Abstract
Epidemiological studies have shown that air particulate matter (PM) can increase respiratory morbidity and mortality being the lungs the main target organ to PM body entrance. Even more, several in vivo and in vitro studies have shown that air PM has a wide toxicity spectra depending among other parameters, on its size, morphology, and chemical composition. The Reconquista River is the second most polluted river from Buenos Aires, and people living around its basin are constantly exposed to its contaminated water, soil and air. However, the air PM from the Reconquista River (RR-PMa) has not been characterized, and its biological impact on lung has yet not been assessed. Therefore, the present investigation was undertaken to study (1) RR-PMa morphochemical characteristic and (2) RR-PMa lung acute effects after intranasal instillation exposure through the analysis of three end points: oxidative stress, inflammation, and apoptosis. A single acute exposure of RR-PMa (1 mg/kg body weight) after 24 h caused significant (p < 0.05) enrichment in bronchoalveolar total cell number and polymorphonuclear (PNM) fraction, superoxide anion generation, production of pro-inflammatory cytokines TNF-α and IL-6, and induction of apoptosis. It was also observed that in lung homogenates, none of the antioxidant enzymes assayed showed differences between exposed RR-PMa and control mice. These data demonstrate that air PM from the Reconquista River induce lung oxidative stress, inflammation, and cell death therefore represents a potential hazard to human health.
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Andreau K, Leroux M, Bouharrour A (2012) Health and cellular impacts of air pollutants: from cytoprotection to cytotoxicity. Biochem Res Int 2012:493894
Araujo JA (2010) Particulate air pollution, systemic oxidative stress, inflammation, and atherosclerosis. Air Qual Atmos Health 4(1):79–93
Baldauf RW, Lane DD, Marote GA (2001) Ambient air quality monitoring network design for assessing human health impacts from exposures to airborne contaminants. Environ Monit Assess 66(1):63–76
Beelen R, Hoek G, Houthuijs D, van den Brandt PA, Goldbohm RA, Fischer P et al (2009) The joint association of air pollution and noise from road traffic with cardiovascular mortality in a cohort study. Occup Environ Med 66(4):243–250
Chirino YI, Sanchez-Perez Y, Osornio-Vargas AR, Morales-Barcenas R, Gutierrez-Ruiz MC, Segura-Garcia Y et al (2010) PM(10) impairs the antioxidant defense system and exacerbates oxidative stress driven cell death. Toxicol Lett 193(3):209–216
Dick CA, Singh P, Daniels M, Evansky P, Becker S, Gilmour MI (2003) Murine pulmonary inflammatory responses following instillation of size-fractionated ambient particulate matter. J Toxicol Environ Health A 66(23):2193–2207
Donaldson K, Stone V, Borm PJ, Jimenez LA, Gilmour PS, Schins RP et al (2003) Oxidative stress and calcium signaling in the adverse effects of environmental particles (PM10). Free Radic Biol Med 34(11):1369–1382
Dreher KL, Jaskot RH, Lehmann JR, Richards JH, McGee JK, Ghio AJ et al (1997) Soluble transition metals mediate residual oil fly ash induced acute lung injury. J Toxicol Environ Health 50(3):285–305
Dye JA, Lehmann JR, McGee JK, Winsett DW, Ledbetter AD, Everitt JI et al (2001) Acute pulmonary toxicity of particulate matter filter extracts in rats: Coherence with epidemiologic studies in Utah Valley residents. Environ Health Perspect 109(Suppl 3):395–403
Evelson P, Gonzalez-Flecha B (2000) Time course and quantitative analysis of the adaptive responses to 85 % oxygen in the rat lung and heart. Biochim Biophys Acta 1523(2–3):209–216
