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Geographical distribution and risk assessment of dichlorodiphenyltrichloroethane and its metabolites in Perna viridis mussels from the northern coast of the South China Sea
Marine Pollution Bulletin 151 (2020) 110819
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Geographical distribution and risk assessment of dichlorodiphenyltrichloroethane and its metabolites in Perna viridis mussels from the northern coast of the South China Sea
T
Runxia Suna, Juan Yub, , Yuhao Liaoa, Jiemin Chena, Zetao Wua, Bixian Maic ⁎
a
School of Marine Sciences, Nanjing University of Information Science and Technology, Nanjing 210044, China School of Materials and Environment, Beijing Institute of Technology, Zhuhai, Zhuhai 519000, China c State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China b
ARTICLE INFO
ABSTRACT
Keywords: DDTs Perna viridis Geographical distribution Risk assessment South China Sea
Mussels (Perna viridis) were collected from the northern coast of the South China Sea (NSCS) to investigate the geographical distribution and potential risk of dichlorodiphenyltrichloroethane and its metabolites (DDTs). DDTs had concentrations that ranged from 248 ng/g to 4650 ng/g lipid weight (lw), with an average of 807 ± 932 ng/ng lw. A comparison of the levels of DDTs in mussels indicated that the NSCS is still one of the most polluted areas in the world, although a decreasing trend was observed. DDT metabolites were predominant in all samples, suggesting that historical residue was the main source of DDT pollution. However, there were new inputs of DDTs which likely associated with antifouling paints. The human health risk assessment revealed that the current concentrations of DDTs in mussels might pose little health risk for the consumers.
Dichlorodiphenyltrichloroethane (DDT) is a persistent organic pollutant (POP) that is ubiquitous, persistent, highly bioaccumulative in nature, and has toxic biological effects (EPA, 2000a; Pheiffer et al., 2018). In China, DDT use reached 0.4 million tons between the 1950s and 1980s, resulting in high levels of residual pesticides in aquatic systems (Sun et al., 2015; Yin et al., 2015). Although DDT has been banned since 1983 (Pan et al., 2016), new input sources of DDT have meant continued discharges into the environment from illegal use (UNDP, 2012; Wang et al., 2011), other pesticides (Huang et al., 2019; Qiu et al., 2005), and antifouling paint (Jin et al., 2008; Xin et al., 2011). It is common that DDT biodegrades into 1,1-dichloro-2,2,-bis(pchlorophenyl) ethane (DDD) and 1,1-dichloro-2,2,-bis (p-chlorophenyl)- ethylene (DDE) (Quensen et al., 1998; Zhao et al., 2018). DDTs (DDT and its metabolites like DDD and DDE) have been found in different aquatic environments due to both old and new pollution sources, all of which pose a danger to humans and animals (Jayasinghe et al., 2019; Mo et al., 2019; Wang et al., 2011; Yin et al., 2015). The coastal regions of the northern South China Sea (NSCS) close to Guangdong province, Guangxi province, and Hainan province have the fast developing economies in the world (Morton and Blackmore, 2001). As a part of that development, various kinds of pesticides were applied in southern China (Li et al., 2018; Wang et al., 2011), increasing the stress of DDT contamination in nearby coastal marine areas (Kaiser
⁎
et al., 2018; Mo et al., 2019; Pan et al., 2016). High levels of DDTs have been detected in the air (Wang et al., 2007), water, and sediment (Fu et al., 2003) from Guangdong province. There was also evidence of a phenomenon where accumulated DDTs in the sediment transferred to aquatic organisms (Leung et al., 2010). Annual levels of DDTs in the tissue of oyster from the coast of the South China Sea increased between 2004 and 2006 (Gan et al., 2009). In addition, the extensive pollution from emerging and aged DDT in the sediments still exists along the coast of the South China Sea (Mo et al., 2019). However, a current regional distribution of DDTs in the NSCS is needed. Thus, the geographical distribution and the possible sources of DDTs in the NSCS have attracted increasing attention. Mussels are widely distributed, have relatively stable habitats, are able to accumulate many contaminants (Monirith et al., 2003), and are often used as ideal bioindicators (over other marine organisms) for marine pollution monitoring (Ramu et al., 2007b). The high protein content of mussels makes them an important part of the human diet in coastal areas. Up to 75% of human DDTs intake has been attributed to the consumption of seafood (Nakata et al., 2002). Unfortunate health and environmental problems may occur due to the exposure to DDTs. In addition, the occurrence of 1-Chloro-2,2-bis(4-chlorophenyl)ethane (p,p′-DDMU), a secondary metabolite of 1,1-dichloro-2,2-bis(4-chlorophenyl)ethane (p,p′-DDD) and 1,1-dichloro-2,2-bis(4-chlorophenyl)
Corresponding author. E-mail address: [email protected] (J. Yu).
https://doi.org/10.1016/j.marpolbul.2019.110819 Received 12 September 2019; Received in revised form 7 December 2019; Accepted 10 December 2019 Available online 29 January 2020 0025-326X/ © 2019 Elsevier Ltd. All rights reserved.
Marine Pollution Bulletin 151 (2020) 110819
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Fig. 1. Concentrations of DDTs (ng/g lw) in mussels from 22 sampling sites in the NSCS.
