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Occurrence of bisphenol-A and its brominated derivatives in tributary and estuary of Xiaoqing River adjacent to Bohai Sea, China
Marine Pollution Bulletin 149 (2019) 110551
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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Occurrence of bisphenol-A and its brominated derivatives in tributary and estuary of Xiaoqing River adjacent to Bohai Sea, China Jing Lana, Zhaoshuang Shenb, Wei Gaoc, Aifeng Liub,
T
⁎
a
Environmental Science and Engineering, Qingdao University, Qingdao 266071, China CAS Key Laboratory of Bio-based Materials, Qingdao Institute of Bioenergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao 266101, China c Research Center for Analytical Sciences, Department of Chemistry, College of Sciences, Northeastern University, Box 332, Shenyang 110819, China b
ARTICLE INFO
ABSTRACT
Keywords: Bisphenol-A Brominated bisphenol-A analogs Distribution Source Bohai Sea estuary Wetlands
The chemical industrial zone located along the Xiaoqing River wetlands adjacent to Bohai Sea is one of the largest production bases for brominated flame retardants in China. Herein, high levels of bisphenol-A, tetrabromobisphenol-A (TBBPA), tribromobisphenol-A, dibromobisphenol-A, and monobromobisphenol-A were detected in sediment, soil, and water samples of this zone in the range of below method detection limit (< MDL)–5.45 × 106 ng/kg dw, < MDL–8.37 × 104 ng/kg dw, and < MDL–5.59 × 102 ng/L, respectively. They were mainly buried in sediments as their highest levels in sediment samples. The small concentration fluctuation between water samples retrieved in the upstream and downstream zones is likely attributed to seawater backflow. The nearby chemical factories were point pollution sources and the less brominated analogs are largely from debromination of TBBPA. High pollution levels and the ecological risks of these pollutants along the Xiaoqing estuary to Bohai Sea need to be further assessed in future studies.
1. Introduction Bisphenol-A (BPA) is the raw material required for the production of polycarbonate, epoxy resin, and tetrabromobisphenol-A (TBBPA) and its derivatives. BPA and TBBPA have been detected in various environmental compartments, including soil, sediment, sludge, water, dust, air, food, and organisms of the Bohai Sea in China (Srivastava et al., 2015; Liu et al., 2016b; Malkoske et al., 2016). The TBBPA analog, tribromobisphenol-A (TriBBPA), was observed at twice the concentration of TBBPA in breast milk, indicating that debromination is an important metabolism pathway of TBBPA in the human body (Akiyama et al., 2015). Due to their endocrine disruption effects, thyroid hormone activities, and potential carcinogenicity, levels of BPA and TBBPA have caused much concern with regards to their pollution, health, and ecological risks (Srivastava et al., 2015; Liu et al., 2016c; Skledar and Masic, 2016; Yin et al., 2018). Like TBBPA, its less brominated analogs also display adverse effects. TriBBPA and dibromobisphenol-A (DBBPA) were shown to promote adipocyte differentiation (Akiyama et al., 2015). TriBBPA, DBBPA, and monobromobisphenol-A (MBBPA) were shown to be more toxic than TBBPA when tested with microtox and algal assays (Debenest et al., 2010). However, these analogs, created as byproducts or transformation and degradation products, have been scarcely studied with regards ⁎
to their environmental emergence and risks, likely due to the lack of available commercial standards (Qu et al., 2016; Liu et al., 2019). During production and usage, BPA, TBBPA, and various analogs are discharged into the environment, emerging as currently unknown pollutants. These chemicals and their related derivatives are mainly released from chemical factories and waste recycling. Additionally, impurities produced along with the chemical products can also be discharged into the environment. TriBBPA, a byproduct of TBBPA, accounts for 3% of the total production yield of TBBPA (Howard and Muir, 2013). Many mono-modified ether-linked TBBPA analogs have been identified as byproducts of TBBPA derivatives detected in soil, seaweed, mollusks, and fish, among other samples (Liu et al., 2016a; Liu et al., 2017; Liu et al., 2018a). Furthermore, a large amount of transformation or degradation products can be formed during the waste treatment process of the chemical products or by the metabolism of TBBPA and BPA in the environment. Through the photolysis, pyrolysis, chemical degradation, microbial degradation, and biological transformation of TBBPA (Liu et al., 2018b), > 120 degradation products have been identified, including TriBBPA, DBBPA, MBBPA, BPA, TBBPA sulfate, TBBPA glucuronide, TBBPA methyl ether, and brominated phenols. TriBBPA, DBBPA, and MBBPA, as the most important brominated analogs, have been determined in several compartments, including breast milk (Akiyama et al., 2015; Nakao et al., 2015), sewage sludge
Corresponding author. E-mail address: [email protected] (A. Liu).
https://doi.org/10.1016/j.marpolbul.2019.110551 Received 31 July 2019; Received in revised form 26 August 2019; Accepted 26 August 2019 Available online 05 September 2019 0025-326X/ © 2019 Elsevier Ltd. All rights reserved.
Marine Pollution Bulletin 149 (2019) 110551
J. Lan, et al.
(Chu et al., 2005), and sediment (Guerra et al., 2010; Lu et al., 2015). The chemical industrial zone of Shouguang City in Shandong Province, China, is one of the largest production bases for various brominated flame retardants (BFRs) worldwide. It is located between Xiaoqing River and its tributary, which flow through wetlands and salt marshes into the Bohai Sea. High levels of TBBPA (> 5.0 × 106 ng/kg dw), as well as of its derivatives and byproducts, have been found in soils collected near this area. Unfortunately, high levels have also been determined in organisms of the Bohai Sea. Furthermore, low brominated products, TriBBPA and DBBPA were also detected in soil samples from this zone. However, TriBBPA, DBBPA, and MBBPA were not quantified due to the lack of chemical standards. Wetlands and salt marshes play important roles as productive estuary ecosystems, acting not only as transition and buffering zones protecting the coastal lines from tidal waves but also serving as essential habitats for coastal wildlife such as fish and seabirds. Over the past few decades, land-derived contaminants from extensive anthropogenic activities have been increasingly transported, dissolved, and deposited in estuarine and coastal environments, strongly influencing regional environments. Furthermore, the BFR factories located along the tributary of Xiaoqing River could be the direct pollution source of the nearby river, wetland, and Bohai Sea (Ruan et al., 2009; Qu et al., 2013). However, to date, no data on their environmental levels and behavior in the tributary and estuaries has been reported. Herein, the levels of TBBPA, BPA, TriBBPA, DBBPA, and MBBPA in soil, water, and sediment samples collected along the tributary river flowing through the BFR factory zones have been determined. The pollution levels and distribution characteristics are assessed, and their pollution sources and environmental risks are discussed. The present results would contribute to the further understanding of the environmental fate and ecological toxicity of TBBPA and BPA.
tubes (ENVI™-carb, Supelclean™, 0.5 g, 6 mL) were used to further purify sediment samples. TriBBPA (97%), DBBPA (including two isomers, 2,6-DBBPA (98%) and 2,2′-DBBPA (97%)), and MBBPA (98%) were synthesized following the related literature (Nakao et al., 2015), purified, and characterized by high resolution mass spectrometry (HRMS) and 1H nuclear magnetic resonance (1H NMR). Chemicals with a purity lower than 95% were further purified by HPLC. The detailed synthesis routines were as described below. 2.2.1. MBBPA, 2,2′-DBBPA, and TriBBPA BPA was dissolved in 5 mL of ethanol, into which a solution of pyridinium tribromide (in 10 mL in ethanol) was slowly added. The molar ratio of pyridinium tribromide to BPA was 1.5:1 (for MBBPA) and 4:1 (for 2,2′-DBBPA and TriBBPA). Following maintenance of the reaction at room temperature for 1.5 h, thin layer chromatography of the products showed the disappearance of BPA. The reaction mixture was diluted with 200 mL of water and extracted three times with 200 mL of ethyl acetate. The organic phase was combined and dried with anhydrous sodium sulfate. After concentration, the residue was purified by silica gel column chromatography (petroleum ether:ethyl acetate = 4:1) to obtain MBBPA at a yield of 85% and purity of 98%, and 2,2′-DBBPA and TriBBPA at yield of 78% and 75%, and purity of 97% and 97%, respectively. The products were further characterized by 1 H NMR and HRMS and used as the standards. 2.2.2. 2,6-DBBPA One of the hydroxyl groups of BPA was protected by reaction with 2-bromopropane in acetone to promote the bromination of BPA at one benzene ring. A sodium hydroxide solution (3.5 M) was carefully added to the reaction mixture and stirred vigorously for 5 h. The purified BPA mono(propyl ether) was then reacted with pyridinium tribromide (molar ratio 1:1) in ethanol to generate 2,6-dibrominated BPA mono (propyl ether). Finally, the protection group was removed by adding BCl3 solution (molar ratio 1:10, in deoxidized and dehydrated DCM) and ethyl mercaptan (molar ratio 1:2.5) in an ice-salt bath. The reaction mixture was stirred overnight and monitored by thin layer chromatography. At the reaction endpoint, the mixture was diluted with 200 mL of saturated sodium thiosulfate ice water and extracted three times with 200 mL of ethyl acetate. After concentration, the residue was purified using silica gel column chromatography (petroleum ether: ethyl acetate = 4:1) to generate 2,6-dibromobisphenol-A at a yield of 90% with a purity of 98%.
