Science of the Total Environment 610–611 (2018) 1138–1146 Contents lists available at ScienceDirect Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv Brominated flame retardants in black plastic kitchen utensils: Concentrations and human exposure implications Jiangmeng Kuang, Mohamed Abou-Elwafa Abdallah, Stuart Harrad ⁎ School of Geography, Earth and Environmental Sciences, University of Birmingham, Birmingham B15 2TT, UK H I G H L I G H T S G R A P H I C A L A B S T R A C T • BFRs detected in plastic kitchen utensils • BFR concentrations significantly higher in older (N 5 years) than newer utensils • BFR transfer from utensils to cooking oil may result in non-negligible exposure. • BFR exposure via dermal contact with kitchen utensils is minimal. a r t i c l e i n f o Article history: Received 18 July 2017 Received in revised form 16 August 2017 Accepted 16 August 2017 Available online 30 August 2017 Editor: Adrian Covaci Keywords: BFR Kitchen utensil Recycled plastic Human exposure UK a b s t r a c t Concerns exist that restricted brominated flame retardants (BFRs) present in waste polymers may have, as a result of recycling, inadvertently contaminated items not required to meet flame retardancy regulations (e.g. plastic kitchen utensils). To investigate the extent to which kitchen utensils are contaminated with BFRs and the potential for resultant human exposure, we collected 96 plastic kitchen utensils and screened for Br content using a hand-held X-ray fluorescence (XRF) spectrometer. Only 3 out of 27 utensils purchased after 2011 contained detectable concentrations of Br (≥3 μg/g). In contrast, Br was detected in 31 out of the 69 utensils purchased before 2011. Eighteen utensils with Br content higher than 100 μg/g, and 12 new utensils were selected for GC–MS analysis of BFRs. BFRs targeted were polybrominated diphenyl ethers (PBDEs) BDE-28, 47, 99, 100, 153, 154, 183 and 209, and novel BFRs (NBFRs) pentabromoethylbenzene (PBEB), 2-ethylhexyl-2,3,4,5tetrabromobenzoate (EH-TBB), 1,2-bis(2,4,6-tribromophenoxy)ethane (BTBPE), bis(2-ethylhexyl)-3,4,5,6tetrabromo-phthalate (BEH-TEBP) and decabromodiphenyl ethane (DBDPE). The ability of XRF to act as a surrogate metric of BFR concentration was indicated by a significant (Spearman coefficient = 0.493; p = 0.006) positive relationship between Br and ΣBFR concentration. Measurements of ΣBFRs were always exceeded by those of Br. This may be due partly to the presence of BFRs not targeted in our study and also to reduced extraction efficiency of BFRs from utensils. Of our target BFRs, BDE-209 was the most abundant one in most samples, but an extremely high concentration (1000 μg/g) of BTBPE was found in one utensil. Simulated cooking experiments were conducted to investigate BFR transfer from selected utensils (n = 10) to hot cooking oil, with considerable transfer (20% on average) observed. Estimated median exposure via cooking with BFR contaminated utensils was 60 ng/day for total BFRs. In contrast, estimated exposure via dermal contact with BFR-containing kitchen utensils was minimal. © 2017 Elsevier B.V. All rights reserved. ⁎ Corresponding author. E-mail addresses: kuangjiangmeng@163.com (J. Kuang), S.J.Harrad@bham.ac.uk (S. Harrad). http://dx.doi.org/10.1016/j.scitotenv.2017.08.173 0048-9697/© 2017 Elsevier B.V. All rights reserved. J. Kuang et al. / Science of the Total Environment 610–611 (2018) 1138–1146 1. Introduction Brominated flame retardants (BFRs) are a group of organic compounds added widely to consumer goods such as electronic devices, textiles, and upholstery etc. to meet flame retardancy regulations. Over the life cycle of such items, BFRs may undergo emission to the environment and as a consequence are ubiquitous in the environment, including air (Abdallah et al., 2008; Sun et al., 2016), dust (Cristale et al., 2016; Harrad et al., 2008; Zhu et al., 2017), soil (Leung et al., 2007; Zhu et al., 2017), sediment (Barón et al., 2014; Guerra et al., 2010), as well as biota (including humans) exposed to such media (Carignan et al., 2013; Drage et al., 2017; Shi et al., 2016; Tao et al., 2017; Zhu et al., 2017). Such environmental contamination, coupled with evidence of their toxicity, means that BFRs are of great concern. As a consequence, BFRs like polybrominated diphenyl ethers (PBDEs) have been listed as persistent organic pollutants (POPs) under the Stockholm Convention and subject to bans and restrictions on their manufacture and new use in a number of jurisdictions. While to date, the majority of attention has focused on BFR exposure as a result of emissions from in-use materials, there is growing realization that the presence of BFRs in waste items also constitutes a potential problem. Waste electrical and electronic equipment (WEEE) may be dismantled to recover precious metals and plastics, with the plastics recovered being recycled. However, use of recycled plastics containing BFRs in new materials has led to concerns that restricted BFRs may be present in newly manufactured goods, including those which are not subject to flame retardancy regulations such as plastic food contact utensils and toys. To minimize contamination of newly manufactured goods that are not subject to flame retardancy regulations (e.g. food contact articles and children's toys) with BFRs via use of BFR-containing recycled polymers, the European Commission has under its Restriction of Hazardous Substances (RoHS) and WEEE directives, set Low POP Concentration Limits (LPCLs) for some BFRs to ensure waste plastics exceeding such limits are not recycled. These values are currently 1000 ppm for PBDEs (not including BDE-209) and hexabromocyclododecane (HBCDD). However, reports exist that plastic goods exceeding LPCLs may still be purchased in the EU. Guzzonato et al. (2017) investigated 26 samples of toys and food-contact articles purchased from the European market, finding that ~ 1/3 of food-contact articles were bromine positive and around half of the toys examined exceeded LPCLs. Samsonek and Puype (2013) investigated the Br and BFR content of 30 black plastic kitchen utensils purchased from the European market, and reported a 30% detection rate for Br. BDE-209 was the major BFR found in Br positive samples, with tetrabromobisphenol-A (TBBPA) and decabromodiphenyl ethane (DBDPE) detected in some samples as well. Elsewhere, Chen et al. (2009) found PBDEs, DBDPE, 1,2bis(2,4,6-tribromophenoxy)ethane (BTBPE) and polybrominated biphenyls (PBBs) in plastic toys purchased from Chinese market, while Ionas et al. (2014) found PBDEs and phosphate flame retardants (PFRs) in toys from the European market. The Br concentrations measured by Samsonek and Puype (2013) ranged from not detected to 2000 μg/g, while BFR concentrations measured by Chen et al. (2009) and Ionas et al. (2014) ranged from not detected to 5000 μg/g, all of which were insufficient to impart flame retardancy, indicating these BFRs were not intentionally added into kitchen utensils or toys, and highly possibly came from recycled plastics. Considering the background above, this study seeks to augment significantly the database on the presence of BFRs in consumer goods by measuring Br (using a hand-held Xray fluorescence (XRF) spectrometer) and a range of BFRs including PBDEs in both used and new plastic kitchen utensils from the UK. Concentrations of PBDEs and other BFRs in these utensils are compared with LPCL values, and for the first time, the potential for human exposure arising from consumer use of such utensils is assessed. This is assessed via examining BFR transfer from selected 1139 utensils to culinary oil during simulated cooking experiments and via modelling dermal uptake from handling utensils. Given the above, the objectives of this study are to: 1) investigate the extent to which kitchen utensils from the UK market are contaminated by Br and BFRs; 2) evaluate the extent to which the XRF measurements of Br provide an accurate metric of BFR concentrations; and; 3) evaluate the potential for human exposure to BFRs as a result of using plastic kitchen utensils containing BFRs. To achieve these objectives, we examined 96 kitchen utensils from the UK. As a first step, these were all screened for their Br content using handheld XRF. Thirty of these utensils were then analysed for their concentrations of BFRs, including 8 polybrominated diphenyl ethers (PBDEs) (BDE28, 47, 99, 100, 153, 154, 183 and 209), pentabromoethylbenzene (PBEB), 2-ethylhexyl-2,3,4,5-tetrabromobenzoate (EH-TBB), BTBPE, bis(2ethylhexyl)-3,4,5,6-tetrabromo-phthalate (BEH-TEBP) and DBDPE. Ten representative utensils were then subjected to controlled experiments to study the transfer of BFRs from kitchen utensils to hot culinary oil. 2. Method and materials 2.1. Sampling New utensils were purchased from retail outlets in Birmingham, UK, while used utensils ≥5 years old were donated by University of Birmingham staff. All utensils were first screened for their Br content using a hand-held XRF spectrometer (Niton™ XL3t GOLDD + XRF Analyzer, Thermo Fisher Scientific). The platform on which utensils were placed for measurement was pre-cleaned with ultra-pure water and ethanol, and measured using XRF to ensure no background interference existed. Measurements of Br were taken at 3–5 randomly selected points on each utensil to minimize the impact of heterogeneity and the highest result was recorded. Utensils displaying a Br content N 100 μg/g (n = 18), along with a further 12 utensils containing b 100 μg/g Br were selected for measurement of their BFR content. 2.2. Chemicals Native BDE-77 was used as the internal standard (IS) to quantify BDE-28, 47, 99, 100, as well as PBEB and EH-TBB; BDE-128 as internal standard for BDE-153, 154 and 183; 13C–BTBPE for BTBPE; 13C–BEHTEBP for BEH-TEBP; and 13C–BDE-209 for BDE-209 and DBDPE. A mixed IS solution of all the above mentioned internal standards (500 pg/μL) in isooctane was prepared. 2,2′,3,3′,4,5-hexachlorobiphenyl (PCB-129) was used as a recovery determination standard (RDS) to determine the recovery of BDE-77, 128, 13C–BTBPE, 13C–BEH-TEBP, and 13 C–BDE-209. The RDS solution was prepared in isooctane at a concentration of 250 pg/μL. All standards were purchased from Wellington Laboratories Inc. and all solvents used (acetone, hexane, isooctane and methanol) were HPLC grade. 2.3. Pre-treatment of plastic samples Plastic utensil samples were first cut into small pieces and then ground into a powder using a Fritsch Pulverisette 0 cryo-vibratory micro mill (Idar-Oberstein, Germany). This was achieved by adding the sample along with a 25 mm diameter stainless steel ball to the stainless steel grinding mortar (50 mL volume), cooled with liquid nitrogen. The cryogenically-cooled sample was then ground at a vibrational frequency of 30 Hz for 5 min and repeated 2–3 times. After 1 min vortexing with 10 mL hexane to achieve complete mixing, the resultant plastic powder was then extracted under 15 min sonication and supernatant was then collected. The process of vortexing and ultrasonication were repeated for 2 more cycles and for the last extraction, the supernatant was left in contact with the sample overnight before collection to maximise recoveries. Combined extracts were reduced in volume to ~2 mL under a gentle stream of nitrogen gas, before mixing with 3–4 mL 98% 1140 J. Kuang et al. / Science of the Total Environment 610–611 (2018) 1138–1146 sulfuric acid. The hexane-acid mixture was then vortexed for 20 s followed by centrifugation at 2000g for 5 min. The supernatant was then collected. To ensure complete transfer, the residue was rinsed with hexane (2 mL) three times. The combined supernatant was then reduced to incipient dryness under a gentle stream of nitrogen gas. The final concentrate was re-dissolved in 200 μL PCB-129 RDS solution prior to analysis of PBDEs and NBFRs by GC–MS. 2.4. Experiments examining BFR transfer from utensil to culinary oil Ten kitchen utensils shown to contain elevated concentrations of BFRs were subjected to experiments designed to mimic the process of cooking in oil. A small portion of kitchen utensil weighing ~ 0.05 g, ~ 5 mm × 4 mm × 2 mm was immersed in 0.5 mL olive oil in a test tube. The test tube was maintained at 160 °C for 15 min to simulate the cooking process and oil collected for analysis. After “cooking” each utensil, the experiment was repeated twice more using the same aliquot of the utensil to investigate the impact of repeated cooking in oil on BFR transfer efficiency. The collected oil samples were first diluted in 3–4 mL hexane, before added with 5–6 mL 98% sulfuric acid. The hexane-acid mixture then underwent the same process describe in Section 2.3, before dissolution in 200 μL PCB-129 RDS solution for analysis. 