standards (PCB 24, 82, and 198) were added prior to instrument analysis. The concentrations of DDTs (the sum of o,p-DDD, p,p′-DDD, o,p -DDE, p,p′-DDE, o,p -DDT, p,p′-DDT, and p,p′-DDMU) were measured by an Agilent 7890A GC coupled to an Agilent 5975B MS with a DB5MS (60 m × 0.25 mm × 0.25 mm, Agilent) capillary column. The elective ion monitoring mode was used, and the injection volume was 1 μl. Helium was the carrier gas flowing at 1.3 ml/min. The injection port and ion source temperatures were 290 °C and 260 °C, respectively. The oven temperature began at 120 °C, increased to 180 °C at a rate of 6 °C/min, later increased to 240 °C at a rate of 1 °C/min, and then increased to 290 °C (15 min hold time) at a rate of 6 °C/min. The instruments were calibrated with regular injections of solvent blanks and standard solutions. All samples were measured in triplicate and after spiking with surrogate standards, and there were regular analyses of procedural blanks, spiked blanks, and spiked matrices. The average recoveries of surrogate standards were 90 ± 14%, 96 ± 9%, and 89 ± 10% for PCB 30, 65, and 204, respectively. The average recoveries were 95%–102% in the spiked blanks, and 92%–105% in matrix-spiked samples for DDTs (o,p-DDD, p,p′-DDD, o,p -DDE, p,p′DDE, o,p -DDT, p,p′-DDT, and p,p′-DDMU). Relative standard deviations were < 15% (n = 3) for all the target chemicals. The method detection limits, set as a signal-to-noise ratio of 3, ranged from 0.005–2.0 ng/g lipid weight (lw). Concentrations of DDTs from the 22 sampling sites in the NSCS are shown in Fig. 1 and Table 1. DDTs concentrations ranged from 248 ng/ g lw to 4650 ng/g lw, and from 6.59 ng/g wet weight (ww) to 105 ng/g ww. The comparison of concentrations of DDTs revealed that DDT levels in mussels in this study were much higher than those from the Marmara Sea coast (Ulusoy et al., 2016), Spanish Mediterranean waters (Campillo et al., 2017), the Black Sea (Georgieva et al., 2016), Italy (Chiesa et al., 2018), and the coastal waters of Korea (Ramu et al., 2007a), but lower than the levels from the River Ravi of Pakistan (Baqar et al., 2018). The higher residual DDT levels in mussels was due to the substantial application of these chemicals during agricultural practices of the past (Monirith et al., 2003). However, the average concentrations in oysters from the coast of Guangdong in 2004–2006 (Gan et al., 2009) and in mussels from the South China Sea (Guo et al., 2010) were 2.64 and 2.27 times higher, respectively than the levels reported in this study. This pattern indicates a decrease in the DDTs contamination
ethene (p,p′-DDE) (Quensen et al., 1998; Sun et al., 2014), has been detected in fish (Guo et al., 2009), birds (Sun et al., 2014), and sediments (Yu et al., 2011a), but information on the contamination of these metabolites in mussels is still relatively scarce. Metabolites of DDT may result in reproductive abnormalities and has been found to be biomagnified through the marine food chain (Falandysz et al., 1999; EPA, 2000a). Therefore, it is necessary to study the residues of mussels in order to evaluate the current levels and risks of DDT and its metabolites. The aims of this study were to determine the level of contamination, the distribution of the contamination, and assess the health risks of DDTs (o,p-DDD, p,p′-DDD, o,p -DDE, p,p′-DDE, o,p -DDT, p,p′-DDT and p,p′-DDMU) associated with consumption of mussels from the NSCS. In addition, we discuss the potential sources of these pollutants. This study will provide a useful reference for environmental protection of these regions. Mussel (Perna viridis) samples were collected from 22 sampling sites along the NSCS coast in 2016. The location and sampling sites are shown in Fig.1. Fifty individuals were obtained at each sampling site through bottom trawling or artificial fishing. Mussels were immediately wrapped in aluminum foil, put into polyethylene bags, and stored on ice in a cooler box for transport from the field. In the laboratory, we collected the total amount of the soft tissues of all mussel samples after removing the shell and mixed the tissues together to create single composite samples by site. All sampled tissues were cut into small pieces, freeze-dried, ground into a uniform powder, and then stored at −20 °C prior to chemical analysis. The samples were extracted and purified according to our previously published method (Sun et al., 2017). Briefly, after the spiking of the samples with surrogate standards polychlorinated biphenyl (PCB) 30, 65, and 204, 3 g of each prepared sample was Soxhlet extracted with 200 ml of dichloromethane and n-hexane (1:1 v/v) for 48 h. The extract was concentrated with a rotary evaporator, and the solvent was changed to hexane. An aliquot of the extract was used to determine lipids by gravimetric measurement. The remaining extract was treated with concentrated sulfuric acid, and further purified using a multilayer column (florisil: neutral silicone: acidic silica gel, 20:2:5 cm). The column was eluted with 80 ml hexane and 60 ml dichloromethane. Under a constant stream of nitrogen gas, the elute was concentrated to near dryness and reconstituted in 200 μl isooctane. The recovery 2
Marine Pollution Bulletin 151 (2020) 110819
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Table 1 Comparison of DDT concentrations (ng/g) in mussels of reported studies from different countries and regions. Location
Sampling year
Concentration
Reference
Marmara Sea coast Spanish Mediterranean waters Black Sea, Bulgaria Italy Kastela Bay (Croatia) Coastal water, Korea River Ravi, Pakistan South China Coast of Guangdong Northern coast of the South China Sea
2010–2011 2003–2013 2015 2016–2017 2002–2011 2005 2015–2016 2004–2005 2003–2007 2016
1.58 ww 2.7–6.9 ww 2.14 ww nd-16.3 ww 0.39–1.4 ww 21–400 lw (144)a 46.4–1010 ww (318)a 3.95–507 ww (65.7)a 58.4–5620 lw (1480)a 6.59–105 ww (27.2)a 248–4650 lw (807)a
Ulusoy et al. (2016) Campillo et al. (2017) Georgieva et al. (2016) Chiesa et al. (2018) Milun et al. (2016) Ramu et al., 2007a Baqar et al. (2018) Guo et al. (2010) Gan et al. (2009) This study
a
Average value.
Table 2 Average concentrations (and ranges) of DDT and its metabolites in mussels from different sites in the NSCS; units of ng/g lw. Regions
Number of sampling sites
DDTs
p,p′-DDE
p,p′-DDD
p,p′-DDMU
(DDD + DDE)/DDTs
ECG PRE WCG CG CH Average (range)
6 2 7 3 4
732 (248-1690) 2546 (441-4650) 462 (270-689) 452 (354-616) 919 (328-1320) 807 (248-4650)
192 455 160 140 248 209
292 1630 224 225 350 394
14.5 (8.60–28.0) 33.5 (12.1–55.0) 13.2 (8.2–20.3) 9.7 (7.5–12.7) 16.4 (6.80–21.5) 15.5 (6.80–55.0)
0.79 0.93 0.93 0.93 0.74 0.86
o,p-DDE
p,p'-DDE
o,p-DDD
p,p'-DDD
o,p-DDT
p,p'-DDT
(0.56–0.92) (0.89–0.97) (0.90–0.97) (0.90–0.97) (0.71–0.77) (0.56–0.97)
p,p'-DDMU
Percentage of DDTs
100% 80% 60% 40% 20% 0% Sampling sites Fig. 2. Composition profiles of DDTs in mussels from sampling sites in the NSCS.
