Organochlorine pesticides in fish from Taihu Lake, China, and associated human health risk assessment

Organochlorine pesticides in fish from Taihu Lake, China, and associated human health risk assessment

Ecotoxicology and Environmental Safety 98 (2013) 383–389 Contents lists available at ScienceDirect Ecotoxicology and Environmental Safety journal ho...

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Ecotoxicology and Environmental Safety 98 (2013) 383–389

Contents lists available at ScienceDirect

Ecotoxicology and Environmental Safety journal homepage: www.elsevier.com/locate/ecoenv

Organochlorine pesticides in fish from Taihu Lake, China, and associated human health risk assessment Deqing Wang a, Yingxin Yu a,n, Xinyu Zhang a, Dongping Zhang a, Shaohuan Zhang a, Minghong Wu b a b

Institute of Environmental Pollution and Health, School of Environmental and Chemical Engineering, Shanghai University, Shanghai 200444, PR China Institute of Applied Radiation, School of Environmental and Chemical Engineering, Shanghai University, Shanghai 200444, PR China

art ic l e i nf o

a b s t r a c t

Article history: Received 12 April 2013 Received in revised form 5 July 2013 Accepted 7 July 2013 Available online 12 October 2013

Because contaminants and nutrients always coexist in fish, the risk from contaminants and the benefit from nutrients, such as eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) are also concomitant via fish consumption. To investigate the risk and benefit via fish consumption, concentrations of dichlorodiphenyltrichloroethane and its metabolites (DDTs), and hexachlorocyclohexanes (HCHs) in the whole- and portion-muscles of fish from Taihu Lake, China, were measured. Based on the contaminant data and nutrients from our previous study, and the associated risk and benefit via fish consumption were estimated. The concentrations of DDTs and HCHs in the whole-muscles ranged from 7.8  102 to 3.4  103 pg g  1 ww, and from 67.3 to 300 pg g  1 ww, respectively. Of DDTs and HCHs measured, p,p ′-DDE and β-HCH were respectively the most abundant pesticides. The composition profiles of DDTs and HCHs suggested that the pesticides were mainly historical residues. The benefit–risk quotient (BRQ) of EPA +DHA vs. POPs (persistent organic pollutants including data of DDTs, HCHs, and those of polychlorinated biphenyls and polybrominated diphenyl ethers cited from our previous study) via consumption of fish from Taihu Lake was calculated. As a result, to achieve the recommended EPA+DHA intake of 250 mg d  1 for a healthy adult, the consumption of most fish species from the lake can cause cancer and non-cancer risks. However, the fish consumption at the rates of 44.9 g d  1 by Chinese would not lead to the risks for most of the species. The results also suggested that the risk of consuming silver carp was generally lower than other fish species, and those of dorsal muscles were lower than ventral and tail muscles. & 2013 Elsevier Inc. All rights reserved.

Keywords: Benefit–risk assessment Fish Organochlorine pesticide Persistent organic pollutant Taihu Lake

1. Introduction Dichlorodiphenyltrichloroethane (DDT) and hexachlorocyclohexanes (HCHs), two kinds of organochlorine pesticides (OCPs), have a long history of use in the world for the control of agricultural pests. They have been of great concern because of their high lipophilicity, persistence, long-range transport properties in the environment and toxic effects on organisms including humans (U.S. DHHS, 2002, 2005; Kannan et al., 2004, 2010). Both of them are typical persistent organic pollutants (POPs), and listed as priority-controlled POPs by Stockholm Convention. China is one of the largest producers and consumers of technical DDT and HCHs, which accounted for 20% and 33% of the total world production with 0.4 and 4.9 million tons, respectively, between the 1950s and 1983s (Zhang et al., 2002). Although most of the developed countries have already banned or restricted the production and usage of these pesticides during the 1970s and 1980s, some developing countries are still using them for agricultural and public

n

Corresponding author. Fax: +86 21 66136928. E-mail address: [email protected] (Y. Yu).

0147-6513/$ - see front matter & 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ecoenv.2013.07.012

purposes (Torres-Dosal et al., 2012; Wassie et al., 2012). Even after the ban of technical DDT and HCHs for agricultural usage in 1983 in China, lindane, a γ-HCH isomer, was further used in forest management until the year 2000, and DDT was produced for export and further producing dicofol, another kind of pesticides from DDT and still in use in China (Yang et al., 2008). Taihu Lake, with an area of 2250 km2 and an average depth of 1.9 m, is the second largest lake as well as one of the five famous freshwater lakes in China. It is located on the border of Jiangsu and Zhejiang provinces, southeast of China. The Taihu Lake region is one of the areas where technical DDT and HCHs were most extensively used from the 1950s to 1980s (Qiu et al., 2004; Wang et al., 2005). In recent years, many contaminants, such as OCPs, polychlorined biphenyls (PCBs), and polybrominated diphenyl ethers (PBDEs), have been detected in the water system (Liu et al., 2009; Nakata et al., 2005; Yu et al., 2012a; Zhang et al., 2012a). However, there is a thriving fishing industry around the lake. Thus, there was a need of better understanding the residue levels of DDTs and HCHs in fish from the lake and the associated human health risks posed by the pesticides via fish consumption. Although several studies had investigated the levels of DDTs and HCHs in fish from the lake (Ke et al.,

