Genotoxic Activity of Particulate Matter and In Vivo Tests in Children Exposed to Air Pollution
Abstract
:1. Introduction
2. Materials and Methods
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Elassouli, S.M.; Alqahtani, M.H.; Milaat, W. Genotoxicity of air borne particulates assessed by comet and the Salmonella mutagenicity test in Jeddah, Saudi Arabia. Int. J. Environ. Res. Public Health. 2007, 4, 216–233. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ceretti, E.; Zani, C.; Zerbini, I.; Viola, G.; Moretti, M.; Villarini, M.; Dominici, L.; Monarca, S.; Feretti, D. Monitoring of volatile and non-volatile urban air genotoxins using bacteria, human cells and plants. Chemosphere 2015, 120, 221–229. [Google Scholar] [CrossRef]
- Billet, S.; Landkocz, Y.; Martin, P.J.; Verdin, A.; Ledoux, F.; Lepers, C.; André, V.; Cazier, F.; Sichel, F.; Shirali, P.; et al. Chemical characterization of fine and ultrafine PM, direct and indirect genotoxicity of PM and their organic extracts on pulmonary cells. J. Environ. Sci. 2018, 71, 168–178. [Google Scholar] [CrossRef] [PubMed]
- Bonetta, S.; Bonetta, S.; Schilirò, T.; Ceretti, E.; Feretti, D.; Covolo, L.; Vannini, S.; Villarini, M.; Moretti, M.; Verani, M.; et al. Mutagenic and genotoxic effects induced by PM0.5 of different Italian towns in human cells and bacteria: The MAPEC_LIFE study. Environ. Pollut. 2019, 245, 1124–1135. [Google Scholar] [CrossRef]
- Platel, A.; Privat, K.; Talahari, S.; Delobel, A.; Dourdin, G.; Gateau, E.; Simar, S.; Saleh, Y.; Sotty, J.; Antherieu, S.; et al. Study of in vitro and in vivo genotoxic effects of air pollution fine (PM2.5-0.18) and quasi-ultrafine (PM0.18) particles on lung models. Sci. Total Environ. 2020, 711, 134666. [Google Scholar] [CrossRef] [PubMed]
- Santovito, A.; Gendusa, C.; Cervella, P.; Traversi, D. In vitro genomic damage induced by urban fine particulate matter on human lymphocytes. Sci. Rep. 2020, 10, 8853. [Google Scholar] [CrossRef] [PubMed]
- Schilirò, T.; Bonetta, S.; Alessandria, L.; Gianotti, V.; Carraro, E.; Gilli, G. PM10 in a background urban site: Chemical characteristics and biological effects. Environ. Toxicol. Pharmacol. 2015, 39, 833–844. [Google Scholar] [CrossRef]
- International Agency for Research on Cancer (IARC). Monograph on the Evaluation of Carcinogenic Risks to Humans; International Agency for Research on Cancer (IARC): Lyon, France, 2016; Volume 109. Available online: https://publications.iarc.fr/Book-And-Report-Series/Iarc-Monographs-On-The-Identification-Of-Carcinogenic-Hazards-To-Humans/Outdoor-Air-Pollution-2015 (accessed on 17 May 2021).
