Primary investigation on contamination pattern of legacy and emerging halogenated organic pollutions in freshwater fish from Liaohe River, Northeast China

Environmental Pollution 172 (2013) 94e99

Contents lists available at SciVerse ScienceDirect

Environmental Pollution journal homepage: www.elsevier.com/locate/envpol

Primary investigation on contamination pattern of legacy and emerging halogenated organic pollutions in freshwater fish from Liaohe River, Northeast China Guofa Ren a, *,1, Zhao Wang a, Zhiqiang Yu b, *,1, Yang Wang a, Shengtao Ma b, Minghong Wu a, Guoying Sheng b, Jiamo Fu a, b a

Institute of Environmental Pollution and Health, School of Environment and Chemical Engineering, Shanghai University, 99 Shangda Road, Baoshan Disrict, Shanghai 200072, China State Key Laboratory of Organic Geochemistry, Guangzhou Key Laboratory of Environment Protection and Resource Utilization, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 9 April 2012 Received in revised form 12 June 2012 Accepted 18 August 2012

Legacy halogenated compounds, including polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs), and emerging organo-halogen pollutants such as Dechlorane Plus (DP), were detected in fish from an old industrial region in Northeast China. PCBs and PBDEs were detected in all of the samples, with concentrations ranging from 38.15 to 170.51 ng/g lipid weight, and 9.40e39.69 ng/g lipid weight, respectively. DP was detected in more than 90% of the samples with concentrations ranging from not detected (ND) to 470 pg g/g lipid weight. Compared with similar data in other areas of the world, PCBs, PBDEs and DP in fish from Liaohe River were at medium or low level. An unusually high percentage of PCB-209 was first reported in the fish samples collected from China. Other halogenated pollutions, such as dichlorodiphenyltrichloroethane (DDT) and its metabolites, octachlorostyrene, chlorinated anisole, chlorinated thioanisole, triclosan-methyl, and other pesticides, have also been identified in the fish samples. Ó 2012 Elsevier Ltd. All rights reserved.

Keywords: Polybrominated diphenyl ethers (PBDEs) Polychlorinated biphenyls (PCBs) Dechlorane Plus (DP) Nontarget screening

1. Introduction Halogenated organic chemicals have been widely used in agriculture and industry. Concern arises as a result of toxic, bioaccumlative, persistent, and potential adverse human and environmental health effects of these substances (Bull et al., 2011; Clarke and Smith, 2011; Muir and Howard, 2006). PCBs and PBDEs are two classes of halogenated organic compounds that are listed in the Stockholm Convention on POPs. PCBs were historically used in a variety of products as dielectric and hydraulic fluids. Although the production and use of PCBs has been banned all over the world since 1970s, its residues are still found in the environment owing to their persistence and bioaccumulation (Domingo and Bocio, 2007). PBDEs are one class of brominated flame retardants (BFRs) widely used in electronic appliances, textiles, furnishings and various other consumer products over world. Like PCBs, PBDEs have become ubiquitous environmental pollutants. There are three primary commercial PBDE formulations:

* Corresponding authors. E-mail address: [email protected] (G. Ren). 1 These authors should be regarded as joint first authors. 0269-7491/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.envpol.2012.08.012

penta-, octa-, and deca-BDE (Hites, 2004). Recently, the main components of penta- and octa-BDE mixtures have been recommended for elimination as persistent organic pollutants under the Stockholm Convention. Deca-BDE is currently the only PBDE product in production and use. Dechlorane Plus (DP) is a highly chlorinated flame retardant mainly used in coating electrical wires and cables, connectors used in computers, and plastic decoration materials (Qiu et al., 2007). It is only recently detected in the environment even though it has been produced for almost fifty years (Hoh et al., 2006). DP is primarily detected in the air and sediment near the Great Lakes (Hoh et al., 2006; Qiu et al., 2007; Sverko et al., 2011). Biotic monitoring data of DP isomers are very limited and the limited information about DP are primarily focused on the “hot” regions because of the presence of DP manufacturing plant or e-waste dismantling. Hoh et al first reported that DP can be bioacuumlated in fish (Hoh et al., 2006). Tomy et al. showed that the bioaccumulation of DP for certain organism is different in food webs of Lakes Winnipeg and Ontario (Tomy et al., 2007). Wu et al reported high level of DP in the mud carp from an e-waste dismantling site in South China (Wu et al., 2010). Urban/industrial regions were ascribed as another main emission source of DP for these regions.

