Occurrence of intersex in wild freshwater fish in Slovenian rivers: a histological evaluation

1. Sumpter JP. Endocrine disrupters in the aquatic environment: An overview. Acta Hydrochim Hydrobiol 2005;33:9-16. doi: 10.1002/aheh.200400555Search in Google Scholar

2. Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, Hauser R, Prins GS, Soto AM, Zoeller RT, Gore AC. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev 2009;30:293-342. doi: 10.1210/er.2009-0002Search in Google Scholar

3. Castano A, Bols N, Braunbeck T, Dierickx P, Halder M, Isomaa B, Kawahara K, Lee LE, Mothersill C, Pärt P, Repetto G, Sintes JR, Rufli H, Smith R, Wood C, Segner H; ECVAM Workshop 47. The use of fish cells in ecotoxicology. The report and recommendations of ECVAM Workshop 47. Altern Lab Anim 2003;31:317-51. PMID: 1561287510.1177/02611929030310031415612875Search in Google Scholar

4. Matthiessen P. Historical perspective on endocrine disruption in wildlife. Pure Appl Chem 2003;75:2197-206. doi: 10.1351/ pac200375112197Search in Google Scholar

5. Harries JE, Sheahan DA, Matthiessen P, Neall P, Rycroft R, Tylor T, Jobling S, Routledge EJ, Sumpter JP. A survey of estrogenic activity in United Kingdom inland waters. Environ Toxicol Chem 1996;15:1993-2002. doi: 10.1002/ etc.5620151118Search in Google Scholar

6. Jobling S. Review of suggested testing methods for endocrine-disrupting chemicals. Pure Appl Chem 1998;70:1805-27. doi: 10.1351/pac199870091805Search in Google Scholar

7. Jobling S, Coey S, Whitmore JG, Kime DE, Van Look KJW, McAllister BG, Beresford N, Henshaw AC, Brighty G, Tyler CR, Sumpter JP. Wild intersex roach (Rutilus rutilus) have reduced fertility. Biol Reprod 2002;67:515-24. doi: 10.1095/ biolreprod67.2.515Search in Google Scholar

8. Jobling S, Nolan M, Tyler CR, Brighty G, Sumpter JP. Widespread sexual disruption in wild fish. Environ Sci Technol 1998;32:2498-506. doi: 10.1021/es9710870Search in Google Scholar

9. Jobling S, Tyler CR. Endocrine disruption, parasites and pollutants in wild freshwater fish. Parasitology 2003;126:S103-8. doi: 10.1017/S0031182003003652Search in Google Scholar

10. Sumpter JP. Feminized responses in fish to environmental estrogens. Toxicol Lett 1995;82-3:737-42. doi: 10.1016/0378-4274(95)03517-6Search in Google Scholar

11. Sumpter JP. Xenoendocrine disrupters - environmental impacts. Toxicol Lett 1998;103: 337-42. doi: 10.1016/S0378-4274(98)00328-2Search in Google Scholar

12. Community programme of research on endocrine disrupters and environmental hormones (COMPREHEND) 1999 [displayed 5 August 2015]. Available at https://ec.europa.eu/research/endocrine/pdf//env4-ct98-0798.pdf.Search in Google Scholar

13. Burkhardt-Holm P, Segner H, Burki R, Peter A, Schubert S, Suter MJF, Borsuk ME. Estrogenic endocrine disruption in Switzerland: Assessment of fish exposure and effects. Chimia 2008;62:376-82. doi: 10.2533/chimia.2008.376Search in Google Scholar

14. Kelly MA, Reid AM, Quinn-Hosey KM, Fogarty AM, Roche JJ, Brougham CA. Investigation of the estrogenic risk to feral male brown trout (Salmo trutta) in the Shannon International River Basin District of Ireland. Ecotoxicol Environ Saf 2010;73:1658-65. doi: 10.1016/j.ecoenv.2010.08.018Search in Google Scholar

