Reproductive health indicators of immature common carp exposed to municipal wastewater of Behbahan, Iran

Document Type : Original Article

Authors

Department of Aquaculture, School of Natural Resource and Environment, Behbahan Khatam Alanbia University of Technology, Behbahan, Iran

Abstract

Exogenous estrogens or pollutants with estrogen-like activity can induce vitellogenin (VTG) synthesis in male and juvenile fish, making this protein a useful indicator of chemicals that mimic estrogenic activity. The purpose of this study was to investigate the impact of municipal wastewater on blood biochemical parameters of common carp (Cyprinus carpio). Under experimental conditions, biomarkers such as sex steroid levels, alkali-labile phosphate levels, cholesterol and triglycerides, high-density lipoprotein (HDL), and low-density lipoprotein (LDL) were assessed in immature fish exposed to municipal wastewaters collected from a sewage canal in Behbahan, Khuzestan Province, Iran. No significant changes were found in testosterone levels on day 21; however, estradiol, alkali-labile phosphate, triglycerides, cholesterol, and LDL-cholesterol significantly increased in the fish exposed to municipal wastewater compared with the control group. A significant decrease in HDL-cholesterol levels was observed in the fish exposed to municipal wastewater at the end of the experiment. In conclusion, the results of the present study indicated that sewage effluent of Behbahan may contain endocrine disrupters and exposure to sublethal concentrations of municipal wastewater may cause dysfunction in reproductive health indicators of common carp.

