Abstract
Globally, the prevalence and pollution of pharmaceutical drugs in aquatic environments have been steadily increasing. This study sought to evaluate the effects of 14 days of exposure to environmental-relevant doses (ibuprofen 0.5, 5, and 50 µg/L, and carbamazepine 0.005, 1, and 10 µg/L) of the nonsteroidal anti-inflammatory drugs ibuprofen and carbamazepine in the freshwater fish Oreochromis mossambicus. The results showed a significant (P < 0.05) decrease in O. mossambicus superoxide dismutase, catalase, biotransformation enzymes, glutathione-s-transferase, glutathione peroxidase, oxidative stress lipid peroxidation, protein carbonyl activity, cellular damage metallothionine, reduced glutathione, immunological activities, and respiratory burst activity. Consequently, the acquired data revealed that O. mossambicus treated with ibuprofen and carbamazepine shows more significant alterations in metabolic depression, biochemical parameters, and oxidative stress. In addition, increased neurotoxic effects were observed in ibuprofen and carbamazepine treated O. mossambicus.
Graphical Abstract
Similar content being viewed by others
Data availability
The data presented in this study is contained within the article.
References
Andreozzi R, Raffaele M, Nicklas P (2003) Pharmaceuticals in STP effluents and their solar photodegradation in aquatic environment. Chemosphere 50(10):1319–1330. https://doi.org/10.1016/S0045-6535(02)00769-5
Bainy ACD, Marques MRF (2003) Global analysis of biomarker responses in aquatic organisms exposed to contaminants. Comments Toxicol 9:271–278. https://doi.org/10.1080/08865140390450368
Ballesteros ML, Wunderlin DA, Bistoni MA (2009) Oxidative stress responses in different organs of Jenynsia multidentata exposed to endosulfan. Ecotoxicol Environ Saf 72(1):199–205. https://doi.org/10.1016/j.ecoenv.2008.01.008
Bartoskova M, Dobsikova R, Stancova V, Zivna D, Blahova J, Marsalek P, Zelnickova L, Bartos M, Di Tocco FC, Faggio C (2013) Evaluation of ibuprofen toxicity for zebrafish (Danio rerio) targeting on selected biomarkers of oxidative stress. Neuro Endocrinol Lett 34(1):102–108
Bols NC, Brubacher JL, Ganassin RC, Lee LE (2001) Ecotoxicology and innate immunity in fish. Dev Comp Immunol 25(8–9):853–873. https://doi.org/10.1016/S0145-305X(01)00040-4
Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310. https://doi.org/10.1016/s0076-6879(78)52032-6
Cohen G, Dembiec D, Marcus J (1970) Measurement of catalase activity in tissue extracts. Anal Biochem 34:30–38. https://doi.org/10.1016/0003-2697(70)90083-7
Ellis AE (1990) Lysozyme assays. In: Stolen JS, Fletcher TC, Anderson DP, Roberson BS, van Muiswinkel WB (eds) Techniques in Fish Immunology. Fish Immunology Technical Communications, pp 101–103
Ellman GL, Courtney KD, Andres V Jr, Featherstone RM (1961) Featherstone. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95. https://doi.org/10.1016/0006-2952(61)90145-9
El-Sayed YS, Saad TT, El-Bahr SM (2007) Acute intoxication of deltamethrin in monosex Nile tilapia, Oreochromis niloticus with special reference to the clinical, biochemical and haematological effects. Enviro Toxicol Pharmacol 24(3):212–217. https://doi.org/10.1016/j.etap.2007.05.006
Fagan JM, Sleczka BG, Sohar I (1999) Quantitation of oxidative damage to tissue proteins. Int J Biochem Cell Biol 31(7):751–757. https://doi.org/10.1016/S1357-2725(99)00034-5
