Environmental Science and Pollution Research

, Volume 26, Issue 5, pp 5164–5175 | Cite as

Evaluation of the oxidative stress in liver of crucian carp (Carassius auratus) exposed to 3,4,4′-tri-CDE, 2-MeO-3′,4,4′-tri-CDE, and 2-HO-3′,4,4′-tri-CDE

  • Danru Cheng
  • Kan Cao
  • Tantan Wang
  • Xuesheng ZhangEmail author
  • Mingbao Feng
  • Hui Liu
Research Article


Polychlorinated diphenyl ethers (PCDEs) are a class of potential persistent organic contaminants, which have been widely detected in aquatic environment. In the present study, the effects of 3,4,4′-tri-CDE and its two possible metabolites (2-MeO-3′,4,4′-tri-CDE and 2-HO-3′,4,4′-tri-CDE) on oxidative stress biomarkers in liver of Carassius auratus were evaluated. The fish were treated with these three compounds at different doses (0.1, 1, and 10 μg/L) via semi-static water exposure. The liver samples were individually taken at 3, 7, and 21 days for analysis of oxidative stress indicators, including superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPx), reduced glutathione (GSH), and malondialdehyde (MDA). Compare to the control group, the hepatic antioxidant enzyme activity and GSH contents showed significant decreases (p < 0.05) at high-dose treatment (10 μg/L) and prolonged exposure time (21 days) in most of the toxicant-treated groups, indicating the occurrence of oxidative stress in fish liver. However, no consistent trend of the variations of antioxidant parameters was observed at low doses (0.1 and 1 μg/L). Meanwhile, the lipid peroxidation was significantly induced with extending exposure time and increasing dose. In addition, the toxicity order of three compounds was discussed using the integrated biomarker response (IBR) index. Notably, 2-HO-3′,4,4′-tri-CDE was indicated to cause the most severe hepatic oxidative stress.


Polychlorinated diphenyl ethers Antioxidant enzymes Lipid peroxidation Integrated biomarker response Freshwater fish 



This research was financially supported by the National Natural Science Foundation of China (No. 21607001 and 21607058), the Anhui Provincial Natural Science Foundation (No. 1608085QB45), and the Science Research Project of Anhui Education Department (No. KJ2015A090).

Supplementary material

11356_2018_3938_MOESM1_ESM.docx (36 kb)
ESM 1 (DOCX 35 kb)