coast of Hainan region, including sites S19 to S22. The average levels of DDTs in ECG, PRE, WCG, CG, and CH were 732 ng/g lw, 2546 ng/g lw, 462 ng/g lw, 452 ng/g lw, and 919 ng/g lw, respectively (Table 2). In a regional comparison, the average level of DDTs deceased in the following order: PRE > CH > ECG > WCG > CG (Table 2). However, no significant differences were found by t-test in comparisons of CH with ECG, or ECG with WCG. The reason for this observation might be due to the small sample numbers (Sun et al., 2014). In addition, some sites with levels exceeding 1000 ng/g lw (S4, S7, S19, S20) increased the average levels of those regions (ECG, PRE, and CH). The highest level recorded was at site S4 in Changsha bay, which was 2.31 times higher than the average level (732 ng/g lw) of the ECG region, and 1.24 times higher than reported for the same area in a previous study measuring DDT levels in oysters from Changsha bay in 2005 (Gan et al., 2008), suggesting the possible increase in DDT loads at site S4. However, the report showed that average levels in oysters in the ECG (1730 ± 1060 ng/g lw) and WCG (1200 ± 1040 ng/g lw) regions between 2003 and 2007 were 2.36 and 2.59 times higher, respectively, than the levels reported in this study (Gan et al., 2009), suggesting the possible decrease in DDT loads in the system. Mussels and oysters were used as potential bioindicators of DDTs. Content differences of DDTs in
Table 3 Peak concentrations of DDTs (ng/g lw) by sampling site. Sample
Location
DDTs
(DDD + DDE)/DDT
o,p-DDT/p,p′-DDT
S4 S7 S19 S20
Changsha bay Shenzhen bay Dongzhai harbor Maniao harbor
1690 4650 1320 1040
0.56 0.97 0.74 0.72
1.01 0.18 0.13 0.13
along the South China Sea coast between 2004 and 2016. The degraded forms of DDT were the predominant form of the pollutant in the sediments of the NSCS, which could also support the conclusion that new DDT pollution has decreased in the last decade (Kaiser et al., 2018; Yu et al., 2011a). To better understand the regional distributions, we divided the sampling sites into five geographical regions. As shown in Fig.1 and Table 2, the sampling regions were named 1) ECG, for the east coast region of Guangdong, including sites S1 to S6, 2) PRE, for the Pearl River estuarine region, including sites S7 to S8, 3) WCG, for the west Coast of Guangdong region, including sites S9 to S15, 4) CG, for the coast of Guangxi region, including sites S16 to S18, and 5) CH, for the 3
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mussels and oysters in the same region were < 300 ng/g lw (Wang et al., 2008). Much higher levels in the past indicated that levels of DDTs around the Guangdong coast may be decreasing. However, our highest level recorded in mussels (site S7, Shenzhen bay) was 2.62 times higher in DDTs than the previous report in oyster (1772 ng/g lw) (Gan et al., 2009). Shenzhen bay was in the PRE region, which is influenced by the runoff discharge from agricultural land erosion and shipping activities in the Pearl River catchment. This indicates the possible influence of sources including historical residues and new inputs of DDTs. Emerging and legacy pollutants were found in the sediments around Hainan Island (Mo et al., 2019). High levels (S19, S20) were observed in the CH region, which might be attributed to the higher background levels of DDTs in the CH region. Possible sources of DDTs in the S4, S7, S19, and S20 sites will be discussed more below. The composition profiles of DDTs in mussels from the NSCS are shown in Fig. 2. DDT and its degraded derivatives (DDD, DDE, DDMU) were all detected. Overall, the composition profile of DDTs showed the highest contribution was from p,p′-DDD (48.8%), followed by p,p′-DDE (25.9%), o,p-DDD (9.89%), p,p′-DDT (9.85%), o,p-DDT (3.2%), p,p′DDMU (1.92%), and o,p-DDE (0.45%) (Fig. 2). Higher proportions of degraded derivatives suggest the enhanced degradation of DDT. p,p′DDD was the predominant compound accumulated in the mussels. Similar accumulation contributions were reported in mussels along the Pearl River Delta (DDD, 49%) (Fang, 2004), in bivalves from the northeast coast of China (DDD, 46%) (Jin et al., 2008), and in shellfish from coast of Xiamen (p,p'-DDD, 54%) (Zhang et al., 2012). Industrial DDT consists of 75% p,p'-DDT, 15% o,p-DDT, 5% p,p'-DDE, < 0.5% o,pDDE, < 0.5% p,p'-DDD, < 0.5% o,p-DDD, and < 5% of unidentified compounds (Gan et al., 2009). DDT can be degraded into DDD and DDE under anaerobic and aerobic conditions, respectively (Yu et al., 2011a). When the ratio of DDD/DDE is higher than 1, this indicates anaerobic metabolism of the DDT. DDE in mussels primarily comes from the ambient environment instead of biotransformation processes, while DDD in mussels follows dietary uptake and biotransformation of DDT inside the organism (Kwong et al., 2009). The predominant form of DDD in mussel tissues indicated that the accumulation in mussels was influenced by dietary uptake and biotransformation of the DDT. The ratios of (DDE + DDD)/DDTs have been used to distinguish the main source of DDTs from fresh inputs (ratio < 0.5) or historical uses (ratio > 0.5) (Yu et al., 2011a). In this study, the ratios of (DDE + DDD)/DDTs ranged from 0.56 to 0.97, with an average value of 0.86 (Table 2). This is consistent with the ratio measured in birds in Guangdong Province (Sun et al., 2014), indicating that historical residues are likely the main source of DDT in the mussels of the NSCS. This result agrees with the banned usage of DDT by the government starting in 1983, which reduced the input of industrial DDT. The properties of DDT make both DDT and its degraded derivatives persistent in the environment. We measured some high levels in sites S4, S7, S19, and S20 with (DDE + DDD)/DDTs ratios of 0.56, 0.97, 0.74, and 0.72, respectively (Table 3). The smallest ratio (0.56) was in site S4
(a)
r=0.93, p<0.01 50 40 30 20 10 0 0
500
1000 1500 2000 2500 3000 3500
p,p-'DDD (ng/g, lw) (b)
p,p-'DDMU (ng/g, lw)
60
r=0.98, p<0.01 50 40 30 20 10 0 0
100 200 300 400 500 600 700 800 900
p,p-'DDE (ng/g, lw) (c)
p,p-'DDMU/DDTs
0.040
r=-0.51, p<0.05
0.035 0.030 0.025 0.020 0.015 0.010 0.4
0.5
0.6
0.7
0.8
0.9
p,p-'DDD/(p,p-'DDD+p,p-'DDE) Fig. 3. Correlations of concentrations of p,p′-DDD (a) and p,p′-DDE (b) plotted against p,p′-DDMU, and concentrations of p,p′-DDMU/DDTs plotted against p,p′-DDD/(p,p′-DDD + p,p′-DDE) and (c) in mussels from the NSCS.
