Chemosphere 118 (2015) 163–169
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Assessment on dioxin-like compounds intake from various marine fish from Zhoushan Fishery, China Xiangyong Wang a,b, Hongxia Zhang a,c, Lei Zhang a, Kai Zhong a,⇑, Xiaohong Shang a, Yunfeng Zhao a, Zhendong Tong d, Xinwei Yu d, Jingguang Li a,b,⇑, Yongning Wu a,b a
Key Laboratory of Food Safety Risk Assessment, Ministry of Health, China National Center for Food Safety Risk Assessment, Beijing 100021, China State Key Laboratory of Food Science and Technology, Nanchang University, Nanchang 330047, China School of Public Health, Shanxi Medical University, Taiyuan 030001, China d Zhoushan Municipal Center for Disease Control and Prevention, Zhoushan 316021, China b c
h i g h l i g h t s 32 Fish species were measure for 29 dioxin-like compounds. The factors effecting the accumulation of the compounds in sea fish were discussed. A risk-based consumption advice for sea fish was developed.
a r t i c l e
i n f o
Article history: Received 24 October 2013 Received in revised form 19 June 2014 Accepted 20 July 2014 Available online 1 September 2014 Handling Editor: H. Fiedler Keywords: Dioxin-like compounds Accumulation Fish species Intake assessment Risk-based consumption advice
a b s t r a c t Sea fish consuming is an important intake source of dioxin-like compounds, especially for the coastal residents. To assess the intake levels of these contaminants from sea fish and to provide risk-based consumption advice, concentrations of 17 polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs) and 12 dioxin-like polychlorinated biphenyls (dl-PCBs) were measured in 32 commonly consumed fish species from Zhoushan Fishery, China. Due to the different accumulation influenced by fat content, feed habits and living zone in the sea area, the levels of PCDDs, PCDFs and dl-PCBs in different fish species varied significantly ranging from 0.002 to 0.078 pg WHO-TEQ/g fresh weight, from 0.002 to 0.553 pg WHOTEQ/g fresh weight and from 0.003 to 2.059 pg WHO-TEQ/g fresh weight, respectively. Based on mean fish consuming rate in China, the estimated maximum possible dioxin-like compounds intake through different fish species ranged from 0.26 to 65.61 pg TEQ kg 1 bw month 1. Bullet mackerel has the highest monthly intake level which was much higher than other fish species and very close to the provisional tolerable monthly intake (70 pg TEQ kg 1 bw month 1) proposed by the Joint FAO/WHO Expert Committee on Food Additives. Hence, comparing to other fish species, the consumption of Bullet mackerel from Zhoushan Fishery should be cautious to reduce the potential health risk. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction Polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/ Fs) and dioxin-like polychlorinated biphenyls (dl-PCBs) are the broad class of environmental pollutants which are ubiquitous in the environment worldwide. PCDD/Fs are unwanted by-products mainly from incomplete combustion as well as manufacture of
⇑ Corresponding authors. Tel./fax: +86 010 67776790 (K. Zhong). Address: Key Laboratory of Food Safety Risk Assessment, Ministry of Health, China National Center for Food Safety Risk Assessment, Beijing 100021, China. Tel.: +86 010 67720035; fax: +86 010 67791253 (J. Li). E-mail addresses: [email protected] (K. Zhong), [email protected] (J. Li). http://dx.doi.org/10.1016/j.chemosphere.2014.07.057 0045-6535/Ó 2014 Elsevier Ltd. All rights reserved.
certain chemicals (Dannenberger et al., 1997; Kim et al., 2005). Dl-PCBs mainly stemmed from the production and usage of the commercial PCBs mixtures, which has been banned in 1970s, as well as leakage from the container (Baars et al., 2004). The great concern on PCDD/Fs and dl-PCBs by humans is their potential risk to human health (Clapp and Ozonoff, 2000; Oh et al., 2003). In literature, effects on the reproductive-, immune- and nervous system have been reported (Safe, 1990; USEPA, 2010). For humans, the exposure pathways to PCDD/Fs and dl-PCBs are dermal contact, inhalation and food intake. Among them, the dietary intake is the main pathway for general population, accounting for more than 90% (van Leeuwen et al., 2000; Wang et al., 2009; Fernandes et al., 2010; Grassi et al., 2010). There are
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many studies reporting fish as main food contributor (Kim et al., 2007; Zhang et al., 2008; Lorber et al., 2009). In China, especially in southeast China, aquatic foods corresponded to the dominant contribution to the dietary intake of PCDD/Fs and PCBs (Li et al., 2007; Zhang et al., 2013). These findings revealed the importance of fish as a source of potential exposure to toxic pollutants such as PCDD/Fs and PCBs. This is of great concern taking into account the nutritional role of fish as a part of a healthy diet, whose relevance has notably increased in recent years. In order to monitor the levels of PCDD/Fs and dl-PCBs in seafood and assure the health of humans, data on these compounds in sea fish and other sea food were reported gradually during recent years in China (Liu et al., 2011; Shen et al., 2009; Zhang et al., 2008). In the developed area of China, especially in southeast China, the high level body burden of dioxin-like compounds may be due to high consumption of aquatic food such as sea fish in these areas (Li et al., 2009; Zhang et al., 2013). Therefore, the detailed advices on edible fish selection regarding to dioxin-like compounds level could be essential to reduce the dietary intake of these contaminations in these area. In the present study, 32 fish species from Zhoushan fishery which is the largest fishery in southeast China were selected. These species are the most consumed by the local general population. Through analyzing the levels of the dioxin-like compounds and characterizing the factors affecting accumulation in these fishes, risk assessment on dioxin-like compounds from fish consumption for general population was conducted and the risk-based consumption advice for fish species selection was recommended.
previously (Li et al., 2007). In brief, after freeze-drying, the 15 congeners of 13C12-labeled PCDD/Fs and 12 congeners of 13 C12-labeled-dioxin-like PCBs were spiked in the samples, followed by Soxhlet-extracted with a mixture n-hexane/dichloromethane (1:1) and the bulk fat was removed by shaking with acid-modified silica-gel. Sample cleanup was performed using a through Power Prep instrument (Fluid Managment Systems, Waltham, MA, USA). The eluting fractions were concentrated to about 10 lL and the 13 C12-labeled injection standard for PCDD/Fs and PCBs was added into the concentrated solutions respectively prior to analysis. 2.4. HRGC/HRMS analysis
2. Materials and methods
The seventeen most toxic congeners of PCDD/Fs and twelve congeners of dioxin-like PCBs were analyzed by HRGC/HRMS (MAT95XP, ThermoFinnigan, German) equipped with DB-5MS capillary column (60 m 0.25 mm 0.25 lm) at 10 000 resolution using the splitless injection mode and multiple ion monitoring (MID). The temperature program for the analysis of PCDD/Fs started with 1 min at 120 °C, raised to 220 °C at 44 °C min 1 holding for 15 min, and then to 250 °C at 2.3 °C min 1 and from 250 °C to 260 °C at 0.9 °C min 1, lastly, ultimately to 310 °C at 20 °C min 1 holding for 11 min. In addition, the temperature was held for 1 min at 90 °C and programmed to 180 °C at 20 °C min 1 holding for 1 min, then further to 300 °C at 3 °C min 1 and held for 2 min for the analysis of dioxin-like PCBs. The temperatures of injector, transfer line, ion source and interface temperatures were 260 °C, 270 °C, 260 °C and 280 °C, respectively, ionization energy 60 eV and trap current 1.00 mA.
