Skip to main content
SpringerLink
Log in

Trace Metals in the Freshwater Fish Cyprinus carpio: Effect to Serum Biochemistry and Oxidative Status Markers

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Interactions between trace metals, serum biochemical parameters, and oxidative status markers were observed. Freshwater fish Cyprinuscarpio blood samples (n = 38) were collected at the beginning of May (n = 19) and at the end of July (n = 19) of 2015. The concentrations of metals (As, Cd, Cr, Cu, Fe, Mn, Ni, Pb, Se, Sr, and Zn) were analyzed in blood serum samples of fishes by inductively coupled plasma optical emission spectrometry (ICP-OES), and Hg was determined by cold-vapor atomic absorption spectroscopy (CV-AAS). The general scheme of descending concentrations of metals in blood serum samples was as follows: Zn > Fe > Cu > Sr > Cr > Ni > Mn > Pb > Se > As > Cd > Hg. Zn was the most accumulated element (4.42–119.64 mg/L) in both seasons. Overall, the trace element content was higher in spring season, except Hg, Ni, Se, and Sr. The seasonal effect was confirmed for Mn, Zn, Mg, Glu, AST, and Chol levels and for most oxidative status markers. The gender effect was confirmed for Sr, GPx, PC, Chol, and CK concentrations. Trace metals (especially Cd, Cr, Cu, Fe, Hg, Mn, Ni, Sr, Zn, As) significantly affected some blood serum chemistry parameters. The correlation analysis between oxidative status markers (ROS, TAC, MDA, SOD, GSH, UA, BHB, and Alb) and trace metal (Cd, Cu, Ni, Sr, Hg, Pb, Fe, Mn) content confirmed statistically significant interactions in both seasons. Obtained results indicate specific actions of trace metals.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  1. Gupta, R. C. (2014) Biomarkers in toxicology, first ed. Academic Press. pages

  2. Binkowski ŁJ, Sawicka-Kapusta K, Szarek J, Strzyżewska E, Felsmann M (2013) Histopathology of liver and kidneys of wild living Mallards Anas platyrhynchos and Coots Fulica atra with considerable concentrations of lead and cadmium. Sci Total Environ 450:326–333. https://doi.org/10.1016/j.scitotenv.2013.02.002

    Article  CAS  PubMed  Google Scholar 

  3. Duarte CA, Giarratano E, Amin OA, Comoglio LI (2011) Heavy metal concentrations and biomarkers of oxidative stress in native mussels (Mytilus edulis chilensis) from Beagle Channel coast (Tierra del Fuego, Argentina). Mar Pollut Bull 62(8):1895–1904. https://doi.org/10.1016/j.marpolbul.2011.05.031

    Article  CAS  PubMed  Google Scholar 

  4. Fırat Ö, Kargın F (2010) Individual and combined effects of heavy metals on serum biochemistry of Nile tilapia Oreochromis niloticus. Arch Environ Contam Toxicol 58(1):151–157. https://doi.org/10.1007/s00244-009-9344-5

    Article  CAS  PubMed  Google Scholar 

  5. Giarratano E, Gil MN, Marinho CH, Malanga G (2016) Metals from mine waste as potential cause of oxidative stress in burrowing crab Neohelice granulata from San Antonio bay. Ecotoxicol Environ Saf 132:68–76. https://doi.org/10.1016/j.ecoenv.2016.05.029

    Article  CAS  PubMed  Google Scholar 

  6. Kovacik A, Arvay J, Tusimova E, Harangozo L, Tvrda E, Zbynovska K, Cupka P, Andrascikova S, Tomas J, Massanyi P (2017) Seasonal variations in the blood concentration of selected heavy metals in sheep and their effects on the biochemical and hematological parameters. Chemosphere 168:365–371. https://doi.org/10.1016/j.chemosphere.2016.10.090

    Article  CAS  PubMed  Google Scholar 

  7. Massanyi P, Stawarz R, Halo M, Formicki G, Lukac N, Cupka P, Schwarz P, Kovacik A, Tusimova E, Kovacik J (2014) Blood concentration of copper, cadmium, zinc and lead in horses and its relation to hematological and biochemical parameters. J Environ Sci Health, Part A: Tox Hazard Subst Environ Eng 49(8):973–979 https://doi.org/10.1080/10934529.2014.894322