  1. Almroth BC, Albertsson E, Sturve J, Förlin L (2008) Oxidative stress, evident in antioxidant defenses and damage products, in rainbow trout caged outside a sewage treatment plant. Ecotoxicol Environ Saf 70:370–378CrossRefGoogle Scholar
  2. Bebianno MJ, Company R, Serafim A, Camus L, Cosson RP, Fiala-Médoni A (2005) Antioxidant systems and lipid peroxidation in Bathymodiolus azoricus from mid-Atlantic ridge hydrothermal vent field. Aquat Toxicol 75:354–373CrossRefGoogle Scholar
  3. Beliaeff B, Burgeot T (2002) Integrated biomarker response: a useful tool for ecological risk assessment. Environ Toxicol Chem 21:1316–1322CrossRefGoogle Scholar
  4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  5. Carlson GP, Smith EN, Johnson KM (1980) Induction of xenobiotic metabolism in rat liver by chlorinated biphenyl ether isomers. Drug Chem Toxicol 3:293–303CrossRefGoogle Scholar
  6. Chen HL, Hsu CH, Hung DZ, Hu ML (2006) Lipid peroxidation and antioxidant status in workers exposed to PCDD/fs of metal recovery plants. Sci Total Environ 372:12–19CrossRefGoogle Scholar
  7. Cheung CCC, Zheng GJ, Li AMY, Richardson BJ, Lam PKS (2001) Relationships between tissue concentrations of polycyclic aromatic hydrocarbons and antioxidative responses of marine mussels. Perna viridis. Aquat Toxicol 52:189–203CrossRefGoogle Scholar
  8. Chui YC, Hansell MM, Addison RF, Law FC (1985) Effects of chlorinated diphenyl ethers on the mixed-function oxidases and ultrastructure of rat and trout liver. Toxicol Appl Pharmacol 81:287–294CrossRefGoogle Scholar
  9. Devasagayam TPA (1986) Lipid peroxidation in rat uterus. BBA-Mol Cell Biol L 876:507–514Google Scholar
  10. Domingo JL, Bocio A, Falcoa G, Llobet JM (2006) Exposure to PBDEs and PCDEs associated with the consumption of edible marine species. Environ Sci Technol 40:4394–4399CrossRefGoogle Scholar
  11. Fang BX, Shi JQ, Qin L, Feng MB, Cheng DR, Wang TT, Zhang XS (2018) Toxicity evaluation of 4,4′-di-CDPS and 4,4′-di-CDE on green algae Scenedesmus obliquus: growth inhibition, change in pigment content, and oxidative stress. Environ Sci Pollut Res 25:15630–15640CrossRefGoogle Scholar
  12. Feng MB, Qu RJ, Wang C, Wang LS, Wang ZY (2013) Comparative antioxidant status in freshwater fish Carassius auratus exposed to six current-use brominated flame retardants: a combined experimental and theoretical study. Aquat Toxicol 140–141:314–323CrossRefGoogle Scholar
  13. Feng MB, Qu RJ, Li Y, Wei ZB, Wang ZY (2014) Biochemical biomarkers in liver and gill tissues of freshwater fish Carassius auratus following in vivo exposure to hexabromobenzene. Environ Toxicol 10:1460–1470CrossRefGoogle Scholar
  14. Feng MB, He Q, Meng LJ, Zhang XL, Sun P, Wang ZY (2015) Evaluation of single and joint toxicity of perfluorooctane sulfonate, perfluorooctanoic acid, and copper to Carassius auratus using oxidative stress biomarkers. Aquat Toxicol 161:108–116CrossRefGoogle Scholar
  15. Góth L (1991) A simple method for determination of serum catalase activity and revision of reference range. Clin Chim Acta 196:143–151CrossRefGoogle Scholar
  16. Husak VV, Mosiichuk NM, Maksymiv IV, Storey JM, Storey KB, Lushchak VI (2016) Oxidative stress responses in gills of goldfish, Carassius auratus, exposed to the metribuzin-containing herbicide Sencor. Environ Toxicol Pharmacol 45:163–169CrossRefGoogle Scholar
  17. Iverson F, Newsome H, Hierlihy L (1987) Induction of rat hepatic monooxygenase activity by polychlorinated diphenyl ethers. Food Chem Toxicol 25:305–307CrossRefGoogle Scholar
  18. Jabeen K, Li BW, Chen QQ, Su L, Wu CX, Hollert H, Shi HH (2018) Effects of virgin microplastics on goldfish (Carassius auratus). Chemosphere 213:323–332CrossRefGoogle Scholar
  19. Jollow DJ, Mitchell JR, Zampagilone N, Gilete JR (1974) Bromobenzene-induced liver necrosis: protective role of glutathione and evidence for 3,4-bromobenzene oxide as the hepatotoxic metabolite. Pharmacology 11:151–169CrossRefGoogle Scholar
  20. Kelly BC, Ikonomou MG, Blair JD, Morin AE, Gobas FAPC (2007) Food web–specific biomagnification of persistent organic pollutants. Science 317:236–239CrossRefGoogle Scholar
  21. Kim WK, Lee SK, Jung JH (2010) Integrated assessment of biomarker responses in common carp (Cyprinus carpio) exposed to perfluorinated organic compounds. J Hazard Mater 180:395–400CrossRefGoogle Scholar
  22. Kodavanti PR, Ward TR, Derryellin EC, Mckinney JD, Tilson HA (2003) Increased [3H]phorbol ester binding in rat cerebellar granule cells and inhibition of 45Ca2+ buffering in rat cerebellum by hydroxylated polychlorinated biphenyls. Neurotoxicology 24:187–198CrossRefGoogle Scholar