2. Materials and methods 2.1. Sampling Soil, sediment, and water samples were collected from along the tributary of Xiaoqing River (Zhangseng River) near the estuary to Bohai Sea (Fig. 1) in Shouguang City, Shandong Province, China. Along the river, there is a small area of wetland covered with reeds and other water plants. The river crosses a chemical park where several large BFR factories are located (near sampling sites 5, 6, and 7 in Fig. 1). The total annual output of TBBPA related to these BFR factories has been stated to be over 70,000 tones (Liu et al., 2017). The Zhangseng River merges with the Xiaoqing River near site 14, and sites 12, 13, and 14 are located in an estuary wetland near a salt field (Fig. 1). Site 15 is located near the entrance to the Bohai Sea. When the tide rises, the sampling river is often irrigated backwards, which occurred during sampling. Surface soil (0–5 cm), river water, and sediment samples were simultaneously collected at each sampling site, and the distance between two adjacent sampling sites was ~2 km. The soil and sediment samples were freeze dried, filtered through a stainless-steel grid (100 mesh), and stored at −20 °C before sample preparation. Water samples were stored at −20 °C after being transported to the laboratory and were liquidliquid extracted within 5 days.
2.3. Instrument parameters of Orbitrap-HRMS Ultra-HPLC (UHPLC, Ultimate 3000) coupled with Orbitrap Fusion Tribrid mass spectrometry (Orbitrap HRMS, Thermo Fisher Scientific, USA) was used for qualitative and quantitative analysis. An Agilent chromatography column ZORBAX ODS (150 × 3.0 mm, 2.5 μm) was used for target chemical separation. The injection volume was 10 μL for each sample and the flow rate was 0.6 mL/min with methanol (A) and water (B) as the mobile phases. The elution program was started as 60/ 40 (A/B) and kept for 3 min, reaching 90/10 (A/B) in 7 min, 100% A in 8 min and kept for 4 min, and finally returned to 60/40 (A/B) in 0.1 min and kept for 4.9 min. Heated electrospray ionization (ESI) was selected for HRMS analysis under a negative mode and collected parent ions in full scan range (m/z), from 100 to 1000. High-energy collisional dissociation was used to fragment the parent ions. The parameters of HRMS followed the recommended values of the equipment, as described elsewhere (Liu et al., 2017).
2.2. Chemicals and materials BPA (≥99%) and TBBPA (≥97%) were obtained from SigmaAldrich. The standard chemicals were dissolved in methanol at a concentration of 100 μg/mL and stored in a refrigerator at 4 °C. High-performance liquid chromatography (HPLC) grade methanol, acetone, dichloromethane (DCM), and hexane were obtained from Merck & Fisher Scientific Co. Deionized water was prepared by a Milli-Q advantage system. Biobeads (S-X3, BIO-RAD) were used as the package materials for gel permeation chromatography (GPC). Solid phase extraction (SPE)
2.4. Sample pretreatment The soil/sediment samples (2.0 g), which had been mixed with anhydrous sodium sulfate (5 g) and isotope-labeled surrogates (D10TBBPA, 20 ng and 13C12-BPA, 20 ng), were extracted with methanol 2
Marine Pollution Bulletin 149 (2019) 110551
J. Lan, et al.
Fig. 1. Map of the sampling sites (sites 1–15) for the surface soils, waters and sediments.
is the location of BFR factory.
(30 mL) three times (20 min per time). The combined supernatant was concentrated by rotary evaporator and solvent exchanged to 1 mL of hexane/DCM (1/1, v/v) for GPC (38 × 2.5 cm i.d.) cleanup. Following sample loading, the GPC column was eluted with hexane/DCM (1/1, v/ v). The initial 100 mL eluted were discarded, and the following 200 mL were collected and concentrated by rotary evaporator. For soil samples, the purified substances were re-dissolved in 1 mL of methanol for instrument analysis. For sediment samples, the purified substances were re-dissolved in 1 mL of hexane/DCM (1/1, v/v) and further purified by an ENVI-Carb™ (500 mg, 6 mL) SPE cartridge. The ENVI-Carb cartridge was balanced by 5 mL of acetone, 5 mL of DCM, and 5 mL of hexane, in that order. The sample was loaded and the cartridge was eluted with 10 mL of acetone (containing 0.5% NH3·H2O), which was concentrated with N2 and re-dissolved in 1 mL of methanol for analysis. The water samples (200 mL) were filtered through a glass fiber filter and the pH was adjusted between 4 and 6 by HCl (1 M). The isotopelabeled surrogates (D10-TBBPA, 20 ng and 13C12-BPA, 20 ng) were then added. Finally, the sample was liquid-liquid extracted three times by DCM (50 mL). The combined extracts were rotary evaporated and redissolved in 1 mL of methanol.
spectrum and the fragmentation mass spectrum data of these chemicals were further confirmed by comparison to the reported data (Chu et al., 2005; Nakao et al., 2015). Following sample extraction and clean-up, the recoveries of TBBPA, TriBBPA, DBBPA, and MBBPA ranged from 78% to 95%. The method detection limits (MDLs) ranged from 0.02 to 3 ng/g dw for the soil/sediment samples, and ranged from 0.2 to 30 ng/ L for water samples. The matrix disturbance effects were < 10%. The recoveries of isotope-labeled surrogates in the sample were higher than 90%, indicating the practicality of the method. A blank sample was treated with every batch of environmental samples (every 10 samples) to avoid cross-contamination.
2.5. Quality control and quality assurance
3.1. Identification of BPA, MBBPA, DBBPA, TriBBPA, and TBBPA
The synthesized chemicals were purified by column chromatography and HPLC chromatography and characterized by 1H NMR and HRMS. The target chemicals were identified with Orbitrap HRMS at a resolution of 120,000 and mass error of < 3 ppm. The full scan mass
Due to the lack of commercial standards for the identification of MBBPA, 2,6-DBBPA, 2,2′-DBBPA, and TriBBPA, herein, these were synthesized in high purity (> 97%) and identified by Orbitrap HRMS. The precision and sensitivity of the method benefitted from the high
2.6. Statistical analyses The raw data was transformed to figures using Origin 9.0, which was also used for Spearman's rank correlation test. When the p value of the test was below 0.05, the linear regression between the two tested variables was regarded as significant. 3. Results and discussion
3
Marine Pollution Bulletin 149 (2019) 110551
J. Lan, et al.
Table 1 Chemical information of TBBPA, BPA and their analogs. Chemicals
Structure
Molecular formula
HRMS Found m/z for [M − H]−
Isotope ratio
Mass error
TBBPA
C15H12O2Br4
538.75006/540.74799/542.74579/544.74365/546.74146
1:4:6:4:1 (Br)
0.476
TriBBPA
C15H13O2Br3
460.83942/462.83731/464.83511/466.83301
1:3:3:1 (Br)
0.280
DBBPA
C15H14O2Br2
382.92880/384.92667/386.92453
1:2:1 (Br)
0.057
MBBPA
C15H15O2Br
305.01819/307.01614
1:1 (Br)
−0.248
BPA
C15H16O2
227.10760/228.11090
5.9:1 (13C)
−0.674
Notes: m/z labeled in bold was used as quantitative ions; m/z labeled in italics was used as qualitative ions.
content ranged within 1.16 × 103 to 2.53 × 105 ng/kg dw (average 4.43 × 104 ng/kg dw), 1.49 × 102 to 9.71 × 104 ng/kg dw (average 2.26 × 104 ng/kg dw), and < MDL to 5.23 × 104 ng/kg dw (average 9.62 × 103 ng/kg dw) for TriBBPA, DBBPA, and MBBPA, respectively. In soil, their content ranged within 1.05 × 102 to 2.23 × 104 ng/kg dw (average 4.79 × 103 ng/kg dw), 7.60 to 3.28 × 103 ng/kg dw (average 1.31 × 103 ng/kg dw), and < MDL to 2.81 × 103 ng/kg dw (average 1.18 × 103 ng/kg dw) for TriBBPA, DBBPA, and MBBPA, respectively. In water, their concentration ranged from within < MDL to 2.05 × 102 ng/L (average 3.83 ng/L), < MDL to 1.48 × 102 ng/L (average 48.2 ng/L), and < MDL to 13.1 ng/L (average 5.2 ng/L) for TriBBPA, DBBPA, and MBBPA, respectively. In sediment, the target concentrations were observed to decrease in concentration in the order of BPA > TBBPA > TriBBPA > DBBPA > MBBPA, as observed in sewage sludge samples from Ontario, Canada, but their sediment levels were much higher than that in the sludge samples (Chu et al., 2005). The detection frequencies of TriBBPA and DBBPA were all 100% in sediment and soil samples, much higher than that in water samples. Furthermore, MBBPA had the lowest detection frequencies in all samples, with 73% in sediment, 60% in soil, and 47% in water samples. All the collected samples displayed higher levels and detection frequencies for TriBBPA, DBBPA, and MBBPA than that in many mediums worldwide, for example, sewage sludge and sediment samples from a waste water treatment plant in Canada (not detectable to 560 ng/g dw, 7.1–50.0%) (Guerra et al., 2010), milk samples (< MDL to 253 ng/L, 0–100%) (Akiyama et al., 2015; Nakao et al., 2015), or sediment from Lake Erie in Canada (< 0.04 ng/g dw). The much higher levels observed are expected given the location of the nearby factories, which act as an important direct pollution source. The total content of the six chemicals in sediment were much higher than in soil and in water. Thus, the results indicate that BPA and TBBPA tend to accumulate in sediments and soils, as they are prone to adsorbing onto the fine particles (Qian et al., 2019; Zhao et al., 2019). Csediment/Cwater for BPA and TBBPA were in the ranges of 3.0 to 1.10 × 104 (average 1.11 × 103, media 1.40 × 102) and 3.55 to 2.27 × 105 (average 1.94 × 104, media 3.14 × 103), respectively. Further, a greater amount of TBBPA tended to absorb onto the sediment than BPA, likely due to its higher soil sorption coefficient (Koc) value (TBBPA, log Koc = 5.24, vs. BPA, log Koc = 3.10) (Liu et al., 2015). Additionally, the higher water solubility and lower octanol/water partition coefficient (Kow) value (log Kow, 3.64) of BPA could be the reasons for the higher proportion of BPA than TBBPA (log Kow, TBBPA, 7.20) in water.