- Environmental European Agency (EEA). Air Quality in Europe–2019; Report No. 10/2019; Environmental European Agency (EEA): Copenhagen, Denmark, 2019. [Google Scholar]
- Environmental European Agency (EEA). Air Quality in Europe–2020; Report No. 09/2020; Environmental European Agency (EEA): Copenhagen, Denmark, 2020. [Google Scholar]
- Claxton, L.D.; de A. Umbuzeiro, G.; DeMarini, D.M. The Salmonella mutagenicity assay: The stethoscope of genetic toxicology for the 21st century. Environ. Health Perspect. 2010, 118, 1515–1522. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Claxton, L.D.; Matthews, P.P.; Warren, S.H. The genotoxicity of ambient outdoor air, a review: Salmonella mutagenicity. Mutat. Res. 2004, 567, 347–399. [Google Scholar] [CrossRef] [PubMed]
- Claxton, L.D.; Woodall, G.M., Jr. A review of the mutagenicity and rodent carcinogenicity of ambient air. Mutat. Res. 2007, 636, 36–94. [Google Scholar] [CrossRef]
- Coronas, M.V.; Pereira, T.S.; Rocha, J.A.; Lemos, A.T.; Fachel, J.M.; Salvadori, D.M.; Vargas, V.M. Genetic biomonitoring of an urban population exposed to mutagenic airborne pollutants. Environ. Int. 2009, 35, 1023–1029. [Google Scholar] [CrossRef]
- Silva da Silva, C.; Rossato, J.M.; Vaz Rocha, J.A.; Vargas, V.M. Characterization of an area of reference for inhalable particulate matter (PM2.5) associated with genetic biomonitoring in children. Mutat. Res. 2015, 778, 44–55. [Google Scholar] [CrossRef]
- Feretti, D.; Pedrazzani, R.; Ceretti, E.; Dal Grande, M.; Zerbini, I.; Viola, G.C.V.; Gelatti, U.; Donato, F.; Zani, C. “Risk is in the air”: Polycyclic aromatic hydrocarbons, metals and mutagenicity of atmospheric particulate matter in a town of Northern Italy (Respira study). Mutat. Res. 2019, 842, 35–49. [Google Scholar] [CrossRef]
- Hoffmann, H.; Speit, G. Assessment of DNA damage in peripheral blood of heavy smokers with the comet assay and the micronucleus test. Mutat. Res. 2005, 581, 105–114. [Google Scholar] [CrossRef] [PubMed]
- Møller, P. The alkaline comet assay: Towards validation in biomonitoring of DNA damaging exposures. Basic Clin. Pharmacol. Toxicol. 2006, 98, 336–345. [Google Scholar] [CrossRef]
- Villarini, M.; Levorato, S.; Salvatori, T.; Ceretti, E.; Bonetta, S.; Carducci, A.; Grassi, T.; Vannini, S.; Donato, F.; Bonetta, S.; et al. Buccal micronucleus cytome assay in primary school children: A descriptive analysis of the MAPEC_LIFE multicenter cohort study. Int. J. Hyg. Environ. Health. 2018, 221, 883–892. [Google Scholar] [CrossRef] [PubMed]
- Szeto, Y.T.; Benzie, I.F.; Collins, A.R.; Choi, S.W.; Cheng, C.Y.; Yow, C.M.; Tse, M.M. A buccal cell model comet assay: Development and evaluation for human biomonitoring and nutritional studies. Mutat. Res. 2005, 578, 371–381. [Google Scholar] [CrossRef] [PubMed]
