Abstract
The present study investigated the effects of polyvinyl chloride (PVC) microparticles (MP) on hepatic antioxidant enzymes activities, serum biochemical and liver histology of juvenile Clarias gariepinus. A total of 180 (25.15 g average weight) C. gariepinus were fed PVC MP (95.41 ± 4.23 μm) spiked diets at 0.5, 1.5, 3.0 percentage inclusion levels and a control diet for 45 days of exposure, then followed by 30 days of depuration trials. Fish specimens (9) from each treatment were sampled every 15-day interval for serum biochemical, liver antioxidant enzymes and histopathological assay. Glucose and triglyceride levels increased significantly in PVC-treated groups when compared with the control. Protein levels of 0.5% and 3.0% PVC-treated groups reduced significantly on the 15th and 30th day exposure periods, while serum enzyme activities of all PVC-treated groups increased significantly in a time-dependent manner. Antioxidant enzymes (superoxide dismutase, glutathione peroxidase, catalase) activity in the liver of the treated groups also decreased progressively in a time-dependent manner. A time-dependent elevation in lipid peroxidation levels was observed in PVC MP-treated groups. Histopathological assessment of the fish liver showed mild to severe levels of glycogen depletion, fatty vacuolation and degeneration, hepatocellular necrosis in PVC-treated groups with reference to the control. The present study revealed that PVC microplastic induced oxidative damage and hepatic histopathological alterations in the exposed fish.
Similar content being viewed by others
References
Abayomi OA, Range P, Al-Ghouti MA, Obbard JP, Almeer SH, Ben-Hamadou R (2017) Microplastics in coastal environments of the Arabian Gulf. Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2017.07.011
Abbasi S, Soltani N, Keshavarzi B, Moore F, Turner A, Hassanaghaei M (2018) Microplastics in different tissues of fish and prawn from the Musa Estuary, Persian Gulf. Chemos 205:80–87
Ajima MNO, Pandey PK, Kumar K, Poojary N (2017) Neurotoxic, molecular responses and oxidative stress biomarkers in Nile tilapia (Oreochromis niloticus) (Lin. 1758) exposed to Verapmil. Comp Biochem Physiol C 196:44–52
Andrady A (2011) Microplastics in the marine environment. Mar Pollut Bull 62(8):1596–1605. https://doi.org/10.1016/j.marpolbul.2011.05.030
Arias-Andres M, Klümper U, Rojas-Jimenez K, Grossart HP (2018) Microplastic pollution increases gene exchange in aquatic ecosystems. Environ Pollut 237:253–261. https://doi.org/10.1016/j.envpol.2018.02.058
Avio CG, Gorbi S, Milan M, Benedetti M, Fattorini D, d’Errico G, Pauletto M, Bargelloni L, Regoli F (2015) Pollutants bioavailability and toxicological risk from microplastics to marine mussels. Environ Pollut 198:211–222. https://doi.org/10.1016/j.envpol.2014.12.021
Barton BA, Morgan JD, Vijayan MM, Adams SM (2002) Physiological and condition-related indicators of environmental stress in fish. In: Adams SM (ed) Biological indicators of aquatic ecosystem stress. American Fisheries Society, Maryland, pp 111–148
Bello OS, Olaifa FE, Emikpe BO (2014) Haematological and blood biochemical changes in African catfish, Clarias gariepinus fed walnut (Tetracarpidium conophorum Mull Arg) leaf and onion (Allium cepa Linn) bulb supplemented diets. Am J Exp Agric 4(12):1593–1603
Beutler E (1984) Red cell membrane metabolism. A manual of biochemical method, 2nd edn. Grune & Stratom, New York, 160p
Bouck RG, Ball RC (1966) Influence of capture methods on blood characteristics and mortality in rainbow trout (Salmo gairdneri). Trans Am Fish Soc 95:167–176
Bråte ILN, Eidsvoll DP, Steindal CC, Thomas KV (2016) Plastic ingestion by Atlantic cod (Gadus morhua) from the Norwegian coast. Mar Pollut Bull 112:105e110
Browne MA, Niven SJ, Galloway TS, Rowland SJ, Thompson RC (2013) Microplastic moves pollutants and additives to worms, reducing functions linked to health and biodiversity. Curr Biol 23(23):2388–2392