DDTs and EDI concentrations
120
DDTs ng/g ww
EDI (ng/kg·d)
CR
14 12
100
10
80
8 60
6 40
4
20
Cancer risks (10-6)
p,p-'DDMU (ng/g, lw)
60
2 0
0 S1 S2 S3 S4 S5 S6 S7 S8 S9 S10 S11 S12 S13 S14 S15 S16 S17 S18 S19 S20 S21 S22
Sampling sites Fig. 4. Concentrations of DDTs and EDI (y coordinate on the left) and cancer risks (y coordinate on the right) in mussels from 22 sites from the NSCS. 4
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along with a high DDT concentration, implying that there might be a new input of DDT in site S4. Site S4 was located in a mariculture zone. It is reported that antifouling paints on the hulls of boats may be an important source of DDTs to the mariculture zones of South China (Yu et al., 2011b). Ratios of o,p-DDT/p,p′-DDT can be diagnostic of their sources (Venkatesan et al., 1996; Zhang et al., 2018). Previous studies confirmed that DDT pollution caused by antifouling paints had a higher o,p-DDT/p,p′-DDT concentration ratio (ranging from 0.4 to 1.1; averaged at 0.75) (Wang et al., 2007) than that of technical DDT (around 0.2–0.3) (Qiu et al., 2005). The o,p-DDT/p,p′-DDT concentration ratio was 1.01 in site S4 (Table 3), indicating a possible antifouling paint input source. Other high DDT levels were measured in sites S7, S19, and S20 with higher (DDE + DDD)/DDTs ratios that implied the residues of historical applications of DDTs. The o,p-DDT/p,p′-DDT concentration ratios in sites S7, S19, and S20 were 0.18, 0.13, and 0.13, respectively, which also confirms the conclusion of historical residues rather than new sources. There were detectable levels of p,p′-DDMU in all the samples. The concentrations ranged from 6.80 ng/g lw to 55.0 ng/g lw, with an average of 15.5 ng/g lw (Table 2); this was the same regional distribution pattern as the concentrations of p,p′-DDE and p,p′-DDD. p,p′DDMU in the mussels in this study was lower than those reported in birds (nd-80 ng/g lw) (Sun et al., 2014), and seawater wild fish (average 25.5 ng/g lw) (Guo et al., 2009) from Guangdong Province. By correlation analysis, p,p′-DDMU levels were significantly correlated with p,p′-DDD (r = 0.93, p < 0.01) and p,p′-DDE (r = 0.98, p < 0.01; Fig. 3a and b), suggesting that p,p′-DDMU in mussels might be derived from the dehydrochlorination of p,p′-DDE or p,p′-DDD (Quensen et al., 1998). The correlation between p,p′-DDD/(p,p′-DDD+ p,p′-DDE) and p,p′-DDMU/DDTs was tighter in the sediments than in farmed fish, indicating that bioaccumulation of p,p′-DDMU was partially related to dehydrochlorinated from DDD in the environment (Guo et al., 2009). A negative linear correlation was found between p,p′DDD/(p,p′-DDD+ p,p′-DDE) and p,p′-DDMU/DDTs (r = 0.51, p < .05) in mussels (Fig. 3c), similar to the correlation seen in seawater fishes (Guo et al., 2009), indicating that DDMU was also partially dehydrochlorinated from DDD in the environment. The concentrations of DDTs based on wet weight in mussels are shown in Fig. 4, ranging from 6.59 ng/g ww to 105 ng/g ww. According to GB2763-2016, the extraneous maximum residual level (EMRL) of DDTs recommended for aquatic products is 500 ng/g ww (China, 2016). The concentrations in the mussels were all below the suggested EMRL set by the Chinese government. DDTs intake from consumption of mussels for local residents was estimated by the equation as follows: the estimated daily intake (EDI, (ng/kg)/d) = contaminant concentration (ng/g)/body mass (kg) × daily consumption (g/d). The average contaminant concentration was 27.2 ng/g. A Chinese adult consumer was assumed to have a mean body mass of 60 kg. The daily consumption levels of mussels was 0.0245 kg/d for males by a dietary survey (Guo et al., 2010). The EDIs of DDTs ranged from 2.67 ng/kg/d to 42.88 ng/kg/d (Fig. 4). The average EDI was estimated to be 11.12 ng/kg/d, which was lower than the average EDI for aquatic organisms from the Pearl and Dongjiang Rivers (Sun et al., 2017), and far below the oral reference dose (RfD, 500 ng/kg/d) proposed by the United States Environmental Protection Agency (EPA, 2000a). To estimate the carcinogenic effects, human carcinogenic risk level (CRL) associated with the consumption of mussels from different locations were estimated by the following equation: CRL = contaminant concentration (ng/g) × daily consumption (g/d) × cancer slope factor (mg/kg/day)−1/body mass (kg) (Watanabe et al., 2003). The DDT contaminant concentrations are shown in Fig. 4. The daily consumption levels of mussels was 0.0245 kg/d (Guo et al., 2010). To compare this result with the EPA guidelines, body mass was assumed to be 70 kg (EPA, 2000a). Cancer slope factor (0.34 (mg/kg/day)−1) was obtained from the EPA Guidance for Assessing Chemical Contaminant Data for
Use in Fish Advisories (EPA, 2000a). The CRL in different samples ranged from 7.85 × 10−8 to 1.25 × 10−5 with an average of 3.24 × 10−6 (Fig. 4). Most samples were below the risk level for carcinogens (10−5), indicating that the risk of cancer in most samples were in an acceptable range. However, the levels of DDTs in 9% of the samples were slightly above the risk level for carcinogens suggested by the USEPA (EPA, 2000b). This suggests that consumption of the mussels from some sites might pose a human health risk. We observed the spatial distribution of DDT concentration and composition in the soft tissues of P. viridis mussels collected from the coast of the NSCS in this study. Our comparison of DDT levels revealed a decrease in DDTs around the South China coast. In a regional comparison, the average concentrations of DDTs decreased in the following order: PRE > CH > ECG > WCG > CG. Higher proportions of degraded derivatives suggested the degradation of DDT. The predominant compound of DDD indicated that the accumulation in mussels was influenced by dietary uptake and biotransformation of DDT. There were detectable levels of p,p′-DDMU in all the samples. p,p′-DDMU levels were significantly correlated with p,p′-DDE and p,p′-DDD, indicating that p,p′-DDMU might be derived from dehydrochlorination of p,p′-DDE or p,p′-DDD. The historical use of DDTs was the main source of DDTs in the NSCS, but there were some new inputs of DDTs, likely associated with antifouling paints. Mussel sample DDT levels were below the suggested EMRL set by China. The EDI was also far below the oral reference dose (RfD, 500 ng/kg/d) proposed by USEPA. However, a cancer risk assessment suggested dietary consumption of mussels exposed to DDTs in some sites might pose a human health risk. Author contribution statement Runxia Sun: Conceptualization, Methodology, Investigation, Software, Data curation, Writing-Reviewing and Editing. Juan Yu: Conceptualization, Investigation, Software, Resources, Writing-Reviewing and Editing. Yuhao Liao: Investigation. Jiemin Chen: Investigation. Zetao Wu: Investigation. Bixian Mai: Resources, Writing-Reviewing and Editing. Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgment This study was funded by the National Natural Science Foundation of China (Nos. 41703100, and 41977302), and the Startup Foundation for Introducing Talent of NUIST (No. 2018r069). References Baqar, M., Sadef, Y., Ahmad, S.R., Mahmood, A., Li, J., Zhang, G., 2018. Organochlorine contaminants in freshwater mussels; occurrence, bioaccumulation pattern, spatiotemporal distribution and human health risk assessment from the tributaries of River Ravi, Pakistan. Hum. Ecol. Risk. Assess. 24, 1268–1290. Campillo, J.A., Fernández, B., García, V., Benedicto, J., León, V.M., 2017. Levels and temporal trends of organochlorine contaminants in mussels from Spanish Mediterranean waters. Chemosphere 182, 584–594. Chiesa, L.M., Nobile, M., Malandra, R., Pessina, D., Panseri, S., Labella, G.F., Arioli, F., 2018. Food safety traits of mussels and clams: distribution of PCBs, PBDEs, OCPs, PAHs and PFASs in sample from different areas using HRMS-Orbitrap® and modified QuEChERS extraction followed by GC-MS/MS. Food Addit. Contam. 35, 959–971. China, 2016. National Food Satety Standard-maximum Redidue Limits for Pesticides in Food. GB 2763–2016. the ministry of agriculture of the People’s Republic of China. EPA, 2000a. Guidance for Assessing Chemical Contaminant Data for Use in Fish Advisories: Risk Assesment and Fish Consuption Limits, 3rd edn. vol 2 US Environmental Protection Agency, Washington, DC.