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D. Wang et al. / Ecotoxicology and Environmental Safety 98 (2013) 383–389

2007; Nakata et al., 2005; Wang et al., 2012), the associated human health risk assessments via fish consumption are very limited (Zhang et al., 2012a, b). Fish are known to provide many benefits for human health due to their high content of semi-essential fatty acids (SEFA, a kind of polyunsaturated fatty acids that humans must ingest because the body requires them for good health and can synthesize them but the synthesis is rather limited) in fish lipids, particularly eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA). A regular consumption of EPA and DHA can reduce risk of coronary heart disease, cardiovascular diseases, diabetes, neural disorders and hypertension (Bang and Dyerberg, 1980; Garg et al., 2006; He et al., 2004). However, industrialization has led to global pollution of POPs. Fish also contain contaminants including these pollutants. The lipophilic features of POPs render them liable to bioaccumulate in organisms and to be biomagnified through food chains (U.S. DHHS, 2002, 2005; Yu et al., 2012a). Once they enter into human body, they may cause significant adverse effects on human health (Borchers et al., 2010; Weyandt et al., 2008). Hence, it is important to investigate whether consumption of contaminated fish is still beneficial to human health. In recent years, there were numerous studies which focused on benefit–risk assessment of co-ingestion of polyunsaturated fatty acids and POPs via fish consumption (Antonijevic et al., 2007; Du et al., 2012; Loring et al., 2010; Sioen et al., 2008; Zhang et al., 2012a, b). If we know the distributions of both polyunsaturated fatty acids and POPs in different types of fish or different portions of them, it may allow consumers to make more selections about fish consumption. A few studies have reported distributions of polyunsaturated fatty acids or POPs in fish (Cheung et al., 2008; Chaijan et al., 2010). However, as well known, only one paper reported the distribution of both polyunsaturated fatty acids and POPs (including PCBs and PBDEs) as well as the corresponding estimation of the benefits and risks of co-ingestion of the compounds in a given fish from different portions (Zhang et al., 2012b). The benefit–risk assessment of co-ingestion of SEFA and contaminants for human health via fish consumption can be simplified to the evaluation of the benefit of SEFA intake and the risk of contaminant intake (Gladyshev et al., 2009). Because many contaminants co-exist in fish, U.S. EPA has proposed the human health risk assessment of multiple contaminants, and it suggests that additive interaction can be used when the contaminants show similar toxic effects (U.S. EPA, 2000a). In a previous study, the benefit–risk of co-ingestion of SEFA and contaminants (PBDEs and PCBs) was evaluated via consumption of fish from Taihu Lake (Zhang et al., 2012b). In that study, we found that the risk consuming the dorsal muscle was generally lower than the ventral and tail muscles. However, that study assessed the risk only considered individual contaminants, not multiple contaminants. We speculate that whether the conclusion is still right when OCPs are added to assess risk considered multiple contaminants. Therefore, the main objective of the present study was to determine the concentrations of DDTs and HCHs in fish collected from Taihu Lake, and focused on (1) the current contamination levels of DDTs and HCHs in fish from Taihu Lake; (2) the distribution of the contaminants in muscles from three portions (i.e., dorsal, ventral, and tail muscle); and (3) the assessments of the benefit from EPA and DHA, and the risks from multiple contaminants regarding carcinogenic and non-carcinogenic effects via consumption of fish from the lake. 2. Material and methods 2.1. Sampling and sample preparation Fish were caught by commercial fishers from Taihu Lake in September 2010, and described in our previous study (Zhang et al., 2012a, b). The fish collected were transported to the laboratory in ice-boxes and dissected after measuring the length

and weight of individual fish (Zhang et al., 2012a, b). The muscles were lyophilized, and the dried powders were stored at  18 1C until use. In the present study, 9 fish species (including Wuchang bream, white amur bream, crucian carp, common carp, silver carp, bighead carp, yellow catfish, spotted steed, and topmouth culter) were used. The whole-muscles (mixed muscle including dorsal, ventral, and tail muscles) of the nine species, and the portion-muscles from three portions (i.e., dorsal, ventral, and tail muscles) of 4 fish species (including silver carp, bighead carp, common carp, and topmouth culter) were used to measure the concentrations of DDTs and HCHs. A total of 125 samples including 56 whole-muscle samples and 69 portion-muscle samples were analyzed. 2.2. Analytical protocol Concentrations of DDTs and HCHs were determined using a previous method with some modifications (Meng et al., 2007). Briefly, the dried samples (2 g) spiked with the surrogate standards (13C-PCB141 and PCB209) were Soxhlet-extracted with n-hexane:acetone (1:1, v/v) for 72 h. The extracts were treated by concentrated sulfuric acid and then purified using a multilayer silica–alumina column as described in our previous study (Zhang et al., 2012b). Finally, the eluates were stored in 50 μL iso-octane at  18 1C until analyses after pentachloronitrobenzene (internal standard) added. 2.3. Instrumental analyses The target chemicals were quantified using an Agilent 6890N gas chromatography (GC) coupled with an electron capture detector (ECD). An HP-5 MS capillary column (30 m  0.25 mm  0.25 μm, J & W Scientific, USA) was used. The oven temperature was programmed from 110 to 170 1C (held for 5 min) at 1.5 1C min  1, from 170 to 226 1C (held for 5 min) at 2 1C min  1, and from 226 to 280 1C at 40 1C min  1, finally held at 280 1C for 10 min. Splitless injection of a 1-μL sample was performed with injector temperature at 280 1C. Ultra-pure helium at a flow rate of 1 mL min  1 was used as the carrier gas under constant flow mode. 2.4. Calculations The benefit–risk quotient (BRQ) via fish consumption was calculated using the following equation (Zhang et al., 2012b): BRQ ¼

