Investigation of the estrogenic risk to feral male brown trout (Salmo trutta) in the Shannon International River Basin District of Ireland

Ecotoxicology and Environmental Safety

Volumn 73, Issue 7, 2010, Pages 1658-1665

  Kelly, Miriam A ^a   Reid, Antoinette M ^a   Quinn Hosey, Kathryn M ^a   Fogarty, Andrew M ^a   Roche, James J ^a   Brougham, Concepta A ^a  

^a Athletic Rehabilitation Therapy Ireland   (Ireland)

Author keywords

Brown trout; Endocrine disruption; Sewage treatment plants; SIRBD of Ireland; Vitellogenin

Indexed keywords

ALKYLPHENOL; ENDOCRINE DISRUPTOR; ESTRADIOL; ESTROGEN RECEPTOR; PHTHALIC ACID; VITELLOGENIN;

CHEMICAL ANALYSIS; CHROMATOGRAPHY; DOSE-RESPONSE RELATIONSHIP; ENDOCRINE DISRUPTOR; ESTROGENIC COMPOUND; FISH; POLLUTION EXPOSURE; QUANTITATIVE ANALYSIS; RIVER POLLUTION; SEWAGE TREATMENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD ANALYSIS; BROWN TROUT; CHEMICAL COMPOSITION; CONTROLLED STUDY; ESTROGEN ACTIVITY; HERMAPHRODITISM; IRELAND; MALE; NONHUMAN; QUANTITATIVE ANALYSIS; RIVER BASIN; SEDIMENT; SEWAGE EFFLUENT; SEWAGE TREATMENT PLANT; WATER ANALYSIS;

ANALYSIS OF VARIANCE; ANIMALS; BODY CONSTITUTION; DISORDERS OF SEX DEVELOPMENT; ENDOCRINE DISRUPTORS; ESTROGENS; IRELAND; MALE; RIVERS; SEWAGE; TROUT; VITELLOGENESIS; WASTE DISPOSAL, FLUID; WATER POLLUTANTS, CHEMICAL;

IRELAND; SHANNON RIVER;

SALMO TRUTTA;

EID: 77957009471     PISSN: 01476513     EISSN: 10902414     Source Type: Journal    
DOI: 10.1016/j.ecoenv.2010.08.018     Document Type: Article

References (58)

