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Malondialdehyde concentrations in the intestine and gills of Vardar chub (Squalius vardarensis Karaman) as indicator of lipid peroxidation

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Abstract

A lipid peroxidation product, malondialdehyde (MDA), was studied in Vardar chub (Squalius vardarensis Karaman) as an indicator of oxidative stress, using native fish from three rivers in northern Macedonia: the mining-impacted Zletovska and Kriva rivers and the agriculturally impacted Bregalnica River. MDA concentrations were measured in the intestine in the spring and autumn of 2012 and in the gills in autumn. The aims of the study were to establish the type of contamination which provokes a more pronounced MDA increase, as well as the organ which more reliably reflects the occurrence of oxidative stress. MDA levels in the intestine in spring amounted to 3.29–155.8 nmol g−1 and in autumn to 4.85–111.1 nmol g−1, whereas MDA concentrations in the gills in autumn were 7.69–147.5 nmol g−1. Stronger influence of organic contamination on development of oxidative stress was observed in both organs, as seen from higher median MDA concentrations in autumn in fish from the highly pesticide-contaminated Bregalnica River (gills 78.4 nmol g−1; intestine 23.5 nmol g−1) compared to the highly metal-contaminated Zletovska River (gills 15.9 nmol g−1; intestine 17.4 nmol g−1). The response of the gills to contamination was twice stronger than that of the intestine. The majority of fish from the pesticide-polluted river had increased MDA in the gills, in contrast to only sporadically increased MDA in the intestine. Our results indicated that development of oxidative stress strongly depends on the selected fish organ and that the gills seem to be a better choice for monitoring oxidative stress than the intestine, due to their continuous and direct exposure to polluted river water.

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References

  • Abudayyak M, Ozden S, Alpertunga B, Özhan G (2014) Effect of bentazone on lipid peroxidation and antioxidant systems in human erythrocytes in vitro. Drug Chem Toxicol 37:410–414

    Article  CAS  Google Scholar 

  • Ahmad I, Hamid T, Fatima M, Chand HS, Jain SK, Athar M, Raisuddin S (2000) Induction of hepatic antioxidants in freshwater catfish (Channa punctatus Bloch) is a biomarker of paper mill effluent exposure. Biochim Biophys Acta 1523:37–48

    Article  CAS  Google Scholar 

  • Alderton DHM, Serafimovski T, Mullen B, Fairall K, James S (2005) The chemistry of waters associated with metal mining in Macedonia. Mine Water Environ 24:139–149

    Article  CAS  Google Scholar 

  • Amaeze NH, Adeyemi RO, Adebesin AO (2015) Oxidative stress, heats shock protein and histopathological effects in the gills of African catfish, Clarias gariepinus induced by bridge runoffs. Environ Monit Assess 187:172

    Article  Google Scholar 

  • Andreevska D, Menkovska M, Andov D (2013) Overview of the current condition, in production consumption and the research potential of the rice crop in the Republic of Macedonia. Maced J Anim Sci 3:219–228

    Google Scholar 

  • Banerjee BD, Seth V, Bhattacharya A (1999) Biochemical effects of some pesticides on lipid peroxidation and free-radical scavengers. Toxicol Lett 107:33–47

    Article  CAS  Google Scholar 

  • Barišić J, Dragun Z, Ramani S, Filipović Marijić V, Krasnići N, Čož-Rakovac R, Kostov V, Rebok K, Jordanova M (2015) Evaluation of histopathological alterations in the gills of Vardar chub (Squalius vardarensis Karaman) as an indicator of river pollution. Ecotox. Environ. Safe. 118:158–166

    Article  Google Scholar 

  • Botsoglou NA, Fletouris DJ, Papageorgiou GE, Vassilopoulos VN, Mantis AJ, Trakatellis AG (1994) Rapid, sensitive, and specific thiobarbituric acid method for measuring lipid peroxidation in animal tissue, food and feedstuff samples. J Agric Food Chem 42:1931–1937

    Article  CAS  Google Scholar 

  • Chovanec A, Hofer R, Schiemer F (2003) Fish as bioindicators. In: Markert BA, Breure AM, Zechmeister HG (eds) Bioindicators and biomonitors: principles, concepts and applications. Elsevier Science Ltd, Amsterdam, pp 639–676

