Abstract
Heavy metals (HMs) constitute a group of persistent toxic pollutants, and the petroleum industry is one of the sources of these metals. This study aimed to evaluate the levels of lead (Pb), cadmium (Cd), nickel (Ni), and vanadium (V) in Plantago ovata and milk and tissues of domestic goats in the eastern region of Saudi Arabia. Plant samples and blood, milk, muscle, liver, and kidney samples were collected from domestic goats and the levels of Pb, Cd, V, and Ni were determined. Liver and kidney tissue injury, oxidative stress, and expression of pro-inflammatory and apoptosis markers were evaluated. Pb, Cd, V, and Ni were increased in Plantago ovata as well as in milk, blood, muscle, liver, and kidney of goats collected from the polluted site. Aminotransferases, creatinine, and urea were increased in serum, and histopathological changes were observed in the liver and kidney of goats at the oil extraction site. Malondialdehyde and the expression levels of pro-inflammatory cytokines, Bax, and caspase-3 were increased, whereas cellular antioxidants and Bcl-2 were decreased in liver and kidney of goats at the polluted site. In conclusion, petroleum industry caused liver and kidney injury, oxidative stress, and upregulated pro-inflammatory and apoptosis markers in goats. These findings highlight the negative impact of petroleum industry on the environment and call attention to the assessment of its effect on the health of nearby communities.
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References
Adegbesan BO, Adenuga GA (2007) Effect of lead exposure on liver lipid peroxidative and antioxidant defense systems of protein-undernourished rats. Biol Trace Elem Res 116:219–225
Ajarem JS, Hegazy AK, Allam GA, Allam AA, Maodaa SN, Mahmoud AM (2021) Effect of visnagin on altered steroidogenesis and spermatogenesis, and testicular injury induced by the heavy metal lead. Comb Chem High Throughput Screening 24:758–766
Ajarem JS, Hegazy AK, Allam GA, Allam AA, Maodaa SN, Mahmoud AM (2022) Heavy metal accumulation, tissue injury, oxidative stress, and inflammation in dromedary camels living near petroleum industry sites in Saudi Arabia. Animals (Basel) 12(6):707
Mahmoud AM, Wilkinson FL, Sandhu MA, Lightfoot AP (2021) The interplay of oxidative stress and inflammation: mechanistic insights and therapeutic potential of antioxidants. Oxid Med Cell Longev 2021:9851914
Al-Otaibi FS, Ajarem JS, Abdel-Maksoud MA, Maodaa S, Allam AA, Al-Basher GI, Mahmoud AM (2018) Stone quarrying induces organ dysfunction and oxidative stress in Meriones libycus. Toxicol Ind Health 34:679–692
Alhusaini A, Fadda L, Hasan IH, Ali HM, El Orabi NF, Badr AM, Zakaria E, Alenazi AM, Mahmoud AM (2019a) Arctium lappa root extract prevents lead-induced liver injury by attenuating oxidative stress and inflammation, and activating Akt/GSK-3β signaling. Antioxidants (Basel, Switzerland) 8(12):582
Alhusaini A, Fadda L, Hasan IH, Zakaria E, Alenazi AM, Mahmoud AM (2019b) Curcumin ameliorates lead-induced hepatotoxicity by suppressing oxidative stress and inflammation, and modulating Akt/GSK-3β signaling pathway. Biomolecules 9(11):703
Almalki A, Ajarem J, Allam AA, El-Serehy HA, Maodaa SN, Mahmoud AM (2019a) Use of Spilopelia senegalensis as a biomonitor of heavy metal contamination from mining activities in Riyadh (Saudi Arabia). Animals (Basel) 9
Almalki AM, Ajarem J, Altoom N, Al-Otaibi FS, Maodaa SN, Allam AA, Mahmoud AM (2019b) Effects of mining activities on Gerbillus nanus in Saudi Arabia: a biochemical and histological study. Animals (basel) 9:664
Alotaibi MF, Al-Joufi F, Abou Seif HS, Alzoghaibi MA, Djouhri L, Ahmeda AF, Mahmoud AM (2020) Umbelliferone inhibits spermatogenic defects and testicular injury in lead-intoxicated rats by suppressing oxidative stress and inflammation, and improving Nrf2/HO-1 signaling. Drug Des Dev Ther 14:4003–4019