2.1. Sample collection
2.5. Quality control and assurance
Zhoushan, the only city on the sea composed of archipelago, is located at the junction of the southeast seashore and the entrance to the sea of Yangtze River, backing Shanghai, Hangzhou and Ningbo City, facing the Pacific Ocean. Zhoushan Fishery is the biggest fishery in China, known as ‘‘East China Sea fish warehouse’’. The annual output of aquatic products is around 1.3 million tons. The offshore ocean fishing output is more than one tenth of the country’s total. During the months of September and October 2011, the 32 fish species which are most consumed by local residents from the Zhoushan Fishery were acquired. Three individual fish were collected for each fish species. Samples were frozen at 20 °C until analysis. More information of these fish is shown in Table A1.
The laboratory performance was validated by successfully participating interlaboratory comparison of POPs in food organized by the Norwegian Institute of Public Health in 2012. In this study, the laboratory method blanks were performed every eight samples. Certified fish reference material WMF-01 (Wellington Laboratories) was analyzed for method validation and as a quality control sample. The method detection limits ranged from 0.001 pg g 1 fresh weight (fw) to 0.008 pg g 1 fw for PCDD/Fs and ranged from 0.020 pg g 1 fw to 0.034 pg g 1 fw for dl-PCBs. The recoveries of the labeled compounds were between 30% and 115% for all samples, which were in the range of the USEPA limits (USEPA-1613, 1994; USEPA-1668A, 1999).
2.2. Standard solutions and chemical reagents
2.6. Estimation of dietary intake of PCDD/Fs and DL-PCBs
The quantification standard solutions of PCDD/Fs and dioxinlike PCBs containing 15 congeners of 13C12-labeled PCDD/Fs and 12 congeners of 13C12-labeled-dioxin-like PCBs respectively and the 2 congeners of 13C12-labeled injection standard for PCDD/Fs and 3 congeners of 13C12-labeled injection standard for PCBs were all purchased from Wellington Laboratories (Guelph, Canada). The solvents including n-hexane, toluene, ethyl acetate, dichloromethane and acetone were purchased from J T Baker (Philipsburg, USA). All solvents were pesticide-grade. In addition, both diatomite and silica gel were bought from Merk (Darmstadt, Germany). The certified fish reference material of WMF-01 was supplied by Wellington Laboratories.
To assess the potential health risk from fish consumption, the possible maximum intakes from each fish species was calculated by multiplying the fish consumption rate (50 g d 1) acquired from the Guide to Chinese Diet (Chinese Nutrition Society, 2007) by TEQs concentration of PCDD/Fs and PCBs in each fish species followed by dividing by the standard body weight about 60 kg (Song et al., 2011).
2.3. Sample preparation and clean-up The edible filet tissues were dissected from each fish, mixed and homogenized by species, weighed and then freeze-dried. The purification procedure for PCDD/Fs and dl-PCBs was described
3. Results and discussion 3.1. PCDD/Fs and dl-PCBs congener’s patterns In this study, all of 17 PCDD/Fs and 12 dl-PCBs can be detected. As shown in Figs. 1–3, the predominating congeners of PCDDs are OCDD followed by 1,2,3,7,8-PeCDD and 1,2,3,4,6,7,8-HpCDD and the most abundant congeners of PCDFs are OCDF, 2,3,4,7,8-PeCDF as well as 2,3,7,8-TCDF and the PCB118 is found as the main dl-PCB congener, similar to some other studies (Isosaari et al.,
X. Wang et al. / Chemosphere 118 (2015) 163–169
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Fig. 1. Profiles of PCDD congeners in various fish samples.
Fig. 2. Profiles of PCDF congeners in various fish samples.
Fig. 3. Profiles of PCB congeners in various fish samples.
2002; Kiviranta et al., 2004; Sasamoto et al., 2006; Szlinder-Richert et al., 2009). But, few study reported that OCDF and PCB105 are the dominant compounds, which were found as main congeners in this study. The patterns of PCDDs, PCDFs and dl-PCBs in various fish exhibited interspecies differences which also can be observed from Figs. 1–3. For example, the percentage of 1,2,3,4,6,7,8-HpCDD is more than 60% in Trichiurus lepturus but it is close to zero in Miichthys miiuy. The contribution of 2,3,4,7,8-PeCDF in Navodon septentrionalis is significantly high close to 100%, however, in Pneumatophorus japonicus is less than 10%. PCB 118 and PCB 105 in all fish samples are dominant but there are some difference
among all dl-PCBs. Reports about the reasons that lead to the differences of compounds pattern in fish are scarce, only Kim et al. (2007) referred to metabolic processes might affect the patterns of PCDDs and PCDFs in biological tissues. 3.2. Levels of PCDD/Fs and dl-PCBs The TEQ levels of PCDDs, PCDFs and dl-PCBs are given in Table 1. The median levels of PCDDs, PCDFs and dl-PCBs were 0.008 pg TEQ g 1 fw, 0.0425 pg TEQ g 1 fw and 0.292 pg TEQ g 1 fw, respectively. The relation between levels of PCDD/Fs and dl-PCBs were analyzed by SPSS. The spearman correlation could
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Table 1 Levels of PCDDs, PCDFs, PCDD/Fs and dl-PCBs (pg TEQ g P Species WHO-TEQs PCDDs (pg/ g fw) Navodon septentrionalis Pneumatophorus japonicus Engraulis japonicus Lateolabrax japonicus Nimbochromis livingstonii Trichiurus lepturus Cephalopholis boenak Pseudosciaena polyactis Bombay duck Collichthys lucidus Goniistius quadricornis Ablennes anastomella Llisha elongata Bullet mackerel Scomberomorus niphonius Mugil cephalus Tenualosa reevesii Rachycentron canadum Oplegnathus fasciatus Pangio kuhlii Astroconger myriaster Miichthys miiuy Percocypris pingi Anguilli formes Pampus chinensis Paralichthys olivaceus Pagrosomus major Anchoa lucida Sebastiscus marmoratus Zebrias zebra Setipinna taty Lepidotrigla micropterus Mean a
1
fw)a in various fish from Zhoushan fishery. P P WHO-TEQs PCDFs (pg/ WHO-TEQs PCDD/Fs (pg/ g fw) g fw)
P WHO-TEQs dl-PCBs (pg/ g fw)
Total WHO-TEQs (pg/ g fw)
0.002
0.006
0.008
0.003
0.011
0.017
0.141
0.158
0.371
0.529
0.004 0.039 0.007
0.058 0.062 0.107
0.062 0.101 0.114
0.207 0.078 0.114
0.269 0.179 0.227
0.011 0.008 0.026
0.037 0.019 0.060
0.048 0.027 0.086
0.025 0.406 0.064
0.073 0.433 0.150
0.003 0.002 0.031 0.003 0.002 0.012 0.003
0.007 0.002 0.170 0.009 0.027 0.553 0.017
0.010 0.004 0.201 0.012 0.029 0.565 0.020
0.023 0.007 0.043 0.040 0.080 2.059 0.195
0.033 0.011 0.243 0.052 0.109 2.624 0.216
0.078 0.031 0.004 0.022 0.008 0.033 0.002 0.039 0.012 0.012 0.004 0.006 0.016 0.006
0.157 0.132 0.042 0.030 0.038 0.161 0.008 0.062 0.033 0.102 0.009 0.175 0.096 0.043
0.235 0.163 0.046 0.052 0.047 0.193 0.010 0.101 0.045 0.115 0.013 0.181 0.112 0.049
0.243 0.341 0.110 0.308 0.288 0.545 0.091 0.078 0.314 0.255 0.048 0.338 0.198 0.022
0.478 0.504 0.156 0.360 0.335 0.738 0.101 0.179 0.359 0.369 0.061 0.519 0.310 0.071
0.004 0.009 0.004
0.031 0.079 0.029
0.035 0.089 0.033
0.018 0.515 0.038
0.053 0.603 0.071
0.014
0.078
0.093
0.233
0.326
Based on WHO-TEQ 1998.