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Geographical distribution and risk assessment of dichlorodiphenyltrichloroethane and its metabolites in Perna viridis mussels from the northern coast of the South China Sea
T
Runxia Suna, Juan Yub, , Yuhao Liaoa, Jiemin Chena, Zetao Wua, Bixian Maic ⁎
a
School of Marine Sciences, Nanjing University of Information Science and Technology, Nanjing 210044, China School of Materials and Environment, Beijing Institute of Technology, Zhuhai, Zhuhai 519000, China c State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China b
ARTICLE INFO
ABSTRACT
Keywords: DDTs Perna viridis Geographical distribution Risk assessment South China Sea
Mussels (Perna viridis) were collected from the northern coast of the South China Sea (NSCS) to investigate the geographical distribution and potential risk of dichlorodiphenyltrichloroethane and its metabolites (DDTs). DDTs had concentrations that ranged from 248 ng/g to 4650 ng/g lipid weight (lw), with an average of 807 ± 932 ng/ng lw. A comparison of the levels of DDTs in mussels indicated that the NSCS is still one of the most polluted areas in the world, although a decreasing trend was observed. DDT metabolites were predominant in all samples, suggesting that historical residue was the main source of DDT pollution. However, there were new inputs of DDTs which likely associated with antifouling paints. The human health risk assessment revealed that the current concentrations of DDTs in mussels might pose little health risk for the consumers.
Dichlorodiphenyltrichloroethane (DDT) is a persistent organic pollutant (POP) that is ubiquitous, persistent, highly bioaccumulative in nature, and has toxic biological effects (EPA, 2000a; Pheiffer et al., 2018). In China, DDT use reached 0.4 million tons between the 1950s and 1980s, resulting in high levels of residual pesticides in aquatic systems (Sun et al., 2015; Yin et al., 2015). Although DDT has been banned since 1983 (Pan et al., 2016), new input sources of DDT have meant continued discharges into the environment from illegal use (UNDP, 2012; Wang et al., 2011), other pesticides (Huang et al., 2019; Qiu et al., 2005), and antifouling paint (Jin et al., 2008; Xin et al., 2011). It is common that DDT biodegrades into 1,1-dichloro-2,2,-bis(pchlorophenyl) ethane (DDD) and 1,1-dichloro-2,2,-bis (p-chlorophenyl)- ethylene (DDE) (Quensen et al., 1998; Zhao et al., 2018). DDTs (DDT and its metabolites like DDD and DDE) have been found in different aquatic environments due to both old and new pollution sources, all of which pose a danger to humans and animals (Jayasinghe et al., 2019; Mo et al., 2019; Wang et al., 2011; Yin et al., 2015). The coastal regions of the northern South China Sea (NSCS) close to Guangdong province, Guangxi province, and Hainan province have the fast developing economies in the world (Morton and Blackmore, 2001). As a part of that development, various kinds of pesticides were applied in southern China (Li et al., 2018; Wang et al., 2011), increasing the stress of DDT contamination in nearby coastal marine areas (Kaiser
⁎
et al., 2018; Mo et al., 2019; Pan et al., 2016). High levels of DDTs have been detected in the air (Wang et al., 2007), water, and sediment (Fu et al., 2003) from Guangdong province. There was also evidence of a phenomenon where accumulated DDTs in the sediment transferred to aquatic organisms (Leung et al., 2010). Annual levels of DDTs in the tissue of oyster from the coast of the South China Sea increased between 2004 and 2006 (Gan et al., 2009). In addition, the extensive pollution from emerging and aged DDT in the sediments still exists along the coast of the South China Sea (Mo et al., 2019). However, a current regional distribution of DDTs in the NSCS is needed. Thus, the geographical distribution and the possible sources of DDTs in the NSCS have attracted increasing attention. Mussels are widely distributed, have relatively stable habitats, are able to accumulate many contaminants (Monirith et al., 2003), and are often used as ideal bioindicators (over other marine organisms) for marine pollution monitoring (Ramu et al., 2007b). The high protein content of mussels makes them an important part of the human diet in coastal areas. Up to 75% of human DDTs intake has been attributed to the consumption of seafood (Nakata et al., 2002). Unfortunate health and environmental problems may occur due to the exposure to DDTs. In addition, the occurrence of 1-Chloro-2,2-bis(4-chlorophenyl)ethane (p,p′-DDMU), a secondary metabolite of 1,1-dichloro-2,2-bis(4-chlorophenyl)ethane (p,p′-DDD) and 1,1-dichloro-2,2-bis(4-chlorophenyl)
Corresponding author. E-mail address: [email protected] (J. Yu).
https://doi.org/10.1016/j.marpolbul.2019.110819 Received 12 September 2019; Received in revised form 7 December 2019; Accepted 10 December 2019 Available online 29 January 2020 0025-326X/ © 2019 Elsevier Ltd. All rights reserved.
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Fig. 1. Concentrations of DDTs (ng/g lw) in mussels from 22 sampling sites in the NSCS.
