Occurrence and congener profiles of polybrominated diphenyl ethers in green mussels (Perna viridis) collected from northern South China Sea and the associated potential health risk

Science of the Total Environment 698 (2020) 134276

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Occurrence and congener profiles of polybrominated diphenyl ethers in green mussels (Perna viridis) collected from northern South China Sea and the associated potential health risk Runxia Sun a, Changgui Pan b,c,⁎, Qing X. Li d, Fengjiao Peng e, Bixian Mai f a

School of Marine Sciences, Nanjing University of Information Science and Technology, Nanjing, 210044, China School of Marine Sciences, Guangxi University, Nanning 530004, China c Guangxi Laboratory on the Study of Coral Reefs in the South China Sea, Guangxi University, Nanning 530004, China d Department of Molecular Biosciences and Bioengineering, University of Hawaii at Manoa, 1955 East-West Road, Honolulu, HI 96822, USA e Department of Population Health, Luxembourg Institute of Health, 1A-B, Rue Thomas Edison, L-1445 Strassen, Luxembourg f State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China b

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

• A comprehensive investigation of PBDEs in green mussels from South China is reported. • PBDES were ubiquitous in green mussels from South China. • PBDE levels and congener profiles varied by geographical location. • BDE-47 and BDE-209 were the predominant PBDE congeners in green mussels. • BDE 47, 99, 153 and 209 in green mussel suggest no health risks for the consumers.

a r t i c l e

i n f o

Article history: Received 17 July 2019 Received in revised form 2 September 2019 Accepted 3 September 2019 Available online 03 September 2019 Editor: Shuzhen Zhang Keywords: Polybrominated diphenyl ethers PBDE Perna viridis Pollution source Congener profile Health risk

a b s t r a c t Polybrominated diphenyl ether (PBDE) contamination has become a major concern over the effects on human health. In the present study, we collected widely consumed green mussels (Perna viridis) samples from the northern South China Sea (NSCS) to investigate the occurrence, spatial distribution, congener profiles as well as potential risk of 18 PBDEs. All the target PBDEs were detected in green mussel samples, indicating their ubiquitous distribution. The concentrations of the total 18 PBDES (ΣPBDEs) in all samples varied from 6.96 to 55.6 ng/g lipid weight (lw), with BDE-47 and BDE-209 being the predominant PBDE congeners. Overall, the ΣPBDEs pollution in green mussels from NSCS was at a moderate to high level in comparison with the PBDEs pollution worldwide. The dietary exposure of the local population in South China to PBDEs via consuming green mussels was estimated to be 0.30–0.80 ng/kg body weight (bw)/day. Evaluation of the exposure risk for BDE-47, 99, 153 and 209 indicated that health risks due to green mussel consumption are substantially lower than the U.S. EPA minimum concern level. © 2019 Elsevier B.V. All rights reserved.

⁎ Corresponding author at: School of Marine Sciences, Guangxi University, Nanning 530004, China E-mail address: [email protected] (C. Pan).

https://doi.org/10.1016/j.scitotenv.2019.134276 0048-9697/© 2019 Elsevier B.V. All rights reserved.

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R. Sun et al. / Science of the Total Environment 698 (2020) 134276