1. Adam E., Decker D.G., Herbst A.L., Noller K.L., Tilley B.C., Townsend D.E. Vaginal and cervical cancers and other abnormalities associated with exposure in utero to diethylstilbestrol and related synthetic hormones. Cancer Res. 1977, 37:1249-1251.
2. Adewolu M.A., Akintola S.L., Jimoh A.A., Owodehinde F.G., Whenu O.O., Fakoya K.A. Environmental threats to the development of aquaculture in Lagos State, Nigeria. Eur. J. Sci. Res. 2009, 34:337-347.
3. Andersson C., Katsiadaki I., Lundstedt-Enkel K., Örberg J. Effects of 17α-ethynylestradiol on EROD activity, spiggin and vitellogenin in three-spined stickleback (Gasterosteus aculeatus). Aquat. Toxicol. 2007, 83:33-42.
4. Belfroid A.C., Van der Horst A., Vethaak A.D., Schäfer A.J., Rijs G.B.J., Wegener J., Colfino W.P. Analysis and occurrence of estrogenic hormones and their glucuronides in surface water and waste water in the Netherlands. Sci. Total Environ. 1999, 225:101-108.
5. Bjerregaard L.B., Korsgaard B., Bjerregaard P. Intersex in wild roach (Rutilus rutilus) from Danish sewage effluent-receiving streams. Ecotoxicol. Environ. Saf. 2006, 64:321-328.
6. Bjerregaard P., Hansen P.R., Larsen K.J., Erratico C., Korsgaard B., Holbech H. Vitellogenin as a biomarker for estrogenic effects in brown trout, Salmo trutta: laboratory and field investigations. Environ. Toxicol. Chem. 2009, 27:2387-2396.
7. Björklund K., Cousins A.P., Strömvall A.-M., Malmqvist P.-A. Phthalates and nonylphenols in urban runoff: occurrence, distribution and area emission factors. Sci. Total Environ. 2009, 407:4665-4672.
8. Bridges J.W., Bridges O. Integrated risk assessment and endocrine disrupters. Toxicology 2004, 205:11-15.
9. Bucheli T.D., Fent K. Induction of cytochrome P450 as a biomarker for environmental contamination in aquatic ecosystems. Environ. Sci. Technol. 1995, 25:201-268.
10. Clara M., Windhofer G., Hartl W., Braun B., Simon M., Gans O., Scheffknecht C., Chovanec A. Occurrence of phthalates in surface runoff, untreated and treated wastewater and fate during wastewater treatment. Chemosphere 2010, 78:1078-1084.
11. Crump D., Lean D., Trudeau V.L. Octylphenol and UV-B radiation alter larval development and hypothalamic gene expression in the Leopard frog (Rana pipiens). Environ. Health Perspect. 2002, 110:277-284.
12. Dargnat C., Teil M.J., Chevreuil M., Blanchard M. Phthalate removal throughout wastewater treatment plant. Case study of Marne Aval station (France). Sci. Total Environ. 2009, 407:1235-1244.
13. Desbrow C., Routledge E.J., Brighty G.C., Sumpter J.P., Waldock M. Identification of estrogenic chemicals in STW effluent. I. Chemical fractionation and in vitro biological screening. Environ. Sci. Technol. 1998, 32:1549-1558.
14. Diniz M.S., Peres I., Magalhães-Antoine I., Falla J., Pihan J.C. Estrogenic effects in crucian carp (Carassius carassius) exposed to treated sewage effluent. Ecotoxicol. Environ. Saf. 2005, 62:427-435.
15. EPA, 2008. Water Quality in Ireland 2004-2006. Available: (accessed August 2009.). http://www.epa.ie/downloads/pubs/water/waterqua/waterrep/waterqualityinIreland1.pdf.
16. Folmar L.C., Denslow N.D., Vijayasri R., Chow M., Crain A.D., Enblom J., Marcino J., Guillette L.J. Vitellogenin induction and reduced serum testosterone concentrations in feral male carp (Cyprinus carpio) captured near a major metropolitan sewage treatment plant. Environ. Health Perspect. 1996, 104:1096-1101.
17. Fromme H., Küchler T., Otto T., Pilz K., Müller J., Wenzel A. Occurrence of phthalates and bisphenol A and F in the environment. Water Res. 2002, 36:1429-1438.
18. García-Reyero N., Raldúa D., Quirós L., Llaveria G., Cerdà J., Barceló D., Grimalt J.O., Piña B. Use of vitellogenin mRNA as a biomarker for endocrine disruption in feral and cultured fish. Anal. Bioanal. Chem. 2004, 378:670-675.