be observed in all fish species (r = 0.576, n = 32, p < 0.01). This indicated that PCDD/Fs and dl-PCBs in these fish were from similar sources. Compared with other studies, the levels of PCDDs, PCDFs and dl-PCBs in the studied fishes were much lower than levels measured by Lorber et al. (2009) and Moon and Ok (2006) and Shen et al. (2009). The polluted conditions of environment and various fish might lead to this difference. As revealed by the results, the levels of these compounds varied among collected fish species. The highest level of total PCDD/Fs and dl-PCBs was found in Bullet mackerel (2.624 pg pg TEQ g 1 fw), followed by Astroconger myriaster (0.738 pg TEQ g 1 fw) and Setipinna taty (0.603 pg TEQ g 1 fw). The lowest levels were observed in N. septentrionalis and Collichthys lucidus with 0.011 pg TEQ g 1 fw. Compared with the mean concentration, 12 fish species were above the mean level and 20 fish contained lower levels. Fish accumulate dioxins and dioxin-like PCBs in their fatty tissue and liver. It had been reported that, based on the fresh weight, a higher fish fat content correlated to a higher levels of PCDD/Fs and dl-PCBs (Rawn et al.,2006; Kim et al., 2007; Pandelova et al., 2008). This relation was found in this research as well. For example, the fat contents of B. mackerel, A. myriaster and S. taty which have higher levels of PCDD/Fs and dl-PCBs based on the fresh weight, were 16.70%, 12.56% and 11.26%, respectively. In contrast, the fat contents of N. septentrionalis and C. lucidus which have low levels of PCDD/Fs and dl-PCBs, were only 0.41% and 1.10%. The
results were analyzed for Spearman correlation. The significant correlation between fat content and total TEQs level was found (r = 0.778, n = 32, p < 0.01). There are also strong correlation between levels of PCDD/Fs and fat content (r = 0.622, n = 32, p < 0.01) as well as levels of dl-PCBs and fat content (r = 0.737, n = 32, p < 0.01). However, some exception was observed. The level of total TEQs in Pagrosomus major is nearly twice as much as Anchoa lucida, but the fat contents of them are similar. Therefore, some other factors except for fat contents affect the dioxin like compounds in fish. The feeding habit can affect the levels to some extent because these compounds can be bio-accumulated along the food chain (Ruus et al., 1999). However, as shown in Tables 2 and 3, the mean levels of total PCDD/Fs and dl-PCBs in carnivorous fish and omnivorous fish were very similar (0.33 pg TEQ g 1 fw and 0.31 pg TEQ g 1 fw, respectively). No significant differences could be discerned (t = 0.114, p > 0.05). The areas in which the fish live could influence the compounds levels in fish species. Generally, bottom dwelling/bottom feeding fish species are more exposed to contaminated sediments than pelagic fish species (The Codex Alimentarius Commission, 2012). As shown in Tables 2 and 3, in the same sea areas but different living zone, the levels of PCDD/ Fs and dl-PCBs are various in these collected fish, especially for omnivorous fish. The results reveal that omnivorous fish which have higher levels of PCDD/Fs and dl-PCBs usually live in the rocks
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X. Wang et al. / Chemosphere 118 (2015) 163–169 Table 2 Correlations between levels of total PCDD/Fs and dl-PCBs and feeding habit, fat content, living habit in omnivorous fish. P Species WHO-TEQs PCDD/Fs and dl-PCBs (pg/g fw) Feeding habit Fat content (%) Astroconger myriaster Tenualosa reevesii Mugil cephalus Oplegnathus fasciatus Pangio kuhlii Ablennes anastomella Bombay duck Navodon septentrionalis Mean
0.738 0.504 0.478 0.36 0.335 0.052 0.033 0.011 0.31
Omnivorous
12.56 14.4 8.08 4.92 3.24 5.86 1.02 0.41 –
Living habit Live in the rocks area and water plants Oceanodromous migration Live in shallow water Live in shallow water Live in the rocks area and water plants Live in the depth of 1–50 m Live in the middle water Live in the depth of 50–120 m –
Table 3 Correlations between levels of total PCDD/Fs and dl-PCBs and feeding habit, fat content, living habit in carnivorous fish. P Species WHO-TEQs PCDD/Fs and dl-PCBs Feeding Fat content Living habit (pg/g fw) habit (%) Bullet mackerel Setipinna taty Pneumatophorus japonicus Pagrosomus major
2.624 0.603 0.529
Carnivorous
0.519
8.34
Cephalopholis boenak Pampus chinensis Anguilli formes Anchoa lucida Engraulis japonicus Goniistius quadricornis Nimbochromis livingstonii Scomberomorus niphonius Percocypris pingi Lateolabrax japonicus Rachycentron canadum Pseudosciaena polyactis Llisha elongata Miichthys miiuy Trichiurus lepturus Lepidotrigla micropterus Sebastiscus marmoratus Paralichthys olivaceus Zebrias zebra Collichthys lucidus Mean
0.433 0.369 0.359 0.31 0.269 0.243
7.46 6.1 6.17 8.72 0.97 7.57
Live in nearshore shallow water and in the rocks area as well as water plants Live in the depth of 1–64 m Live in the depth of 1–10 m Live in the depth of 50–80 m Live in shallow water Live in the depth of 180–360 m Live in nearshore shallow water
0.227
3.83
Live in shallow water
0.216
3.34
Oceanodromous migration
0.179 0.179 0.156
0.69 0.53 3.74
Live in the depth of 1–70 m Live in nearshore shallow water Oceanodromous migration
0.15
3.6
Oceanodromous migration, live in the depth of 20–80 m
0.109 0.101 0.073 0.071
7.85 2.05 3.74 0.56
Live Live Live Live
0.071
1.84
Live in the rocks area
0.061 0.053 0.011 0.33
0.34 1.01 1.1
Live in shallow water Live in the sediments Live in the depth of about 20 m and in the sediment –
area and water plants, shallow waters or belong to oceanodromous migration. For example, A. myriaster, Tenualosa reevesii and Mugil cephalus which have higher levels of PCDD/Fs and dl-PCBs, all live in the above different areas. The carnivorous fish which live in the above areas do not always have high levels of PCDD/Fs and dl-PCBs. For instance, Sebastiscus marmoratus and Paralichthys olivaceus which live in the rocks area and shallow waters have low levels of PCDD/Fs and dl-PCBs. However, B mackerel and S. taty which live in the rocks area and shallow waters have high levels of these compounds. This difference can be influenced by the fat content mainly. Compared with other studies, in the different sea areas, the levels of PCDD/Fs and dl-PCBs in the same fish species such as Scomberomorus niphonius and Bombay duck have great difference (Bergkvist et al., 2008; Shen et al., 2009). The polluted situation in these different sea areas may lead to the differences. Furthermore, other than diet habits and living zone/area which depend on the fish species, the levels of these contaminants in fish may vary
16.7 11.26 15.51
–
Live in the rocks area Live in the depth of 4–13 m and in the sediments Oceanodromous migration
in in in in
nearshore shallow water the depth of 15–70 m the middle water the sediment
depending on the age, size and physiological characteristics of the fish (Kim et al., 2007; Pandelova et al., 2008; Szlinder-Richert et al., 2009). This study combined with other researches indicated that the levels of these compounds in fish might be influenced by complicated factors. 3.3. Health risk assessment and consuming advice Owing to the bioaccumulation characteristics of PCDD/Fs and dioxin-like PCBs, the Joint FAO/WHO Expert Committee on Food Additives (JECFA) proposed a provisional tolerable monthly intake (PTMI) of 70 pg TEQ/kg body weight (bw) as being protective of human health (JECFA, 2002). In the present study, the possible maximum monthly intake from each fish species was estimated and the results have been depicted in Table 4. The levels of dietary intake by fish consuming showed interspecies difference due to various levels of PCDD/Fs and dl-PCBs in these fish species. The current PCDD/Fs
