Abstract
Wild boars (Sus scrofa) are part of the hunting economy and are highly consumed in the Iberian Peninsula, including in the Castile and Leon regions. As zoonotic diseases, chemical pollutants in wild boars’ internal tissues should be interpreted as evidence of environmental contamination and a matter of concern for animal, human and ecosystem health; in other words, a One Health concern. Twenty-eight wild boars’ livers and kidneys (n = 28) from Castile and Leon were submitted to metal(loid) determination (As, Cd, Co, Cr, Cu, Ni, Pb, and Zn) with inductively coupled plasma mass spectrophotometry (ICP-MS) and histopathological exam. Cd levels, especially in the kidneys (7.063 ± 7.271 mg/kg dw), were the most concerning results, considering the calculated maximum values for consumption (EC No. 915/2023) (2.491 mg/kg dw or 1.0 mg/kg ww). Wild boars with hydropic changes in the liver presented higher concentrations of Ni. Thus, the metal(loid) contamination of wild boar carcasses seems to be a “no trace” but very relevant problem that should raise awareness of a more accurate monitoring program and other strategies to avoid public health consequences.
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References
Ali H, Khan E (2019) Trophic transfer, bioaccumulation, and biomagnification of non-essential hazardous heavy metals and metalloids in food chains/webs—Concepts and implications for wildlife and human health. Hum Ecol Risk Assess 25:1353–1376. https://doi.org/10.1080/10807039.2018.1469398
Ali H, Khan E, Ilahi I (2019) Environmental Chemistry and Ecotoxicology of Hazardous Heavy Metals: Environmental Persistence, Toxicity, and Bioaccumulation. J of Chemist. 2019. 1–14. https://doi.org/10.1155/2019/6730305
Balali-Mood M, Naseri K, Tahergorabi Z et al (2021) Toxic mechanisms of five heavy metals: Mercury, lead, Chromium, Cadmium, and Arsenic. Front Pharmacol 12. https://doi.org/10.3389/fphar.2021.643972
Buttke DE (2011) Toxicology, environmental health, and the One Health concept. J Med Toxicol 7:329–332. https://doi.org/10.1007/S13181-011-0172-4
Carneiro MA, Oliveira PA, Brandão R et al (2016) Lead Poisoning due to lead-pellet ingestion in Griffon vultures (Gyps fulvus) from the Iberian Peninsula. J Avian Med Surg 30:274–279. https://doi.org/10.1647/2014-051
Castellanos P, Reglero MM, Taggart MA, Mateo R (2010) Changes in fatty acid profiles in testis and spermatozoa of red deer exposed to metal pollution. Reprod Toxicol 29:346–352. https://doi.org/10.1016/j.reprotox.2010.01.005
Cebulska K, Sobiech P, Tobolski D et al (2021) Comparison of the content of selected heavy metals in the liver tissue of the wild boar (Sus scrofa), red fox (Vulpes vulpes) and red deer (Cervus elaphus), living in north-eastern Poland. Pol J Vet Sci 24:424–432. https://doi.org/10.24425/pjvs.2021.138734
Centers of Disease Control and Prevention (CDC) (2023) One Health Basics. One Health. Available online: https://www.cdc.gov/onehealth/basics/index.html (accessed on 8 October 2023)
Ciobanu MM, Munteanu M, Postolache AN, Boișteanu PC (2020) Toxic heavy metals content in wild boar and venison meat: a brief review. Scietific Papers Series D Animal Science 63:435–441
Comission R (2023) No 915/2023: of 25 April 2023 on maximum levels for certain contaminants in food and repealing Regulation (EC) No 1881/2006
Comission Regulation (2014) Recommendation for reduction of Cadmium in food (2014/193/UE)
Cooke JA (2011) Cadmium in small mammals. In: Beyer WN, Meador JP (eds) Environmental contaminants in Biota, 2nd edn. CRC Press, pp 627–639
Dahiya V (2022) Heavy metal toxicity of drinking water: a silent killer. GSC Biol and Pharma Sci 19:20–25. https://doi.org/10.30574/GSCBPS.2022.19.1.0107