19. Gimeno S., Komen H., Gerritsen A.G.M., Bowmer T. Feminisation of young males of the common carp, Cyprinus carpio, exposed to 4-tert-pentylphenol during sexual differentiation. Aquat. Toxicol. 1998, 43:77-92.
20. Gray, N.F., 2004. How nature deals with waste. In: Biology of wastewater treatment. Imperial College Press, UK, pp. 83-93.
21. Harries J.E., Shehan D.A., Jobling S., Matthiessen P., Neall P., Sumpter J.P., Tylir T., Zaman N. Estrogenic activity in five United Kingdom rivers detected by measurement of vitellogenesis in caged male trout. Environ. Toxicol. Chem. 1997, 16:534-542.
22. Herman R.L., Kincaid H.L. Pathological effects of orally administered estradiol to rainbow trout. Aquaculture 1988, 72(1-2):165-172.
23. Høgåsen H.R. The River Migration. In: Physiological Changes Associated with the Diadromous Migration of Salmonids 1998, Monogram Publishing, Canada, pp. 5-6.
24. Huggett D.B., Foran C.M., Brooks B.W., Weston J., Peterson B., Marsh K.E., La Point T.W., Schlenk D. Comparison of in vitro and in vivo bioassays for estrogenicity in effluent from North American municipal wastewater facilities. Toxicol. Sci. 2003, 72:77-83.
25. Jenkins J.A. Fish bioindicators of ecosystem condition at the Calcasieu Estuary. Louisiana: USGS Open-File Report 2004, 1323-1347.
26. Jobling S., Sheahan D., Osborne J.A., Matthiessen P., Sumpter J.P. Inhibition of testicular growth in rainbow trout (Oncorhynchus mykiss) exposed to estrogenic alkylphenolic chemicals. Environ. Toxicol. Chem. 1996, 15:194-202.
27. Jobling S., Nolan M., Tyler C.R., Brighty G., Sumpter J.P. Widespread sexual disruption in wild fish. Environ. Sci. Technol. 1998, 32:2498-2506.
28. Jobling S., Coey S., Whitmore J.G., Kime D.E., Van Look K.J.W., McAllister B.G., Beresford N., Henshaw A.C., Brighty G., Tyler C.R., Sumpter J.P. Wild intersex roach (Rutilus rutilus) have reduced fertility. Biol. Reprod. 2002, 67:515-524.
29. Jobling S., Williams R., Johnson A., Taylor A., Gross-Sorokin M., Nolan M., Tyler C.R., van Aerle R., Santos E., Brighty G. Predicted exposures to steroid estrogens in U.K. rivers correlate with widespread sexual disruption in wild fish populations. Environ. Health Perspect. 2006, 114:32-39.
30. Kinnberg K., Korsgaard B., Bjerregaard P., Jespersen A. Effects of nonylphenol and 17beta-estradiol on vitellogenin synthesis and testis morphology in male platyfish Xiphophorus maculates. J. Exp. Biol. 2000, 203:171-181.
31. Körner 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, 20:2142-2151.
32. Knudsen F.R., Pottinger T.G. Interaction of endocrine disrupting chemicals, singly and in combination, with estrogen-, androgen-, and corticosteroid-binding sites in rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 1999, 44:159-170.
33. Latini G., Del Vecchio A., Massaro M., Verrotti A., De Felice C. Phthalate exposure and male infertility. Toxicology 2006, 226:90-98.
34. Lin B.L., Hagino S., Kagoshima M., Iwamatsu T. The fragmented testis method: development and its advantages of a new quantitative evaluation technique for detection of testis-ova in male fish. Ecotoxicol. Environ. Saf. 2009, 72:286-292.
35. Matthiessen P., Allen Y., Bamber S., Craft J., Hurst M., Hutchinson T., Feist S., Katsiadaki I., Kirby M., Robinson C., Scott S., Thain J., Thomas K. The impact of oestrogenic and androgenic contamination on marine organisms in the United Kingdom-summary of the EDMAR programme. Mar. Environ. Res. 2002, 54:645-649.
36. Milnes M.R., Bermudez D.S., Bryan T.A., Edwards T.M., Gunderson M.P., Larkin I.L.V., Moore B.C., Guillette L.J. Contaminant-induced feminization and demasculinization of nonmammalian vertebrate males in aquatic environments. Environ. Res. 2006, 100:3-17.
37. Nolan M., Jobling S., Brighty G., Sumpter J.P., Tyler C.R. A histological description of intersexuality in the roach. J. Fish Biol. 2001, 58:160-176.