Fatima M, Mandiki SNM, Douxfils J, Silvestre F, Coppe P, Kestemont P (2007) Combined effects of herbicides on biomarkers reflecting immune–endocrine interactions in goldfish: immune and antioxidant effects. Aquat Toxicol 81(2):159–167. https://doi.org/10.1016/j.aquatox.2006.11.013
Fent K, Weston AA, Caminada D (2006) Ecotoxicology of human pharmaceuticals. Aquat Toxicol 76(2):122–159. https://doi.org/10.1016/j.aquatox.2005.09.009
Fick J, Lindberg RH, Parkkonen J, Arvidsson B, Tysklind M, Larsson DJ (2010) Therapeutic levels of levonorgestrel detected in blood plasma of fish: results from screening rainbow trout exposed to treated sewage effluents. Environ Sci Technol 44(7):2661–2666. https://doi.org/10.1021/es903440m
Gate L, Paul J, Ba GN, Tew KD, Tapiero H (1999) Oxidative stress induced in pathologies: the role of antioxidants. Biomed Pharmacother 53(4):169–180. https://doi.org/10.1016/S0753-3322(99)80086-9
Glassmeyer ST, Furlong ET, Kolpin DW, Cahill JD, Zaugg SD, Werner SL, Meyer MT, Kryak DD (2005) Transport of chemical and microbial compounds from known wastewater discharges: potential for use as indicators of human faecal contamination. Environ Sci Technol 39(14):5157–5169. https://doi.org/10.1021/es048120k
Gopi N, Vijayakumar S, Thaya R, Govindarajan M, Alharbi NS, Kadaikunnan S, Khaled JM, Al-Anbr MN, Vaseeharan B (2019) Chronic exposure of Oreochromis niloticus to sub-lethal copper concentrations: effects on growth, antioxidant, non-enzymatic antioxidant, oxidative stress and non-specific immune responses. J Trace Elem Med Biol 55:170–179. https://doi.org/10.1016/j.jtemb.2019.06.011
Heberer T (2002) Occurrence, fate, and removal of pharmaceutical residues in the aquatic environment: a review of recent research data. Toxicol Lett 131(1–2):5–17. https://doi.org/10.1016/S0378-4274(02)00041-3
Huang CH, Chang RJ, Huang SL, Chen W (2003) Dietary vitamin E supplementation affects tissue lipid peroxidation of hybrid tilapia, Oreochromis niloticus O. aureus. Comp Biochem Physiol Part C: Toxicol Pharmacol 134(2):265–70. https://doi.org/10.1016/S1096-4959(02)00256-7
Isik I, Celik I (2008) Acute effects of methyl parathion and diazinon as inducers for oxidative stress on certain biomarkers in various tissues of rainbow trout (Oncorhynchus mykiss). Pestic Biochem Phys 92(1):38–42. https://doi.org/10.1016/j.pestbp.2008.06.001
Jollow DJ, Mitchell JR, Zampaglione N, Gillette JR (1974) Bromobenzene induced liver necrosis. Protective role of glutathione and evidence for 3, 4-bromobenzene oxide as the hepato toxic metabolite. Pharmacol 11:151–169. https://doi.org/10.1159/000136485
Kumari J, Sahoo PK (2006) Dietary β-1, 3 glucan potentiates innate immunity and disease resistance of Asian catfish, Clarias batrachus (L.). J Fish Dis 29:95–101. https://doi.org/10.1111/j.1365-2761.2006.00691.x
Letzel M, Metzner G, Letzel T (2009) Exposure assessment of the pharmaceutical diclofenac based on long-term measurements of the aquatic input. Environ Int 35(2):363–368. https://doi.org/10.1016/j.envint.2008.09.002
Li ZH, Randak T (2009) Residual pharmaceutically active compounds (PhACs) in aquatic environment–status, toxicity and kinetics: a review. Vet Med 54(7):295–314. https://doi.org/10.17221/97/2009-VETMED