Cedervall T, Hansson LA, Lard M, Frohm B, Linse S (2012) Food chain transport of changes water movement and heat transfer through beach sediments. Mar Pollut Bull 6:1708–1713
Cole M, Lindeque P, Fileman E, Halsband C, Galloway TS (2015) The impact of polystyrene microplastics on feeding, function and fecundity in the marine copepod Calanus helgolandicus. Environ Sci Technol 49:1130–1137. https://doi.org/10.1021/es504525u
Critchell K, Hoogenboom MO (2018) Effects of microplastic exposure on the body condition and behaviour of planktivorous reef fish (Acanthochromis polyacanthus). PLoS One 13(3):e0193308. https://doi.org/10.1371/journal.pone.0193308
Dekic R, Savic N, Manojlovic M, Golub D, Pavlicevic J (2016) Condition factor and organosomatic indices of rainbow trout (Onchorhynchus mykiss) from different brood stock. Biotechhnol Anim Husband 32(2):229–237
Egea J, Fabregat I, Frapart YM, Ghezzi P (2017) European contribution to the study of ROS: a summary of the findings and prospects for the future from the COST action BM1203 (EU-ROS). Redox Biol 13:94–162. https://doi.org/10.1016/j.redox.2017.05.007
Epinosa C, Cnesta A, Esteban MA (2017) Effects of dietary polyvinyl chloride microparticles on general health, immune status and expression of several genes related to stress in gilthead and seabream (Sparus aurata). Fish Shell fish Immunol 68:251–259
Espinosa C, Garcia BJM, Esteba MA, Cuesta A (2018) Invitro effects of virgin microplastic on fish head-kidney leucocytes activities. Environ Pollut 235:30–38
Espinosa CR, Esteban AA, Cuesta A (2019) Dietary administration of polyvinylchloride and polyethene microplastics produces histological damage, oxidative stress and immunoregulation in European sea bass (Dicentrarchus labrax L.). Fish Shellfish Immunol. https://doi.org/10.1016/j.fsi.2019.10.072
Ezeoyili I, Mgbenka BO, Atama CI, Ngwu G, Madu JC, Nwani CD (2019) Changes in brain acetylcholinesterase and oxidative stress biomarkers in C. gariepinus exposed to carbendazim. J Aquat Anim Health 31(4). https://doi.org/10.1002/aah.10089
Foley CJ, Feiner ZS, Malinich TD, Höök TO (2018) A meta-analysis of the effects of exposure to microplastics on fish and aquatic invertebrates. Sci Total Environ 631–632(2018):550–559. https://doi.org/10.1016/j.scitotenv.2018.03.046
Gallo F, Fossi C, Weber R, Santillo D, Sousa J, Ingram I, Nadal A, Romano D (2018) Marine litter plastics and microplastics and their toxic chemicals components: the need for urgent preventive measures. Environ Sci Eur 30:13. https://doi.org/10.1186/s12302-018-0139-z
Galloway TS, Cole M, Lewis C (2017) Interactions of microplastic debris throughout the marine ecosystem. Natr Ecol Evol 1:116
Gomiero A, Strafella P, Pellini G, Salvalaggio V, Fabi G (2018) Comparative effects of ingested PVC micro particles with and without adsorbed Benzo(a) pyrene vs. spiked sediments on the cellular and subcellular processes of the benthic organism Hediste diversicolor. Front Mar Sci 5:99. https://doi.org/10.3389/fmars.2018.00099
Gomiero A, Strafella P, Oysaed KB, Fabi G (2019) First occurrence and composition assessment of microplastics in native mussels collected from coastal and offshore areas of the northern and central Adriatic Sea. Environ Sci Pollut Res 26:24407–24416
Graca B, Szewck K, Zarknewska D, Dolega A, Boruchowska MS (2017) Sources and fate of microplastics in marine and beach sediments of sourthern Baltic sea-a preliminary study. Environ Sci Pollut Res 24:7650–7661. https://doi.org/10.1007/s11356-017-8419-5
Greven AC, Merk T, Karagöz F, Mohr K, Klapper M, Jovanovic B, Palic D (2016) Polycarbonate and polystyrene nanoplastic particles act as stressors to the innate immune system of fathead minnow (Pimephale spromelas). Environ Toxicol Chem 35:3093–3100
Güven O, Gökdağ K, Jovanović B, Kıdeyş AE (2017) Microplastic litter composition of the Turkish territorial waters of the Mediterranean Sea, and its occurrence in the gastrointestinal tract of fish. Environ Pollut 223:286–294
