Abstract
In the last two decades, awareness grew on the matter of the impact of environment on human health. Contaminants sorbed onto soil and settled dust can be ingested and thus represent a hazard, particularly to young children, who play on the ground and bring their hands and objects to their mouth. Metal(loid)s and polycyclic aromatic hydrocarbons (PAHs) are of concern as they are both carcinogenic to humans and ubiquitous in outdoor environments. The present study aims to assess the total and bioaccessible fractions of PAHs and metal(loid)s present in settled dust of four preschools located in industrial, urban, and suburban areas. On the one hand, children’s incremental life cancer risks (ILCR) were calculated according to ingestion pathway. On the other hand, the genotoxicities of the bioaccessible dust-bonded contaminants were determined on gastric cells. PAH concentrations ranged from 50.9 to 2267.3 ng/g, and the bioaccessible fraction represented 10.7% of the total in average. Metal(loid) concentration ranged from 12,430 to 38,941 µg/g, and the mean bioaccessibility was of 40.1%. Cancer risk ranged from 2.8.105 to 8.6.105, indicating that there is a potential cancer risk for children linked to the ingestion of settled dust. The inorganic bioaccessible fraction induced little DNA (< 20%TailDNA) and chromosomal damages (30% increase in micronuclei), whereas the organic bioaccessible fraction induced higher DNA (17–63%TailDNA) and chromosomal damages (88% increase in micronuclei). Such experimental approach needs to be deepen, as a tool complementary to cancer risk calculation, since the latter only lays on a set of targeted contaminants with known toxicity values.
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References
Alloway BJ (ed) (2013) Heavy metals in soils: trace metals and metalloids in soils and their bioavailability. Springer, Netherlands, Dordrecht
Armada D, Martinez-Fernandez A, Celeiro M et al (2023) Assessment of the bioaccessibility of PAHs and other hazardous compounds present in recycled tire rubber employed in synthetic football fields. Sci Total Environ 857:159485. https://doi.org/10.1016/j.scitotenv.2022.159485
ATSDR (1995) Toxicological profile for polycyclic aromatic hydrocarbons (PAHs). Department of Health and Human Services, Public Health Service, Atlanta, GA USA, U.S
Beriro DJ, Cave MR, Wragg J et al (2016) A review of the current state of the art of physiologically-based tests for measuring human dermal in vitro bioavailability of polycyclic aromatic hydrocarbons (PAH) in soil. J Hazard Mater 305:240–259. https://doi.org/10.1016/j.jhazmat.2015.11.010
Bonnefoy A, Plumejeaud S, Noack Y et al (2017) Fine atmospheric particles emitted by industrial, traffic and urban sources in France: characterization and genotoxicity. Toxicol Environ Chem 99:340–361. https://doi.org/10.1080/02772248.2016.1176169
Budak M, Gunal H, Celik İ et al (2018) Soil quality assessment of upper Tigris basin. Carpathian J Earth Environ Sci 13:301–316. https://doi.org/10.26471/cjees/2018/013/026
Castel R, Tassistro V, Claeys-Bruno M et al (2023b) In vitro genotoxicity evaluation of pahs in mixtures using experimental design. Toxics 11:470. https://doi.org/10.3390/toxics11050470
Castel R, Bertoldo R, Lebarillier S, et al (2023a) Toward an interdisciplinary approach to assess the adverse health effects of dust-containing polycyclic aromatic hydrocarbons (PAHs) and metal(loid)s on preschool children. Environ Pollut 122372. https://doi.org/10.1016/j.envpol.2023.122372