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X. Wang et al. / Chemosphere 118 (2015) 163–169 Table 4 Estimated dietary intake of PCDD/Fs and dl-PCBs for population in Zhoushan city. Species
Monthly intake (pg WHO-TEQ/kg bw,/month)
Species
Navodon septentrionalis Pneumatophorus japonicus Engraulis japonicus Lateolabrax japonicus Nimbochromis livingstonii Trichiurus lepturus Cephalopholis boenak Pseudosciaena polyactis Bombay duck Collichthys lucidus Goniistius quadricornis Ablennes anastomella Llisha elongata Bullet mackerel Scomberomorus niphonius
0.26 13.22
Rachycentron canadum Oplegnathus fasciatus
3.91 9.01
6.72 4.48 5.68 1.83 10.83 3.75 0.82 0.28 6.09 1.29 2.73 65.61 5.39
8.38 18.45 2.52 4.48 8.97 9.24 1.52 12.96 7.75 1.77 1.32 15.08 1.77
Mugil cephalus Tenualosa reevesii
11.94 12.60
Pangio kuhlii Astroconger myriaster Miichthys miiuy Percocypris pingi Anguilli formes Pampus chinensis Paralichthys olivaceus Pagrosomus major Anchoa lucida Sebastiscus marmoratus Zebrias zebra Setipinna taty Lepidotrigla micropterus Mean –
and dl-PCBs intake through different fish species range from 0.26 to 65.61 pg TEQ kg 1 bw month 1. The mean dietary intake of total PCDD/Fs and dl-PCBs was 10.39 pg TEQ kg 1 bw month 1, only accounting for 14.8% of the PTMI. Compared with other studies, the mean level of dietary intake in this study was lower than the value (18.5 pg TEQ kg 1 bw month 1) acquired in south China (Zhang et al. 2008). However, it should be noted that the highest monthly intake level (65.61 pg TEQ kg 1 bw month 1) from B. mackerel was much more than that from other species and was very close to the PMTI of 70 pg TEQ kg 1 bw month 1 accounting for 93.7% of PMTI. Although the possible maximum monthly intake of dioxin-like compounds from B. mackerel was based on the assumption that only this species was consumed, the present study suggested the potential health risk should be concerned seriously. Except B. mackerel, the dioxin-like compounds intakes from most consumed fish were far from the PTMI. However, as a country with rapid industrialization, health risk associated with various contaminants released from industries to environment would continue to increase in the future years in China. In some previous studies, increasing trend for dioxin-like compounds in environment and human in China were estimated (Zheng et al., 2008; Li et al., 2009). From China total dietary study, increasing trend on dietary intake of dioxin-like compounds was also found for most of residents in China between 2000 and 2007 (Zhang et al., 2013). Therefore, to protect health, we should select the fish species which accumulate less dioxin-like compounds. The present study provides essential information for the selection. Additionally, the monitoring of these contaminants in fish should be conducted continuously to assess the intake levels and to provide risk-based consumption advice in time. Acknowledgements This study was financially supported by the National Nature Science of Foundation of China (No. 81172675), the Special Foundation for Young Scientists of Department of Health of Hubei Province (QJX2010-33) and the Welfare Technology Applied Research Program of Zhejiang Province, China (2011C33001, 2012C23034). Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.chemosphere. 2014.07.057.
Monthly intake(pg WHO-TEQ/kg bw,/month)
8.14 –
References
Baars, A.J., Bakker, M.I., Baumann, R.A., Boon, P.E., Freijer, J.I., Hoogenboom, L.A.P., Hoogerbrugge, R., Klaveren van, J.D., Liem, A.K.D., Traag, W.A., Vries de, J., 2004. Dioxins, dioxin-like PCBs and non-dioxin-like PCBs in foodstuffs: occurrence and dietary intake in The Netherlands. Toxicol. Lett. 151, 51–61. Bergkvist, C., Öberg, M., Appelgren, M., Becker, W., Aune, M., Ankarberg, H.E., Berglund, M., Håkansson, H., 2008. Exposure to dioxin-like pollutants via different food commodities in Swedish children and young adults. Food Chem. Toxicol. 46, 3360–3367. Clapp, R., Ozonoff, D., 2000. Where the boys aren’t: dioxin and the sex ratio. Lancet 335, 1838–1839. Chinese Nutrition Society, 2007. The guide to Chinese diet. . Dannenberger, D., Andersson, R., Rappe, C., 1997. Levels and patterns of polychlorinated dibenzo-p-dioxins, dibenzofurans and biphenyls in surface sediments from the western Baltic Sea (Arkona Basin) and the Oder River estuarine system. Mar. Pollut. Bull. 34, 1016–1024. Fernandes, A., Mortimer, D., Rose, M., Gem, M., 2010. Dioxins (PCDD/Fs) and PCBs in offal: occurrence and dietary exposure. Chemosphere 81, 536–540. Grassi, P., Fattore, E., Generoso, C., Fanelli, R., Arvati, M., Zuccato, E., 2010. Polychlorobiphenyls (PCBs), polychlorinated dibenzo-p-dioxins (PCDDs) and dibenzofurans (PCDFs) in fruit and vegetables from an industrial area in northern Italy. Chemosphere 79, 292–298. Isosaari, P., Vartiainen, T., Hallikainen, A., Ruohonen, K., 2002. Feeding trial on rainbow trout: comparison of dry fish feed and Baltic herring as a source of PCDD/Fs and PCBs. Chemosphere 48, 795–804. Joint FAO/WHO Expert Committee on Food Additives (JECFA), 2002. Evaluation of Certain Food Additives and Contaminants 57th Report of the Joint FAO/WHO Expert Committee on Foods Additives. WHO Technical Report Series, No. 909. . Kim, B.H., Ikonomou, M.G., Lee, S.J., Kim, H.S., Chang, Y.S., 2005. Concentrations of polybrominated diphenylethers, polychlorinated dibenzo-p-dioxins and dibenzofurans, and polychlorinated biphenyls in human blood samples from Korea. Sci. Total Environ. 336, 45–56. Kim, M., Kim, S., Yun, S.J., Kim, D.G., Chung, G.S., 2007. Background levels and dietary intake of PCDD/Fs in domestic and imported meat in South Korea. Chemosphere 69, 479–484. Kiviranta, H., Ovaskainen, L.M., Vartiainen, T., 2004. Market basket study on dietary intake of PCDD/Fs, PCBs, and PBDEs in Finland. Environ. Int. 30, 923–932. Li, J.G., Wu, Y.N., Zhang, L., Zhao, Y.F., 2007. Dietary intake of polychlorinated dioxins, furans and dioxin-like polychlorinated biphenyls from foods of animal origin in China. Food Addit. Contam. 24, 186–193. Li, J.G., Zhang, L., Wu, Y.N., LiuY, P., Zhou, P.P., Wen, S., Liu, J.Y., Zhao, Y.F., Li, X.W., 2009. A national survey of polychlorinated dioxins, furans (PCDD/Fs) and dioxin-like polychlorinated biphenyls (dl-PCBs) in human milk in China. Chemosphere 75, 1236–1242. Liu, Y.P., Li, J.G., Zhao, Y.F., Wen, S., Huang, F.F., Wu, Y.N., 2011. Polybrominated diphenyl ethers (PBDEs) and indicator polychlorinated biphenyls (PCBs) in marine fish from four areas of China. Chemosphere 83, 168–174. Lorber, M., Patterson, D., Huwe, J., Kahn, H., 2009. Evaluation of background exposures of Americans to dioxin-like compounds in the 1990s and the 2000s. Chemosphere 77, 640–651. Moon, H.B., Ok, G., 2006. Dietary intake of PCDDs, PCDFs and dioxin-like PCBs, due to the consumption of various marine organisms from Korea. Chemosphere 62, 1142–1152.