G. Ren et al. / Environmental Pollution 172 (2013) 94e99

Recently, DP isomers were detected in fish collected from 22 river sites across South Korea. The result demonstrated that DP urban concentrations were approximately 25 times greater than those measured in rural areas, for which industrial emission played a vital role (Kang et al., 2010). It is necessary to pay attention to the environmental fate and risk assessment of this emerging contaminant in fish from regions close to urban/industrial regions. In addition to the so called legacy and emerging pollutants, there is a diverse group of unregulated halogenated organic pollutants, including pesticide, pharmaceuticals, personal care products, and their environmental transformation products (Muir and Howard, 2006). Screening, identification, and quantification of these chemicals are essential to modern society. The challenge for the analysis of these “unknown” is the separation and identification of these compounds from the complex matrix. Recently, Comprehensive twodimensional gas chromatography/time of flight mass spectrometry (GC
GCeTOFMS) has been proved to be a powerful tool for the screening of priority and emerging pollutants in environmental samples (Hilton et al., 2010; Johanningsmeier and McFeeters, 2011; Jose Gomez et al., 2011). The major benefits of GC
GC in environmental analysis are improvements in trace analysis by increasing sensitivity and the resolution of target compounds from coextracted impurities and interferences. The high scanning rate and full-scan mass spectral acquisition of the TOFMS additionally opens the possibility for identification of other (un)expected halogenated toxicants that are potentially present in samples. The benefit of coupling GC
GC with TOFMS includes simultaneous determination of hundreds if not thousands of pollutants at low levels in a single analysis. In this study we used GC
GCeTOFMS to screen for all detectable halogenated pollutants in fish samples collected from the Liaohe River, Northeast China. To our knowledge, few studies focused on the legacy halogenated compounds, including polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs), in Northeast China, an important old industrial base. In particular, no previous study has been conducted to examine the DP level in fish samples collected from this region. The general aim of this study was to determine the levels, congener profiles of above-mentioned legacy and emerging halogenated organic pollutions in freshwater fish from Liaohe River, Northeast China. Moreover, analysis of samples for nontargeted halogenated pollutants in fish samples by GC
GCe TOFMS is also presented in this study. 2. Materials and methods 2.1. Sampling program and collection The Liaohe River, located in the southwestern part of Northeast China, is one of the most heavily polluted rivers in China. The study area (122 350 e123 350 E, 41090 e41490 N) is located in the middle of Liaoning province, Northeast China. All fish samples were collected by commercial fisherman from six sites in early August 2010. The detailed information on the sampling site and the investigated fish species is shown in Fig. S1 and Table S1. The samples were stored in ice-boxes and transported to laboratory immediately after collection. After the body size and body weight were recorded, the collected fish were filleted, and only muscle tissues were selected for analysis. Several individual fish muscle in the same site were combined and homogenized to provide a pooled sample, which contributed to 18 pool samples. The samples were freeze-dried, transferred to a glass jar, and frozen until analysis. 2.2. Sample extraction and clean-up A detailed description of the method used for extraction and gravimetric lipid weight determination has been described in elsewhere (Xiang et al., 2007). Briefly, approximately 5 g freeze-dried sample were subjected to soxhlet extraction using a mixture of 400 mL n-hexane/acetone (1:1, V/V) for 72 h. The concentrated extracts were purified by GPC and on a multilayer silicaealumina column chromatography which was packed (in order, from the base) with 6 cm of alumina, 2 cm of silica gel (100e200 mesh), 5 cm of alkaline silica gel, 2 cm of silica gel, 6 cm of acidic silica gel,

95

and 1 cm anhydrous sodium sulfate. Internal standard (13C-PCB-208) was added prior to GCeMS analysis. Detailed information is given in the Supplemental Data. 2.3. Instrumental analysis Target PCB standards included 41 congeners (IUPAC congener numbers 17, 18, 28, 31, 33, 44, 49, 52, 70, 74, 82, 87, 95, 99, 101, 105, 110, 118, 128, 132, 138, 149, 151, 153, 156, 158, 169, 170, 171, 177, 183, 186, 187, 191, 194, 195, 199, 205, 206, 208, 209). The determination of PCBs was performed with an Agilent 6890N gas chromatograph (GC) coupled to an Agilent 5975 mass spectrometer (MS). A DB-XLB capillary column (30 m, 250 mm internal diameter, 0.25 mm film thickness, Agilent) was used to determine the PCBs. The GC program comprised a GC ramp of 110  C held for 2 min; 5  C/min to 200  C; held for 2 min and 2  C/min to 280  C held for 5 min. The injector and interface temperatures were held at 280  C and 290  C, respectively. Helium was used as the carrier gas and a 1 mL of sample was injected in splitless mode. The MS was operated in electron ionization (EIþ) selected ion monitoring mode (SIM), using the two most intense ions of the molecular ion cluster. Target PBDE standards included 13 congeners (IUPAC congener numbers 17, 28, 47, 66, 71, 85, 99, 100, 153, 154, 183, 190, 209). PBDEs and DP (syn- and anti-) were analyzed by gas chromatographemass spectrometer (GCeMS; Agilent 7890A with Agilent 5975C) in negative chemical ionization (NCI) and operated in selected ion monitoring (SIM) mode. A DB5-MS capillary column (30 m, 250 mm internal diameter, 0.25 mm film thickness, Agilent) was used to determine the tri- to heptaBDEs (BDE-17,-28,-47,-66,-71,-85,-99,-100,-138,154,-183,-190). For deca-BDEs (BDE209) and DP, a DB-5HT capillary column (15 m, 250 mm internal diameter, 0.10 mm film thickness, Agilent) was used. Details of the GC temperature program and monitored ions for all analyses were given in our previous report (Ren et al., 2009). Analysis of samples for non-targeted halogenated pollutants was achieved by the comprehensive two-dimensional gas chromatography/time of flight mass spectrometer (GC
GCeTOFMS). The GC
GCeTOFMS instrument was the Pegasus 4D (Leco Corp., St Joseph, MI). Instrumental analysis details were adopted from reference with a minimal change and only a brief description was given here (Focant et al., 2004). The GC column set used was made of the combination of a DB5-MS (30 m, 250 mm internal diameter, 0.25 mm film thickness, Agilent) as 1D and a high temperature HT-8 (1.2 m, 250 mm internal diameter, 0.10 mm film thickness, SGE) as 2D. During chromatographic separation, the primary GC oven was programmed as follows: 110  C (1 min hold), then to 180  C at 8  C/min, then to 240  C at 2  C/min (5 min hold), then to 280  C at 2  C/min (5 min hold), and finally to 300  C at 20  C/min (5min hold). The 2D column was coiled into the secondary oven that was 20  C higher than the primary oven and was operated in the iso-ramping mode. The temperature of the modulator had an offset of 30  C compared with the temperature of the primary GC oven. Modulation was carried out on the very beginning of the 2D column. The modulator period was 4 s with a hot-pulse duration set at 1200 ms and a cooling time between stages of 800 ms. The mass spectrometer was used in the EI mode. The mass range of 50e750 Da was acquired at a data acquisition rate of 50 Hz. 2.4. Quality assurance/quality control/(QA/QC) and data analysis For the target compounds, quality assurance/quality control (QA/QC) measures include matrix spiked samples, procedural blanks, and sample triplicates. Only trace of BDE-209 and BDE-47 were detected in the procedural blanks, and the mean concentrations were subtracted from those in samples Concentrations were presented as ng/g lipid weight and pg/g wet weight for PCBs and PBDEs and pg/g lipid weight for DP to keep the data consistent with most of literature. The recoveries of the spiked standards were 85  14% for PCBs congeners, 92  11% for PBDEs congeners, and 95  4 for DP isomers, respectively. Data analyses were performed using SPSS 13.0 for Windows. For the analysis of samples for non-targeted halogenated pollutants, GC
GCeTOFMS software’s library search function was used for analyte matches. Compounds containing chlorine or bromine were identified automatically and further manually corrected when required.