2.5. GC–MS protocols PBDEs and NBFRs were analysed by GC–MS in electron capture negative ionisation (ECNI) mode using the same method to our previous study (Kuang et al., 2016). For some plastic kitchen utensil samples with extremely high BDE-209 concentrations and the corresponding oil extracts, recoveries of 13C–BDE-209 could reach 400% ~ 1000%, which exceeded the normal range. The reason is that when intensity is too high, the overlap between response peaks of ions on mass spectrometer could not be neglected, especially when peaks are very close. In this case, response of 13C–BDE-209 (m/z 492.6, 494.6) was severely interfered by the extremely high response of BDE-209 (m/z 486.6, 488.6), so an exceptional high “apparent recovery” was observed. To address this issue, we re-injected affected samples in electron ionisation (EI) mode and satisfactory recoveries were obtained, as interference between the quantifying ions used for BDE-209 (m/z 799.4, 801.4) and 13 C–BDE-209 (809.4, 811.4) was weaker given the greater difference in m/z values. 2.6. QA/QC For measurement of Br, the XRF analyzer was calibrated regularly using manufacturer-supplied solid disk standards. And for BFR measurement, three blank oil samples were analysed along with experimental samples. Satisfactory results were obtained with recoveries of internal standards ranging from 60% ~ 130% (Table S1) with all native compounds not detected, except BDE-209 (Table S2). Concentrations of BDE-209 in oil samples were corrected for blank contamination by subtracting the mean value detected in blanks. Satisfactory recoveries of 70% ~ 130% were obtained for both kitchen utensil plastic (Table S3) and cooking experiment oil (Table S4) samples. In addition, to evaluate BFR losses during cooking experiments, a matrix spike experiment was conducted 5 times by spiking known amounts of all target compounds and internal standards into blank oil samples before the cooking experiment. These matrix spike samples were then analysed and recoveries of all compounds calculated (Table S5). Recoveries of all compounds showed good performance ranging from 70% to 170%, and recoveries of target compound showed consistent deviation with coordinating internal standard recoveries (Table S5), ensuring a precise quantification. 3. Results and discussion 3.1. Bromine content of kitchen utensils Table 1 reports Br concentrations in the utensil samples analysed using hand-held XRF. Of the 96 samples analysed, 69 were reported by the donors to be 5 years or older, 6 were aged 2 years, while 21 were purchased for this study between December 2015 and July 2016. It should be noted that “age” in this study refers only to the donorreported date of purchase to the nearest year. It is important to note not only the uncertainty associated with such self-reported data, but that the date of purchase does not equate to the date of manufacture but to the date of availability on the market. Notwithstanding this, for convenience, we use “age” as an abbreviation of “date of availability on the market” from herein. Table 1 also lists the utensil type, with the main categories being: spoons (n = 33), spatulas (n = 18) and ladles (n = 12). Of the 27 utensils aged b 5 years, only 1 (3.7%) contained N100 μg Br/g, 2 (7.4%) contained ~ 5 μg Br/g, with the remaining 24 (88.9%) containing b 3 μg Br/g. In contrast, for utensils aged ≥5 years, 17 (24.6%) contained N100 μg Br/g, 13 (18.9%) contained between 5 and 100 μg Br/g, and 34 (49.3%) containing b3 μg Br/g. Given this apparent dichotomy between “older” and “newer” utensils, we evaluated the significance of this using non-parametric statistical tests as our data did not display a normal distribution. We first conducted a Mann-Whitney rank test to compare Br concentrations between the two age groups. This revealed Br concentrations to be significantly greater in utensils ≥5 years old (p = 0.016). This was consistent with a Spearman correlation analysis which showed utensil age and Br content to be significantly and positively correlated (r = 0.237, p = 0.020). 3.2. BFR concentrations in kitchen utensils Based on the Br concentration data, those utensils containing N100 μg Br/g (n = 18) were subjected to GC–MS determination of their BFR content, together with 12 utensils containing b100 μg Br/g to provide context. These 30 samples are numbered 1–30 in Table 1. Table 2 shows that utensils with high Br content (N100 μg/g) display a higher BFR concentration than those indicated by XRF to contain b 100 μg/g Br. We tested the statistical significance of this relationship using non-parametric tests as our data did not display a normal distribution. Specifically, a Mann-Whitney rank test showed the difference to be statistically significant (p = 0.007), with the positive relationship between Br and BFR concentrations confirmed by Spearman correlation analysis (r = 0.493, p = 0.006). However, more detailed inspection of Table 2 reveals there is substantial discrepancy between our BFR and Br data for the same samples. To be explicit, our ΣBFR measurements are always lower than the corresponding Br measurements – and in some cases substantially so, for example, sample 18 contained 6000 μg Br/g, but displayed a ΣBFR concentration of 0.6 μg/g. This is most likely due to some compounds not included in our list of target BFRs for example TBBP-A, and/or low extraction efficiency for BFRs using our method. We first tested the hypothesis that the discrepancy between Br and ΣBFR was because the former was due to the presence of one or more BFRs not targeted by our GC–MS analyses. To do so, we studied sample 18 in more detail. Tentative support for this explanation is supplied by the observation of several unidentified peaks on the m/z 79 and 81 traces in the GC mass chromatogram for sample 18. Hence, following solvent exchange from isooctane to methanol we re-analysed this sample on a LC-high resolution MS system (UPLC-Orbitrap-MS, Thermo Fisher Scientific, Bremen, Germany) in an attempt to identify BFRs not quantified via our GC–MS method such as TBBP-A or HBCDD. However, this did not provide an obvious explanation for the discrepancy, and thus incomplete extraction efficiency can not be ruled out as a cause in this instance at least. To avoid dissolving the plastic during BFR extraction and thus expedite more rapid analysis, a low polarity aliphatic solvent (hexane) was chosen for extraction. We note that other studies 1141 J. Kuang et al. / Science of the Total Environment 610–611 (2018) 1138–1146 Table 