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Feminisation of Fish Environmental Project No. 729 2002 Miljøprojekt Feminisation of fish The effect of estrogenic compounds and their fate in sewage treatment plants and nature Lisette Bachmann Christiansen University of Southern Denmark Magrethe Winther-Nielsen and Christian Helweg DHI - Water & Environment The Danish Environmental Protection Agency will, when opportunity offers, publish reports and contributions relating to environmental research and development projects financed via the Danish EPA. Please note that publication does not signify that the contents of the reports necessarily reflect the views of the Danish EPA. The reports are, however, published because the Danish EPA finds that the studies represent a valuable contribution to the debate on environmental policy in Denmark. Contents CONTENTS 3 PREFACE 7 1 SUMMARY (ENGLISH) 9 2 RESUMÉ (DANSK) 21 3 REPRODUCTIVE DISTURBANCES IN FERAL AND CAGED FISH FROM SEWAGE EFFLUENT AFFECTED AQUATIC ENVIRONMENTS 33 3.1 THE FRESHWATER ENVIRONMENT 33 3.1.1 Feral fish 33 3.1.2 Cage experiments and other controlled sewage effluent exposure studies 37 3.2 THE MARINE ENVIRONMENT 40 4 QUANTIFICATION OF THE ESTROGENICITY OF SEWAGE EFFLUENT USING IN VITRO ASSAYS AND THE TIE APPROACH. 43 5 OCCURRENCE OF ESTROGENS AND XENOESTROGENS IN SEWAGE EFFLUENT AND OCCURRENCE AND FATE IN THE AQUATIC ENVIRONMENT 47 5.1 ESTROGENS 47 5.1.1 Occurrence in sewage effluent 47 5.1.2 Occurrence in surface water 54 5.1.3 Fate and behaviour in the environment 54 5.2 ALKYLPHENOLS 56 5.2.1 Concentrations in sewage effluent 56 5.2.2 Concentrations in surface water 57 5.2.3 Fate and behaviour in the environment 58 5.3 BISPHENOL A 59 5.3.1 Concentrations in sewage effluent 59 5.3.2 Concentrations in surface water 60 5.3.3 Fate and behaviour in the environment 60 6 ESTABLISHED DOSE-RESPONSE RELATIONS BETWEEN THE ESTROGENS/XENOESTROGENS AND THEIR FEMINISING POTENTIAL. 63 6.1 17β-ESTRADIOL 63 6.2 ESTRONE 64 6.3 ESTRIOL 65 6.4 ETHINYLESTRADIOL 65 6.5 ALKYLPHENOLS 66 6.5.1 Nonylphenol 66 6.5.2 Octylphenol 67 6.5.3 Bisphenol A 68 6.5.4 Phthalates 68 3 7 RELATION BETWEEN ENVIRONMENTAL LEVELS OF ESTROGENS/XENOESTROGENS AND KNOWN EFFECT CONCENTRATIONS. 71 8 CONSEQUENCES OF FEMINISATION ON THE REPRODUCTIVE SUCCESS/FERTILITY OF MALE FISH. 75 9 EFFECTS OF (XENO-)ESTROGENS ON THE REPRODUCTIVE SUCCESS/FERTILITY OF FEMALE FISH. 77 10 POTENTIAL SOURCES OF ESTROGENS AND XENOESTROGENS 79 10.1 ESTROGENS 79 10.1.1 Men 79 10.1.2 Women 79 10.1.3 Metabolism 81 10.1.4 Hormone therapy 82 10.2 RELEASE OF ESTROGENS 83 10.2.1 Other sources 85 10.3 ALKYLPHENOLS 85 10.3.1 Nonylphenolethoxylates 85 10.3.2 Other derivatives of alkylphenols 87 10.4 RELEASE OF ALKYLPHENOLS 88 10.4.1 Release from processing/formulation 88 10.4.2 Release from use 88 10.4.3 Release from disposal 90 10.5 BISPHENOL A 90 10.5.1 Polycarbonate 91 10.5.2 Epoxy resins 91 10.5.3 Phenoplast resins 91 10.5.4 Can coating manufacture 91 10.5.5 Thermal paper 91 10.5.6 PVC 92 10.5.7 Other uses 92 10.5.8 Brake fluid 92 10.5.9 Tyre manufacture 92 10.5.10 Fire retardant 92 10.6 RELEASE OF BISPHENOL A 92 10.6.1 Release from processing 93 10.6.2 Release during use 93 10.6.3 Release from disposal 94 10.6.4 Release from recycling 94 11 FATE IN MUNICIPAL SEWAGE TREATMENT PLANTS 97 11.1 ESTROGENS 97 11.1.1 Biodegradation in sludge of STPs 97 11.1.2 Sorption to sludge particles 100 11.1.3 Fate in STPs 100 11.2 ALKYLPHENOLS 103 11.2.1 Biodegradation in sludge of STPs 103 11.2.2 Sorption to sludge particles 105 11.2.3 Fate in STPs 105 11.3 BISPHENOL A 110 11.3.1 Biodegradation in sludge of STPs 110 11.3.2 Sorption to sludge particles 110 4 11.3.3 Fate in STPs 110 12 INFLUENCE OF THE TYPE OF TREATMENT PLANTS ON THE REMOVAL EFFICIENCY OF ESTROGENS AND XENOESTROGENS 113 12.1 ESTROGENS 113 12.2 ALKYLPHENOLS 115 12.3 BISPHENOL A 116 13 ADVANCED TREATMENT PROCESSES 117 14 POSSIBLE NON-SEWAGE EFFLUENT RELATED SOURCES OF ESTROGENS TO THE AQUATIC ENVIRONMENT 121 15 CONCLUSIONS (ENGLISH) 123 16 KONKLUSION (DANSK) 129 17 REFERENCE LIST 135 18 APPENDIX A 157 5 6 Preface This report aims to give an overview of the existing knowledge on selected endocrine disrupting compounds including their fate in sewage treatment works, their occurrence in the aquatic environment and their endocrine disrupting effects on fish. Both effects observed among wild species of fish in their natural environments and effects which can be induced by controlled exposure of fish to the compounds in question will be described. Studies from a number of European countries during recent years have demonstrated that feminisation of fish in their aquatic environment in many cases can be ascribed to the natural steroids, 17β-estradiol and estrone, and the synthetic estrogen, ethinylestradiol, used in contraceptives and all being excreted with domestic sewage by women. The main focus of this report will therefore be on these three hormones. Additional information will be given in lesser detail on the less potent natural estrogen estriol and on alkylphenols and bisphenol A which are known estrogenic chemicals which can be detected in sewage effluent. This report will therefore concentrate on endocrine disruption via estrogenic mechanisms, though it should be born in mind that endocrine disruption is a larger subject which also covers i.e. antiestrogenic, androgenic and antiandrogenic effects. The latter are, however, outside the scope of this report. 