    Article  CAS  Google Scholar 

  8. Mohanty D, Samanta L (2016) Multivariate analysis of potential biomarkers of oxidative stress in Notopterus notopterus tissues from Mahanadi River as a function of concentration of heavy metals. Chemosphere 155:28–38. https://doi.org/10.1016/j.chemosphere.2016.04.035

    Article  CAS  PubMed  Google Scholar 

  9. Pilote M, André C, Turcotte P, Gagné F, Gagnon C (2018) Metal bioaccumulation and biomarkers of effects in caged mussels exposed in the Athabasca oil sands area. Sci Total Environ 610:377–390. https://doi.org/10.1016/j.scitotenv.2017.08.023

    Article  CAS  PubMed  Google Scholar 

  10. Ruas CBG, dos Santos Carvalho C, de Araújo HSS, Espíndola ELG, Fernandes MN (2008) Oxidative stress biomarkers of exposure in the blood of cichlid species from a metal-contaminated river. Ecotoxicol Environ Saf 71(1):86–93. https://doi.org/10.1016/j.ecoenv.2007.08.018

    Article  CAS  PubMed  Google Scholar 

  11. Falandysz J, Wyrzykowska B, Warzocha J, Barska I, Garbacik-Wesołowska A, Szefer P (2004) Organochlorine pesticides and PCBs in perch Perca fluviatilis from the Odra/Oder river estuary, Baltic Sea. Food Chem 87(1):17–23. https://doi.org/10.1016/j.foodchem.2003.10.011

    Article  CAS  Google Scholar 

  12. Kaya H, Çelik EŞ, Yılmaz S, Tulgar A, Akbulut M, Demir N (2015) Hematological, serum biochemical, and immunological responses in common carp (Cyprinus carpio) exposed to phosalone. Comp Clin Pathol 24(3):497–507. https://doi.org/10.1007/s00580-014-1930-x

    Article  CAS  Google Scholar 

  13. Sepici-Dinçel A, Benli AÇK, Selvi M, Sarıkaya R, Şahin D, Özkul IA, Erkoç F (2009) Sublethal cyfluthrin toxicity to carp (Cyprinus carpio L.) fingerlings: biochemical, hematological, histopathological alterations. Ecotoxicol Environ Saf 72(5):1433–1439. https://doi.org/10.1016/j.ecoenv.2009.01.008

    Article  CAS  PubMed  Google Scholar 

  14. Slaninova A, Smutna M, Modra H, Svobodova Z (2009) Oxidative stress in fish induced by pesticides. Neuroendocrinol Lett 30(1):2

    CAS  PubMed  Google Scholar 

  15. Corcoran J, Winter MJ, Tyler CR (2010) Pharmaceuticals in the aquatic environment: a critical review of the evidence for health effects in fish. Crit Rev Toxicol 40(4):287–304. https://doi.org/10.3109/10408440903373590

    Article  CAS  PubMed  Google Scholar 

  16. Nunes B, Carvalho F, Guilhermino L (2006) Effects of widely used pharmaceuticals and a detergent on oxidative stress biomarkers of the crustacean Artemia parthenogenetica. Chemosphere 62(4):581–594. https://doi.org/10.1016/j.chemosphere.2005.06.013

    Article  CAS  PubMed  Google Scholar 

  17. Rodrigues S, Antunes SC, Correia AT, Nunes B (2016) Acute and chronic effects of erythromycin exposure on oxidative stress and genotoxicity parameters of Oncorhynchus mykiss. Sci Total Environ 545:591–600. https://doi.org/10.1016/j.scitotenv.2015.10.138

    Article  CAS  PubMed  Google Scholar 

  18. Jambor T, Tvrdá E, Tušimová E, Kováčik A, Bistáková J, Forgács Z, Lukáč N (2017) In vitro effect of 4-nonylphenol on human chorionic gonadotropin (hCG) stimulated hormone secretion, cell viability and reactive oxygen species generation in mice Leydig cells. Environ Pollut 222:219–225. https://doi.org/10.1016/j.envpol.2016.12.053

    Article  CAS  PubMed  Google Scholar 

  19. Mills LJ, Chichester C (2005) Review of evidence: are endocrine-disrupting chemicals in the aquatic environment impacting fish populations? Sci Total Environ 343(1):1–34. https://doi.org/10.1016/j.scitotenv.2004.12.070

