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An evaluation of the levels of organochlorine compounds (OCPs and PCBs) in cultured freshwater and wild sea fish eggs as an exposure biomarker for environmental contamination

  • Enes AtmacaEmail author
  • Yavuz Kursad Das
  • Oguzhan Yavuz
  • Abdurrahman Aksoy
Research Article
  • 139 Downloads

Abstract

In this study, the eggs of 30 wild Black Sea whiting (Merlangius merlangus euxinus, Nordmann, 1840) and 30 farmed freshwater rainbow trout (Oncorhynchus mykiss, Walbaum, 1792) collected from Samsun Province in Turkey were analyzed to determine the level of contamination by nine organochlorine pesticides (OCPs), namely α-hexachlorocyclohexane (α-HCH), β-HCH, γ-HCH (lindane), hexachlorobenzene (HCB), aldrin, 2,4′-dichlorodiphenyltrichloroethane (DDT), 4,4′-DDT, 2,4′-dichlorodiphenyldichloroethylene (DDE), 4,4′-DDE, and 15 polychlorinated biphenyls (PCBs) (PCB-28, -70, -74, -81, -99, -101, -118, -138, -153, -156, -170, -180, -183, -187, and -208), and their potential use as biomarkers to monitor levels of environmental contamination. OCPs and PCBs in the fat of fish eggs were extracted cryogenically and their concentrations were determined with a gas chromatography-electron capture detector (GC-ECD). The whiting eggs showed high OCP and PCB levels compared to the rainbow trout eggs. The median ∑ DDT values for whiting and rainbow trout eggs were 1601.62 ng g−1 fat (range 824.87–5049.81) and 406.49 ng g−1 fat (range 199.88–588.82); median ∑Indicator PCBs were 1264.24 ng g−1 fat (range 520.05–6140.32) and 82.11 ng g−1 fat (range 2.85–215.97); and median ∑ HCHs were 155.66 ng g−1 fat (range 35.45–330.40) and 13.48 ng g−1 fat (range 4.44–66.44), respectively. In the whiting eggs, the ∑Indicator PCB level was above the maximum residue limit (MRL) of 200 ng g−1 fat stated in the European Commission Regulation (EC) and Turkish Food Codex (TFC). In addition, there was a significant difference between the contamination levels of the eggs of the two species. In conclusion, it appears that fish eggs can serve as a valuable biomarker for the level of contamination of persistent organochlorine contaminants in different aquatic environments.