  23. Kodavanti PR, Royland JE, Richards JE, Besas J, Macphail RC (2011) Toluene effects on oxidative stress in brain regions of young-adult, middle-age, and senescent brown Norway rats. Toxicol Appl Pharmacol 256(3):386–398CrossRefGoogle Scholar
  24. Koistinen J (2000) Polychlorinated diphenyl ethers, the handbook of environmental chemistry, vol 13 Ppart K. Springer Verlag, Berlin, pp 157–201Google Scholar
  25. Koistinen J, Paasivirta J, Suonpera M (1995) Contamination of pike and sediments from Kymijoki River by PCDEs, PCDDs, and PCDFs: contents and patterns compared to pike and sediment from the Bothnian Bay and seals from Lake Saimaa. Environ Sci Technol 29:2541–2547CrossRefGoogle Scholar
  26. Koistinen K, Herve S, Ruokojärvi P, Koponen J, Vartiainen T (2010) Persistent organic pollutants in two Finnish watercourses: levels, congener profiles and source estimation by mussel incubation. Chemosphere 80:625–633CrossRefGoogle Scholar
  27. Kruz J, Ballschmiter K (1995) Isomer specific determination of 79 polychlorinated diphenyl ethers (PCDEs) in cod liver oil, chlorophenols and a fly ash. Fresenius J Anal Chem 351:98–109CrossRefGoogle Scholar
  28. Kurz J, Ballschmiter K (1999) Vapour pressures, aqueous solubilities, Henry’s law constants, partition coefficients between gas/water (K gw), n-octanol/water (K ow) and gas/n-octanol (K go) of 106 polychlorinated diphenyl ethers (PCDE). Chemosphere 38:573–586CrossRefGoogle Scholar
  29. Lawrence RA, Burk RF (1976) Glutathione peroxidase activity in selenium deficient rat liver. Biochem Biophys Res Commun 71:952–958CrossRefGoogle Scholar
  30. Li Y, Li M, Shi JQ, Yang X, Wang ZY (2012) Hepatic antioxidative responses to PCDPSs and estimated short-term biotoxicity in freshwater fish. Aquat Toxicol 120-121:90–98CrossRefGoogle Scholar
  31. Li CG, Qin L, Qu RJ, Sun P, Wang ZY (2016) Responses of antioxidant defense system to polyfluorinated dibenzo-p-dioxins (PFDDs) exposure in liver of freshwater fish Carassius auratus. Ecotoxicol Environ Saf 126:170–176CrossRefGoogle Scholar
  32. Luo Y, Su Y, Lin RZ, Shi HH, Wang XR (2006) 2-Chlorophenol induced ROS generation in fish Carassius auratus based on the EPR method. Chemosphere 65:1064–1073CrossRefGoogle Scholar
  33. Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30CrossRefGoogle Scholar
  34. Majeed SA, Nambi KS, Taju G, Vimal S, Venkatesan C, Hameed AS (2014) Cytotoxicity, genotoxicity and oxidative stress of malachite green on the kidney and gill cell lines of freshwater air breathing fish channa striata. Environ Sci Pollut Res 21(23):13539–13550CrossRefGoogle Scholar
  35. Metcalfe CD, Metcalfe TL, Cormier JA, Huestis SY, Niimi AJ (1997) Early life-stage mortalities of Japanese medaka (Oryzias Latipes) exposed to polychlorinated diphenyl ethers. Environ Toxicol Chem 16:1749–1754CrossRefGoogle Scholar
  36. Mittal M, Siddiqui MR, Tran K, Reddy SP, Malik AB (2014) Reactive oxygen species in inflammation and tissue injury. Antioxid Redox Signal 20:1126–1167CrossRefGoogle Scholar
  37. Pandey S, Parvez S, Sayeed L, Haque R, Bin-Hafeez B, Raisuddin S (2003) Biomarkers of oxidative stress: a comparative study of river yamuna fish wallago Attu (B1.&Schn.). Sci Total Environ 309:105–115CrossRefGoogle Scholar
  38. Pandey S, Parvez S, Ansari RA, Ali M, Kaur M, Hayat F, Ahmad F, Raisuddin S (2008) Effects of exposure to multiple trace metals on biochemical, histological and ultrastructural features of gills of a freshwater fish, Channa punctate Bloch. Chem Biol Interact 174:183–192CrossRefGoogle Scholar
  39. Qin L, Liu F, Liu H, Wei ZB, Sun P, Wang ZY (2014) Evaluation of HODE-15, FDE-15, CDE-15, and BDE-15 toxicity on adult and embryonic zebrafish (Danio rerio). Environ Sci Pollut Res 21:14047–14057CrossRefGoogle Scholar
  40. Qin L, Feng MB, Zhang XS, Wang LS, Wang ZY (2015) Occurrence of polychlorinated diphenyl ethers in Nanjing section of the Yangtze River: level and distribution pattern. Environ Sci Pollut Res 22:9224–9232CrossRefGoogle Scholar
  41. Rosiaka KL, Seo BW, Chu I, Francis BM (1997) Effects of maternal exposure to chlorinated diphenyl ethers on thyroid hormone concentrations in maternal and juvenile rats. J Environ Sci Health B 32:377–393CrossRefGoogle Scholar
  42. Samanta P, Im H, Na J, Jung J (2018) Ecological risk assessment of a contaminated stream using multi-level integrated biomarker response in Carassius auratus. Environ Pollut 233:429–438CrossRefGoogle Scholar