Ferraro SA, Yakisich JS, Gallo FT, Tasat DR (2011) Simvastatin pretreatment prevents ambient particle-induced lung injury in mice. Inhal Toxicol 23(14):889–896
Ferraro SA, Curutchet G, Tasat DR (2012) Bioaccessible heavy metals-sediment particles from Reconquista River induce lung inflammation in mice. Environ Toxicol Chem 31(9):2059–2068
Forastiere F, Stafoggia M, Picciotto S, Bellander T, D’Ippoliti D, Lanki T et al (2005) A case-crossover analysis of out-of-hospital coronary deaths and air pollution in Rome, Italy. Am J Respir Crit Care Med 172(12):1549–1555
Ghio AJ, Devlin RB (2001) Inflammatory lung injury after bronchial instillation of air pollution particles. Am J Respir Crit Care Med 164(4):704–708
Ghio AJ, Suliman HB, Carter JD, Abushamaa AM, Folz RJ (2002) Overexpression of extracellular superoxide dismutase decreases lung injury after exposure to oil fly ash. Am J Physiol Lung Cell Mol Physiol 283(1):L211–L218
GoogleMaps La Carcova, Buenos Aires Argentina. Images ©2012 Cnes/Spot Image, DigitalGlobe, TerraMetrics, data from map ©2012 Google, Inav/Geosystems SRL. Undetermined scale, “Google Maps.” https://maps.google.com.ar/?ll=-34.522788,-58.581719&spn=0.020048,0.042272&t=k&z=15. Accessed 2 Dec 2013
Gurgueira SA, Lawrence J, Coull B, Murthy GG, Gonzalez-Flecha B (2002) Rapid increases in the steady-state concentration of reactive oxygen species in the lungs and heart after particulate air pollution inhalation. Environ Health Perspect 110(8):749–755
Henderson RF (2005) Use of bronchoalveolar lavage to detect respiratory tract toxicity of inhaled material. Exp Toxicol Pathol 57(Suppl 1):155–159
Krewski D, Snyder R, Beatty P, Granville G, Meek B, Sonawane B (2000) Assessing the health risks of benzene: a report on the benzene state-of-the-science workshop. J Toxicol Environ Health A 61(5–6):307–338
Leong BK, Coombs JK, Sabaitis CP, Rop DA, Aaron CS (1998) Quantitative morphometric analysis of pulmonary deposition of aerosol particles inhaled via intratracheal nebulization, intratracheal instillation or nose-only inhalation in rats. J Appl Toxicol 18(2):149–160
Li N, Venkatesan MI, Miguel A, Kaplan R, Gujuluva C, Alam J et al (2000) Induction of heme oxygenase-1 expression in macrophages by diesel exhaust particle chemicals and quinones via the antioxidant-responsive element. J Immunol 165(6):3393–3401
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275
Maehly AC, Chance B (1954) The assay of catalases and peroxidases. Methods Biochem Anal 1:357–424
Magnani ND, Marchini T, Tasat DR, Alvarez S, Evelson PA (2011) Lung oxidative metabolism after exposure to ambient particles. Biochem Biophys Res Commun 412(4):667–672
Mantecca P, Farina F, Moschini E, Gallinotti D, Gualtieri M, Rohr A et al (2010) Comparative acute lung inflammation induced by atmospheric PM and size-fractionated tire particles. Toxicol Lett 198(2):244–254
Marchini T, Magnani N, D’Annunzio V, Tasat D, Gelpi RJ, Alvarez S et al (2013) Impaired cardiac mitochondrial function and contractile reserve following an acute exposure to environmental particulate matter. Biochim Biophys Acta 1830(3):2545–2552
Miller MR, Shaw CA, Langrish JP (2012) From particles to patients: Oxidative stress and the cardiovascular effects of air pollution. Future Cardiol 8(4):577–602
Misra HP, Fridovich I (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
Molinari BL, Tasat DR, Fernandez ML, Duran HA, Curiale J, Stoliar A et al (2000) Automated image analysis for monitoring oxidative burst in macrophages. Anal Quant Cytol Histol 22(5):423–427