X. Wang et al. / Chemosphere 118 (2015) 163–169 Oh, J.R., Ikonomou, M.G., Fernandez, M.P., Hong, S.H., 2003. PCB and PCDD/F totals, TEQs and congener patterns in Korean coastal marine environments, 1987, 1988, 1990, and 1996–1999. Arch. Environ. Contam. Toxicol. 44, 224– 236. Pandelova, M., Henkelmann, B., Roots, O., Simm, M., Jarv, L., Benfenati, E., Schramm, K.-W., 2008. Levels of PCDD/F and dioxin-like PCB in Baltic fish of different age and gender. Chemosphere 71, 369–378. Rawn, F.K.D., Forsyth, S.D., Ryan, J.J., Breakell, K., Verigin, V., Nicolidakis, H., Hayward, S., Laffey, P., Conacher, B.S.H., 2006. PCB, PCDD and PCDF residues in fin and non-fin fish products from the Canadian retail market 2002. Sci. Total Environ. 359, 101–110. Ruus, A., Ugland, K.I., Espeland, O., Skaare, J.U., 1999. Organochlorine contaminants in a local marine food chain from Jarfjord, Northern Norway. Mar. Environ. Res. 48, 131–146. Safe, S., 1990. Polychlorinated biphenyls (PCBs) dibenzo-p-dioxins (PCDDs) dibenzofurans (PCDFs) and related compounds: environmental and mechanistic considerations which support the development of toxic equivalency factors (TEFs). Crit. Rev. Toxicol. 21, 51–88. Sasamoto, T., Ushio, F., Kikutani, N., Saitoh, Y., Yamaki, Y., Hashimoto, T., Horii, S., Nakagawa, J., Ibe, A., 2006. Estimation of 1999–2004 dietary daily intake of PCDDs, PCDFs and dioxin-like PCBs by a total diet study in metropolitan Tokyo, Japan. Chemosphere 64, 634–641. Shen, H.T., Han, J.L., Tie, X.W., Xu, W., Ren, Y.P., Ye, C.S., 2009a. Polychlorinated dibenzo-p-dioxins/furans and polychlorinated biphenyls in human adipose tissue from Zhejiang province, China. Chemosphere 74, 384–388. Shen, H.T., Yu, C., Ying, Y., Zhao, Y.F., Wu, Y.N., Han, J.L., Xu, Q.Y., 2009b. Levels and congener profiles of PCDD/Fs, PCBs and PBDEs in seafood from China. Chemosphere 77, 1206–1211. Song, Y., Wu, N.X., Han, J.L., Shen, H.T., Tan, Y.F., Ding, G.Q., Xiang, J.X., Tao, H., Jin, S.L., 2011. Levels of PCDD/Fs and DL-PCBs in selected foods and estimated dietary intake for the local residents of Luqiao and Yuhang in Zhejiag, China. Chemosphere 85, 329–334.
169
Szlinder-Richert, J., Barska, I., Usydus, Z., Ruczynska, W., Grabic, R., 2009. Investigation of PCDD/Fs and dl-PCBs in fish from the southern Baltic Sea during the 2002–2006 period. Chemosphere 74, 1509–1515. The Codex Alimentarius Commission, 2012. Prevention and Reduction of Food and Feed Contamination, first ed. World Health Organization, Food and Agriculture Organization of the United nations, Rome. USEPA Method1613, 1994. Tetra- through octa-chlorinated dioxins and furans by isotope dilution HRGC/HRMS. Washington, D.C. USEPA Method1668A, 1999. Interlaboratory Validation Study Report. Washington, D.C. United States Environment Protection Agency (USEPA), 2010. Persistent Organic Pollutants: A Global Issue, A Global Response. van Leeuwen, F.X.R., Feeley, M., Schrenk, D., Larsen, C.J., Farland, W., Younes, M., 2000. Dioxins WHOs tolerable daily intake (TDI) revisited. Chemosphere 40, 1095–1101. Wang, I.C., Wu, Y.L., Lin, L.F., Chang-Chien, G.P., 2009. Human dietary exposure to polychlorinated dibenzo-p-dioxins and polychlorinated dibenzofurans in Taiwan. J. Hazard. Mater. 164, 621–626. Zhang, J.Q., Jiang, Y.S., Zhou, J., Fang, D.K., Jiang, J., Liu, G.H., Zhang, H.Y., Xie, J.B., Huang, W., Zhang, J.Z., Li, H., Wang, Z., Pan, L.B., 2008. Concentrations of PCDD/ PCDFs and PCBs in retail foods and an assessment of dietary intake for local population of Shenzhen in China. Environ. Int. 34, 799–803. Zhang, L., Li, J.G., Liu, X., Zhao, Y.F., Li, X.W., Wen, S., Wu, Y.N., 2013a. Dietary intake of PCDD/Fs and dioxin-like PCBs from the Chinese total diet study in 2007. Chemosphere 90, 1625–1630. Zhang, L., Li, J.G., Zhao, Y.F., Li, X.W., Wen, S., Shen, H.T., Wu, Y.N., 2013b. Polybrominated diphenyl ethers (PBDEs) and indicator polychlorinated biphenyls (PCBS) in foods from China: levels, dietary intake, and risk assessment. Agric. Food Chem. 61, 6544–6551. Zheng, J.G., Leung, O.W.A., Jiao, P.L., Wong, H.M., 2008. Polychlorinated dibenzo-pdioxins and dibenzofurans pollution in China: sources, environmental levels and potential human health impacts. Environ. Int. 34, 1050–1061.
