Skip to main content
Log in

Toxicity assessment of municipal sewage treatment plant effluent by an integrated biomarker response in the liver of crucian carp (Carassius auratus)

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

In this study, crucian carp (Carassius auratus) was exposed to the increasing concentrations of municipal sewage treatment plant effluent (MSTPE) for 15 days, and the activities of antioxidant enzymes including superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPx), and acetylcholinesterase (AChE), together with the contents of malondialdehyde (MDA) and glutathione (GSH) in the liver of C. auratus were investigated. Moreover, the integrated biomarker response (IBR) approach was applied to assess the adverse effects of MSTPE in freshwater. The aim of the study was to provide an effective biological indicator for evaluating the toxicity effects and ecological risks of MSTPE in the freshwater environment quantitatively. Results showed that MSTPE could cause oxidative damage to the liver of C. auratus, which reflected through the increasing MDA content over the exposure period. MSTPE also led to the biochemical responses of antioxidant defense in C. auratus liver, such as the enhancement of SOD, CAT, and GPx activities, as well as the inhibition of AChE activity and GSH content. It was found that MDA, SOD, GPx, and GSH could be used as the biomarkers for reflecting the adverse effects of MSTPE in the receiving freshwater on the 12th day of exposure. A significant increase of IBR values was observed as the increasing concentration of MSTPE, and the IBR values presented a significant positive correlation (r = 0.891, P < 0.05) with the increasing concentrations of MSTPE, indicating that IBR approach is a promising tool for assessing the toxicity effects of MSTPE in environmental freshwater.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aitio A, Anderson D, Blain P (1993) Biomarkers and risk assessment: concepts and principles. Switzerland, Geneva

    Google Scholar 

  • Al-Ghais SM (2013) Acetylcholinesterase, glutathione and hepatosomatic index as potential biomarkers of sewage pollution and depuration in fish. Mar Pollut Bull 74:183–186

    CAS  Google Scholar 

  • Alves de Almeida E, Celso Dias Bainy A, Paula de Melo Loureiro A et al (2007) Oxidative stress in Perna perna and other bivalves as indicators of environmental stress in the Brazilian marine environment: antioxidants, lipid peroxidation and DNA damage. Comp Biochem Phys A 146:588–600

    Google Scholar 

  • Beliaeff B, Burgeot T (2002) Integrated biomarker response: a useful tool for ecological risk assessment. Environ Toxicol Chem 21:1316–1322

    CAS  Google Scholar 

  • Bertrand L, Asis R, Monferrán MV, Amé MV (2016) Bioaccumulation and biochemical response in South American native species exposed to zinc: boosted regression trees as novel tool for biomarkers selection. Ecol Indic 67:769–778

    CAS  Google Scholar 

  • Bolong N, Ismail AF, Salim MR, Matsuura T (2009) A review of the effects of emerging contaminants in wastewater and options for their removal. Desalination 239:229–246

    CAS  Google Scholar 

  • Capolupo M, Valbonesi P, Kiwan A, Buratti S, Franzellitti S, Fabbri E (2016) Use of an integrated biomarker-based strategy to evaluate physiological stress responses induced by environmental concentrations of caffeine in the Mediterranean mussel Mytilus galloprovincialis. Sci Total Environ 563-564:538–548

    CAS  Google Scholar 

  • Carvalho Cdos S, Bernusso VA, de Araujo HS, Espindola EL, Fernandes MN (2012) Biomarker responses as indication of contaminant effects in Oreochromis niloticus. Chemosphere 89:60–69

    Google Scholar 

  • Cazenave J, Bacchetta C, Rossi A, Ale A, Campana M, Parma MJ (2014) Deleterious effects of wastewater on the health status of fish: a field caging study. Ecol Indic 38:104–112

    CAS  Google Scholar 

  • Chris (2018) How to dechlorinate pond water (safe for fish guide). Pond informer. https://pondinformer.com/how-to-dechlorinate-pond-water/.

