Investigation of hepatotoxicity induced by polymetallic pollution and conventional breeding system in chickens

Sameh Elkribi; Iteb Boughattas; Sondes Hellaoui; Moncef Mokni; Mohamed Banni

doi:10.56027/JOASD.302025

Authors

Sameh Elkribi Department of Biological Sciences, Faculty of Science of Tunis
Iteb Boughattas Laboratory of Agrobiodiversity and Ecotoxicology, Higher Institute of Agronomy, Chott-Mariem Tunisia
Sondes Hellaoui 2 Laboratory of Agrobiodiversity and Ecotoxicology, Higher Institute of Agronomy, Chott-Mariem Tunisia
Moncef Mokni Department of Pathology, CHU Farhat Hached, Sousse, Tunisia
Mohamed Banni Department of Pathology, CHU Farhat Hached, Sousse, Tunisia

DOI:

https://doi.org/10.56027/JOASD.302025

Keywords:

Conventional breeding, genotoxicity, heavy metal, histological damage, hepatotoxicity, oxidative stress

Abstract

Modernization has led to environmental contamination from various chemicals, raising concerns about their impact on animal health. To investigate the specific effects of breeding methods on liver health in hens (Gallus gallus domesticus), focusing on two potential environmental pollution factors: heavy metal contamination and the use of veterinary additives and drugs. To achieve our purpose, the study analyzed three batches of hens: (1) controls from free-range organic farms, (2) conventional farming, and (3) free range breeding in an industrial site (Jebel Ressas old mine). After a six-month period, liver tissues were examined for the accumulation of malondialdehyde (MDA), the frequency of micronuclei (MN) as a marker for genotoxicity, and histological alterations.

The current study highlighted that varying breeding environment, potentially associated with increased use of additives, drugs, and antibiotics, notably impact the overall health of the animal liver. Moreover, exposure to heavy metals has been identified as a severe cause of health issues due to its interference with normal biological mechanisms and disruption of natural reactions. Given their non-biodegradable nature, these metals persist for extended periods, posing long-term health risks. While these findings raise concerns about the potential health risks associated with such practices. Our results suggest that exposure to heavy metals poses more serious threat. This underscores the urgent need for stricter regulations and more sustainable approaches to protect both animal welfare and public health.

References

Ahmet Semih U. and Münise Dilli, (2023). Estimating Chicken Meat Productions of Leader Countries for 2019-2025 Years. Agribusiness 53 (2). https://doi.org/10.1590/0103-8478cr20210477

Amri S., Mohamed-Faouzi S., Sellem F., Ouali K., (2017). Seasonal antioxidant responses in the sea urchin Paracentrotus lividus (Lamarck 1816) used as a bioindicator of the environmental contamination in the South-East Mediterranean. Marine Pollution Bulletin 122 : 1-2. https://doi.org/10.1016/j.marpolbul.2017.06.079

Attig H., Kamel N., Sforzinib S., Dagnino A., Boussettaa H., Banni M., (2014). Effects of thermal stress and nickel exposure on biomarkers responses in Mytilus galloprovincialis. Environmental Research 94 : 65-71. https://doi.org/10.1016/j.marenvres.2013.12.006

Bolognesi C., Lando C., Forni A., Landini E., Scarpato R., Migliore L., Bonassi S., (1999). Chromosomal damage and ageing: effect on micronuclei frequency in peripheral blood lymphocytes. Age and Ageing. 28-4 : 393-397. https://doi.org/10.1093/ageing/28.4.393

Botelho R.G., Christofoletti C.A., et al (2015). Genotoxic responses of juvenile tilapia (Oreochromis niloticus) exposed to florfenicol and oxytetracycline. Chemosphere 132:206-212. https://doi.org/10.1016/j.chemosphere.2015.02.053

Banni M., Bouraoui Z., Clerandeau C., Narbonne J.F. , Boussetta H., (2009). Mixture toxicity assessment of cadmiumand benzo[a]pyrene in the sea worm Hediste diversicolor. Chemosphere 77 : 902–906. https://doi.org/10.1016/j.chemosphere.2009.08.041

Boughattas I., Hattab S., Boussetta H., Sappin-Didier V., Viarengo A., Banni M., Sforzini S., (2016). Biomarker responses of Eisenia andrei to a polymetallic gradient near a lead mining site in North Tunisia. Environ Pollut 530-541:530–541. https://doi.org/10.1016/j.envpol.2016.07.033

Cardoso O., (2015). Towards a better understanding of the ecotoxicological, effects induced by pharmaceutical industrial releases in chronically exposed wild fish. Doctoral thesis, University of Reims Champagne-Ardenne.

