Abstract
Redox-active substances in fine particulate matter (PM) contribute to inhalation health risks through their potential to generate reactive oxygen species in epithelial lung lining fluid (ELF). The ELF’s air–liquid interface (ALI) can play an important role in the phase transfer and multi-phase reactions of redox-active PM constituents. We investigated the influence of interfacial processes and properties by scrubbing of coated nano-particles with simulated ELF in a nebulizing mist chamber. Weakly water-soluble redox-active organics abundant in ambient fine PM were reproducibly loaded into ELF via ALI mixing. The resulting oxidative potential (OP) of selected quinones and other PAH derivatives were found to exceed the OP resulting from bulk mixing of the same amounts of redox-active substances and ELF. Our results indicate that the OP of PM components depends not only on the PM substance properties but also on the ELF interface properties and uptake mechanisms. OP measurements based on bulk mixing of phases may not represent the effective OP in the human lung.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
Fine particulate matter (PM2.5) is believed to contribute 80% to the total excess mortality of ambient air pollution, which causes millions of excess deaths per year (COMEAP 2018; Burnett et al. 2018; Lelieveld et al. 2020). PM2.5 contains redox-active species, i.e. transition metal ions, such as copper and iron, and oxidized polycyclic aromatic compounds, such as quinones (O2PAH). Quinones and also other nitrated and oxygenated polycyclic aromatic compounds (PACs) are toxic (Andersson et al. 2009; Park & Park 2009; Kovacic & Somanathan 2014) and known to trigger and maintain catalytic reaction cycles causing oxidative stress and inflammation at the cellular level (Bolton et al. 2000; Andersson et al. 2009; Song & Buettner 2010). Antioxidants in epithelial lining fluid (ELF) to redox-cycle quinones (Roginsky et al. 1999; Kelly et al. 2018). The redox-active species produce reactive oxygen species (ROS) in the ELF of the respiratory tract (Charrier and Anastasio 2011; Lakey et al. 2016). ROS cause oxidative stress associated with chronic diseases (Sarnat et al. 2008; Krall et al. 2017).
PACs are emitted by combustion of fossil fuel and biomass or can be formed by photochemistry. They are found in urban aerosols (Albinet et al. 2008; Lammel 2015; Shen et al. 2016), but also in the continental background and at remote sites (Lammel et al. 2017; Nežiková et al. 2021; Wietzoreck et al. 2022) in both gaseous and particulate phases.
The potential to cause oxidative stress can be estimated utilizing cellular or acellular oxidative potential (OP) assays, which quantify ROS formation or antioxidant consumption. Hereby, PM is added to an assay reagent either directly or as an extract (bulk mixing; Ayres et al. 2008; Verma et al. 2015; Crobeddu et al. 2017;Calas et al. 2018; Daellenbach et al. 2020) or as air–liquid interface (ALI) cell exposure system (Paur et al. 2011; Endes et al. 2014).
Redox-active components of PM2.5 can become effective in the lung through the following mechanisms: (i) molecular dissolution in ELF, (ii) deposition of inhaled particles to alveolar or tracheobronchial surfaces covered by ELF, or (iii) carriage by ultrafine particles (UFPs) penetrating the lung epithelia (Geiser et al. 2005; Li et al. 2017). The surface area presented by the alveoli of the human lung is large (≈100 m2) relative to the volume (≈0.35 L, adult; USEPA 2011, 2019), resulting in alveolar-specific surface area to volume of ≈285 m2 L−1 (Weibel 1963). The ELF-covered surface area could play an important role in the phase transfer and/or the efficiency of catalytic activity of redox-active components of UFPs (Borm et al. 2006; Hussain et al. 2009), i.e. mechanism (ii), which has not been explored yet. Many redox-active species are insoluble in water and thus difficult to disperse in aqueous solution. To our knowledge, no method has been described to load poorly water-soluble organics into ELF. Batch experiments with the target substances provided in bulk solution or as solids may cover mechanism (i) but are expected to largely underestimate mechanism (ii) and completely neglect (iii). Furthermore, organic solvents needed to mimic (ii) may be incompatible with cellular and even acellular biotests (Ayres et al. 2008).