CRSEFA CRlim

ð1Þ

where CRSEFA (g d  1) is the fish consumption rate to achieve the recommended intake of EPA and DHA (herein SEFA refers to EPA+DHA); CRlim (g d  1) is the maximum allowable fish consumption rate of contaminated fish. A BRQ value less than one indicates that there is no obvious potential risk to humans via consumption of contaminated fish, and vice versa. The CRSEFA is calculated using the following equation: CRSEFA ¼

RSEFA C SEFA

ð2Þ

where RSEFA (mg d–1) is the recommended SEFA intake rate of 250 mg d  1 for a healthy adult (Mozaffarian, 2006); CSEFA (mg g  1) is the measured concentration of SEFA in fish which were cited from our previous studies (Zhang et al., 2012a, b). Toxic effects of a contaminant can be divided into carcinogenic (if the contaminant is a carcinogen or possible carcinogen) and non-carcinogenic effects. The CRlim of multiple contaminants lead to the similar toxic effect endpoints in a single fish species was calculated according to the following equations regarding carcinogenic and non-carcinogenic effects of contaminants (U.S. EPA, 2000a; Yu et al., 2012b): CRlim ¼

BW  ARL ∑xm ¼ 1 C m  CSFm

ð3Þ

CRlim ¼

BW ∑xm ¼ 1 ðC m =RfDm Þ

ð4Þ

where ARL (dimensionless) is the maximum acceptable lifetime risk level; BW (kg) is the consumer body weight; x is the number of contaminants; Cm (mg g  1) is the measured concentration of contaminant m in a given fish species; CSFm ((mg/kg day)  1) is the cancer slope factor of contaminant m; and RfDm (mg (kg d)  1) is reference dose of contaminant m. In the present study, a BW value of 63.1 kg was used (Yu et al., 2012c). The contaminants including DDTs, HCHs, PCBs, and PBDEs were considered. The CSF and RfD values of 0.34 (mg/kg d)  1 and 5  10  4 mg (kg d)  1 for DDTs, and 1.3 (mg/kg d)  1 and 3  10  4 mg (kg d)  1 for HCHs were used, respectively (U.S. EPA, 2000a). For PCBs, 1 (mg/kg d)  1 and 2  10  5 mg (kg d)  1 were used as the CSF and RfD values, respectively (U.S. EPA, 2000a). Because the CSF and RfD values of total PBDEs are not available, a CSF value of 7  10  4 (mg/kg d)  1 for BDE209 (a deca-BDE congener) and a RfD value of 1  10  4 mg (kg d)  1 for BDE47 (a tetraBDE congener) were added into the calculation for total PBDEs based on the data in

D. Wang et al. / Ecotoxicology and Environmental Safety 98 (2013) 383–389 the Integrated Risk Information System (IRIS) of U.S. EPA (http://www.epa.gov/IRIS/). The appropriate risk level for a given population is determined by risk managers. In the present study, an ARL of 1 in 1,000,000 (10  6) was used to calculate the CRlim for non-occupational exposure scenarios where food intake in large populations (U.S. EPA, 2000b). In addition, to assess the public health risk of exposure to multiple contaminants via fish consumption, hazard ratios (HRs) were calculated via dividing the fish consumption rate by the maximum allowable fish consumption rate of contaminated fish using the following equation: HRs ¼