    Article  CAS  PubMed  Google Scholar 

  20. Árvay J, Tomáš J, Hauptvogl M, Kopernická M, Kováčik A, Bajčan D, Massányi P (2014) Contamination of wild-grown edible mushrooms by heavy metals in a former mercury-mining area. J Environ Sci Heal B 49(11):815–827. https://doi.org/10.1080/03601234.2014.938550

    Article  CAS  Google Scholar 

  21. Bernet D, Schmidt H, Wahli T, Burkhardt-Holm P (2001) Effluent from a sewage treatment works causes changes in serum chemistry of brown trout (Salmo trutta L.). Ecotoxicol Environ Saf 48(2):140–147. https://doi.org/10.1006/eesa.2000.2012

    Article  CAS  PubMed  Google Scholar 

  22. de Oliveira LF, Cabral MT, Vieira CED, Antoniazzi MH, Risso WE, dos Reis Martinez CB (2016) Metals bioaccumulation and biomarkers responses in the Neotropical freshwater clam Anodontites trapesialis: implications for monitoring coal mining areas. Sci Total Environ 571:983–991. https://doi.org/10.1016/j.scitotenv.2016.07.086

    Article  CAS  PubMed  Google Scholar 

  23. Javed M, Ahmad I, Usmani N, Ahmad M (2016) Bioaccumulation, oxidative stress and genotoxicity in fish (Channa punctatus) exposed to a thermal power plant effluent. Ecotoxicol Environ Saf 127:163–169. https://doi.org/10.1016/j.ecoenv.2016.01.007

    Article  CAS  PubMed  Google Scholar 

  24. Brumbaugh WG, Schmitt CJ, May TW (2005) Concentrations of cadmium, lead, and zinc in fish from mining-influenced waters of northeastern Oklahoma: sampling of blood, carcass, and liver for aquatic biomonitoring. Arch Environ Contam Toxicol 49(1):76–88. https://doi.org/10.1007/s00244-004-0172-3

    Article  CAS  PubMed  Google Scholar 

  25. Canli EG, Canli M (2015) Low water conductivity increases the effects of copper on the serum parameters in fish (Oreochromis niloticus). Environ Toxicol Pharmacol 39(2):606–613. https://doi.org/10.1016/j.etap.2014.12.019

    Article  CAS  PubMed  Google Scholar 

  26. Gopal V, Parvathy S, Balasubramanian PR (1997) Effect of heavy metals on the blood protein biochemistry of the fish Cyprinus carpio and its use as a bio-indicator of pollution stress. Environ Monit Assess 48(2):117–124. https://doi.org/10.1023/A:1005767517819

    Article  CAS  Google Scholar 

  27. Öner M, Atli G, Canli M (2008) Changes in serum biochemical parameters of freshwater fish Oreochromis niloticus following prolonged metal (Ag, Cd, Cr, Cu, Zn) exposures. Environ Toxicol Chem 27(2):360–366. https://doi.org/10.1897/07-281R.1

    Article  PubMed  Google Scholar 

  28. Abarikwu SO, Essien EB, Iyede OO, John K, Mgbudom-Okah C (2017) Biomarkers of oxidative stress and health risk assessment of heavy metal contaminated aquatic and terrestrial organisms by oil extraction industry in Ogale, Nigeria. Chemosphere 185:412–422. https://doi.org/10.1016/j.chemosphere.2017.07.024

    Article  CAS  PubMed  Google Scholar 

  29. Eyckmans M, Celis N, Horemans N, Blust R, De Boeck G (2011) Exposure to waterborne copper reveals differences in oxidative stress response in three freshwater fish species. Aquat Toxicol 103(1):112–120. https://doi.org/10.1016/j.aquatox.2011.02.010

    Article  CAS  PubMed  Google Scholar 

  30. Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101(1):13–30. https://doi.org/10.1016/j.aquatox.2010.10.006

    Article  CAS  PubMed  Google Scholar 

  31. Livingstone DR (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42(8):656–666

    Article  CAS  Google Scholar 

  32. Zbynovska K, Petruska P, Kalafova A, Ondruska L, Jurcik R, Chrastinova L, Tusimova E, Kovacik A, Capcarova M (2016) Antioxidant status of rabbits after treatment with epicatechin and patulin. Biologia 71(7):835–842