- Lemos, A.T.; Coronas, M.V.; Rocha, J.A.; Vargas, V.M. Mutagenicity of particulate matter fractions in areas under the impact of urban and industrial activities. Chemosphere 2012, 89, 1126–1134. [Google Scholar] [CrossRef]
- de Brito, K.C.; de Lemos, C.T.; Rocha, J.A.; Mielli, A.C.; Matzenbacher, C.; Vargas, V.M. Comparative genotoxicity of airborne particulate matter (PM2.5) using Salmonella, plants and mammalian cells. Ecotoxicol. Environ. Saf. 2013, 94, 14–20. [Google Scholar] [CrossRef]
- Ceretti, E.; Feretti, D.; Viola, G.C.; Zerbini, I.; Limina, R.M.; Zani, C.; Capelli, M.; Lamera, R.; Donato, F.; Gelatti, U. DNA damage in buccal mucosa cells of pre-school children exposed to high levels of urban air pollutants. PLoS ONE 2014, 9, e96524. [Google Scholar] [CrossRef] [Green Version]
- Dumax-Vorzet, A.F.; Tate, M.; Walmsley, R.; Elder, R.H.; Povey, A.C. Cytotoxicity and genotoxicity of urban particulate matter in mammalian cells. Mutagenesis 2015, 30, 621–633. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- de Oliveira Alves, N.; Pereira, G.M.; Di Domenico, M.; Costanzo, G.; Benevenuto, S.; de Oliveira Fonoff, A.M.; Costa, N.D.; Júnior, G.R.; Kajitani, G.S.; Moreno, N.C.; et al. Inflammation response, oxidative stress and DNA damage caused by urban air pollution exposure increase in the lack of DNA repair XPC protein. Environ. Int. 2020, 145, 106150. [Google Scholar] [CrossRef]
- Zani, C.; Ceretti, E.; Zerbini, I.; Viola, G.C.V.; Donato, F.; Gelatti, U.; Feretti, D. Comet Test in Saliva Leukocytes of Pre-School Children Exposed to Air Pollution in North Italy: The Respira Study. Int. J. Environ. Res. Public Health 2020, 17, 3276. [Google Scholar] [CrossRef] [PubMed]
- Rogula-Kozłowska, W.; Kozielska, B.; Majewski, G.; Rogula-Kopiec, P.; Mucha, W.; Kociszewska, K. Submicron particle-bound polycyclic aromatic hydrocarbons in the polish teaching rooms: Concentrations, origin and health hazard. J. Environ. Sci. 2018, 64, 235–244. [Google Scholar] [CrossRef] [PubMed]
- Nisbet, I.C.T.; LaGoy, P.K. Toxic equivalency factors (TEFs) for polycyclic aromatic hydrocarbons (PAHs). Regul. Toxicol. Pharmacol. 1992, 16, 290–300. [Google Scholar] [CrossRef]
- Greim, H. Gesundheitsschädliche Arbeitsstoffe, Toxikologisch-Arbeitsmedizinische Begründungen von MAK-Werten und Einstufungen; Wiley-VCH, Verlag GmbH & Co. KGaA: Weinheim, Germany, 2008. [Google Scholar]
- Willett, K.L.; Gardinali, P.R.; Sericano, J.L.; Wade, T.L.; Safe, S.H. Characterization of the H4IIE rat hepatoma cell bioassay for evaluation of environmental samples containing polynuclear aromatic hydrocarbons (PAHs). Arch. Environ. Contam. Toxicol. 1997, 32, 442–448. [Google Scholar] [CrossRef]
- MDH. Guidance for Evaluating the Cancer Potency of Polycyclic Aromatic Hydrocarbon (PAH) Mixtures in Environmental Samples; Minnesota Department of Health: St. Paul, MN, USA, 2016.