IRfish CRlim

ð5Þ 1

where IRfish (g d ) is the fish consumption rate by Chinese, which was set at 44.9 g d  1 for Chinese in cities (Du et al., 2012; Zhai and Yang, 2006). CRlim is that defined above. Risks associated with carcinogenic and non-carcinogenic effects of the contaminants were considered. If a hazard ratio greater than one, it indicates that there is potential risk to human health via the fish consumption, and vice versa. Two HRs, based on the mean and 90th percentile measured concentrations, were calculated to assess the potential health risks to humans regarding carcinogenic and non-carcinogenic multiple contaminants. 2.5. Quality assurance and quality control Each batch of samples, a procedural blank was run to monitor interfering peaks during sample treatment. Every set of twenty samples consisted of duplicate samples to examine the reproducibility. Spiked samples of DDTs and HCHs were used to check the accuracy of sample analysis (recover rate generally ranged between 75% and 125%). Five working solutions of the standards including 10 pesticides (i.e., o,p′-DDE, p,p′-DDE, o,p′-DDD, p,p′-DDD, o,p′-DDT, p,p′-DDT, α-HCH, β-HCH, γ-HCH, and δ-HCH) ranged from 20 to 500 ng mL  1 in iso-octane were used with the linear regression coefficients of R2 40.99 for all of the pesticides. The reported concentrations were not corrected against the recovery rates of surrogates of 13C-PCB141 (89–105%) and PCB209 (70–120%). The instrumental detection limits (IDL) varied between 0.21 and 0.96 pg g  1 ww for the pesticides. The concentration of a pesticide was reported as zero when it was below its IDL.

3. Results and discussion 3.1. Concentrations of DDTs and HCHs 3.1.1. DDTs DDTs were detected in all samples. ∑DDTs presented as the sum concentrations of DDT and its metabolites (i.e., p,p′-DDT, o,p′-DDT, p, p′-DDE, o,p′-DDE, p,p′-DDD, and o,p′-DDD). In the present study, concentrations were reported on the basis of wet weight (ww) if there was no special explanation. The concentrations of DDTs in the whole- and portion-muscles are listed in Tables 1 and 2, respectively. ∑DDTs in the whole-muscles ranged from 7.9  102 to 3.4  103 pg g  1 ww with a mean of 1.5  103 pg g  1 ww. The lowest and highest ∑DDTs were observed in silver carp (an omnivorous fish) and topmouth culter (a carnivorous fish), respectively. This may be

385

attributed to their different living and feeding habits (Zhou et al., 2007). For different portion-muscles, the lowest and highest ∑DDTs were observed in the dorsal muscle of silver carp (5.3  102 pg g  1 ww) and ventral muscle of topmouth culter (1.3  104 pg g  1 ww). Generally, the following sequence was observed for portion-muscles: ventral muscle4tail muscle4dorsal muscle. Our data in crucian carp (∑DDT: 1.5  103 pg g  1 ww) was lower than that in fish from the same lake reported by Ke et al. (2007), who reported that ∑DDTs was 4600 pg g  1 ww. Similarly, ∑DDTs in common carp, topmouth culter, and spotted steed were lower than those in the same fish species from the same lake in a previous study reported by Nakata et al. (2005). This might be because of the prohibition of the usage of technical DDT in China. Compared with wild fish collected from other water bodies in China and other countries (Table S1), fish in Taihu Lake were moderately contaminated by DDTs. 3.1.2. HCHs HCHs were detected in all samples. ∑HCHs presented the sum concentrations of HCH isomers including α-HCH, β-HCH, γ-HCH, and δ-HCH. Concentrations of HCHs in the whole- and portionmuscles are listed in Tables 1 and 2, respectively. ∑HCHs in the whole- and portion-muscles ranged from 63.7 to 3.0  102 pg g  1 ww and from 69.2 to 6.6  102 pg g  1 ww, respectively, which were much lower than ∑DDTs. The lowest and highest ∑HCHs in the whole-muscle samples were observed in bighead carp and crucian carp, and those in the portion-muscle samples were detected in the tail muscle (bighead carp) and ventral muscle (topmouth culter), respectively. Our data in crucian carp (∑HCH: 300 pg g  1 ww) was much lower than that in the study by Ke et al. (2007), who reported that ∑HCHs was 2500 pg g  1 ww. The mean ∑HCHs in common carp, topmouth culter, and spotted steed in the present study was lower than those in the same species collected from the same lake in August 2000 (Nakata et al., 2005), which might be because of the prohibition of the usage of HCHs in China. Similar to DDTs, fish in Taihu Lake were moderately contaminated by HCHs compared with wild fish collected from other water bodies in China and other countries (Table S2). 3.2. Composition profiles and source implications 3.2.1. DDTs Of DDTs measured, p,p′-DDE (mean: 1.3  103 pg g  1 ww), derived from p,p′-DDT under aerobic condition, had the highest concentration and was detected in all whole-muscle samples. p,p

Table 1 Concentrations of DDTs and HCHs (pg g  1 ww) in whole-muscles of fish collected from Taihu Lake, Chinaa.