1 Bromine concentrations (μg/g) in kitchen utensils. Table 1 (continued) Sample #a Utensil type Br content, μg/g Date of purchaseb Age, years P1 P2 P3 P4 P5 P6 P7 P8 P9 P10 P11 P12 P13 P14 P15 P16 P17 P18 P19 P20 P21 P22 P23 P24 P25 P26 P27 P28 P29 P30 b3 b3 180 b3 b3 b3 b3 b3 b3 350 300 b3 b3 b3 b3 100 600 6000 200 120 400 150 90 170 150 140 100 170 130 4000 b3 b3 b3 b3 40 b3 b3 b3 b3 b3 30 b3 b3 50 b3 b3 b3 b3 85 b3 b3 b3 b3 b3 b3 b3 10 20 b3 b3 b3 b3 b3 20 b3 b3 b3 b3 10 b3 60 b3 b3 10 b3 b3 Solid spoon Thermos cup lid Thermos cup lid Thermos cup lid Thermos cup lid Food package Food package Food package Food package Ladle Slotted spatula Spaghetti server Solid spatula Solid spatula Food clip Slotted spoon Solid spoon Solid Spoon Solid spoon (grip) Ladle Slotted spatula Solid spoon (grip) Masher Solid spoon (grip) Slotted spoon (grip) Ladle (grip) Slotted spoon Slotted spoon (grip) Scissors Scissors Slotted spatula Solid spatula Ladle Slotted spatula Slotted spoon Solid Spoon Slotted spoon Solid Spoon Ladle Slotted spatula Solid spoon Solid spoon Masher Slotted spatula Slotted spatula Spaghetti server Solid spoon Ladle Slotted spoon Skimming spoon Masher Not recorded Not recorded Not recorded Not recorded Not recorded Cut board Spatula Ladle Solid spoon Slotted spatula Solid spoon Ladle Slotted spoon Masher Spatula Dotted spoon Masher Spatula Masher Scissors Whisk Masher Spaghetti server Slotted spatula Ladle 2015 2015 2015 2015 2015 2015 2015 2015 2015 2008 2008 2013 2013 2013 2013 2009 2009 2006 Before 2011 2001 2001 2006 2009 2006 2006 2006 2009 2002 2002 2002 2009 2009 2009 2009 Before 2011 2007 2001 2016 2016 2016 2009 2009 2008 2008 2008 2008 2008 2008 2006 2006 2006 2006 2006 2006 2006 2006 2009 2009 2009 2006 1996 1996 1996 1996 1996 1998 1998 1998 2002 2002 2002 2014 2014 2001 2001 2001 New New New New New New New New New 8 8 2 2 2 2 7 7 10 N5 15 15 10 7 10 10 10 7 14 14 14 7 7 7 7 N5 9 15 New New New 7 7 8 8 8 8 8 8 10 10 10 10 10 10 10 10 7 7 7 New 20 20 20 20 20 18 18 18 14 14 14 2 2 15 15 15 Sample #a Utensil type Slotted spoon Masher Solid spoon Slotted spatula Masher Ladle Slotted spoon Slotted spoon Slotted spoon Scissors Solid spoon Slotted spatula Ladle Ladle Fork Spatula Solid spoon Solid spoon Slotted spoon Skimming spoon Br content, μg/g Date of purchaseb Age, years b3 30 b3 b3 b3 5 b3 b3 7 b3 b3 b3 b3 8 b3 b3 50 b3 60 b3 2001 2001 2016 2016 2016 2016 2016 2016 2016 2016 2011 2011 2011 2011 2011 Before 2011 Before 2011 Before 2011 Before 2011 Before 2011 15 15 New New New New New New New New 5 5 5 5 5 N5 N5 N5 N5 N5 a Sample # refers to sample analysed for BFR content – see Table 2. Samples not assigned a number were not analysed for their BFR content. b Owner's estimate of purchase date. have used different solvents (Allen et al., 2008, Aldrian et al., 2015 used toluene, and Gallen et al. (2014) used dichloromethane), and thus our BFR measurements may be underestimates of the true value. Also, as TBBP-A is a reactive BFR which binds more firmly with polymers than additive BFRs like PBDEs, hexane may be less effective at extracting it from polymers, leading it to be not detected even in our LC-high resolution MS screening. Given our observation that Br concentrations were significantly higher in samples ≥5 years old, than in younger utensils, we examined our data for similar age-related differences in ΣBFR concentrations, again using non-parametric tests in accordance with the distribution of our data. A Mann-Whitney rank test found significantly (p = 0.014) higher ΣBFR concentrations in utensils ≥ 5 years old than in those b5 years in age. This was consistent with Spearman correlation analysis (r = 0.501, p = 0.005) that showed a positive relationship between BFR concentration and utensil age. These findings are likely attributable to two main factors: (1) the introduction in restrictions in use of PBDEs in the mid-2000s onwards, and (2) the more recent introduction of restrictions on the recycling of BFR-treated plastics. In terms of the BFR distribution pattern, BDE-209 was the most abundant BFR detected and in 17 out of 30 samples (56.7%), BDE-209 accounted for N 70% of ΣBFR. This is consistent with the fact that BDE209 is mainly used in hard plastics like polyamide (Arias, 2001 cited by Alaee et al., 2003) which is used widely in kitchen utensils. Aside of this general predominance of BDE-209 however, the BFR pattern varied widely between individual utensils. For example, while P22, P23 and P24, which came from the same donor and were purchased at the same time, all contained a high percentage of BEH-TEBP (65% ~ 75% ΣBFR); P10 and P11 (donated by the same individual and purchased at the same time) contained substantial contributions of less brominated PBDEs like BDE-47 and -99; while P29 and P30 (which were the two handles of the same pair of scissors) were dominated (~80% ΣBFR) by BTBPE. These 3 examples indicate that as well as age, production batch may be an important additional factor influencing the Br and BFR concentration and pattern. 3.3. BFR transfer from utensil to oil in simulated cooking process Table 3, as well as Figs. 1 and 2 show the transfer of individual BFRs and ΣBFR from the aliquots of utensils subjected to the simulated cooking experiments. The percentage transfer in Figs. 1 and 2 was calculated as r =mBFR−oil/(cBFR−plastic × mplastic) ×100%, where mBFR−oil is the 1142 J. Kuang et al. / Science of the Total Environment 610–611 (2018) 1138–1146 Table 2 BFR concentrations in kitchen utensils, ng/g. Sample # BDE-28 PBEB BDE-47 BDE-100 BDE-99 EH-TBB BDE-154 BDE-153 BDE-183 BTBPE BEH-TEBP BDE-209 DBDPE ΣBFRs, μg/g Br, μg/g P1 P2 P3 P4 P5 P6 P7 P8 P9 P10 P11 P12 P13 P14 P15 P16 P17 P18 P19 P20 P21 P22 P23 P24 P25 P26 P27 P28 P29 P30 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 130 100 b0.2 0.6 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 120 79 15 b0.2 64 b0.2 b0.2 0.2 b0.2 b0.2 b0.2 b0.2 0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 1.1 b0.2 b0.2 b0.2 4.0 b0.2 11 14 8.4 b0.2 8.3 b0.2 33 6.3 37.4 110 0.5 1.2 b0.2 b0.2 b0.2 b0.2 360 210 7.4 25 11 38 9.5 36 15 8.8 b0.2 b0.2 57 b0.2 1000 1000 970 b0.2 82 10 b0.2 7.0 6.9 36 b0.2 0.3 0.5 b0.2 b0.2 b0.2 68 82 1.3 4.8 4.1 9.9 b0.2 34 82 1.8 b0.2 b0.2 30 b0.2 110 110 43 b0.2 30 0.2 b0.2 42 26 150 1.4 2.3 4.6 1.3 1.1 0.7 330 93 7.7 30 21 49 10 180 100 10 b0.2 b0.2 240 b0.2 530 370 130 9.0 260 12 12 b0.2 b0.2 b0.2 b0.2 b0.2 