7 1 Summary (English) Feminisation of male fish in freshwater and marine environments During the past ten years feminisation of male fish has been detected in several European countries and in USA and Japan (1-12). These cases are examples of disturbances of the male reproductive system which are believed to be consequences of endocrine disruption caused by female hormones, estrogens, or chemicals mimicking estrogens present in the aquatic environment. The majority of estrogens are believed to reach the aquatic environment by sewage effluent. In Europe feminisation of male fish exposed to sewage effluent has been seen in England (1), Sweden (3), Norway (4), Germany (5), The Netherlands (6), France (7;13), Spain (8;14) and Denmark (2). Further, the observations of feminisation in wild populations of fish have been made in a range of different species including the freshwater species roach (1), gudgeon (15), carp (8;14), bream (5;6), chub (7;13) and brown trout (2) and the saltwater species flounder(16-22), eelpout (18) and two species of sand gobies (23). Thus, these kinds of disruption of the male reproductive system have both been found in freshwater and marine environments though most cases have been reported from freshwater environments. Controlled exposure of fish to sewage effluent i.e. in cage experiments have further added proof to the estrogenic nature of the sewage effluent and estrogens or estrogenic chemicals as causative agents of the disruptions. The signs of feminisation in male fish are the production of a female yolk protein which is known only to be produced as a response to an estrogen exposure, and the occurrence of intersex – an abnormal form of hermaphroditism. Males with the intersex condition have early stages of egg cells in the testis and in some cases they have also developed the female duct which leads eggs to the oviduct. Feminisation has been found in varying degrees among individual fish from mild to very severe disturbances of the male reproductive system. England is the country in which feminisation of fish has been most widely detected and where the most severe degrees of feminisation have been seen, both compared to countries inside and outside Europe. The feminisation of fish which has been detected in Denmark does not, however, differ markedly from the extent found in other countries. In these a lower occurrence and severity of feminisation compared to England have generally been seen though feminisation has been detected at several of the examined sites. There are, however, also sites where the fish populations appear unaffected. It should be pointed out that short-term exposure experiments, where fish are exposed to sewage effluent for a short period of time, do not always give a correct estimate of the risk for wild populations of fish which live their entire life in the stream or river. It has been demonstrated that increasing the exposure time for sewage effluent lowers the concentration of sewage effluent needed to cause feminisation of fish (24). 9 Estrogenicity of sewage effluent Support to the theory of estrogenic compounds in sewage effluent as the cause of the feminising effects, which have been found among male fish, has also come from a number of studies using cell culture assays designed to detect estrogenic activity. These have demonstrated the estrogenicity of sewage effluent from a number of countries (England, Germany, The Netherlands, Belgium, China, Korea and USA) and quantified the estrogenic potential in relation to the potency of 17ß-estradiol (6;25-33). Further, chemical analysis of the composition of sewage effluent and determinations of concentrations of estrogens and estrogenic compounds in the effluent have in a large number of cases demonstrated the natural estrogens, 17ß-estradiol, estrone and the synthetic estrogen, ethinylestradiol used in contraceptives as likely candidates for the observed disturbances in fish species from the sewage effluent receiving rivers. In single cases alkylphenols were also suggested as possible causative agents (34).
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