3. Results and discussion 3.1. Concentrations of PCBs, PBDEs and DP P P P Concentrations of PCBs, PBDEs, and DP in freshwater fish samples from Liaohe River were shown in Fig. 1. Concentrations of P PCBs ranged from 38.15 to 170.51 ng/g lipid weight, with the mean value of 89.14 ng/g lipid weight (median value 72.60 ng/g lipid weight). The PCB concentrations in the present study were similar to those collected from Taihu Lake (Yu et al., 2012), Baiyangdian Lake (Dai et al., 2011), but a little higher than those from Pearl River Estuary and Tibetan Plateau in China (Meng et al., 2007; Yang et al., 2010) (Table 1). Globally PCB concentrations in fish samples have been reviewed in literature (Bettinetti et al.,

96

G. Ren et al. / Environmental Pollution 172 (2013) 94e99

Fig. 1. Concentrations of from Liaohe River.

P

PCBs,

P P PBDEs and DP in fish muscle samples collected

2012; Letcher et al., 2010; Turyk et al., 2012). Comparatively, concentration levels of PCBs in this study were quite lower than those from other countries, which is in line with the fact that the amounts of PCBs manufactured and used in China were relatively minor. Compared to PCBs, the concentrations of PBDEs were signifiP cantly (t-test: p < 0.05) less in these fish samples with the PBDEs ranging from 9.40 to 39.69 ng/g lipid weight (mean and median value was 18.89 and 16.41 ng/g lipid weight, respectively). To compare the PBDE levels with other studies, total PBDE concentrations and concentrations of an individual congener (BDE-47, the most abundant and commonly congeners analyzed) were used P (Table 1). The mean PBDEs concentrations (18.89 ng/g lw) were comparable to those from Pearl River Estuary, which were 14.9 ng/g lipid weight (Meng et al., 2007), from Nongkeng River, which were 35.0 ng/g lipid weight (Xu et al., 2009), and those from Taihu Lake, which varied from 8.6 to 74.3 ng/g lipid weight (Yu et al., 2012). The average BDE-47 concentration in the muscle of freshwater fish samples in the present study (6.05 ng/g lipid weight) is also similar to that in fish from Nongkeng River (15 ng/g lipid weight) (Xu et al., 2009) and the Taihu Lake in China (1.99e33.98 ng/g lipid weight) (Yu et al., 2012). The total PBDE concentrations in fish investigated in our study were much lower than those from other countries.