    Google Scholar 

  • De Domenico E, Mauceri A, Giordano D et al (2013) Biological responses of juvenile European sea bass (Dicentrarchus labrax) exposed to contaminated sediments. Ecotoxicol Environ Saf 97:114–123

    Google Scholar 

  • Draper HH, Hadley M (1990) Malondialdehyde determination as index of lipid peroxidation. Method Enzymol 186:421–431

    CAS  Google Scholar 

  • Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95

    CAS  Google Scholar 

  • Gül Ş, Belge-Kurutaş E, Yıldız E, Şahan A, Doran F (2004) Pollution correlated modifications of liver antioxidant systems and histopathology of fish (Cyprinidae) living in Seyhan Dam Lake, Turkey. Environ Int 30:605–609

    Google Scholar 

  • Góth L (1991) A simple method for determination of serum catalase activity and revision of reference range. Clin Chim Acta 196:143–151

    Google Scholar 

  • Götz ME, Künig G, Riederer P, Youdim MBH (1994) Oxidative stress: free radical production in neural degeneration. Pharmacol Ther 63:37–122

    Google Scholar 

  • Ghedira J, Jebali J, Bouraoui Z, Banni M, Chouba L, Boussetta H (2009) Acute effects of chlorpyryphos-ethyl and secondary treated effluents on acetylcholinesterase and butyrylcholinesterase activities in Carcinus maenas. J Environ Sci 21:1467–1472

    CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Bioch 48:909–930

    CAS  Google Scholar 

  • Gravato C, Santos MA (2003) Dicentrarchus labrax biotransformation and genotoxicity responses after exposure to a secondary treated industrial/urban effluent. Ecotoxicol Environ Saf 55:300–306

    CAS  Google Scholar 

  • Hafeman DG, Sunde RA, Hoekstra WG (1974) Effect of dietary selenium on erythrocyte and liver glutathione peroxidase in the rat. J Nutr 104:580–587

    CAS  Google Scholar 

  • Hou J, You G, Xu Y, Wang C, Wang P, Miao L, Dai S, Lv B, Yang Y (2016) Antioxidant enzyme activities as biomarkers of fluvial biofilm to ZnO NPs ecotoxicity and the integrated biomarker responses (IBR) assessment. Ecotoxicol Environ Saf 133:10–17

    CAS  Google Scholar 

  • Houde M, Giraudo M, Douville M et al (2014) A multi-level biological approach to evaluate impacts of a major municipal effluent in wild St. Lawrence River yellow perch (Perca flavescens). Sci Total Environ 497-498:307–318

    CAS  Google Scholar 

  • Ighodaro OM, Akinloye OA (2019) First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): their fundamental role in the entire antioxidant defence grid. Ale J Med 54:287–293

    Google Scholar 

  • Iturburu FG, Bertrand L, Mendieta JR, Amé MV, Menone ML (2018) An integrated biomarker response study explains more than the sum of the parts: oxidative stress in the fish Australoheros facetus exposed to imidacloprid. Ecol Indic 93:351–357

    CAS  Google Scholar 

  • Kamel N, Jebali J, Banni M, Ben Khedher S, Chouba L, Boussetta H (2012) Biochemical responses and metals levels in Ruditapes decussatus after exposure to treated municipal effluents. Ecotoxicol Environ Saf 82:40–46

    CAS  Google Scholar 

  • Kim WK, Jung J (2016) In situ impact assessment of wastewater effluents by integrating multi-level biomarker responses in the pale chub (Zacco platypus). Ecotoxicol Environ Saf 128:246–251

    CAS  Google Scholar 

  • Kim WK, Lee SK, Jung J (2010) Integrated assessment of biomarker responses in common carp (Cyprinus carpio) exposed to perfluorinated organic compounds. J Hazard Mater 180:395–400

    CAS  Google Scholar 

  • Kruger NJ (1994) The Bradford method for protein quantitation. In: Walker JM (ed) The protein protocols handbook, 2nd edn. Humana Press Inc., New Jersey, pp 15–19

    Google Scholar 

  • Li C, Qin L, Qu R, Sun P, Wang Z (2016a) Responses of antioxidant defense system to polyfluorinated dibenzo-p-dioxins (PFDDs) exposure in liver of freshwater fish Carassius auratus. Ecotoxicol Environ Saf 126:170–176

