Pulmonary oxidative stress in wild bats exposed to coal dust: A model to evaluate the impact of coal mining on health
Graphical abstract
Introduction
Coal is a combustible, sedimentary rock constituted by organic elements, minerals, heavy metals, and other inorganic compounds (Chen et al., 2005; Dalal et al., 1995; León-Mejía et al., 2011), and fossilized over millions of years, similar to all fossil fuels (Castranova and Vallyathan, 2000; Gupta, 2007), which vary depending on the site of their origin (Donbak et al., 2005; Dontala et al., 2015). Despite the serious environmental impacts of mining and coal use (Adibee et al., 2013; Choi, 2015; Limbri et al., 2013; Sun et al., 2011; Zocche et al., 2014, 2017), coal is still an important resource used for electric power generation, once fulfilling 41% of global electricity needs (Bian et al., 2010; Dai and Finkelman, 2018; Yu, 2017).
Coal dust is a fine, powdered form of coal classified as a very dangerous fossil pollutant (León et al., 2007; Zakrzewski, 1991). It contains more than 50 chemical elements (Ketris and Yudovich, 2009), including heavy metals, and comprise inorganic compounds, like oxides, silica, and ash (Caballero-Gallardo and Olivero-Verbel, 2016; Finkelman, 1994; León et al., 2007; Singh et al., 2012, 2015). Nowadays, many coal mining sites are no longer active; however, the closure of mining areas does not mean the end of the polluting process, nor exhaustion of the source of pollution, because the environmental effects of coal mining persist for a long time (Dontala et al., 2015; Zocche et al., 2010).
Coal mining releases large amounts of coal dust (Huertas et al., 2012; Sinitsky et al., 2016; Yu, 2017) that is rich in chemical elements such as Co, Cu, Ni, Pb, Zn, Al, Cr, Mn, Co (Zocche et al., 2014, 2017), mineral nanoparticles, and inorganic substances (León-Mejía et al., 2014) that form heterogeneous compounds containing COX, NOX, SOX, Al, Si, crystals, quartz, and sulfur (León et al., 2007; Stephens and Ahern, 2001; Zhou et al., 2005). Once in the environment, these pollutants present a high risk to the health of wildlife, due to the potential synergistic effects of these complex mixtures (Dontala et al., 2015; Gold and Ames, 1990; Stephens and Ahern, 2001).
In addition, inhalation of dust generated during the extraction and deposition of coal can lead to significant harmful effects, especially those that affect the respiratory system, that can lead to morbidity and decreased life expectancy (Pinho et al., 2004). Workers in the coal industry, and wildlife and people who live near coal mining areas, are commonly exposed to coal dust and its contaminants, including heavy metals and quinones (Li et al., 2008) that can cause severe occupational hazards. The lungs are the first target sites of oxidants produced during oxygen combustion (Mossman, 2003).
Studies have suggested that, after exposure to industrial particles, significant biochemical changes occur in the lungs. Specifically, mineral coal, in addition to the toxic elements present in its composition, releases other components aggregated during extraction, such as silica and iron. These substances, after inhalation, can alter both the physical structure and the physiology of the pulmonary system (Tao et al., 2003). The activation of macrophages and recruitment of polymorphonuclear cells, caused by the deposition of industrial particles, probably results in the induction of lung damage. This process activates cytokines, chemokines, and ROS as inflammatory mediators, which promote local and systemic oxidative stress and, consequently, cause deleterious effects involving lung tissue (Mossman, 2003).
DNA damage from oxidative stress has been observed in peripheral blood lymphocytes of coal mining employees (Schins et al., 1995; Schoket et al., 1999). These effects arise from interaction between ROS and DNA, forming adducts with purines after metabolic activation (Baird et al., 2005; León-Mejía et al., 2011; Sinitsky et al., 2016). Additionally, other natural sources, such as ionizing radiation, also induce DNA damage through double-strand DNA breaks in coal miners (Robertson et al., 2013).
Biomonitors, also known as sentinel organisms, have been used for a long period to alert people about dangerous environments. For the selection of a biomonitor, the main aspects to be observed are: (a) the animals must share the same environment with humans; (b) respond in a similar fashion to toxic chemicals; and (c) develop similar pathologies in response to these effects (Silva et al., 2003). According to Jones et al. (2009), bats can serve as biomonitors for human health in mining areas, as well in other anthropic environments (Benvindo-Souza et al., 2019a, 2019b), since these animals are at the same trophic level and may accumulate toxic elements in their organs (O'Shea et al., 2001). Therefore, the objective of this study was to verify possible alterations in histological and oxidative stress parameters in the lungs of wild bats in the Carboniferous Basin of Santa Catarina state, Southern Brazil, as a model system to evaluate the impact of coal dust on the health of wildlife.