Nel AE, Diaz-Sanchez D, Li N (2001) The role of particulate pollutants in pulmonary inflammation and asthma: Evidence for the involvement of organic chemicals and oxidative stress. Curr Opin Pulm Med 7(1):20–26
Nurkiewicz TR, Porter DW, Barger M, Millecchia L, Rao KM, Marvar PJ et al (2006) Systemic microvascular dysfunction and inflammation after pulmonary particulate matter exposure. Environ Health Perspect 114(3):412–419
Oberdorster G (2001) Pulmonary effects of inhaled ultrafine particles. Int Arch Occup Environ Health 74(1):1–8
Osornio-Vargas AR, Bonner JC, Alfaro-Moreno E, Martinez L, Garcia-Cuellar C, Ponce-de-Leon Rosales S et al (2003) Proinflammatory and cytotoxic effects of Mexico City air pollution particulate matter in vitro are dependent on particle size and composition. Environ Health Perspect 111(10):1289–1293
Perrone MG, Gualtieri M, Consonni V, Ferrero L, Sangiorgi G, Longhin E et al (2013) Particle size, chemical composition, seasons of the year and urban, rural or remote site origins as determinants of biological effects of particulate matter on pulmonary cells. Environ Pollut 176:215–227
Pope CA 3rd, Burnett RT, Krewski D, Jerrett M, Shi Y, Calle EE et al (2009) Cardiovascular mortality and exposure to airborne fine particulate matter and cigarette smoke: shape of the exposure–response relationship. Circulation 120(11):941–948
Ristovski ZD, Miljevic B, Surawski NC, Morawska L, Fong KM, Goh F et al (2012) Respiratory health effects of diesel particulate matter. Respirology 17(2):201–212
Rosas Perez I, Serrano J, Alfaro-Moreno E, Baumgardner D, Garcia-Cuellar C, Martin Del Campo JM et al (2007) Relations between PM10 composition and cell toxicity: A multivariate and graphical approach. Chemosphere 67(6):1218–1228
Saldiva PH (1998) Air pollution in urban areas: the role of automotive emissions as a public health problem. Int J Tuberc Lung Dis 2(11):868
Schins RP (2002) Mechanisms of genotoxicity of particles and fibers. Inhal Toxicol 14(1):57–78
Segal AW (1974) Nitroblue-tetrazolium tests. Lancet 2(7891):1248–1252
Singhal PC, Sharma P, Kapasi AA, Reddy K, Franki N, Gibbons N (1998) Morphine enhances macrophage apoptosis. J Immunol 160(4):1886–1893
Southam DS, Dolovich M, O’Byrne PM, Inman MD (2002) Distribution of intranasal instillations in mice: Effects of volume, time, body position, and anesthesia. Am J Physiol Lung Cell Mol Physiol 282(4):L833–L839
Tao F, Gonzalez-Flecha B, Kobzik L (2003) Reactive oxygen species in pulmonary inflammation by ambient particulates. Free Radic Biol Med 35(4):327–340
Tasat DR, de Rey BM (1987) Cytotoxic effect of uranium dioxide on rat alveolar macrophages. Environ Res 44(1):71–81
Torricelli AA, Novaes P, Matsuda M, Alves MR, Monteiro ML (2011) Ocular surface adverse effects of ambient levels of air pollution. Arq Bras Oftalmol 74(5):377–381
Acknowledgments
We especially thank Gisela Maxia for technical assistance with SEM and EDX and Paulo H. Saldiva for kindly providing the collector sampler. This study was supported by the Agencia de Promoción Científica y Técnica from Argentina (Grant No. PICT-2010-1660).
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Astort, F., Sittner, M., Ferraro, S.A. et al. Pulmonary Inflammation and Cell Death in Mice After Acute Exposure to Air Particulate Matter From an Industrial Region of Buenos Aires. Arch Environ Contam Toxicol 67, 87–96 (2014). https://doi.org/10.1007/s00244-013-9975-4
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DOI: https://doi.org/10.1007/s00244-013-9975-4