1. Introduction Polybrominated diphenyl ethers (PBDEs) are a group of synthetic chemicals with a common structure of a brominated diphenyl ether molecule that may have anywhere from one to ten bromine atoms attached. In total, there are 209 theoretical PBDE congeners. These chemicals are brominated flame retardants (BFRs) used as additives in a wide range of manufactured products, including furnishings, textiles, paints, carpets, sofas, polymers, and electronic equipment (de Wit, 2002; Alaee et al., 2003). There are three major PBDE commercial mixtures: penta-, octa- and deca-brominated diphenyl ether (BDE) (Alaee et al., 2003). The estimated annual consumption of commercial decaBDE ranges from 20,000 to 40,000 tons in China (Li et al., 2014). Because these chemicals are not chemically bound to products, they can easily be released into the surrounding environment (EFSA, 2011). Due to their environmental persistence, lipophilicity and bioaccumulation characteristics, PBDEs have become ubiquitous in various matrices, including water, air, sediment, soil, biota and even in the human (Li et al., 2016; Xiong et al., 2016; Parry et al., 2018; Markham et al., 2018; Chai et al., 2019, Naidu, 2019). Studies have suggested potential association of some PBDE congeners with the inhibition of cell division, genotoxicity, thyroid, reproductive, developmental, hepatotoxic, immunological and endocrinological effects, etc. (Gascon et al., 2011; Ji et al., 2011; Su et al., 2014; Wang et al., 2015b; Xu et al., 2015; Glazer et al., 2018; Tang et al., 2018; Zhao et al., 2019, Naidu, 2019). Because of their unique characteristics and detrimental health effects, production of penta- and octa-BDE formulations was first phased-out in the U.S. in 2004 (Renner, 2004). These compounds have been listed as persistent organic pollutants (POPs) in the Stockholm Convention (Stockholm Convention, 2009). The most widely used PBDE formulation, deca-BDE, was banned in the European Union in 2008 (Betts, 2008). Although the mass production and usage of these PBDEs have been banned, a considerable number of products containing PBDE congeners are still available on the market. Moreover, deca-BDE is still being used in many Asian countries, such as China (Wang et al., 2016). The green mussel, Perna viridis, is medium-sized edible marine bivalve mollusk which lives in subtropical/tropical area. They are consumed by humans globally for their high protein, omega-3 polyunsaturated fatty acids (PUFAs), and carbohydrates (Grienke et al., 2014). They are sessile filter-feeders and can be used a bioindicator for water pollution in the coastal and estuarine areas due to their wide distribution and availability in the whole year (Vasanthi et al., 2012). However, green mussels have a limited ability to metabolize contaminants and can accumulate them to high levels exceeding those found in surrounding environment (Vasanthi et al., 2017). As a result, they may become a source of pollutants and subsequently pose potential risks to human through dietary exposure (Sharma et al., 2014). This mussel has been widely used as a bioindicator for many years in various countries worldwide for legacy contaminants, such as polychlorinated biphenyls (PCBs), dichlorodiphenyltrichloroethanes (DDTs) and PBDEs (Monirith et al., 2003; Ramu et al., 2007; Sundar et al., 2010) and more recently extended to various contaminants of emerging concern, such as pharmaceutically active compounds and microplastics (Bayen et al., 2016; Naidu, 2019). It is the ideal species for marine pollution monitoring and important for the research of biogeochemical cycle of persistent organic pollutants, fishery environment and quality of aquatic product. The South China Sea (SCS), located between 3 and 25° N and 102–122° E, is a marginal sea. The northern South China Sea (NSCS) is an important marine aquaculture production base in China. Additionally, NSCS is adjacent to Pearl River Delta (PRD), which is one of the largest manufacturing bases for PBDE-related (electronic/electrical) products as well as the largest dumping sites of e-waste in the world (Sun et al., 2012). The riverine and atmospheric inputs, as well as high density of population with a legacy of rapid industrial development