This study aimed to (a) design a method to load poorly water-soluble redox-active organics abundant in ambient fine PM into ELF via an ALI area and (b) determine the OP of this loaded ELF using off-line acellular assays. To this end, an aerosol of UFPs, loaded with the target compounds, is scrubbed by a simulated ELF nebulized in a mist chamber providing the large interface area. Hereby, we test the hypothesis that a high target substance concentration in ELF can be achieved, higher than by bulk mixing. The OP of ELF loaded via ALI mixing is compared with the OP of the same amounts of redox-active substances in ELF following bulk mixing.
Methodology
Choice of ELF
The ELF chosen is a widely used modified Gamble’s solution (Boisa et al. 2014; composition see Table S1) which accounts for realistic levels of electrolytes, antioxidants (namely ascorbic acid, uric acid, and glutathione), proteins, and surfactants. The preparation of the ELF accounting for various requirements is explained in the supplementary material (SM), S1.2.
ELF loading with redox-active organics
ELF loaded by scrubbing nano-particles coated with redox-active organics
Dry coated UFPs were produced by an atomizer and downstream diffusion dryer (Fig. 1). Un-modified, hydrophobic polystyrene latex (PSL) spheres were used in an 80:20 mixture of dimethyl sulfoxide (DMSO) and ultrapure water. PSL provide an inert and suitable matrix for delivery of hydrophobic substances (Lieberherr et al. 2021). The performance characteristics of the atomizer are detailed in the SM, S1.2, and Fig. S1. The targeted organics were added to the 80:20 DMSO:H2O solution containing ≈0.1% PSL spheres with a mean diameter of 57 nm (5%w polystyrene, 1.05 g cm−3, < 0.1%w surfactant tenside solution PS055LT from ConSenxus, Ober-Hilbersheim, Germany). Particles were then atomized by a slightly modified atomizer (model 3076 Constant Output Atomizer, TSI, Shoreview, USA) under stirring agitation with particle-free N2. The 2–4 ring quinones and nitrated PAHs (NPAHs) were targeted based on their abundance in ambient air as well as their expected OP (listed in Table S2). In the downstream dryer, the organic solvent was completely removed due to evaporation. The repeated precision of the generated UFPs with mode around 60 nm is illustrated in Fig. S1.
During operation, the TSI atomizer in combination with the dryer effectively generated ≈4.5 × 10−3 m2 s−1 of total surface area for distributions shown in Fig. S1. The scanning mobility particle sizer (SMPS) consisted of a differential mobility analyser (DMA) and a condensation particle counter (CPC model 5416, Grimm, Ainring, Germany). This aerosol was scrubbed in a mist chamber, model BF61400 Aero Mist nebulizer (Allied Healthcare Products, St. Louis, USA), originally designed for application of aerosolized drugs. It is modified from Cofer et al. (1985), operates on the Venturi principle, and can nebulize up to 15-mL liquid. Supersaturation conditions had been successfully used for efficient scrubbing of aerosols earlier (Orsini et al. 2008). In this chamber, in a volume of ≈15 mL, a mist of the extracting solution (ELF) is nebulized, impinged on a hydrophobic membrane (Teflon filter), and recycled at a rate of ≈0.5 mL min−1 with a total droplet surface area of ≈10−7 m2 s−1 (extrapolated to ≈1 L min−1 sample aerosol flow from Fig. S4). Considering scrubbing periods of 20–40 min, the total effective ELF surface area provided for reactive uptake was (1.5 ± 0.5) × 10−5 m2 L−1.
The generated particles are deposited onto the quartz fibre filter (QF) in one channel and are scavenged by refluxed ELF (15 mL, PTFE filter) in a mist chamber. The mass flux of target substances from the atomizer is quantified by analysis of the deposit on the QF. To this end, the filter was extracted with dichloromethane (DCM), and the extract was purified with solid-phase extraction using a SiOH cartridge and then quantified (Chemical analysis).
The interfacial surface area produced in the mist chamber at 1 L min−1 was 0.4 ± 0.1 m2 min−1, which yielded an operation time dependent total interface area between 8 and 17 m2 for the given test run times between 20 and 40 min (Table 1). Note that the lung of an adult human averages 100 m2 (Weibel 1963).