Chardon H. and Burger H., (2014). Uses of antibiotics in livestock and meat sectors. Cahiers sanitary safety, animal health, Meat Information Center, Paris, France.

Dupuy C., (2012). Responses of fish populations to chemical stress in estuarine environments: integration of molecular, biochemical and immunotoxicological responses. Agricultural sciences. University of Western Brittany - Brest; National Institute of Scientific Research. Quebec province.

D. Bernet, H. Schmidt, W. Meier, P. Burkhardt-Holm, T. Wahli, (2001). Histopathology in fish: proposal for a protocol to assess aquatic pollution. Fish Diseases. https://doi.org/10.1046/j.1365-2761.1999.00134.x

Elkribi-Boukhris S., Boughattas I., Zitouni N., Hellaoui S., Sappin-Didier V., Coriou C., Bussiere S., Banni M., (2020). Ecotoxicity of trace elements to chicken GALLUS gallus domesticus exposed to a gradient of polymetallic-polluted sites. Environ.Pollut. 265:114831. https:// doi.org/10.1016/j.envpol.2020.114831

Elkribi-Boukhris S., M’hamdi N., Boughattas I., Helaoui S., Coriou C., Bussiere S., Sappin-Didier V., Banni M., (2021). Assessment of heavy metal pollution transfer and human exposure risks from the consumption of chicken grown in mining-surrounding areas. Environmental Science and Pollution Research. 29 : 5661–5673 https://doi.org/10.1007/s11356-021-15995-9

Fenech M., Crott J., Turner J., Brown S., (1999). Necrosis, apoptosis, cytostasis and DNA damage in human lymphocytes measured simultaneously within the cytokinesis-block micronucleus assay: description of the method and results for hydrogen peroxide. Oxford, Journals Medicine & Health & Science & Mathematics, Mutagenesis. 14-6 :605-612. https://doi.org/10.1093/mutage/14.6.605

Grinwis G.C.M., Vethaak A.D., Waster P.W., Vos J.G., (2000). Toxicology of environment al chemicals in the flounder Platichthys flesus with emphasis on the immune system: Field, semi-field (mescocosm) and laboratory studies. Toxicology letters 112-113: 289-301. https://doi.org/10.1016/S0378-4274(99)00239-8

Hamdy S.M., Shaban A.M., Aziz Y.S.A., Mahmoud A.M., Moemen L.A.A., Ibrahim W.M., Gad N.S., (2018). Ameliorative role of jania rubens alga against toxicity of heavy metal polluted water in male rats. Science, Technology & Public Policy 2(2): 38-46. https://doi:10.11648/j.stpp.20180202.13

Iskandar A., Carman O., Zairin M. Jr., Suprayudi M.A., Winarto A., Effendi I., Sudrajat A.O., (2023)Domestication of Javaen Barb (Puntius orphoides) as Indonesian Endemic Fish: Breeding the Aquaculture Commodity Candidate to Increase Seed Productivity. Earth and Environmental Science. https://doi.org/10.1088/1755-1315/1221/1/012053

Jebali J., Ben-Khedher S., Ghedira J., Kamel K., Boussetta H., (2011). Integrated assessment of biochemical responses in Mediterranean crab (Carcinus maenas) collected from Monastir Bay, Tunisia. Journal of Environmental Sciences 23(10): 1714–1720. https://doi.org/10.1016/S1001-0742(10)60617-1

Kleinkauf A., Connor L., et al (2004). General condition biomarkers in relation to contaminant burden in European flounder (Platichthys flesus). Ecotoxicology and Environmental Safety 58-3 : 335-355. https://doi.org/10.1016/j.ecoenv.2004.03.007

Kumar A., Kumar A., et al (2020). Lead toxicity: health hazards, influence on food chain, and sustainable remediation approaches. Int. J. Environ. Res. Public Health 17(7): 2179 https://doi.org/10.3390/ijerph17072179

Lam and Gris, (2003). The use of biomarkers in environmental monitoring programmes. Mar. Pollut. Bull 46 : 182-186. https://doi.org/10.1016/S0025-326X(02)00449-6

