Abstract
To evaluate the nutritional status and the environmental exposure to toxic elements of the wild boar Sus scrofa L. (n = 20) from northwestern (NW) Russia, we determined the contents of the essential (Co, Cu, Fe, Mg, Mn, Ni, and Zn) and toxic (Cd and Pb) elements in the muscle, kidney, and liver. A second aim was to study the interactions between these elements and several antioxidants, namely, the activity of superoxide dismutase (SOD) and catalase, and the contents of glutathione (GSH), retinol, and α-tocopherol. A third aim was to assess whether the meat and offal of the wild boar are suitable for consumption or unsuitable due to the level of toxic elements. According to reference values of elements reported for domestic pigs, the wild boar from NW Russia was deficient in most of the essential elements (Co, Cu, Mn, Ni, and Zn) but had optimal values of Fe and Mg. The concentrations of Cd and Pb were lower than the values reported for pigs and wild boars living in heavily polluted areas. The correlations between antioxidants and elements could indicate that mineral balance in the body is regulated by antioxidants, among which the SOD activity, GSH, and retinol levels are the most sensitive parameters. Our assessment indicates that consumption of wild boar meat and liver, either rarely (4 times a year) or regularly (monthly), does not pose a health risk to adults and children, although wild boar kidney is not suitable for consumption.
Similar content being viewed by others
Availability of data and material
All data can be found in Supplemental Information.
References
Alasia D, Emem-Chioma P, Ojeka S (2020) An evaluation of the mitigating effects of α-tocopherol (vitamin E) and ascorbic acid (vitamin C) on the renal function and histology of adult male albino Wistar rats with sub-acute lead acetate exposure. Occupational Diseases and Environmental Medicine 8:35–49. https://doi.org/10.4236/odem.2020.82003
Alonso ML, Montaña FP, Miranda M, Castillo C, Hernández J, Benedito JL (2004) Interactions between toxic (As, Cd, Hg and Pb) and nutritional essential (Ca Co, Cr, Cu, Fe, Mn, Mo, Ni, Se, Zn) elements in the tissues of cattle from NW Spain. Biometals 17(4):389–397
Amici A, Danieli PP, Russo C, Primi R, Ronchi B (2012) Concentrations of some toxic and trace elements in wild boar (Sus scrofa) organs and tissues in different areas of the Province of Viterbo. Central Italy Ital J Anim Sci 11(4):e65. https://doi.org/10.4081/ijas.2011.e65
Babicz M, Kasprzyk A (2019) Comparative analysis of the mineral composition in the meat of wild boar and domestic pig. Ital J Anim Sci 18(1):1013–1020. https://doi.org/10.1080/1828051X.2019.1610337
Ballari SA, Barrios-García MN (2014) A review of wild boar (Sus scrofa) diet and factors affecting food selection in native and introduced ranges. Mammal Rev 44(2):124–134. https://doi.org/10.1111/mam.12015
Baltaci AK, Yuce K, Mogulkoc R (2018) Zinc metabolism and metallothioneins. Biol Trace Elem Res 183(1):22–31. https://doi.org/10.1007/s12011-017-1119-7
Bears RF, Sizes IN (1952) A spectral method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195(1):133–140
Bilandžić N, Sedak M, Vratarić D, Perić T, Šimić B (2009) Lead and cadmium in red deer and wild boar from different hunting grounds in Croatia. Sci Total Environ 407(14):4243–4247. https://doi.org/10.1016/j.scitotenv.2009.04.009
Bremner I, Beattie JH (1995) Copper and zinc metabolism in health and disease: speciation and interactions. Proc Nutr Soc 54:489–499. https://doi.org/10.1079/PNS19950017