Keywords


  1. Shaigan JA, Afshari A. The treatment situation of municipal and industrial wastewater in Iran. Water
  2. and Wastewater 2004; 15(1): 58-69. [In Persian].
  3. Jobling S, Tyler CR. Introduction: The ecological relevance of chemically induced endocrine disruption in wildlife. Environ Health Perspect 2006; 114(Suppl 1): 7-8.
  4. Jobling S, Burn RW, Thorpe K, Williams R, Tyler C. Statistical modeling suggests that antiandrogens in effluents from wastewater treatment works contribute to widespread sexual disruption in fish living in English rivers. Environ Health Perspect 2009; 117(5): 797-802.
  5. Gilbert N. Water under pressure. Nature 2012; 483(7389): 256-7.
  6. Kanda R, Churchley J. Removal of endocrine disrupting compounds during conventional wastewater treatment. Environ Technol 2008; 29(3): 315-23.
  7. Johnson AC, Sumpter JP. Removal of endocrine-disrupting chemicals in activated sludge treatment works. Environ Sci Technol 2001; 35(24): 4697-703.
  8. Orn S, Svenson A, Viktor T, Holbech H, Norrgren L. Male-biased sex ratios and vitellogenin induction in zebrafish exposed to effluent water from a Swedish pulp mill. Arch Environ Contam Toxicol 2006; 51(3): 445-51.
  9. Miller DH, Jensen KM, Villeneuve DL, Kahl MD, Makynen EA, Durhan EJ, et al. Linkage of biochemical responses to population-level effects: a case study with vitellogenin in the fathead minnow (Pimephales promelas). Environ Toxicol Chem 2007; 26(3): 521-7.
  10. 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 Physiol C Toxicol Pharmacol 2006; 144(1): 10-5.
  11. Al-Salhi R, Abdul-Sada A, Lange A, Tyler CR, Hill EM. The xenometabolome and novel contaminant markers in fish exposed to a wastewater treatment works effluent. Environ Sci Technol 2012; 46(16): 9080-8.
  12. Coe TS, Soffker MK, Filby AL, Hodgson D, Tyler CR. Impacts of early life exposure to estrogen on subsequent breeding behavior and reproductive success in zebrafish. Environ Sci Technol 2010; 44(16): 6481-7.
  13. Harris CA, Hamilton PB, Runnalls TJ, Vinciotti V, Henshaw A, Hodgson D, et al. The consequences of feminization in breeding groups of wild fish. Environ Health Perspect 2011; 119(3): 306-11.
  14. Kolodziej EP, Gray JL, Sedlak DL. Quantification of steroid hormones with pheromonal properties in municipal wastewater effluent. Environ Toxicol Chem 2003; 22(11): 2622-9.
  15. Geem ZW, Kim JH. Wastewater treatment optimization for fish migration using harmony search. MATH PROBL ENG 2014; 2014: 5.
  16. Coe TS, Hamilton PB, Hodgson D, Paull GC, Tyler CR. Parentage outcomes in response to estrogen exposure are modified by social grouping in zebrafish. Environ Sci Technol 2009; 43(21): 8400-5.
  17. Barber LB, Loyo-Rosales JE, Rice CP, Minarik TA, Oskouie AK. Endocrine disrupting alkylphenolic chemicals and other contaminants in wastewater treatment plant effluents, urban streams, and fish in the Great Lakes and Upper Mississippi River Regions. Sci Total Environ 2015; 517: 195-206.
  18. Gilannejad N, Dorafshan S, Heyrati FP, Soofiani NM, Asadollah S, Martos-Sitcha JA, et al. Vitellogenin expression in wild cyprinid Petroleuciscus esfahani as a biomarker of endocrine disruption along the Zayandeh Roud River, Iran. Chemosphere 2016; 144: 1342-50.
  19. Wang J, Bing X, Yu K, Tian H, Wang W, Ru S. Preparation of a polyclonal antibody against goldfish (Carassius auratus) vitellogenin and its application to detect the estrogenic effects of monocrotophos pesticide. Ecotoxicol Environ Saf 2015; 111: 109-16.
  20. Wang J, Wang W, Zhang X, Tian H, Ru S. Development of a lipovitellin-based goldfish (Carassius auratus) vitellogenin ELISA for detection of environmental estrogens. Chemosphere 2015; 132: 166-71.
  21. Hecker M, Kim WJ, Park JW, Murphy MB, Villeneuve D, Coady KK, et al. Plasma concentrations of estradiol and testosterone, gonadal aromatase activity and ultrastructure of the testis in Xenopus laevis exposed to estradiol or atrazine. Aquat Toxicol 2005; 72(4): 383-96.
  22. Gagne F, Blaise C. Organic alkali-labile phosphates in biological materials: A generic assay to detect vitellogenin in biological tissues. Environmental Toxicology 2000; 15(3): 243-7.
  23. Snyder SA, Villeneuve DL, Snyder EM, Giesy JP. Identification and quantification of estrogen receptor agonists in wastewater effluents. Environ Sci Technol 2001; 35(18): 3620-5.
  24. Folmar LC, Hemmer M, Denslow ND, Kroll K, Chen J, Cheek A, et al. A comparison of the estrogenic potencies of estradiol, ethynylestradiol, diethylstilbestrol, nonylphenol and methoxychlor in vivo and in vitro. Aquat Toxicol 2002; 60(1-2): 101-10.
  25. Rutishauser BV, Pesonen M, Escher BI, Ackermann GE, Aerni HR, Suter MJ, et al. Comparative analysis of estrogenic activity in sewage treatment plant effluents involving three in vitro assays and chemical analysis of steroids. Environ Toxicol Chem 2004; 23(4): 857-64.
  26. Shore LS, Shemesh M. Naturally produced steroid hormones and their release into the environment. Pure Appl Chem 2003; 75(11-12): 1859-71.
  27. Diniz MS, Peres I, Magalhaes-Antoine I, Falla J, Pihan JC. Estrogenic effects in crucian carp (Carassius carassius) exposed to treated sewage effluent. Ecotoxicol Environ Saf 2005; 62(3): 427-35.
  28. Loomis AK, Thomas P. Effects of estrogens and xenoestrogens on androgen production by Atlantic croaker testes in vitro: evidence for a nongenomic action mediated by an estrogen membrane receptor. Biol Reprod 2000; 62(4): 995-1004.
  29. Randak T, Zlabek V, Pulkrabova J, Kolarova J, Kroupova H, Siroka Z, et al. Effects of pollution on chub in the River Elbe, Czech Republic. Ecotoxicol Environ Saf 2009; 72(3): 737-46.
  30. Palumbo AJ. Vitellogenin, a marker of estrogen mimicking contaminants in fishes: Characterization, quantification and interference by anti-estrogens [PhD Thesis]. Berkeley, CA: University of California; 2008. p. 121.
  31. Lv XF, Zhao YB, Zhou QF, Jiang GB, Song MY. Determination of alkali-labile phosphoprotein phosphorus from fish plasma using the Tb(3+)-tiron complex as a fluorescence probe. J Environ Sci (China) 2007; 19(5): 616-21.
  32. Hemming JM, Allen HJ, Thuesen KA, Turner PK, Waller WT, Lazorchak JM, et al. Temporal and spatial variability in the estrogenicity of a municipal wastewater effluent. Ecotoxicol Environ Saf 2004;
  33. (3): 303-10.
  34. Diniz MS, Peres I, Pihan JC. Comparative study of the estrogenic responses of mirror carp (Cyprinus carpio) exposed to treated municipal sewage effluent (Lisbon) during two periods in different seasons. Sci Total Environ 2005; 349(1-3): 129-39.
  35. Murray RK, Bender DA, Botham KM, Kennelly PJ, Rodwell VW, Weil PA. Harpers illustrated biochemistry. 26th ed. New York, NY: McGraw-Hill Medical; 2003. p. 702.
  36. Ikonomou MG, Cai SS, Fernandez MP, Blair JD, Fischer M. Ultra-trace analysis of multiple endocrine-disrupting chemicals in municipal and bleached kraft mill effluents using gas chromatography-high-resolution mass spectrometry. Environ Toxicol Chem 2008; 27(2): 243-51.
  37. Quinn B, Gagne F, Costello M, McKenzie C, Wilson J, Mothersill C. The endocrine disrupting effect of municipal effluent on the zebra mussel (Dreissena polymorpha). Aquat Toxicol 2004; 66(3): 279-92.
  38. Samuelsson LM, Bjorlenius B, Forlin L, Larsson DG. Reproducible (1)H NMR-based metabolomic responses in fish exposed to different sewage effluents in two separate studies. Environ Sci Technol 2011; 45(4): 1703-10.
  39. Mardones P, Quinones V, Amigo L, Moreno M, Miquel JF, Schwarz M, et al. Hepatic cholesterol and bile acid metabolism and intestinal cholesterol absorption in scavenger receptor class B type I-deficient mice. J Lipid Res 2001; 42(2): 170-80.