standards (PCB 24, 82, and 198) were added prior to instrument analysis. The concentrations of DDTs (the sum of o,p-DDD, p,p′-DDD, o,p -DDE, p,p′-DDE, o,p -DDT, p,p′-DDT, and p,p′-DDMU) were measured by an Agilent 7890A GC coupled to an Agilent 5975B MS with a DB5MS (60 m × 0.25 mm × 0.25 mm, Agilent) capillary column. The elective ion monitoring mode was used, and the injection volume was 1 μl. Helium was the carrier gas flowing at 1.3 ml/min. The injection port and ion source temperatures were 290 °C and 260 °C, respectively. The oven temperature began at 120 °C, increased to 180 °C at a rate of 6 °C/min, later increased to 240 °C at a rate of 1 °C/min, and then increased to 290 °C (15 min hold time) at a rate of 6 °C/min. The instruments were calibrated with regular injections of solvent blanks and standard solutions. All samples were measured in triplicate and after spiking with surrogate standards, and there were regular analyses of procedural blanks, spiked blanks, and spiked matrices. The average recoveries of surrogate standards were 90 ± 14%, 96 ± 9%, and 89 ± 10% for PCB 30, 65, and 204, respectively. The average recoveries were 95%–102% in the spiked blanks, and 92%–105% in matrix-spiked samples for DDTs (o,p-DDD, p,p′-DDD, o,p -DDE, p,p′DDE, o,p -DDT, p,p′-DDT, and p,p′-DDMU). Relative standard deviations were < 15% (n = 3) for all the target chemicals. The method detection limits, set as a signal-to-noise ratio of 3, ranged from 0.005–2.0 ng/g lipid weight (lw). Concentrations of DDTs from the 22 sampling sites in the NSCS are shown in Fig. 1 and Table 1. DDTs concentrations ranged from 248 ng/ g lw to 4650 ng/g lw, and from 6.59 ng/g wet weight (ww) to 105 ng/g ww. The comparison of concentrations of DDTs revealed that DDT levels in mussels in this study were much higher than those from the Marmara Sea coast (Ulusoy et al., 2016), Spanish Mediterranean waters (Campillo et al., 2017), the Black Sea (Georgieva et al., 2016), Italy (Chiesa et al., 2018), and the coastal waters of Korea (Ramu et al., 2007a), but lower than the levels from the River Ravi of Pakistan (Baqar et al., 2018). The higher residual DDT levels in mussels was due to the substantial application of these chemicals during agricultural practices of the past (Monirith et al., 2003). However, the average concentrations in oysters from the coast of Guangdong in 2004–2006 (Gan et al., 2009) and in mussels from the South China Sea (Guo et al., 2010) were 2.64 and 2.27 times higher, respectively than the levels reported in this study. This pattern indicates a decrease in the DDTs contamination
ethene (p,p′-DDE) (Quensen et al., 1998; Sun et al., 2014), has been detected in fish (Guo et al., 2009), birds (Sun et al., 2014), and sediments (Yu et al., 2011a), but information on the contamination of these metabolites in mussels is still relatively scarce. Metabolites of DDT may result in reproductive abnormalities and has been found to be biomagnified through the marine food chain (Falandysz et al., 1999; EPA, 2000a). Therefore, it is necessary to study the residues of mussels in order to evaluate the current levels and risks of DDT and its metabolites. The aims of this study were to determine the level of contamination, the distribution of the contamination, and assess the health risks of DDTs (o,p-DDD, p,p′-DDD, o,p -DDE, p,p′-DDE, o,p -DDT, p,p′-DDT and p,p′-DDMU) associated with consumption of mussels from the NSCS. In addition, we discuss the potential sources of these pollutants. This study will provide a useful reference for environmental protection of these regions. Mussel (Perna viridis) samples were collected from 22 sampling sites along the NSCS coast in 2016. The location and sampling sites are shown in Fig.1. Fifty individuals were obtained at each sampling site through bottom trawling or artificial fishing. Mussels were immediately wrapped in aluminum foil, put into polyethylene bags, and stored on ice in a cooler box for transport from the field. In the laboratory, we collected the total amount of the soft tissues of all mussel samples after removing the shell and mixed the tissues together to create single composite samples by site. All sampled tissues were cut into small pieces, freeze-dried, ground into a uniform powder, and then stored at −20 °C prior to chemical analysis. The samples were extracted and purified according to our previously published method (Sun et al., 2017). Briefly, after the spiking of the samples with surrogate standards polychlorinated biphenyl (PCB) 30, 65, and 204, 3 g of each prepared sample was Soxhlet extracted with 200 ml of dichloromethane and n-hexane (1:1 v/v) for 48 h. The extract was concentrated with a rotary evaporator, and the solvent was changed to hexane. An aliquot of the extract was used to determine lipids by gravimetric measurement. The remaining extract was treated with concentrated sulfuric acid, and further purified using a multilayer column (florisil: neutral silicone: acidic silica gel, 20:2:5 cm). The column was eluted with 80 ml hexane and 60 ml dichloromethane. Under a constant stream of nitrogen gas, the elute was concentrated to near dryness and reconstituted in 200 μl isooctane. The recovery 2
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Table 1 Comparison of DDT concentrations (ng/g) in mussels of reported studies from different countries and regions. Location
Sampling year
Concentration
Reference
Marmara Sea coast Spanish Mediterranean waters Black Sea, Bulgaria Italy Kastela Bay (Croatia) Coastal water, Korea River Ravi, Pakistan South China Coast of Guangdong Northern coast of the South China Sea
2010–2011 2003–2013 2015 2016–2017 2002–2011 2005 2015–2016 2004–2005 2003–2007 2016
1.58 ww 2.7–6.9 ww 2.14 ww nd-16.3 ww 0.39–1.4 ww 21–400 lw (144)a 46.4–1010 ww (318)a 3.95–507 ww (65.7)a 58.4–5620 lw (1480)a 6.59–105 ww (27.2)a 248–4650 lw (807)a
Ulusoy et al. (2016) Campillo et al. (2017) Georgieva et al. (2016) Chiesa et al. (2018) Milun et al. (2016) Ramu et al., 2007a Baqar et al. (2018) Guo et al. (2010) Gan et al. (2009) This study
a
Average value.
Table 2 Average concentrations (and ranges) of DDT and its metabolites in mussels from different sites in the NSCS; units of ng/g lw. Regions
Number of sampling sites
DDTs
p,p′-DDE
p,p′-DDD
p,p′-DDMU
(DDD + DDE)/DDTs
ECG PRE WCG CG CH Average (range)
6 2 7 3 4
732 (248-1690) 2546 (441-4650) 462 (270-689) 452 (354-616) 919 (328-1320) 807 (248-4650)
192 455 160 140 248 209
292 1630 224 225 350 394
14.5 (8.60–28.0) 33.5 (12.1–55.0) 13.2 (8.2–20.3) 9.7 (7.5–12.7) 16.4 (6.80–21.5) 15.5 (6.80–55.0)
0.79 0.93 0.93 0.93 0.74 0.86
o,p-DDE
p,p'-DDE
o,p-DDD
p,p'-DDD
o,p-DDT
p,p'-DDT
(0.56–0.92) (0.89–0.97) (0.90–0.97) (0.90–0.97) (0.71–0.77) (0.56–0.97)
p,p'-DDMU
Percentage of DDTs
100% 80% 60% 40% 20% 0% Sampling sites Fig. 2. Composition profiles of DDTs in mussels from sampling sites in the NSCS.