α-HCH β-HCH γ-HCH δ-HCH o,p′-DDE p,p′-DDE o,p′-DDD p,p′-DDD o,p′-DDT p,p′-DDT ∑HCHs ∑DDTs ∑OCPs

Wuchang bream

White amur bream

Crucian carp

Common carp

Silver carp

Bighead carp

Yellow catfish

Spotted steed

Topmouth culter

29.5 7 6.5 1247 27.2 1.9 7 3.8 14.2 7 10.6 18.17 13.4 10027 139 24.57 4.0 51.3 7 16.5 9.6 7 13.6 164 7 267 1707 39.9 1269 7 189 1439 7 195

46.0 7 28.7 75.5 7 39.1 nd 16.9 710.6 57.5 722.8 988 7 601 1597 383 148 7 145 7.0 7 8.5 18.9 7 24.5 138.5 762.1 13777 1106 15167 1077

8.2 7 5.7 288 7167 nd 3.7 7 4.7 1.9 75.0 1402 7 473 19.17 13.0 82.6 7 36.8 6.4 7 8.5 25.0 7 19.6 3007 163 1537 7517 1838 7 578

33.9 7 10.2 96.5 7 21.5 0.5 7 1.2 13.7 7 8.8 14.17 13.3 7197 638 20.2 7 8.8 42.0 7 42.3 17.5 7 10.6 55.2 7 14.4 1457 31.1 868 7 682 10137 706

34.0 7 14.6 66.87 15.0 0.9 7 1.7 6.17 6.5 35.97 18.4 622 7 234 37.2 7 12.1 60.2 7 40.8 14.0 7 3.6 17.5 7 15.0 1087 34.3 786 7 298 894 7 324

21.6 7 11.0 38.8 720.6 nd 6.9 75.6 29.0 718.4 705 7282 34.17 10.4 44.7 7 26.7 6.4 77.4 62.3 729.1 67.3 721.3 886 7 358 949 7 370

48.07 38.2 1337 73.0 nd 1.6 7 4.2 46.2 7 47.7 23317 1076 41.9 7 18.3 113.17 83.6 35.0745.8 52.9 7 55.7 1827 106 2620 7 1268 2802 7 1262

27.3 7 15.1 106 7 61.7 nd 5.4 7 5.1 nd 7357 257 15.9 7 5.8 42.8 7 25.5 0.7 7 1.1 23.0 7 4.5 1397 65.8 8177 284 956 7 301

44.1 733.1 90.8 764.0 1.3 73.1 21.9 712.0 124 760.6 2993 71472 75.7 755.1 85.8 757.7 47.6 742.5 62.6 718.5 158 776.3 3389 71586 3547 71645

nd: not detected. a

Data were listed in the format of arithmetic mean 7standard deviation.

D. Wang et al. / Ecotoxicology and Environmental Safety 98 (2013) 383–389

32.1 79.2 1087 45.9 nd 7.9 7 9.2 14.9 7 12.0 1287 7397 18.2 713.3 89.8 7 38.5 19.5 7 28.5 83.7 7 55.0 148 7 40.3 1513 7516 1661 7549

32.17 31.5 43.2 7 28.7 3.3 7 3.1 11.2 7 23.4 41.5 7 28.5 904 7 491 23.0 7 17.5 37.0 7 31.4 34.8 7 38.3 47.8 7 27.3 74.9 7 80.7 9077 701 982 7 757

1427 185 492 7 596 nd 29.0 7 26.8 503 7 535 10,842 79957 285 7 286 6617 700 818 7831 362 7 300 663 7 805 13,470 712354 14,1347 13151

74.7 7 44.1 210 7154 nd 6.6 73.7 208 7 184 57797 3074 97.5 7 93.5 247 7215 256 7 282 1397 150 2917 192 67267 3927 70177 4098

′-DDD (74.4 pg g  1 ww) and p,p′-DDT (53.5 pg g  1 ww) followed. p,p′-DDE accounted for 83.4% (from 71.7% to 91.2%) of total DDTs (Fig. 1A). The composition profiles of DDTs in the portion-muscles of the four species are similar to those in the whole-muscles samples, which p,p′-DDE had the highest concentration and was detected in all portion-muscle samples (Fig. 1C). The composition profiles were in agreement with the patterns of DDTs in fish collected previously from Taihu Lake (Nakata et al., 2005). Similar composition profiles were usually observed in the environment in China (Dai et al., 2011; Dong et al., 2004; Jiang et al., 2005; Nakata et al., 2005). The contamination profiles of DDTs in the environmental matrices can reveal their sources. Technical DDT generally contains 75% p,p′-DDT, 15% o,p′-DDT, 5% p,p′-DDE, and less than 5% other metabolites (Zhou et al., 2006). DDT can be metabolized into DDD under anaerobic or DDE in aerobic or oxidation environment (Hitch and Day, 1992). Thus, the ratios of (p,p′-DDE+p,p′-DDD)/ ∑DDTs can indicate past or recent usage of technical DDT (Hitch and Day, 1992). A ratio of it more than 0.5 generally indicates longterm biotransformation of DDT, while a ratio of less than 0.5 may indicate recent input of DDT (Hitch and Day, 1992). In the present study, the ratios of it ranged from 0.82 to 0.97, which suggested that DDTs in fish from Taihu Lake were mainly due to historical use.

Data were listed in the format of arithmetic mean 7standard deviation. a

nd: not detected.

