Abstract
Heavy metal accumulation changes the immune system and leads to oxidative damage in aquatic animals. The present study evaluated the correlation between heavy metal accumulation, with immunological and oxidative stress parameters, in various species in the aquatic environment of Western Iran. Fresh samples included fish (trout and carp) and shrimp obtained from Sanandaj aquaculture. After blood sampling and serum isolation for immunological study, meat sections of these animals were used to measure heavy metal concentrations to determine the oxidative stress and immunological parameters. The highest concentrations of Pb (0.82 ± 0.10), As (0.53 ± 0.18), Hg (0.47 ± 0.08), and Zn (28.77 ± 1.88) (µg/g) were found in trout, while the lowest accumulation of heavy metals except for Cd (0.24 ± 0.11) and Se (1.57 ± 0.42) (µg/g) were observed in shrimp. The antioxidant enzymes glutathione peroxidase (GPx) (1.89 ± 0.13) and superoxide dismutase (SOD) (1.96 ± 0.62) U/mg showed the highest concentrations in shrimp and lowest in the trout. Significant negative correlations were found between these enzymes with As and Pb in trout and carp. A significant positive correlation was determined between Se and Zn with GPx and a negative correlation with malondialdehyde (MDA) in shrimp. Immunological biomarkers indicated the concentrations of IL-6, TNF-α, and IFN-Ƴ were higher in fish than in shrimp, and the lowest IgM level was obtained in Shrimp. Increased Pb and Cd showed a significant relationship with increased IL-6 and TNF-α in trout compared to shrimp and carp. An increase in As and Se concentration beyound maximum permissible limits (MPL) were recorded in fish and shrimp, while a Zn level less than MPL was recorded. The target hazard quotients (THQ) and target cancer risk (TR) values of non-essential heavy metals were obtained under acceptable ranges. We suggest reducing the As and Pb content under aquaculture farms and increase in the amount of Zn through diets to keep healthy immunological and physiological conditions for aquatic species in the west of Iran.
Similar content being viewed by others
Data Availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Shrestha R et al (2021) Technological trends in heavy metals removal from industrial wastewater: a review. J Environ Chem Eng 9(4):105688
Isangedighi IA, David GS (2019) Heavy metals contamination in fish: effects on human health. J Aquat Sci Mar Biol 2(4):7–12
Kanu I, Achi O (2011) Industrial effluents and their impact on water quality of receiving rivers in Nigeria. J Appl Technol Environ Sanitation 1(1):75–86
Raeeszadeh M, Fallah M (2018) The comparison of the effect of origanum vulgar aqueous extract and vitamin C on the control of cadmium chloride damage in testicular tissue in male rats. J Babol Univ Med Sci 20(8):44–50
Taslima K et al (2022) Impacts of heavy metals on early development, growth and reproduction of fish–a review. Toxicol Rep 9:858–868
Chowdhury S, Saikia S (2020) Oxidative stress in fish: a review. J Sci Res 12(1):145–160
Raeeszadeh M et al (2022) The comparison of the effect of Origanum vulgare L. extract and vitamin C on the gentamycin-induced nephrotoxicity in rats. Drug Chem Toxicol 45(5):2031–2038
Theron AJ, Tintinger GR, Anderson R (2012) Harmful interactions of non-essential heavy metals with cells of the innate immune system. J Toxicol Clin S 3:005
Ebrahimi M et al (2020) Effects of lead and cadmium on the immune system and cancer progression. J Environ Health Sci Eng 18(1):335–343
Valaperti A et al (2020) Diagnostic methods for the measurement of human TNF-alpha in clinical laboratory. J Pharm Biomed Anal 179:113010
Zou J et al (2005) Identification and bioactivities of IFN-γ in rainbow trout Oncorhynchus mykiss: the first Th1-type cytokine characterized functionally in fish. J Immunol 175(4):2484–2494
Colosio C et al (2005) Low level exposure to chemicals and immune system. Toxicol Appl Pharmacol 207(2):320–328
Rajeshkumar S et al (2017) Effects of exposure to multiple heavy metals on biochemical and histopathological alterations in common carp, Cyprinus carpio L. Fish Shellfish Immunol 70:461–472
Sevcikova M et al (2011) Metals as a cause of oxidative stress in fish: a review. Vet Med 56(11):537–546
Akinsanya B et al (2020) Heavy metals, parasitologic and oxidative stress biomarker investigations in Heterotis niloticus from Lekki Lagoon, Lagos, Nigeria. Toxicol Rep 7:1075–1082
Raeeszadeh M, Gravandi H, Akbari A (2022) Determination of some heavy metals levels in the meat of animal species (sheep, beef, turkey, and ostrich) and carcinogenic health risk assessment in Kurdistan province in the west of Iran. Environ Sci Pollut Res Int 29(41):62248–62258. https://doi.org/10.1007/s11356-022-19589-x
Liu HP, Watts BM (1970) Catalysts of lipid peroxidation in meats. 3. Catalysts of oxidative rancidity in meats. J Food Sci 35(5):596–598
Brucka-Jastrzębska E (2010) The effect of aquatic cadmium and lead pollution on lipid peroxidation and superoxide dismutase activity in freshwater fish. Pol J Environ Stud 19(6):1139–1150
Vlahogianni T et al (2007) Integrated use of biomarkers (superoxide dismutase, catalase and lipid peroxidation) in mussels Mytilus galloprovincialis for assessing heavy metals’ pollution in coastal areas from the Saronikos Gulf of Greece. Mar Pollut Bull 54(9):1361–1371