result in the NSCS a hotspot of pollution (Sun et al., 2015a). For example, several booming e-waste dismantling stations have been located in Guangdong province, where PBDEs have been extensively detected with high levels in soils, sediment and water samples (Zhang et al., 2013). Dietary intake has been estimated to be the main exposure pathway for PBDE in human (Fromme et al., 2009). Fish and shellfish have relatively higher PBDEs contents than other foodstuffs (Bocio et al., 2003; Domingo, 2012; Trabalón et al., 2017). Actually, mussel consumption has been proven to be one of the main pathways of human exposed to PBDEs (Bocio et al., 2003). Therefore, it is required to assess the potential human health risk of PBDEs via mussel consumption. Monitoring of PBDEs in blue and green mussels has been reported in some areas in the world, such as China, France, Japan, Korea, and Malaysia (Ramu et al., 2007). Meanwhile, many studies have been performed on PBDE pollution in SCS with focus on sediments, water and fish samples (Mai et al., 2005; Lam et al., 2009). However, there is limited knowledge of PBDEs in green mussels and the associated human exposure risk. The objectives of the present study were to 1) investigate the contamination levels and profiles of 18 PBDE congeners and their spatial distribution along NSCS using green mussels as bioindicator; 2) examine the dietary intake of PBDEs and characterize the associated health risk for local population via consuming green mussel. The results of the present study will provide baseline information on the PBDE contamination of the NSCS and be important to establish seafood consumption guideline. 2. Material and methods 2.1. Chemicals Eighteen target PBDEs were BDEs-28, -47, -66, -85, -99, -100, -138, -153, -154, -183, -196, -197, -202, -203, -206, -207, -208, and -209. They were purchased from AccuStandard (New Haven, CT, USA). Silica gel (0.063–0.200 mm) and concentrated sulfuric acid were obtained from Merck (Darmstadt, Germany). Hexane, dichloromethane and isooctane (GC grade) were of the highest purity and were bought from Sigma-Aldrich (St. Louis, MO, USA). Florisil (60–100 mesh) was supplied by Supelco (Bellefonte, PA, USA). Ultrapure water was supplied by Milli-Q system (Watford, UK). 2.2. Sample collection Fifty green mussels were collected at each of the 22 sampling sites from the NSCS in 2016 (Fig. S1). After collection, samples wrapped in aluminum foil were placed in polyethylene (PE) bags, preserved in a cooler box with ice bags, and immediately transported to the laboratory. All mussels were dissected once in the laboratory. Soft tissues of all mussels from the same sampling site were mixed together, cut into small pieces, freeze-dried, homogenized and stored at −20 °C until chemical extraction. Information of the sampling sites and samples are shown in Table S1 in the Supplementary material. 2.3. Sample extraction and instrumental analysis The methods for extraction and purification of target PBDEs in mussel samples have been established and validated previously (Sun et al., 2018). In brief, 3 g of freeze-dried, homogenized sample was spiked with surrogate mixture standards (BDEs-77, −181, −205, and 13CBDE 209), and Soxhlet extracted with 200 mL of hexane/dichloromethane (1/1, v/v) for 48 h. After gravimetric lipid determination, the extracts were treated with concentrated sulfuric acid to remove fat and purified using a multilayer Florisil-silica gel column fractionation. PBDEs were eluted from the multilayer column with 80 mL of hexane. The clean extract was concentrated to near dryness and reconstituted with isooctane to a final volume of 100 μL. Known amounts of recovery

R. Sun et al. / Science of the Total Environment 698 (2020) 134276

standards (BDE-118, BDE-128, 4-F-BDE 67, and 3-F-BDE 153) were added to the final extract prior to instrumental analysis. Concentrations of PBDEs were determined on an Agilent 7890 gas chromatograph (GC) coupled with an Agilent 5975 mass spectrometer (MS) (Agilent Technologies, Santa Clara, CA) operated in selected ionmonitoring (SIM) mode with negative chemical ionization (NCI) mode. Helium was the carrier gas with a constant flow rate of 1.3 mL/min. Tri- to hepta-BDEs were separated with a DB-XLB capillary column (30 m × 0.25 mm i.d., 0.25 μm film thickness, Agilent). For octato deca-BDEs, a DB-5HT capillary column (15 m × 0.25 mm i.d., 0.10 μm film thickness, Agilent) was used for the separation. Details on instrumental analysis can be found elsewhere (Luo et al., 2009). 2.4. Quality assurance and quality control Quality assurance and quality control (QA/QC) measures were strictly followed throughout the field sampling and indoor experiment. Three replicates were performed and the relative standard deviations (RSDs) were below 20% for all target analytes in the triplicate samples. Field blanks and method blanks were treated identically to the real samples. Solvent blank and standards were run every 10 samples to check for any carryover, background contamination, and instrument drift. The limit of detection (LOD) and limit of quantification (LOQ) were set as three and ten times of the signal to noise ratio (S/N), respectively. The S/N was calculated by Agilent Masshunter qualitative software. The mean recoveries of surrogate in the spiked matrices (n = 3) ranged from 94% to 116%. The average recoveries were in the range of 92–112% for individual BDE congeners in the matrix spiked samples (Table S2). The LOD for individual PBDE congeners was between 0.01 and 6.1 ng/g lipid weight (lw). 2.5. Estimated daily intake and potential health risks The average daily intake (ADI, ng/kg body weight/d) of PBDEs via consumption of green mussels was estimated based on Eq. (1):