Concentrations of total PBDEs in fish from Kuwait ranged from 0.50 to 3.78 ng/g wet weight (BDE-47 ranged from 0.22 to 1.21 ng/g wet weight) (Helaleh et al., 2012), and in fish from the Hudson River ranged from 2.12 to 169.0 ng/g wet weight (BDE-47 ranged from 1.26 to 88.6 ng/g wet weight) (Skinner, 2011). These concentrations found in fish were higher than the results found in this study. DP was detected in more than 90% (17 out of 18 pooled samples) of the fish samples. P Mean concentrations of DP in the freshwater fish were 223 pg/g lipid weight (ranging from N.D. to 470 pg g/g lipid weight, median value 215 pg/g lipid weight), which were also significantly (t-test: p < 0.05) less than those of PCBs and PBDEs. Limited data on DP levels in fish samples have been reported in literature. Table 2 summarized the reported values from different areas of the world. A simple comparison based on average concentration was made between our data and the data from these studies. As Table 2 indicated, the highest ever-reported DP levels in fish samples came from a reservoir near the e-waste recycling plants, South China (Wu et al., 2010), with 4e5 orders of magnitude higher than those in our samples. Relatively high DP concentrations compared to those found in the Great Lakes had been reported in fish samples collected in urban-industrial areas of South Korea (Kang et al., 2010), which was about 1e2 orders of magnitude higher than those in this study. Comparatively, lower DP levels were observed, with mean concentrations 223 pg/g lipid weight in this study, similar to those of some remote areas of the Great Lakes (Hoh et al., 2006; Tomy et al., 2007). 3.2. Compositional patterns of PCBs, PBDEs and the isomer ratios of DP In all fish samples, deca-chlorinated homolog (PCB-209) was the most abundant congener with the average contribution of 44.0% to total PCB concentrations. Fig. 2, which was obviously different from those previously reported in most of the world. In those studies, the contributions of PCB-209 to total PCBs were usually small (Domingo and Bocio, 2007; Srogi, 2008). PCB-209 had even been used as surrogate standard for determination of PBDEs due to its similar structure to PBDEs and low detection frequency in the natural environment (Xiang et al., 2007). Except PCB-209, the tri-, tetra-, penta-, and hexa-chlorinated homolog made almost equal contributions to the observed total PCB concentrations (average contributions of 10.6%, 9.3%, 15.9%, and 11.0%, respectively,

Table 1 Comparison of the mean concentrations of PCBs and PBDEs in fish samples collected from Liaohe River with those in wild freshwater fish in different areas of the world. Contaminants Area

Sample year

Congeners (numbers)

Mean/mean range

References

Liaohe River, Liaoning Province

2010

Tri- to deca-PCBs (40)

This study

Taihu Lake, Jiangsu Province Baiyangdian Lake, Hebei Province Pearl River Estuary, Guangdong Province Tibetan Plateau, China Maggiore Lake, Northern Italy

2009 2008 2004e2005

Tri- to nona-PCBs (32) Tri- to hepta-PCBs, (5) Aroclor mixture (70)

89.14 ng/g lipid weight or 1.4 ng/g wet weight 10.3e165.2 ng/g lw 0.53e3.28 ng/g ww 14.9 ng/g lw

2007 2009e2010

Liaohe river, Liaoning Province

2010

Taihu Lake, Jiangsu Province

2009

Pearl River Estuary, Guangdong Province Nongkang River, Jiangsu Province Kuwait Hudson River, USA

2004e2005

Mon- to deca-PCBs (25) 0.32 ng/g ww Tri- to hepta-PCBs (9) 500e2500 ng/g lw P PBDEs Tri- to hepta-BDEs, 18.9 ng/g lipid weight and BDE-209 (13) or 0.31 ng/g wet weight Tri- to hepta-BDEs, 8.6e74.3 ng/g lw and BDE-209 (13) Tri- to hepta-BDEs, 14.9 ng/g lw and BDE-209 (11) Tri- to hepta-BDEs (13) 35 ng/g lw

PCBs

PBDEs

2007e2008

Not available Tri- to deca-BDEs (18) 2003 Tri- to hepta-BDEs (46)

0.50e3.78 ng/g ww 2.12e169.0 ng/g ww

(Yu et al., 2012) (Dai et al., 2011) (Meng et al., 2007) (Yang et al., 2010) (Bettinetti et al., 2012) BDE-47 6.05 ng/g lipid weight This study or 0.17 ng/g wet weight 1.99e33.98 ng/g lw (Yu et al., 2012) Not available

(Meng et al., 2007)

13 ng/g lw

(Xu et al., 2009)

0.22e1.21 ng/g ww 1.26e88.60 ng/g ww

(Helaleh et al., 2012) (Skinner, 2011)

G. Ren et al. / Environmental Pollution 172 (2013) 94e99

97

Table 2 Comparison mean DP concentrations (pg/g lipid weight) and fractions (fanti) in fish samples collected in different areas of the world. Location

Sample description

Sample year

Syn-DP

Anti-DP

DP

fanti

Reference

USA USA

Lake Erie Lake Winnipeg Lake Ontario E-waste site Reference sample Urban sites Rural sites Urban sites

Archived fish 2000e2003 2000e2003 2006 2006 2008 2008 2010

e 29e450 7e1307 64,130-496,200 1350 250e30,000 170e900 82

e N.De760 8e3108 30,030e1,212,000 7410 560e97,000 440e2700 141

140e910 35e820 15e4410 255,000e1,970,000 e 36,100 1400 223

0.60 0.039e0.961 0.512e0.704 0.14e0.54 0.84 0.67 0.71 0.57

(Hoh et al., 2006) (Tomy et al., 2007) (Tomy et al., 2007) (Wu et al., 2010) (Wu et al., 2010) (Kang et al., 2010) (Kang et al., 2010) This study