Altamirano-Lozano MA, Alvarez-Barrera L, Mateos-Nava RA, Fortoul TI, Rodriguez-Mercado JJ (2014) Potential for genotoxic and reprotoxic effects of vanadium compounds due to occupational and environmental exposures: an article based on a presentation at the 8th International Symposium on Vanadium Chemistry, Biological Chemistry, and Toxicology, Washington DC, August 15–18, 2012. J Immunotoxicol 11:19–27
Bancroft JD, Gamble M (2008) Theory and practice of histological techniques. Elsevier health sciences, Churchill Livingstone, Elsevier, London, UK
Barwise AJG (1990) Role of nickel and vanadium in petroleum classification. Energy Fuels 4:647–652
Beutler E, Duron O, Kelly BM (1963) Improved method for the determination of blood glutathione. J Lab Clin Med 61:882–888
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Brown P (2003) Qualitative methods in environmental health research. Environ Health Perspect 111:1789–1798
Castagnetto JM, Hennessy SW, Roberts VA, Getzoff ED, Tainer JA, Pique ME (2002) MDB: the Metalloprotein Database and Browser at The Scripps Research Institute. Nucleic Acids Res 30:379–382
Castellini C, Mourvaki E, Sartini B, Cardinali R, Moretti E, Collodel G, Fortaner S, Sabbioni E, Renieri T (2009) In vitro toxic effects of metal compounds on kinetic traits and ultrastructure of rabbit spermatozoa. Reprod Toxicol (Elmsford, N.Y.) 27:46–54
Cohen G, Dembiec D, Marcus J (1970) Measurement of catalase activity in tissue extracts. Anal Biochem 34:30–38
Dahlgren J, Takhar H, Anderson-Mahoney P, Kotlerman J, Tarr J, Warshaw R (2007) Cluster of systemic lupus erythematosus (SLE) associated with an oil field waste site: a cross sectional study. Environ Health : A Glob Access Sci Source 6:8
de Kok TM, Hogervorst JG, Briede JJ, van Herwijnen MH, Maas LM, Moonen EJ, Driece HA, Kleinjans JC (2005) Genotoxicity and physicochemical characteristics of traffic-related ambient particulate matter. Environ Mol Mutagen 46:71–80
Dey T, Gogoi K, Unni B, Bharadwaz M, Kalita M, Ozah D, Kalita M, Kalita J, Baruah PK, Bora T (2015) Role of environmental pollutants in liver physiology: special references to peoples living in the oil drilling sites of Assam. PLoS One 10:e0123370
El-Nekeety AA, El-Kady AA, Soliman MS, Hassan NS, Abdel-Wahhab MA (2009) Protective effect of Aquilegia vulgaris (L.) against lead acetate-induced oxidative stress in rats. Food Chem Toxicol: An International Journal Published for the British Industrial Biological Research Association 47:2209–2215
El-Tantawy WH (2016) Antioxidant effects of Spirulina supplement against lead acetate-induced hepatic injury in rats. J Tradit Complement Med 6:327–331
Filby RH, Branthaver JF (1987): Metal complexes in fossil fuels: geochemistry, characterization, and processing. US:N., web
Flora SJS, Flora G, Saxena G (2006) Environmental occurrence, health effects and management of lead poisoning. In: Cascas SB, Sordo J (eds) Lead Chemistry, Analytical Aspects, Environmental Impacts and Health Effects. Elsevier Publication, Amsterdam, The Netherlands, pp 158–228
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
Guo H, Cui H, Fang J, Zuo Z, Deng J, Wang X, Zhao L, Wu B, Chen K, Deng J (2016) Nickel chloride-induced apoptosis via mitochondria- and Fas-mediated caspase-dependent pathways in broiler chickens. Oncotarget 7:79747–79760
Heidari R, Ahmadi A, Mohammadi H, Ommati MM, Azarpira N, Niknahad H (2018) Mitochondrial dysfunction and oxidative stress are involved in the mechanism of methotrexate-induced renal injury and electrolytes imbalance. Biomed Pharmacother 107:834–840
Jarup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182
Jia Q, Ha X, Yang Z, Hui L, Yang X (2012) Oxidative stress: a possible mechanism for lead-induced apoptosis and nephrotoxicity. Toxicol Mech Methods 22:705–710
Johnston JE, Lim E, Roh H (2019) Impact of upstream oil extraction and environmental public health: a review of the evidence. Sci Total Environ 657:187–199