Cave MR, Wragg J, Harrison I et al (2010) Comparison of batch mode and dynamic physiologically based bioaccessibility tests for PAHs in soil samples. Environ Sci Technol 44:2654–2660. https://doi.org/10.1021/es903258v
Cave MR, Vane CH, Kim A et al (2015) Measurement and modelling of the ingestion bioaccessibility of polyaromatic hydrocarbons in soils. Environ Technol Innov 3:35–45. https://doi.org/10.1016/j.eti.2014.11.001
Chen X, He T, Yang X et al (2023) Analysis, environmental occurrence, fate and potential toxicity of tire wear compounds 6PPD and 6PPD-quinone. J Hazard Mater 452:131245. https://doi.org/10.1016/j.jhazmat.2023.131245
Collins CD, Craggs M, Garcia-Alcega S et al (2015) Towards a unified approach for the determination of the bioaccessibility of organic pollutants. Environ Int 78:24–31. https://doi.org/10.1016/j.envint.2015.02.005
DeMarini DM. The role of genotoxicity in carcinogenesis. In: Baan RA, Stewart BW, Straif K, editors. Tumour site concordance and mechanisms of carcinogenesis. Lyon (FR): International Agency for Research on Cancer; 2019. (IARC Scientific Publications, No. 165.) Chapter 12. Available from: https://www.ncbi.nlm.nih.gov/books/NBK570347/
Denys S, Caboche J, Tack K et al (2012) In vivo validation of the unified BARGE method to assess the bioaccessibility of arsenic, antimony, cadmium, and lead in soils. Environ Sci Technol 46:6252–6260. https://doi.org/10.1021/es3006942
Dergham M, Lepers C, Verdin A et al (2015) Temporal–spatial variations of the physicochemical characteristics of air pollution particulate matter (PM2.5–0.3) and toxicological effects in human bronchial epithelial cells (BEAS-2B). Environ Res 137:256–267. https://doi.org/10.1016/j.envres.2014.12.015
Du B, Liang B, Li Y et al (2022) First report on the occurrence of N-(1,3-dimethylbutyl)-N′-phenyl-p-phenylenediamine (6PPD) and 6PPD-quinone as pervasive pollutants in human urine from South China. Environ Sci Technol Lett 9:1056–1062. https://doi.org/10.1021/acs.estlett.2c00821
Duan L, Palanisami T, Liu Y et al (2014) Effects of ageing and soil properties on the oral bioavailability of benzo[a]pyrene using a swine model. Environ Int 70:192–202. https://doi.org/10.1016/j.envint.2014.05.017
EFSA (2012) Scientific opinion on emerging and novel brominated flame retardants (BFRs) in food. EFSA J 10. https://doi.org/10.2903/j.efsa.2012.2908
Fang L, Fang C, Di S et al (2023) Oral exposure to tire rubber-derived contaminant 6PPD and 6PPD-quinone induce hepatotoxicity in mice. Sci Total Environ 869:161836. https://doi.org/10.1016/j.scitotenv.2023.161836
Fenech M (2000) The in vitro micronucleus technique. Mutat Res Mol Mech Mutagen 455:81–95. https://doi.org/10.1016/S0027-5107(00)00065-8
Franco CFJ, de Resende MF, de Almeida FL et al (2017) Polycyclic aromatic hydrocarbons (PAHs) in street dust of Rio de Janeiro and Niterói, Brazil: particle size distribution, sources and cancer risk assessment. Sci Total Environ 599–600:305–313. https://doi.org/10.1016/j.scitotenv.2017.04.060
French National Agency of Food, Environment & Work Safety (ANSES) (2019) Exposure to settled dust in indoors environment. ANSES, Maisons-Alfort
Gabarrón M, Faz A, Acosta JA (2017) Soil or dust for health risk assessment studies in urban environment. Arch Environ Contam Toxicol 73:442–455. https://doi.org/10.1007/s00244-017-0413-x