In order to preserve the target compounds, the ELF used for scavenging was employed with a modified composition; namely antioxidants (ascorbic acid, uric acid, and glutathione) as well as cysteine were not included. The reason being antioxidants might modify the redox-active substances, while cysteine bears the risk of unwanted reactions with amino acid groups during storage. Storage temperature was 4 °C. Right before OP measurements, the antioxidants ascorbic and uric acid were added to the loaded ELF solution. OP measurements were done using the H2O2 assay (OPH2O2; MAK-165, Sigma-Aldrich 2014), antioxidant assay (OPAA; Shahpoury et al. 2019), and the DTT assay (OPDTT; Tong et al. 2018), described in the SM. These acellular methods are the most frequent choices to determine the OP of organics and especially quinones (Guo et al. 2020). The H2O2 assay presents the physiological conditions best, since it includes the endogenous antioxidant in physiologically relevant concentrations in a simulated ELF measuring a product, which is also produced in the human body. Acellular OP assays including these have recently been intercompared (Shahpoury et al. 2022). Samples from the QF and the mist chamber were blank controlled (producing daily minimum of one ELF and one QF blank, which remained unloaded but otherwise followed the exact same lab treatment and handling as the loaded ELF and QF samples, respectively). At the beginning of each day’s experiments, the atomizer was flushed first with a blank 80:20 DMSO:H2O solution.
ELF loaded by bulk mixing of redox-active organics
The identical concentrations of redox-active substances in bulk mixtures in ELF as in the samples of scrubbing ELF were produced in a beaker. For at least some of the compounds, these concentrations (100–1000 µg L−1; Table 1) were limited by the substances’ solubility in ELF. The concentrations were achieved in several dilution steps, assuring the organic solvent not to exceed organic:H2O of 1:100. Two microlitres of the respective PAC stock solution in DMSO (0.1 g L−1, then diluted to the tenfold targeted concentration) with the respective concentration was added to 198-µL ELF and vortexed (2 min). The OPH2O2 was determined subsequently (S1.4.1) after adding the antioxidants ascorbic and uric acid.
Chemical analysis
The quartz filter samples were extracted by vortexing with dichloromethane (DCM) and then cleaned-up using solid-phase extraction (SPE, SiOH cartridge, Macherey Nagel, Düren, Germany; Albinet et al. 2014). The target substances were isolated from ELF scrubber samples by applying an aliquot (0.5, 1, or 3 mL depending on the substance) by protein precipitation (in a centrifuge vial with equivalent volume of isopropanol, vortexing and centrifugation) and SPE (HLB cartridge, Macherey Nagel). Because of low recovery of SPE in case of 1,4-naphthoquinone (1,4-O2NAP), 2-methyl-1,4-naphthoquinone (2 M-(1,4)O2NAP), and 9,10-phenanthrenequinone (9,10-O2PHE), liquid–liquid extraction using DCM was performed with subsequent purification by SPE (SiOH cartridge) for these three quinones. The analytes were separated and quantified using a Trace 1310 gas chromatograph (GC; Thermo Scientific, Waltham, USA) interfaced to a TSQ8000 Evo triple quadrupole mass selective detector (MS/MS; Thermo Scientific). The analysis was performed in negative chemical ionization mode with methane used as the ionization gas. The analytes were separated on a 30 m DB-5 ms capillary column (0.25 mm ID, 0.25 μm film thickness; J&W, Santa Clara, USA) with helium (99.99%; Westfalen, Münster, Germany) as a carrier gas (Shahpoury et al. 2018). Analyte recoveries (Table S2) from ELF and QFs ranged 85–116% (n = 4 replicates).
Results and discussion
ELF loading by air–liquid interface and related OP
The concentration of the target substances in the scrubbed ELF increased with the loading time (i.e. collection time of mist chamber, Table S3) and was proportional to the amounts of loaded compounds. However, a trend for volatilizational losses from the loaded PSL was found in the QF samples, suggesting that low vapour pressure (high molecular weight or MW) substances were enriched, as high vapour pressure substances likely partitioned to some extent to the gas-phase (gas-particle partitioning). The amounts of redox-active substances loaded into ELF by scrubbing were similar to those collected on the filter for the high MW (low vapour pressure) compounds (relative difference between 50 and 300%) but were higher for the low MW (high vapour pressure) compounds (relative difference exceeding 1 order of magnitude; Table S3). This points to the advantage of using mist chamber for scavenging of the gas-phase in equilibrium with suspended particles by the scrubbing ELF. This is a more realistic representation of the uptake into ELF in the lung than using particles’ deposits, collected by phase separation.