0.5 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 900 950 830 b0.2 b0.2 b0.2 b0.2 7.8 1.3 12 0.4 b0.4 b0.4 b0.4 b0.4 b0.4 48 4.6 0.9 2.9 3.6 5.4 8.9 1000 21 1.3 b0.4 b0.4 15 b0.4 40 23 5.2 3.7 30 7.6 210 16 2.7 22 1.1 0.5 0.7 b0.4 b0.4 1.1 90 21 1.8 6.2 5.6 9.1 36 1800 14 2.3 b0.4 b0.4 25 b0.4 170 110 29 14 560 1600 120,000 36 14 100 16 3.9 b1.0 b1.0 b1.0 4.4 330 36 14 34 24 46 27 1600 23 8.8 b1.0 b1.0 130 b1.0 139 66 49 45 1100 180 13,000 530 78 1200 3.8 5.4 b1.0 b1.0 b1.0 8.4 1400 60 b1.0 1.1 b1.0 b1.0 b1.0 b1.0 210 b1.0 b1.0 b1.0 b1.0 b1.0 280 180 200 35 1500 18,000 1100,000 b0.2 b0.2 b0.2 27 b0.2 150 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 6.8 b0.2 b0.2 350 b0.2 17 46 b0.2 30,000 25,000 22,000 10 140 5.7 b0.2 1100 620 2500 260 37 14 b2.6 b2.6 340 17,000 2200 1300 2500 1200 2100 660 1000 140 260 81 220 110,000 78 8100 1900 2700 2500 81,000 3200 140,000 72 16 23 b9.2 b9.2 12 b9.2 b9.2 290 b9.2 b9.2 b9.2 b9.2 b9.2 b9.2 58 340 b9.2 110 b9.2 b9.2 5500 b9.2 5200 3700 7200 280 5700 420 1900 1.8 0.8 4.1 0.3 0.1 0.2 b0.01 b0.01 0.6 20 2.8 1.4 2.6 1.3 2.3 0.8 6.0 0.6 0.8 0.1 0.2 120 0.1 47 34 34 2.9 90 23 1400 b3 b3 180 b3 b3 b3 b3 b3 b3 350 300 b3 b3 b3 b3 100 600 6000 200 120 400 150 90 170 150 140 100 170 130 4000 mass of BFR extracted by oil, measured by GC–MS, cBFR −plastic is BFR concentration in plastic utensils and mplastic is mass of plastic used in cooking experiment. Transfer was substantial for all compounds, especially during the 1st cooking exposure (batch 1), ranging from 20% to 100%. The extent of transfer decreased in the order batch 1 N batch 2 N batch 3 and with increasing degree of bromination for PBDEs. In particular, while BDE-209 was abundant in most utensils, its transfer to oil was negligible in 6 of 10 cases. However, for samples P22, P24, P28 and P30 that contained BDE-209 concentrations in the range 10–100 μg/g, more substantial transfer was observed. The generally lower transfer efficiency of BDE-209 in our experiments is likely due to a combination of lower solubility in oil of BDE-209 compared to other BFRs, alongside greater binding of BDE-209 to plastic. In some cases, the transfer exceeded 100%. This may be attributable to a number of factors, namely: (a) inhomogeneous distribution of BFRs in the kitchen utensils which could result in the BFR content of the aliquot of the utensil subjected to cooking differing from that in the aliquot used to determine BFR concentration; and (b) that hot oil may be a more effective solvent for extracting BFRs from kitchen utensils than hexane. 3.4. Preliminary exposure assessment We considered two pathways via which human exposure to BFRs in kitchen utensils may occur: (a) transfer to food when cooking, and (b) transfer through dermal contact. The following are preliminary evaluations of the likely magnitude of human exposure via such pathways. these are that: 1) over the useful “lifetime” of every 200 mL oil (assumed 1 week) used for deep frying, the utensil is in contact with oil at 160 °C for a total period over that week of 15 min; and 2) the extent of BFR transfer is proportional to the specific surface area (i.e. surface area per unit utensil volume) of the utensil in contact with oil. We further assumed that the utensil dimensions likely to come into contact with oil during cooking are 10 cm × 8 cm × 2 mm (equivalent to that of a typical spatula), yielding a specific surface area of 10 cm−1. This compares quite closely with the specific surface area of 19 cm−1 of the 5 mm × 4 mm × 2 mm plastic cuboids used in our cooking experiments. Based on these assumptions, we estimated the amount of BFR transferred from kitchen utensils to hot oil during cooking via the equation below. cBFR−oil ¼ ðcBFR−utensil " mutensil " r real Þ=V oil ð1Þ where: cBFR−oil is BFR concentration transferred to hot cooking oil (ng/mL); cBFR − utensil is BFR concentration (ng/g) in kitchen utensils coming into contact with hot oil; mutensil is mass of utensil contact with hot oil when cooking, whose size is 10 cm × 8 cm × 2 mm, and for density, a value of 1.4 g/cm3 was applied based on the average measured value for several utensils on this study. So mutensil = Vutensil × ρutensil = 10 cm × 8 cm × 2 mm × 1.4 g/cm3 = 22.4 g; rreal is BFR transfer rate (unitless) in real-life scenario and is calculated based on transfer rate obtained in cooking experiment (rexp), specific surface area of utensil in experiment (Aexp) and in real-life scenario (Areal): cm " r exp ¼ 10 " r exp ¼ 0:53r exp ; r real ¼ AAreal 19 cm‐1 exp ‐1 3.4.1. Exposure via cooking Exposure via cooking was estimated based on the results of our simulated cooking experiments – note that as some utensils for which BFR concentrations were determined were unlikely to come into contact with hot oil during use (e.g. scissors), these utensils (P2-P5, P6-P9, plus P29 and 30) were excluded from our estimations. To estimate exposure resulting from contact between the utensil and hot oil and subsequent ingestion of the oil we made several assumptions. The first of Voil is volume of oil involved in cooking which is assumed to be 200 mL. Thus, cBFR−utensil " 22:4 g " 0:53r exp 200mL ¼ 0:059cBFR−utensil r exp ng=mL cBFR−oil ¼ ð2Þ 1143 J. Kuang et al. / Science of the Total Environment 610–611 (2018) 1138–1146 Table 3 BFR transfer from kitchen utensils (ng BFR/g plastica) in simulated cooking experiments. Sample BDE-28 PBEB BDE-47 BDE-100 BDE-99 EH-TBB BDE-154 BDE-153 BDE-183 BTBPE BEH-TEBP BDE-209 DBDPE ΣBFRs P1 Batch1 Batch2 Batch3 b0.2 b0.2 b0.2 b0.2 0.2 b0.2 b0.2 b0.2 6.3 b0.2 b0.2 b0.2 7.0 b0.2 b0.2 b0.2 42 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 7.8 b0.4 b0.4 b0.4 16 14 b0.4 b0.4 36 b1.0 b1.0 b1.0 530 100 b1.0 b1.0 b0.2 b0.2 b0.2 b0.2 1100 62 b2.6 b2.6 72 b9.2 b9.2 b9.2 1800 170 b16 b16 P3 Batch1 Batch2 Batch3 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 110 b0.2 5.8 b0.2 35.6 b0.2 b0.2 b0.2 150 13 0.3 b0.2 b0.2 b0.2 b0.2 b0.2 12 b0.4 b0.4 b0.4 22 7.4 b0.4 b0.4 100 b1.0 b1.0 b1.0 1200 b1.0 b1.0 b1.0 b0.2 b0.2 b0.2 b0.2 2500 b2.6 11 b2.6 23 b9.2 b9.2 b9.2 4100 21 17 b16 P10 Batch1 Batch2 Batch3 130 270 86 68 b0.2 2.0 1.2 1.3 360 410 110 85 68 170 41 26 330 170 41 30 b0.2 b0.2 b0.2 b0.2 48 b0.4 b0.4 b0.4 90 21 5.2 4.0 330 b1.0 b1.0 b1.0 1400 92 b1.0 20 b0.2 b0.2 b0.2 b0.2 17,000 4.8 3.6 10 b9.2 b9.2 b9.2 b9.2 20,000 1100 290 250 P11 Batch1 Batch2 Batch3 100 200 63 53 b0.2 2.3 0.5 0.9 210 320 57 33 81 140 14 