ADI ¼ PBDE concentration  daily consumption ½g=kg body weight=d

ð1Þ

In the present study, we use the mean and 95th percentile concentrations of individual and ΣPBDEs to calculate the ADI value, mimicking the average and high exposure scenarios, respectively. Also, the average amount of the daily mussel consumption was estimated by a questionnaire-based dietary survey in South China (Guo et al., 2010). For the ADI calculation, we divided the population into different groups according to the age (children, 2–5 years; youth, 6–18 years; and adults, N18 years) and gender (male and female). The body weight for these population groups was from Yang et al. (2005) and values are shown in Table S3. The potential health risk due to dietary intake of PBDEs was estimated using Eq. (2), the same methodology as reported by Pan et al. (2018). HQ ¼ ADI=RfD

ð2Þ

where HQ and RfD respectively represent hazard quotient and reference dose. RfD values of PBDEs can be found in Staskal et al. (2008), which were derived from the draft U.S. EPA IRIS Toxicological Evaluations. A HQ value N1 indicates that PBDEs at the exposure level probably induce potential adverse effects on human. RfD values were only available for BDE-47, BDE-99, BDE-153 and BDE-209, and they were 100, 100, 200 and 7000 ng/kg/d, respectively (Staskal et al., 2008).

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2.6. Statistics and data analysis All analyses were conducted in triplicate and the mean value of the three measurements was reported here. Concentrations of PBDEs in the green mussels were presented on lipid weight (lw) and ΣPBDEs represents the sum of all the 18 congeners. Concentrations below detection limits were set as zero. Data were examined for normality using Shapiro-Wilk test before statistic comparison. Principal component analysis (PCA) was applied to characterize the possible differentiation of the PBDE congeners. Spearman correlation analysis was used to determine the potential relationships among PBDE congeners. All the statistical analyses were performed using SPSS (SPSS 22.0 for Windows, SPSS Inc.) except for heatmap which was performed using the R software. The level of significance was set at p b 0.05. 3. Results and discussion 3.1. Occurrence of PBDEs in green mussels from the NSCS Concentrations of the ΣPBDEs in the soft tissue of green mussels from the NSCS are summarized in Table 1. ΣPBDEs were found in all the sites/samples, suggesting the widespread distribution of PBDEs in aquatic environment of the NSCS. Geographically speaking, the concentrations of ΣPBDEs varied greatly among different sites, and the levels ranged from 6.96 to 55.6 ng/g lw with the median value of 17.7 ng/g lw. Generally, higher levels of ΣPBDEs in the green mussel were observed in the eastern region of the NSCS (S1-S8) and the concentrations were approximately 3 times greater than the west region of the NSCS (S9–S18). This might be attributed to the several e-waste dismantling stations, shipping as well as numerous industrial complexes in the eastern region (Guo et al., 2010; Sun et al., 2015b). The highest level of ΣPBDEs was found at site S22 in Sanya city (Fig. 1), which is very likely related to the uncontrolled discharge from point sources in this region. The lowest level of ΣPBDEs was observed at site S15, which indicates this area is probably least contaminated by PBDEs compared to other locations. To get a better understanding of the contamination status of the ΣPBDEs in the NSCS, we compared our results with those reported in other regions of the world. Since the reported PBDEs concentration units for biota in the literatures are different (expressed in ng/g lw, ng/g wet weight or dry wt), we standardized all previous data to ng/g wet weight (ww) for the comparison and results are shown in

Table 1 Concentrations (ng/g lw) and detection frequencies (df, %) of PBDEs in green mussels from the northern South China Sea.