Comparison of air–liquid interface (ALI) mixing with bulk mixing
For two substances tested, 7,12-O2BAA and 1-NPYR, a significant OPH2O2 is found following uptake across the large ALI, while no OP was detected for the same (stoichiometric) mixture produced by bulk mixing of the redox-active compounds into ELF (Table 1). For one other quinone, 9,10-O2ANT, and two other NPAHs, 1-NNAP and 9-NPHE, no or very low OP was found regardless of the type of mixing or uptake (Table 1). The observed effect reflects a more efficient phase transfer in the mist compared to the bulk, validating the hypothesis. While bulk mixing bears impediments of agglomeration, insolubility, and poor miscibility, the scrubbing process provides a large surfactant surface area for molecules at the PSL particles’ surface to adsorb on and become available and accessible for reaction later on. The water solubility of the studied 2-ring substances is high (> 1 g L−1), but of the 3–4 ring substances limited (0.3–54 mg L−1). 1-NPYR is known to get redox cycled by proteins (present in ELF; Table S1; Nachtman 1986; Park & Park 2009), which was not reported from the other studied NPAHs. A surface effect on redox activity has not been reported for quinones or other oxidized aromatics yet, to the best of our knowledge. However, the decomposition of gaseous ozone on water droplets (and related formation of H2O2; Gallo et al. 2022) was found to be mediated by the interface surface area. Possibly, a reaction could be facilitated, if the condensed phase matrix enhanced the exposure of one of the reactants, through reducing degree of freedom of molecules and/or accumulation at the interface. This was reported for the reactivity of an aromatic alkene on the surface of ice (Ray et al. 2013).
Apart from interface area in the alveolar space and water solubility, the efficiency of the uptake of particulate phase redox-active compounds into ELF in the lung will also depend on PM matrix (wettability, morphology) and on the distribution of redox-active compounds in the particles (surface, bulk). This is suggested by leaching PM samples from various sources and of different morphology with simulated ELF (Xie et al. 2018; Liu et al. 2019). Up to date, such aerosol parameters’ effects have not been specifically addressed and were beyond the scope of this study.
Conclusions
Through reproducible generation of nano-particles coated with redox-active compounds, a large surface area for uptake of these compounds into ELF was provided. The mist chamber allows for both uptake mechanisms following dissolution as well as surface-mediated multiphase reactions at the ELF-nano-particle interface and provides soft deposition conditions. OP quantified by application of a mist chamber also includes the gas-phase of semi-volatile components of PM, which is more realistic to the actual uptake in the lung than quantification based on filter deposits, whose constituents had been separated from the gas-phase.
Among the 5 substances comparing effects from ALI mixing with bulk mixing, a significant OP signal (t-test, 0.05 level of significance) was found for two oxidants (7,12-O2BAA and 1-NPYR) when the ELF uptake occurred via a large ALI, while all 5 compounds yielded negligible OP signal when mixed in bulk. This suggests that the OP of ambient PM as determined in acellular assays by bulk mixing of extracts of filter or impactor samples might be lower than the effective OP exerted in the lung upon inhalation. The specific surface concentration of the experimental setup used, 8 m2 during 20 min or 0.03 m2 per 5 s (average duration of breath), still corresponds to 3 orders of magnitude which reduced area relative to the conditions in the deep lung, i.e. ≈102 m2 exposed every 5 s. Hence, the effect of redox-active components of ambient PM might be even stronger in the deep lung, and the effective OP is correspondingly higher. Our results indicate that the OP of PM components depends not only on the PM substance properties but also on the ELF interface properties and uptake pathways. OP measurements based on bulk mixing of phases, for which data have been accumulating rapidly in recent years, may not represent the effective OP in the human lung with its large interfacial area.