Keywords

Bioaccumulation Fish eggs Organochlorine pesticides Polychlorinated biphenyls 

Notes

Compliance with ethical standards

Conflicts of interest

The authors declare no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

References

  1. Aksoy A, Das YK, Yavuz O, Guvenc D, Atmaca E, Agaoglu S (2011) Organochlorine pesticide and polychlorinated biphenyls levels in fish and mussel in Van region, Turkey. Bull Environ Contam Toxicol 87:65–69.  https://doi.org/10.1007/s00128-011-0286-z CrossRefGoogle Scholar
  2. Aksoy A, Guvenc D, Yavuz O, Das YK, Atmaca E (2012) Seasonal variation of polychlorinated biphenyls and organochlorine pesticide levels of sea and cultured farm fish in the Samsun region of Turkey. Bull Environ Contam Toxicol 88:842–849.  https://doi.org/10.1007/s00128-012-0561-7 CrossRefGoogle Scholar
  3. Ankley GT, Tillitt DE, Giesy JP, Jones PD, Verbrugge DA (1991) Bioassay-derived 2,3,7,8-tetrachlorodibenzo-para-dioxin equivalents in PCB-containing extracts from the flesh and eggs of Lake-Michigan chinook salmon (Oncorhynchus tshawytscha) and possible implications for reproduction. Can J Fish Aquat Sci 48:1685–1690.  https://doi.org/10.1139/f91-200 CrossRefGoogle Scholar
  4. Ben Ameur W, el Megdiche Y, Eljarrat E, Ben Hassine S, Badreddine B, Souad T, Bèchir H, Barceló D, Ridha Driss M (2013) Organochlorine and organobromine compounds in a benthic fish (Solea solea) from Bizerte Lagoon (northern Tunisia): implications for human exposure. Ecotoxicol Environ Saf 88:55–64.  https://doi.org/10.1016/j.ecoenv.2012.10.021 CrossRefGoogle Scholar
  5. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917.  https://doi.org/10.1139/o59-099 CrossRefGoogle Scholar
  6. Bordet F, Inthavong D, Fremy J-M (2002) Interlaboratory study of a multiresidue gas chromatographic method for determination of organochlorine and pyrethroid pesticides and polychlorobiphenyls in milk, fish, eggs, and beef fat. J AOAC Int 85:1398–1409Google Scholar
  7. Cakirogullari GC, Secer S (2011) Seasonal variation of organochlorine contaminants in bonito (Sarda sarda L. 1758) and anchovy (Engraulis encrasicolus L. 1758) in Black Sea region, Turkey. Chemosphere 85:1713–1718.  https://doi.org/10.1016/j.chemosphere.2011.09.017 CrossRefGoogle Scholar
  8. Coatu V, Oros A, Tiganus D, Lazar L (2015) Assessment of chemical contamination in biota from Romanian marine waters in respect with maximum admissible levels regulated by legislation for human consumption. J Environ Prot Ecol 16:117–125Google Scholar
  9. EC (2006) European Commission, setting maximum levels for certain contaminants in foodstuffs. Off J Eur Union. https://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2006:364:0005:0024:EN:PDF. Accessed 17 September 2018
  10. Fang W et al (2007) Organochlorine pesticides in soils under different land usage in the Taihu Lake region, China. J Environ Sci 19:584–590.  https://doi.org/10.1016/S1001-0742(07)60097-7 CrossRefGoogle Scholar
  11. Ferrante MC, Fusco G, Naccari C, Meli R, Clausi MT (2016) Are biometric parameters helpful to assess the health risk of consuming organochlorine compounds contaminated silver European eel (Anguilla anguilla)? J Food Sci 81:T1024–T1030.  https://doi.org/10.1111/1750-3841.13259 CrossRefGoogle Scholar
  12. Galaţchi M, Oros A, Coatu V, Costache M, Coprean D, Galaţchi L-D (2017) Pollutant bioaccumulation in anchovy (Engraulis encrasicolus) tissue, fish species of commercial interest at the Romanian Black Sea coast. OUAC 28:11–17.  https://doi.org/10.1515/auoc-2017-0003 Google Scholar
  13. Hook SE, Gallagher EP, Batley GE (2014) The role of biomarkers in the assessment of aquatic ecosystem health. Integr Environ Assess Manag 10:327–341.  https://doi.org/10.1002/ieam.1530 CrossRefGoogle Scholar
  14. Hosseini SV, Behrooz RD, Esmaili-Sari A, Bahramifar N, Hosseini SM, Tahergorabi R, Hosseini SF, Feás X (2008) Contamination by organochlorine compounds in the edible tissue of four sturgeon species from the Caspian Sea (Iran). Chemosphere 73:972–979.  https://doi.org/10.1016/j.chemosphere.2008.06.036 CrossRefGoogle Scholar
  15. Jensen S, Häggberg L, Jörundsdóttir H, Odham G (2003) A quantitative lipid extraction method for residue analysis of fish involving nonhalogenated solvents. J Agric Food Chem 51:5607–5611.  https://doi.org/10.1021/jf0301201 CrossRefGoogle Scholar