resolution of HRMS. The isotopic abundance ratios, accurate m/z values of the targets, and their retention times in mass chromatography can be used as the typical characteristics to identify target chemicals from the full scan spectra of samples. The isotope ratios indicated the number of bromine atoms in the molecule, and thus target chemicals containing 4, 3, 2, and 1 bromine atoms presented with isotope ratios of 1:4:6:4:1, 1:3:3:1, 1:2:1, and 1:1, respectively. These target chemicals were determined using the most abundant isotopic peak of [M − H]− in HRMS spectra as the quantitative ion and the adjacent isotopic ions as qualitative ions (Table 1). The mass errors for the observed m/z values of the target chemicals were all < 1 ppm. BPA, MBBPA, DBBPA (both 2,2′DBBPA and 2,6-DBBPA), TriBBPA, and TBBPA were detected at 3.6, 5.8, 7.6, 8.9, and 10.1 min, respectively. Due to the same mass spectra and retention time of two isomers of DBBPA, 2,6-DBBPA and 2,2′DBBPA were determined by the total amount of these two isomers. For BPA, the most abundant mass peak at m/z 227.10760 was used for quantification, and its 13C isotopic peak at m/z 228.11090 was used for qualitative analysis. 3.2. Environmental levels in sediment, soil, and water samples Both BPA and TBBPA were detected in all the collected samples. BPA was detected in the range of 1.03 × 103 to 5.45 × 106 ng/kg dw in sediment (average 5.21 × 105 ng/kg dw), 1.85 × 102 to 1.87 × 104 ng/ kg dw in soil (average 4.61 × 103 ng/kg dw), and 2.73 × 102 to 5.59 × 102 ng/L in water (average 4.15 × 102 ng/L) (Fig. 2). TBBPA was detected in ranges of 2.08 × 103 to 1.35 × 106 ng/kg dw in sediment (average 2.61 × 105 ng/kg dw), 2.63 × 102 to 8.37 × 104 ng/kg dw in soil (average 1.79 × 104 ng/kg dw), and 6.0–1.13 × 102 ng/L in water (average 37.1 ng/L) (Fig. 2). The BPA and TBBPA content in sediment was similar and much higher than other chemical contents in sediment. The levels of TBBPA in sediment were comparable to those in estuaries in the Netherlands and England (< 0.1–9750 μg/kg) (Morris et al., 2004) and higher than those in sediments of the aquatic environment of south China (0.19–82.3 ng/g dw) (He et al., 2013). The TBBPA content in soil along the tributary of Xiaoqing River adjacent to the Bohai Sea were lower than those in the chemical park (< MDL–4.10 × 108 ng/kg dw) (Liu et al., 2017). These observations were attributed to the production, transport, and unorganized discharge of BPA and TBBPA related to BFRs, resulting in a higher concentration near the BFR factories than in other sampling sites (Fig. 3). The less brominated BPA analogs were observed at lower levels than BPA and TBBPA in the respective samples (Fig. 2). In sediment, their 4
Marine Pollution Bulletin 149 (2019) 110551
J. Lan, et al.
Fig. 2. Sample concentrations of BPA, TBBPA and other analogs in sediment and soil (ng/kg dw), water (ng/L). The concentration of 25th and 75th percentiles is represented by box, the median concentration is represented by middle line, the mean concentration is represented by “□”, The whiskers extending from the box are the lowest and highest non-outlier values. “×” represents the outlier value.
1E+06 1E+05
Concentration
1E+04 1E+03 1E+02 1E+01 1E+00 1E-01
B
PA -s
ed i B me P B A- nt PA s M -w oil B B at PA er -s M ed Q1 M BB ime B PA n B PA -s t D -w oil B B at PA er -s e R D di 1 D BB me B PA n B PA -s t Tr iB -w oil B at PA er -s Tr ed S Tr iBB im 1 iB P en B A- t PA s TB -w oil B at PA er -s e TB di T1 TB BP me B A- nt PA s -w oil at er
1E-02
3.3. Distribution characteristics along the river to estuary of Bohai Sea
showed an overall trend of gradual reduction along the Zhangseng River to Bohai Sea. The same results were also observed for BPA, MBBPA, DBBPA, and TriBBPA, suggesting that pollution sources were single and likely from water transport of sewage disposal. Site 15 and its adjacent area might be the deposit accumulation area for terrestrial source pollutants. Besides the direct pollution from the factories, a large amount of transformation products can also be generated from the chemical products, e.g., debromination is the main degradation pathway for anaerobic degradation of TBBPA (Liu et al., 2018b). The debromination products were low brominated BPA, including TriBBPA, DBBPA, and MBBPA, with BPA as the terminal product. Values of (TriBBPA + DBBPA + MBBPA) / TBBPA in 15 sediment samples were of 7.5–151.8% (average, 36.6%), indicating that some transformation products were likely to be from debromination of TBBPA in sediment. Meanwhile, significant Spearman correlations (p < 0.05) were observed for sedimental TBBPA, TriBBPA, DBBPA, MBBPA, and BPA, indicating that they could arise from the same pollution sources and in situ generation of low debromination products in sediment. Environmental conditions can obviously affect the debromination of TBBPA. Values of (TriBBPA + DBBPA + MBBPA) / TBBPA in 8 water samples were higher than in soil and sediment samples of the same sites (Fig. 4), while values in 5 soil samples were higher than in water and sediment samples of the same sites. These results are consistent with the degradation rate of TBBPA under different conditions, e.g., a water phase (lower TBBPA concentration) and oxic conditions facilitate the transformation of TBBPA (Liu et al., 2018b). In water samples, BPA accounted for the largest proportion of chemicals, while TBBPA accounted for the largest proportion in soil and sediment samples (Fig. 4). These observations are in good agreement with the quick debromination of TBBPA in water. In soil and sediment samples, the proportion of each analyte in their total amount was in the order of MBBPA < DBBPA < TriBBPA < TBBPA, corresponding to the gradual debromination degradation of TBBPA. BPA was the second largest composition in sediment which was relevant to the complete debromination of TBBPA. The second largest composition is TriBBPA rather than BPA in most of soil samples which may be likely due to further oxidation of
In water samples, the highest concentration of BPA was 5.60 × 102 ng/L, which was also the highest concentration for the chemicals observed in all the 15 water samples (Fig. 3). The average concentration values were in the order of BPA > TBBPA > DBBPA > TriBBPA > MBBPA. In all sites, TriBBPA, DBBPA, and MBBPA presented similar levels. Additionally, BPA, TBBPA, TriBBPA, DBBPA, and MBBPA in water samples showed no significant differences along the river towards the Bohai Sea (Fig. 3). The Spearman correlation analysis also presented no significant correlations (p > 0.05) between these concentrations. Values of (TriBBPA + DBBPA + MBBPA) / TBBPA in 15 water samples were 8.0–721.5% (average, 227.2%) (Fig. 4), indicating a large proportion of these less brominated analogs could be derived from TBBPA. In soil samples, the highest content of TBBPA was of 8.37 × 104 ng/ kg dw in most sampling site of S1 (Fig. 3). The average values presented in the order of TBBPA > BPA > TriBBPA > DBBPA > MBBPA. Along the river flow direction all the targets in soil samples generally presented a decreasing concentration trend. TBBPA, TriBBPA, and DBBPA presented significant correlations (p < 0.05) between each other, indicating that they shared the pollution sources. Compared with sediment and water samples, the accumulation of contaminants in soils can be affected by more factors such as factory dust, wind direction, atmosphere settlement, soil adsorption ability, etc. Soil samples of sampling sites 2, 3, and 5 (near the factories) presented higher concentrations, corresponding to the possible dust from the factories. Values of (TriBBPA + DBBPA + MBBPA) / TBBPA in 15 soil samples were within the range 5.9–394.6% (average, 102.2%), much higher than the byproducts proportion in chemical products (generally < 3%). Since sediment is less affected by factors of atmospheric sedimentation, pollution levels are commonly used to analyze the sources of target pollutants (Zhao et al., 2018). Since the highest content for all chemicals in sediment was observed in sampling site 6, it is likely that the sewage outlet of the factories could be close to this site (Fig. 3, sediment). Except for sites 5, 6, and 15, the sediment content of TBBPA 5
1E+05
BPA MBBPA DBBPA TriBBPA TBBPA
1E+03
600
200
1E+02
1E+01
1E+00
1E-01
0 100
0 S1 S2 S3 S4 S5 S6 S7 S8 S9 S10 S11 S12 S13 S14 S15
S1 S2 S3 S4 S5 S6 S7 S8 S9 S10 S11 S12 S13 S14 S15
Sampling sites
Sampling Site 1E+06
BPA MBBPA DBBPA TriBBPA TBBPA
content
1E+05
Fig. 4. Variations of (MBBPA + DBBPA + TriBBPA) / TBBPA (top lines) and distribution ratios of BPA, MBBPA, DBBPA, TriBBPA and TBBPA (bar chart) in sediment, soil and water samples.