Charkiewicz AE, Backstrand JR (2020) Lead toxicity and pollution in Poland. Int J Environ Res Public Health 17(12):4385
Kachhawa K, Varma M, Kachhawa P, Agrawal D, Shaikh M, Kumar S (2016) Study of dyslipidemia and antioxidant status in chronic kidney disease patients at a hospital in South East Asia. J Health Res Rev 3:28–30
Sarawi WS, Alhusaini AM, Fadda LM, Alomar HA, Albaker AB, Alghibiwi HK, Aljrboa AS, Alotaibi AM, Hasan IH, Mahmoud AM (2022) Nano-curcumin prevents copper reproductive toxicity by attenuating oxidative stress and inflammation and improving Nrf2/HO-1 signaling and pituitary-gonadal axis in male rats. Toxics 30;10(7):356
Khan MS, Zaidi A, Wani PA, Oves M, SpringerLink (2008) Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environ. chem. lett. 7:1–19
Kong L, Gao X, Zhu J, Cheng K, Tang M (2016) Mechanisms involved in reproductive toxicity caused by nickel nanoparticle in female rats. Environ Toxicol 31:1674–1683
Livak KJ, Schmittgen TDJm (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25, 402–408
Markiewicz-Górka I, Januszewska L, Michalak A, Prokopowicz A, Januszewska E, Pawlas N, Pawlas K (2015) Effects of chronic exposure to lead, cadmium, and manganese mixtures on oxidative stress in rat liver and heart. Arh Hig Rada Toksikol 66:51–62
Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. FEBS Eur J Biochem 47:469–474
Markopoulou S, Kontargiris E, Batsi C, Tzavaras T, Trougakos I, Boothman DA, Gonos ES, Kolettas E (2009) Vanadium-induced apoptosis of HaCaT cells is mediated by c-fos and involves nuclear accumulation of clusterin. FEBS J 276:3784–3799
Miedico O, Iammarino M, Paglia G, Tarallo M, Mangiacotti M, Chiaravalle AE (2016) Environmental monitoring of the area surrounding oil wells in Val d’Agri (Italy): element accumulation in bovine and ovine organs. Environ Monit Assess 188:338
Mudipalli A (2007) Lead hepatotoxicity & potential health effects. Indian J Med Res 126:518–527
Nesbitt JA, Lindsay MB (2017) Vanadium geochemistry of oil sands fluid petroleum coke. Environ Sci Technol 51:3102–3109
Norouzirad R, González-Montaña J-R, Martínez-Pastor F, Hosseini H, Shahrouzian A, Khabazkhoob M, Ali Malayeri F, Moallem Bandani H, Paknejad M, Foroughi-nia B, Fooladi Moghaddam A (2018) Lead and cadmium levels in raw bovine milk and dietary risk assessment in areas near petroleum extraction industries. Sci Total Environ 635:308–314
O’Callaghan-Gordo C, Orta-Martínez M, Kogevinas M (2016) Health effects of non-occupational exposure to oil extraction. Environ Health : A Global Access Science Source 15:56
Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358
Pareja-Carrera J, Mateo R, Rodríguez-Estival J (2014) Lead (Pb) in sheep exposed to mining pollution: implications for animal and human health. Ecotoxicol Environ Saf 108:210–216
Park EJ, Lee GH, Yoon C, Kim DW (2016) Comparison of distribution and toxicity following repeated oral dosing of different vanadium oxide nanoparticles in mice. Environ Res 150:154–165
Paz-y-Miño C, López-Cortés A, Arévalo M, Sánchez ME (2008) Monitoring of DNA damage in individuals exposed to petroleum hydrocarbons in Ecuador. Ann N Y Acad Sci 1140:121–128
Qi K, Ren L, Bai Z, Yan J, Deng X, Zhang J, Peng Y, Li X (2020) Detecting cadmium during ultrastructural characterization of hepatotoxicity. J Trace Elem Med Biol: Organ of the Society for Minerals and Trace Elements (GMS) 62:126644
Rojas-Lemus M, López-Valdez N, Bizarro-Nevares P, González-Villalva A, Ustarroz-Cano M, Zepeda-Rodríguez A, Pasos-Nájera F, García-Peláez I, Rivera-Fernández N, Fortoul TI (2021) Toxic effects of inhaled vanadium attached to particulate matter: a literature review. Int J Environ Res Public Health 18(16):8457
Rzymski P, Niedzielski P, Klimaszyk P, Poniedzialek B (2014) Bioaccumulation of selected metals in bivalves (Unionidae) and Phragmites australis inhabiting a municipal water reservoir. Environ Monit Assess 186:3199–3212