BDE-28 BDE-47 BDE-66 BDE-85 BDE-99 BDE-100 BDE-153 BDE-154 BDE-138 BDE-183 BDE-196 BDE-197 BDE-202 BDE-203 BDE-206 BDE-207 BDE-208 BDE-209 ΣPBDEs n.d: not detected.

Min

Max

Mean

Median

df (%)

0.266 1.58 0.253 0.006 1.06 0.754 0.104 n.d n.d 0.023 0.036 n.d n.d n.d 0.129 n.d n.d 0.604 6.96

3.23 14.0 3.54 3.09 13.2 3.36 2.05 1.52 0.438 0.289 0.558 0.336 1.01 0.504 3.07 2.66 1.40 43.01 55.6

0.907 5.26 0.936 0.220 3.45 1.58 0.588 0.244 0.065 0.131 0.100 0.022 0.087 0.052 0.618 0.451 0.233 5.71 20.7

0.619 3.83 0.609 0.065 2.03 1.35 0.341 0.095 0.036 0.120 0.065 n.d n.d 0.028 0.444 0.223 0.115 3.65 17.7

100% 100% 100% 100% 100% 100% 100% 64% 95% 100% 100% 23% 27% 91% 100% 100% 91% 100% 100%

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R. Sun et al. / Science of the Total Environment 698 (2020) 134276

Fig. 1. Sampling site locations and concentrations of ∑PBDEs in green mussels at the sites along the northern South China Sea. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Table 2. The levels of ΣPBDEs in mussel samples from NSCS were comparable to those in the mussels from coastal areas of France and Japan (Johansson et al., 2006; Ramu et al., 2007), but was approximately four to seventy times higher than those from most other areas worldwide, such as Vietnam, Malaysia, India, Cambodian, Central Adriatic Sea, Southern Greenland, eastern coastal area of China and Bohai sea of China (Christensen et al., 2002; Ramu et al., 2007; Wang et al., 2009; Piersanti et al., 2015). However, higher ΣPBDEs concentrations in mussels have been reported in Korea and Maggiore of Italy (Ramu et al., 2007; Binelli et al., 2008). Overall, the concentrations of ΣPBDEs in mussel samples from the NSCS were at moderate to high levels around the world. Meanwhile, we compared the ΣPBDE concentrations in mussel samples with other marine organisms in the NSCS (Table 2). Almost the same level of ΣPBDEs was found in fish, shrimp, crab and cephalopoda,

but lower than those in the flathead fish and robust tonguefish (Xiang et al., 2007; Yu et al., 2009). These could be attributed to the different trophic levels of these organisms, which resulted in different ΣPBDEs bioaccumulation ability of various species. However, it should be noted that the sampling time is crucial for the PBDEs contamination in biota samples, as our previous study has demonstrated that there was a decreasing trend in ΣPBDE levels in fish samples in the past decade due to the phase-out of the commercial PBDEs (Sun et al., 2015c). 3.2. Congener profiles of PBDEs in green mussels from the NSCS The composition profiles of PBDE congeners were presented in Table 1 and Fig. 2. Of the 18 PBDE congeners measured, BDEs-28, 47, 66, 85, 99, 100, 153, 183, 196, 206, 207 and 209 were detected in all the samples, followed by BDE-138 (detection frequencies = 95%),

Table 2 Concentrations of PBDEs (pg/g ww) in different biota samples around the world. Location

Sampling year

Species

Range (mean)

Number of measured congeners

Reference

Cambodia East China India Japan Korea Malaysia Vietnam Bohai sea of China Maggiore (Italy) Southern Greenland Coastal area of France Central Adriatic Sea Pearl River Estuary

2003–2005 2003–2005 2003–2005 2003–2005 2003–2005 2003–2005 2003–2005 2006 2005 2000 1981–2003 2013 2013 2013 2013 2013 2005 2005 2016

Green and blue mussels Green and blue mussels Green and blue mussels Green and blue mussels Green and blue mussels Green and blue mussels Green and blue mussels Blue mussels Zebra mussels Blue mussels Blue mussels Mussels Fish Shrimp Crab Cephalopoda Baby croaker fish Mullet Green mussels