Brown JCW, Strain JJ (1990) Effect of dietary homocysteine on copper status in rats. J Nutr 120:1068–1074. https://doi.org/10.1093/jn/120.9.1068
Brzóska MM, Moniuszko-Jakoniuk J (2001) Interactions between cadmium and zinc in the organism. Food Chem Toxicol 39(10):967–980. https://doi.org/10.1016/S0278-6915(01)00048-5
Canesi L, Viarengo A, Leonzio C, Filippelli M, Gallo G (1999) Heavy metals and glutathione metabolism in mussel tissues. Aquatic Toxicol 46(1):67–76. https://doi.org/10.1016/S0166-445X(98)00116-7
Casalino E, Calzaretti G, Sblano C, Landriscina C (2002) Molecular inhibitory mechanisms of antioxidant enzymes in rat liver and kidney by cadmium. Toxicology 179(1–2):37–50. https://doi.org/10.1016/S0300-483X(02)00245-7
Chiari M, Cortinovis C, Bertoletti M, Alborali L, Zanoni M, Ferretti E, Caloni F (2015) Lead, cadmium and organochlorine pesticide residues in hunted red deer and wild boar from northern Italy. Food Add Contam: Part A 32(11):1867–1874. https://doi.org/10.1080/19440049.2015.1087058
Commission Regulation (EC) (2008) No 629, 2008 of 2, 2008. Amending Regulation (EC) No 1881/2006 setting maximum levels for certain contaminants in foodstuffs. Off J Eur Union L 173(6):3–7
Crnić AP, Šuran J, Madunić HC, Božić F (2015) Cadmium concentrations in the tissues of young wild boar (Sus scrofa L.) from Moslavina and Slavonia in lowland Croatia. Vet Arh 85:323–334
Danieli PP, Serrani F, Primi R, Ponzetta MP, Ronchi B, Amici A (2012) Cadmium, lead, and chromium in large game: a local-scale exposure assessment for hunters consuming meat and liver of wild boar. Arch Environ Contam Toxicol 63(4):612–627. https://doi.org/10.1007/s00244-012-9791-2
Danilkin AA (2002) Svinye (Suidae). GEOS, Moscow, p 309
Dannenberg D, Nuernberg G, Nuernberg K, Haegemann E (2013) The effects of gender, age and region on marco- and micro-nutrient contents and fatty acid profiles in the muscles of roe deer and wild boar in Mecklenburg-Western Pomerania (Germany). Meat Sci 94:39–46. https://doi.org/10.1016/j.meatsci.2012.12.010
Dardenne M (2002) Zinc and immune function. Eur J Clin Nutr 56:S20–S23. https://doi.org/10.1038/sj.ejcn.1601479
Długaszek M, Kopczyński K (2011) Porównawcza analiza składu pierwiastkowego wątroby zwierząt dziko żyjących. Probl Hig Epidemiol 92:859–863
Długaszek M, Kopczyński K (2013) Elemental composition of muscle tissue of wild animals from central region of Poland. Int J Environ Res 7(4):973–978. https://doi.org/10.22059/IJER.2013.680
Długaszek M (2019) Studies on relationships between essential and toxic elements in selected body fluids, cells and tissues. Chem Biol Interact 297:57–66. https://doi.org/10.1016/j.cbi.2018.10.011
Doyle JJ, Pfander WH (1975) Interactions of cadmium with copper, iron, zinc, and manganese in ovine tissues. J Nutr 105(5):599–606. https://doi.org/10.1093/jn/105.5.599
Durkalec M, Szkoda J, Kolacz R, Opalinski S, Nawrocka A, Zmudzki J (2015) Bioaccumulation of lead, cadmium and mercury in roe deer and wild boars from areas with different levels of toxic metal pollution. Int J Environ Res 9(1):205–212
Ercal N, Gurer-Orhan H, Aykin-Burns N (2001) Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative damage. Curr Topics Med Chem 1(6):529–539
Erikson KM, Syversen T, Aschner T, Aschner JL, Aschner M (2005) Interactions between excessive manganese exposure and dietary iron-deficiency in neurodegeneration. Environ Toxicol Pharmacol 19:415–421. https://doi.org/10.1016/j.etap.2004.12.053
Espinosa-Diez C, Miguel V, Mennerich D, Kietzmann T, Sánchez-Pérez P, Cadenas S, Lamas S (2015) Antioxidant responses and cellular adjustments to oxidative stress. Red Biol 6:183–197. https://doi.org/10.1016/j.redox.2015.07.008