coast of Hainan region, including sites S19 to S22. The average levels of DDTs in ECG, PRE, WCG, CG, and CH were 732 ng/g lw, 2546 ng/g lw, 462 ng/g lw, 452 ng/g lw, and 919 ng/g lw, respectively (Table 2). In a regional comparison, the average level of DDTs deceased in the following order: PRE > CH > ECG > WCG > CG (Table 2). However, no significant differences were found by t-test in comparisons of CH with ECG, or ECG with WCG. The reason for this observation might be due to the small sample numbers (Sun et al., 2014). In addition, some sites with levels exceeding 1000 ng/g lw (S4, S7, S19, S20) increased the average levels of those regions (ECG, PRE, and CH). The highest level recorded was at site S4 in Changsha bay, which was 2.31 times higher than the average level (732 ng/g lw) of the ECG region, and 1.24 times higher than reported for the same area in a previous study measuring DDT levels in oysters from Changsha bay in 2005 (Gan et al., 2008), suggesting the possible increase in DDT loads at site S4. However, the report showed that average levels in oysters in the ECG (1730 ± 1060 ng/g lw) and WCG (1200 ± 1040 ng/g lw) regions between 2003 and 2007 were 2.36 and 2.59 times higher, respectively, than the levels reported in this study (Gan et al., 2009), suggesting the possible decrease in DDT loads in the system. Mussels and oysters were used as potential bioindicators of DDTs. Content differences of DDTs in
Table 3 Peak concentrations of DDTs (ng/g lw) by sampling site. Sample
Location
DDTs
(DDD + DDE)/DDT
o,p-DDT/p,p′-DDT
S4 S7 S19 S20
Changsha bay Shenzhen bay Dongzhai harbor Maniao harbor
1690 4650 1320 1040
0.56 0.97 0.74 0.72
1.01 0.18 0.13 0.13
along the South China Sea coast between 2004 and 2016. The degraded forms of DDT were the predominant form of the pollutant in the sediments of the NSCS, which could also support the conclusion that new DDT pollution has decreased in the last decade (Kaiser et al., 2018; Yu et al., 2011a). To better understand the regional distributions, we divided the sampling sites into five geographical regions. As shown in Fig.1 and Table 2, the sampling regions were named 1) ECG, for the east coast region of Guangdong, including sites S1 to S6, 2) PRE, for the Pearl River estuarine region, including sites S7 to S8, 3) WCG, for the west Coast of Guangdong region, including sites S9 to S15, 4) CG, for the coast of Guangxi region, including sites S16 to S18, and 5) CH, for the 3
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mussels and oysters in the same region were < 300 ng/g lw (Wang et al., 2008). Much higher levels in the past indicated that levels of DDTs around the Guangdong coast may be decreasing. However, our highest level recorded in mussels (site S7, Shenzhen bay) was 2.62 times higher in DDTs than the previous report in oyster (1772 ng/g lw) (Gan et al., 2009). Shenzhen bay was in the PRE region, which is influenced by the runoff discharge from agricultural land erosion and shipping activities in the Pearl River catchment. This indicates the possible influence of sources including historical residues and new inputs of DDTs. Emerging and legacy pollutants were found in the sediments around Hainan Island (Mo et al., 2019). High levels (S19, S20) were observed in the CH region, which might be attributed to the higher background levels of DDTs in the CH region. Possible sources of DDTs in the S4, S7, S19, and S20 sites will be discussed more below. The composition profiles of DDTs in mussels from the NSCS are shown in Fig. 2. DDT and its degraded derivatives (DDD, DDE, DDMU) were all detected. Overall, the composition profile of DDTs showed the highest contribution was from p,p′-DDD (48.8%), followed by p,p′-DDE (25.9%), o,p-DDD (9.89%), p,p′-DDT (9.85%), o,p-DDT (3.2%), p,p′DDMU (1.92%), and o,p-DDE (0.45%) (Fig. 2). Higher proportions of degraded derivatives suggest the enhanced degradation of DDT. p,p′DDD was the predominant compound accumulated in the mussels. Similar accumulation contributions were reported in mussels along the Pearl River Delta (DDD, 49%) (Fang, 2004), in bivalves from the northeast coast of China (DDD, 46%) (Jin et al., 2008), and in shellfish from coast of Xiamen (p,p'-DDD, 54%) (Zhang et al., 2012). Industrial DDT consists of 75% p,p'-DDT, 15% o,p-DDT, 5% p,p'-DDE, < 0.5% o,pDDE, < 0.5% p,p'-DDD, < 0.5% o,p-DDD, and < 5% of unidentified compounds (Gan et al., 2009). DDT can be degraded into DDD and DDE under anaerobic and aerobic conditions, respectively (Yu et al., 2011a). When the ratio of DDD/DDE is higher than 1, this indicates anaerobic metabolism of the DDT. DDE in mussels primarily comes from the ambient environment instead of biotransformation processes, while DDD in mussels follows dietary uptake and biotransformation of DDT inside the organism (Kwong et al., 2009). The predominant form of DDD in mussel tissues indicated that the accumulation in mussels was influenced by dietary uptake and biotransformation of the DDT. The ratios of (DDE + DDD)/DDTs have been used to distinguish the main source of DDTs from fresh inputs (ratio < 0.5) or historical uses (ratio > 0.5) (Yu et al., 2011a). In this study, the ratios of (DDE + DDD)/DDTs ranged from 0.56 to 0.97, with an average value of 0.86 (Table 2). This is consistent with the ratio measured in birds in Guangdong Province (Sun et al., 2014), indicating that historical residues are likely the main source of DDT in the mussels of the NSCS. This result agrees with the banned usage of DDT by the government starting in 1983, which reduced the input of industrial DDT. The properties of DDT make both DDT and its degraded derivatives persistent in the environment. We measured some high levels in sites S4, S7, S19, and S20 with (DDE + DDD)/DDTs ratios of 0.56, 0.97, 0.74, and 0.72, respectively (Table 3). The smallest ratio (0.56) was in site S4
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p,p-'DDD/(p,p-'DDD+p,p-'DDE) Fig. 3. Correlations of concentrations of p,p′-DDD (a) and p,p′-DDE (b) plotted against p,p′-DDMU, and concentrations of p,p′-DDMU/DDTs plotted against p,p′-DDD/(p,p′-DDD + p,p′-DDE) and (c) in mussels from the NSCS.