15. Lye CM, Frid CLJ, Gill ME, McCormick D. Abnormalities in the reproductive health of flounder Platichthys flesus exposed to effluent from a sewage treatment works. Mar Pollut Bull 1997;34:34-41. doi: 10.1016/S0025-326X(96) 00061-6Search in Google Scholar

16. Sepulveda MS, Johnson WE, Higman JC, Denslow ND, Schoeb TR, Gross TS. An evaluation of biomarkers of reproductive function and potential contaminant effects in Florida largemouth bass (Micropterus salmoides floridanus) sampled from the St. Johns River. Sci Total Environ 2002;289:133-44. PMID: 1204939010.1016/S0048-9697(01)01029-4Search in Google Scholar

17. Simpson MG, Parry M, Kleinkauf A, Swarbreck D, Walker P, Leah RT. Pathology of the liver, kidney and gonad of flounder (Platichthys flesus) from a UK estuary impacted by endocrine disrupting chemicals. Mar Environ Res 2000;50:283-7. doi: 10.1016/S0141-1136(00)00089-1Search in Google Scholar

18. Sole M, Raldua D, Piferrer F, Barcelo D, Porte C. Feminization of wild carp, Cyprinus carpio, in a polluted environment: plasma steroid hormones, gonadal morphology and xenobiotic metabolizing system. Comp Biochem Physiol C 2003;136:145-56. doi: 10.1016/S1532-0456(03)00192-3Search in Google Scholar

19. Tetreault GR, Bennett CJ, Shires K, Knight B, Servos MR, McMaster ME. Intersex and reproductive impairment of wild fish exposed to multiple municipal wastewater discharges. Aquat Toxicol 2011;104:278-90. doi: 10.1016/j.aquatox.2011.05.008Search in Google Scholar

20. Vajda AM, Barber LB, Gray JL, Lopez EM, Bolden AM, Schoenfuss HL, Norris DO. Demasculinization of male fish by wastewater treatment plant effluent. Aquat Toxicol 2011;103:213-21. doi: 10.1016/j.aquatox.2011.02.007Search in Google Scholar

21. Gill ME, Spiropoulos J, Moss C. Testicular structure and sperm production in flounders from a polluted estuary: a preliminary study. J Exp Mar Biol Ecol 2002;281:41-51. doi:10.1016/S0022-0981(02)00396-9Search in Google Scholar

22. Chiang G, Barra R, Diaz-Jaramillo M, Rivas M, Bahamonde P, Munkittrick KR. Estrogenicity and intersex in juvenile rainbow trout (Oncorhynchus mykiss) exposed to Pine/ Eucalyptus pulp and paper production effluent in Chile. Aquat Toxicol 2015;164:126-34. doi: 10.1016/j.aquatox.2015.04.025Search in Google Scholar

23. Woodling JD, Lopez EM, Maldonado TA, Norris DO, Vajda AM. Intersex and other reproductive disruption of fish in wastewater effluent dominated Colorado streams. Comp Biochem Phys C 2006;144:10-5. doi: 10.1016/j. cbpc.2006.04.019Search in Google Scholar

24. Blazer VS. Histopathological assessment of gonadal tissue in wild fishes. Fish Physiol Biochem 2002;26:85-101. doi: 10.1023/A:1023332216713Search in Google Scholar

25. Leino RL, Jensen KM, Ankley GT. Gonadal histology and characteristic histopathology associated with endocrine disruption in the adult fathead minnow (Pimephales promelas). Environ Toxicol Pharmacol 2005;19:85-98. doi: 10.1016/j.etap.2004.05.010Search in Google Scholar

26. Bateman KS, Stentiford GD, Feist SW. A ranking system for the evaluation of intersex condition in European flounder (Platichthys flesus). Environ Toxicol Chem 2004;23:2831-6. doi: 10.1897/03-541.1Search in Google Scholar