Galażyn-Sidorczuk M, Brzóska MM, Moniuszko-Jakoniuk J (2008) Estimation of Polish cigarettes contamination with cadmium and lead, and exposure to these metals via smoking. Environ Monit Assess 137:481–493. https://doi.org/10.1007/s10661-007-9783-2
Ghanavati N, Nazarpour A, Watts MJ (2019) Status, source, ecological and health risk assessment of toxic metals and polycyclic aromatic hydrocarbons (PAHs) in street dust of Abadan. Iran CATENA 177:246–259. https://doi.org/10.1016/j.catena.2019.02.022
Glorennec P, Lucas J-P, Mandin C, Le Bot B (2012) French children’s exposure to metals via ingestion of indoor dust, outdoor playground dust and soil: contamination data. Environ Int 45:129–134. https://doi.org/10.1016/j.envint.2012.04.010
Hassanien MA, Abdel-Latif NM (2008) Polycyclic aromatic hydrocarbons in road dust over Greater Cairo. Egypt J Hazard Mater 151:247–254. https://doi.org/10.1016/j.jhazmat.2007.05.079
IARC (2022) IARC Monographs on the identification of carcinogenic hazards to Humans. https://monographs.iarc.who.int/list-of-classifications
James K, Peters RE, Laird BD et al (2011) Human exposure assessment: a case study of 8 PAH contaminated soils using in vitro digestors and the juvenile swine model. Environ Sci Technol 45:4586–4593. https://doi.org/10.1021/es1039979
Juhasz AL, Weber J, Stevenson G et al (2014) In vivo measurement, in vitro estimation and fugacity prediction of PAH bioavailability in post-remediated creosote-contaminated soil. Sci Total Environ 473–474:147–154. https://doi.org/10.1016/j.scitotenv.2013.12.031
Kang Y, Cheung KC, Wong MH (2011) Mutagenicity, genotoxicity and carcinogenic risk assessment of indoor dust from three major cities around the Pearl River Delta. Environ Int 37:637–643. https://doi.org/10.1016/j.envint.2011.01.001
Kang Y, Zeng D, Man YB et al (2018) Comparison of sorption kinetics of PAHs by sorptive sinks and caco-2 cell and the correlation between bioaccessibility and bioavailability of PAHs in indoor dust. Sci Total Environ 645:170–178. https://doi.org/10.1016/j.scitotenv.2018.07.102
Koch I, Reimer K (2012) Bioaccessibility extractions for contaminant risk assessment. In: Comprehensive sampling and sample preparation. Elsevier, pp 487–507
Li X, Gao Y, Zhang M et al (2020) In vitro lung and gastrointestinal bioaccessibility of potentially toxic metals in Pb-contaminated alkaline urban soil: the role of particle size fractions. Ecotoxicol Environ Saf 190:110151. https://doi.org/10.1016/j.ecoenv.2019.110151
Longhin E, Pezzolato E, Mantecca P et al (2013) Season linked responses to fine and quasi-ultrafine Milan PM in cultured cells. Toxicol in Vitro 27:551–559. https://doi.org/10.1016/j.tiv.2012.10.018
Lu H, Rosenbaum S (2014) Developmental pharmacokinetics in pediatric populations. J Pediatr Pharmacol Ther 19:262–276. https://doi.org/10.5863/1551-6776-19.4.262
Maertens RM, Gagné RW, Douglas GR et al (2008a) Mutagenic and carcinogenic hazards of settled house dust II: Salmonella mutagenicity. Environ Sci Technol 42:1754–1760. https://doi.org/10.1021/es702448x
Maertens RM, Yang X, Zhu J et al (2008b) Mutagenic and carcinogenic hazards of settled house dust I: polycyclic aromatic hydrocarbon content and excess lifetime cancer risk from preschool exposure. Environ Sci Technol 42:1747–1753. https://doi.org/10.1021/es702449c
Masto RE, Singh MK, Rout TK et al (2019) Health risks from PAHs and potentially toxic elements in street dust of a coal mining area in India. Environ Geochem Health 41:1923–1937. https://doi.org/10.1007/s10653-019-00250-5