Li ZH, Velisek J, Zlabek V, Grabic R, Machova J, Kolarova J, Randak T (2010) Hepatic antioxidant status and haematological parameters in rainbow trout, Oncorhynchus mykiss, after chronic exposure to carbamazepine. Chem Biol Interact 183(1):98–104. https://doi.org/10.1016/j.cbi.2009.09.009
Li ZH, Zlabek V, Velisek J, Grabic R, Machova J, Kolarova J, Li P, Randak T (2011) Acute toxicity of carbamazepine to juvenile rainbow trout (Oncorhynchus mykiss): effects on antioxidant responses, haematological parameters and hepatic EROD. Ecotoxicol Environ Saf 74(3):319–327. https://doi.org/10.1016/j.ecoenv.2010.09.008
Lowry O, Rosebrough N, Farr A, Randall R (1951) Protein measurements with the folin phenol reagent. J Biol Chem 193:265–275. https://doi.org/10.1016/S0021-9258(19)52451-6
Magor BG, Magor KE (2001) Evolution of effectors and receptors of innate immunity. Dev Comp Immunol 25:651–682. https://doi.org/10.1016/S0145-305X(01)00029-5
Malarvizhi A, Kavitha C, Saravanan M, Ramesh M (2012) Carbamazepine (CBZ) induced enzymatic stress in gill, liver and muscle of a common carp, Cyprinus carpio. J King Saud Univ Sci 24(2):179–186. https://doi.org/10.1016/j.jksus.2011.01.001
Manoj K, Padhy PK (2013) Oxidative stress and heavy metals: an appraisal with reference to environmental biology. Int Res J Biol 2:91–101
Mathias FT, Fockink DH, Disner GR, Prodocimo V, Ribas JLC, Ramos LP, Cestari MM, de Assis HCS (2018) Effects of low concentrations of ibuprofen on freshwater fish Rhamdia quelen. Enviro Toxicol Pharmacol 59:105–113. https://doi.org/10.1016/j.etap.2018.03.008
Nakada N, Yasojima M, Okayasu Y, Komori K, Suzuki Y (2010) Mass balance analysis of triclosan, diethyltoluamide, crotamiton and carbamazepine in sewage treatment plant. Water Sci Technol 61(7):1739–1747. https://doi.org/10.2166/wst.2010.100
Nordberg J, Arnér ES (2001) Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic Biol Med 31(11):1287–1312. https://doi.org/10.1016/S0891-5849(01)00724-9
Patel A, Panter GH, Trollope HT, Glennon YC, Owen SF, Sumpter JPR, Weaver M (2016) Testing the “read-across hypothesis” by investigating the effects of ibuprofen on fish. Chemosphere 163:592–600. https://doi.org/10.1016/j.chemosphere.2016.08.041
Rezaei M, MashinchianMoradi A, Mortazavi P, Jamili S (2020) Effects of chronic exposure to carbamazepine on hematological parameters in Cyprinus carpio, Iran. J Fish Sci 19(1):443–56. https://doi.org/10.22092/ijfs.2019.119014
Reznick AZ, Packer L (1994) Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol 233:357–363. https://doi.org/10.1016/S0076-6879(94)33041-7
Roberts PH, Thomas KV (2006) The occurrence of selected pharmaceuticals in wastewater effluent and surface waters of the lower Tyne catchment. Sci Total Environ 356(1–3):143–153. https://doi.org/10.1016/j.scitotenv.2005.04.031
Rodríguez A, Esteban MÁ, Meseguer J (2003) Phagocytosis and peroxidase release by seabream (Sparus aurata L.) leucocytes in response to yeast cells. Anat Rec A Discov Mol Cell Evol Biol 272:415–424. https://doi.org/10.1002/ar.a.10048
Rotruck JT, Pope AL, Ganther HE, Swanson AB, Hafeman DG, Hoekstra W (1973) Selenium biochemical role as a component of glutathione peroxidase. Science 179:588–590. https://doi.org/10.1126/science.179.4073.588
Saravanan M, Devi KU, Malarvizhi A, Ramesh M (2012) Effects of Ibuprofen on hematological, biochemical and enzymological parameters of blood in an Indian major carp. Cirrhinus Mrigala Environ Toxicol Pharmacol 34(1):14–22. https://doi.org/10.1016/j.etap.2012.02.005