    CAS  Google Scholar 

  • Li J, Zheng X, Liu K, Sun S, Li X (2016b) Effect of tetracycline on the growth and nutrient removal capacity of Chlamydomonas reinhardtii in simulated effluent from wastewater treatment plants. Bioresour Technol 218:1163–1169

    CAS  Google Scholar 

  • Li Y, Men B, He Y, Xu H, Liu M, Wang D (2017) Effect of single-wall carbon nanotubes on bioconcentration and toxicity of perfluorooctane sulfonate in zebrafish (Danio rerio). Sci Total Environ 607-608:509–518

    CAS  Google Scholar 

  • Li ZH, Zlabek V, Velisek J, Grabic R, Machova J, Randak T (2010) Modulation of antioxidant defence system in brain of rainbow trout (Oncorhynchus mykiss) after chronic carbamazepine treatment. Comp Biochem Physiol C Toxicol Pharmacol 151:137–141

    Google Scholar 

  • Liu J, Cai Y, Lu G, Dan X, Wu D, Yan Z (2017) Interaction of erythromycin and ketoconazole on the neurological, biochemical and behavioral responses in crucian carp. Environ Toxicol Pharmacol 55:14–19

    CAS  Google Scholar 

  • Liu J, Wang R, Huang B, Lin C, Zhou J, Pan X (2012) Biological effects and bioaccumulation of steroidal and phenolic endocrine disrupting chemicals in high-back crucian carp exposed to wastewater treatment plant effluents. Environ Pollut 162:325–331

    CAS  Google Scholar 

  • Lopes DFC, Assis CRD, Sant'Anna MCS, Silva JFD, Bezerra RS, Frédou FL (2019) Brain acetylcholinesterase of three perciformes: from the characterization to the in vitro effect of metal ions and pesticides. Ecotoxicol Environ Saf 173:494–503

    CAS  Google Scholar 

  • Lu G, Liu J, Zhang F, Nkoom M, Wu D (2018a) Interactive effects of BDE-153 and its metabolite 2,4-DBP on biochemical status in crucian carp (Carassius auratus). Pol J Environ Stud 27:1155–1163

    CAS  Google Scholar 

  • Lu G, Wu H, Ding J (2018b) Interactive effects of copper, fluorene, and fluoranthene on enzymatic biomarkers and metallothionein levels in crucian carp (Carassius auratus). Pol J Environ Stud 27:183–190

    CAS  Google Scholar 

  • Mccord JM, Fridovich I (1969) Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055

    CAS  Google Scholar 

  • Meng SL, Chen JZ, Hu GD, Song C, Fan LM, Qiu LP, Xu P (2014) Effects of chronic exposure of methomyl on the antioxidant system in liver of Nile tilapia (Oreochromis niloticus). Ecotoxicol Environ Saf 101:1–6

    Google Scholar 

  • Pérez MR, Rossi AS, Bacchetta C, Elorriaga Y, Carriquiriborde P, Cazenave J (2018) In situ evaluation of the toxicological impact of a wastewater effluent on the fish Prochilodus lineatus: biochemical and histological assessment. Ecol Indic 84:345–353

    Google Scholar 

  • Pizzimenti S, Toaldo C, Pettazzoni P, Dianzani MU, Barrera G (2010) The “two-faced” effects of reactive oxygen species and the lipid peroxidation product 4-hydroxynonenal in the hallmarks of cancer. Cancers (Basel) 2:338–363

    CAS  Google Scholar 

  • Qu R, Feng M, Wang X, Qin L, Wang C, Wang Z, Wang L (2014) Metal accumulation and oxidative stress biomarkers in liver of freshwater fish Carassius auratus following in vivo exposure to waterborne zinc under different pH values. Aquat Toxicol 150:9–16

    CAS  Google Scholar 

  • Rhee JS, Kim BM, Jeong CB, Park HG, Leung KM, Lee YM, Lee JS (2013) Effect of pharmaceuticals exposure on acetylcholinesterase (AchE) activity and on the expression of AchE gene in the monogonont rotifer, Brachionus koreanus. Comp Biochem Physiol C Toxicol Pharmacol 158:216–224

    CAS  Google Scholar 

  • Richetti SK, Rosemberg DB, Ventura-Lima J, Monserrat JM, Bogo MR, Bonan CD (2011) Acetylcholinesterase activity and antioxidant capacity of zebrafish brain is altered by heavy metal exposure. Neurotoxicology 32:116–122