Data availability
All data generated or analysed during this study are included in this published article, supplied as supplementary material, or are available from the corresponding author on reasonable request.
References
Albinet A, Leoz-Garziandia E, Budzinski H, Villenave E, Jaffrezo JL (2008) Nitrated and oxygenated derivatives of polycyclic aromatic hydrocarbons in the ambient air of two French alpine valleys - part 1: concentrations, sources and gas/particle partitioning. Atmos Environ 42:43–54
Albinet A, Nalin F, Tomaz S, Beaumont J, Lestremau F (2014) A simple QuEChERS-like extraction approach for molecular chemical characterization of organic aerosols: application to nitrated and oxygenated PAH derivatives (NPAH and OPAH) quantified by GC–NICIMS. Anal Bioanal Chem 406:3131–3148
Andersson H, Piras E, Demma J, Hellman B, Brittebo E (2009) Low levels of the air pollutant 1-nitropyrene induce DNA damage, increased levels of reactive oxygen species and endoplasmic reticulum stress in human endothelial cells. Toxicol 262:57–64
Atkinson R, Arey J (1994) Atmospheric chemistry of polycyclic aromatic hydrocarbons: formation of atmospheric mutagens. Environ Health Persp 102:117–126
Ayres JG, Borm P, Cassee FR, Castranova V, Donaldson K, Ghio A, Harrison RM, Hider R, Kelly F, Kooter IM, Marano F, Maynard RL, Mudway I, Nel A, Sioutas C, Smith S, Baeza-Squiban A, Cho A, Duggan S, Froines J (2008) Evaluating the toxicity of airborne particulate matter and nano-particles by measuring oxidative stress potential - a workshop report and consensus statement. Inhal Toxicol 20:75–99
Boisa N, Elom N, Dean JR, Deary ME, Bird G, Entwistle JA (2014) Development and application of an inhalation bioaccessibility method (IBM) for lead in the PM10 size fraction of soil. Environ Internat 70:132–142
Bolton JL, Trush MA, Penning TM, Dryhurst G, Monks TJ (2000) Role of quinones in toxicology. Chem Res Toxicol 13:135–160
Borm PJ, Robbins D, Haubold S, Kuhlbusch T, Fissan H, Donaldson K, Schins R, Stone V, Kreyling W, Lademann J, Krutmann J, Warheit D, Oberdörster E (2006) The potential risks of nanomaterials: a review carried out for ECETOC. Part Fibre Toxicol 3:11
Burnett R, Chen H, Szyszkowicz M, Fann N, Hubbell B, Pope CA, Apte JS, Brauer M, Cohen A, Weichenthal S, Coggins J, Di Q, Brunekreef B, Frostad J, Lim SS, Kan H, Walker KD, Thurston GD, Hayes RB, Lim CC, Turner MC, Jerrett M, Krewski D, Gapstur SM, Diver WR, Ostro B, Goldberg D, Crouse DL, Martin RV, Peters P, Pinault L, Tjepkema M, van Donkelaar A, Villeneuve PJ, Miller AB, Yin P, Zhou M, Wang L, Janssen NAH, Marra M, Atkinson RW, Tsang H, Quoc Thach T, Cannon JB, Allen RT, Hart JE, Laden F, Cesaroni G, Forastiere F, Weinmayr G, Jaensch A, Nagel G, Concin H, Spadaro JV (2018) Global estimates of mortality associated with long-term exposure to outdoor fine particulate matter. Proc Natl Acad Sci USA 115:9592–9597
Calas A, Uzu G, Kelly FJ, Houdier S, Martins JMF, Thomas F, Molton F, Charron A, Dunster C, Oliete A, Jacob V, Besombes JL, Chevrier F, Jaffrezo JL (2018) Comparison between five acellular oxidative potential measurement assays performed with detailed chemistry on PM10 samples from the city of Chamonix (France). Atmos Chem Phys 18:7863–7875
Charrier JG, Anastasio C (2011) Impacts of antioxidants on hydroxyl radical production from individual and mixed transition metals in a surrogate lung fluid. Atmos Environ 45:7555–7562
Cofer WR, Collins VG, Talbot RW (1985) Improved aqueous scrubber for collection of soluble atmospheric trace gases. Environ Sci Technol 19:557–560