Qingyuan, China South Korea Liaohe River, China

see Fig. 2.). Unusually high concentration of PCB-209 has also been detected in water, sediment, and aquatic biota in the Houston Ship Channel, Texas, which were quite similar to the results in this study (Howell et al., 2008; Hu et al., 2011; Lakshmanan et al., 2010). PCB209 was not present in the most common commercial Aroclor mixtures (Aroclors 1016, 1242, 1248, 1254, and 1260). Some studies have attributed PCB-209 to Aroclor 1268, a heavier technical mixture that contains PCB-209 (Kannan et al., 1997). Other studies have demonstrated PCB-209 can be formed during the process of perchlorination from phthalocyanine blue to phthalocyanine green and titanium dioxide purification (Hu and Hornbuckle, 2010; Rowe et al., 2007). The unusually high concentrations in the fish samples indicated that there were distinct sources of pure PCB-209 in the region of Liaohe River. However, current information on the use and production of PCB-209 is limited in China and many questions need further investigation. Amongst all fish samples, the prominent congeners were BDEs28, -47 -153, -154 and 209, which constituted 71.7e88.9% of the total PBDE concentration. BDE-47 was the most abundant congener with the average contribution of 34.0% to total PBDE concentrations, which was in line with the results from many other studies (Supplemental data, Fig. S2). After BDE-47, BDE-209 was the second most predominant PBDEs congener with the average contribution of 18.9% to total PBDE concentrations. These results were consistent with those reported in freshwater fish and marine fish samples collected in China (Su et al., 2010; Wang et al., 2011). However, they were obviously different from those reported in North America and Europe, where penta- and octa-BDEs were the mainly-used brominated flame retardants (BFRs) and BDE-99/100 or BDE-154/ 153 were the second most dominant congeners in the fish samples (Perez-Fuentetaja et al., 2010; Sormo et al., 2009). The

relative abundance of BDE-209 may be related to the fact that BDE209 was the main brominated fire retardant used in China.BDE-154, BDE-153, BDE-99 and BDE-100 were in a lower percent of less than 8% in samples from this study, which could be linked to the metabolic debromination in the organism. Stapleton et al observed significant debromination of BDE-99 to BDE-47 and BDE-183 to BDE-154 and other congers in the intestinal tract of the common carp (Stapleton et al., 2004). Another possible explanation might be that some congeners simply make up a smaller percentage of the commercial mixture. It has been previously reported that the commercial penta-flame-retardant mixtures consists of six isomers (tri- through hexa-PBDEs) with BDE-47, BDE-99 and BDE-100 contributing >80% and the other three isomers (BDE-153, BDE154 and BDE-85) making up <12% of the product (LaA Guardia et al., 2006). Technical DP has two conformational isomers: syn (u shaped) and anti (chair shaped). Stereoisomers could have different physical and chemical properties leading to variation in their persistence in the environment. Generally, the fraction of anti-DP or syn-DP in total DP has always been used to discuss the environmental transportation and fate of the two structural isomers. In this study, fanti was calculated (Table 1) with the concentration of anti-DP being divided by the sum of the concentrations of anti-DP and syn-DP for fish samples. Average fanti is 0.57, which is significantly lower than those of commercial DP (fanti ¼ 0.65e0.75) (Wu et al., 2010). Significantly lower fanti value than that of the technical DP standard have also been observed in other studies (Hoh et al., 2006; Kang et al., 2010; Tomy et al., 2007; Wu et al., 2010), which supported the hypothesis that syn-DP isomer more easily accumulates in biota samples than anti-DP isomer.

Fig. 2. The relative contribution of PCB homologs in the fish muscle samples collected from Liaohe River.

Fig. 3. Comprehensive two-dimensional gas chromatography results for a contour plot of total ion chromatogram of the fish sample.

98

G. Ren et al. / Environmental Pollution 172 (2013) 94e99

Table 3 The major halogenated compounds identified by GC
GCeTOFMS. Peak no

Name

1st dimension time (s)

2nd dimension time (s)

Similarity

Probability

Reverse

Quant Masse

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15

o,p’-DDE p,p’-DDE p,p’-DDD DDMU DDMS Octachlorostyrene Pentachloro-anisole Pentachloro-thioanisole Triclosan-methyl Hexachlorobenzene HCH Chlorpyrifos Trans-Nonachlor Endosulfan Sulfate Mirex

2028 2100 2300 1944 2036 1776 1252 1588 1968 1124 1364 1628 2004 2460 3100

3.325 3.450 3.775 3.775 1.350 3.750 3.325 0.100 0.350 2.450 3.400 3.075 3.025 0.275 0.550