Section snippets
Description of the study areas
The study was carried out in two regions of south of Brazil, where one was free of contamination by coal mining activities (control area) and the other under the influence of coal mining activities (mined area). Bats were collected from the Natural Reserve of Salto Morato (25°10′ S and 48°15′W), a municipality of Guaraqueçaba, north of Parana state (control area), and from the municipalities of Criciúma (28°40′ S and 49°22′ W) and Treviso (28°30′ S and 49°27′ W), south Santa Catarina state, in
Chemical analysis of the lungs of bats
Table 1 presents the pulmonary levels of chemical elements on a dry weight (μg·g−1) basis, which varied across both the species and studied areas. The lung levels of Na, Cl, Cu, and Br in the individuals of both species from the coal mining areas were higher than those in animals collected from the control area. On the other hand, the lung levels of K and Rb in A. lituratus from coal mining areas were higher than in A. lituratus from the control area, while Si, Ca and Fe were higher in S. lilium
Discussion
Unlike organic substances, several chemical elements such as trace metals and metalloids are non-biodegradable and therefore remain in the soil and sediment compartments for a long time (Kabata-Pendias, 2011). This enduring permanence presents deleterious risks to human and wildlife health (Kabata-Pendias, 2011; Khan et al., 2010). In biochemical processes, chemical elements are recognized as being essential and non-essential, based on their physiological function (Kabata-Pendias, 2011).
Conclusions
The results of this study suggest that chronic exposure of bats to an environment filled with coal dust particles promotes histological and oxidative damage and, therefore, these animals may act as bioindicators of the ecotoxicological potential for wild populations that inhabit such coal dust particle-enriched areas. Additional studies are needed so that we can more accurately assess the damage generated in the respiratory and other organic systems of Chiroptera, and thus use these animals as
CRediT authorship contribution statement
Giulia dos Santos Pedroso-Fidelis: Investigation, Data curation, Writing - original draft. Hémelin Resende Farias: Investigation. Gustavo Antunes Mastella: Investigation. Liana Appel Boufleur-Niekraszewicz: Investigation, Data curation. Johnny Ferraz Dias: Investigation, Resources. Marcio Correa Alves: Investigation. Paulo Cesar Lock Silveira: Investigation, Formal analysis, Writing - original draft. Renata Tiscoski Nesi: Investigation, Formal analysis. Fernando Carvalho: Investigation,
Declaration of competing interest
The authors declare that there are no conflicts of interest.
Acknowledgments
The authors wish to thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brazil, and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brazil, for research support.
References (100)
Catalase in vitro
Methods Enzymol.
(1984)- et al.
Changes in thiol content and expression of glutathione redox system genes in the hippocampus and cerebellum in Alzheimer's disease
Neurosci. Lett.
(2001) - et al.
Phytoremediation of heavy metals - concepts and applications
Chemosphere
(2013) - et al.
Enzymatic responses to metal exposures in a freshwater fish Oreochromis niloticus
Comp. Biochem. Physiol. C Toxicol. Pharmacol.
(2007) - et al.
Propolis reversed cigarette smoke-induced emphysema through macrophage alternative activation independent of Nrf2
Bioorg. Med. Chem.
(2017) - et al.
Genotoxicological analyses of insectivorous bats (Mammalia: Chiroptera) in central Brazil: the oral epithelium as an indicator of environmental quality
Environ. Pollut.
(2019) - et al.
Environmental issues from coal mining and their solutions
Min. Sci. Technol.
(2010) Reduced free-radical production and extreme longevity in the little brown bat (Myotis lucifugus) versus two nonflying mammals
Mech. Ageing Dev.
(2004)- et al.
Mice housed on coal dust-contaminated sand: a model to evaluate the impacts of coal mining on health
Toxicol. Appl. Pharmacol.
(2016) Sustainable management of mining operations with accidents: a mean-variance optimization model
Resour. Policy
(2015)
Betulin inhibited cigarette smoke-induced COPD in mice
Biomed. Pharmacother.
Effects of chronic exposure to coal in wild rodents (Ctenomys torquatus) evaluated by multiple methods and tissues
Mutat. Res. Genet. Toxicol. Environ. Mutagen.
