Methodological factors influencing inhalation bioaccessibility of metal(loid)s in PM2.5 using simulated lung fluid☆
Graphical abstract
Introduction
Epidemiological studies have consistently linked chronic and short term exposure to fine particulate matter with an aerodynamic diameter of <2.5 μm (PM2.5) to adverse health outcomes, e.g. cardiovascular and pulmonary morbidity, mortality, increased risk of chronic obstructive pulmonary disease (COPD), pneumonia and lung cancer mortality (Fajersztajn et al., 2017; Pinault et al., 2017; Pope and Dockery, 2006; Pun et al., 2017). The main constituents of airborne PM2.5 include sulphate (20%), crustal materials (soil, sand, road and desert dust; 13.4%), equivalent black carbon (11.9%), NH4NO3 (4.7%), sea salt (2.3%), trace element oxides (1%), water (7.2%) and residual matter (40%) (Snider et al., 2016). A systemic review and meta-analysis of mortality and hospital admissions associated with daily PM2.5 in 110 peer reviewed studies (until May 2011) found that an increase of 10 μg m3 PM2.5 was linked to an increased risk of hospital admissions and 1.04% rise in mortality (Atkinson et al., 2014). Furthermore, 1.51% of the rise in mortality risk was associated with respiratory illnesses (e.g. COPD, asthma, lower respiratory infections) and 0.84% rise in mortality risk associated with cardiovascular causes (e.g. heart failure, stroke, ischemic heart disease and dysrhythmia) (Atkinson et al., 2014). Recent research highlighted that metals in PM2.5 (e.g. Cu, Fe, Mn and Ni) collected at traffic intersections may have considerable reactive oxygen species generation capabilities (Fujitani et al., 2017). Additionally, metals in aqueous extracts of PM2.5 were demonstrated to cause lung inflammation and injury, oxidative stress, lipid and protein damage and cardiovascular injury in mouse and rat models (Gavett et al., 2003; Pardo et al., 2016; Shuster-Meiseles et al., 2016). Similarly, Fe, Cu, Ni, Co and Cr in PM2.5 were also associated with inflammatory responses in mouse type II alveolar cells by increasing the expression of pro-inflammatory genes and proteins (He et al., 2017). Therefore, although metal oxides may comprise a small proportion of PM2.5, it may represent substantial potential to cause human health injuries. Furthermore, because of its small mass, PM2.5 may stay airborne for extended periods and travel long distances, impacting communities far from point sources.
Instead of using total meta(loid) concentration for human exposure assessment, it is more relevant to use the concentration of metal(loid)s in PM2.5 that may potentially dissolve in lung fluid and be absorbed into the blood (Leclercq et al., 2017; Li et al., 2016; Pelfrêne and Douay, 2017). Although using metal(loid) bioavailability (i.e. metal(loid)s absorbed into the systemic circulation in-vivo) remains the most appropriate for exposure assessment, metal(loid) bioaccessibility (i.e. metal(loid)s extracted using simulated lung fluid (SLF) in-vitro) is often more desirable as a rapid and cost effective approach (Mukhtar and Limbeck, 2013a; Stopford et al., 2003). PM2.5 may stimulate engulfment by lung macrophages in the respiratory system (d'Angelo et al., 2014) and metal(loid) dissolution may take place within the acidic environment of phagolysosomes (Kanapilly, 1977). Several SLFs have been developed to simulate phagolysosomal fluid, e.g. simulated intracellular fluid (Thelohan and De Meringo, 1994), artificial lysosomal fluid (ALF) (Midander et al., 2007; Stopford et al., 2003) and phagolysosomal simulant fluid (PSF) (Stefaniak et al., 2005), the latter two being more popular in bioaccessibility assays (Kastury et al., 2017). However, the extraction efficiencies of these SLFs with an acidic pH of 4.5 have not been compared. Additionally, significant knowledge gaps exist in methods currently used to determine metal(loid) bioaccessibility in PM2.5 (Kastury et al., 2017; Wiseman, 2015). For example, the solid to liquid (S/L) ratio ranged from 1:100–1:1163 (Hamad et al., 2014; Potgieter-Vermaak et al., 2012; Wiseman and Zereini, 2014) or not reported because a part of the filter paper with which the particles were collected was used directly in assays (Mukhtar and Limbeck, 2013a; Schaider et al., 2007). Varying agitation frequencies and types have been used in the literature, for example, occasional (Wiseman and Zereini, 2014), continuous (Hamad et al., 2014; Potgieter-Vermaak et al., 2012) or ultrasonic (Mukhtar and Limbeck, 2013a). Large variability in extraction time is also observed in the literature, such as, 1 h in Mukhtar and Limbeck (2013a), 120 h in Schaider et al. (2007) or 30 days in Zereini et al. (2012). Furthermore, incidental ingestion of surface dust may be considered an important pathway for Pb exposure in children due to frequent hand to mouth activity (Scheckel et al., 2013). However, limited research has been conducted on the oral bioaccessibility of PM2.5 from Pb mining/smelting impacted region.
This study aimed to investigate how assay parameters affect metal(loid) bioaccessibility outcomes using PM2.5 in order to recommend a standardised method. In addition, oral bioaccessibility of PM2.5 metal(loid)s was also investigated to compare inhalation exposure to incidental ingestion of surface dust. To achieve this aim, the effect of solid to liquid (S/L) ratio, agitation, SLF composition and extraction time on metal(loid) bioaccessibility in PM2.5 was assessed and compared to bioaccessibility results using simulated GIT solutions.
Section snippets
Collection of PM2.5
Surface soils (0–20 cm) from three Australian mining/smelting impacted sites were collected: historic non-ferrous slag impacted soil from York Peninsula (SH15), smelting impacted soil from Port Pirie (PP) and calcinated mine waste (CMW) from the golden triangle region of Victoria. Soil (<2 mm) was dried at 40 °C and sieved to recover the <53 μm particle size fraction using an Endecotts Octagon digital shaker. To extract the fine dust fraction (PM2.5), 2–5 g of the <53 μm particle size fraction
Results and discussion
The complex nature of PM2.5 composition, deposition and clearance has contributed to variability in in-vitro methods used for bioaccessibility assessment. This study focused on investigating the effects of methodological factors that influence metal(loid) bioaccessibility using SLF in order to standardise a conservative method that is biologically relevant to a human inhalation scenario. Although PM2.5 may contain fine (0.1–2.5 μm) and ultrafine (≤0.1 μm) particles, those with aerodynamic sizes
Conclusion
The results of this study demonstrate that S/L ratio, fluid composition, as well as extraction time significantly influences metal(loid) bioaccessibility in PM2.5. A S/L ratio of 1:5000, end-over-end rotation (45 rpm), 24-h extraction time using ALF is recommended for inhalation bioaccessibility assay to simulate exposure from fine particulate matter via macrophage engulfment. Furthermore, in addition to inhalation, incidental ingestion of PM2.5 with elevated toxic metal(loid)s may be a
Acknowledgements
Farzana Kastury acknowledges the Commonwealth Government of Australia, Research Training program scholarship (RTPd), University of South Australia for the VC and President's Scholarship and the MF & MH Joyner Scholarship in Science. Ranju Karna was supported by Internship/Research Participation Program at the National Risk Management Research Laboratory, U.S. Environmental Protection Agency, administered by the Oak Ridge Institute for Science and Education via an interagency agreement between
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This paper has been recommended for acceptance by Prof. Haidong Kan.