Soil
estuary compared with other sites. Therefore, these chemicals could be easily discharged into the Bohai Sea and elevate the exposure levels of marine organisms. TBBPA and its analogs have been determined in various organisms of the Bohai Sea, including fish, crustaceans, mollusks, octopus, and algae (Liu et al., 2015; Liu et al., 2016a). Rivers flowing through chemical parks constitute important and long-distance pollution sources for BPA analogs in the Bohai Sea. These chemicals possess higher log Koc values, preferring to adsorb onto fine particles. The mollusks and algae in the Bohai Sea can uptake these pollutants from the environment and transfer them to higher trophic levels (Zhu et al., 2012; Liu et al., 2016a). TBBPA and six byproducts displayed trophic dilution tendencies, indicating that these chemicals are prone to accumulation in organisms of low trophic levels (Liu et al., 2016a). Besides the direct discharge from the factories, the debromination of TBBPA in the environment is also an important source for TriBBPA, DBBPA, MBBPA, and BPA. It has been shown that TBBPA in sediment, sewage, and water, even during a waste-recycling process, can be degraded, with the number of transformation or degradation products of TBBPA reaching > 120, and with low debrominated products of MBBPA, DBBPA, and TriBBPA being the main transformation or degradation products (Liu et al., 2018b). TriBBPA was observed in a twofold higher concentration than TBBPA in breast milk, indicating that large amount of these analogs were generated from TBBPA in the human body (Akiyama et al., 2015). These less brominated analogs have been shown to promote adipocyte differentiation and elevate the lipid accumulation (Akiyama et al., 2015) indicating their potential health risks to human beings. Currently, many efforts have been concentrated on TBBPA and BPA. However, due to the lack of commercial standards, the environmental behaviors of the less brominated analogs are rarely reported.
1E+04
1E+03
1E+02
S1 S2 S3 S4 S5 S6 S7 S8 S9 S10S11S12S13S14S15
Sampling Site
BPA MBBPA DBBPA TriBBPA TBBPA
1E+07 1E+06
Content
800 sediment soil water
400
Relative abundance / %
Concentration
1E+04
TBBPA TriBBPA DBBPA MBBPA BPA
Water
MBBPA+DBBPA+TriBBPA)/TBBPA / %
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Sediment
1E+05 1E+04 1E+03 1E+02
4. Conclusion
1E+01 S1 S2 S3 S4 S5 S6 S7 S8 S9 S10S11S12S13S14S15
For the first time, the pollution levels and distribution characteristics of TBBPA, BPA, and their less brominated analogs in water, soil, and sediment along the tributary of Xiaoqing River to the estuary of the Bohai Sea were studied. The highest levels of TBBPA, BPA, MBBPA, DBBPA, and TriBBPA were found in sediment samples, indicating its major sink role for these contaminants. The backflow of seawater is likely the main reason for the minimal concentration fluctuation of these chemicals in water samples. Besides direct production pollution, a large proportion of MBBPA, DBBPA, and TriBBPA could arise from the debromination of TBBPA in the environment. Due to the properties of bioaccumulation, high levels of TBBPA and BPA discharged into the
Sampling Site Fig. 3. Comparison of TBBPA, BPA, MBBPA, DBBPA and TriBBPA in water (ng/ L), soil (ng/kg dw) and sediment (ng/kg dw) samples from 15 sampling sites.
BPA in surface soil. 3.4. Environmental implications The levels of TBBPA, BPA, and their brominated analogs were observed to be at high levels in the environment near the Bohai Sea 6
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Bohai Sea, as well as their degradation into TriBBPA, DBBPA, and MBBPA, would impose potential environmental risks. As a result of high pollution levels, these emerging contaminants in the Bohai Bay Area should be of concern given their great potential ecological risks to marine organisms.
Liu, A., Shi, J., Qu, G., Hu, L., Ma, Q., Song, M., Jing, C., Jiang, G., 2017. Identification of emerging brominated chemicals as the transformation products of tetrabromobisphenol A (TBBPA) derivatives in soil. Environ. Sci. Technol. 51, 5434–5444. Liu, A., Shi, J., Shen, Z., Lin, Y., Qu, G., Zhao, Z., Jiang, G., 2018a. Identification of unknown brominated bisphenol S congeners in contaminated soils as the transformation products of tetrabromobisphenol S derivatives. Environ. Sci. Technol. 52, 10480–10489. Liu, A., Zhao, Z., Qu, G., Shen, Z., Shi, J., Jiang, G., 2018b. Transformation/degradation of tetrabromobisphenol A and its derivatives: a review of the metabolism and metabolites. Environ. Pollut. 243, 1141–1153. Liu, A., Zhao, Z., Qu, G., Shen, Z., Liang, X., Shi, J., Jiang, G., 2019. Identification of transformation/degradation products of tetrabromobisphenol a and its derivatives. TrAC Trends Anal. Chem. 111, 85–99. Lu, Z., Letcher, R.J., Chu, S., Ciborowski, J.J.H., Haffner, G.D., Drouillard, K.G., MacLeod, S.L., Marvin, C.H., 2015. Spatial distributions of polychlorinated biphenyls, polybrominated diphenyl ethers, tetrabromobisphenol A and bisphenol A in Lake Erie sediment. J. Great Lakes Res. 41, 808–817. Malkoske, T., Tang, Y., Xu, W., Yu, S., Wang, H., 2016. A review of the environmental distribution, fate, and control of tetrabromobisphenol A released from sources. Sci. Total Environ. 569, 1608–1617. Morris, S., Allchin, C.R., Zegers, B.N., Haftka, J.J., Boon, J.P., Belpaire, C., Leonards, P.E., Van Leeuwen, S.P., De Boer, J., 2004. Distribution and fate of HBCD and TBBPA brominated flame retardants in North Sea estuaries and aquatic food webs. Environ. Sci. Technol. 38, 5497–5504. Nakao, T., Akiyama, E., Kakutani, H., Mizuno, A., Aozasa, O., Akai, Y., Ohta, S., 2015. Levels of tetrabromobisphenol A, tribromobisphenol A, dibromobisphenol A, monobromobisphenol A, and bisphenol A in Japanese breast milk. Chem. Res. Toxicol. 28, 722–728. Qian, Z., Xu, Y., Zheng, C., Zhang, A., Sun, J., 2019. Enhanced emissions of brominated flame retardants from indoor sources by direct contact with dust. Environ. Monit. Assess. 191. Qu, G., Liu, A., Wang, T., Zhang, C., Fu, J., Yu, M., Sun, J., Zhu, N., Li, Z., Wei, G., Du, Y., Shi, J., Liu, S., Jiang, G., 2013. Identification of tetrabromobisphenol A allyl ether and tetrabromobisphenol A 2,3-dibromopropyl ether in the ambient environment near a manufacturing site and in mollusks at a coastal region. Environ. Sci. Technol. 47, 4760–4767. Qu, G., Liu, A., Hu, L., Liu, S., Shi, J., Jiang, G., 2016. Recent advances in the analysis of TBBPA/TBBPS, TBBPA/TBBPS derivatives and their transformation products. TrACTrends in Analytical Chemistry 83 (Part B), 14–24. Ruan, T., Wang, Y., Wang, C., Wang, P., Fu, J., Yin, Y., Qu, G., Wang, T., Jiang, G., 2009. Identification and evaluation of a novel heterocyclic brominated flame retardant tris (2,3-dibromopropyl) isocyanurate in environmental matrices near a manufacturing plant in Southern China. Environ. Sci. Technol. 43, 3080–3086. Skledar, D.G., Masic, L.P., 2016. Bisphenol A and its analogs: do their metabolites have endocrine activity? Environ. Toxicol. Pharmacol. 47, 182–199. Srivastava, S., Gupta, P., Chandolia, A., Alam, I., 2015. Bisphenol A: a threat to human health? J. Environ. Health 77, 20–26. Yin, N., Liang, S., Liang, S., Yang, R., Hu, B., Qin, Z., Liu, A., Faiola, F., 2018. TBBPA and its alternatives disturb the early stages of neural development by interfering with the NOTCH and WNT pathways. Environ. Sci. Technol. 52, 5459–5468. Zhao, Z., Jia, J., Wang, J., Liu, A., Lan, J., Zhang, H., Zhao, M., 2018. Pollution levels of DDTs and their spatiotemporal trend from sediment records in the Southern Yellow Sea, China. Mar. Pollut. Bull. 127, 359–364. Zhao, X., Qiu, W., Zheng, Y., Xion, J., Gaao, C., Hu, S., 2019. Occurrence, distribution, bioaccumulation, and ecological risk of bisphenol analogues, parabens and their metabolites in the Pearl River Estuary, South China. Ecotoxicol. Environ. Saf. 180, 43–52. Zhu, N.L., Li, A., Wang, T., Wang, P., Qu, G.B., Ruan, T., Fu, J.J., Yuan, B., Zeng, L.X., Wang, Y.W., Jiang, G.B., 2012. Tris(2,3-dibromopropyl) isocyanurate, hexabromocyclododecanes, and polybrominated diphenyl ethers in mollusks from Chinese Bohai Sea. Environ. Sci. Technol. 46, 7174–7181.