Dobrowolska A, Melosik M (2008) Bullet-derived lead in tissues of the wild boar (Sus scrofa) and red deer (Cervus elaphus). Eur J Wildl Res 54:231–235. https://doi.org/10.1007/s10344-007-0134-y
Donskoy E, Donskoy M, Forouhar F et al (1986) Hepatic toxicity of Nickel Chloride in rats. Ann Clin Lab Sci 16:108–117
Eisler R (1988) Arsenic hazards to fish, wildlife, and invertebrates: a synoptic review. Biological Report 85 (1.12) - Contaminant Hazard Reviews. https://pubs.usgs.gov/publication/5200037
Ertl K, Kitzer R, Goessler W (2016) Elemental composition of game meat from Austria. Food Addit Contam Part B Surveill 9:120–126. https://doi.org/10.1080/19393210.2016.1151464
Gašparík J, Binkowski ŁJ, Jahnátek A et al (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 177:258–266. https://doi.org/10.1007/s12011-016-0884-z
Gluhcheva YG, Atanasov VN, Ivanova JM, Pavlova EH (2014) Chronic exposure to cobalt compounds - an in vivo study. Cent Eur J Biol 9:973–981. https://doi.org/10.2478/s11535-014-0334-x
Gomes-Neves E, Abrantes AC, Vieira-Pinto M, Müller A (2021) Wild Game Meat—a Microbiological Safety and Hygiene Challenge? Current Clinical Microbiology Reports 2021 8:2 8:31–39. https://doi.org/10.1007/S40588-021-00158-8
González-Gómez X, Cambeiro-Pérez N, Figueiredo-González M, Martínez-Carballo E (2021) Wild boar (Sus scrofa) as bioindicator for environmental exposure to organic pollutants. Chemosphere 268. https://doi.org/10.1016/j.chemosphere.2020.128848
Höfle Ú, Vincente J, Fernández de Mera IG et al (2004) Health risks in game production: the wild boar. Galemys 16:197–206
Kalinina S, Panchenko D, Ilyukha V et al (2022) Elements and antioxidants in wild boar from northwestern Russia. Eur J Wildl Res 68. https://doi.org/10.1007/s10344-022-01570-1
Kicińska A, Glichowska P, Mamak M (2019) Micro- and macroelement contents in the liver of farm and wild animals and the health risks involved in liver consumption. Environ Monit Assess 191:132. https://doi.org/10.1007/s10661-019-7274-x
Levengood JM, Heske EJ (2008) Heavy metal exposure, reproductive activity, and demographic patterns in white-footed mice (Peromyscus leucopus) inhabiting a contaminated floodplain wetland. Sci Total Environ 389:320–328. https://doi.org/10.1016/j.scitotenv.2007.08.050
Lopes FJV, Fonseca Borges JM (2004) Wild boar in Portugal. Galemys 16:243–251
Malmsten A, Dalin A-M, Pettersson J, Persson S (2021) Concentrations of cadmium, lead, arsenic, and some essential metals in wild boar from Sweden. Eur J Wildl Res 67:18. https://doi.org/10.1007/s10344-021-01460-y/Published
Mathur AK, Datta KK, Tandon SK, Dikshith TSS (1977) Effect of Nickel Sulphate on male rats. Bull Environ Contam Toxicol 17:241–248. https://doi.org/10.1007/BF01685557
Mccall KA, Huang C-C, Fierke CA (2000) Zinc and health: current status and future directions function and mechanism of Zinc Metalloenzymes 1. J Nutr 130:1437–1446
Medvedev N (1999) Levels of Heavy metals in Karelian wildlife 1989-91. Environ Monit Assess 56, 177–193 (1999). https://doi.org/10.1023/A:1005988511058
Neila C, Hernández-Moreno D, Fidalgo LE et al (2017) Does gender influence the levels of heavy metals in liver of wild boar? Ecotoxicol Environ Saf 140:24–29
Nielsen F (2021) Nickel. Adv Nutr 12:281–282. https://doi.org/10.1093/advances/nmaa154
Nriagu JO (1988) A silent epidemic of environmental metal Poisoning? Environ Pollut 50:139–161. https://doi.org/10.1016/0269-7491(88)90189-3
Owumi SE, Olayiwola YO, Alao GE et al (2020) Cadmium and nickel co-exposure exacerbates genotoxicity and not oxido-inflammatory stress in liver and kidney of rats: protective role of omega-3 fatty acid. Environ Toxicol 35:231–241. https://doi.org/10.1002/tox.22860