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Assessment on dioxin-like compounds intake from various marine fish from Zhoushan Fishery, China Xiangyong Wang a,b, Hongxia Zhang a,c, Lei Zhang a, Kai Zhong a,⇑, Xiaohong Shang a, Yunfeng Zhao a, Zhendong Tong d, Xinwei Yu d, Jingguang Li a,b,⇑, Yongning Wu a,b a
Key Laboratory of Food Safety Risk Assessment, Ministry of Health, China National Center for Food Safety Risk Assessment, Beijing 100021, China State Key Laboratory of Food Science and Technology, Nanchang University, Nanchang 330047, China School of Public Health, Shanxi Medical University, Taiyuan 030001, China d Zhoushan Municipal Center for Disease Control and Prevention, Zhoushan 316021, China b c
h i g h l i g h t s 32 Fish species were measure for 29 dioxin-like compounds. The factors effecting the accumulation of the compounds in sea fish were discussed. A risk-based consumption advice for sea fish was developed.
a r t i c l e
i n f o
Article history: Received 24 October 2013 Received in revised form 19 June 2014 Accepted 20 July 2014 Available online 1 September 2014 Handling Editor: H. Fiedler Keywords: Dioxin-like compounds Accumulation Fish species Intake assessment Risk-based consumption advice
a b s t r a c t Sea fish consuming is an important intake source of dioxin-like compounds, especially for the coastal residents. To assess the intake levels of these contaminants from sea fish and to provide risk-based consumption advice, concentrations of 17 polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs) and 12 dioxin-like polychlorinated biphenyls (dl-PCBs) were measured in 32 commonly consumed fish species from Zhoushan Fishery, China. Due to the different accumulation influenced by fat content, feed habits and living zone in the sea area, the levels of PCDDs, PCDFs and dl-PCBs in different fish species varied significantly ranging from 0.002 to 0.078 pg WHO-TEQ/g fresh weight, from 0.002 to 0.553 pg WHOTEQ/g fresh weight and from 0.003 to 2.059 pg WHO-TEQ/g fresh weight, respectively. Based on mean fish consuming rate in China, the estimated maximum possible dioxin-like compounds intake through different fish species ranged from 0.26 to 65.61 pg TEQ kg 1 bw month 1. Bullet mackerel has the highest monthly intake level which was much higher than other fish species and very close to the provisional tolerable monthly intake (70 pg TEQ kg 1 bw month 1) proposed by the Joint FAO/WHO Expert Committee on Food Additives. Hence, comparing to other fish species, the consumption of Bullet mackerel from Zhoushan Fishery should be cautious to reduce the potential health risk. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction Polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/ Fs) and dioxin-like polychlorinated biphenyls (dl-PCBs) are the broad class of environmental pollutants which are ubiquitous in the environment worldwide. PCDD/Fs are unwanted by-products mainly from incomplete combustion as well as manufacture of
⇑ Corresponding authors. Tel./fax: +86 010 67776790 (K. Zhong). Address: Key Laboratory of Food Safety Risk Assessment, Ministry of Health, China National Center for Food Safety Risk Assessment, Beijing 100021, China. Tel.: +86 010 67720035; fax: +86 010 67791253 (J. Li). E-mail addresses: [email protected] (K. Zhong), [email protected] (J. Li). http://dx.doi.org/10.1016/j.chemosphere.2014.07.057 0045-6535/Ó 2014 Elsevier Ltd. All rights reserved.
certain chemicals (Dannenberger et al., 1997; Kim et al., 2005). Dl-PCBs mainly stemmed from the production and usage of the commercial PCBs mixtures, which has been banned in 1970s, as well as leakage from the container (Baars et al., 2004). The great concern on PCDD/Fs and dl-PCBs by humans is their potential risk to human health (Clapp and Ozonoff, 2000; Oh et al., 2003). In literature, effects on the reproductive-, immune- and nervous system have been reported (Safe, 1990; USEPA, 2010). For humans, the exposure pathways to PCDD/Fs and dl-PCBs are dermal contact, inhalation and food intake. Among them, the dietary intake is the main pathway for general population, accounting for more than 90% (van Leeuwen et al., 2000; Wang et al., 2009; Fernandes et al., 2010; Grassi et al., 2010). There are
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many studies reporting fish as main food contributor (Kim et al., 2007; Zhang et al., 2008; Lorber et al., 2009). In China, especially in southeast China, aquatic foods corresponded to the dominant contribution to the dietary intake of PCDD/Fs and PCBs (Li et al., 2007; Zhang et al., 2013). These findings revealed the importance of fish as a source of potential exposure to toxic pollutants such as PCDD/Fs and PCBs. This is of great concern taking into account the nutritional role of fish as a part of a healthy diet, whose relevance has notably increased in recent years. In order to monitor the levels of PCDD/Fs and dl-PCBs in seafood and assure the health of humans, data on these compounds in sea fish and other sea food were reported gradually during recent years in China (Liu et al., 2011; Shen et al., 2009; Zhang et al., 2008). In the developed area of China, especially in southeast China, the high level body burden of dioxin-like compounds may be due to high consumption of aquatic food such as sea fish in these areas (Li et al., 2009; Zhang et al., 2013). Therefore, the detailed advices on edible fish selection regarding to dioxin-like compounds level could be essential to reduce the dietary intake of these contaminations in these area. In the present study, 32 fish species from Zhoushan fishery which is the largest fishery in southeast China were selected. These species are the most consumed by the local general population. Through analyzing the levels of the dioxin-like compounds and characterizing the factors affecting accumulation in these fishes, risk assessment on dioxin-like compounds from fish consumption for general population was conducted and the risk-based consumption advice for fish species selection was recommended.
previously (Li et al., 2007). In brief, after freeze-drying, the 15 congeners of 13C12-labeled PCDD/Fs and 12 congeners of 13 C12-labeled-dioxin-like PCBs were spiked in the samples, followed by Soxhlet-extracted with a mixture n-hexane/dichloromethane (1:1) and the bulk fat was removed by shaking with acid-modified silica-gel. Sample cleanup was performed using a through Power Prep instrument (Fluid Managment Systems, Waltham, MA, USA). The eluting fractions were concentrated to about 10 lL and the 13 C12-labeled injection standard for PCDD/Fs and PCBs was added into the concentrated solutions respectively prior to analysis. 2.4. HRGC/HRMS analysis
2. Materials and methods
The seventeen most toxic congeners of PCDD/Fs and twelve congeners of dioxin-like PCBs were analyzed by HRGC/HRMS (MAT95XP, ThermoFinnigan, German) equipped with DB-5MS capillary column (60 m 0.25 mm 0.25 lm) at 10 000 resolution using the splitless injection mode and multiple ion monitoring (MID). The temperature program for the analysis of PCDD/Fs started with 1 min at 120 °C, raised to 220 °C at 44 °C min 1 holding for 15 min, and then to 250 °C at 2.3 °C min 1 and from 250 °C to 260 °C at 0.9 °C min 1, lastly, ultimately to 310 °C at 20 °C min 1 holding for 11 min. In addition, the temperature was held for 1 min at 90 °C and programmed to 180 °C at 20 °C min 1 holding for 1 min, then further to 300 °C at 3 °C min 1 and held for 2 min for the analysis of dioxin-like PCBs. The temperatures of injector, transfer line, ion source and interface temperatures were 260 °C, 270 °C, 260 °C and 280 °C, respectively, ionization energy 60 eV and trap current 1.00 mA.
2.1. Sample collection
2.5. Quality control and assurance
Zhoushan, the only city on the sea composed of archipelago, is located at the junction of the southeast seashore and the entrance to the sea of Yangtze River, backing Shanghai, Hangzhou and Ningbo City, facing the Pacific Ocean. Zhoushan Fishery is the biggest fishery in China, known as ‘‘East China Sea fish warehouse’’. The annual output of aquatic products is around 1.3 million tons. The offshore ocean fishing output is more than one tenth of the country’s total. During the months of September and October 2011, the 32 fish species which are most consumed by local residents from the Zhoushan Fishery were acquired. Three individual fish were collected for each fish species. Samples were frozen at 20 °C until analysis. More information of these fish is shown in Table A1.