    Chapter  Google Scholar 

  • Chuang Y-C (2010) Mitochondrial dysfunction and oxidative stress in seizure-induced neuronal cell death. Acta Neurol Taiwanica 19:3–15

    Google Scholar 

  • Danabas D, Yildirim NC, Yildirim N, Onal AO, Uslu G, Unlu E, Danabas S, Ergin C, Tayhan N (2015) Changes in antioxidant defense system in gills of Capoeta umbla caught from Uzuncayir Dam Lake, Turkey. Biochem Syst Ecol 63:72–79

    Article  CAS  Google Scholar 

  • Dolenec T, Serafimovski T, Dobnikar M, Tasev G, Dolenec M (2005) Mineralogical and heavy metal signature of acid mine drainage impacted paddy soil from the western part of the Kočani field (Macedonia). RMZ Mater Geoenviron 52:397–402

    CAS  Google Scholar 

  • Dragun Z, Raspor B, Podrug M (2007) The influence of the season and the biotic factors on the cytosolic metal concentrations in the gills of the European chub. Chemosphere 69:911–919

    Article  CAS  Google Scholar 

  • Durmaz H, Sevgiler Y, Üner N (2006) Tissue-specific antioxidative and neurotoxic responses to diazinon in Oreochromis niloticus. Pestic. Biochem. Phys. 84:215–226

    Article  CAS  Google Scholar 

  • Fatima M, Ahmad I, Sayeed I, Athar M, Raisuddin S (2000) Pollutant-induced over-activation of phagocytes is concomitantly associated with peroxidative damage in fish tissues. Aquat Toxicol 49:243–250

    Article  CAS  Google Scholar 

  • Feng M, Qu R, Li Y, Wei Z, Wang Z (2014) Biochemical biomarkers in liver and gill tissues of freshwater fish Carassius auratus following in vivo exposure to hexabromobenzene. Environ Toxicol 29:1460–1470

    Article  CAS  Google Scholar 

  • Filipović Marijić V, Raspor B (2010) The impact of the fish spawning on metal and protein levels in gastrointestinal cytosol of indigenous European chub. Comp Biochem Physiol C 152:133–138

    Google Scholar 

  • Filipović Marijić V, Raspor B (2012) Site-specific gastrointestinal metal variability in relation to the gut content and fish age of indigenous European chub from the Sava River. Water Air Soil Poll 223:4769–4783

    Article  Google Scholar 

  • Huang DJ, Zhang YM, Song G, Long J, Liu JH, Ji WH (2007) Contaminants-induced oxidative damage on the carp Cyprinus carpio collected from the upper Yellow River, China. Environ Monit Assess 128:483–488

    Article  CAS  Google Scholar 

  • 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 92:38–42

    Article  CAS  Google Scholar 

  • Jordanova M, Rebok K, Dragun Z, Ramani S, Ivanova L, Kostov V, Valić D, Krasnići N, Filipović Marijić V, Kapetanović D (2016) Histopathology investigation on the Vardar chub (Squalius vardarensis) populations captured from the rivers impacted by mining activities. Ecotox Environ Safe 129:35–42

    Article  CAS  Google Scholar 

  • Jos Á, Pichardo S, Prieto AI, Repetto G, Vázquez CM, Moreno I, Cameán AM (2005) Toxic cyanobacterial cells containing microcystins induce oxidative stress in exposed tilapia fish (Oreochromis sp.) under laboratory conditions. Aquat Toxicol 72:261–271

    Article  CAS  Google Scholar 

  • Kamunde C, MacPhail R (2011) Effect of humic acid during concurrent chronic waterborne exposure of rainbow trout (Oncorhynchus mykiss) to copper, cadmium and zinc. Ecotox. Environ. Safe. 74:259–269

    Article  CAS  Google Scholar 

  • Khessiba A, Roméo M, Aïssa P (2005) Effects of some environmental parameters on catalase activity measured in the mussel (Mytilus galloprovincialis) exposed to lindane. Environ Pollut 133:275–281

    Article  CAS  Google Scholar 

  • Kehrer JP (1993) Free radicals as mediators of tissue injury and disease. Crit Rev Toxicol 23:21–48