27. Bjerregaard LB, Korsgaard B, Bjerregaard P. Intersex in wild roach (Rutilus rutilus) from Danish sewage effluent-receiving streams. Ecotoxicol Environ Saf 2006;64:321-8. doi: 10.1016/j.ecoenv.2005.05.018Search in Google Scholar

28. Nolan M, Jobling S, Brighty G, Sumpter JP, Tyler CR. A histological description of intersexuality in the roach. J Fish Biol 2001;58:160-78. doi: 10.1111/j.1095-8649.2001. tb00505.xSearch in Google Scholar

29. Bahamonde PA, Munkittrick KR, Martyniuk CJ. Intersex in teleost fish: are we distinguishing endocrine disruption from natural phenomena? Gen Comp Endocrinol 2013;192:25-35. doi: 10.1016/j.ygcen.2013.04.005Search in Google Scholar

30. Tyler CR, Spary C, Gibson R, Santos EM, Shears J, Hill EM. 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;39:2599-607. doi: 10.1021/es0488939Search in Google Scholar

31. Ospina-Alvarez N, Piferrer F. Temperature-dependent sex determination in fish revisited: prevalence, a single sex ratio response pattern, and possible effects of climate change. PLoS One 2008;3:e2837. doi: 10.1371/journal.pone.0002837Search in Google Scholar

32. Blazer VS, Iwanowicz LR, Iwanowicz DD, Smith DR, Young JA, Hedrick JD, Foster SW, Reeser SJ. Intersex (testicular oocytes) in smallmouth bass from the Potomac River and selected nearby drainages. J Aquat Anim Health 2007;19:242-53. doi: 10.1577/H07-031.1Search in Google Scholar

33. Gross-Sorokin MY, Roast SD, Brighty GC. Assessment of feminization of male fish in English rivers by the environment agency of England and Wales. Environ Health Perspect 2006;114(Suppl 1):147-51. doi: 10.1289/ehp.8068Search in Google Scholar

34. Beresford N, Jobling S, Williams R, Sumpter JP. Endocrine disruption in juvenile roach from English rivers: a preliminary study. J Fish Biol 2004;64:580-6. doi: 10.1111/j.0022-1112.2004.00311.xSearch in Google Scholar

35. Allen Y, Matthiessen P, Scott AP, Haworth S, Feist S, Thain JE. The extent of oestrogenic contamination in the UK estuarine and marine environments - further surveys of flounder. Sci Total Environ 1999;233:5-20. doi: 10.1016/ S0048-9697(99)00175-8Search in Google Scholar

36. van Aerle R, Nolan M, Jobling S, Christiansen LB, Sumpter JP, Tyler CR. Sexual disruption in a second species of wild cyprinid fish (the Gudgeon, Gobio gobio) in United Kingdom freshwaters. Environ Toxicol Chem 2001;20:2841-7. doi: 10.1002/etc.5620201225Search in Google Scholar

37. Stentiford GD, Longshaw M, Lyons BP, Jones G, Green M, Feist SW. Histopathological biomarkers in estuarine fish species for the assessment of biological effects of contaminants. Mar Environ Res 2003;55:137-59. doi: 10.1016/S0141-1136(02)00212-XSearch in Google Scholar

38. Stentiford GD, Feist SW. First reported cases of intersex (ovotestis) in the flatfish species dab Limanda limanda: Dogger Bank, North Sea. Mar Ecol Prog Ser 2005;301:307-10. doi: 10.3354/meps301307Search in Google Scholar

39. Bjerregaard LB, Madsen AH, Korsgaard B, Bjerregaard P. Gonad histology and vitellogenin concentrations in brown trout (Salmo trutta) from Danish streams impacted by sewage effluent. Ecotoxicology 2006;15:315-27. doi:10.1007/ s10646-006-0061-9Search in Google Scholar