6.1 93 160 21 12 b0.2 b0.2 b0.2 b0.2 4.6 b0.4 b0.4 b0.4 21 21 2.3 b0.4 36 b1.0 b1.0 b1.0 60 150 35 b1.0 b0.2 0.6 b0.2 b0.2 2200 4.6 b2.6 b2.6 b9.2 b9.2 b9.2 b9.2 2800 1000 190 100 P17 Batch1 Batch2 Batch3 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 36 12 4.9 3.5 34 b0.2 14 21 180 59 16 19 b0.2 b0.2 b0.2 b0.2 1000 210 54 86 1800 560 140 180 1600 1300 310 330 b1.0 b1.0 Ib Ib b0.2 b0.2 b0.2 b0.2 990 41 5.0 b2.6 250 b9.2 b9.2 b9.2 6000 2200 740 920 P18 Batch1 Batch2 Batch3 b0.2 b0.2 b0.2 b0.2 1.1 2.3 b0.2 b0.2 15 36 19 12 82 140 52 33 100 340 140 91 b0.2 b0.2 b0.2 b0.2 21 38 20 22 14 13 4.8 4.3 23 b1.0 b1.0 b1.0 210 100 52 30 b0.2 b0.2 b0.2 b0.2 140 8.4 b2.6 2.7 b9.2 b9.2 b9.2 b9.2 600 670 290 200 P22 Batch1 Batch2 Batch3 b0.2 b0.2 b0.2 b0.2 4.0 b0.2 b0.2 0.4 57 11 b0.2 5.7 30 b0.2 b0.2 b0.2 249 130 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 15 4.1 b0.4 b0.4 25 610 240 94 130 59 21 b1.0 b1.0 270 390 390 46 17 b0.2 b0.2 110,000 100,000 34,000 16,000 5500 6400 1900 1200 120,000 110,000 36,000 18,000 P24 Batch1 Batch2 Batch3 120 b0.2 b0.2 b0.2 11 4.9 b0.2 b0.2 1000 990 810 920 110 55 29 22 530 230 78 53 900 370 160 140 40 15 4.5 2.9 170 61 16 7.9 130 43 10 5.3 280 220 220 200 30,000 7800 3100 1800 8100 3400 1000 570 5200 3300 1200 820 47,000 17,000 6700 4600 P28 Batch1 Batch2 Batch3 64 7.7 b0.2 b0.2 8.3 3.3 b0.2 5.7 82 34 9.8 b0.2 30 b0.2 b0.2 b0.2 260 77 53 14 b0.2 4.5 b0.2 b0.2 30 16 9.4 2.7 560 620 260 100 1100 870 380 150 1,500 1100 430 170 140 82 36 26 81,000 48,000 21,000 10,000 5700 4300 2200 1100 90,000 55,000 25,000 12,000 P30 Batch1 Batch2 Batch3 Batch4 b0.2 b0.2 b0.2 b0.2 b0.2 33 7.2 4.6 3.0 2.7 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 12 0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 210 66 25 30 24 120,000 39,000 12,000 13,000 7400 13,000 2900 1200 1200 980 1100,000 100,000 56,000 51,000 40,000 b0.2 b0.2 b0.2 b0.2 0.2 140,000 32,000 15,000 15,000 13,000 1900 220 120 140 120 1400,000 180,000 85,000 81,000 62,000 a b Amount of BFRs extracted in oil (Batch 1, 2, 3) is expressed as mBFR-oil/mplastic, i.e. mass of BFR detected in each olive oil extract divided by the mass of plastic tested. Interference prevented quantification. Fig. 1. Average percentage transfer of PBDEs from kitchen utensils in simulated cooking experiments (y-error bar represents σn-1). Fig. 2. Average percentage transfer of NBFRs and ΣBFRs from kitchen utensils in simulated cooking experiments (y-error bar represents σn-1). 1144 J. Kuang et al. / Science of the Total Environment 610–611 (2018) 1138–1146 Table 4 BFR exposure (ng/day) via cooking in median and high exposure scenariosa. rexp Median High BDE-28 PBEB BDE-47 BDE-100 BDE-99 EH-TBB BDE-154 BDE-153 BDE-183 BTBPE BEH-TEBP BDE-209 DBDPE ΣBFRs 53.4% NAb 18.7 19.8% NAb 0.7 45.0% 2.4 125.2 37.6% 0.8 10.3 40.0% 4.4 51.0 12.5% NAb 31.6 22.3% 0.3 58.2 27.9% 1.1 135.7 13.2% 1.3 55.9 32.9% 0.1 130.6 20.6% NAb 1651.4 11.7% 52.2 3545.0 20.7% 1.7 393.0 – 64.2 6207.3 a Low exposure scenario was not calculated because minimum concentrations of all BFRs but BDE-209 were not detected; median and high exposure scenarios assume transfer from a utensil containing the median and maximum values of cBFR−utensil respectively; b Not available due to a not detected concentration. According to 2015–2020 dietary guidelines for Americans (U.S. DHHS and DA, 2015), the recommended daily oil intake for an adult is 27 g. We assume that deep fried oil accounts for 15% of daily oil intake on average, and that as noted on the food information label of the oil used, the density of olive oil was 0.9 g/mL; thus the daily BFR exposure amount is: EBFR−oil ¼ 15% " cBFR−oil " 27 g=day 0:9 g=mL ¼ 15% " 0:059cBFR−utensil r exp ¼ 0:27cBFR−utensil r exp ng=day ng 27 g=day " mL 0:9 g=mL ð3Þ Here we use median and maximum concentration of the 20 utensils (P1, P10 ~ P28) as the value of cBFR−utensil for median and high exposure scenario estimates, and the mean transfer rate of the 3 batches in the cooking experiments is used for the value of rexp. The resultant exposure estimates are shown in Table 4. As shown in Table 4, daily exposure to total BFRs are ~ 60 ng and ~6000 ng under median and high scenarios, respectively; while those for ΣBDEs are ~60 ng and 4000 ng respectively. To place these exposure estimates into context, Besis and Samara (2012) reviewed daily intake of PBDEs via different exposure pathways in different countries, and found that dust ingestion could amount to up to 400 ng/day intake in the US and the UK. Intake in other countries was lower, ranging from 50 to 200 ng/day. Dietary intake, as another important exposure pathway, ranged from 50 to 75 ng/day according to Besis's review. Harrad et al. (2004) investigated concentrations of tetra-hexa BDEs in UK duplicate diet samples and estimated dietary exposure of 90 ng/day for ΣPBDEs (tetra- to hexa-BDEs only). D'Silva et al. (2006) investigated concentrations of 17 PBDEs in typical UK diet composite samples in 2003, and the daily dietary exposure for tri- to hepta-BDEs and BDE209 were estimated to be 80 ng/day and 270 ng/day, respectively. For NBFRs, Tao et al. (2017) detected several NBFRs including EH-TBB, BEH-TEBP, BTBPE, DBPDE and tetrabromoethylcyclohexane (DBEDBCH) in UK food samples, estimating the average total daily dietary exposure to the sum of these NBFRs for adults was 90 ng/day. This compares with the median and high-end estimates in this study of ~2 and ~ 2000 ng/day. To place our exposure estimates into context against non-dietary exposure, Harrad et al. (2008) estimated indoor dust ingestion of PBDEs, DBDPE and BTBPE, and the median exposure for UK adult was about 200 ng/day. Ni et al. (2013) estimated PBDE exposure via indoor dust ingestion in different cities of China, the median exposure for adult ranged from 20 to 100 ng/day. Compared with estimates of exposure via other pathways from by previous studies, exposure via cooking using BFR-containing utensils is not negligible. Moreover, although the transfer rate of BDE-209 during cooking is not high, it still accounts for the largest proportion (80%) of exposure via cooking due to its high concentration in utensils. It is important to emphasise the preliminary nature of our assessment of dietary exposure arising from using BFR-containing utensils. Our simulated cooking experiments involved deep frying, which is likely a worst-case scenario with respect to BFR extraction. Moreover, our