European Food Safety Authority (2009) Cadmium in food. Scientific opinion of the Panel on Contaminants in the Food Chain. EFSA J 980:1–139
European Food Safety Authority (2010) Scientific opinion on lead in food. EFSA Panel on Contaminants in the Food Chain (CONTAM). EFSA J 8(4):1570
Fedorets NG, Bakhmet ON, Solodovnikov AN, Morozov AK (2008) Pochvy Karelii: geokhimicheskii atlas [Soils of Karelia: geochemical atlas]. Nauka, In-t lesa KarNTs RAN. Moscow, p 47
Gašparík J, Binkowski ŁJ, Jahnátek A, Šmehýl P, Dobiaš M, Lukáč N, Błaszczyk M, Semla M, Massanyi P (2017) Levels of metals in kidney, liver, and muscle tissue and their influence on the fitness for the consumption of wild boar from western Slovakia. Biol Trace Elem Res 177(2):258–266. https://doi.org/10.1007/s12011-016-0884-z
Gasparik J, Dobias M, CapCarova M et al (2012) Concentration of cadmium, mercury, zinc, copper and cobalt in the tissues of wild boar (Sus scrofa) hunted in the western Slovakia. J Environ Sci Health Part A Tox Hazard Subst Environ Eng 47:1212–1216. https://doi.org/10.1080/10934529.2012.672065
Genchi G, Carocci A, Lauria G, Sinicropi MS, Catalano A (2020) Nickel: human health and environmental toxicology. Int J Environ Res Public Health 17(3):679. https://doi.org/10.3390/ijerph17030679
Groten JP, Sinkeldam EJ, Muys T, Luten JB, Van Bladeren PJ (1991) Interaction of dietary Ca, P, Mg, Mn, Cu, Fe, Zn and Se with the accumulation and oral toxicity of cadmium in rats. Food Chem Toxicol 29(4):249–258. https://doi.org/10.1016/0278-6915(91)90022-Y
Isaksson C (2010) Pollution and its impact on wild animals: a meta-analysis on oxidative stress. EcoHealth 7(3):342–350. https://doi.org/10.1007/s10393-010-0345-7
Jin T, Nordberg M, Frech W, Dumont X, Bernard A, Ye T, Kong Q, Wang Z, Li P, Lundström N-G, Li Y, Nordberg GF (2002) Cadmium biomonitoring and renal dysfunction among a population environmentally exposed to cadmium from smelting in China (ChinaCad). Biometals 15:397–410. https://doi.org/10.1023/A:1020229923095
Jones RL (2002) Zinc, iron, and sodium in hair of deer from areas of contrasting soil productivity. Biol Trace Elem Res 86:217–226. https://doi.org/10.1385/BTER:86:3:217
Jorhem L, Sundström B, Åstrand C, Haegglund G (1989) The levels of zinc, copper, manganese, selenium, chromium, nickel, cobalt, and aluminium in the meat, liver and kidney of Swedish pigs and cattle. Zeitschrift Fuèr Lebensmittel-Untersuchung Und Forschung 188(1):39–44. https://doi.org/10.1007/BF01027620
Kalisińska E (2019) Mammals and birds as bioindicators of trace element contaminations in terrestrial environments: an ecotoxicological assessment of the Northern Hemisphere. Springer. https://doi.org/10.1007/978-3-030-00121-6
Koivula MJ, Eeva T (2010) Metal-related oxidative stress in birds. Environ Pollut 158(7):2359–2370. https://doi.org/10.1016/j.envpol.2010.03.013
Lazarus M, Prevendar Crnić A, Bilandžić N, Kusak J, Reljić S (2014) Cadmium, lead, and mercury exposure assessment among Croatian consumers of free-living game. Arh Hig Rada Toksikol 65(3):281–291. https://doi.org/10.2478/10004-1254-65-2014-2527
Lowry OH, Rosenbrough NJ, Farr AL, Randan RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275
Majchrzak D, Fabian E, Elmadfa I (2006) Vitamin A content (retinol and retinyl esters) in livers of different animals. Food Chem 98(4):704–710. https://doi.org/10.1016/j.foodchem.2005.06.035
Malmsten A, Dalin AM, Pettersson J, Persson S (2021) Concentrations of cadmium, lead, arsenic, and some essential metals in wild boar from Sweden. Eur J Wildl Res 67(2):1–8. https://doi.org/10.1007/s10344-021-01460-y
