Estrogen mediated effects in the Sydney rock oyster, Saccostrea glomerata, following field exposures to sewage effluent containing estrogenic compounds and activity

Aquatic Toxicology

Volumn 120-121, Issue , 2012, Pages 99-108

  Andrew Priestley, M N ^a   O'Connor, W A ^c   Dunstan, R H ^b   Van Zwieten, L ^d   Tyler, T ^d   Kumar, A ^e   MacFarlane, G R ^b  

^a INTECSEA   (Canada)

^b UNIVERSITY OF NEWCASTLE   (Australia)

^c Industry and Investment NSW   (Australia)

^d Wollongbar Primary Industries Institute   (Australia)

^e CSIRO   (Australia)

Author keywords

Female gonadal development; Oocyte area; Oyster; Vitellogenin gene; Vitellogenin protein

Indexed keywords

4 NONYLPHENOL; 4 TERT OCTYLPHENOL; 4,4' ISOPROPYLIDENEDIPHENOL; ESTRADIOL; ESTRIOL; ESTROGEN DERIVATIVE; ESTRONE; ETHINYLESTRADIOL; SEA WATER; VITELLOGENIN;

BIOMONITORING; EFFLUENT; ESTROGENIC COMPOUND; MOLLUSC; PROTEIN; SEWAGE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUSTRALIA; BIOLOGICAL MONITORING; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; ESTROGEN ACTIVITY; FEMALE; FRACTIONATION; GENE EXPRESSION; GONAD DEVELOPMENT; MALE; NONHUMAN; OYSTER; PRIORITY JOURNAL; SACCOSTREA GLOMERATA; SEWAGE EFFLUENT; SEXUAL DEVELOPMENT;

ANIMALS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL MONITORING; ESTROGENS; FEMALE; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GONADS; MALE; NEW SOUTH WALES; OOCYTES; OSTREIDAE; REAL-TIME POLYMERASE CHAIN REACTION; SEWAGE; SEX RATIO; TIME FACTORS; VITELLOGENINS; WATER POLLUTANTS, CHEMICAL;

AUSTRALIA; NEW SOUTH WALES; NEWCASTLE [NEW SOUTH WALES];

AYTHYA AMERICANA; OSTREIDAE; SACCOSTREA GLOMERATA;

EID: 84861723172     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2012.03.020     Document Type: Article

References (59)