Coal as a promising source of critical elements: progress and future prospects
Int. J. Coal Geol.
Hydroxyl radical generation by coal mine dust: possible implication to coal workers' pneumoconiosis (CWP)
Free Radic. Biol. Med.
The genotoxic risk of underground coal miners from Turkey
Mutat. Res.
Environmental aspects and impacts its mitigation measures of corporate coal mining
Procedia Earth and Planetary Science
Metabolism and functions of glutathione in brain
Prog. Neurobiol.
TNF alpha and increased chemokine expression in rat lung after particle exposure
Toxicol. Lett.
Biomarkers measured by cytokinesis-block micronucleus cytome assay for evaluating genetic damages induced by polycyclic aromatic hydrocarbons
Mutat. Res.
Modes of occurrence of potentially hazardous elements in coal: levels of confidence
Fuel Process. Technol.
Glutathione: overview of its protective roles, measurement, and biosynthesis
Mol. Asp. Med.
Coal and tire burning mixtures containing ultrafine and nanoparticulate materials induce oxidative stress and inflammatory activation in macrophages
Sci. Total Environ.
Analysis of nitrate, nitrite and [15N] nitrate in biological fluids
Anal. Biochem.
Rapid quantification of malondialdehyde in plasma by high performance liquid chromatography-visible detection
J. Pharm. Biomed. Anal.
Target preparation for trace element determination of biological materials using nuclear techniques
Nucl. Instrum. Methods A
A fluorometric method for determination of oxidized and reduced glutathione in tissues
Anal. Biochem.
Air quality impact assessment of multiple open pit coal mines in northern Colombia
J. Environ. Manag.
Expression of antioxidant enzymes in rat lungs after inhalation of asbestos or silica
J. Biol. Chem.
The role of free radicals in asbestos induced diseases
Free Radic. Biol. Med.
Estimations of Clarkes for carbonaceous biolithes: world averages for trace element contents in black shales and coals
Int. J. Coal Geol.
Superoxide radical inhibits Catalase
J. Biol. Chem.
Organometal-induced increases in oxygen reactive species: the potential of 2',7'-dichlorofluorescin diacetate as an index of neurotoxic damage
Toxicol. Appl. Pharmacol.
Genotoxic effects in wild rodents (Rattus rattus and Mus musculus) in an open coal mining area
Mutat. Res.
Assessment of DNA damage in coal open-cast mining workers using the cytokinesis-blocked micronucleus test and the comet assay
Sci. Total Environ.
Genetic damage in coal miners evaluated by buccal micronucleus cytome assay
Ecotoxicol. Environ. Saf.
The role of oxidative stress in ambient particulate matter-induced lung diseases and its implications in the toxicity of engineered nanoparticles
Free Radic. Biol. Med.
Mineral and chemical composition and some trace element contents in coals and coal ashes from Huaibei coal field
Energy Convers. Manag.
Introduction to serial reviews on the role of reactive oxygen and nitrogen species (ROS/RNS) in lung injury and diseases
Free Radic. Biol. Med.
Contribution of NAD(P)H:quinone oxidoreductase 1 to protection against carcinogenesis, and regulation of its gene by the Nrf2 basic-region leucine zipper and the arylhydrocarbon receptor basic helix-loop-helix transcription factors
Mutat. Res.
Lung oxidative response after acute coal dust exposure
Environ. Res.
N-Acetylcysteine and deferoxamine reduce pulmonary oxidative stress and inflammation in rats after coal dust exposure
Environ. Res.
Genetic and oxidative damage of peripheral blood lymphocytes in workers with occupational exposure to coal
Mutat. Res.
Metals in liver and kidneys and the effects of chronic exposure to pyrite mine pollution in the shrew Crocidura russula inhabiting the protected wetland of Doñana
Chemosphere
Mechanisms and mediators in coal dust induced toxicity: a review
Ann. Occup. Hyg.
Biomonitoring of human genotoxicity induced by complex occupational exposures
Mutat. Res.
Mixed bacterial consortium as an emerging tool to remove hazardous trace metals from coal
Fuel
Reactive oxygen species in pulmonary Inflammation by ambient particulates
Free Radic. Biol. Med.
The importance of glutathione in human disease
Biomed. Pharmacother.
High oxidative stress in patients with stable coronary heart disease
Atherosclerosis
Gallic acid induced lung cancer cell death is related to glutathione; depletion as well as reactive oxygen species increase
Toxicol. In Vitro
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