COMEAP (2018) Committee on the medical effects of air pollutants: associations of long-term average concentrations of nitrogen dioxide with mortality. Public Health England, London, p 152
Crobeddu B, Aragao-Santiago L, Bui LC, Boland S, Squiban AB (2017) Oxidative potential of particulate matter 2.5 as predictive indicator of cellular stress. Environ Poll 230:125–133
Daellenbach KR, Uzu G, Jiang J, Cassagnes LE, Leni Z, Vlachou A, Stefenelli G, Canonaco F, Weber S, Segers A, Kuenen JJP, Schaap M, Favez O, Albinet A, Aksoyoglu S, Dommen J, Baltensperger U, Geiser M, el Haddad I, Jaffrezo JL, Prévôt ASH (2020) Sources of particulate-matter air pollution and its oxidative potential in Europe. Nature 587:414–419
Endes C, Schmid O, Kinnear C, Mueller S, Camarero-Espinosa S, Vanhecke D, Foster EJ, Petri-Fink A, Rothen-Rutishauser B, Weder C, Clift MJD (2014) An in vitro testing strategy towards mimicking the inhalation of high aspect ratio nanoparticle. Part Fibre Toxicol 11:40
Gallo A, Musskopf NH, Liu XL, Yang ZQ, Petry J, Zhang P, Thoroddsen S, Im H, Mishra H (2022) On the formation of hydrogen peroxide in water microdroplets. Chem Sci 13:2574
Geiser M, Rothen-Rutishauser B, Kapp N, Schürch S, Kreyling W, Schulz H, Semmler M, Im Hof V, Heyder J, Gehr P (2005) Ultrafine particles cross cellular membranes by nonphagocytic mechanisms in lungs and in cultured cells. Environ. Health Persp. 113:1555–1560
Guo L, Jim L, Huang S (2020) Effect of PM characterization on PM oxidative potential by acellular assays: a review. Rev Environ Health 35:461–470
Hussain S, Boland S, Baeza-Squiban A, Hamel R, Thomassen LCJ, Martens JA, Billon-Galland A, Fleury-Feith J, Moisan F, Pairon JC, Marano F (2009) Oxidative stress and proinflammatory effects of carbon black and titanium dioxide nanoparticles: role of particle surface area and internalized amount. Toxicology 260:142–149
Kelly RA, Leedale J, Calleja D, Enoch SJ, Harrell A, Chadwick AE, Webb S (2019) Modelling changes in glutathione homeostasis as a function of quinone redox metabolism. Sci Rep 9:6333
Kovacic P, Somanathan R (2014) Nitro-aromatic compounds: environmental toxicology, carcinogenicity, mutagenicity, therapy and mechanism. J Appl Toxicol 34:810–824
Krall JR, Mulholland JA, Russell AG, Balachandran S, Winquist A, Tolbert PE, Waller LA, Sarnat SE (2017) Associations between source-specific fine particulate matter and emergency department visits for respiratory disease in four U.S. cities. Environ Health Perspect 125:97–103
Lakey PSJ, Berkemeier T, Tong H, Arangio AM, Lucas K, Pöschl U, Shiraiwa M (2016) Chemical exposure-response relationship between air pollutants and reactive oxygen species in the human respiratory tract. Sci Rep 6:32916
Lammel G (2015) Polycyclic aromatic compounds in the atmosphere – a review identifying research needs. Polycyclic Aromat Compd 35:316–329
Lammel G, Mulder MD, Shahpoury P, Kukučka P, Lišková H, Příbylová P, Prokeš R, Wotawa G (2017) Nitro-polycyclic aromatic hydrocarbons – gas–particle partitioning, mass size distribution, and formation along transport in marine and continental background air. Atmos Chem Phys 17:6257–6270
Lammel G, Kitanovski Z, Kukučka P, Novák J, Arangio A, Codling GP, Filippi A, Hovorka J, Kuta J, Leoni C, Příbylová P, Prokeš R, Sáňka O, Shahpoury P, Tong HJ, Wietzoreck M (2020) Levels, phase partitioning, mass size distributions and bioaccessibility of oxygenated and nitrated polycyclic aromatic hydrocarbons (OPAHs, NPAHs) in ambient air. Environ Sci Technol 54:2615–2625