1. Allinson M., Shiraishi F., Salzman A., Allinson G. In vitro and immunological assessment of the estrogenic activity and concentrations of 17β-estradiol, estrone, and ethinyl estradiol in treated effluent from 45 wastewater treatment plants in Victoria, Australia. Archives of Environment Contamination and Toxicology 2010, 58(3):576-586.
2. Al-Rifai J.H., Gabelish C.L., Schafer A.I. Occurrence of pharmaceutically active and nonsteroidal estrogenic compounds in three different wastewater recycling schemes in Australia. Chemosphere 2007, 69(5):803-815.
3. Anderson K., Burnell A., Roiko A., Andrew M., O'Connor W., Elizur A. Development of a method for identifying elevated vitellogenin gene expression in the Sydney rock oyster (Saccostrea glomerata) as an indicator of endocrine disruption on the Sunshine Coast. Ecological Management & Restoration 2010, 11(2):143-146.
4. Andrew M., Dunstan R., O'Connor W., Van Zwieten L., Nixon B., MacFarlane G. Effects of 4-nonylphenol and 17α-ethynylestradiol exposure in the Sydney rock oyster, Saccostrea glomerata, Vitellogenin induction and gonadal development. Aquatic Toxicology 2008, 88:39-47.
5. Andrew M., O'Connor W., Dunstan H., MacFarlane G. Exposure to 17α-ethynylestradiol causes dose and temporally dependent changes in intersex, females and vitellogenin production in the Sydney rock oyster. Ecotoxicology 2010, 19:1440-1451.
6. Andrew-Priestley, M., 2011. Molluscan biomonitor for quantification and impact assessment of estrogenic and metallic contaminants in Australian marine ecosystems. PhD Thesis, Discipline of Biological Sciences, University of Newcastle.
7. Asif M. Hermphroditism and sex reversal in the four common oviparous species of oysters from the coast of Karachi. Hydrobiologia 1979, 66:49-55.
8. Baronti C., Curini R., D'Ascenzo G., Di Corcia A., Gentili A., Samperi R. Monitoring natural and synthetic estrogens at activated sludge sewage treatment plants and in a receiving river water. Environmental Science and Technology 2000, 34:5059-5066.
9. Blackburn M., Waldock M. Concentrations of alkyphenols in rivers and estuaries in England and Wales. Water Research 1995, 29:1623-1629.
10. Blaise C., Gagné F., Pellerin J., Hansen P. Determination of vitellogenin-like properties in Mya arenaria hemolymph (Saguenay Fjord, Canada): a potential bio-marker for endocrine disruption. Environmental Toxicology and Chemistry 1999, 4:455-465.
11. Blaise C., Gagné F., Salazar M., Salazar S., Trottier S., Hansen P. Experimentally induced feminisation of freshwater mussels after long-term exposure to a municipal effluent. Fresenius Environment Bulletin 2003, 12:865-870.
12. Boutet I., Morage D., Marinovic L., Obreque J., Chavez-Crooker Characterization of reproduction-specific genes in a marine bivalve mollusc: influence of maturation stage and sex on mRNA expression. Gene 2008, 407:130-138.
13. Braga O., Smythe G.A., Schafer A.I., Feitz A. Fate of steroid estrogens in Australian inland and coastal wastewater treatment plants. Environmental Science and Technology 2005, 39:3351-3358.
14. Chesman B., Langston W. Intersex in the clam Scrobicularia plana: a sign of endocrine disruption in estuaries?. Biology Letters 2006, 2:420-422.
15. Ciocan C., Cubero-Leon E., Puinean A., Hill E., Minier C., Osada M., Fenlon K., Rotchell J. Effects of estrogen exposure in mussels, Mytilus edulis, at different stages of gametogenesis. Environmental Pollution 2010, 158(9):2977-2984.
16. Denslow N. Vitellogenin as a biomarker of exposure for estrogens or estrogen mimics. Ecotoxicology 1999, 8:385-398.
17. Desbrow C., Routledge E.J., Brighty G.C., Sumpter J.P., Waldock M. Identification of estrogenic chemicals in STW effluent. 1. Chemical fractionation and in vitro biological screening. Environmental Science and Technology 1998, 32:1549-1558.
18. Desbrow C., Routledge E., Sheehan D., Waldock M., Sumpter J. The Identification and Assessment of Oestrogenic Substances in Sewage Treatment Works Effluents 1996, UK Environment Agency, Bristol.
19. Dinamani P. Reproductive cycle and gonadial changes in the New Zealand rock oyster Crassostrea glomerata. New Zealand Journal of Marine and Freshwater Research 1974, 8(1):39-65.
20. EPA, 1997. Special report on environmental endocrine disruption: an effects assessment and analysis. Office of Research and Development, Washington, DC. EPA/630/R-96/012.