38. OECD, 2007. Phase-3 OECD 21-day fish screening assay validation report additional test substance studies. Available: (accessed May 2007.). http://www.oecd.org/dataoecd/62/36/38784404.pdf.
39. Park J.D., Habeebu S.S.M., Klaassen C.D. Testicular toxicity of di-(2-ethylhexyl) phthalate in young Sprague-Dawley rats. Toxicology 2002, 171:105-115.
40. Paxéus N. Organic pollutants in the effluents of large wastewater treatment plants in Sweden. Water Res. 1996, 30:1115-1122.
41. 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, 18:129-138.
42. Purdom C.E., Hardiman P.A., Bye V.J., Eno N.C., Tyler C.R., Sumpter J.P. Estrogenic effects of effluents from sewage treatment works. Chem. Ecol. 1994, 8:275-285.
43. Randak T., Zlabek V., Pulkrabova J., Kolarova J., Kroupova H., Siroka Z., Velisek J., Svobodova Z., Hajslova J. Effects of pollution on chub in the River Elbe, Czech Republic. Ecotoxicol. Environ. Saf. 2009, 72:737-746.
44. Reid A.M., Brougham C.A., Fogarty A.M., Roche J.J. Isocratic LC methods for the trace analysis of phthalates and 4-nonylphenol in varying types of landfill and adjacent run-offs. Toxicol. Environ. Chem. 2007, 89:399-410.
45. Rodgers-Gray T.P., Jobling S., Morris S., Kelly C., Kirby S., Janbakhsh A., Harries J.E., Waldock M.J., Sumpter J.P., Tyler C.R. Long-term temporal changes in the estrogenic composition of treated sewage effluent and its biological effects on fish. Environ. Sci. Technol. 2000, 34:1521-1528.
46. 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, 15:241-248.
47. 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, 32:1559-1565.
48. Soares A., Guieysse B., Jefferson B., Cartmell E., Lester J.N. Nonylphenol in the environment: a critical review on occurrence, fate, toxicity and treatment in wastewaters. Environ. Int. 2008, 34:1033-1049.
49. Streck G. Chemical and biological analysis of estrogenic, progestagenic and androgenic steroids in the environment. Trends Anal. Chem. 2009, 28:635-652.
50. Tarrant H., Mousakitis G., Wylde S., Tattersall N., Lyons A., Maloney M., Llewellyn N. Raised plasma vitellogenin in male wild brown trout (Salmo trutta) near a wastewater treatment plant in Ireland. Environ. Toxicol. Chem. 2008, 27:1773-1779.
51. Ternes T.A., Stumpf M., Mueller J., Haberer K., Wilken R.D., Servos M. Behavior and occurrence of estrogens in municipal sewage treatment plants-I. Investigations in Germany, Canada and Brazil. Sci. Total Environ. 1999, 225:81-90.
52. Tilghman A., Coquery M., Dulio V., Garric J. Integrated chemical and biomonitoring strategies for risk assessment of emerging substances. Trends Anal. Chem. 2009, 28:1-9.
53. Tyler C.R., Spary C., Gibson R., Santos E.M., Shears J., Hill E.M. Accounting for differences in estrogenic responses in rainbow trout (Oncorhynchus mykiss: Salmonidae) and roach (Rutilus rutilus: Cyprinidae) exposed to effluents from wastewater treatment works. Environ. Sci. Technol. 2005, 39:2599-2607.
54. US EPA, 2007. Wetlands: wetlands algae. Available: (accessed March 2009.). http://www.epa.gov/OWOW/wetlands/wqual/algae.html.
55. Vermeire T., Munns W.R., Sekizawa J., Suter G., Van der Kraak G. An assessment of integrated risk assessment. Hum. Ecol. Risk Assessment 2007, 13:339-354.
56. WHO, 2002. Damstra, T., Barlow, S., Bergman, A., Kavlock, R., Van Der Kraak, G. Global assessment of the state-of-the-science of endocrine disruptors. Available: 〈http://www.who.int/ipcs/publications/new_issues/endocrine_disruptors/en/〉 (accessed October 2006.).
57. Ying G.G., Kookana R.S., Kumar A., Mortimer M. Occurrence and implications of estrogens and xenoestrogens in sewage effluents and receiving waters from South East Queensland. Sci. Total Environ. 2009, 407:5147-5155.
58. Yokota H., Seki M., Maeda M., Oshima Y., Tadokoro H., Honjo T., Kobayashi K. Life-cycle toxicity of 4-nonylphenol to medaka (Oryzias latipes). Environ. Toxicol. Chem. 2001, 20:2552-2560.