    Article  CAS  Google Scholar 

  33. Eroglu A, Dogan Z, Kanak EG, Atli G, Canli M (2015) Effects of heavy metals (Cd, Cu, Cr, Pb, Zn) on fish glutathione metabolism. Environ Sci Pollut Res 22(5):3229–3237. https://doi.org/10.1007/s11356-014-2972-y

    Article  CAS  Google Scholar 

  34. Sies H (1997) Oxidative stress: oxidants and antioxidants. Exp Physiol 82(2):291–295. https://doi.org/10.1113/expphysiol.1997.sp004024

    Article  CAS  PubMed  Google Scholar 

  35. Sedlak TW, Saleh M, Higginson DS, Paul BD, Juluri KR, Snyder SH (2009) Bilirubin and glutathione have complementary antioxidant and cytoprotective roles. Proc Natl Acad Sci 106(13):5171–5176. https://doi.org/10.1073/pnas.0813132106

    Article  PubMed  Google Scholar 

  36. Tvrdá E, Tušimová E, Kováčik A, Paál D, Greifová H, Abdramanov A, Lukáč N (2016a) Curcumin has protective and antioxidant properties on bull spermatozoa subjected to induced oxidative stress. Anim Reprod Sci 172:10–20. https://doi.org/10.1016/j.anireprosci.2016.06.008

    Article  CAS  PubMed  Google Scholar 

  37. Tvrdá E, Tušimová E, Kováčik A, Paál D, Libová Ľ, Lukáč N (2016b) Protective effects of quercetin on selected oxidative biomarkers in bovine spermatozoa subjected to ferrous ascorbate. Reprod Domest Anim 51(4):524–537. https://doi.org/10.1111/rda.12714

    Article  CAS  PubMed  Google Scholar 

  38. Kolesarova, A., Slamecka, J., Jurcik, R., Tataruch, F., Lukac, N., Kovacik, J., Capcarova, M., Valent, M., Massanyi, P. (2008). Environmental levels of cadmium , lead and mercury in brown hares and their relation to blood metabolic parameters. J Environ Sci Health, Part A: Tox Hazard Subst Environ Eng, 43, 646–650. https://doi.org/10.1080/10934520801893741

  39. Kashou, A. H., Sharma, R., & Agarwal, A. (2013). Assessment of oxidative stress in sperm and semen. Spermatogenesis: Methods and Protocols, 351–361. doi https://doi.org/10.1007/978-1-62703-038-0_30

  40. Muller, C. H., Lee, T. K. Y., & Montaño, M.A. (2013). Improved chemiluminescence assay for measuring antioxidant capacity of seminal plasma. In Carrell, D. A., & Aston, K. I. (2013). Spermatogenesis. Methods and Protocols (1st ed.). New York, NY: Springer Science+Business Media. pp. 363–376. https://doi.org/10.1007/978-1-62703-038-0_31

  41. Beers RF, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195(1):133–140

    CAS  PubMed  Google Scholar 

  42. Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82(1):70–77. https://doi.org/10.1016/0003-9861(59)90090-6

    Article  CAS  PubMed  Google Scholar 

  43. Tvrda E, Mackovich A, Greifova H, Hashim F, Lukac N (2017) Antioxidant effects of lycopene on bovine sperm survival and oxidative profile following cryopreservation. Vet Med 62(8). https://doi.org/10.17221/86/2017-VETMED

  44. Weber D, Davies MJ, Grune T (2015) Determination of protein carbonyls in plasma, cell extracts, tissue homogenates, isolated proteins: focus on sample preparation and derivatization conditions. Redox Biol 5:367–380. https://doi.org/10.1016/j.redox.2015.06.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Andreji J, Stranai I, Massanyi P, Valent M (2006) Accumulation of some metals in muscles of five fish species from lower Nitra River. J Environ Sci Heal A 41(11):2607–2622. https://doi.org/10.1080/10934520600928003

    Article  CAS  Google Scholar 

  46. Canli M, Atli G (2003) The relationships between heavy metal (Cd, Cr, Cu, Fe, Pb, Zn) levels and the size of six Mediterranean fish species. Environ Pollut 121(1):129–136. https://doi.org/10.1016/S0269-7491(02)00194-X