21. Gagné F., André C., Blaise C. Increased vitellogenin gene expression in the mussel Elliptio complanata exposed to estradiol-17β. Fresenius Environment Bulletin 2005, 14:861-866.
22. Gagné F., Blaise C., Salazar M., Salazar S., Hansen P. Evaluation of estrogenic effects of municipal effluents to the freshwater mussel Elliptio complanata. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 2001, 128:213-225.
23. Gagné F., Bouchard B., André C., Farcy E., Fournier M. Evidence of feminization in wild Elliptio complanata mussels in the receiving waters downstream of a municipal effluent outfall. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 2011, 153:99-106.
24. Glamore, W., Hawker, K., Miller, B., 2007. Burwood Ocean outfall monitoring and modelling 2007. Technical Report 2007/11 for Hunter Water. The University of New South Wales, Water Research Laboratory, Manly Vale, NSW, Australia.
25. Hemmer M., Bowman C., Hemmer B., Friedman S., Marcovich D., Kroll K., Denslow N. Vitellogenin mRNA regulation and plasma clearance in male sheepshead minnows (Cyprinodon variegatus) after cessation of exposure to 17β-estradiol and p-nonylphenol. Aquatic Toxicology 2002, 58(1-2):99-112.
26. Huggett R., Kimerle R., Mehrle P.J., Bergman H., Dickson K., Fava J., McCarthy J., Parrish R., Dorn P., McFarland V., Lavis G. Introduction. BIOMARKERS: Biochemical, Physiological and Histological Markers of Anthropogenic Stress 1992, Lewis Publishers, USA. R. Huggett, R. Kimerle, P.J. Mehrle, H. Bergman (Eds.).
27. Ingrand V., Herry G., Beausse J., Roubin M.R. Analysis of steroid hormones in effluents of wastewater treatment plants by liquid chromatography-tandem mass spectrometry. Journal of Chromatography A 2003, 1020(1):99-104.
28. Langston W., Burt G., Chesman B. Feminisation of male clams Scrobicularia plana from estuaries in Southwest UK and its induction by endocrine-disrupting chemicals. Marine Ecology Progress Series 2007, 333:173-184.
29. Langston W., Burt G., Chesman B., Vane C. Partitioning, bioavailability and effects of oestrogens and xeno-oestrogens in the aquatic environment. Journal of the Marine Biological Association of the United Kingdom 2005, 85:1-31.
30. Lee B., Peart T. Determination of 4-NP in effluent and sludge from sewage treatment plants. Analytical Chemistry 1995, 67:1967-1980.
31. Legler J., Dennekamp M., Vethaak A., Brouwer A., Koeman J., Van der Burg B., Murk A. Detection of estrogenic activity in sediment-associated compounds using in vitro reporter gene assays. Science of the Total Environment 2002, 293:69-83.
32. Leusch F.D., Chapman H.F., Korner W., Gooneratne S.R., Tremblay L.A. Efficacy of an advanced sewage treatment plant in Southeast Queensland, Australia, to remove estrogenic chemicals. Environmental Science and Technology 2005, 39:5781-5786.
33. Li C., Tyler T., Van Zwieten L., Lee N., Kennedy I. Optimisation of analytical method for estrogen in surface water and primary risk assessment in South Creek. International Journal of Water 2007, 3(4):334-346.
34. Li Q., Osada M., Suzuki T., Mori K. Changes in vitellin during oogenesis and effect of estradiol 17b in the Pacific oyster, Crassostrea gigas. Invertebrate Reproduction and Development 1998, 33:87-93.
35. Matsui S., Takigami H., Matsuda T., Taniguchi N., Adachi J., Kawami H., Shimzu Y. Estrogen and estrogen mimics contamination in water and the role of sewage treatment. Water Science and Technology 2000, 42:173-179.
36. Matsumoto T., Nakamura A., Mori K., Kayano T. Molecular characterisation of a cDNA encoding putative vitellogenin from the Pacific oyster Crassostrea gigas. Zoological Science 2003, 20:37-42.
37. Mispagel C., Allinson G., Allison M., Shiraishi F., Nishikawa M., Moore M. Observations on the estrogenic activity and concentration of 17b-estradiol in the discharges of 12 wastewater treatment plants in Southern Australia. Archives of Environment Contamination and Toxicology 2009, 56:631-637.
38. Mori K., Muramatsu T., Nakamura Y. Effect of steroid on oyster. III. Sex reversal from male to female in Crassostrea gigas by estradiol-17B. Bulletin of the Japanese Society of Scientific Fisheries 1969, 35(11):1072-1076.