- Monarca, S.; Feretti, D.; Zanardini, A.; Falistocco, E.; Nardi, G. Monitoring of mutagens in urban air samples. Mutat. Res. 1999, 426, 189–192. [Google Scholar] [CrossRef]
- Buschini, A.; Cassoni, F.; Anceschi, E.; Pasini, L.; Poli, P.; Rossi, C. Urban airborne particulate: Genotoxicity evaluation of different size fractions by mutagenesis tests on microorganisms and comet assay. Chemosphere 2001, 44, 1723–1736. [Google Scholar] [CrossRef]
- Marangon, D.; Traversi, D.; D’Agostino, A.M.; Gea, M.; Fontana, M.; Schilirò, T. The North-western Italy air quality monitoring network: Improving experience of PM2.5 assessment with mutagenicity assay. Environ. Res. 2021, 195, 110699. [Google Scholar] [CrossRef]
- Valle-Hernández, B.L.; Mugica-Alvarez, V.; Salinas-Talavera, E.; Amador-Muñoz, O.; Murillo-Tovar, M.A.; Villalobos-Pietrini, R.; De Vizcaya-Ruíz, A. Temporal variation of nitro-polycyclic aromatic hydrocarbons in PM10 and PM2.5 collected in Northern Mexico City. Sci. Total Environ. 2010, 408, 5429–5438. [Google Scholar] [CrossRef]
- Slezakova, K.; Castro, D.; Pereira, M.C.; Moralis, S.; Delerue-Matos, C.; Alvim-Ferraz, M.C. Influence of traffic emissions on the carcinogenic polycyclic aromatic hydrocarbons in outdoor breathable particles. J. Air Waste Manag. Assoc. 2010, 60, 393–401. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Oliveira, M.; Slezakova, K.; Delerue-Matos, C.; Pereira, M.C.; Morais, S. Children environmental exposure to particulate matter and polycyclic aromatic hydrocarbons and biomonitoring in school environments: A review on indoor and outdoor exposure levels, major sources and health impacts. Environ. Int. 2019, 124, 180–204. [Google Scholar] [CrossRef]
- Li, J.; Li, W.X.; Bai, C.; Song, Y. Particulate matter-induced epigenetic changes and lung cancer. Clin. Respir. J. 2017, 11, 539–546. [Google Scholar] [CrossRef]
- Choi, H.; Song, W.M.; Wang, M.; Sram, R.J.; Zhang, B. Benzo[a]pyrene is associated with dysregulated myelo-lymphoid hematopoiesis in asthmatic children. Environ. Int. 2019, 128, 218–232. [Google Scholar] [CrossRef]
- Annangi, B.; Bonassi, S.; Marcos, R.; Hernández, A. Biomonitoring of humans exposed to arsenic, chromium, nickel, vanadium, and complex mixtures of metals by using the micronucleus test in lymphocytes. Mutat. Res. 2016, 770 PtA, 140–161. [Google Scholar] [CrossRef]
- Nersesyan, A.; Kundi, M.; Waldherr, M.; Setayesh, T.; Mišík, M.; Wultsch, G.; Filipic, M.; Mazzaron Barcelos, G.R.; Knasmueller, S. Results of micronucleus assays with individuals who are occupationally and environmentally exposed to mercury, lead and cadmium. Mutat. Res. 2016, 770 PtA, 119–139. [Google Scholar] [CrossRef]
- Briffa, J.; Sinagra, E.; Blundell, R. Heavy metal pollution in the environment and their toxicological effects on humans. Heliyon 2020, 6, e04691. [Google Scholar] [CrossRef]