Matschke GH (1967) Aging European wild hogs by dentition. J Wildl Manag 31(1):109–113
Medvedev N (1999) Levels of heavy metals in Karelian wildlife, 1989–91. Environ Monit Assess 56:177–193. https://doi.org/10.1023/A:1005988511058
Misra HP, Fridovich F (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247(10):3170–3175. https://doi.org/10.1016/S0021-9258(19)45228-9
Moore CD, Fahlman A, Crocker DE, Robbins KA, Trumble SJ (2015) The degradation of proteins in pinniped skeletal muscle: viability of post-mortem tissue in physiological research. Conserv Physiol 3(1):1–8. https://doi.org/10.1093/conphys/cov019
Nielsen FH, Zimmerman TJ, Shuler TR, Brossart B, Uthus EO (1989) Evidence for a cooperative metabolic relationship between nickel and vitamin B12 in rats. J Trace Elem Exp Med 2:21–29
NRC (2005) Mineral tolerance of animals. National Academy Press, Washington, DC, National Research Council
Panchenko DV, Danilov PI, Tirronen KF, Paasivaara A, Krasovsky Yu (2019) Features of ungulates distribution in the Karelian part of the Green belt of Fennoscandia. Transactions of Karelian Research Center of Russian Academy of Science 4:119–129. https://doi.org/10.17076/them997
Parmalee NL, Aschner M (2016) Manganese and aging. Neurotoxicology 56:262–268. https://doi.org/10.1016/j.neuro.2016.06.006
Pilarczyk B, Tomza-Marciniak A, Pilarczyk R, Udała J, Kruzhel B, Ligocki M (2020) Content of essential and non-essential elements in wild animals from western Ukraine and the health risks associated with meat and liver consumption. Chemosphere 244:125506. https://doi.org/10.1016/j.chemosphere.2019.125506
Puls R (1994) Mineral levels in animal health. Diagnostic data, 2nd ed. Sherpa International, Clearbrook BC, Canada
Rayssiguier Y, Alexandre-Gouabau MC, Lyan B, Gueux E, Mazur A, Rock E (2008) Inflammation interferes with the assessment of vitamin A status in magnesium deficiency. Magnes Res 21(4):237–239
Reglero MM, Monsalve-González L, Taggart MA, Mateo R (2008) Transfer of metals to plants and red deer in an old lead mining area in Spain. Sci Total Environ 406(1–2):287–297. https://doi.org/10.1016/j.scitotenv.2008.06.001
Rodríguez-Estival J, Taggart MA, Mateo R (2011) Alterations in vitamin A and E levels in liver and testis of wild ungulates from a lead mining area. Arch Environ Contam Toxicol 60(2):361–371. https://doi.org/10.1007/s00244-010-9597-z
De Romaña DL, Olivares M, Uauy R, Araya M (2011) Risks and benefits of copper in light of new insights of copper homeostasis. J Trace Elem Med Biol 25(1):3–13. https://doi.org/10.1016/j.jtemb.2010.11.004
Sauer JM, Waalkes MP, Hooser SB, Baines AT, Kuester RK, Sipes IG (1997) Tolerance induced by all-trans-retinol to the hepatotoxic effects of cadmium in rats: role of metallothionein expression. Toxicol Appl Pharmacol 143(1):110–119. https://doi.org/10.1006/taap.1996.8050
Sedki A, Lekouch N, Gamon S, Pineau A (2003) Toxic and essential trace metals in muscle, liver and kidney of bovines from a polluted area of Morocco. Sci Total Environ 317(1–3):201–205. https://doi.org/10.1016/S0048-9697(03)00050-0
Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 25:192–205
Shields G, Coulson W, Kimball D, Carnes WH, Cartwright G, Wintrobe M (1962) Studies on copper metabolism: Xxxii. Cardiovascular lesions in copper-deficient swine. Am J Clin Pathol 41(5):603
Shi H, Almutairi M, Moskovitz J, Xu YG (2021) Recent advances in iron homeostasis and regulation - a focus on epigenetic regulation and stroke. Free Rad Res 1:23. https://doi.org/10.1080/10715762.2020.1867314