Secombes C (1990) Isolation of salmonid macrophages and analysis of their killing activity. In: Stolen JS, Fletcher TC, Anderson DP, Robertsen BS, van Muiswinkel WB (eds) Techniques in Fish Immunology. Fish Immunology Technical Communications, pp 137–154
Shacter E (2000) Quantification and significance of protein oxidation in biological samples. Drug Metab Rev 32(3–4):307–326. https://doi.org/10.1081/DMR-100102336
Storey KB (1996) Oxidative stress: animal adaptations in nature. Braz J Med Biol 29:1715–1733
Stumpf M, Ternes TA, Wilken RD, Rodrigues SV, Baumann W (1999) Polar drug residues in sewage and natural waters in the state of Rio de Janeiro, Brazil. Sci Total Environ 225(1–2):135–141. https://doi.org/10.1016/S0048-9697(98)00339-8
Ternes TA (1998) Occurrence of drugs in German sewage treatment plants and rivers. Water Res 32(11):3245–3260. https://doi.org/10.1016/S0043-1354(98)00099-2
Van der Oost R, Beyer J, Vermeulen NP (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Enviro Toxicol Pharmacol 13(2):57–149. https://doi.org/10.1016/S1382-6689(02)00126-6
Viarengo A, Ponzano E, Dondero F, Fabbri R (1997) A simple spectrophotometric method for metallothionein evaluation in marine organisms: an application to Mediterranean and Antarctic molluscs. Mar Environ Res 44:69–84. https://doi.org/10.1016/S0141-1136(96)00103-1
Xia L, Zheng L, Zhou JL (2017) Effects of ibuprofen, diclofenac and paracetamol on hatch and motor behavior in developing zebrafish (Danio rerio). Chemosphere 182:416–425. https://doi.org/10.1016/j.chemosphere.2017.05.054
Ying GG, Kookana RS, Kolpin DW (2009) Occurrence and removal of pharmaceutically active compounds in sewage treatment plants with different technologies. J Environ Moni 11(8):1498–1505. https://doi.org/10.1039/B904548A
Acknowledgements
The authors would like to thank and acknowledge the Ministry of Human Resource Development, Government of India, and Alagappa University, Karaikudi, for providing support in RUSA Phase 2.0 grant sanctioned No. F.24-51/ 2014-U, Policy (TNMulti-Gen), Dept. of Edn. Govt of India. The authors express their sincere appreciation to the Researchers Supporting Project Number (RSP2023R436) King Saud University, Riyadh, Saudi Arabia.
Funding
This study is supported by the Researchers Supporting Project Number (RSP2023R436) King Saud University, Riyadh, Saudi Arabia.
Author information
Authors and Affiliations
Contributions
Ashokkumar Sibiya: conceptualization, methodology, software; Jeyaraj Jeyavani: formal analysis; Manoharan Saravanan: formal analysis; Mohammed F Albeshr: resources, visualization, validation; Marcello Nicoletti: writing—review and editing; Marimuthu Govindarajan: writing—review and editing; Baskaralingam Vaseeharan: conceptualization, visualization, validation.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Ethical approval
Not applicable.
Consent for publication
All authors agree to submit the paper for publication in the Journal of Fish Physiology and Biochemistry.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Sibiya, A., Jeyavani, J., Saravanan, M. et al. Response of hepatic biochemical parameters and neurotoxicity to carbamazepine and ibuprofen in Oreochromis mossambicus. Fish Physiol Biochem 49, 787–799 (2023). https://doi.org/10.1007/s10695-023-01172-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-023-01172-x