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Effects of Long-Term Lead Exposure on Antioxidant Enzyme Defense System in Organs of Brown Hare (Lepus europaeus Pallas) as a Bioindicator of Environmental Pollution in Croatia

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In Croatia, Podravina is a well-known lead-polluted region due to the intensive exploitation of natural gas, a highly developed agricultural industry, and a traffic hub with several heavily traveled roads. It represents a natural environment with a great variety of wildlife, especially hares (Lepus europaeus Pallas), which may serve as an indicator for environmental quality assessment. This study was conducted to estimate the bioaccumulation of lead in hare liver, kidney, muscle, and brain during long-term exposure and its impact on the oxidative status of the organism and to investigate a possible lead exchange ionic mechanism in the brain. In the organs of two hare groups (experimental from polluted area and control from the island of Krk), Ca, Fe, Mg, Na, lead concentrations, and antioxidant enzyme defense system were analyzed. The accumulation of lead was highest in the brain (3.7-fold higher compared to the control group) and lowest in the liver (1.6-fold higher compared to the control group). Kendall-Tau and multiple regression analysis showed that the increased lead content caused a stronger exchange of Ca and Na ions in the brain. We proposed that lead either mobilizes intracellular cation stores or causes competitive displacement of Ca from the binding site in intoxicated cells. A linear predictive model for cell intoxication by lead was proposed, where GPx and SOD were predominantly influenced by long-term lead exposure. The presented results showed that long-term lead exposure in hares negatively affected their oxidative status and caused the strongest toxicity in the brain and muscles, making their survival and/or population vulnerable.

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This study was supported by a grant from the Croatian Ministry of Science (Project Nos. 053–0532400-2362 and 062–0621341-0061), a grant from the Program of the European Community for Research and Technological Development (Project No. FOODCT-2006–016253), and a grant from the University of Rijeka, Croatia (Grant No. Uniri-biomed-18–155-1304).

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Authors and Affiliations



Željko Linšak: Investigation, formal analysis, data curation, and writing—original draft preparation.

Ivana Gobin: Validation and reviewing and editing.

Dijana Tomić Linšak: Conceptualization, methodology, formal analysis, data curation, writing, reviewing and editing, and supervision.

Dalibor Broznić: Formal analysis, data curation, software, visualization, writing, and reviewing and editing.

All authors read and approved the final draft of the manuscript.

Corresponding author

Correspondence to Dijana Tomić Linšak.

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The animals were hunted during the regular hunting period in Croatia, in compliance with the Law on Hunting taken from the European Union Directive, and donated by the hunters, so no approval of research ethics committees was required to accomplish the goals of this study.

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The authors declare no competing interests.

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Linšak, Ž., Gobin, I., Linšak, D.T. et al. Effects of Long-Term Lead Exposure on Antioxidant Enzyme Defense System in Organs of Brown Hare (Lepus europaeus Pallas) as a Bioindicator of Environmental Pollution in Croatia. Biol Trace Elem Res 200, 5091–5103 (2022).

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