905 934 931 873 897 889 934 878 850 922 892 915 912 872 910

8059 7811 5450 4006 8017 9744 9832 9716 9651 4407 6153 9684 7665 9385 9796

919 943 936 876 937 907 934 899 852 930 896 917 913 874 918

246 318 235 248 235 308 280 296 304 284 183 314 409 272 272

3.3. Screening of nontarget halogenous pollutants After identifying and quantifying the target compounds, additional experiments were carried out to screen other potential halogenous pollutions residue in the investigated fish samples. The GC
GCeTOFMS contour plot of a typical fish sample is depicted in Fig. 3. It can be seen from Fig. 3, a broadband along the x-axis (spread at 1 s in the second dimension) is present. It can be tentatively identified as acyclic alkanes and column bleed. A wide spreading of spots distributed on the 2D separation map, which played an important role in the separation of the target analytes from matrix interferences. Identification of the majority of peaks was based on comparison of deconvoluted mass spectra with the NIST 08 spectral library using ChromaTOF automated searching software, which led to a large list of compounds identified. Because the goal of this work was to investigate non-targeted halogenated pollutions, special care was taken with the identification of compounds based on the following mentioned criteria. Firstly, the peak table was automatically filtered by name to identify organo-halogen compounds. Secondly, the resulted peak table was sorted by similarity to identify compounds with library match similarity >850. Finally, identified compound was manually conformed in each instance. Obviously, this approach was time-consuming and less powerful at low concentration compounds presented in the samples. However, the evident advantage of this approach was minimizing the risk of possible incorrect identification which was essential for the screening purpose. Table 3 provided a summary of compounds identified using this strategy in all the fish samples. Compounds identified included dichlorodiphenyltrichloroethane (DDT) and its metabolites, octachlorostyrene, chlorinated anisole, chlorinated thioanisole, triclosan-methyl, and other pesticides. DDT is a legacy component of persistent organic pollutants. Field and microcosm experiment have confirmed that DDT can be degraded to a series of metabolites that may be more hazardous ecologically (Yu et al., 2011). In this study, some of its metabolites, such as DDD and DDE, and the high-order DDT metabolites, such as DDMU, DDMS and DDNU, were also identified in the fish samples. Octachlorostyrene is a by-product of magnesium and chlorinated solvent production, aluminum plasma etching, aluminum degassing with hexachloroethane, chlorination of titanium, and waste incineration. It is regarded as persistent organic pollutants (Yanagiba et al., 2009). Pentachloro-anisole is the major metabolite products of pentachlorophenol, a widely used fungicide (Vorkamp et al., 2004). Pentachloro-thioanisole has been described as primary degradation product of pentachloronitrobenzene(Li et al., 2009). Triclosan is an antimicrobial agent which is widely used in household and personal care products. Under aerobic conditions, a small amount of the triclosan can be

transformed to triclosan-methyl. Triclosan-methyl is more persistent, lipophilic, bio-accumulative and less sensitive toward photodegradation in the environment than its parent compound (Chen et al., 2011). The identification of above-mentioned pesticide-transformation products may indicate serious contamination of their parent compounds in the fish samples. These compounds found in the fish samples, alone with their parent compounds, should be verified with the analytical standard and added to the list of target compounds to be quantified in future analyses. Acknowledgment This study was financially supported by the National Science Foundation of China (No. 21007037), National Program for Water Pollution Control (2009ZX07528-002-04), Open Fund of State Key Laboratory of Organic Geochemistry (OGL-200901), and Shanghai Leading Academic Disciplines (S30109). Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.envpol.2012.08.012. References Bettinetti, R., Quadroni, S., Manca, M., Piscia, R., Volta, P., Guzzella, L., et al., 2012. Seasonal fluctuations of DDTs and PCBs in zooplankton and fish of Lake Maggiore (Northern Italy). Chemosphere 88 (3), 344e351. Bull, R.J., Reckhow, D.A., Li, X., Humpage, A.R., Joll, C., Hrudey, S.E., 2011. Potential carcinogenic hazards of non-regulated disinfection by-products: haloquinones, halo-cyclopentene and cyclohexene derivatives, N-halamines, halonitriles, and heterocyclic amines. Toxicology 286 (1e3), 1e19. Chen, X., Nielsen, J.L., Furgal, K., Liu, Y., Lolas, I.B., Bester, K., 2011. Biodegradation of triclosan and formation of methyl-triclosan in activated sludge under aerobic conditions. Chemosphere 84 (4), 452e456. Clarke, B.O., Smith, S.R., 2011. Review of ‘emerging’ organic contaminants in biosolids and assessment of international research priorities for the agricultural use of biosolids. Environment International 37 (1), 226e247. Dai, G.H., Liu, X.H., Liang, G., Xu, M.Z., Han, X., Shi, L., 2011. Health risk assessment of organochlorine contaminants in fish from a major lake (Baiyangdian Lake) in North China. Bulletin of Environmental Contamination and Toxicology 87 (1), 58e64. Domingo, J.L., Bocio, A., 2007. Levels of PCDD/PCDFs and PCBs in edible marine species and human intake: a literature review. Environment International 33 (3), 397e405. Focant, J.F., Sjodin, A., Turner, W.E., Patterson, D.G., 2004. Measurement of selected polybrominated diphenyl ethers, polybrominated and polychlorinated biphenyls, and organochlorine pesticides in human serum and milk using comprehensive two-dimensional gas chromatography isotope dilution time-of-flight mass spectrometry. Analytical Chemistry 76 (21), 6313e6320. Helaleh, M.I.H., Al-Rashdan, A., Ibtisam, A., 2012. Levels of polybrominated biphenyl ethers in some selected fish and Shellfish from Kuwait. Critical Reviews in Analytical Chemistry 42 (1), 79e86.