Moya J, Bearer CF, Etzel RA (2004) Children’s behavior and physiology and how it affects exposure to environmental contaminants. Pediatrics 113:996–1006. https://doi.org/10.1542/peds.113.S3.996
Nazzal Y, Rosen MA, Al-Rawabdeh AM (2013) Assessment of metal pollution in urban road dusts from selected highways of the Greater Toronto Area in Canada. Environ Monit Assess 185:1847–1858. https://doi.org/10.1007/s10661-012-2672-3
Oak Ridge National Laboratory (ORNL), United Cleanup Oak Ridge LLC (UCOR), U.S. Department of Energy (DOE) (2023) RAIS toxicity values and physical parameters search. In: Risk assess. Inf. Syst. https://rais.ornl.gov/cgi-bin/tools/TOX_search?select=chemtox. Accessed 16 Mar 2023
Oh SM, Kim HR, Park YJ et al (2011) Organic extracts of urban air pollution particulate matter (PM2.5)-induced genotoxicity and oxidative stress in human lung bronchial epithelial cells (BEAS-2B cells). Mutat Res Toxicol Environ Mutagen 723:142–151. https://doi.org/10.1016/j.mrgentox.2011.04.003
Ojo AF, Peng C, Ng JC (2022) Genotoxicity assessment of per- and polyfluoroalkyl substances mixtures in human liver cells (HepG2). Toxicology 482:153359. https://doi.org/10.1016/j.tox.2022.153359
Oomen AG, Hack A, Minekus M et al (2002) Comparison of five in vitro digestion models to study the bioaccessibility of soil contaminants. Environ Sci Technol 36:3326–3334. https://doi.org/10.1021/es010204v
Ossai CJ, Iwegbue CMA, Tesi GO et al (2021) Distribution, sources and exposure risk of polycyclic aromatic hydrocarbons in soils, and indoor and outdoor dust from Port Harcourt city, Nigeria. Environ Sci Process Impacts 23:1328–1350. https://doi.org/10.1039/D1EM00094B
Palacio IC, Barros SBM, Roubicek DA (2016) Water-soluble and organic extracts of airborne particulate matter induce micronuclei in human lung epithelial A549 cells. Mutat Res Toxicol Environ Mutagen 812:1–11. https://doi.org/10.1016/j.mrgentox.2016.11.003
Pelfrêne A, Sahmer K, Waterlot C et al (2020) Evaluation of single-extraction methods to estimate the oral bioaccessibility of metal(loid)s in soils. Sci Total Environ 727:138553. https://doi.org/10.1016/j.scitotenv.2020.138553
Plumejeaud S, Reis AP, Tassistro V et al (2016) Potentially harmful elements in house dust from Estarreja, Portugal: characterization and genotoxicity of the bioaccessible fraction. Environ Geochem Health 40:127–144. https://doi.org/10.1007/s10653-016-9888-z
Putaud J-P, Van Dingenen R, Alastuey A et al (2010) A European aerosol phenomenology – 3: physical and chemical characteristics of particulate matter from 60 rural, urban, and kerbside sites across Europe. Atmos Environ 44:1308–1320. https://doi.org/10.1016/j.atmosenv.2009.12.011
Raffy G, Mercier F, Glorennec P et al (2018) Oral bioaccessibility of semi-volatile organic compounds (SVOCs) in settled dust: a review of measurement methods, data and influencing factors. J Hazard Mater 352:215–227. https://doi.org/10.1016/j.jhazmat.2018.03.035
Rasmussen PE, Subramanian KS, Jessiman BJ (2001) A multi-element profile of house dust in relation to exterior dust and soils in the city of Ottawa, Canada. Sci Total Environ 267:125–140. https://doi.org/10.1016/S0048-9697(00)00775-0
Rasmussen PE, Beauchemin S, Nugent M et al (2008) Influence of matrix composition on the bioaccessibility of copper, zinc, and nickel in urban residential dust and soil. Hum Ecol Risk Assess Int J 14:351–371. https://doi.org/10.1080/10807030801934960