Livingstone, D.R., (2001). Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar. Pollut. Bull. 656e666

Lourenço J., Silva A., Carvalho F., Oliveira J., Malta M., Mendo S., Gonçalves F., Pereira F., (2011). Histopathological changes in the earthworm Eisenia andrei associated with the exposure to metals and radionuclides. Chemosphere 85 : 1630–1634. https://doi.org/10.1016/j.chemosphere.2011.08.027

M. Estévez, (2015). Oxidative damage to poultry: from farm to fork. Poultry Science 94 :6. https://doi.org/10.3382/ps/pev094

Missawi O., Bousserrhine N., Zitouni N., Maisano M., et al. (2021). Uptake, accumulation and associated cellular alterations of environmental samples of microplastics in the seaworm Hediste diversicolor. Journal of Hazardous Materials 406 : 124287. https://doi.org/10.1016/j.jhazmat.2020.124287

Morcillo P., Esteban M., Cuesta A., (2016). Heavymetals produce toxicity, oxidative stress and apoptosis in the marine teleost fish SAF-1 cellline. Chemosphere 144: 225-233. https://doi.org/10.1016/j.chemosphere.2015.08.020

OECD FAO Agricultural Outlook (2018 2027), page 238.

Okeke E.S., Okoye C.O., et al., (2022). Microplastics in agroecosystems-impacts on ecosystem functions and food chain. Resources, Conservation and Recycling 177: (105961). https://doi.org/10.1016/j.resconrec.2021.105961

Peter F. Surai, Ivan I. Kochish,Vladimir I. Fisinin, Michael T. Kidd, (2019). Antioxidant Defence Systems and Oxidative Stress in Poultry Biology: An Update. Antioxidants 8(7), 235. https://doi.org/10.3390/antiox8070235

Rehman U., Khan R., Khan A., et al., (2021). Fate of arsenic in living systems: Implications for sustainable and safe food chains. Journal of Hazardous Materials 417 : 126050. https://doi.org/10.1016/j.jhazmat.2021.126050

Rezaei R.O., Sobhanardakani S., Cheraghi M., (2016). Health risk assessment of citrus contaminated with heavy metals in Hamedan city, potential risk of Al and Cu. Environ. Health Eng. Manag 3-3 : 131-135

Ritchie H., and Roser M., (2020). Environmental impact of food production. Our world in data. https://ourworldindata.org/environmental-impacts-of-food'

Rodrigues S., Antunesa S.C., Correiab A.T., Nunesc B., (2016). Acute and chronic effects of erythromycin exposure on oxidative stress and genotoxicity parameters of Oncorhynchus mykiss. 545-546 : 591–600. https://doi.org/10.1016/j.scitotenv.2015.10.138

Romdhani I., De Marcob G., Cappello T., Ibala S., Zitouni N., Boughattas I., Banni M., (2022). Impact of environmental microplastics alone and mixed with benzo[a]pyrene on cellular and molecular responses of Mytilus galloprovincialis. Journal of Hazardous Materials 435 : 128952. https://doi.org/10.1016/j.jhazmat.2022.128952

Saif M. Al-Ghais, (2013). Acetylcholinesterase, glutathione and hepatosomatic index as potential biomarkers of sewage pollution and depuration in fish, Marine Pollution Bulletin, 74(1):183-186. https://doi.org/10.1016/j.marpolbul.2013.07.005

Shubhangi P., (2016). Plant used in preparation of agricultural implement in Jalgaon district Maharashtra, India. Lifesciences Leaflets. 81 : 67-69.

Wang Y., Zhao H., Shao Y., Liu J., Li J., Luo L., Xing M., (2018). Copper (II) and/or arsenite-induced oxidative stress cascades apoptosis and autophagy in the skeletal muscles of chicken. Chemosphere 206 : 597-605. https://doi.org/10.1016/j.chemosphere.2018.05.013

Youcef Mehdi, Marie-Pierre Létourneau-Montminy, Marie-Lou Gaucher, Younes Chorfi, Gayatri Suresh, Tarek Rouissi, Satinder Kaur Brar, Caroline Côté, Antonio Avalos Ramirez, Stéphane Godbout, (2018). Use of antibiotics in broiler production: Global impacts and alternatives. Animal Nutrition 4(2) :170-178. https://doi.org/10.1016/j.aninu.2018.03.002