Declaration of competing interest The authors declare that they have no conflicts of interest in this work. Acknowledgements This work was supported by the National Natural Science Foundation of China (21707148), State Key Laboratory of Environmental Chemistry and Ecotoxicology Open Fund (KF2016-12). We thank Lin Yongfeng and Ruan Ting from the Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, for their technical support. References Akiyama, E., Kakutani, H., Nakao, T., Motomura, Y., Takano, Y., Sorakubo, R., Mizuno, A., Aozasa, O., Tachibana, K., Doi, T., Ohta, S., 2015. Facilitation of adipocyte differentiation of 3T3-L1 cells by debrominated tetrabromobisphenol A compounds detected in Japanese breast milk. Environ. Res. 140, 157–164. Chu, S.G., Haffner, G.D., Letcher, R.J., 2005. Simultaneous determination of tetrabromobisphenol A, tetrachlorobisphenol A, bisphenol A and other halogenated analogues in sediment and sludge by high performance liquid chromatographyelectrospray tandem mass spectrometry. J. Chromatogr. A 1097, 25–32. Debenest, T., Gagne, F., Petit, A.N., Andre, C., Kohli, M., Blaise, C., 2010. Ecotoxicity of a brominated flame retardant (tetrabromobisphenol A) and its derivatives to aquatic organisms. Comp. Biochem. Physiol., C: Toxicol. Pharmacol. 152, 407–412. Guerra, P., Eljarrat, E., Barcelo, D., 2010. Simultaneous determination of hexabromocyclododecane, tetrabromobisphenol A, and related compounds in sewage sludge and sediment samples from Ebro River basin (Spain). Anal. Bioanal. Chem. 397, 2817–2824. He, M.-J., Luo, X.-J., Yu, L.-H., Wu, J.-P., Chen, S.-J., Mai, B.-X., 2013. Diasteroisomer and enantiomer-specific profiles of hexabromocyclododecane and tetrabromobisphenol A in an aquatic environment in a highly industrialized area, South China: vertical profile, phase partition, and bioaccumulation. Environ. Pollut. 179, 105–110. Howard, P.H., Muir, D.C.G., 2013. Identifying new persistent and bioaccumulative organics among chemicals in commerce. III: byproducts, impurities, and transformation products. Environmental Science & Technology 47, 5259–5266. Liu, A., Tian, Y., Yin, N., Yu, M., Qu, G., Shi, J., Du, Y., Jiang, G., 2015. Characterization of three tetrabromobisphenol-S derivatives in mollusks from Chinese Bohai Sea: a strategy for novel brominated contaminants identification. Sci. Rep. 5, 1–12. Liu, A.F., Qu, G.B., Yu, M., Liu, Y.W., Shi, J.B., Jiang, G.B., 2016a. TetrabromobisphenolA/S and nine novel analogs in biological samples from the Chinese Bohai Sea: implications for trophic transfer. Environ. Sci. Technol. 50, 4203–4211. Liu, K., Li, J., Yan, S., Zhang, W., Li, Y., Han, D., 2016b. A review of status of tetrabromobisphenol A (TBBPA) in China. Chemosphere 148, 8–20. Liu, Q., Ren, X., Long, Y., Hu, L., Qu, G., Zhou, Q., Jiang, G., 2016c. The potential neurotoxicity of emerging tetrabromobisphenol A derivatives based on rat pheochromocytoma cells. Chemosphere 154, 194–203.
7
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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Occurrence of bisphenol-A and its brominated derivatives in tributary and estuary of Xiaoqing River adjacent to Bohai Sea, China Jing Lana, Zhaoshuang Shenb, Wei Gaoc, Aifeng Liub,
T
⁎
a
Environmental Science and Engineering, Qingdao University, Qingdao 266071, China CAS Key Laboratory of Bio-based Materials, Qingdao Institute of Bioenergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao 266101, China c Research Center for Analytical Sciences, Department of Chemistry, College of Sciences, Northeastern University, Box 332, Shenyang 110819, China b
ARTICLE INFO
ABSTRACT
Keywords: Bisphenol-A Brominated bisphenol-A analogs Distribution Source Bohai Sea estuary Wetlands
The chemical industrial zone located along the Xiaoqing River wetlands adjacent to Bohai Sea is one of the largest production bases for brominated flame retardants in China. Herein, high levels of bisphenol-A, tetrabromobisphenol-A (TBBPA), tribromobisphenol-A, dibromobisphenol-A, and monobromobisphenol-A were detected in sediment, soil, and water samples of this zone in the range of below method detection limit (< MDL)–5.45 × 106 ng/kg dw, < MDL–8.37 × 104 ng/kg dw, and < MDL–5.59 × 102 ng/L, respectively. They were mainly buried in sediments as their highest levels in sediment samples. The small concentration fluctuation between water samples retrieved in the upstream and downstream zones is likely attributed to seawater backflow. The nearby chemical factories were point pollution sources and the less brominated analogs are largely from debromination of TBBPA. High pollution levels and the ecological risks of these pollutants along the Xiaoqing estuary to Bohai Sea need to be further assessed in future studies.
1. Introduction Bisphenol-A (BPA) is the raw material required for the production of polycarbonate, epoxy resin, and tetrabromobisphenol-A (TBBPA) and its derivatives. BPA and TBBPA have been detected in various environmental compartments, including soil, sediment, sludge, water, dust, air, food, and organisms of the Bohai Sea in China (Srivastava et al., 2015; Liu et al., 2016b; Malkoske et al., 2016). The TBBPA analog, tribromobisphenol-A (TriBBPA), was observed at twice the concentration of TBBPA in breast milk, indicating that debromination is an important metabolism pathway of TBBPA in the human body (Akiyama et al., 2015). Due to their endocrine disruption effects, thyroid hormone activities, and potential carcinogenicity, levels of BPA and TBBPA have caused much concern with regards to their pollution, health, and ecological risks (Srivastava et al., 2015; Liu et al., 2016c; Skledar and Masic, 2016; Yin et al., 2018). Like TBBPA, its less brominated analogs also display adverse effects. TriBBPA and dibromobisphenol-A (DBBPA) were shown to promote adipocyte differentiation (Akiyama et al., 2015). TriBBPA, DBBPA, and monobromobisphenol-A (MBBPA) were shown to be more toxic than TBBPA when tested with microtox and algal assays (Debenest et al., 2010). However, these analogs, created as byproducts or transformation and degradation products, have been scarcely studied with regards ⁎
to their environmental emergence and risks, likely due to the lack of available commercial standards (Qu et al., 2016; Liu et al., 2019). During production and usage, BPA, TBBPA, and various analogs are discharged into the environment, emerging as currently unknown pollutants. These chemicals and their related derivatives are mainly released from chemical factories and waste recycling. Additionally, impurities produced along with the chemical products can also be discharged into the environment. TriBBPA, a byproduct of TBBPA, accounts for 3% of the total production yield of TBBPA (Howard and Muir, 2013). Many mono-modified ether-linked TBBPA analogs have been identified as byproducts of TBBPA derivatives detected in soil, seaweed, mollusks, and fish, among other samples (Liu et al., 2016a; Liu et al., 2017; Liu et al., 2018a). Furthermore, a large amount of transformation or degradation products can be formed during the waste treatment process of the chemical products or by the metabolism of TBBPA and BPA in the environment. Through the photolysis, pyrolysis, chemical degradation, microbial degradation, and biological transformation of TBBPA (Liu et al., 2018b), > 120 degradation products have been identified, including TriBBPA, DBBPA, MBBPA, BPA, TBBPA sulfate, TBBPA glucuronide, TBBPA methyl ether, and brominated phenols. TriBBPA, DBBPA, and MBBPA, as the most important brominated analogs, have been determined in several compartments, including breast milk (Akiyama et al., 2015; Nakao et al., 2015), sewage sludge
Corresponding author. E-mail address: [email protected] (A. Liu).
https://doi.org/10.1016/j.marpolbul.2019.110551 Received 31 July 2019; Received in revised form 26 August 2019; Accepted 26 August 2019 Available online 05 September 2019 0025-326X/ © 2019 Elsevier Ltd. All rights reserved.