    Article  CAS  PubMed  Google Scholar 

  47. Jarić I, Višnjić-Jeftić Ž, Cvijanović G, Gačić Z, Jovanović L, Skorić S, Lenhardt M (2011) Determination of differential heavy metal and trace element accumulation in liver, gills, intestine and muscle of sterlet (Acipenser ruthenus) from the Danube River in Serbia by ICP-OES. Microchem J 98(1):77–81. https://doi.org/10.1016/j.microc.2010.11.008

    Article  CAS  Google Scholar 

  48. Karadede H, Ünlü E (2000) Concentrations of some heavy metals in water, sediment and fish species from the Atatürk Dam Lake (Euphrates), Turkey. Chemosphere 41(9):1371–1376. https://doi.org/10.1016/S0045-6535(99)00563-9

    Article  CAS  PubMed  Google Scholar 

  49. Malik N, Biswas AK, Qureshi TA, Borana K, Virha R (2010) Bioaccumulation of heavy metals in fish tissues of a freshwater lake of Bhopal. Environ Monit Assess 160(1):267–276. https://doi.org/10.1007/s10661-008-0693-8

    Article  CAS  PubMed  Google Scholar 

  50. Mendil D, Ünal ÖF, Tüzen M, Soylak M (2010) Determination of trace metals in different fish species and sediments from the River Yeşilırmak in Tokat, Turkey. Food Chem Toxicol 48(5):1383–1392. https://doi.org/10.1016/j.fct.2010.03.006

    Article  CAS  PubMed  Google Scholar 

  51. Tóth T, Andreji J, Tóth J, Slávik M, Árvay J, Stanovic R (2012) Cadmium, lead and mercury content in fishes—case study. J Microbiol, Biotechnol Food Sci 1:837–847

    Google Scholar 

  52. Vinodhini R, Narayanan M (2008) Bioaccumulation of heavy metals in organs of fresh water fish Cyprinus carpio (common carp). Int J Environ Sci Technol 5(2):179–182. https://doi.org/10.1007/BF03326011

    Article  CAS  Google Scholar 

  53. Adams DH, Sonne C, Basu N, Dietz R, Nam DH, Leifsson PS, Jensen AL (2010) Mercury contamination in spotted seatrout, Cynoscion nebulosus: an assessment of liver, kidney, blood, and nervous system health. Sci Total Environ 408(23):5808–5816. https://doi.org/10.1016/j.scitotenv.2010.08.019

    Article  CAS  PubMed  Google Scholar 

  54. 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. https://doi.org/10.1016/j.aquatox.2014.02.008

    Article  CAS  PubMed  Google Scholar 

  55. Çoğun H, Yüzereroğlu TA, Kargin F, Firat Ö (2005) Seasonal variation and tissue distribution of heavy metals in shrimp and fish species from the Yumurtalik coast of Iskenderun Gulf, Mediterranean. Bull Environ Contam Toxicol 75(4):707–715. https://doi.org/10.1007/s00128-005-0809-6

    Article  CAS  PubMed  Google Scholar 

  56. Rotchell JM, Clarke KR, Newton LC, Bird DJ (2001) Hepatic metallothionein as a biomarker for metal contamination: age effects and seasonal variation in European flounders (Pleuronectes flesus) from the Severn Estuary and Bristol Channel. Mar Environ Res 52(2):151–171. https://doi.org/10.1016/S0141-1136(00)00270-1

    Article  CAS  PubMed  Google Scholar 

  57. Al-Yousuf MH, El-Shahawi MS, Al-Ghais SM (2000) Trace metals in liver, skin and muscle of Lethrinus lentjan fish species in relation to body length and sex. Sci Total Environ 256(2):87–94. https://doi.org/10.1016/S0048-9697(99)00363-0

    Article  CAS  PubMed  Google Scholar 

  58. Squadrone S, Prearo M, Brizio P, Gavinelli S, Pellegrino M, Scanzio T, Abete MC (2013) Heavy metals distribution in muscle, liver, kidney and gill of European catfish (Silurus glanis) from Italian rivers. Chemosphere 90(2):358–365. https://doi.org/10.1016/j.chemosphere.2012.07.028

    Article  CAS  PubMed  Google Scholar 

  59. Borges, A., Scotti, L. V, Siqueira, D. R., Jurinitz, D. F., & Wassermann, G. F. (2004). Hematologic and serum biochemical values for jundiá (Rhamdia quelen). Fish Physiol Biochem, 30(2004), 21–25