  43. Sun YY, Yu HX, Zhang JF (2006) Bioaccumulation, depuration and oxidative stress in fish Carassius auratus under phenanthrene exposure. Chemosphere 63:1319–1327CrossRefGoogle Scholar
  44. Van de Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149CrossRefGoogle Scholar
  45. Varanka Z, Rojik I, Varanka I, Nemcsok J, Abraham M (2001) Biochemical and morphological changes in carp (Cyprinus carpio L.) liver following exposure to copper sulfate and tannic acid. Comp Biochem Physiol C 128: 467–477Google Scholar
  46. Villeneuve JY, Niimi AJ, Metcalfe CD (1999) Distribution and bioaccumulation of chlorinated diphenyl ethers in a contaminated embayment of Lake Ontario. J Great Lakes Res 25:760–771CrossRefGoogle Scholar
  47. Wang XR, Luo Y, Shi HH, Zhang JF (2006) Application of molecular biomarkers in early diagnosis and ecological risk assessment for water and soil. Environ Chem 25:320–325Google Scholar
  48. Xie XC, Wu YX, Zhu MY, Zhang YK, Wang XR (2011) Hydroxyl radical generation and oxidative stress in earthworms (Eisenia fetida) exposed to decabromodiphenyl ether (BDE-209). Ecotoxicology 20:993–999CrossRefGoogle Scholar
  49. Xie ZX, Lu GH, Qi PD (2014) Effects of BDE-209 and its mixtures with BDE-47 and BDE-99 on multiple biomarkers in Carassius auratus. Environ Toxicol Pharmacol 38:554–561CrossRefGoogle Scholar
  50. Xing YZ, Nong Y, Lu YZ, Yang ML, Yan B (2017) Response characteristics of oxidative stress biomarkers of Polymesoda erosa to exposure of SCCPs. China Environ Sci 37:3962–3971Google Scholar
  51. Xu D, Zhao J, Hang HC, Wen J (2011) Determination of SOD specific activity in animal and plant tissues by improved xanthine oxidase method. Food Sci 32:237–241Google Scholar
  52. Xu X, Cui Z, Wang X, Wang X, Zhang S (2018) Toxicological responses on cytochrome P450 and metabolic transferases in liver of goldfish (Carassius auratus) exposed to lead and paraquat. Ecotoxicol Environ Saf 151:161–169CrossRefGoogle Scholar
  53. Yan LQ, Feng MB, Liu JQ, Wang LS, Wang ZY (2016) Antioxidant defenses and histological changes in Carassius auratus after combined exposure to zinc and three multi-walled carbon nanotubes. Ecotoxicol Environ Saf 125:61–71CrossRefGoogle Scholar
  54. Yin Y, Jia HX, Sun YY, Yu HX, Wang XR, Wu JC, Xue YQ (2007) Bioaccumulation and ROS generation in liver of Carassius auratus, exposed to phenanthrene. Comp Biochem Physiol C 145:288–293Google Scholar
  55. Zeng XL, Wang ZY, Ge ZG, Liu HX (2007) Quantitative structure-property relationships for predicting subcooled liquid vapor pressure (P L) of 209 polychlorinated diphenyl ethers (PCDEs) by DFT and the position of cl substitution (PCS) methods. Atmos Environ 41:3590–3603CrossRefGoogle Scholar
  56. Zhang X, Yang FX, Zhang XL, Xu Y, Liao T, Song SB, Wang JW (2008) Induction of hepatic enzymes and oxidative stress in Chinese rare minnow (Gobiocypris rarus) exposed to waterborne hexabromocyclododecane (HBCDD). Aquat Toxicol 86:4–11CrossRefGoogle Scholar
  57. Zhang XS, Liu F, Wei ZB, Wang ZY (2013) Synthesis of diaryl ethers by CuIcatalyed C-O bond formation via Ullman coupling: assessing the reactivity of aryl halides. Lett Org Chem 10:31–36Google Scholar
  58. Zhang XS, Feng MB, Liu F, Qin L, Qu RJ, Li DL, Wang ZY (2014) Subacute oral toxicity of BDE-15, CDE-15, and HODE-15 in ICR male mice: assessing effects on hepatic oxidative stress and metals status and ascertaining the protective role of vitamin E. Environ Sci Pollut Res 21:1924–1935CrossRefGoogle Scholar
  59. Zhang XS, Zeng XL, Qin L, Qu RJ, Shi JQ, Wei ZB, Yang SG, Wang ZY (2015) Experimental investigation on the soil sorption properties and hydrophobicity of polymethoxylated, polyhydroxylated diphenyl ethers and methoxylated-, hydroxylated-polychlorinated diphenyl ethers. Chemosphere 134:84–90CrossRefGoogle Scholar
  60. Zhang XS, Wang TT, Gao L, Feng MB, Qin L, Shi JQ, Cheng DR (2018) Polychlorinated diphenyl ethers (PCDEs) in surface sediments, suspended particulate matter (SPM) and surface water of Chaohu Lake, China. Environ Pollut 241:441–450CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Danru Cheng
    • 1
  • Kan Cao
    • 2
  • Tantan Wang
    • 1
  • Xuesheng Zhang
    • 1
    Email author
  • Mingbao Feng
    • 3
  • Hui Liu
    • 4
  1. 1.School of Resources and Environmental EngineeringAnhui UniversityHefeiChina
  2. 2.Environmental Monitoring Department of Jiangxi ProvinceNanchangChina
  3. 3.Department of Environmental and Occupational Health, School of Public HealthTexas A&M UniversityCollege StationUSA
  4. 4.College of Biological and Chemical EngineeringJiaxing UniversityJiaxingChina

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