α-HCH β-HCH γ-HCH δ-HCH o,p′-DDE p,p′-DDE o,p′-DDD p,p′-DDD o,p′-DDT p,p′-DDT ∑HCHs ∑DDTs ∑OCPs

37.8 7 35.3 82.8 7 59.1 1.2 72.0 nd 30.17 29.8 6517 372 39.7 7 24.0 68.9 750.0 22.7 7 16.1 4.5 7 7.5 122 790.7 817 7488 939 7578

28.6 7 10.0 37.1 718.3 1.8 74.0 12.4 75.7 32.17 11.0 477 7139 14.0 7 12.6 29.2 7 14.3 nd 57.1 728.5 79.9 7 22.2 609 7185 689 7 201 42.6 7 28.3 84.5 7 59.4 0.8 7 2.1 13.7 7 9.4 39.0 7 23.6 581 7 304 30.7 7 20.1 63.8 7 44.8 23.6 7 14.4 21.2 7 18.6 1427 85.0 759 7 413 9017 494 28.5 7 16.2 56.3 7 18.1 1.8 7 2.0 14.0 7 11.1 10.17 7.7 4137 156 23.2 7 13.2 42.2 7 23.2 10.4 7 9.9 28.6 7 21.8 1017 35.3 5277 208 628 7 230

22.9 7 16.5 51.0 7 28.7 nd 1.0 72.1 6.7 7 6.2 8357 302 30.9 7 13.1 65.5 7 36.2 7.17 7.3 68.0 719.1 74.8 7 44.2 10147 362 1088 7 398

13.5 7 15.2 41.6 7 51.1 0.2 7 0.5 13.9 7 15.1 18.4 7 21.8 7127 501 27.17 22.8 62.2 7 47.4 14.3 7 24.5 45.5 7 54.4 69.2 7 79.1 879 7 650 948 7 723

26.3 7 10.1 50.9 7 16.4 nd 6.3 7 7.3 19.7 7 20.9 6777 254 13.4 7 3.9 43.8 7 19.8 25.6 7 20.9 48.8 7 60.7 83.5 7 30.6 829 7 359 9127 377

16.0 7 12.7 66.8 7 29.8 0.9 7 2.2 nd 7.17 5.7 8247 500 3.6 7 5.0 50.2 7 29.8 5.6 7 13.3 48.17 42.6 83.7 7 43.2 938 7 547 1022 7 576

Dorsal Tail Ventral Dorsal Tail Ventral Dorsal Ventral Dorsal

Tail

Bighead carp Silver carp

Table 2 Concentrations of DDTs and HCHs (pg g  1 ww) in portion-muscles of fish collected from Taihu Lake, Chinaa.

Common carp

Topmouth culter

Ventral

Tail

386

3.2.2. HCHs Compared with DDTs, HCH residues in the samples had much lower, which contributed only 10.7% (from 4.5% to 16.3%) of total OCPs measured. However, the amount of technical HCHs used in China (4900 kt) was much higher than that of technical DDT (400 kt) (Zhang et al., 2002). This might be because HCHs are less bioaccumulative, lipophilic, and shorter half-life in biological systems than DDTs (Davodi et al., 2011; Guo et al., 2007). Furthermore, semi-volatile characteristics of HCHs also indicate that these pesticides are easily evaporated into the air (Wania and Mackay, 1996). Of HCHs measured, the relative contributions of individual HCH isomers to total HCHs followed the sequence of β-HCH 4 α-HCH4 δ-HCH4γ-HCH. β-HCH accounted for an average of 68.5% (from 54.5% to 96.0%) of ∑HCHs in the whole-muscles (Fig.1B), which was consistent with the previous results obtained in fish from Taihu Lake (Dong et al., 2004; Nakata et al., 2005). Similar results were generally observed in biota (Yang et al., 2006; Zhou and Wong, 2004). Commercial HCHs include pure γ-HCH isomer (lindane) and mixture of HCH isomers (α-HCH: 65–70%, β-HCH: 5–6%, γ-HCH: 12–14%, and δ-HCH: 6%) (Willett et al., 1998). The higher β-HCH concentrations in the samples might be because it has a higher bioconcentration factor in aquatic organisms and is more persistent and stable than other HCH isomers (Willett et al., 1998). Hence, the abundance of β-HCH suggested that HCH contamination in the lake may be aged residues related to mobilization of the compounds. In addition, migration of HCHs from surface soil to the lake was suggested by Liu et al. (2009). In the present study, γ-HCH was the lowest, which accounted for only 0.4% (from 0% to 1.1%) of total HCHs in the whole-muscles, which indicated that lindane (γ-HCH499%) were not used in Taihu Lake region. This was consistent with the results of our previous study (Wang et al., 2012). The HCH composition profiles in the portionmuscles of the four species are similar to those in the wholemuscles, β-HCH had the highest concentration and was detected in all portion-muscles (Fig. 1D), and γ-HCH was the lowest. 3.3. Benefit–risk assessment The BRQ values of co-ingestion SEFA and POPs (including DDTs, HCHs, PCBs, and PBDEs) via consumption of whole- and portionmuscles considering carcinogenic and non-carcinogenic effects of

100%

100%

80%

80%

Relative abundance (%)

Relative abundance (%)