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(Chu et al., 2005), and sediment (Guerra et al., 2010; Lu et al., 2015). The chemical industrial zone of Shouguang City in Shandong Province, China, is one of the largest production bases for various brominated flame retardants (BFRs) worldwide. It is located between Xiaoqing River and its tributary, which flow through wetlands and salt marshes into the Bohai Sea. High levels of TBBPA (> 5.0 × 106 ng/kg dw), as well as of its derivatives and byproducts, have been found in soils collected near this area. Unfortunately, high levels have also been determined in organisms of the Bohai Sea. Furthermore, low brominated products, TriBBPA and DBBPA were also detected in soil samples from this zone. However, TriBBPA, DBBPA, and MBBPA were not quantified due to the lack of chemical standards. Wetlands and salt marshes play important roles as productive estuary ecosystems, acting not only as transition and buffering zones protecting the coastal lines from tidal waves but also serving as essential habitats for coastal wildlife such as fish and seabirds. Over the past few decades, land-derived contaminants from extensive anthropogenic activities have been increasingly transported, dissolved, and deposited in estuarine and coastal environments, strongly influencing regional environments. Furthermore, the BFR factories located along the tributary of Xiaoqing River could be the direct pollution source of the nearby river, wetland, and Bohai Sea (Ruan et al., 2009; Qu et al., 2013). However, to date, no data on their environmental levels and behavior in the tributary and estuaries has been reported. Herein, the levels of TBBPA, BPA, TriBBPA, DBBPA, and MBBPA in soil, water, and sediment samples collected along the tributary river flowing through the BFR factory zones have been determined. The pollution levels and distribution characteristics are assessed, and their pollution sources and environmental risks are discussed. The present results would contribute to the further understanding of the environmental fate and ecological toxicity of TBBPA and BPA.
tubes (ENVI™-carb, Supelclean™, 0.5 g, 6 mL) were used to further purify sediment samples. TriBBPA (97%), DBBPA (including two isomers, 2,6-DBBPA (98%) and 2,2′-DBBPA (97%)), and MBBPA (98%) were synthesized following the related literature (Nakao et al., 2015), purified, and characterized by high resolution mass spectrometry (HRMS) and 1H nuclear magnetic resonance (1H NMR). Chemicals with a purity lower than 95% were further purified by HPLC. The detailed synthesis routines were as described below. 2.2.1. MBBPA, 2,2′-DBBPA, and TriBBPA BPA was dissolved in 5 mL of ethanol, into which a solution of pyridinium tribromide (in 10 mL in ethanol) was slowly added. The molar ratio of pyridinium tribromide to BPA was 1.5:1 (for MBBPA) and 4:1 (for 2,2′-DBBPA and TriBBPA). Following maintenance of the reaction at room temperature for 1.5 h, thin layer chromatography of the products showed the disappearance of BPA. The reaction mixture was diluted with 200 mL of water and extracted three times with 200 mL of ethyl acetate. The organic phase was combined and dried with anhydrous sodium sulfate. After concentration, the residue was purified by silica gel column chromatography (petroleum ether:ethyl acetate = 4:1) to obtain MBBPA at a yield of 85% and purity of 98%, and 2,2′-DBBPA and TriBBPA at yield of 78% and 75%, and purity of 97% and 97%, respectively. The products were further characterized by 1 H NMR and HRMS and used as the standards. 2.2.2. 2,6-DBBPA One of the hydroxyl groups of BPA was protected by reaction with 2-bromopropane in acetone to promote the bromination of BPA at one benzene ring. A sodium hydroxide solution (3.5 M) was carefully added to the reaction mixture and stirred vigorously for 5 h. The purified BPA mono(propyl ether) was then reacted with pyridinium tribromide (molar ratio 1:1) in ethanol to generate 2,6-dibrominated BPA mono (propyl ether). Finally, the protection group was removed by adding BCl3 solution (molar ratio 1:10, in deoxidized and dehydrated DCM) and ethyl mercaptan (molar ratio 1:2.5) in an ice-salt bath. The reaction mixture was stirred overnight and monitored by thin layer chromatography. At the reaction endpoint, the mixture was diluted with 200 mL of saturated sodium thiosulfate ice water and extracted three times with 200 mL of ethyl acetate. After concentration, the residue was purified using silica gel column chromatography (petroleum ether: ethyl acetate = 4:1) to generate 2,6-dibromobisphenol-A at a yield of 90% with a purity of 98%.
2. Materials and methods 2.1. Sampling Soil, sediment, and water samples were collected from along the tributary of Xiaoqing River (Zhangseng River) near the estuary to Bohai Sea (Fig. 1) in Shouguang City, Shandong Province, China. Along the river, there is a small area of wetland covered with reeds and other water plants. The river crosses a chemical park where several large BFR factories are located (near sampling sites 5, 6, and 7 in Fig. 1). The total annual output of TBBPA related to these BFR factories has been stated to be over 70,000 tones (Liu et al., 2017). The Zhangseng River merges with the Xiaoqing River near site 14, and sites 12, 13, and 14 are located in an estuary wetland near a salt field (Fig. 1). Site 15 is located near the entrance to the Bohai Sea. When the tide rises, the sampling river is often irrigated backwards, which occurred during sampling. Surface soil (0–5 cm), river water, and sediment samples were simultaneously collected at each sampling site, and the distance between two adjacent sampling sites was ~2 km. The soil and sediment samples were freeze dried, filtered through a stainless-steel grid (100 mesh), and stored at −20 °C before sample preparation. Water samples were stored at −20 °C after being transported to the laboratory and were liquidliquid extracted within 5 days.
2.3. Instrument parameters of Orbitrap-HRMS Ultra-HPLC (UHPLC, Ultimate 3000) coupled with Orbitrap Fusion Tribrid mass spectrometry (Orbitrap HRMS, Thermo Fisher Scientific, USA) was used for qualitative and quantitative analysis. An Agilent chromatography column ZORBAX ODS (150 × 3.0 mm, 2.5 μm) was used for target chemical separation. The injection volume was 10 μL for each sample and the flow rate was 0.6 mL/min with methanol (A) and water (B) as the mobile phases. The elution program was started as 60/ 40 (A/B) and kept for 3 min, reaching 90/10 (A/B) in 7 min, 100% A in 8 min and kept for 4 min, and finally returned to 60/40 (A/B) in 0.1 min and kept for 4.9 min. Heated electrospray ionization (ESI) was selected for HRMS analysis under a negative mode and collected parent ions in full scan range (m/z), from 100 to 1000. High-energy collisional dissociation was used to fragment the parent ions. The parameters of HRMS followed the recommended values of the equipment, as described elsewhere (Liu et al., 2017).
2.2. Chemicals and materials BPA (≥99%) and TBBPA (≥97%) were obtained from SigmaAldrich. The standard chemicals were dissolved in methanol at a concentration of 100 μg/mL and stored in a refrigerator at 4 °C. High-performance liquid chromatography (HPLC) grade methanol, acetone, dichloromethane (DCM), and hexane were obtained from Merck & Fisher Scientific Co. Deionized water was prepared by a Milli-Q advantage system. Biobeads (S-X3, BIO-RAD) were used as the package materials for gel permeation chromatography (GPC). Solid phase extraction (SPE)
2.4. Sample pretreatment The soil/sediment samples (2.0 g), which had been mixed with anhydrous sodium sulfate (5 g) and isotope-labeled surrogates (D10TBBPA, 20 ng and 13C12-BPA, 20 ng), were extracted with methanol 2
Marine Pollution Bulletin 149 (2019) 110551
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Fig. 1. Map of the sampling sites (sites 1–15) for the surface soils, waters and sediments.
is the location of BFR factory.
(30 mL) three times (20 min per time). The combined supernatant was concentrated by rotary evaporator and solvent exchanged to 1 mL of hexane/DCM (1/1, v/v) for GPC (38 × 2.5 cm i.d.) cleanup. Following sample loading, the GPC column was eluted with hexane/DCM (1/1, v/ v). The initial 100 mL eluted were discarded, and the following 200 mL were collected and concentrated by rotary evaporator. For soil samples, the purified substances were re-dissolved in 1 mL of methanol for instrument analysis. For sediment samples, the purified substances were re-dissolved in 1 mL of hexane/DCM (1/1, v/v) and further purified by an ENVI-Carb™ (500 mg, 6 mL) SPE cartridge. The ENVI-Carb cartridge was balanced by 5 mL of acetone, 5 mL of DCM, and 5 mL of hexane, in that order. The sample was loaded and the cartridge was eluted with 10 mL of acetone (containing 0.5% NH3·H2O), which was concentrated with N2 and re-dissolved in 1 mL of methanol for analysis. The water samples (200 mL) were filtered through a glass fiber filter and the pH was adjusted between 4 and 6 by HCl (1 M). The isotopelabeled surrogates (D10-TBBPA, 20 ng and 13C12-BPA, 20 ng) were then added. Finally, the sample was liquid-liquid extracted three times by DCM (50 mL). The combined extracts were rotary evaporated and redissolved in 1 mL of methanol.
spectrum and the fragmentation mass spectrum data of these chemicals were further confirmed by comparison to the reported data (Chu et al., 2005; Nakao et al., 2015). Following sample extraction and clean-up, the recoveries of TBBPA, TriBBPA, DBBPA, and MBBPA ranged from 78% to 95%. The method detection limits (MDLs) ranged from 0.02 to 3 ng/g dw for the soil/sediment samples, and ranged from 0.2 to 30 ng/ L for water samples. The matrix disturbance effects were < 10%. The recoveries of isotope-labeled surrogates in the sample were higher than 90%, indicating the practicality of the method. A blank sample was treated with every batch of environmental samples (every 10 samples) to avoid cross-contamination.