    Article  CAS  Google Scholar 

  • Kohen R, Nyska A (2002) Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicol Pathol 30:620–650

    Article  CAS  Google Scholar 

  • Laganà A, Bacaloni A, De Leva I, Faberi A, Fago G, Marino A (2002) Occurrence and determination of herbicides and their major transformation products in environmental waters. Anal Chim Acta 462:187–198

    Article  Google Scholar 

  • Li L, Chen H, Bi R, Xie L (2015) Bioaccumulation, subcellular distribution, and acute effects of chromium in Japanese medaka (Oryzias latipes). Environ Toxicol Chem 34:2611–2617

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lovrić J, Mesić M, Macan M, Koprivanac M, Kelava M, Bradamante V (2008) Measurement of malondialdehyde (MDA) level in rat plasma after simvastatin treatment using two different analytical methods. Period Biol 110:63–67

    Google Scholar 

  • Ozcan Oruc E, Sevgiler Y, Uner N (2004) Tissue-specific oxidative stress responses in fish exposed to 2,4-D and azinphosmethyl. Comp Biochem Phys C 137:43–51

    Article  Google Scholar 

  • Palace VP, Dick TA, Brown SB, Baron CL, Klaverkamp JF (1996) Oxidative stress in lake sturgeon (Acipenser fulvescens) orally exposed to 2,3,7,8-tetrachlorodibenzofuran. Aquat Toxicol 35:79–92

    Article  CAS  Google Scholar 

  • Pandey S, Parvez S, Ansari RA, Ali M, Kaur M, Hayat F, Ahmad F, Raisuddin S (2008) Effects of exposure to multiple trace metals on biochemical, histological and ultrastructural features of gills of a freshwater fish, Channa punctata Bloch. Chem Biol Interact 174:183–192

    Article  CAS  Google Scholar 

  • Papadakis EN, Vryzas Z, Kotopoulou A, Kintzikoglou K, Makris KC, Papadopoulou-Mourkidou E (2015) A pesticide monitoring survey in rivers and lakes of northern Greece and its human and ecotoxicological risk assessment. Ecotox Environ Safe 116:1–9

    Article  CAS  Google Scholar 

  • Pereira S, Pinto AL, Cortes R, Fontaínhas-Fernandes A, Coimbra AM, Monteiro SM (2013) Gill histopathological and oxidative stress evaluation in native fish captured in Portuguese northwestern rivers. Ecotox. Environ. Safe. 90:157–166

    Article  CAS  Google Scholar 

  • Ramani S, Dragun Z, Kapetanović D, Kostov V, Jordanova M, Erk M, Hajrulai-Musliu Z (2014) Surface water characterization of three rivers in the lead/zinc mining region of northeastern Macedonia. Arch Environ Contam Toxicol 66:514–528

    Article  CAS  Google Scholar 

  • Rätz, H.-J., Lloret J (2003) Variation in fish condition between Atlantic cod (Gadus morhua) stocks, the effect on their productivity and management implications. Fisheries Research 60:369–380

  • Rebok, K., (2013) A toxicopathology survey of the River Bregalnica using the barbel (Barbus peloponnesius, Valenciennes 1844) as bioindicator. Doctoral Thesis, University Ss. Cyril and Methodius, Skopje, Macedonia

  • Saravanan M, Kumar KP, Ramesh M (2010) Haematological and biochemical responses of freshwater teleost fish Cyprinus carpio (Actinopterygii: Cypriniformes) during acute and sublethal exposure to lindane. Pestic Biochem Physiol 100:206–211

    Article  Google Scholar 

  • Şaşi, H (2004) The reproduction biology of chub (Leuciscus cephalus L., 1758.) in Topçam Dam Lake (Aydin, Turkey). Turkish Journal of Veterinary and Animal Sciences 28:693–699

  • Sayeed I, Parvez S, Pandey S, Bin-Hafeez B, Haque R, Raisuddin S (2003) Oxidative stress biomarkers of exposure to deltamethrin in freshwater fish, Channa punctatus Bloch. Ecotoxicol Environ Saf 56:295–301

    Article  CAS  Google Scholar 

  • Scandalios JG (2005) Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Braz J Med Biol Res 38:995–1014