    CAS  Google Scholar 

  • Samanta P, Im H, Na J, Jung J (2018a) Ecological risk assessment of a contaminated stream using multi-level integrated biomarker response in Carassius auratus. Environ Pollut 233:429–438

    CAS  Google Scholar 

  • Samanta P, Im H, Yoo J, Lee H, Kim NY, Kim W, Hwang SJ, Kim WK, Jung J (2018b) Comparative assessment of the adverse outcome of wastewater effluents by integrating oxidative stress and histopathological alterations in endemic fish. J Hazard Mater 344:81–89

    CAS  Google Scholar 

  • Sanchez W, Burgeot T, Porcher JM (2013) A novel “Integrated Biomarker Response” calculation based on reference deviation concept. Environ Sci Pollut Res Int 20:2721–2725

    CAS  Google Scholar 

  • Sharonov BP, Churilova IV (1992) Inactivation and oxidative modification of Cu, Zn superoxide dismutase by stimulated neutrophils: the appearance of new catalytically active structures. Biochem Bioph Res Co 189:1129–1135

    CAS  Google Scholar 

  • Sies H (1993) Strategies of antioxidant defense. Eur J Biochem 215:213–219

    CAS  Google Scholar 

  • Stamatis N, Hela D, Konstantinou I (2010) Occurrence and removal of fungicides in municipal sewage treatment plant. J Hazard Mater 175:829–835

    CAS  Google Scholar 

  • Tietze F (1969) Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal Biochem 27:502–522

    CAS  Google Scholar 

  • Üner N, Oru E, Canli M, Sevgler Y (2001) Effects of cypermethrin on antioxidant enzyme activities and lipid peroxidation in liver and kidney of the freshwater fish, Oreochromis niloticus and Cyprinus carpio (L.). Bull Environ Contam Toxicol 67:657–664

    Google Scholar 

  • Wan R, Meng F, Fu W, Wang Q, Su E (2015) Biochemical responses in the gills of Meretrix meretrix after exposure to treated municipal effluent. Ecotoxicol Environ Saf 111:78–85

    CAS  Google Scholar 

  • Wan R, Meng F, Su E, Fu W, Wang Q (2018) Development of a classification scheme for evaluating water quality in marine environment receiving treated municipal effluent by an integrated biomarker approach in Meretrix meretrix. Ecol Indic 93:697–703

    CAS  Google Scholar 

  • Winston GW, Di Giulio RT (1991) Prooxidant and antioxidant mechanisms in aquatic organisms. Aquat Toxicol 19:137–161

    CAS  Google Scholar 

  • Xie J, Zhao Y, Wang Q, Wu H, Teng J, Yang D, Cao R, Chen L, Li F, Ji C, Cong M, Zhao J (2016a) An integrative biomarker approach to assess the environmental stress in the north coast of Shandong Peninsula using native oysters, Crassostrea gigas. Mar Pollut Bull 112:318–326

    CAS  Google Scholar 

  • Xie Z, Lu G, Hou K, Qin D, Yan Z, Chen W (2016b) Bioconcentration, metabolism and effects of diphenhydramine on behavioral and biochemical markers in crucian carp (Carassius auratus). Sci Total Environ 544:400–409

    CAS  Google Scholar 

  • Zhang W, Liu W, Zhang J, Zhao H, Zhang Y, Quan X, Jin Y (2012) Characterisation of acute toxicity, genotoxicity and oxidative stress posed by textile effluent on zebrafish. J Environ Sci 24:2019–2027

    CAS  Google Scholar 

Download references

Funding

This study received financial support from the Natural Science Foundation of Shandong Province (ZR2017PH060).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Tong Chang or Chenjie Wang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Responsible editor: Philippe Garrigues

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chang, T., Wei, B., Wang, Q. et al. Toxicity assessment of municipal sewage treatment plant effluent by an integrated biomarker response in the liver of crucian carp (Carassius auratus). Environ Sci Pollut Res 27, 7280–7288 (2020). https://doi.org/10.1007/s11356-019-07463-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-07463-2

Keywords

Navigation