  60. Groff JM, Zinkl JG (1999) Hematology and clinical chemistry of cyprinid fish: common carp and goldfish. Vet Clin North Am Exot Anim Pract 2(3):741–776. https://doi.org/10.1016/S1094-9194(17)30120-2

    Article  CAS  PubMed  Google Scholar 

  61. Javed M, Usmani N (2013) Assessment of heavy metal (Cu, Ni, Fe, Co, Mn, Cr, Zn) pollution in effluent dominated rivulet water and their effect on glycogen metabolism and histology of Mastacembelus armatus. SpringerPlus 2(1):390. https://doi.org/10.1186/2193-1801-2-390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Datta S, Saha DR, Ghosh D, Majumdar T, Bhattacharya S, Mazumder S (2007) Sub-lethal concentration of arsenic interferes with the proliferation of hepatocytes and induces in vivo apoptosis in Clarias batrachus L. Comp Biochem Physiol C: Toxicol Pharmacol 145(3):339–349

    Google Scholar 

  63. Yang JL, Chen HC (2003) 2003. Serum metabolic enzyme activities and hepatocyte ultrastructure of common carp after gallium exposure. Zool Stud 42(3):455–461

    CAS  Google Scholar 

  64. Li XY, Chung IK, Kim JI, Lee JA (2004) Subchronic oral toxicity of microcystin in common carp (Cyprinus carpio L.) exposed to Microcystis under laboratory conditions. Toxicon 44(8):821–827. https://doi.org/10.1016/j.toxicon.2004.06.010

    Article  CAS  PubMed  Google Scholar 

  65. Wallace, A. D., Meyer, S. A. 2010. Hepatotoxicity, in: Hodgson. (2010). A textbook of modern Toxicology 4th ed. John Wiley & Sons, Inc., Hoboken, New Jersey, pp. 277–289

  66. Bressler J, Kim KA, Chakraborti T, Goldstein G (1999) Molecular mechanisms of lead neurotoxicity. Neurochem Res 24(4):595–600. https://doi.org/10.1023/A:1022596115897

    Article  CAS  PubMed  Google Scholar 

  67. Prozialeck WC, Grunwald GB, Dey PM, Reuhl KR, Parrish AR (2002) Cadherins and NCAM as potential targets in metal toxicity. Toxicol Appl Pharmacol 182(3):255–265. https://doi.org/10.1006/taap.2002.9422

    Article  CAS  PubMed  Google Scholar 

  68. Bradbury SP, Carlson RW, Henry TR, Padilla S, Cowden J (2008) Toxic responses of the fish nervous system. In: Di Giulio RT, Hinton DE (Eds.). (2008). The toxicology of fishes. Crc Press, pp 417–455

  69. Larsson Å, Haux C, Sjöbeck ML (1985) Fish physiology and metal pollution: results and experiences from laboratory and field studies. Ecotoxicol Environ Saf 9(3):250–281. https://doi.org/10.1016/0147-6513(85)90045-4

    Article  CAS  PubMed  Google Scholar 

  70. Nussey, G., Van Vuren, J. H. J., & Du Preez, H. H. (1995). Effect of copper on the haematology and osmoregulation of the Mozambique tilapia, Oreochromis mossambicus (Cichlidae). Comp Biochem Physiol, Part C: Pharmacol, Toxicol Endocrinol, 111(3), 369–380. https://doi.org/10.1016/0742-8413(95)00063-1

  71. Nelson K, Jones J, Jacobson S, Reimschuessel R (1999) Elevated blood urea nitrogen (BUN) levels in goldfish as an indicator of gill dysfunction. J Aquat Anim Health 11(1):52–60 https://doi.org/10.1577/1548-8667(1999)011<0052:EBUNBL>2.0.CO;2

    Article  Google Scholar 

  72. Parris WE, Adeli K (2002) In Vitro Toxicological assessment of heavy metals and intracellular mechanisms of toxicity. In: Sarkar B (ed) Heavy Metals in the Environment. Marcel Dekker, Inc., New York, pp 69–93

    Google Scholar 

  73. Bocchetti R, Lamberti CV, Pisanelli B, Razzetti EM, Maggi C, Catalano B, Sesta G, Martuccio G, Gabellini M, Regoli F (2008) Seasonal variations of exposure biomarkers, oxidative stress responses and cell damage in the clams, Tapes philippinarum, and mussels, Mytilus galloprovincialis, from Adriatic Sea. Mar Environ Res 66(1):24–26. https://doi.org/10.1016/j.marenvres.2008.02.013