- Valko, M.; Morris, H.; Cronin, M.T. Metals, toxicity and oxidative stress. Curr. Med. Chem. 2005, 12, 1161–1208. [Google Scholar] [CrossRef] [Green Version]
- Eastmond, D.A.; Hartwig, A.; Anderson, D.; Anwar, W.A.; Cimino, M.C.; Dobrev, I.; Douglas, G.R.; Nohmi, T.; Phillips, D.H.; Vickers, C. Mutagenicity testing for chemical risk assessment: Update of the WHO/IPCS Harmonized Scheme. Mutagenesis 2009, 24, 341–349. [Google Scholar] [CrossRef] [Green Version]
- Zhi, M.; Zhang, X.; Zhang, K.; Ussher, S.J.; Lv, W.; Li, J.; Gao, J.; Luo, Y.; Meng, F. The characteristics of atmospheric particles and metal elements during winter in Beijing: Size distribution, source analysis, and environmental risk assessment. Ecotoxicol. Environ. Saf. 2021, 211, 111937. [Google Scholar] [CrossRef]
- Bonassi, S.; Milić, M.; Neri, M. Frequency of micronuclei and other biomarkers of DNA damage in populations exposed to dusts, asbestos and other fibers. A systematic review. Mutat. Res. 2016, 770 PtA, 106–118. [Google Scholar] [CrossRef]
- Coronas, M.V.; Rocha, J.A.; Salvadori, D.M.; Vargas, V.M. Evaluation of area contaminated by wood treatment activities: Genetic markers in the environment and in the child population. Chemosphere 2016, 144, 1207–1215. [Google Scholar] [CrossRef]
Sites | PM Fractions (µm) | Comet Test on Leukocytes Visual Score |
---|---|---|
1 | <0.5 | 1.8 |
0.5–3 | 1.6 | |
3–10 | 0.1 | |
2 | <0.5 | 2.4 |
0.5–3 | 1.1 | |
3–10 | 1.3 | |
3 | <0.5 | 2.7 |
0.5–3 | 1.7 | |
3–10 | 1.7 | |
4 | <0.5 | 3.4 |
0.5–3 | 2.2 | |
3–10 | 1.8 | |
5 | <0.5 | 3.2 |
0.5–3 | 1.0 | |
3–10 | 0.1 | |
6 | <0.5 | 3.1 |
0.5–3 | 1.1 | |
3–10 | 0.1 |
Sites | PM Fractions (µm) | Carcinogenic PAHs (ng) |
---|---|---|
1 | <0.5 | 3.9 |
0.5–3 | 3.9 | |
3–10 | 2.3 | |
2 | <0.5 | 2.9 |
0.5–3 | 0.1 | |
3–10 | 3.6 | |
3 | <0.5 | 3.3 |
0.5–3 | 0.1 | |
3–10 | 3.6 | |
4 | <0.5 | 4.5 |
0.5–3 | 0.1 | |
3–10 | 1.9 | |
5 | <0.5 | 4.8 |
0.5–3 | 0.1 | |
3–10 | 1.9 | |
6 | <0.5 | 2.6 |
0.5–3 | 0.0 | |
3–10 | 0.3 | |
Mean ± SD | <0.5 | 3.6 ± 0.8 |
0.5–3 | 0.7 ± 1.5 | |
3–10 | 2.2 ± 1.2 |
PM Fractions (µm) | Metals (ppb) | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Fe | As | Al | V | Cr | Mn | Ni | Zn | Cd | Hg | Pb | ||
Mean ± SD | <0.5 | 909.7 ± 1536.9 | 1.2 ± 0.5 | 2270.3 ± 1302.6 | 1.8 ± 1.5 | 161.9 ± 371.5 | 35.2 ± 31.4 | 75.6 ± 171.3 | 500.4 ± 302.2 | 0.4 ± 0.2 | 0.7 ± 0.6 | 20.8 ± 8.4 |
0.5–3 | 1078.2 ± 259.6 | 0.4 ± 0.1 | 5223.4 ± 2580.5 | 1.2 ± 0.3 | 18.4 ± 2.2 | 40.1 ± 9.2 | 5.9 ± 1.6 | 17,839.6 ± 14,895.4 | 4.6 ± 3.7 | 0.3 ± 0.07 | 36.7 ± 21.4 | |
3–10 | 1256.7 ± 358.1 | 1.2 ± 0.2 | 7480.9 ± 3706.5 | 1.5 ± 0.3 | 22.0 ± 2.4 | 63.0 ± 13.6 | 9.1 ± 0.6 | 27,150.6 ± 22,141.8 | 7.2 ± 5.4 | 0.3 ± 0.08 | 69.8 ± 32.7 |
Sites | PM Fractions (µm) | BaP-PEQ ng/m3 | CEQ ng/m3 | MEQ ng/m3 | TCDD-TEQ µg/m3 | TEQ ng/m3 |