Raeeszadeh M et al (2021) Protective effect of nano-vitamin C on infertility due to oxidative stress induced by lead and arsenic in male rats. J Chem 2021. https://doi.org/10.1155/2021/9589345
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(1–2):248–254
Haahr P et al (1991) Effect of physical exercise on in vitro production of interleukin 1, interleukin 6, tumour necrosis factor-α, interleukin 2 and interferon-γ. Int J Sports Med 12(02):223–227
Kane AE et al (2019) A murine frailty index based on clinical and laboratory measurements: links between frailty and pro-inflammatory cytokines differ in a sex-specific manner. J Gerontol A 74(3):275–282
Gan Z et al (2020) Fish type I and type II interferons: composition, receptor usage, production and function. Rev Aquac 12(2):773–804
Tellez-Bañuelos MC et al (2010) Endosulfan increases seric interleukin-2 like (IL-2L) factor and immunoglobulin M (IgM) of Nile tilapia (Oreochromis niloticus) challenged with Aeromona hydrophila. Fish Shellfish Immunol 28(2):401–405
Hikima J-i et al (2001) Molecular cloning, expression and evolution of the Japanese flounder goose-type lysozyme gene, and the lytic activity of its recombinant protein. Biochim Biophys Acta Gene Struct Expr 1520(1):35–44
Jezierska B, Witeska M (2006) The metal uptake and accumulation in fish living in polluted waters. soil and water pollution monitoring, protection and remediation. Springer, pp 107–114
Khabbazi M et al (2014) Histopathology of rainbow trout gills after exposure to copper. Iran J Ichthyol 1(3):191–196
Strungaru S-A et al (2018) Patterns of toxic metals bioaccumulation in a cross-border freshwater reservoir. Chemosphere 207:192–202
Moghadasi M, Heshmati A, Vahidinia A (2021) Measurement of heavy metals (nickel, chromium, and cobalt) in wild and farmed carps (Cyprinus carpio) of Hamadan Province. Avicenna J Environ Health Eng 8(2):97–101
Zahra K et al (2012) Determination of Cd, Pb, Hg, Cu, Fe, Mn, Al, As, Ni and Zn in important commercial fish species in northern of Persian Gulf. J Cell Anim Biol 6(1):1–9
Fakhri Y et al (2018) Systematic review and health risk assessment of arsenic and lead in the fished shrimps from the Persian gulf. Food Chem Toxicol 113:278–286
Heidarieh M et al (2013) Evaluate of heavy metal concentration in shrimp (Penaeus semisulcatus) and crab (Portunus pelagicus) with INAA method. Springerplus 2(1):1–5
Kaya G, Turkoglu S (2018) Toxic and essential metals in Cyprinus carpio, Carassius gibelio, and Luciobarbus esocinus tissues from Keban Dam Lake, Pertek, Turkey. Food Addit Contam B 11(1):1–8
Kaya G, Turkoglu S (2017) Bioaccumulation of heavy metals in various tissues of some fish species and green tiger shrimp (Penaeus semisulcatus) from İskenderun Bay, Turkey, and risk assessment for human health. Biol Trace Elem Res 180(2):314–326
Álvarez-González C et al (2020) Effects on the growth and digestive enzyme activity in Nile tilapia fry (Oreochromis niloticus) by lead exposure. Water Air Soil Pollut 231(9):1–15
Zhao L et al (2020) Toxic effects of waterborne lead (Pb) on bioaccumulation, serum biochemistry, oxidative stress and heat shock protein-related genes expression in Channa argus. Chemosphere 261:127714
Guo J et al (2021) Lead impaired immune function and tissue integrity in yellow catfish (Peltobargus fulvidraco) by mediating oxidative stress, inflammatory response and apoptosis. Ecotoxicol Environ Saf 226:112857
Shi B et al (2021) Dietary organic zinc promotes growth, immune response and antioxidant capacity by modulating zinc signaling in juvenile Pacific white shrimp (Litopenaeus vannamei). Aquaculture Reports 19:100638
Ogawa D et al (2011) High glucose increases metallothionein expression in renal proximal tubular epithelial cells. Exp Diabetes Res 2011:534872. https://doi.org/10.1155/2011/534872
Lin S et al (2013) Comparison of chelated zinc and zinc sulfate as zinc sources for growth and immune response of shrimp (Litopenaeus vannamei). Aquaculture 406:79–84
Metryka E et al (2018) Lead (Pb) exposure enhances expression of factors associated with inflammation. Int J Mol Sci 19(6):1813
Zahran E, Risha E (2014) Modulatory role of dietary Chlorella vulgaris powder against arsenic-induced immunotoxicity and oxidative stress in Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 41(2):654–662
Wang X et al (2021) Systemic inflammation mediates the association of heavy metal exposures with liver injury: a study in general Chinese urban adults. J Hazard Mater 419:126497
Acknowledgements
The authors would like to sincerely appreciate the Research Vice-Chancellor at the Islamic Azad University, Sanandaj Branch, for the collaboration to facilitate research.
Author information
Authors and Affiliations
Contributions
Conceptualization, data curation, formal analysis, investigation, methodology, and project administration: M. R and S. P. Software, supervision, validation, and visualization: M. R. Writing—original draft: M. R and F.T. Writing—review and editing: A.J and B. S.
Corresponding author
Ethics declarations
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
Raeeszadeh, M., Khoei, A.J., Parhizkar, S. et al. Assessment of Some Heavy Metals and Their Relationship with Oxidative Stress and Immunological Parameters in Aquatic Animal Species. Biol Trace Elem Res 201, 4547–4557 (2023). https://doi.org/10.1007/s12011-022-03507-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12011-022-03507-w