The laboratory performance was validated by successfully participating interlaboratory comparison of POPs in food organized by the Norwegian Institute of Public Health in 2012. In this study, the laboratory method blanks were performed every eight samples. Certified fish reference material WMF-01 (Wellington Laboratories) was analyzed for method validation and as a quality control sample. The method detection limits ranged from 0.001 pg g 1 fresh weight (fw) to 0.008 pg g 1 fw for PCDD/Fs and ranged from 0.020 pg g 1 fw to 0.034 pg g 1 fw for dl-PCBs. The recoveries of the labeled compounds were between 30% and 115% for all samples, which were in the range of the USEPA limits (USEPA-1613, 1994; USEPA-1668A, 1999).
2.2. Standard solutions and chemical reagents
2.6. Estimation of dietary intake of PCDD/Fs and DL-PCBs
The quantification standard solutions of PCDD/Fs and dioxinlike PCBs containing 15 congeners of 13C12-labeled PCDD/Fs and 12 congeners of 13C12-labeled-dioxin-like PCBs respectively and the 2 congeners of 13C12-labeled injection standard for PCDD/Fs and 3 congeners of 13C12-labeled injection standard for PCBs were all purchased from Wellington Laboratories (Guelph, Canada). The solvents including n-hexane, toluene, ethyl acetate, dichloromethane and acetone were purchased from J T Baker (Philipsburg, USA). All solvents were pesticide-grade. In addition, both diatomite and silica gel were bought from Merk (Darmstadt, Germany). The certified fish reference material of WMF-01 was supplied by Wellington Laboratories.
To assess the potential health risk from fish consumption, the possible maximum intakes from each fish species was calculated by multiplying the fish consumption rate (50 g d 1) acquired from the Guide to Chinese Diet (Chinese Nutrition Society, 2007) by TEQs concentration of PCDD/Fs and PCBs in each fish species followed by dividing by the standard body weight about 60 kg (Song et al., 2011).
2.3. Sample preparation and clean-up The edible filet tissues were dissected from each fish, mixed and homogenized by species, weighed and then freeze-dried. The purification procedure for PCDD/Fs and dl-PCBs was described
3. Results and discussion 3.1. PCDD/Fs and dl-PCBs congener’s patterns In this study, all of 17 PCDD/Fs and 12 dl-PCBs can be detected. As shown in Figs. 1–3, the predominating congeners of PCDDs are OCDD followed by 1,2,3,7,8-PeCDD and 1,2,3,4,6,7,8-HpCDD and the most abundant congeners of PCDFs are OCDF, 2,3,4,7,8-PeCDF as well as 2,3,7,8-TCDF and the PCB118 is found as the main dl-PCB congener, similar to some other studies (Isosaari et al.,
X. Wang et al. / Chemosphere 118 (2015) 163–169
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Fig. 1. Profiles of PCDD congeners in various fish samples.
Fig. 2. Profiles of PCDF congeners in various fish samples.
Fig. 3. Profiles of PCB congeners in various fish samples.
2002; Kiviranta et al., 2004; Sasamoto et al., 2006; Szlinder-Richert et al., 2009). But, few study reported that OCDF and PCB105 are the dominant compounds, which were found as main congeners in this study. The patterns of PCDDs, PCDFs and dl-PCBs in various fish exhibited interspecies differences which also can be observed from Figs. 1–3. For example, the percentage of 1,2,3,4,6,7,8-HpCDD is more than 60% in Trichiurus lepturus but it is close to zero in Miichthys miiuy. The contribution of 2,3,4,7,8-PeCDF in Navodon septentrionalis is significantly high close to 100%, however, in Pneumatophorus japonicus is less than 10%. PCB 118 and PCB 105 in all fish samples are dominant but there are some difference
among all dl-PCBs. Reports about the reasons that lead to the differences of compounds pattern in fish are scarce, only Kim et al. (2007) referred to metabolic processes might affect the patterns of PCDDs and PCDFs in biological tissues. 3.2. Levels of PCDD/Fs and dl-PCBs The TEQ levels of PCDDs, PCDFs and dl-PCBs are given in Table 1. The median levels of PCDDs, PCDFs and dl-PCBs were 0.008 pg TEQ g 1 fw, 0.0425 pg TEQ g 1 fw and 0.292 pg TEQ g 1 fw, respectively. The relation between levels of PCDD/Fs and dl-PCBs were analyzed by SPSS. The spearman correlation could
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Table 1 Levels of PCDDs, PCDFs, PCDD/Fs and dl-PCBs (pg TEQ g P Species WHO-TEQs PCDDs (pg/ g fw) Navodon septentrionalis Pneumatophorus japonicus Engraulis japonicus Lateolabrax japonicus Nimbochromis livingstonii Trichiurus lepturus Cephalopholis boenak Pseudosciaena polyactis Bombay duck Collichthys lucidus Goniistius quadricornis Ablennes anastomella Llisha elongata Bullet mackerel Scomberomorus niphonius Mugil cephalus Tenualosa reevesii Rachycentron canadum Oplegnathus fasciatus Pangio kuhlii Astroconger myriaster Miichthys miiuy Percocypris pingi Anguilli formes Pampus chinensis Paralichthys olivaceus Pagrosomus major Anchoa lucida Sebastiscus marmoratus Zebrias zebra Setipinna taty Lepidotrigla micropterus Mean a
1
fw)a in various fish from Zhoushan fishery. P P WHO-TEQs PCDFs (pg/ WHO-TEQs PCDD/Fs (pg/ g fw) g fw)
P WHO-TEQs dl-PCBs (pg/ g fw)
Total WHO-TEQs (pg/ g fw)
0.002
0.006
0.008
0.003
0.011
0.017
0.141
0.158
0.371
0.529
0.004 0.039 0.007
0.058 0.062 0.107
0.062 0.101 0.114
0.207 0.078 0.114
0.269 0.179 0.227
0.011 0.008 0.026
0.037 0.019 0.060
0.048 0.027 0.086
0.025 0.406 0.064
0.073 0.433 0.150
0.003 0.002 0.031 0.003 0.002 0.012 0.003
0.007 0.002 0.170 0.009 0.027 0.553 0.017
0.010 0.004 0.201 0.012 0.029 0.565 0.020
0.023 0.007 0.043 0.040 0.080 2.059 0.195
0.033 0.011 0.243 0.052 0.109 2.624 0.216
0.078 0.031 0.004 0.022 0.008 0.033 0.002 0.039 0.012 0.012 0.004 0.006 0.016 0.006
0.157 0.132 0.042 0.030 0.038 0.161 0.008 0.062 0.033 0.102 0.009 0.175 0.096 0.043
0.235 0.163 0.046 0.052 0.047 0.193 0.010 0.101 0.045 0.115 0.013 0.181 0.112 0.049
0.243 0.341 0.110 0.308 0.288 0.545 0.091 0.078 0.314 0.255 0.048 0.338 0.198 0.022
0.478 0.504 0.156 0.360 0.335 0.738 0.101 0.179 0.359 0.369 0.061 0.519 0.310 0.071
0.004 0.009 0.004
0.031 0.079 0.029
0.035 0.089 0.033
0.018 0.515 0.038
0.053 0.603 0.071
0.014
0.078
0.093
0.233
0.326
Based on WHO-TEQ 1998.