D. Wang et al. / Ecotoxicology and Environmental Safety 98 (2013) 383–389

60% 40% 20% 0%

WB

o,p'-DDE

WAB

CrC

p,p'-DDE

CoC

SC

o,p'-DDD

BC

p,p'-DDD

YC

SS

o,p'-DDT

387

60% 40% 20% 0%

TC

WB

WAB

CrC

α-HCH

p,p'-DDT

CoC

SC

BC

β-HCH

YC

γ-HCH

SS

TC

δ-HCH

o,p'-DDE

p,p'-DDE

o,p'-DDD

Common carp

p,p'-DDD

o,p'-DDT

20%

Bighead carp

α-HCH

p,p'-DDT

Common carp

β-HCH

γ-HCH

Tail

Dorsal

Ventral

Tail

Ventral

Dorsal

Silver carp

Topmouth culter

Tail

0%

Tail

Ventral

Tail

Dorsal

Ventral

Tail

Bighead carp

Dorsal

Dorsal

Silver carp

Ventral

Tail

Ventral

Dorsal

0%

40%

Dorsal

20%

60%

Ventral

40%

80%

Tail

60%

100%

Dorsal

80%

Ventral

Relative abundance (%)

Relative abundance (%)

100%

Topmouth culter δ-HCH

Fig. 1. Composition profiles of DDTs and HCHs in fish from Taihu Lake, China: (A) DDTs (whole-muscles); (B) HCHs (whole-muscles); (C) DDTs (portion-muscles); and (D) HCHs (portion-muscles). WB¼ Wuchang bream; WAB¼ white amur bream; CrC¼ crucian carp; CoC ¼ common carp; SC ¼ silver carp; BC ¼ bighead carp; YC ¼yellow catfish; SS ¼spotted steed; TC¼topmouth culter.

14 12

40 C-POPs(mean) NC-POPs(mean)

C-POPs(90%) NC-POPs(90%)

C-POPs(mean) NC-POPs(mean)

30

C-POPs(90%) NC-POPs(90%)

BRQ

BRQ

10 8 6

20 10

WB

WAB

CrC

CoC

SC

BC

YC

SS

TC

Silver carp

3.0 C-POPs(mean) NC-POPs(mean)

2.5

12

C-POPs(90%) NC-POPs(90%)

Tail

Ventral

Dorsal

Tail

Ventral

Tail

Ventral

Dorsal

Dorsal

Common carp

Topmouth culter

C-POPs(90%) NC-POPs(90%)

8

HRs

1.5

6 4

1.0

WB

WAB

CrC

CoC

SC

BC

YC

SS

TC

Silver carp

Bighead carp

Common carp

Tail

Ventral

Dorsal

Tail

Ventral

Dorsal

Tail

Ventral

0

Dorsal

0.5

Tail

2 Ventral

HRs

Bighead carp

C-POPs(mean) NC-POPs(mean)

10

2.0

0.0

Tail

0

Dorsal

0

Ventral

2

Dorsal

4

Topmouth culter

Fig. 2. The BRQ and HRs values via fish consumption considering carcinogenic and non-carcinogenic effects of multiple contaminants: (A) whole-muscles (BRQ); (B) portionmuscles (BRQ); (C) whole-muscles (HRs); and (D) portion-muscles (HRs). The dashed means the BRQ and HR value of one. C ¼carcinogenic effect; NC¼non-carcinogenic effect; POPs¼ persistent organic pollutants; WB¼ Wuchang bream; WAB ¼white amur bream; CrC ¼crucian carp; CoC ¼ common carp; SC¼ silver carp; BC ¼bighead carp; YC ¼yellow catfish; SS ¼ spotted steed; TC ¼topmouth culter.