Ruby MV, Schoof R, Brattin W et al (1999) Advances in evaluating the oral bioavailability of inorganics in soil for use in human health risk assessment. Environ Sci Technol 33:3697–3705. https://doi.org/10.1021/es990479z
Sasaki YF, Sekihashi K, Izumiyama F et al (2000) The comet assay with multiple mouse organs: comparison of comet assay results and carcinogenicity with 208 chemicals selected from the IARC Monographs and U.S. NTP Carcinogenicity Database. Crit Rev Toxicol 30:629–799. https://doi.org/10.1080/10408440008951123
Sena MM, Frighetto RTS, Valarini PJ et al (2002) Discrimination of management effects on soil parameters by using principal component analysis: a multivariate analysis case study. Soil Tillage Res 67:171–181. https://doi.org/10.1016/S0167-1987(02)00063-6
Sevastyanova O, Binkova B, Topinka J et al (2007) In vitro genotoxicity of PAH mixtures and organic extract from urban air particles part II: human cell lines. Mutat Res Mol Mech Mutagen 620:123–134. https://doi.org/10.1016/j.mrfmmm.2007.03.002
Shen M, Liu G, Zhou L et al (2022) Spatial distribution, driving factors and health risks of fine particle-bound polycyclic aromatic hydrocarbons (PAHs) from indoors and outdoors in Hefei, China. Sci Total Environ 851:158148. https://doi.org/10.1016/j.scitotenv.2022.158148
Shi G, Chen Z, Bi C et al (2011) A comparative study of health risk of potentially toxic metals in urban and suburban road dust in the most populated city of China. Atmos Environ 45:764–771. https://doi.org/10.1016/j.atmosenv.2010.08.039
Škrbić BD, Buljovčić M, Jovanović G, Antić I (2018) Seasonal, spatial variations and risk assessment of heavy elements in street dust from Novi Sad, Serbia. Chemosphere 205:452–462. https://doi.org/10.1016/j.chemosphere.2018.04.124
Škrbić B, Đurišić-Mladenović N, Živančev J, Tadić Đ (2019) Seasonal occurrence and cancer risk assessment of polycyclic aromatic hydrocarbons in street dust from the Novi Sad city, Serbia. Sci Total Environ 647:191–203. https://doi.org/10.1016/j.scitotenv.2018.07.442
Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. In: Luch A (ed) Molecular, clinical and environmental toxicology. Springer Basel, Basel, pp 133–164
Temkin AM, Hocevar BA, Andrews DQ et al (2020) Application of the key characteristics of carcinogens to per and polyfluoroalkyl substances. Int J Environ Res Public Health 17:1668. https://doi.org/10.3390/ijerph17051668
Tepanosyan G, Maghakyan N, Sahakyan L, Saghatelyan A (2017) Heavy metals pollution levels and children health risk assessment of Yerevan kindergartens soils. Ecotoxicol Environ Saf 142:257–265. https://doi.org/10.1016/j.ecoenv.2017.04.013
Tice RR, Agurell E, Anderson D et al (2000) Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen 35:206–221. https://doi.org/10.1002/(SICI)1098-2280(2000)35:3%3c206::AID-EM8%3e3.0.CO;2-J
Trasande L, Thurston GD (2005) The role of air pollution in asthma and other pediatric morbidities. J Allergy Clin Immunol 115:689–699. https://doi.org/10.1016/j.jaci.2005.01.056
Turner A, Simmonds L (2006) Elemental concentrations and metal bioaccessibility in UK household dust. Sci Total Environ 371:74–81. https://doi.org/10.1016/j.scitotenv.2006.08.011
U.S. EPA (1989) Risk assessment guidance for superfund Vol. I - human health evaluation manual (part A). U.S. Environmental Protection Agency, Washington, D.C.
U.S. EPA (2005) Supplemental guidance for assessing susceptibility from early-life exposure to carcinogens. U.S. Environmental Protection Agency, Washington, D.C.