    Article  CAS  Google Scholar 

  • Sheehan D, Power A (1999) Effects of seasonality on xenobiotic and antioxidant defence mechanisms of bivalve molluscs. Comp Biochem Physiol C 123:193–199

    Article  CAS  Google Scholar 

  • Simonato JD, Fernandes MN, Martinez CBR (2011) Gasoline effects on biotransformation and antioxidant defenses of the freshwater fish Prochilodus lineatus. Ecotoxicology 20:1400–1410

    Article  CAS  Google Scholar 

  • Spasovski O (2011) Heavy and toxic metals and nutrients in separate places in the river Bregalnica, (eastern Macedonia). Annual of the University of Mining and Geology St. Ivan Rilski, vol. 54, part II: Mining and mineral processing. pp. 118–120

  • Spasovski O, Dambov R (2009) Heavy metals in the water of the river Kalnistanska and the vicinity. Balkanmine 2009 - 3rd Balkan Mining Congress. Izmir, pp. 667–670

  • Stipaničev D, Dragun Z, Repec S, Rebok K, Jordanova M (2017) Broad spectrum screening of 463 organic contaminants in rivers in Macedonia. Ecotox Environ Safe 135:48–59

    Article  Google Scholar 

  • Stohs SJ, Bagchi D (1994) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18:321–336

    Article  Google Scholar 

  • Stohs SJ, Bagchi D, Hassoun E, Bagchi M (2000) Oxidative mechanisms in the toxicity of chromium and cadmium ions. J Environ Pathol Toxicol Oncol 19:201–213

    CAS  Google Scholar 

  • Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M (2006) Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol Environ Safe 64:178–189

    Article  CAS  Google Scholar 

  • Valko M, Morris H, Cronin MTD (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208

    Article  CAS  Google Scholar 

  • Víg E, Nemcsók J (1989) The effects of hypoxia and paraquat on the superoxide dismutase activity in different organs of carp, Cyprinus carpio L. J Fish Biol 35:23–25

    Article  Google Scholar 

  • Yonar ME, Yonar SM, Ural MŞ, Silici S, Düşükcan M (2012) Protective role of propolisin chlorpyrifos-induced changes in the haematological parameters and the oxidative/antioxidative status of Cyprinus carpio carpio. Food Chem Toxicol 50:2703–2708

    Article  Google Scholar 

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Acknowledgements

This study was carried out as a part of two bilateral projects between Macedonia and Croatia, titled “The assessment of the availability and effects of metals on fish in the rivers under the impact of mining activities” and “Bacterial and parasitical communities of chub as indicators of the status of environment exposed to mining activities”. The financial support by the Ministry of Science, Education and Sport of the Republic of Croatia (project nos. 098-0982934-2721 and 098-0982934-2752) is acknowledged.

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Authors and Affiliations

  1. Laboratory for Biological Effects of Metals, Division for Marine and Environmental Research, Ruđer Bošković Institute, P.O. Box 180, HR-10002, Zagreb, Croatia

    Zrinka Dragun, Vlatka Filipović Marijić, Nesrete Krasnići & Marijana Erk

  2. Hydrology and Ecology Department, National Hydrometeorological Service, Skupi 28, 1000, Skopje, Macedonia

    Sheriban Ramani

  3. Laboratory for Aquaculture and Pathology of Aquatic Organisms, Division for Marine and Environmental Research, Ruđer Bošković Institute, P.O. Box 180, HR-10002, Zagreb, Croatia

    Damir Valić

  4. Faculty of Natural Sciences and Mathematics, Ss. Cyril and Methodius University in Skopje, Arhimedova 3, 1000, Skopje, Macedonia

    Katerina Rebok & Maja Jordanova

  5. Institute of Animal Sciences, Ile Ilievski 92a, 1000, Skopje, Macedonia

    Vasil Kostov

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  1. Zrinka Dragun
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  2. Vlatka Filipović Marijić
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Correspondence to Zrinka Dragun.

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Dragun, Z., Filipović Marijić, V., Krasnići, N. et al. Malondialdehyde concentrations in the intestine and gills of Vardar chub (Squalius vardarensis Karaman) as indicator of lipid peroxidation. Environ Sci Pollut Res 24, 16917–16926 (2017). https://doi.org/10.1007/s11356-017-9305-x

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