Hesser EF (1960) Method for routine fish haematology prog. Fish cult22: 164–171
Horton AA, Svendsen C, Williams RJ, Spurgeon DJ, Lahive E (2017) Large microplastic particles in sediments of tributaries of the River Tames, UK–abundance, sources and methods for effective quantification. Mar Poll Bull 114(1):218–226
Hugla JL, Thome JP (1999) Effects of polychlorinated biphenyls on liver ultrastructure, hepatic monoxygenases, and reproductive success in the barbel. Ecotoxicol Environ Saf 42:265–273
Idodo-Umeh G (2003) Freshwater fishes of Nigeria; taxonomy, ecological notes, diet and utilization. Idodo-Umeh publishers Benin City, 123p
Iheanacho SC, Odo GE (2020) Neurotoxicity, oxidative stress biomarkers and haematological responses in African catfish (Clarias gariepinus) exposed to polyvinyl chloride microparticles. Comp Biochem Physiol C 232:108741. https://doi.org/10.1016/j.cbpc.2020.108741
Iheanacho SC, Ikwo TN, Igweze N, Chukwuidha C, Ogueji EO, Onyeneke R (2018) Effect of different dietary inclusion levels of melon seed (Citrullus lanatus) peel on growth, haematology and histology of Oroechromis niloticus juvenile. Turk J Fish Aquat Sci 18(3):377–384
Iheanacho SC, Ogueji E, Igberi C, Avwemoya F, Amadi-eke A, Yaji A, Mbah C (2019) Suitability of discarded cashew nut (Anacardium occidentale) meal as replacement of soybean meal (Glycine max) in the diet of juvenile African catfish Clarias gariepinus (Burchell, 1822). Indian J Fish 66(3):78–86
Jovanović B (2017) Ingestion of microplastics by fish and its potential consequences from a physical perspective. Int Environ Assess Mgt 13:510–515
Jovanovic B, Palic D (2012) Immunotoxicology of non-functionalized engineered nanoparticles in aquatic organisms with special emphasis on fish. Aquat Toxicol. https://doi.org/10.1016/j.aquatox.2012.04.005
Jovanovic B, Gokdag K, Guven O, Emre Y, Whitely EM, Kideys AE (2018) Virgin microplastics are not causing imminent harm to fish after dietary exposure. Mar Pollut Bull 130:123–131
Jung SH, Sim DS, Park MS, Jo QT, Kim Y (2003) Effects of formalin on hematological and blood chemistry in olive flounder, Paralichthys olivaceus (Temminck at Schlegel). Aquat Res 34:1269–1275
Kettner MT, Rojas-Jimenez K, Oberbeckman S, Labrenoz M, Grossert HP (2017) Microplastics altered composition of fungal communities in aquatic ecosystem. Environ Microbiol 19(11):4447–4459
Lavanya S, Ramesh M, Kavitha C, Malarvizhi A (2011) Hematological, biochemical and ionoregulatory responses of Indian major carp Catla catla during chronic sublethal exposure to inorganic arsenic. Chemosphere 82:977–985
Leonardi M, Tarifeno E, Vera J (2009) Diseases of the Chilenean flounder, Paralichthys adspersus (Steindachner, 1867), as a biomarker of marine coastal pollution near the Itata River (Chile): Part II. Histopathological lesions. Arch Environ ContamToxicol 56:546–556
Li ZH, Velisek J, Zlabek V, Grabic R, Machova J, Kolarova J, Randak T (2011) Chronic toxicity of verapamil on juvenile rainbow trout (Oncorhynchus mykiss): effects on morphological indices, hematological parameters and antioxidant responses. J Hazard Mater 185:870–880
Li J, Yang D, Li L, Jabeen K, Shi H (2015) Microplastics in commercial bivalves from China. Environ Pollut 207:190–195
Lu Y, Zhang Y, Deng Y, Jiang W, Zhao Y, Geng J, Ren H (2016) Uptake and accumulation of polystyrene microplastics in Zebrafish (Danio rerio) and toxic effects in liver. Environ Sci Technol 50(7):4054–4060
Lusher A, O’Donnell C, Officer R, O’Connor I (2015) Microplastic interactions with North Atlantic mesopelagic fish. ICES J Mar Sci 73(4):1214–1225. https://doi.org/10.1093/icesjms/fsv241
Mahon AM, O’Connell B, Healy MG, O’Connor I, Officer R, Nash R, Morrison L (2017) Microplastics in sewage sludge: effects of treatment. Environ Sci Technol 51(2):810–818
Min EY, Kane JC (2008) Effect of waterborne benomyl on the hematological and antioxidant parameters of the Nile tilapia, Oreochromis niloticus. Pestic Biochem Physiol 92:138–143