Lelieveld J, Pozzer A, Pöschl U, Fnais M, Haines A, Münzel T (2020) Loss of life expectancy from air pollution compared to other risk factors: a worldwide perspective. Cardiovasc Res 116:1910–1917
Lelieveld S, Wilson J, Dovrou E, Mishra A, Lakey PSJ, Shiraiwa M, Pöschl U, Berkemeier T (2021) Hydroxyl radical production by air pollutants in epithelial lining fluid governed by interconversion and scavenging of reactive oxygen species. Environ Sci Technol 55:14069–14079
Li XY, Hao L, Liu YH, Chen CY, Pai VJ, Kang JX (2017) Protection against fine particle-induced pulmonary and systemic inflammation by omega-3 polyunsaturated fatty acids. Biochim Biophys Acta 1861:577–584
Lieberherr G, Auderset K, Calpini B, Clot B, Crouzy B, Gysel-Beer M, Konzelmann T, Manzano J, Mihajlovic A, Moallemi A, O’Connor D, Sikoparija B, Sauvageat E, Tummon F, Vasilatou K (2021) Assessment of real-time bioaerosol particle counters using reference chamber experiments. Atmos Meas Tech 14:7693–7706
Liu XL, Ji R, Shi Y, Wang F, Che W (2019) Release of polycyclic aromatic hydrocarbons from biochar fine particles in simulated lung fluids: implications for bioavailability and risks of airborne aromatics. Sci Total Environ 655:1159–1168
Nachtman JP (1986) Superoxide generation by 1-nitropyrene in rat lung microsomes. Res Commun Chem Path Pharmacol 51:73–80
Nežiková B, Degrendele C, Bandowe BAM, Holubová Smejkalová A, Kukučka P, Martiník J, Mayer L, Prokeš R, Přibylová P, Klánová J, Lammel G (2021) Three years of atmospheric concentrations of nitrated and oxygenated polycyclic aromatic hydrocarbons and oxygen heterocycles at a central European background site. Chemosphere 269:128738
Orsini DA, Ma Y, Sullivan A, Sierau B, Baumann K, Weber RJ (2003) Refinements to the particle-into-liquid sampler (PILS) for ground and airborne measurements of water soluble aerosol composition. Atmos Environ 37:1243–1259
Park EJ, Park K (2009) Induction of pro-inflammatory signals by 1-nitropyrene in cultured BEAS-2B cells. Toxicol Lett 184:126–133
Paur HR, Cassee FR, Teeguarden J, Fissan H, Diabate S, Aufderheide M, Kreyling W, Hänninen O, Kasper G, Riediker M, Rothen-Rutishauser B, Schmid O (2011) In-vitro cell exposure studies for the assessment of nano-particle toxicity in the lung—a dialog between aerosol science and biology. J Aerosol Sci 42:668–690
Ray D, Malongwe JK, Klán P (2013) Rate acceleration of the heterogeneous reaction of ozone with a model alkene at the air−ice interface at low temperatures, Environ Sci Technol 44:6773–6780
Roginsky VA, Barsukova TK, Stegmann HB (1999) Kinetics of redox interaction between substituted quinones and ascorbate under aerobic conditions. Chem Biol Interact 121:177–197
Sarnat JA, Marmur A, Klein M, Kim E, Russell AG, Sarnat SE, Mulholland JA, Hopke PK, Tolbert PE (2008) Fine particle sources and cardiorespiratory morbidity: an application of chemical mass balance and factor analytical source-apportionment methods. Environ Health Perspect 116:459–466
Shahpoury P, Kitanovski Z, Lammel G (2018) Snow scavenging and phase partitioning of nitrated and oxygenated aromatic hydrocarbons in polluted and remote environments in central Europe and the European Arctic. Atmos Chem Phys 18:13495–13510
Shahpoury P, Harner T, Lammel G, Leliveld S, Tong H, Wilson J (2019) Development of an antioxidant assay to study oxidative potential of airborne particulate matter. Atmos Meas Techn 12:6529–6539
Shahpoury P, Zhang ZW, Filippi A, Hildmann S, Lelieveld S, Mashtakov B, Patel BR, Traub A, Umbrio D, Wietzoreck M, Wilson J, Berkemeier T, Celo V, Dabek-Zlotorzynska E, Evans G, Harner T, Kerman K, Lammel G, Noorozifar M, Pöschl U, Tong H (2022) Inter-comparison of oxidative potential metrics for airborne particles identifies differences between acellular chemical assays. Atmos Pollut Res 13:101596