Skobrak EB, Javor A, Gundel J, Bodnar K (2010) Analyses of macro-and microelements of wild boar meat in three different regions of Hungary. Lucrări Ştiinţifice, Seria Agronomie 53(1):22–25
Slukovskii Z, Medvedev M, Siroezhko E (2020) Long-range transport of heavy metals as a factor of the formation of the geochemistry of sediments in the southwest of the Republic of Karelia. Russia J Elem 25(1):125–137. https://doi.org/10.5601/jelem.2019.24.1.1816
Stangl G, Schwarz F, Jahn B, Kirchgessner M (2000) Cobalt-deficiency-induced hyperhomocysteinaemia and oxidative status of cattle. British J Nutr 83(1):3–6. https://doi.org/10.1017/S0007114500000027
State report on the status of the environment of the Republic of Karelia in (2018) Izhevsk: Print 314
State report on the status of the environment of the Republic of Karelia in (2019) Petrozavodsk: Verso 248
Spears JW (1984) Nickel as a newer trace element in the nutrition of domestic animals. J Anim Sci 59(3):823–835. https://doi.org/10.2527/jas1984.593823x
Thomas VG, Pain DJ, Kanstrup N, Green RE (2020) Setting maximum levels for lead in game meat in EC regulations: an adjunct to replacement of lead ammunition. Ambio 49:2026–2037. https://doi.org/10.1007/s13280-020-01336-6
Vertuani S, Angusti A, Manfredini S (2004) The antioxidants and pro-oxidants network: an overview. Curr Pharm Des 10:1677–1694. https://doi.org/10.2174/1381612043384655
Warenik-Bany M, Strucinski P, Piskorska-Pliszczynska J (2016) Dioxins and PCBs in game animals: interspecies comparison and related consumer exposure. Environ Int 89:21–29. https://doi.org/10.1016/j.envint.2016.01.007
WVDL (2015) Normal range values for WVDL Toxicology. https://www.yumpu.com/en/document/read/52919318/normal-range-values-for-wvdl-toxicology. Accessed 10 Nov 2021
Wieloch M, Kamiński P, Ossowska A et al (2012) Do toxic heavy metals affect antioxidant defense mechanisms in humans? Ecotoxicol Environ Safety 78:195–205. https://doi.org/10.1016/j.ecoenv.2011.11.017
Acknowledgements
The research was carried out using the equipment of the Core Facility of the Karelian Research Centre of the Russian Academy of Sciences. We are deeply grateful to M.Y. Shilyaev (Inspector of the Ministry of Ecology and Natural Resources, Lakhdenpoh’ya, Russia) for help in organizing sample collection.
Funding
The study was performed under state order (project FMEN-2022–0003).
Author information
Authors and Affiliations
Contributions
All the authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Svetlana Kalinina, Danila Panchenko, Viktor Ilyukha, Irina Baishnikova, Ekaterina Antonova, and Kseniya Nikerova. The first draft of the manuscript was written by Svetlana Kalinina and all the authors commented on previous versions of the manuscript. Conceptualization, review, and editing were performed by Andrea Canfield. All the authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval
All samples were collected during regular hunting activities and no animals were sacrificed for the sake of this study; therefore, no ethical approval was needed for compliance with our institutional or governmental organizations.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
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.
Supplementary information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kalinina, S., Panchenko, D., Ilyukha, V. et al. Elements and antioxidants in wild boar from northwestern Russia. Eur J Wildl Res 68, 22 (2022). https://doi.org/10.1007/s10344-022-01570-1
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10344-022-01570-1