G. Ren et al. / Environmental Pollution 172 (2013) 94e99 Hilton, D.C., Jones, R.S., Sjoedin, A., 2010. A method for rapid, non-targeted screening for environmental contaminants in household dust. Journal of Chromatography A 1217 (44), 6851e6856. Hites, R.A., 2004. Polybrominated diphenyl ethers in the environment and in people: a meta-analysis of concentrations. Environmental Science & Technology 38 (4), 945e956. Hoh, E., Zhu, L.Y., Hites, R.A., 2006. Dechlorane plus, a chlorinated flame retardant, in the Great Lakes. Environmental Science & Technology 40 (4), 1184e1189. Howell, N.L., Suarez, M.P., Rifai, H.S., Koenig, L., 2008. Concentrations of polychlorinated biphenyls (PCBs) in water, sediment, and aquatic biota in the Houston Ship Channel, Texas. Chemosphere 70 (4), 593e606. Hu, D., Hornbuckle, K.C., 2010. Inadvertent polychlorinated biphenyls in commercial paint pigments. Environmental Science & Technology 44 (8), 2822e2827. Hu, D., Martinez, A., Hornbuckle, K.C., 2011. Sedimentary records of non-aroclor and aroclor PCB mixtures in the Great Lakes. Journal of Great Lakes Research 37 (2), 359e364. Johanningsmeier, S.D., McFeeters, R.F., 2011. Detection of volatile spoilage metabolites in fermented cucumbers using nontargeted, comprehensive 2-dimensional gas chromatography-time-of-flight mass spectrometry (GC
GCTOFMS). Journal of Food Science 76 (1), C168eC177. Jose Gomez, M., Herrera, S., Sole, D., Garcia-Calvo, E., Fernandez-Alba, A.R., 2011. Automatic searching and evaluation of priority and emerging contaminants in wastewater and river water by stir bar sorptive extraction followed by comprehensive two-dimensional gas chromatography-time-of-flight mass spectrometry. Analytical Chemistry 83 (7), 2638e2647. Kang, J.H., Kim, J.C., Jin, G.Z., Park, H., Baek, S.Y., Chang, Y.S., 2010. Detection of Dechlorane Plus in fish from urban-industrial rivers. [Research Support, NonU.S. Gov’t]. Chemosphere 79 (8), 850e854. Kannan, K., Maruya, K.A., Tanabe, S., 1997. Distribution and characterization of polychlorinated biphenyl congeners in soil and sediments from a superfund site contaminated with aroclor 1268. Environmental Science & Technology 31 (5), 1483e1488. La Guardia, M.J., Hale, R.C., Harvey, E., 2006. Detailed polybrominated diphenyl ether (PBDE) congener composition of the widely used penta-, octa-, and decaPBDE technical flame-retardant mixtures. Environmental Science and Technology 40 (20), 6247e6254. Lakshmanan, D., Howell, N.L., Rifai, H.S., Koenig, L., 2010. Spatial and temporal variation of polychlorinated biphenyls in the Houston Ship Channel. Chemosphere 80 (2), 100e112. Letcher, R.J., Bustnes, J.O., Dietz, R., Jenssen, B.M., Jorgensen, E.H., Sonne, C., et al., 2010. Exposure and effects assessment of persistent organohalogen contaminants in arctic wildlife and fish. [Research Support, Non-U.S. Gov’t Review]. The Science of Total Environment 408 (15), 2995e3043. Li, J., Dong, F., Liu, X., Zheng, Y., Yao, J., Zhang, C., 2009. Determination of pentachloronitrobenzene and its metabolites in ginseng by matrix solid-phase dispersion and GCeMSeMS. Chromatographia 69 (9e10), 1113e1117. Meng, X.-Z., Zeng, E.Y., Yu, L.-P., Mai, B.-X., Luo, X.-J., Ran, Y., 2007. Persistent halogenated hydrocarbons in consumer fish of China: regional and global implications for human exposure. Environmental Science & Technology 41 (6), 1821e1827. Muir, D.C.G., Howard, P.H., 2006. Are there other persistent organic pollutants? A challenge for environmental chemists. Environmental Science & Technology 40 (23), 7157e7166. Perez-Fuentetaja, A., Lupton, S., Clapsadl, M., Samara, F., Gatto, L., Biniakewitz, R., et al., 2010. PCB and PBDE levels in wild common carp (Cyprinus carpio) from eastern Lake Erie. Chemosphere 81 (4), 541e547. Qiu, X., Marvin, C.H., Hites, R.A., 2007. Dechlorane plus and other flame retardants in a sediment core from Lake Ontario. Environmental Science & Technology 41 (17), 6014e6019. Ren, G., Yu, Z., Ma, S., Li, H., Peng, P., Sheng, G., et al., 2009. Determination of dechlorane plus in serum from electronics dismantling workers in South China. Environmental Science & Technology 43 (24), 9453e9457.