    Article  CAS  PubMed  Google Scholar 

  74. Shi X, Kasprzak KS, Dalal NS (1993) Generation of free radicals in reactions of Ni (II)-thiol complexes with molecular oxygen and model lipid hydroperoxides. J Inorg Biochem 50(3):211–225. https://doi.org/10.1016/0162-0134(93)80026-6

    Article  CAS  PubMed  Google Scholar 

  75. Flora SJS (2014) Metals. In: Gupta, R. C., Biomarkers in toxicology, first ed. Academic Press, pp. 485-519

  76. Bols NC, Dayeh VR, Lee LEJ, Schirmer K (2005) Use of fish cell lines in the toxicology and ecotoxicology of fish. Piscine cell lines in environmental toxicology. In: Mommsen TP, Moon TW (eds) Biochemistry and Molecular Biology of Fishes, 6. Elsevier Science, pp. 43–84. https://doi.org/10.1016/S1873-0140(05)80005-0

  77. Timbrell J (2000) Principles of biochemical toxicology, third edn. CRC Press, London

Download references

Funding

This work was supported by the Grant Agency of SUA in Nitra, project no. 06-GA SPU-16 (0.20), VEGA 1/0625/15 (0.10) and by the Slovak Research and Development Agency under the contract No. APVV-16-0289 (0.50). This work was also supported by AgroBioTech Research Centre built in accordance with the project Building “AgroBioTech” Research Centre ITMS 26220220180 (0.20).

Author information

Authors and Affiliations

  1. Department of Animal Physiology, Faculty of Biotechnology and Food Sciences, Slovak University of Agriculture in Nitra, Tr. A. Hlinku 2, 949 76, Nitra, Slovak Republic

    Anton Kovacik, Eva Tvrda, Katarina Zbynovska, Peter Cupka & Peter Massanyi

  2. AgroBioTech Research Centre, Slovak University of Agriculture in Nitra, Tr. A. Hlinku 2, 949 76, Nitra, Slovak Republic

    Michal Miskeje & Eva Kovacikova

  3. Department of Chemistry, Faculty of Biotechnology and Food Sciences, Slovak University of Agriculture in Nitra, Tr. A. Hlinku 2, 949 76, Nitra, Slovak Republic

    Julius Arvay

  4. Department of Biochemistry and Biotechnology, Faculty of Biotechnology and Food Sciences, Slovak University of Agriculture in Nitra, Tr. A. Hlinku 2, 949 76, Nitra, Slovak Republic

    Marian Tomka

  5. Department of Poultry Science and Small Animal Husbandry, Faculty of Agrobiology and Food Resources, Slovak University of Agriculture in Nitra, Tr. A. Hlinku 2, 949 76, Nitra, Slovak Republic

    Jaroslav Andreji & Martin Fik

  6. Department of Microbiology, Faculty of Biotechnology and Food Sciences, Slovak University of Agriculture in Nitra, Tr. A. Hlinku 2, 949 76, Nitra, Slovak Republic

    Lukas Hleba

  7. Department of Food Hygiene and Safety, Faculty of Biotechnology and Food Sciences, Slovak University of Agriculture in Nitra, Tr. A. Hlinku 2, 949 76, Nitra, Slovak Republic

    Jozef Nahacky

Authors
  1. Anton Kovacik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eva Tvrda
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michal Miskeje
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Julius Arvay
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marian Tomka
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Katarina Zbynovska
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jaroslav Andreji
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Lukas Hleba
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Eva Kovacikova
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Martin Fik
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Peter Cupka
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Jozef Nahacky
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Peter Massanyi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anton Kovacik.

Ethics declarations

The study was approved by the Ethics Committee of the Slovak University of Agriculture in Nitra, protocol number 48/2013.

Conflict of Interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kovacik, A., Tvrda, E., Miskeje, M. et al. Trace Metals in the Freshwater Fish Cyprinus carpio: Effect to Serum Biochemistry and Oxidative Status Markers. Biol Trace Elem Res 188, 494–507 (2019). https://doi.org/10.1007/s12011-018-1415-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-018-1415-x

Keywords

Search

Navigation