39. Nice H., Morritt D., Crane M., Thorndyke M. Long-term and transgenerational effects of nonylphenol exposure at a key stage in the development of Crassostrea gigas. Possible endocrine disruption?. Marine Ecology Progress Series 2003, 256:293-300.
40. Pampanin D., Marangon I., Volpato E., Campesan G., Nasci C. Stress biomarkers and alkali-labile phosphate level in mussels (Mytilus galloprovincialis) collected in the urban area of Venice (Venice Lagoon, Italy). Environmental Pollution 2005, 136(1):103-107.
41. Puinean A., Rotchell J. Vitellogenin gene expression as a biomarker of endocrine disruption in the invertebrate Mytilus edulis. Marine Environment Research 2006, 62:211-214.
42. Quinn B., Gagné F., Costello M., McKenzie C., Wilson J., Mothersill C. The endocrine disrupting effect of municipal effluent on the zebra mussel (Dreissena polymorpha). Aquatic Toxicology 2004, 66:279-292.
43. Quinn B., Gagné F., Weber J.P., Blaise C. Ecotoxicological effects of a semisubmerged municipal dump (Castle harbour, Bermuda) on the Calico scallop Argopecten gibbus. Marine Pollution Bulletin 2005, 51:534-544.
44. Routledge E.J., Sumpter J.P. Estrogenic activity of surfactants and some of their degradation products assessed using a recombinant yeast screen. Environmental Toxicology and Chemistry 1996, 15:241-248.
45. Routledge E., Sheahan D., Desbrow C., Brighty G., Waldock M., Sumpter J. Identification of estrogenic chemicals in STW effluent. 2. In vivo responses in trout and roach. Environmental Toxicology and Chemistry 1998, 32:1559-1565.
46. Rutishauser B.V., Pesonen M., Escher B.I., Ackermann G.E., Aerni H.R., Suter M.J., Eggen R.I. Comparative analysis of estrogenic activity in sewage treatment plant effluents involving three in vitro assays and chemical analysis of steroids. Environmental Toxicology and Chemistry 2004, 23:857-864.
47. Sánchez-Avila J., Quintana J., Ventura F., Tauler R., Duarte C.M., Lacorte S. Stir bar sorptive extraction-thermal desorption-gas chromatography-mass spectrometry: an effective tool for determining persistent organic pollutants and nonylphenol in coastal waters in compliance with existing Directives. Marine Pollution Bulletin 2009, 60(1):103-112.
48. Staples C., Dorn P., Klecka G., O'Block S., Harris L. A review of the environmental fate, effects and exposures of bisphenol A. Chemosphere 1998, 36:2149-2173.
49. Sumpter J., Jobling S. Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environmental Health Perspectives 1995, 103:173-178.
50. Svenson A., Allard A.S., Ek M. Removal of estrogenicity in Swedish municipal sewage treatment plants. Water Research 2003, 37:4433-4443.
51. Tan D., Hawker J., Muller J., Leusch F., Chapman H. Comprehensive study of endocrine disrupting compounds using grab and passive sampling at selected wastewater treatment plants in South East Queensland, Australia. Environment International 2007, 33:654-669.
52. Ternes T., Stumpf M., Mueller J., Haberer K., Wilken R.D., Servos M. Behaviour and occurrence of estrogens in municipal sewage treatment plants. 1. Investigations in Germany, Canada and Brazil. Science of the Total Environment 1999, 225:81-90.
53. Tilton F., Benson W.H., Schlenk D. Evaluation of estrogenic activity from a municipal wastewater treatment plant with predominantly domestic input. Aquatic Toxicology 2002, 61:211-224.
54. Underwood A., Chapman M. GMAV-5 1984, University of Sydney, Sydney.
55. Underwood A. Experiments in Ecology: Their Logical Design and Interpretation Using Analysis of Variance 1997, Cambridge University Press, Cambridge, UK.
56. Williams, M., Woods, M., Kumar, A., Ying, A., Karkkainen, M., Kookana, R.S., 2007. Endocrine disrupting chemicals in the Australian riverine environment: a pilot study on estrogenic compounds. L. W. Australia, Canberra. Report No. PR071403.
57. Wu R., Sui W., Shin P. Induction, adaptation and recovery of biological responses: implications for environmental monitoring. Marine Pollution Bulletin 2005, 51(8-12):623-634.
58. Ying G., Kookana R., Kumar A. Fate of estrogens and xenoestrogens in four sewage treatment plants with different technologies. Environmental Science & Technology 2008, 27(1):87-94.
59. Zhang A., Hibberd A., Zhou J. Optimisation of derivatisation for the analysis of estrogenic compounds in water by solid-phase extraction gas chromatography-mass spectrometry. Analytica Chimica Acta 2003, 577:52-61.