Rzymski P, Tomczyk K, Rzymski P, Poniedzialek B, Opala T, Wilczak M (2015) Impact of heavy metals on the female reproductive system. Annals Agric Environ Med: AAEM 22:259–264
Sarawi WS, Alhusaini AM, Fadda LM, Alomar HA, Albaker AB, Aljrboa AS, Alotaibi AM, Hasan IH, Mahmoud AM (2021a) Nano-curcumin prevents cardiac injury, oxidative stress and inflammation, and modulates TLR4/NF-κB and MAPK signaling in copper sulfate-intoxicated rats. Antioxidants (Basel, Switzerland) 10(9):1414
Sarawi WS, Alhusaini AM, Fadda LM, Alomar HA, Albaker AB, Aljrboa AS, Alotaibi AM, Hasan IH, Mahmoud AM (2021b) Curcumin and nano-curcumin mitigate copper neurotoxicity by modulating oxidative stress, inflammation, and Akt/GSK-3β signaling. Molecules 26:5591
Satarug S, Gobe CG, Vesey DA, Phelps KR (2020) Cadmium and lead exposure, nephrotoxicity, and mortality. Toxics 8(4):86
Schlesinger WH, Klein EM, Vengosh A (2017) Global biogeochemical cycle of vanadium. Proc Natl Acad Sci U S A 114:E11092–E11100
Singh R, Gautam N, Mishra A, Gupta R (2011) Heavy metals and living systems: an overview. Indian J Pharmacol 43:246–253
Wang J, Hao M, Liu C, Liu R (2015) Cadmium induced apoptosis in mouse primary hepatocytes: the role of oxidative stress-mediated ERK pathway activation and the involvement of histone H3 phosphorylation. RSC Adv 5:31798–31806
Wang J, Huang X, Zhang K, Mao X, Ding X, Zeng Q, Bai S, Xuan Y, Peng H (2017) Vanadate oxidative and apoptotic effects are mediated by the MAPK-Nrf2 pathway in layer oviduct magnum epithelial cells. Metallomics 9:1562–1575
Wang Y, Fang J, Leonard SS, Rao KM (2004) Cadmium inhibits the electron transfer chain and induces reactive oxygen species. Free Radical Biol Med 36:1434–1443
Yedjou CG, Milner JN, Howard CB, Tchounwou PB (2010) Basic apoptotic mechanisms of lead toxicity in human leukemia (HL-60) cells. Int J Environ Res Public Health 7:2008–2017
Yermukhanova LS, Zhexenova AN, Izimbergenova GN, Turebaev MN, Bekbauova AU, Zhumabekov EB, Umbetov MU (2017) Immunodeficiency states in persons residing in the oil-producing regions of Kazakhstan. Res J Med Sci 11:16–18
Yuan Y, Zhang Y, Zhao S, Chen J, Yang J, Wang T, Zou H, Wang Y, Gu J, Liu X, Bian J, Liu Z (2018) Cadmium-induced apoptosis in neuronal cells is mediated by Fas/FasL-mediated mitochondrial apoptotic signaling pathway. Sci Rep 8:8837
Acknowledgements
The authors would like to thank the National Plan for Sciences, Technology and Innovation (MAARIFAH), King Abdulaziz City for Science and Technology, Kingdom of Saudi Arabia for funding this research (grant number 13-ENV922-02).
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This study has been funded by the National Plan for Sciences, Technology and Innovation (MAARIFAH), King Abdulaziz City for Science and Technology, Kingdom of Saudi Arabia (grant number 13-ENV922-02).
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Conceptualization: Jamaan S. Ajarem, Ahmed A. Allam and Ayman M. Mahmoud; methodology and investigation: Jamaan S. Ajarem, Ahmad K. Hegazy, Gamal A. Allam, Ahmed A. Allam, Saleh N. Maodaa, Ayman M. Mahmoud; data curation: Ahmed A. Allam, Saleh N. Maodaa, Ayman M. Mahmoud; writing original draft: Ayman M. Mahmoud; Revision: Ayman M. Mahmoud; supervision: Jamaan S. Ajarem, Ahmed A. Allam and Ayman M. Mahmoud; Validation: Ayman M. Mahmoud; funding acquisition: Jamaan S. Ajarem, Ahmed A. Allam and Ayman M. Mahmoud.
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Ajarem, J.S., Hegazy, A.K., Allam, G.A. et al. Impact of petroleum industry on goats in Saudi Arabia: heavy metal accumulation, oxidative stress, and tissue injury. Environ Sci Pollut Res 30, 2836–2849 (2023). https://doi.org/10.1007/s11356-022-22309-0
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DOI: https://doi.org/10.1007/s11356-022-22309-0