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Susan Jobling,¹ Richard Williams,² Andrew Johnson,² Ayesha Taylor,³ Melanie Gross-Sorokin,⁴ Monique Nolan,⁵ Charles R. Tyler,⁶ Ronny van Aerle,⁶ Eduarda Santos,⁶ and Geoff Brighty⁴

¹Beyond The Basics Ltd, Burnham, Bucks, United Kingdom, and Institute for the Environment, Brunel University, Uxbridge, Middlesex, United Kingdom; ²Centre for Ecology and Hydrology, Wallingford, Oxon, United Kingdom; ³Environment Agency, National Fisheries Technical Team, Warrington, ⁵Environment Agency, National Fish Health Laboratory, Brampton, Cambridgeshire, United Kingdom; ⁶Environmental and Molecular Fish Biology Group, The Hatherly Laboratories, School of Biological and Chemical Sciences, University of Exeter, Devon, United Kingdom

Abstract
Steroidal estrogens, originating principally from human excretion, are likely to play a major role in causing widespread endocrine disruption in wild populations of the roach (Rutilus rutilus) , a common cyprinid fish, in rivers contaminated by treated sewage effluents. Given the extent of this problem, risk assessment models are needed to predict the location and severity of endocrine disruption in river catchments and to identify areas where regulation of sewage discharges to remove these contaminants is necessary. In this study we attempted to correlate the extent of endocrine disruption in roach in British rivers, with their predicted exposure to steroid estrogens derived from the human population. The predictions of steroid estrogen exposure at each river site were determined by combining the modeled concentrations of the individual steroid estrogens [17β-estradiol (E₂) , estrone (E₁) , and 17-ethinylestradiol (EE₂) ] in each sewage effluent with their predicted dilution in the immediate receiving water. This model was applied to 45 sites on 39 rivers throughout the United Kingdom. Each site studied was then categorized as either high, medium, or low "risk" on the basis of the assumed additive potency of the three steroid estrogens calculated from data derived from published studies in various cyprinid fish species. We sampled 1,438 wild roach from the predicted high-, medium-, and low-risk river sites and examined them for evidence and severity of endocrine disruption. Both the incidence and the severity of intersex in wild roach were significantly correlated with the predicted concentrations of the natural estrogens (E₁ and E₂) and the synthetic contraceptive pill estrogen (EE₂) present. Predicted steroid estrogen exposure was, however, less well correlated with the plasma vitellogenin concentration measured in the same fish. Moreover, we found no correlation between any of the end points measured in the roach and the proportion of industrial effluents entering the rivers we studied. Overall, our results provide further and substantive evidence to support the hypothesis that steroidal estrogens play a major role in causing intersex in wild freshwater fish in rivers in the United Kingdom and clearly show that the location and severity of these endocrine-disrupting effects can be predicted. Key words: disruption, endocrine, estrogen, estrone, estradiol, ethinylestradiol, intersex, roach, vitellogenin. Environ Health Perspect 114(suppl 1) : 32-39 (2006) . doi:10.1289/ehp.8050 available via http://dx.doi.org/ [Online 21 October 2005]

This article is part of the monograph "The Ecological Relevance of Chemically Induced Endocrine Disruption in Wildlife."

Address correspondence to S. Jobling, Institute for the Environment, Brunel University, Uxbridge, Middlesex, U.K. Telephone: 44 793 2066351. E-mail: drsusanjobling@beyondthebasic.co.uk

We thank all the Environment Agency's fisheries officers involved in the project for their sterling efforts in collecting the samples of roach. We also thank the staff at the National Fisheries Laboratory for receiving and processing the samples.

This project was funded by the Environment Agency. S.J. was funded by the Environment Agency and by European Chemical Industry Council Long Range Initiative project number BTBL-0409. R.vA. was sponsored by the European Union (EVK1-CT-2002-00129) , and E.S. was funded by the Biotechnology and Biological Science Research Council (S15001) .

S.J. is employed by Beyond the Basics Ltd, an idependent consultancy. The remaining authors declare they have no competing financial interests.

Received 31 January 2005 ; accepted 22 August 2005.