2.5. Quality control and quality assurance
3.1. Identification of BPA, MBBPA, DBBPA, TriBBPA, and TBBPA
The synthesized chemicals were purified by column chromatography and HPLC chromatography and characterized by 1H NMR and HRMS. The target chemicals were identified with Orbitrap HRMS at a resolution of 120,000 and mass error of < 3 ppm. The full scan mass
Due to the lack of commercial standards for the identification of MBBPA, 2,6-DBBPA, 2,2′-DBBPA, and TriBBPA, herein, these were synthesized in high purity (> 97%) and identified by Orbitrap HRMS. The precision and sensitivity of the method benefitted from the high
2.6. Statistical analyses The raw data was transformed to figures using Origin 9.0, which was also used for Spearman's rank correlation test. When the p value of the test was below 0.05, the linear regression between the two tested variables was regarded as significant. 3. Results and discussion
3
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Table 1 Chemical information of TBBPA, BPA and their analogs. Chemicals
Structure
Molecular formula
HRMS Found m/z for [M − H]−
Isotope ratio
Mass error
TBBPA
C15H12O2Br4
538.75006/540.74799/542.74579/544.74365/546.74146
1:4:6:4:1 (Br)
0.476
TriBBPA
C15H13O2Br3
460.83942/462.83731/464.83511/466.83301
1:3:3:1 (Br)
0.280
DBBPA
C15H14O2Br2
382.92880/384.92667/386.92453
1:2:1 (Br)
0.057
MBBPA
C15H15O2Br
305.01819/307.01614
1:1 (Br)
−0.248
BPA
C15H16O2
227.10760/228.11090
5.9:1 (13C)
−0.674
Notes: m/z labeled in bold was used as quantitative ions; m/z labeled in italics was used as qualitative ions.
content ranged within 1.16 × 103 to 2.53 × 105 ng/kg dw (average 4.43 × 104 ng/kg dw), 1.49 × 102 to 9.71 × 104 ng/kg dw (average 2.26 × 104 ng/kg dw), and < MDL to 5.23 × 104 ng/kg dw (average 9.62 × 103 ng/kg dw) for TriBBPA, DBBPA, and MBBPA, respectively. In soil, their content ranged within 1.05 × 102 to 2.23 × 104 ng/kg dw (average 4.79 × 103 ng/kg dw), 7.60 to 3.28 × 103 ng/kg dw (average 1.31 × 103 ng/kg dw), and < MDL to 2.81 × 103 ng/kg dw (average 1.18 × 103 ng/kg dw) for TriBBPA, DBBPA, and MBBPA, respectively. In water, their concentration ranged from within < MDL to 2.05 × 102 ng/L (average 3.83 ng/L), < MDL to 1.48 × 102 ng/L (average 48.2 ng/L), and < MDL to 13.1 ng/L (average 5.2 ng/L) for TriBBPA, DBBPA, and MBBPA, respectively. In sediment, the target concentrations were observed to decrease in concentration in the order of BPA > TBBPA > TriBBPA > DBBPA > MBBPA, as observed in sewage sludge samples from Ontario, Canada, but their sediment levels were much higher than that in the sludge samples (Chu et al., 2005). The detection frequencies of TriBBPA and DBBPA were all 100% in sediment and soil samples, much higher than that in water samples. Furthermore, MBBPA had the lowest detection frequencies in all samples, with 73% in sediment, 60% in soil, and 47% in water samples. All the collected samples displayed higher levels and detection frequencies for TriBBPA, DBBPA, and MBBPA than that in many mediums worldwide, for example, sewage sludge and sediment samples from a waste water treatment plant in Canada (not detectable to 560 ng/g dw, 7.1–50.0%) (Guerra et al., 2010), milk samples (< MDL to 253 ng/L, 0–100%) (Akiyama et al., 2015; Nakao et al., 2015), or sediment from Lake Erie in Canada (< 0.04 ng/g dw). The much higher levels observed are expected given the location of the nearby factories, which act as an important direct pollution source. The total content of the six chemicals in sediment were much higher than in soil and in water. Thus, the results indicate that BPA and TBBPA tend to accumulate in sediments and soils, as they are prone to adsorbing onto the fine particles (Qian et al., 2019; Zhao et al., 2019). Csediment/Cwater for BPA and TBBPA were in the ranges of 3.0 to 1.10 × 104 (average 1.11 × 103, media 1.40 × 102) and 3.55 to 2.27 × 105 (average 1.94 × 104, media 3.14 × 103), respectively. Further, a greater amount of TBBPA tended to absorb onto the sediment than BPA, likely due to its higher soil sorption coefficient (Koc) value (TBBPA, log Koc = 5.24, vs. BPA, log Koc = 3.10) (Liu et al., 2015). Additionally, the higher water solubility and lower octanol/water partition coefficient (Kow) value (log Kow, 3.64) of BPA could be the reasons for the higher proportion of BPA than TBBPA (log Kow, TBBPA, 7.20) in water.
resolution of HRMS. The isotopic abundance ratios, accurate m/z values of the targets, and their retention times in mass chromatography can be used as the typical characteristics to identify target chemicals from the full scan spectra of samples. The isotope ratios indicated the number of bromine atoms in the molecule, and thus target chemicals containing 4, 3, 2, and 1 bromine atoms presented with isotope ratios of 1:4:6:4:1, 1:3:3:1, 1:2:1, and 1:1, respectively. These target chemicals were determined using the most abundant isotopic peak of [M − H]− in HRMS spectra as the quantitative ion and the adjacent isotopic ions as qualitative ions (Table 1). The mass errors for the observed m/z values of the target chemicals were all < 1 ppm. BPA, MBBPA, DBBPA (both 2,2′DBBPA and 2,6-DBBPA), TriBBPA, and TBBPA were detected at 3.6, 5.8, 7.6, 8.9, and 10.1 min, respectively. Due to the same mass spectra and retention time of two isomers of DBBPA, 2,6-DBBPA and 2,2′DBBPA were determined by the total amount of these two isomers. For BPA, the most abundant mass peak at m/z 227.10760 was used for quantification, and its 13C isotopic peak at m/z 228.11090 was used for qualitative analysis. 3.2. Environmental levels in sediment, soil, and water samples Both BPA and TBBPA were detected in all the collected samples. BPA was detected in the range of 1.03 × 103 to 5.45 × 106 ng/kg dw in sediment (average 5.21 × 105 ng/kg dw), 1.85 × 102 to 1.87 × 104 ng/ kg dw in soil (average 4.61 × 103 ng/kg dw), and 2.73 × 102 to 5.59 × 102 ng/L in water (average 4.15 × 102 ng/L) (Fig. 2). TBBPA was detected in ranges of 2.08 × 103 to 1.35 × 106 ng/kg dw in sediment (average 2.61 × 105 ng/kg dw), 2.63 × 102 to 8.37 × 104 ng/kg dw in soil (average 1.79 × 104 ng/kg dw), and 6.0–1.13 × 102 ng/L in water (average 37.1 ng/L) (Fig. 2). The BPA and TBBPA content in sediment was similar and much higher than other chemical contents in sediment. The levels of TBBPA in sediment were comparable to those in estuaries in the Netherlands and England (< 0.1–9750 μg/kg) (Morris et al., 2004) and higher than those in sediments of the aquatic environment of south China (0.19–82.3 ng/g dw) (He et al., 2013). The TBBPA content in soil along the tributary of Xiaoqing River adjacent to the Bohai Sea were lower than those in the chemical park (< MDL–4.10 × 108 ng/kg dw) (Liu et al., 2017). These observations were attributed to the production, transport, and unorganized discharge of BPA and TBBPA related to BFRs, resulting in a higher concentration near the BFR factories than in other sampling sites (Fig. 3). The less brominated BPA analogs were observed at lower levels than BPA and TBBPA in the respective samples (Fig. 2). In sediment, their 4
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Fig. 2. Sample concentrations of BPA, TBBPA and other analogs in sediment and soil (ng/kg dw), water (ng/L). The concentration of 25th and 75th percentiles is represented by box, the median concentration is represented by middle line, the mean concentration is represented by “□”, The whiskers extending from the box are the lowest and highest non-outlier values. “×” represents the outlier value.