36.8–74.2 38.8–581 5.55–33.6 30.4–931 47.5–10,120 5.88–240 2.31–64.8 60–546 880–10,380 (22) 44–5194 14–40 8.1–874 179–248 (63.7) (208) (306) (1728) 300–2376

15 15 15 15 15 15 15 14 14 4 11 4 10 10 10 10 10 10 18

Ramu et al. (2007) Ramu et al. (2007) Ramu et al. (2007) Ramu et al. (2007) Ramu et al. (2007) Ramu et al. (2007) Ramu et al. (2007) Wang et al. (2009) Binelli et al. (2008) Christensen et al. (2002) Johansson et al. (2006) Piersanti et al. (2015) Sun et al. (2015b) Sun et al. (2015b) Sun et al. (2015b) Sun et al. (2015b) Sun et al. (2015c) Sun et al. (2015c) This study

Pearl River Estuary NSCS

Some data had converted to ng/g ww for the comparison assuming the water content was 80% in biota sample.

R. Sun et al. / Science of the Total Environment 698 (2020) 134276

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Fig. 2. Relative percentage contribution of individual PBDE congeners to ∑PBDEs in green mussels along the northern South China Sea. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

BDE-208 and BDE-203 (91%), BDE-154 (64%), BDE-202 (27%) and BDE197(23%) (Table 1). BDE-47, BDE-209 and BDE-99 were the dominant congeners, which indicates the wide use of penta- and deca-BDE in the NSCS. Likewise, previous studies reported that BDE-47 was the predominant congener in most biota samples or areas around the world (Hu et al., 2010; Piersanti et al., 2015). For example, BDE-47 was the predominant PBDE congener in most biota samples (e.g., shrimp, crab, northern snakehead and grass carp) collected in Baiyangdian Lake, North China (Hu et al., 2010), and mussels from Central Adriatic Sea

(Piersanti et al., 2015). This could be due to the large use of the commercial penta- BDE, and wide use of commercial mixture of congeners of penta- and deca- BDE (BDE-47, BDE-99, BDE-100 and BDE-209) (Alaee et al., 2003). In addition, higher brominated congeners degrading to lower brominated congeners could be another explanation (Kierkegaard et al., 1999; Noyes et al., 2011; Tang et al., 2017). The PBDE congener profiles in green mussels were different among locations, which may be linked to their differences in sources and environmental behaviors.

Fig. 3. Correlation matrix between the PBDE congeners in the green mussels from the northern South China Sea. The colour and size of the circle indicates the strength of the correlation. The colour scale is shown on the right. Significance level was set at 0.05. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

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BDE-209 was the second predominant congener in NSCS, which indicates the large use of this chemical. It is noteworthy that BDE-209 accounted for approximately 80% and 60% of the ΣPBDEs at S22 and S6, respectively. This might be related to the PBDEs discharge from point source. Actually, BDE-209 has quickly become one of the major BFRs in China since the phase-out of the commercial penta-, and octaBDE mixtures (Li et al., 2014). Additionally, high levels of BDE-209 have been detected in the riverine and coastal sediments of South China (Mai et al., 2005; Chen et al., 2013). Due to the high log Kow value of 9.98 (Braekevelt et al., 2003), BDE-209 can easily bound to the surface of particulates in the aquatic environment. Mussels, as filter feeders, can accumulate these contaminants from suspended particulate matter, which is an important pathway for the BDE 209 burden in green mussel (De Boer et al., 2003). The wide detection with high levels of BDE-209 in mussel samples suggests the prevalence of deca-BDE in the NSCS. This congener pattern is in line with our previous study that BDE-209 was the predominant PBDE congener in most aquatic species collected from the Zhujiang river of South China (Sun et al., 2018) and hyperbenthic mysid shrimp from the Scheldt Estuary of the Netherlands (Verslycke et al., 2005). BDE-99 was the third most abundant congener, which exhibited significantly higher abundance than BDE-100 in green mussels (p b 0.05). This was contrary to PBDE congener profiles in many fish species with high metabolic debromination ability, such as Cyprinidae fish and Cichlidae fish (Sun et al., 2016). Although BDE-99 and BDE-100 are isomers, BDE-99 can be more easily metabolized to low brominated congener (BDE-47) than BDE-100 (Xiang et al., 2007). Therefore, high BDE100 abundance was observed in the species with high metabolic activity. However, for the fish species with little or no debromination ability, BDE-99 exhibited higher proportion compared to BDE-100, which is the same as green mussels in present study (Sun et al., 2016). The results indicate green mussels have a lower metabolic ability for PBDEs.