---|---|---|---|---|---|---|
1 | <0.5 | 2.985097 | 0.49464 | 1.936413 | 4.20021 | 1.258376 |
0.5–3 | 0.223235 | 0.012657 | 0.156956 | 0.13165 | 0.168213 | |
3–10 | 1.207709 | 0.18187 | 0.672044 | 2.33371 | 0.535057 | |
2 | <0.5 | 2.505132 | 0.409552 | 1.624128 | 3.6108 | 1.013315 |
0.5–3 | 0.232974 | 0.012972 | 0.158597 | 0.13692 | 0.171557 | |
3–10 | 1.781841 | 0.277915 | 0.948737 | 3.9429 | 0.692266 | |
3 | <0.5 | 2.860301 | 0.46415 | 1.898558 | 3.93091 | 1.181743 |
0.5–3 | 0.232694 | 0.015112 | 0.165548 | 0.13395 | 0.176227 | |
3–10 | 1.518079 | 0.223874 | 0.965435 | 3.20357 | 0.722432 | |
4 | <0.5 | 2.402421 | 0.453998 | 1.477876 | 5.49091 | 1.057894 |
0.5–3 | 0.202135 | 0.01118 | 0.143572 | 0.08954 | 0.158247 | |
3–10 | 1.006692 | 0.135052 | 0.5868 | 2.11792 | 0.455188 | |
5 | <0.5 | 2.769771 | 0.60323 | 1.690773 | 5.62284 | 1.233482 |
0.5–3 | 0.21174 | 0.011946 | 0.152389 | 0.10247 | 0.165811 | |
3–10 | 1.142164 | 0.214775 | 0.595705 | 2.15638 | 0.47243 | |
6 | <0.5 | 1.602095 | 0.344192 | 0.960746 | 3.27267 | 0.704601 |
0.5–3 | 0.179467 | 0.007851 | 0.136448 | 0.03739 | 0.153379 | |
3–10 | 0.401406 | 0.046982 | 0.242765 | 0.57702 | 0.222601 |
PM Fractions (µm) | Coefficient ± SE | p |
---|---|---|
<0.5 | ||
Total PAHs (ng) | 0.038 ± 0.008 | <0.001 |
Carcinogenic PAHs (ng) | 0.054 ± 0.013 | <0.001 |
BaP (ng) | 0.274 ± 0.082 | 0.001 |
BaP-PEQ (ng/m3) | 0.06 ± 0.02 | 0.01 |
CEQ (ng/m3) | 0.46 ± 0.12 | <0.001 |
MEQ (ng/m3) | ns | |
TCDD-TEQ (µg/m3) | 0.045 ± 0.012 | 0.001 |
TEQ (ng/m3) | 0.17 ± 0.05 | 0.002 |
0.5–3 | ||
Total PAHs (ng) | 0.016 ± 0.004 | 0.001 |
Carcinogenic PAHs (ng) | 0.026 ± 0.007 | 0.001 |
BaP (ng) | 0.19 ± 0.05 | 0.001 |
BaP-PEQ (ng/m3) | ns | |
CEQ (ng/m3) | ns | |
MEQ (ng/m3) | ns | |
TCDD-TEQ (µg/m3) | ns | |
TEQ (ng/m3) | ns |
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Zani, C.; Donato, F.; Ceretti, E.; Pedrazzani, R.; Zerbini, I.; Gelatti, U.; Feretti, D. Genotoxic Activity of Particulate Matter and In Vivo Tests in Children Exposed to Air Pollution. Int. J. Environ. Res. Public Health 2021, 18, 5345. https://doi.org/10.3390/ijerph18105345
Zani C, Donato F, Ceretti E, Pedrazzani R, Zerbini I, Gelatti U, Feretti D. Genotoxic Activity of Particulate Matter and In Vivo Tests in Children Exposed to Air Pollution. International Journal of Environmental Research and Public Health. 2021; 18(10):5345. https://doi.org/10.3390/ijerph18105345
Chicago/Turabian StyleZani, Claudia, Francesco Donato, Elisabetta Ceretti, Roberta Pedrazzani, Ilaria Zerbini, Umberto Gelatti, and Donatella Feretti. 2021. "Genotoxic Activity of Particulate Matter and In Vivo Tests in Children Exposed to Air Pollution" International Journal of Environmental Research and Public Health 18, no. 10: 5345. https://doi.org/10.3390/ijerph18105345