99

Rowe, A.A., Totten, L.A., Xie, M., Fikslin, T.J., Eisenreich, S.J., 2007. Airewater exchange of polychlorinated biphenyls in the delaware river. Environmental Science & Technology 41 (4), 1152e1158. Skinner, L.C., 2011. Distributions of polyhalogenated compounds in Hudson River (New York, USA) fish in relation to human uses along the river. Environmental Pollution 159 (10), 2565e2574. Sormo, E.G., Jenssen, B.M., Lie, E., Skaare, J.U., 2009. Brominated flame retardants in aquatic organisms from the North Sea in comparison with biota from the high arctic marine environment. Environmental Toxicology and Chemistry 28 (10), 2082e2090. Srogi, K., 2008. Levels and congener distributions of PCDDs, PCDFs and dioxin-like PCBs in environmental and human samples: a review. Environmental Chemistry Letters 6 (1), 1e28. Stapleton, H.M., Letcher, R.J., Baker, J.E., 2004. Debromination of polybrominated diphenyl ether congeners BDE 99 and BDE 183 in the intestinal tract of the common carp (Cyprinus carpio). Environmental Science & Technology 38 (4), 1054e1061. Su, G.-y., Gao, Z.-s., Yu, Y., Ge, J.-c., Wei, S., Feng, J.-f., et al., 2010. Polybrominated diphenyl ethers and their methoxylated metabolites in anchovy (Coilia sp.) from the Yangtze River Delta, China. Environmental Science and Pollution Research 17 (3), 634e642. Sverko, E., Tomy, G.T., Reiner, E.J., Li, Y.F., McCarry, B.E., Arnot, J.A., et al., 2011. Dechlorane plus and related compounds in the environment: a review. Environmental Science & Technology 45 (12), 5088e5098. Tomy, G.T., Pleskach, K., Ismail, N., Whittle, D.M., Helm, P.A., Sverko, E., et al., 2007. Isomers of dechlorane plus in Lake Winnipeg and Lake Ontario food webs. Environmental Science & Technology 41 (7), 2249e2254. Turyk, M.E., Bhavsar, S.P., Bowerman, W., Boysen, E., Clark, M., Diamond, M., et al., 2012. Risks and benefits of consumption of Great Lakes fish. [Research Support, Non-U.S. Gov’t]. Environmental Health Perspectives 120 (1), 11e18. Vorkamp, K., Riget, F., Glasius, M., Pecseli, M., Lebeuf, M., Muir, D., 2004. Chlorobenzenes, chlorinated pesticides, coplanar chlorobiphenyls and other organochlorine compounds in Greenland biota. Science of the Total Environment 331 (1e3), 157e175. Wang, J., Lin, Z., Lin, K., Wang, C., Zhang, W., Cui, C., et al., 2011. Polybrominated diphenyl ethers in water, sediment, soil, and biological samples from different industrial areas in Zhejiang, China. Journal of Hazardous Materials 197, 211e219. Wu, J.P., Zhang, Y., Luo, X.J., Wang, J., Chen, S.J., Guan, Y.T., et al., 2010. Isomerspecific bioaccumulation and trophic transfer of dechlorane plus in the freshwater food web from a highly contaminated site, South China. Environmental Science & Technology 44 (2), 606e611. Xiang, C.-H., Luo, X.-J., Chen, S.-J., Yu, M., Mai, B.-X., Zeng, E.Y., 2007. Polybrominated diphenyl ethers in biota and sediments of the Pearl River Estuary, South China. Environmental Toxicology and Chemistry 26 (4), 616e623. Xu, J., Gao, Z., Xian, Q., Yu, H., Feng, J., 2009. Levels and distribution of polybrominated diphenyl ethers (PBDEs) in the freshwater environment surrounding a PBDE manufacturing plant in China. Environmental Pollutution 157 (6), 1911e1916. Yanagiba, Y., Ito, Y., Kamijima, M., Gonzalez, F.J., Nakajima, T., 2009. Octachlorostyrene induces cytochrome P450, UDP-glucuronosyltransferase, and sulfotransferase via the aryl hydrocarbon receptor and constitutive androstane receptor. Toxicological Sciences 111 (1), 19e26. Yang, R., Wang, Y., Li, A., Zhang, Q., Jing, C., Wang, T., et al., 2010. Organochlorine pesticides and PCBs in fish from lakes of the Tibetan Plateau and the implications. Environmental Pollution 158 (6), 2310e2316. Yu, H.-Y., Bao, L.-J., Liang, Y., Zeng, E.Y., 2011. Field validation of anaerobic degradation pathways for dichlorodiphenyltrichloroethane (DDT) and 13 metabolites in marine sediment cores from China. Environmental Science & Technology 45 (12), 5245e5252. Yu, Y.-X., Zhang, S.-H., Huang, N.-B., Li, J.-L., Pang, Y.-P., Zhang, X.-Y., et al., 2012. Polybrominated diphenyl ethers and polychlorinated biphenyls in freshwater fish from Taihu Lake, China: their levels and the factors that influence biomagnification. Environmental Toxicology and Chemistry 31 (3), 542e549.