuarine algae, crustaceans and fishes. Environ. Pollut. 21: 169– 179. 46 Ahel, M., J. McEvoy and W. Giger, 1993. Bioaccumulation of the lipophilic metabolites of nonionic surfactants in freshwater organisms. Environ. Pollut. 79: 243– 248. 47 McLeese, D. W., V. Zitko, D. B. Sergeant, L. Burridge and C. D. Metcalfe, 1981. Lethality and accumulation of alklyphenols in aquatic fauna. Chemosphere 10: 723– 730. 48 Sumpter, J. P. and S. Jobling, 1995. Vitellogenesis as a bio-marker for estrogenic contamination of the aquatic environment. Environ. Health Perspect. 103 (Suppl 7): 173– 178. 49 Copeland, P. A., J. P. Sumpter, T. K. Walker and M. Croft, 1986. Vitellogenin levels in male and female rainbow trout, Salmo gairdneri Richardson, at various stages of the reproductive cycle. Comp. Biochem. Physiol. B 83: 487– 493. 50 Elliott, J. A. K., N. R. Bromage and C. Whitehead, 1979. Effects of estradiol-17β on serum calcium and vitellogenin levels in rainbow trout. J. Endocrinol. 83: 54P– 55P. 51 Herman, R. L. and H. L. Kincaid, 1988. Pathological effects of orally administered estradiol to rainbow trout. Aquaculture 72: 165– 172. 52 Carragher, J. F. and J. P. Sumpter, 1991. The mobilization of calcium from calcified tissues of rainbow trout (Oncorhynchus mykiss) induced to synthesize vitellogenin. Comp. Biochem. Physiol. A 99: 169– 172. Citing Literature Volume16, Issue3March 1997Pages 534-542 ReferencesRelatedInformation