Misra HP, Friedovich I (1972) The role of superoxide anions in the auto-oxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175
Nadal MA, Alomar C, Deudero S (2016) High levels of microplastic ingestion by the semi pelagic fish bogue Boops boops (L.) around the Balearic Islands. Environ Pollut 214:517–523
National Oceanic and Atmospheric Administration (NOAA) (2016) How much would it cost to clean up the Pacific Garbage Patches? [cited 2016 December 11]. http://response.restoration.noaa.gov/about/media/howmuch- would-it-cost-clean-pacific-garbage-patches.html
Nwani CD, Somdare PO, Ukonze JA, Ejere VC, Nwadinigwe AO, Nwani JC, Odo GE, Ugbor ON (2016) Subchronic exposure to fenthion induces hematological changes in liver tissue of African catfish Clarias gariepinus. J Aquat Anim Health 28:229–234
Odo GE, Agwu JE, Ivoke N, Ejere VC, Atama CI, Ezea CO, Aguoru GC, Anya BC (2017) Effect of short-term exposure to Cyperdicot on behavioural and haematological responses in African catfish (Clarias gariepinus). Turk J Fish Aquat Sci 17:61–70
Ogata Y, Takada H, Mizukawa K, Hirai H, Iwasa S, Endo S, Mato Y, Saha M, Okuda K, Nakashima A, Murakami M, Zurcher N, Booyatumanondo R, Zakaria MP, Dung le Q, Gordon M, Miguez C, Suzuki S, Moore C, Karapanagioti HK, Weerts S, McClurg T, Burres E, Smith W, Van Velkenburg M, Lang JS, Lang RC, Laursen D, Danner B, Stewardson N, Thompson RC (2009) International pellet watch: global monitoring of persistent organic pollutants (POPs) in coastal waters. 1. Initial phase data on PCBs, DDTs, and HCHs. Mar Pollut Bull 58(10):1437–1446. doi: https://doi.org/10.1016/j.marpolbul.2009.06.014
Ogueji EO, Nwani CD, Iheanacho SC, Mbah CE, Okeke CO, Yaji A (2018) Acute toxicity effects of ibuprofen on behaviour and haematological parameters of African catfish Clarias gariepinus (Burchell, 1822). Afr J Aquat Sci 43(3):293–303. https://doi.org/10.2989/16085914.2018.1465393
Okoro N, Iheanacho SC, Nwakpa J, Eze C (2019) Effects of Chromolaena odorata leaf extract on behavior and haematology of Clarias gariepinus (Burchell, 1822). Afr J Aquat Sci 44(4):421–427. https://doi.org/10.2989/16085914.2019.1661823
Oliveira M, Ribeiro A, Hylland K, Guilhermino L (2013) Single and combined effects of microplastics and pyrene on juveniles (0+ group) of the common goby Pomatoschistus microps (Teleostei, gobiidae). Ecol Indic 34:641–647
Organisation of Economic Coorperation and Development (OECD) (2012) Guidelines for the testing of chemicals. Test guidelines No. 301. OECD, Paris
Pedà C, Caccamo L, Fossi MC, Gai F, Andaloro F, Genovese L, Perdichizzi A, Romeo T, Maricchiolo G (2016) Intestinal alterations in European sea bass Dicentrarchus labrax (Linnaeus, 1758) exposed to microplastics: preliminary results. Environ Pollut 212:251–256. https://doi.org/10.1016/j.envpol.2016.01.083
Pellini G, Gomiero A, Ferr FC, Grati F, Tassetti N, Polidori P, Fabi G, Scarcella G (2018) Characterization of microplastic litter in the gastrointestinal tract of Solea solea from the Adriatic Sea. Environ Pollut 234(2018):943–952. https://doi.org/10.1016/j.envpol.2017.12.038
Plastics Team (2016) Density. http://www.tworzywa.pwr.wroc. pl/pl/dydaktyka/gestosc. Accessed 4 September 2016 (in Polish)
Ramsden CS, Smith TJ, Shaw BJ, Handy RD (2009) Dietary exposure to titanium dioxide nanoplaticles in rainbow trout, (Oncorhynchus mykiss): no effect on growth, but subtle biochemical disturbances in the brain. Ecotoxicol 18:939–951
Ribeiro F, Garcia AR, Pereira BP, Fonseca M, Mestre NC, Fonseca TG, IIharco LM (2017) Microplastic effects in Scrobicularia plana. Mar Pollut Bull 122(1–2):379–391
Rochman CM, Hoh E, Kurobe T, Teh SJ (2013) Ingested plastic transfers hazardous chemicals to fish and induces hepatic stress. Sci Report 3(3263). https://doi.org/10.1038/srep03263
Romeo T, Pietro B, Peda C, Consoli P, Andaloro F, Fossi MC (2015) First evidence of presence of plastic debris in stomach of large pelagic fish in the Mediterranean Sea. Mar Pollut Bull 95:358–361