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POPs were calculated and are shown in Fig. 2. The data of PCBs, PBDEs and SEFA were cited from our previous study (Zhang et al., 2012a, b). The BRQ values calculated based on mean concentrations of the contaminants ranged from 2.4 to 7.4 and from 0.6 to 2.1 for whole-muscles (Fig. 2A), and ranged from 2.6 to 19.5 and from 0.7 to 3.8 for portion-muscles (Fig. 2B) regarding carcinogenic and non-carcinogenic effects of the contaminants, respectively. For whole-muscles, the highest BRQ values were observed in yellow catfish regarding both carcinogenic and noncarcinogenic effects of the contaminants, and the lowest for both were observed in silver carp. For portion-muscles, the highest BRQ values were observed in the ventral muscle of topmouth culter regarding both carcinogenic and non-carcinogenic effects, and the lowest were observed in the dorsal muscle of silver carp (carcinogenic effect) and the dorsal muscle of silver carp and topmouth culter (non-carcinogenic effect). When 90th percentile concentrations of the contaminants were incorporated into the calculation, much higher BRQ values were obtained (Fig. 2). Generally, the BRQ value of silver carp was lower than those of the other fish species, and those in the dorsal muscles were lower than those in the ventral and tail muscles. This indicated that there were generally lower cancer and non-cancer risk via consumption of silver carp than the other fish species, and the dorsal muscle is lower than the ventral and tail muscles. The present results were consistent with our previous studies only considering PCBs and PBDEs (Zhang et al., 2012a, b). In the present study, most of the BRQ values based on both mean and 90th percentile concentrations were larger than one. These indicated that there were cancer and non-cancer risks via consumption of most of the fish to achieve the recommended SEFA intake of 250 mg d  1 for a healthy adult. The results revealed that it was not a suitable method to intake the recommended SEFA only via consuming the fish from Taihu Lake for a healthy adult. Based on the contents of SEFA in the fish species, the fish consumption rate would be mostly higher than 150 g d  1 to achieve the recommended SEFA intake of 250 mg d  1 (Zhang et al., 2012b). However, to achieve the recommended SEFA intake of 250 mg d  1 for a healthy adult, it would lead to both cancer and non-cancer health risks via consumption of most of the fish species measured based on the present study. Actually, in China, the fish consumption rates were much lower than 150 g d  1. The average daily aquatic product consumption of Chinese in cities was 44.9 g d  1 according to the Chinese National Report 2002 (Zhai and Yang, 2006). Based on the consumption rate, the HR values were calculated and are shown in Fig. 2. Considering non-carcinogenic effects of the contaminants, all the HR values based on mean and 90th percentile concentrations for the whole- and portion-muscles were less than one except for the ventral and tail muscles of topmouth culter (Fig. 2D). This indicated that daily exposure to the contaminants via fish consumption at the rates of 44.9 g d  1 by Chinese for a lifetime would not lead to obvious non-cancer risk except for the ventral and tail muscles of topmouth culter. When considering the carcinogenic effect of the contaminants, the HR values were generally lower than one except for crucian carp (1.2), yellow catfish (1.6), and topmouth culter (1.5) based on mean concentrations for whole-muscles (Fig. 2C). For portion-muscles, the HR values were also lower than one except for the tail muscles (5.4) and ventral muscle (2.8) of topmouth culter. The results indicated that consumption of most of the fish species would not yield a cancer risk at 10  6 level at a fish consumption rate of 44.9 g d  1. However, it needs to note that for carcinogens there are assumed to have no “safe” thresholds for human exposure. That is, any exposure to a carcinogen may pose some cancer risk (U.S. EPA, 2000a). It may not be absolutely “safe” to consume the fish even though the BRQ and HRs values were less than one. A zero risk is not possible in food safety issues, since carcinogens are ubiquitous.

3.4. Uncertainty analysis It is necessary to note that there are a number of important limitations for our evaluation of benefit–risk assessment. First, the RfD and CSF values measured in the literature have an uncertainty of perhaps an order of magnitude, which means that there may be a large uncertainty on the risk assessment of fish consumption. In addition, the RfD and CSF values for total PBDEs are still not available. BDE47 is one of PBDE congeners with the greatest toxicity, while BDE209 has the lowest. In the present study, RfD of BDE47 and CSF of BDE209 were used as the data of total PBDEs. Thus, it would overestimate the non-cancer risk, while underestimate the risk leading to cancer. Second, in the present study, only a limited number of contaminants such as DDTs, HCHs, PCBs, and PBDEs were considered. Other trace contaminants such as other OCPs, dibenzo-p-dioxins/ dibenzofurans, polycyclic aromatic hydrocarbons, perfluorinated compounds, heavy metals, and so on, were not added into the evaluation. The risk to human health via fish consumption could be underestimated, which meant that the BRQ values would be lower when other contaminants were considered. Third, in the present calculation, the additive interactions were used according to the suggestion by U.S. EPA (2000a), and we did not consider the possible interactions among various toxic chemicals. An et al. (2011) reported that there are a synergistic effect between BDE47 and benzo(a)pyrene, which means that it is more harmful to expose mixtures of BDE47 and benzo(a) pyrene compared with the sum effects of individual compound. Thus, the risk to human health via fish consumption could be underestimated if there were synergistic effects among the contaminants. Overall, although there are a number of limitations associated with the evaluation, the assessment undertaken indicates a potentially high cancer risk due to POP contaminants in fish if a healthy adult consumes fish from Taihu Lake to achieve the recommended SEFA intake of 250 mg d  1.

4. Conclusions The concentrations of OCPs measured in dorsal muscles were generally lower than those in ventral and tail muscles. The fish from the lake were moderately contaminated compared with those from other water bodies in China and other countries. The results showed that consumption of most of the fish species could cause cancer and non-cancer risks to achieve the recommended SEFA intake of 250 mg d  1 for a healthy adult. However, the fish consumption at the rate of 44.9 g d  1 by Chinese would generally not lead to cancer and non-cancer risks. Furthermore, consumption of dorsal muscles usually had lower risks than other portions.

Acknowledgment This work was financially supported by the National Nature Science Foundation of China (No. 21277086), the China National Funds for Distinguished Young Scientists (No. 11025526), and the Graduates′ Innovation Fund of Shanghai University (No. SHUCX120068).

Appendix A. Supporting information Supplementary data associated with this article can be found in the online version at http://dx.doi.org/10.1016/j.ecoenv.2013.07.012.

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