Fig. 4. PCA factor loading of individual PBDE congeners in green mussels collected from the northern South China Sea. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

total variances (Fig. 4). These congeners are the major components of commercial penta- and octa-BDEs (La Guardia et al., 2006) with moderate octanol-air partition coefficients (log Koa ≈ 9.50–12.78) (Wania and Dugani, 2003). Due to the regulation of penta and octa-BDEs in 2004, most products containing these banned chemicals were discarded. PBDEs in these products would eventually leach out and enter into the surrounding environment, and transported to SCS via surface runoff and atmospheric deposition (Wang et al., 2015a). Consequently, PC1 was considered as the surface runoff and atmospheric deposition of PBDEs from commercial products. PC2 was characterized by high loadings of higher brominated congeners, such as BDE-196, 203, 206, 207, 208 and 209, accounting for 25.7% of the total variances (Fig. 4).

3.3. Possible sources of PBDEs in the NSCS There are many possible sources of which PBDEs can be emitted to the environment, such as plastic and electronic wastes, construction materials, textiles, and sewage plants or direct emissions from industrial plants (de Wit et al., 2002). The high levels of BDE-209 at S22 and S6 are very likely to be associated with the direct discharge from the point source. Less brominated congeners in the green mussels in the present study might originate from the direct emission, atmospheric inputs as well as the metabolic products of higher brominated congeners, as discussed above (Kierkegaard et al., 1999; Stapleton et al., 2006; Noyes et al., 2011). For example, BDE-209 can be debrominated into lower-brominated congeners, such as BDEs-154, 99, 100 and 47 in carp and rainbow trout (Kierkegaard et al., 1999; Stapleton et al., 2006; Wang and Li, 2010). Correlation analysis can provide useful information on sources of pollutants. Results indicated that significant correlations were present among BDEs-28, 47, 66, 85, 99, 100, and 153, and among BDEs-203, 206, 207, 208 and 209 (p b 0.05). The results suggest that these PBDEs in the green mussels might originate from the similar sources, such as commercial penta-, octa-, and deca-BDE products, or they show similar environmental behavior. However, there were no significant correlations between BDE-154 and all other congeners (p N 0.05) (Fig. 3 and Tables S4), indicating the different source between BDE-154 and other BDE congeners. This could be attributed to the different profile and physical processes of BDE-154 from other congeners prior to mussel ingestion. Principal component analysis (PCA) was performed on 16 individual BDE congeners (detection rate N 50%) to investigate the sources of PBDE contamination in green mussels. For PBDE levels below LOD, the value was imputed using 1/2 LOD. The first two components explained the majority of the total variance (62%). PC1 was dominated by BDE-28, 47, 66, 85, 99, 100, 153 and 183, which accounted for 35.9% of the

Table 3 Average daily intakes (ADI, ng/kg bw/day) of selected PBDEs based on the mean and 95th concentrations through consumption of green mussels for different population groups in South China. BDE-47 BDE-99 BDE-153 BDE-209 ∑PBDEs Mean

Children (2–5 years) Male Female Mean Youth (6–18 years) Male Female Mean Adults (N18 years) Male Female Mean 95th Children (2–5 percentile years) Male Female Mean Youth (6–18 years) Male Female Mean Adults (N18 years) Male Female Mean