Ronlad WG, Bruce AB (1990) Organosomatic indices and an autopsy-based assessment as indicators of health condition of fish. Am Fish Soc 8:93–108
Rummel C (2014) Occurrence and potential effects of plastic ingestion by pelagic and demersal fish from the North Sea and Baltic Sea Diplom thesis, Johannes Gutenberg-Universität Mainz
Santana MFM, Ascer LG, Cust-odio MR, Moreira FT, Turra A (2016) Microplastic contamination in natural mussel beds from a Brazilian urbanized coastal region: rapid evaluation through bioassessment. Mar Pollut Bull 106:183–189
Santillo D, Miller K, Johnston P (2017) Microplastics as contaminants in commercially important seafood species. Integr Environ Assess Mgt 13(3):516–521. https://doi.org/10.1002/ieam.1909
Saravanan M, Ussha-Devik K, Malarvizhi A, Ramesh M (2012) Effects of Ibuprofen on haematological, biochemical and enzymological parameters of blood in an Indian major carp Cirrhinus mrigala. Environ Toxicol Pharmacol 34:14–22
Scherer C, Weber A, Lambert S, Wagner M (2018) Interaction of microplastics with freshwater biota. Hdb Environ Chem 58. https://doi.org/10.1007/978-3-319-61615-5_8
Shahsavani D, Mohri M, Gholipour H (2010) Determination of normal values of some blood serum enzymes in Acipenser stellatus Pallas. Fish Physiol Biochem 36:39–43
Sharma SK, Krishna-Murti CR (1968) Production of lipid peroxides by brain. J Neurochem 15:147–149
Sogbanmu TO, Osibona AO, Oguntunde OA, Otitoloju AA (2018) Biomarkers of toxicity in Clarias gariepinus exposed to sublethal concentrations of polycyclic aromatic hydrocarbons. Afr J Aquat Sci 43(3):281–292
Song SB, Xu Y, Zhou BS (2006) Effects of hexachlorobenzene on antioxidant status of liver and brain of common cap (Cyprinus carpio). Chemosphere 65:699–706
Terry B (2012) Plastic free: how I kicked the plastic habit and how you can too. Sky House Publishing, New York
Tiwari BSS (2015) Microplastics: the hidden contaminant in aquatic ecosystems. DOI: https://doi.org/10.13140/RG.2.1.1559.0566
Wagner T, Congleton JL (2004) Blood-chemistry correlates of nutritional condition, tissue damage, and stress in migrating juvenile Chinook salmon Oncorhynchus tshawytscha. Can J Fish Aquat Sci 61:1066–1074
World Economic Forum (2016) The new plastics economy: rethinking the future of plastics. Industry Agenda REF 080116. 34 p. Cologny/Geneva, Switzerland
Wright SL, Thompson RC, Galloway TS (2013) The physical impacts of microplastics on marine organisms: a review. Environ Pollut 178:483–492
Wu WM, Yang J, Criddle CS (2017) Microplastic pollution and reduction strategies. Front Environ Sci Eng 11(1):6–23. https://doi.org/10.1007/S11783-017-0897-7
Yaj AJ, Iheanacho SC, Ogueji EO (2018) Sublethal exposure and toxicity effect of propanil on haematology and serum biochemistry in Oreochromis niloticus in a static bioassay. Gazi Uni J Sci 31(4):1048–1062
Zhang C, Chen X, Wang J, Tan L (2017) Toxic effects of microplastic on marine microalgae Skeletonema costatum: interactions between microplastic and algae. Environ Pollut 220:1282–1288
Acknowledgements
The authors express their gratitude to the Department of Zoology and Environmental Biology, University of Nigeria Nsukka for their support during the conceptualization of the study. Prof. Dr. Johnny Ogunji is appreciated for critiquing the manuscript.
Funding
This research was supported by Tertiary Education Trust Fund, (TETfund, AE-FUNAI/AST &D/2018/2019) Nigeria.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict 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
About this article
Cite this article
Iheanacho, S.C., Odo, G.E. Dietary exposure to polyvinyl chloride microparticles induced oxidative stress and hepatic damage in Clarias gariepinus (Burchell, 1822). Environ Sci Pollut Res 27, 21159–21173 (2020). https://doi.org/10.1007/s11356-020-08611-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-08611-9