1E+06 1E+05
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PA -s
ed i B me P B A- nt PA s M -w oil B B at PA er -s M ed Q1 M BB ime B PA n B PA -s t D -w oil B B at PA er -s e R D di 1 D BB me B PA n B PA -s t Tr iB -w oil B at PA er -s Tr ed S Tr iBB im 1 iB P en B A- t PA s TB -w oil B at PA er -s e TB di T1 TB BP me B A- nt PA s -w oil at er
1E-02
3.3. Distribution characteristics along the river to estuary of Bohai Sea
showed an overall trend of gradual reduction along the Zhangseng River to Bohai Sea. The same results were also observed for BPA, MBBPA, DBBPA, and TriBBPA, suggesting that pollution sources were single and likely from water transport of sewage disposal. Site 15 and its adjacent area might be the deposit accumulation area for terrestrial source pollutants. Besides the direct pollution from the factories, a large amount of transformation products can also be generated from the chemical products, e.g., debromination is the main degradation pathway for anaerobic degradation of TBBPA (Liu et al., 2018b). The debromination products were low brominated BPA, including TriBBPA, DBBPA, and MBBPA, with BPA as the terminal product. Values of (TriBBPA + DBBPA + MBBPA) / TBBPA in 15 sediment samples were of 7.5–151.8% (average, 36.6%), indicating that some transformation products were likely to be from debromination of TBBPA in sediment. Meanwhile, significant Spearman correlations (p < 0.05) were observed for sedimental TBBPA, TriBBPA, DBBPA, MBBPA, and BPA, indicating that they could arise from the same pollution sources and in situ generation of low debromination products in sediment. Environmental conditions can obviously affect the debromination of TBBPA. Values of (TriBBPA + DBBPA + MBBPA) / TBBPA in 8 water samples were higher than in soil and sediment samples of the same sites (Fig. 4), while values in 5 soil samples were higher than in water and sediment samples of the same sites. These results are consistent with the degradation rate of TBBPA under different conditions, e.g., a water phase (lower TBBPA concentration) and oxic conditions facilitate the transformation of TBBPA (Liu et al., 2018b). In water samples, BPA accounted for the largest proportion of chemicals, while TBBPA accounted for the largest proportion in soil and sediment samples (Fig. 4). These observations are in good agreement with the quick debromination of TBBPA in water. In soil and sediment samples, the proportion of each analyte in their total amount was in the order of MBBPA < DBBPA < TriBBPA < TBBPA, corresponding to the gradual debromination degradation of TBBPA. BPA was the second largest composition in sediment which was relevant to the complete debromination of TBBPA. The second largest composition is TriBBPA rather than BPA in most of soil samples which may be likely due to further oxidation of
In water samples, the highest concentration of BPA was 5.60 × 102 ng/L, which was also the highest concentration for the chemicals observed in all the 15 water samples (Fig. 3). The average concentration values were in the order of BPA > TBBPA > DBBPA > TriBBPA > MBBPA. In all sites, TriBBPA, DBBPA, and MBBPA presented similar levels. Additionally, BPA, TBBPA, TriBBPA, DBBPA, and MBBPA in water samples showed no significant differences along the river towards the Bohai Sea (Fig. 3). The Spearman correlation analysis also presented no significant correlations (p > 0.05) between these concentrations. Values of (TriBBPA + DBBPA + MBBPA) / TBBPA in 15 water samples were 8.0–721.5% (average, 227.2%) (Fig. 4), indicating a large proportion of these less brominated analogs could be derived from TBBPA. In soil samples, the highest content of TBBPA was of 8.37 × 104 ng/ kg dw in most sampling site of S1 (Fig. 3). The average values presented in the order of TBBPA > BPA > TriBBPA > DBBPA > MBBPA. Along the river flow direction all the targets in soil samples generally presented a decreasing concentration trend. TBBPA, TriBBPA, and DBBPA presented significant correlations (p < 0.05) between each other, indicating that they shared the pollution sources. Compared with sediment and water samples, the accumulation of contaminants in soils can be affected by more factors such as factory dust, wind direction, atmosphere settlement, soil adsorption ability, etc. Soil samples of sampling sites 2, 3, and 5 (near the factories) presented higher concentrations, corresponding to the possible dust from the factories. Values of (TriBBPA + DBBPA + MBBPA) / TBBPA in 15 soil samples were within the range 5.9–394.6% (average, 102.2%), much higher than the byproducts proportion in chemical products (generally < 3%). Since sediment is less affected by factors of atmospheric sedimentation, pollution levels are commonly used to analyze the sources of target pollutants (Zhao et al., 2018). Since the highest content for all chemicals in sediment was observed in sampling site 6, it is likely that the sewage outlet of the factories could be close to this site (Fig. 3, sediment). Except for sites 5, 6, and 15, the sediment content of TBBPA 5
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Fig. 4. Variations of (MBBPA + DBBPA + TriBBPA) / TBBPA (top lines) and distribution ratios of BPA, MBBPA, DBBPA, TriBBPA and TBBPA (bar chart) in sediment, soil and water samples.
Soil
estuary compared with other sites. Therefore, these chemicals could be easily discharged into the Bohai Sea and elevate the exposure levels of marine organisms. TBBPA and its analogs have been determined in various organisms of the Bohai Sea, including fish, crustaceans, mollusks, octopus, and algae (Liu et al., 2015; Liu et al., 2016a). Rivers flowing through chemical parks constitute important and long-distance pollution sources for BPA analogs in the Bohai Sea. These chemicals possess higher log Koc values, preferring to adsorb onto fine particles. The mollusks and algae in the Bohai Sea can uptake these pollutants from the environment and transfer them to higher trophic levels (Zhu et al., 2012; Liu et al., 2016a). TBBPA and six byproducts displayed trophic dilution tendencies, indicating that these chemicals are prone to accumulation in organisms of low trophic levels (Liu et al., 2016a). Besides the direct discharge from the factories, the debromination of TBBPA in the environment is also an important source for TriBBPA, DBBPA, MBBPA, and BPA. It has been shown that TBBPA in sediment, sewage, and water, even during a waste-recycling process, can be degraded, with the number of transformation or degradation products of TBBPA reaching > 120, and with low debrominated products of MBBPA, DBBPA, and TriBBPA being the main transformation or degradation products (Liu et al., 2018b). TriBBPA was observed in a twofold higher concentration than TBBPA in breast milk, indicating that large amount of these analogs were generated from TBBPA in the human body (Akiyama et al., 2015). These less brominated analogs have been shown to promote adipocyte differentiation and elevate the lipid accumulation (Akiyama et al., 2015) indicating their potential health risks to human beings. Currently, many efforts have been concentrated on TBBPA and BPA. However, due to the lack of commercial standards, the environmental behaviors of the less brominated analogs are rarely reported.
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1E+01 S1 S2 S3 S4 S5 S6 S7 S8 S9 S10S11S12S13S14S15
For the first time, the pollution levels and distribution characteristics of TBBPA, BPA, and their less brominated analogs in water, soil, and sediment along the tributary of Xiaoqing River to the estuary of the Bohai Sea were studied. The highest levels of TBBPA, BPA, MBBPA, DBBPA, and TriBBPA were found in sediment samples, indicating its major sink role for these contaminants. The backflow of seawater is likely the main reason for the minimal concentration fluctuation of these chemicals in water samples. Besides direct production pollution, a large proportion of MBBPA, DBBPA, and TriBBPA could arise from the debromination of TBBPA in the environment. Due to the properties of bioaccumulation, high levels of TBBPA and BPA discharged into the
Sampling Site Fig. 3. Comparison of TBBPA, BPA, MBBPA, DBBPA and TriBBPA in water (ng/ L), soil (ng/kg dw) and sediment (ng/kg dw) samples from 15 sampling sites.
BPA in surface soil. 3.4. Environmental implications The levels of TBBPA, BPA, and their brominated analogs were observed to be at high levels in the environment near the Bohai Sea 6
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Bohai Sea, as well as their degradation into TriBBPA, DBBPA, and MBBPA, would impose potential environmental risks. As a result of high pollution levels, these emerging contaminants in the Bohai Bay Area should be of concern given their great potential ecological risks to marine organisms.
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Declaration of competing interest The authors declare that they have no conflicts of interest in this work. Acknowledgements This work was supported by the National Natural Science Foundation of China (21707148), State Key Laboratory of Environmental Chemistry and Ecotoxicology Open Fund (KF2016-12). We thank Lin Yongfeng and Ruan Ting from the Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, for their technical support. References Akiyama, E., Kakutani, H., Nakao, T., Motomura, Y., Takano, Y., Sorakubo, R., Mizuno, A., Aozasa, O., Tachibana, K., Doi, T., Ohta, S., 2015. Facilitation of adipocyte differentiation of 3T3-L1 cells by debrominated tetrabromobisphenol A compounds detected in Japanese breast milk. Environ. Res. 140, 157–164. Chu, S.G., Haffner, G.D., Letcher, R.J., 2005. Simultaneous determination of tetrabromobisphenol A, tetrachlorobisphenol A, bisphenol A and other halogenated analogues in sediment and sludge by high performance liquid chromatographyelectrospray tandem mass spectrometry. J. Chromatogr. A 1097, 25–32. Debenest, T., Gagne, F., Petit, A.N., Andre, C., Kohli, M., Blaise, C., 2010. Ecotoxicity of a brominated flame retardant (tetrabromobisphenol A) and its derivatives to aquatic organisms. Comp. Biochem. Physiol., C: Toxicol. Pharmacol. 152, 407–412. Guerra, P., Eljarrat, E., Barcelo, D., 2010. Simultaneous determination of hexabromocyclododecane, tetrabromobisphenol A, and related compounds in sewage sludge and sediment samples from Ebro River basin (Spain). Anal. Bioanal. Chem. 397, 2817–2824. He, M.-J., Luo, X.-J., Yu, L.-H., Wu, J.-P., Chen, S.-J., Mai, B.-X., 2013. Diasteroisomer and enantiomer-specific profiles of hexabromocyclododecane and tetrabromobisphenol A in an aquatic environment in a highly industrialized area, South China: vertical profile, phase partition, and bioaccumulation. Environ. Pollut. 179, 105–110. Howard, P.H., Muir, D.C.G., 2013. Identifying new persistent and bioaccumulative organics among chemicals in commerce. III: byproducts, impurities, and transformation products. Environmental Science & Technology 47, 5259–5266. Liu, A., Tian, Y., Yin, N., Yu, M., Qu, G., Shi, J., Du, Y., Jiang, G., 2015. Characterization of three tetrabromobisphenol-S derivatives in mollusks from Chinese Bohai Sea: a strategy for novel brominated contaminants identification. Sci. Rep. 5, 1–12. Liu, A.F., Qu, G.B., Yu, M., Liu, Y.W., Shi, J.B., Jiang, G.B., 2016a. TetrabromobisphenolA/S and nine novel analogs in biological samples from the Chinese Bohai Sea: implications for trophic transfer. Environ. Sci. Technol. 50, 4203–4211. Liu, K., Li, J., Yan, S., Zhang, W., Li, Y., Han, D., 2016b. A review of status of tetrabromobisphenol A (TBBPA) in China. Chemosphere 148, 8–20. Liu, Q., Ren, X., Long, Y., Hu, L., Qu, G., Zhou, Q., Jiang, G., 2016c. The potential neurotoxicity of emerging tetrabromobisphenol A derivatives based on rat pheochromocytoma cells. Chemosphere 154, 194–203.
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