  16. Lyons K, Lowe CG (2013) Quantification of maternal offloading of organic contaminants in elasmobranchs using the histotrophic round stingray (Urobatis halleri) as a model. Environ Sci Technol 47:12450–12458.  https://doi.org/10.1021/es402347d CrossRefGoogle Scholar
  17. Madenjian CP, Ebener MP, Sepúlveda MS (2015) PCB concentrations of lake whitefish (Coregonus clupeaformis) vary by sex. J Great Lakes Res 41:1185–1190.  https://doi.org/10.1016/j.jglr.2015.09.010 CrossRefGoogle Scholar
  18. Malakhova L, Voronov V (2008) Organochlorine pollution of mariculture objects of the Crimea coastal area (Black Sea). In: Faye B, Sinyavskiy Y (eds) Impact of pollution on animal products. NATO science for peace and security series C-environmental security. Springer, Dordrecht, pp 169–176.  https://doi.org/10.1007/978-1-4020-8359-4_18 Google Scholar
  19. Miller M, Amrhein J (1995) Maternal transfer of organochlorine compounds in Lake Superior siscowet (Salvelinus namaycush siscowet) to their eggs. Bull Environ Contam Toxicol 55:96–103.  https://doi.org/10.1007/BF00212394 CrossRefGoogle Scholar
  20. Miller MA (1993) Maternal transfer of organochlorine compounds in salmonines to their eggs. Can J Fish Aquat Sci 50:1405–1413.  https://doi.org/10.1139/f93-161 CrossRefGoogle Scholar
  21. Ondarza PM, Gonzalez M, Fillmann G, Miglioranza KSB (2014) PBDEs, PCBs and organochlorine pesticides distribution in edible fish from Negro River basin, Argentinean Patagonia. Chemosphere 94:135–142.  https://doi.org/10.1016/j.chemosphere.2013.09.064 CrossRefGoogle Scholar
  22. Peakall DB, Walker CH (1994) The role of biomarkers in environmental assessment (3). Vertebrates. Ecotoxicology 3:173–179.  https://doi.org/10.1007/bf00117082 CrossRefGoogle Scholar
  23. Samsun S, Erdem Y, Kalayci F (2011) Feeding regime of whiting (Gadus merlangus euxinus Nordmann, 1840) in Turkish middle Black Sea coast. Turk J Fish Aquat Sci 11:515–522.  https://doi.org/10.4194/1303-2712-v11_4_02 Google Scholar
  24. Ssebugere P, Kiremire BT, Kishimba M, Wandiga SO, Nyanzi SA, Wasswa J (2009) DDT and metabolites in fish from Lake Edward, Uganda. Chemosphere 76:212–215.  https://doi.org/10.1016/j.chemosphere.2009.03.049 CrossRefGoogle Scholar
  25. Stancheva M, Georgieva S, Makedonski L (2017) Polychlorinated biphenyls in fish from Black Sea, Bulgaria. Food Control 72:205–210.  https://doi.org/10.1016/j.foodcont.2016.05.012 CrossRefGoogle Scholar
  26. Stoichev T, Makedonski L, Trifonova T, Stancheva M, Ribarova F (2007) DDT in fish from the Bulgarian region of the Black Sea. Chem Ecol 23:191–200.  https://doi.org/10.1080/02757540701339851 CrossRefGoogle Scholar
  27. Sudaryanto A, Monirith I, Kajiwara N, Takahashi S, Hartono P, Muawanah, Omori K, Takeoka H, Tanabe S (2007) Levels and distribution of organochlorines in fish from Indonesia. Environ Int 33:750–758.  https://doi.org/10.1016/j.envint.2007.02.009 CrossRefGoogle Scholar
  28. TFC (2011) Turkish Food Codex, Turk Gida Kodeksi Bulasanlar Yonetmeligi. Resmi Gazete. http://www.resmigazete.gov.tr/eskiler/2011/12/20111229M3-8.htm. Accessed 17 September 2018
  29. Van der Oost R, Beyer J, Vermeulen NP (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149.  https://doi.org/10.1016/S1382-6689(02)00126-6 CrossRefGoogle Scholar
  30. Wilson P, Tillitt D (1996) Rainbow trout embryotoxicity of a complex contaminant mixture extracted from Lake Michigan lake trout. Mar Environ Res 42:129–134.  https://doi.org/10.1016/0141-1136(95)00047-X CrossRefGoogle Scholar
  31. Zhang X, Gandhi N, Bhavsar SP (2016) Persistent organohalogens in paired fish fillet and eggs: implications for fish consumption advisories. J Agric Food Chem 64:2832–2840.  https://doi.org/10.1021/acs.jafc.6b00089 CrossRefGoogle Scholar
  32. Zhou R, Zhu L, Chen Y, Kong Q (2008) Concentrations and characteristics of organochlorine pesticides in aquatic biota from Qiantang River in China. Environ Pollut 151:190–199.  https://doi.org/10.1016/j.envpol.2007.02.015 CrossRefGoogle Scholar
  33. Zhulidov AV et al (2003) A review of riverine fluxes of hexachlorocyclohexane and DDT to the Azov and black seas from the former USSR and Russian federation. J Environ Sci Health A Tox Hazard Subst Environ Eng 38:753–769.  https://doi.org/10.1081/ese-120018589 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Pharmacology and Toxicology, Faculty of Veterinary MedicineOndokuz Mayis UniversitySamsunTurkey

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