U.S. EPA (2017) Exposure factors handbook chapter 5 (update): soil and dust ingestion. U.S. EPA Office of Research and Development, Washington, DC
Vergnoux A, Malleret L, Asia L et al (2011) Impact of forest fires on PAH level and distribution in soils. Environ Res 111:193–198. https://doi.org/10.1016/j.envres.2010.01.008
Walker-Smith J, MacDonald T (1989) Insights provided by the study of the small intestine in the child and the foetus. Gut 30:11–16. https://doi.org/10.1136/gut.30.Spec_No.11
Wang W, Wu F, Zheng J, Wong MH (2013a) Risk assessments of PAHs and Hg exposure via settled house dust and street dust, linking with their correlations in human hair. J Hazard Mater 263:627–637. https://doi.org/10.1016/j.jhazmat.2013.10.023
Wang W, Wu F-Y, Huang M-J et al (2013b) Size fraction effect on phthalate esters accumulation, bioaccessibility and in vitro cytotoxicity of indoor/outdoor dust, and risk assessment of human exposure. J Hazard Mater 261:753–762. https://doi.org/10.1016/j.jhazmat.2013.04.039
Wang C-C, Zhang Q-C, Kang S-G et al (2023) Heavy metal(loid)s in agricultural soil from main grain production regions of China: bioaccessibility and health risks to humans. Sci Total Environ 858:159819. https://doi.org/10.1016/j.scitotenv.2022.159819
World Health Organization (2010) WHO Guidelines for indoor air quality: selected pollutants. WHO, Copenhagen
Živančev J, Antić I, Buljovčić M, Đurišić-Mladenović N (2022) A case study on the occurrence of polycyclic aromatic hydrocarbons in indoor dust of Serbian households: distribution, source apportionment and health risk assessment. Chemosphere 295:133856. https://doi.org/10.1016/j.chemosphere.2022.133856
Acknowledgements
We would like to thank the competitiveness clusters SAFE and EUROBIOMED for granting their label to our project. The authors would like to warmly acknowledge Franck Marot from ADEME for the fruitful scientific discussions. Mathieu Izard, from Atmo Sud, is also thanked for his sound advice for preschools recruitment and on-site sampling. The authors acknowledge Bernard Angeletti from CEREGE for technical support in MMs analyses and the masters’ work of Vanary Nhek, from Aix Marseille University, Laboratoire Chimie Environnement for her assistance in sampling and validating a method for the extraction of the bioaccessible fraction.
Funding
The Plan for Regional Environmental Health (PRSE-3) and the Regional Directorate for the Environment, Development and Housing (DREAL-PACA) co-funded this work. DRIIHM Cluster of Excellence (Labex DRIIHM, ANR-11-LABX-0010) and Excellence Initiative of Aix-Marseille University A*MIDEX (AMX-19-IET-012), both “Investissements d’Avenir” French Programs managed by the ANR, also provided financial support, together with the research federation ECCOREV. Rebecca Castel received a PhD grant from The French Agency for Ecological Transition (ADEME) and from France Southern Region (Région Sud) with our partner AtmoSud.
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Rebecca Castel, Yves Noack, Thierry Orsière, and Laure Malleret contributed to the study conception and design. Material preparation, formal analysis, and investigation were carried out by Rebecca Castel, Virginie Tassistro, Stéphanie Lebarillier, and Yves Noack. Data treatment and visualization were performed by Rebecca Castel, Nathalie Dupuy, and Laure Malleret. Laure Malleret, Thierry Orsière, and Yves Noack contributed to funding acquisition, supervision, and administration of the project. The original draft of the manuscript was written by Rebecca Castel. Laure Malleret, Thierry Orsière, and Yves Noack participated in the final writing—review and editing of the manuscript. All authors read and approved the final version of the manuscript.
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Castel, R., Tassistro, V., Lebarillier, S. et al. Chemical and genotoxic characterization of bioaccessible fractions as a comprehensive in vitro tool in assessing the health risk due to dust-bound contaminant ingestion. Environ Sci Pollut Res (2024). https://doi.org/10.1007/s11356-024-33248-3
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DOI: https://doi.org/10.1007/s11356-024-33248-3