40. Bernet D, Liedtke A, Bittner D, Eggen RIL, Kipfer S, Kung C, Largiader CR, Suter Marc JF, Wahli T, Segner H. Gonadal malformations in whitefish from Lake Thun: Defining the case and evaluating the role of EDCs. Chimia 2008;62:383-8. doi: 10.2533/chimia.2008.383Search in Google Scholar

41. Gercken J, Sordyl H. Intersex in feral marine and freshwater fish from northeastern Germany. Mar Environ Res 2002;54:651-5. doi: 10.1016/S0141-1136(02)00156-3Search in Google Scholar

42. Gimeno S, Gerritsen A, Bowmer T, Komen H. Feminization of male carp. Nature 1996;384:221-2. doi: 10.1038/384221a0Search in Google Scholar

43. Vigano L, Arillo A, Bottero S, Massari A, Mandich A. First observation of intersex cyprinids in the Po River (Italy). Sci Total Environ 2001;269:189-94. doi: 10.1016/S0048-9697(00)00821-4Search in Google Scholar

44. Lavado R, Thibaut R, Raldua D, Martin R, Porte C. First evidence of endocrine disruption in feral carp from the Ebro River. Toxicol Appl Pharm 2004;196:247-57. doi: 10.1016/j. taap.2003.12.012Search in Google Scholar

45. Martin-Skilton R, Lavado R, Thibaut R, Minier C, Porte C. Evidence of endocrine alteration in the red mullet, Mullus barbatus from the NW Mediterranean. Environ Pollut 2006;141:60-8. doi: 10.1016/j.envpol.2005.08.016Search in Google Scholar

46. Barnhoorn IE, Bornman MS, Pieterse GM, van Vuren JH. Histological evidence of intersex in feral sharptooth catfish (Clarias gariepinus) from an estrogen-polluted water source in Gauteng, South Africa. Environ Toxicol 2004;19:603-8. doi: 10.1002/tox.20068Search in Google Scholar

47. Barnhoorn IE, van Dyk JC, Pieterse GM, Bornman MS. Intersex in feral indigenous freshwater Oreochromis mossambicus, from various parts in the Luvuvhu River, Limpopo Province, South Africa. Ecotoxicol Environ Saf 2010;73:1537-42. doi: 10.1016/j.ecoenv.2010.07.026Search in Google Scholar

48. Harshbarger JC, Coffey MJ, Young MY. Intersexes in Mississippi River shovelnose sturgeon sampled below Saint Louis, Missouri, USA. Mar Environ Res 2000;50:247-50. doi: 10.1016/S0141-1136(00)00055-6Search in Google Scholar

49. Hinck JE, Blazer VS, Schmitt CJ, Papoulias DM, Tillitt DE. Widespread occurrence of intersex in black basses (Micropterus spp.) from US rivers, 1995-2004. Aquat Toxicol 2009;95:60-70. doi: 10.1016/j.aquatox.2009.08.001Search in Google Scholar

50. Vajda AM, Barber LB, Gray JL, Lopez EM, Woodling JD, Norris DO. Reproductive disruption in fish downstream from an Estrogenic wastewater effluent. Environ Sci Technol 2008;42:3407-14. doi: 10.1021/es0720661Search in Google Scholar

51. Kavanagh RJ, Balch GC, Kiparissis Y, Niimi AJ, Sherry J, Tinson C, Metcalfe CD. Endocrine disruption and altered gonadal development in white perch (Morone americana) from the lower Great Lakes region. Environ Health Perspect 2004;112:898-902. doi: 10.1289/ehp.6514Search in Google Scholar

52. Hashimoto S, Bessho H, Hara A, Nakamura M, Iguchi T, Fujita K. Elevated serum vitellogenin levels and gonadal abnormalities in wild male flounder (Pleuronectes yokohamae) from Tokyo Bay, Japan. Mar Environ Res 2000;49:37-53. doi: 10.1016/S0141-1136(99)00047-1Search in Google Scholar