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Sampling sites Fig. 4. Concentrations of DDTs and EDI (y coordinate on the left) and cancer risks (y coordinate on the right) in mussels from 22 sites from the NSCS. 4
Marine Pollution Bulletin 151 (2020) 110819
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along with a high DDT concentration, implying that there might be a new input of DDT in site S4. Site S4 was located in a mariculture zone. It is reported that antifouling paints on the hulls of boats may be an important source of DDTs to the mariculture zones of South China (Yu et al., 2011b). Ratios of o,p-DDT/p,p′-DDT can be diagnostic of their sources (Venkatesan et al., 1996; Zhang et al., 2018). Previous studies confirmed that DDT pollution caused by antifouling paints had a higher o,p-DDT/p,p′-DDT concentration ratio (ranging from 0.4 to 1.1; averaged at 0.75) (Wang et al., 2007) than that of technical DDT (around 0.2–0.3) (Qiu et al., 2005). The o,p-DDT/p,p′-DDT concentration ratio was 1.01 in site S4 (Table 3), indicating a possible antifouling paint input source. Other high DDT levels were measured in sites S7, S19, and S20 with higher (DDE + DDD)/DDTs ratios that implied the residues of historical applications of DDTs. The o,p-DDT/p,p′-DDT concentration ratios in sites S7, S19, and S20 were 0.18, 0.13, and 0.13, respectively, which also confirms the conclusion of historical residues rather than new sources. There were detectable levels of p,p′-DDMU in all the samples. The concentrations ranged from 6.80 ng/g lw to 55.0 ng/g lw, with an average of 15.5 ng/g lw (Table 2); this was the same regional distribution pattern as the concentrations of p,p′-DDE and p,p′-DDD. p,p′DDMU in the mussels in this study was lower than those reported in birds (nd-80 ng/g lw) (Sun et al., 2014), and seawater wild fish (average 25.5 ng/g lw) (Guo et al., 2009) from Guangdong Province. By correlation analysis, p,p′-DDMU levels were significantly correlated with p,p′-DDD (r = 0.93, p < 0.01) and p,p′-DDE (r = 0.98, p < 0.01; Fig. 3a and b), suggesting that p,p′-DDMU in mussels might be derived from the dehydrochlorination of p,p′-DDE or p,p′-DDD (Quensen et al., 1998). The correlation between p,p′-DDD/(p,p′-DDD+ p,p′-DDE) and p,p′-DDMU/DDTs was tighter in the sediments than in farmed fish, indicating that bioaccumulation of p,p′-DDMU was partially related to dehydrochlorinated from DDD in the environment (Guo et al., 2009). A negative linear correlation was found between p,p′DDD/(p,p′-DDD+ p,p′-DDE) and p,p′-DDMU/DDTs (r = 0.51, p < .05) in mussels (Fig. 3c), similar to the correlation seen in seawater fishes (Guo et al., 2009), indicating that DDMU was also partially dehydrochlorinated from DDD in the environment. The concentrations of DDTs based on wet weight in mussels are shown in Fig. 4, ranging from 6.59 ng/g ww to 105 ng/g ww. According to GB2763-2016, the extraneous maximum residual level (EMRL) of DDTs recommended for aquatic products is 500 ng/g ww (China, 2016). The concentrations in the mussels were all below the suggested EMRL set by the Chinese government. DDTs intake from consumption of mussels for local residents was estimated by the equation as follows: the estimated daily intake (EDI, (ng/kg)/d) = contaminant concentration (ng/g)/body mass (kg) × daily consumption (g/d). The average contaminant concentration was 27.2 ng/g. A Chinese adult consumer was assumed to have a mean body mass of 60 kg. The daily consumption levels of mussels was 0.0245 kg/d for males by a dietary survey (Guo et al., 2010). The EDIs of DDTs ranged from 2.67 ng/kg/d to 42.88 ng/kg/d (Fig. 4). The average EDI was estimated to be 11.12 ng/kg/d, which was lower than the average EDI for aquatic organisms from the Pearl and Dongjiang Rivers (Sun et al., 2017), and far below the oral reference dose (RfD, 500 ng/kg/d) proposed by the United States Environmental Protection Agency (EPA, 2000a). To estimate the carcinogenic effects, human carcinogenic risk level (CRL) associated with the consumption of mussels from different locations were estimated by the following equation: CRL = contaminant concentration (ng/g) × daily consumption (g/d) × cancer slope factor (mg/kg/day)−1/body mass (kg) (Watanabe et al., 2003). The DDT contaminant concentrations are shown in Fig. 4. The daily consumption levels of mussels was 0.0245 kg/d (Guo et al., 2010). To compare this result with the EPA guidelines, body mass was assumed to be 70 kg (EPA, 2000a). Cancer slope factor (0.34 (mg/kg/day)−1) was obtained from the EPA Guidance for Assessing Chemical Contaminant Data for
Use in Fish Advisories (EPA, 2000a). The CRL in different samples ranged from 7.85 × 10−8 to 1.25 × 10−5 with an average of 3.24 × 10−6 (Fig. 4). Most samples were below the risk level for carcinogens (10−5), indicating that the risk of cancer in most samples were in an acceptable range. However, the levels of DDTs in 9% of the samples were slightly above the risk level for carcinogens suggested by the USEPA (EPA, 2000b). This suggests that consumption of the mussels from some sites might pose a human health risk. We observed the spatial distribution of DDT concentration and composition in the soft tissues of P. viridis mussels collected from the coast of the NSCS in this study. Our comparison of DDT levels revealed a decrease in DDTs around the South China coast. In a regional comparison, the average concentrations of DDTs decreased in the following order: PRE > CH > ECG > WCG > CG. Higher proportions of degraded derivatives suggested the degradation of DDT. The predominant compound of DDD indicated that the accumulation in mussels was influenced by dietary uptake and biotransformation of DDT. There were detectable levels of p,p′-DDMU in all the samples. p,p′-DDMU levels were significantly correlated with p,p′-DDE and p,p′-DDD, indicating that p,p′-DDMU might be derived from dehydrochlorination of p,p′-DDE or p,p′-DDD. The historical use of DDTs was the main source of DDTs in the NSCS, but there were some new inputs of DDTs, likely associated with antifouling paints. Mussel sample DDT levels were below the suggested EMRL set by China. The EDI was also far below the oral reference dose (RfD, 500 ng/kg/d) proposed by USEPA. However, a cancer risk assessment suggested dietary consumption of mussels exposed to DDTs in some sites might pose a human health risk. Author contribution statement Runxia Sun: Conceptualization, Methodology, Investigation, Software, Data curation, Writing-Reviewing and Editing. Juan Yu: Conceptualization, Investigation, Software, Resources, Writing-Reviewing and Editing. Yuhao Liao: Investigation. Jiemin Chen: Investigation. Zetao Wu: Investigation. Bixian Mai: Resources, Writing-Reviewing and Editing. Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgment This study was funded by the National Natural Science Foundation of China (Nos. 41703100, and 41977302), and the Startup Foundation for Introducing Talent of NUIST (No. 2018r069). References Baqar, M., Sadef, Y., Ahmad, S.R., Mahmood, A., Li, J., Zhang, G., 2018. Organochlorine contaminants in freshwater mussels; occurrence, bioaccumulation pattern, spatiotemporal distribution and human health risk assessment from the tributaries of River Ravi, Pakistan. Hum. Ecol. Risk. Assess. 24, 1268–1290. Campillo, J.A., Fernández, B., García, V., Benedicto, J., León, V.M., 2017. Levels and temporal trends of organochlorine contaminants in mussels from Spanish Mediterranean waters. Chemosphere 182, 584–594. Chiesa, L.M., Nobile, M., Malandra, R., Pessina, D., Panseri, S., Labella, G.F., Arioli, F., 2018. Food safety traits of mussels and clams: distribution of PCBs, PBDEs, OCPs, PAHs and PFASs in sample from different areas using HRMS-Orbitrap® and modified QuEChERS extraction followed by GC-MS/MS. Food Addit. Contam. 35, 959–971. China, 2016. National Food Satety Standard-maximum Redidue Limits for Pesticides in Food. GB 2763–2016. the ministry of agriculture of the People’s Republic of China. EPA, 2000a. Guidance for Assessing Chemical Contaminant Data for Use in Fish Advisories: Risk Assesment and Fish Consuption Limits, 3rd edn. vol 2 US Environmental Protection Agency, Washington, DC.
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