0.15 0.09 0.12

0.10 0.06 0.08

0.02 0.01 0.01

0.17 0.10 0.13

0.59 0.37 0.48

0.20 0.13 0.17

0.13 0.09 0.11

0.02 0.01 0.02

0.23 0.15 0.19

0.80 0.52 0.66

0.08 0.08 0.08

0.05 0.05 0.05

0.01 0.01 0.01

0.08 0.09 0.09

0.30 0.32 0.31

0.36 0.23 0.30

0.30 0.19 0.24

0.02 0.03 0.02

0.17 0.39 0.28

0.59 0.96 0.77

0.49 0.32 0.41

0.41 0.26 0.34

0.06 0.04 0.05

0.84 0.54 0.69

2.08 1.34 1.71

0.18 0.20 0.19

0.15 0.17 0.16

0.02 0.03 0.02

0.32 0.34 0.33

0.78 0.84 0.81

R. Sun et al. / Science of the Total Environment 698 (2020) 134276 Table 4 Average daily intake (ADI, ng/kg/d), reference dose (RfD, ng/kg/d) and hazard quotient (HQ) of selected PBDE congeners through green mussel consumption by the population in South China.

EDI RfD HQ

BDE-47

BDE-99

BDE-153

BDE-209

0.08–0.49 100 8–49 × 10−4

0.05–0.41 100 5–41 × 10−4

0.01–0.06 200 5–30 × 10−5

0.08–0.84 7000 1.1–12 × 10−7

BDE209 is the main ingredient in the commercial Deca-BDE formulation, consists of 97–98% Deca-BDE. These high brominated chemicals have high values of Kow (log Kow ≈ 7.89–9.97) and short range of transportation (Wania and Dugani, 2003). Therefore, PC2 likely reflected the direct discharge from local regions due to anthropogenic activities. 3.4. Dietary intake of PBDEs and risk assessment Table 3 shows association of estimated dietary intakes with the consumption of mussels by the population in South China, as well as the corresponding exposure health risks of PBDEs. The mean ADIs of ∑PBDEs through mussel consumption for children, youth, and adults in South China were 0.48, 0.66 and 0.31 ng/kg bw/day, respectively (Table 3). The corresponding 95th percentile ADIs of ∑PBDEs were 0.77, 1.71 and 0.81 ng/kg bw/day, respectively. The ADIs of BDE-47, BDE-99 and BDE-209 were almost at the same level and approximately one order of magnitude greater than BDE-153 (Table 3). Also, in the children and adult youth groups, both mean and 95th percentile ADIs of PBDEs in male were slightly higher than female (p b 0.05). Here ADIs of ∑PBDEs in the present study were lower than those in other fishes from South China (Xiang et al., 2007), but were slightly higher than other marine biota species (Meng et al., 2007; Sun et al., 2014; Sun et al., 2015b). The HQ values of BDE-47, BDE-99, BDE-153 and BDE-209 were 8–49 × 10−4, 5–41 × 10−4, 5–30 × 10−5, and 1.1–12 × 10−7, which were far lower than 1 (Table 4), even when assessed according to the 95th percentile values. These results indicate that consuming green mussels collected from South China would not pose health risk to human. In the present study, there might be uncertainties caused by reference dose used. For example, these reference doses are draft values while the toxic mechanisms are very complex in human body with other co-existing pollutants. Furthermore, for each BDE congener there is only one reference dose, regardless of the different susceptibility to PBDE exposure among different population groups. A more accurate assessment of the potential health risk is required in the future when more information becomes available. 4. Conclusions The present study investigated PBDEs contamination in green mussels collected from the NSCS. Our results indicate that there are large regional differences in PBDEs levels and congener profiles in green mussels. High levels of PBDEs were frequently detected in highly industrialized, urbanized and populated areas. BDE-47 and BDE-209 were the predominant PBDE congeners. Concentrations of ΣPBDEs in NSCS were at moderate to high levels around the globe. The dietary intake of PBDEs through consuming green mussels would not pose health risks to local residents in South China. Acknowledgments This study was supported in part by the National Natural Science Foundation of China (Nos. 41703100, and 41977302), Guangxi Innovation-driven Development Projects (GuikeAA18242031), Natural Science Foundation of Guangxi Province (2018GXNSFAA050144), and the Startup Foundation for Introducing Talent of NUIST (No. 2018r069).

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Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi. org/10.1016/j.scitotenv.2019.134276.

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