estimate of oil-utensil contact occurring for 15 min over 1 week is subject to considerable uncertainty and will vary considerably between households, along with the frequency with which individuals will consume deep-fried food. Finally, we focused only on those utensils displaying elevated BFR concentrations, with our high-end exposure estimates based on the most contaminated utensil; thus our high-end estimates are likely a worst-case scenario, with our median estimates more representative of exposure at the population level. Balanced against this, it is not unreasonable to assume that utensils will have contained higher BFR concentrations when new and thus greater BFR transfer will have occurred earlier in the life of some of the older utensils studied here. On the whole therefore, we consider our estimates a reasonable first-level evaluation, and that they provide evidence to suggest that further investigation of the potential for human exposure arising from use of such utensils is warranted. 3.4.2. Dermal exposure Considering the high BFR concentration not only in the main body but also in the grip of kitchen utensils, exposure via dermal contact is of concern. Dermal uptake is a complex process involving two major steps. First, the transfer of BFRs from the plastic polymer to the skin surface film liquid (i.e. becomes bioaccessible). Second, the penetration of the skin barrier to reach the blood circulation (i.e. becomes bioavailable) (Abdallah et al., 2015). With the exception of HBCDDs (Pawar et al., 2017), an extensive survey of the literature revealed no available data on the dermal bioaccessibility of BFRs. For the second process, Abdallah et al. (2015) reported on the dermal uptake rates of mono to deca BDEs over a 24 h exposure period. Therefore, our exposure model adopts a conservative approach with the assumption of 100% bioaccessibility of PBDEs (in the absence of relevant data), and data from Abdallah et al. (2015) were applied for estimation of bioavailability. Daily exposure (ng/day) via dermal contact was calculated by the equation below. E ¼ C " SA " F " EF ð4Þ where E is daily dermal exposure (ng/day), C is the concentration of BFRs in the utensil (ng/cm2), SA is the skin surface area exposed (cm2), F is the fraction absorbed by the skin (unitless), EF is the fraction of time in contact with the item (day−1). To transfer BFR concentration in ng/g to concentration per surface area, a 0.5 mm depth (h) plastic from the surface of the utensil was assumed. For utensil density (ρutensil) a value of 1.4 g/cm3 was applied as indicated in Section 3.4.1. So C ðareaÞ ¼ h " ρutensil " C ðmassÞ ¼ 0:05 cm " 1:4 g=cm3 " C ðmassÞ ¼ 0:07C ðmassÞ: ð5Þ For the exposure area, we used data from the US EPA exposure factors handbook (U.S. EPA, 2011) stating the average surface area of an adult hand is 1070 cm2 for male and 890 cm2 for a female. The average area of a single palm was estimated as 1/2 × 1/2 × (1070 + 890)/2 cm2 = 245 cm2. Considering that not the whole palm will contact with kitchen utensils upon handling, a 75% coefficient was assumed resulting in an exposed skin area (SA) of 184 cm2. Finally, parameters F and EF were obtained from Abdallah et al. (2015), who measured various absorbed fraction of PBDEs at different exposure times from 15 min to 24 h. 1145 J. Kuang et al. / Science of the Total Environment 610–611 (2018) 1138–1146 Table 5 PBDE exposure (ng/day) via dermal contact in median and high scenariosa. F (0.5 h)b Median High F (1 h) Median High BDE-28 BDE-47 BDE-100 BDE-99 BDE-154 BDE-153 BDE-183 BDE-209 0.07% NAd 1.19 0.20% NA 3.40 0.04% 0.05 5.41 0.13% 0.17 17.58 –c – – 0.08% 0.03 1.18 – – – 0.08% 0.17 5.51 – – – 0.03% 0.02 3.85 – – – 0.03% 0.04 456.43 – – – – – – – – – – – – ΣPBDEs 0.05 6.60 0.43 487.95 a Exposure in low scenario was not calculated because minimum concentrations of all BFRs but BDE-209 were not detected; median and high exposure scenarios were calculated based on median and maximum BFR concentration of P1 ~ P30; b Data obtained from Abdallah et al. (2015); c No transfer observed; d Not available due to a not detected concentration. Over a daily contact time of 15 min, no dermal uptake was observed for any PBDEs which is consistent with the “lag time” reported by Abdallah et al. (2015) for the studied compounds. Lag time is defined as the time required by a specific chemical from its initial contact with the skin surface to reach the systemic circulation. Low dermal uptake was observed when the contact time was prolonged to 0.5 h and 1 h, except for higher brominated BDEs (Table 5). Our results indicate that human uptake of PBDEs via dermal contact with cooking utensils is much lower than our intake estimates based on cooking and other pathways (Section 3.4.1). The exception to this is for BDE-153 in the 1 h contact high-end scenario, due to the extremely high BDE-153 concentration in scissor sample P30. This could be attributed to the limited daily contact time with utensils, and low penetration efficiency into skin, especially for BDE-209 whose concentration was the highest. Therefore, our findings suggest when using BFR-contaminated kitchen utensils, exposure is dominated by utensil-oil transfer, rather than utensil-skin transfer. 4. Conclusions • 34% of plastic kitchen utensils analysed in this study contained measurable concentrations of Br. • Under our extraction procedure, BDE-209 was predominant among our target BFRs in most utensils, but the pattern of other BFRs varied substantially between utensils. Elevated concentrations of BTBPE and BDE-153 were found in some utensils. • BFR transfer from utensils into hot oil during simulated cooking experiments was considerable, and differed between BFRs and utensils. Transfer efficiency decreased with increasing Br substitution of PBDEs. • Using BFR containing utensils for frying may lead to considerable dietary exposure, whilst exposure via dermal contact is negligible due to limited contact time and barrier effect of skin. Acknowledgements Jiangmeng Kuang is supported by a Li Siguang scholarship funded by the University of Birmingham and the China Scholarship Council (Scholarship ID No. 201306210057). The authors also gratefully acknowledge additional financial support from the Food Standards Agency (Project Reference FS410016). Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.scitotenv.2017.08.173. References Abdallah, M.A.E., Harrad, S., Covaci, A., 2008. Hexabromocyclododecanes and tetrabromobisphenol-A in indoor air and dust in Birmingham, UK: implications for human exposure. Environ. Sci. Technol. 42, 6855–6861. Abdallah, M.A.E., Pawar, G., Harrad, S., 2015. Effect of bromine substitution on human dermal absorption of polybrominated diphenyl ethers. Environ. Sci. Technol. 49, 10976–10983. Alaee, M., Arias, P., Sjödin, A., Bergman, Å., 2003. An overview of commercially used brominated flame retardants, their applications, their use patterns in different countries/ regions and possible modes of release. Environ. Int. 29, 683–689. Aldrian, A., Ledersteger, A., Pomberger, R., 2015. Monitoring of WEEE plastics in regards to brominated flame retardants using handheld XRF. Waste Manag. 36, 297–304. Allen, J.G., McClean, M.D., Stapleton, H.M., Webstert, T.F., 2008. Linking PBDEs in house dust to consumer products using X-ray fluorescence. Environ. Sci. Technol. 42, 4222–4228. Barón, E., Santín, G., Eljarrat, E., Barceló, D., 2014. Occurrence of classic and emerging halogenated flame retardants in sediment and sludge from Ebro and Llobregat river basins (Spain). J. Hazard. Mater. 265, 288–295. Besis, A., Samara, C., 2012. Polybrominated diphenyl ethers (PBDEs) in the indoor and outdoor environments - a review on occurrence and human exposure. Environ. Pollut. 169, 217–229. Carignan, C.C., Heiger-Bernays, W., McClean, M.D., Roberts, S., Stapleton, H.M., Sjodin, A., Webster, T.F., 2013. Flame retardant exposure among collegiate U.S. gymnasts. Environ. Sci. Technol. 47 (23), 13848–13856. Chen, S.J., Ma, Y.J., Wang, J., Chen, D., Luo, X.J., Mai, B.X., 2009. Brominated flame retardants in children's toys: concentration, composition, and children's exposure and risk assessment. Environ. Sci. Technol. 43, 4200–4206. Cristale, J., Hurtado, A., Gomez-Canela, C., Lacorte, S., 2016. Occurrence and sources of brominated and organophosphorus flame retardants in dust from different indoor environments in Barcelona, Spain. Environ. Res. 149, 66–76. Drage, D.S., Mueller, J.F., Hobson, P., Harden, F.A., Toms, L.-M.L., 2017. Demographic and temporal trends of hexabromocyclododecanes (HBCDD) in an Australian population. Environ. Res. 152, 192–198. D'Silva, K., Fernandes, A., White, S., Rose, M., Mortimer, D., Gem, M., 2006. Brominated organic micro-pollutants in the united kingdom diet – results of the 2003 total diet study. Organohalogen Compd. 68, 770–773. Gallen, C., Banks, A., Brandsma, S., Baduel, C., Thai, P., Eaglesham, G., Heffernan, A., Leonards, P., Bainton, P., Mueller, J.F., 2014. Towards development of a rapid and effective non-destructive testing strategy to identify brominated flame retardants in the plastics of consumer products. Sci. Total Environ. 491, 255–265. Guerra, P., Eljarrat, E., Barcelo, D., 2010. Analysis and occurrence of emerging brominated flame retardants in the Llobregat River basin. J. Hydrol. 383, 39–43. Guzzonato, A., Puype, F., Harrad, S.J., 2017. Evidence of bad recycling practices: BFRs in children's toys and food-contact articles. Environ. Sci. Processes Impacts. Harrad, S., Wijesekera, R., Hunter, S., Halliwell, C., Baker, R., 2004. Preliminary assessment of UK human dietary and inhalation exposure to polybrominated diphenyl ethers. Environ. Sci. Technol. 38, 2345–2350. Harrad, S., Ibarra, C., Abdallah, M.A.-E., Boon, R., Neels, H., Covaci, A., 2008. Concentrations of brominated flame retardants in dust from United Kingdom cars, homes, and offices: causes of variability and implications for human exposure. Environ. Int. 34, 1170–1175. Ionas, A.C., Dirtu, A.C., Anthonissen, T., Neels, H., Covaci, A., 2014. Downsides of the recycling process: harmful organic chemicals in children's toys. Environ. Int. 65, 54–62. Kuang, J., Ma, Y., Harrad, S., 2016. Concentrations of “legacy” and novel brominated flame retardants in matched samples of UK kitchen and living room/bedroom dust. Chemosphere 149, 224–230. Leung, A.O.W., Luksemburg, W.J., Wong, A.S., Wong, M.H., 2007. Spatial distribution of Polybrominated diphenyl ethers and polychlorinated dibenzo-p-dioxins and dibenzofurans in soil and combusted residue at Guiyu, an electronic waste recycling site in Southeast China. Environ. Sci. Technol. 41, 2730–2737. Ni, K., Lu, Y.L., Wang, T.Y., Kannan, K., Gosens, J., Xu, L., Li, Q.S., Wang, L., Liu, S.J., 2013. A review of human exposure to polybrominated diphenyl ethers (PBDEs) in China. Int. J. Hyg. Environ. Health 216, 607–623. Pawar, G., Abdallah, M.A.E., de Saa, E.V., Harrad, S., 2017. Dermal bioaccessibility of flame retardants from indoor dust and the influence of topically applied cosmetics. J. Expo. Sci. Environ. Epidemiol. 27, 100–105. Samsonek, J., Puype, F., 2013. Occurrence of brominated flame retardants in black thermo cups and selected kitchen utensils purchased on the European market. Food Addit. Contam. Part A 1–11. Shi, Z., Zhang, L., Li, J., Zhao, Y., Sun, Z., Zhou, X., Wu, Y., 2016. Novel brominated flame retardants in food composites and human milk from the Chinese total diet study in 2011: concentrations and a dietary exposure assessment. Environ. Int. 96, 82–90. 1146 J. Kuang et al. / Science of the Total Environment 610–611 (2018) 1138–1146 Sun, J., Wang, Q., Zhuang, S., Zhang, A., 2016. Occurrence of polybrominated diphenyl ethers in indoor air and dust in Hangzhou, China: level, role of electric appliances, and human exposure. Environ. Pollut. 218, 942–949. Tao, F., Abou-Elwafa Abdallah, M., Ashworth, D.C., Douglas, P., Toledano, M.B., Harrad, S., 2017. Emerging and legacy flame retardants in UK human milk and food suggest slow response to restrictions on use of PBDEs and HBCDD. Environ. Int. 105, 95–104. U.S. Department of Health and Human Services, U.S. Department of Agriculture, 2015. 2015–2020 Dietary Guidelines for Americans. 8th edition. (December. Available at). http://health.gov/dietaryguidelines/2015/guidelines/. U.S. Environmental Protection Agency (EPA), 2011. Exposure Factors Handbook: 2011 Edition. National Center for Environmental Assessment, Washington, DC (EPA/600/ R-09/052F. Available from the National Technical Information Service, Springfield, VA, and online at). http://www.epa.gov/ncea/efh. Zhu, H., Zhang, K., Sun, H., Wang, F., Yao, Y., 2017. Spatial and temporal distributions of hexabromocyclododecanes in the vicinity of an expanded polystyrene material manufacturing plant in Tianjin, China. Environ. Pollut. 222, 338–347.