Reglero MM, Taggart MA, Monsalve-González L, Mateo R (2009) Heavy metal exposure in large game from a lead mining area: effects on oxidative stress and fatty acid composition in liver. Environ Pollut 157:1388–1395. https://doi.org/10.1016/J.ENVPOL.2008.11.036
Santos N, Correla-Neves M, Ghebremichael S et al (2009) Epidemiology of Mycobacterium bovis Infection in wild boar (Sus scrofa) from Portugal. J Wildl Dis 45:1048–1061. https://doi.org/10.7589/0090-3558-45.4.1048
Swiergosz R, Perzanowski K, Makosz U, Bitek I (1993) The incidence of heavy metals and other toxic elements in big game tissues. Sci Total Environ 225–231. https://doi.org/10.1016/s0048-9697(05)80022
Tataruch F, Kierdorf H (2003) Mammals as biomonitors. In: Markert BA, Breure AM, Zechmeister HG (eds) Bioindicators and biomonitors. Elsevier Science Ltd., pp 737–773
Teschke R (2022) Aluminum, Arsenic, Beryllium, Cadmium, Chromium, Cobalt, copper, Iron, lead, Mercury, Molybdenum, Nickel, Platinum, Thallium, Titanium, Vanadium, and zinc: Molecular aspects in Experimental Liver Injury. Int J Mol Sci 23:12213. https://doi.org/10.3390/ijms232012213
Vieira-Pinto M, Morais L, Caleja C et al (2011) Salmonella spp. in wild boar (Sus scrofa): a public and animal health concern. Game meat hygiene in focus. 131–136. https://doi.org/10.3920/978-90-8686-723-3_10
Vieira-Pinto M, Fernandes ARG, Santos MH, Marucci G (2021) Trichinella britovi Infection in wild boar in Portugal. Zoonoses Public Hlth 68:103–109. https://doi.org/10.1111/zph.12800
Yarsan E, Yipel M, Dikmen B et al (2014) Concentrations of essential and non-essential toxic trace elements in wild boar (Sus Scrofa L., 1758) tissues from Southern Turkey. Bull Environ Contam Toxicol 92:10–14. https://doi.org/10.1007/s00128-013-1134-0
Acknowledgements
We would like to thank the Laboratory of Quality of Animal Products from the Centre for Interdisciplinary Research in Animal Health (CIISA- Al4Animals), University of Lisbon, for their support during the lyophilisation of the samples, namely, José Prates, Mónica Martins and Maria P. Spínola. We also would like to thank Mrs. Lígia Bento from UTAD´s Histology and Surgical Pathology Lab for her excellent technical assistance.
Funding
This work was supported by National Funds by the Fundação para a Ciência e Tecnologia (FCT) e and Ministério da Ciência e Tecnologia (MCT). The authors of the research unit CITAB (CJB and PAO) received funding from FCT—reference of the project: UIDB/04033/2020. The authors of the research unit CECAV-Al4Animals (FS) also received funding from FCT — references of the projects: UIDB/CVT/00772/2020 and LA/P/0059/2020. FCT supported CJB due to the PhD scholarship 2021.04520.BD. Finally, CP, PP and EFS received financial support for the research unit GEOBIOTEC (UID/GEO/04035/2020).
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Conceptualisation, C.J.B., J.M.G.-O., F.S. and P.A.O.; sampling, J.M.G.-O and L.J.M.-G; methodology, C.J.B., F.S., P.P., C.P. and E.F.S.; writing—original draft preparation, C.J.B., writing—review and editing, all authors; supervision, J.M.G.-O., F.S. and P.A.O. All authors have read and agreed to the published version of the manuscript.
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None of the wild boars was killed specifically for this study; they were part of the hunting program and populational control, so no ethical approval was required. All the animals were killed according to the Spanish hunting laws.
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Jota Baptista, C., Seixas, F., Gonzalo-Orden, J.M. et al. Heavy metals and metalloids in wild boars (Sus Scrofa) – a silent but serious public health hazard. Vet Res Commun 48, 1015–1023 (2024). https://doi.org/10.1007/s11259-023-10272-1
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DOI: https://doi.org/10.1007/s11259-023-10272-1