Shen GF, Chen YC, Du W, Lin N, Wang XL, Cheng HF, Liu JF, Xue CY, Liu GQ, Zeng EY, Xing BS (2016) Exposure and size distribution of nitrated and oxygenated PAHs among the population using different household fuels. Environ Pollut 216:935–942
Sigma-Aldrich (2014) Fluorimetric hydrogen peroxide assay kit MAK165, Sigma Aldrich Tech. Bulletin. p 3. https://www.sigmaaldrich.cn/deepweb/assets/sigmaaldrich/product/documents/187/223/mak165bul.pdf. Accessed 21 Dec 2022
Song Y, Buettner GR (2010) Thermodynamic and kinetic considerations for the reaction of semiquinone radicals to form superoxide and hydrogen peroxide, Free Rad Biol Med 49:919–962
USEPA (2011) Exposure factors handbook, Chapter 6: Inhalation rates, US Environmental Protection Agency. p 96. https://www.epa.gov/expobox/exposure-factors-handbook-chapter-6 . Accessed 1 Apr 2022
USEPA (2019) Integrated science assessment for particulate matter. Report No. EPA600/R-19/188, US Environmental Protection Agency, Office of Research and Development, Research Triangle Park, USA, p 1986
Verma V, Wang Y, el Afifi R, Fang T, Rowland J, Russell AG, Weber RJ (2015) Fractionating ambient humic-like substances (HULIS) for their reactive oxygen species activity - assessing the importance of quinones and atmospheric aging. Atmos Environ 120:351–359
Weibel ER (1963) Morphometry of the human lung. Springer, Berlin, p 164
Wietzoreck M, Kyprianou M, Bandowe BAM, Celik S, Crowley JN, Drewnick F, Eger P, Fischer H, Friedrich N, Iakovides M, Kukučka P, Kuta J, Nežiková B, Pokorná P, Pribylová P, Prokeš R, Rohloff R, Tadic I, Tauer S, Wilson J, Harder H, Lelieveld J, Pöschl U, Stephanou E, Lammel G (2022) Polycyclic aromatic hydrocarbons (PAHs) and their alkylated-, nitro- and oxy-derivatives in the atmosphere over the Mediterranean and Middle East seas. Atmos Chem Phys 22:8739–8766
Xie SY, Lao JY, Wu CC, Bao LJ, Zeng EY (2018) In vitro inhalation bioaccessibility for particle-bound hydrophobic organic chemicals: method development, effects of particle size and hydrophobicity, and risk assessment. Environ Int 120:295–303
Zhuo S, Du W, Shen G, Li B, Liu J, Cheng H, Xing B, Tao S (2017) Estimating relative contributions of primary and secondary sources of ambient nitrated and oxygenated polycyclic aromatic hydrocarbons. Atmos Environ 159:126–134
Acknowledgements
The authors thank Kurt Lucas and Jake Wilson (MPIC) for discussion and Uwe Kuhn and Kira Ziegler (MPIC) for technical help.
Funding
Open Access funding enabled and organized by Projekt DEAL. Open access funding enabled and organized by Projekt DEAL. This work was supported by the Max Planck Society.
Author information
Authors and Affiliations
Contributions
KB and GL designed the research. KB designed and conducted the experiments. AF, SH, SL, PS, and MW did the chemical and OP, and KB, AF, and MW analysed the data. KB, GL, and MW discussed the results with input from all, and KB and GL wrote the paper with input from all.
Corresponding author
Ethics declarations
Ethical approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Philippe Garrigues
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Baumann, K., Wietzoreck, M., Shahpoury, P. et al. Is the oxidative potential of components of fine particulate matter surface-mediated?. Environ Sci Pollut Res 30, 16749–16755 (2023). https://doi.org/10.1007/s11356-022-24897-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-022-24897-3