be observed in all fish species (r = 0.576, n = 32, p < 0.01). This indicated that PCDD/Fs and dl-PCBs in these fish were from similar sources. Compared with other studies, the levels of PCDDs, PCDFs and dl-PCBs in the studied fishes were much lower than levels measured by Lorber et al. (2009) and Moon and Ok (2006) and Shen et al. (2009). The polluted conditions of environment and various fish might lead to this difference. As revealed by the results, the levels of these compounds varied among collected fish species. The highest level of total PCDD/Fs and dl-PCBs was found in Bullet mackerel (2.624 pg pg TEQ g 1 fw), followed by Astroconger myriaster (0.738 pg TEQ g 1 fw) and Setipinna taty (0.603 pg TEQ g 1 fw). The lowest levels were observed in N. septentrionalis and Collichthys lucidus with 0.011 pg TEQ g 1 fw. Compared with the mean concentration, 12 fish species were above the mean level and 20 fish contained lower levels. Fish accumulate dioxins and dioxin-like PCBs in their fatty tissue and liver. It had been reported that, based on the fresh weight, a higher fish fat content correlated to a higher levels of PCDD/Fs and dl-PCBs (Rawn et al.,2006; Kim et al., 2007; Pandelova et al., 2008). This relation was found in this research as well. For example, the fat contents of B. mackerel, A. myriaster and S. taty which have higher levels of PCDD/Fs and dl-PCBs based on the fresh weight, were 16.70%, 12.56% and 11.26%, respectively. In contrast, the fat contents of N. septentrionalis and C. lucidus which have low levels of PCDD/Fs and dl-PCBs, were only 0.41% and 1.10%. The
results were analyzed for Spearman correlation. The significant correlation between fat content and total TEQs level was found (r = 0.778, n = 32, p < 0.01). There are also strong correlation between levels of PCDD/Fs and fat content (r = 0.622, n = 32, p < 0.01) as well as levels of dl-PCBs and fat content (r = 0.737, n = 32, p < 0.01). However, some exception was observed. The level of total TEQs in Pagrosomus major is nearly twice as much as Anchoa lucida, but the fat contents of them are similar. Therefore, some other factors except for fat contents affect the dioxin like compounds in fish. The feeding habit can affect the levels to some extent because these compounds can be bio-accumulated along the food chain (Ruus et al., 1999). However, as shown in Tables 2 and 3, the mean levels of total PCDD/Fs and dl-PCBs in carnivorous fish and omnivorous fish were very similar (0.33 pg TEQ g 1 fw and 0.31 pg TEQ g 1 fw, respectively). No significant differences could be discerned (t = 0.114, p > 0.05). The areas in which the fish live could influence the compounds levels in fish species. Generally, bottom dwelling/bottom feeding fish species are more exposed to contaminated sediments than pelagic fish species (The Codex Alimentarius Commission, 2012). As shown in Tables 2 and 3, in the same sea areas but different living zone, the levels of PCDD/ Fs and dl-PCBs are various in these collected fish, especially for omnivorous fish. The results reveal that omnivorous fish which have higher levels of PCDD/Fs and dl-PCBs usually live in the rocks
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X. Wang et al. / Chemosphere 118 (2015) 163–169 Table 2 Correlations between levels of total PCDD/Fs and dl-PCBs and feeding habit, fat content, living habit in omnivorous fish. P Species WHO-TEQs PCDD/Fs and dl-PCBs (pg/g fw) Feeding habit Fat content (%) Astroconger myriaster Tenualosa reevesii Mugil cephalus Oplegnathus fasciatus Pangio kuhlii Ablennes anastomella Bombay duck Navodon septentrionalis Mean
0.738 0.504 0.478 0.36 0.335 0.052 0.033 0.011 0.31
Omnivorous
12.56 14.4 8.08 4.92 3.24 5.86 1.02 0.41 –
Living habit Live in the rocks area and water plants Oceanodromous migration Live in shallow water Live in shallow water Live in the rocks area and water plants Live in the depth of 1–50 m Live in the middle water Live in the depth of 50–120 m –
Table 3 Correlations between levels of total PCDD/Fs and dl-PCBs and feeding habit, fat content, living habit in carnivorous fish. P Species WHO-TEQs PCDD/Fs and dl-PCBs Feeding Fat content Living habit (pg/g fw) habit (%) Bullet mackerel Setipinna taty Pneumatophorus japonicus Pagrosomus major
2.624 0.603 0.529
Carnivorous
0.519
8.34
Cephalopholis boenak Pampus chinensis Anguilli formes Anchoa lucida Engraulis japonicus Goniistius quadricornis Nimbochromis livingstonii Scomberomorus niphonius Percocypris pingi Lateolabrax japonicus Rachycentron canadum Pseudosciaena polyactis Llisha elongata Miichthys miiuy Trichiurus lepturus Lepidotrigla micropterus Sebastiscus marmoratus Paralichthys olivaceus Zebrias zebra Collichthys lucidus Mean
0.433 0.369 0.359 0.31 0.269 0.243
7.46 6.1 6.17 8.72 0.97 7.57
Live in nearshore shallow water and in the rocks area as well as water plants Live in the depth of 1–64 m Live in the depth of 1–10 m Live in the depth of 50–80 m Live in shallow water Live in the depth of 180–360 m Live in nearshore shallow water
0.227
3.83
Live in shallow water
0.216
3.34
Oceanodromous migration
0.179 0.179 0.156
0.69 0.53 3.74
Live in the depth of 1–70 m Live in nearshore shallow water Oceanodromous migration
0.15
3.6
Oceanodromous migration, live in the depth of 20–80 m
0.109 0.101 0.073 0.071
7.85 2.05 3.74 0.56
Live Live Live Live
0.071
1.84
Live in the rocks area
0.061 0.053 0.011 0.33
0.34 1.01 1.1
Live in shallow water Live in the sediments Live in the depth of about 20 m and in the sediment –
area and water plants, shallow waters or belong to oceanodromous migration. For example, A. myriaster, Tenualosa reevesii and Mugil cephalus which have higher levels of PCDD/Fs and dl-PCBs, all live in the above different areas. The carnivorous fish which live in the above areas do not always have high levels of PCDD/Fs and dl-PCBs. For instance, Sebastiscus marmoratus and Paralichthys olivaceus which live in the rocks area and shallow waters have low levels of PCDD/Fs and dl-PCBs. However, B mackerel and S. taty which live in the rocks area and shallow waters have high levels of these compounds. This difference can be influenced by the fat content mainly. Compared with other studies, in the different sea areas, the levels of PCDD/Fs and dl-PCBs in the same fish species such as Scomberomorus niphonius and Bombay duck have great difference (Bergkvist et al., 2008; Shen et al., 2009). The polluted situation in these different sea areas may lead to the differences. Furthermore, other than diet habits and living zone/area which depend on the fish species, the levels of these contaminants in fish may vary
16.7 11.26 15.51
–
Live in the rocks area Live in the depth of 4–13 m and in the sediments Oceanodromous migration
in in in in
nearshore shallow water the depth of 15–70 m the middle water the sediment
depending on the age, size and physiological characteristics of the fish (Kim et al., 2007; Pandelova et al., 2008; Szlinder-Richert et al., 2009). This study combined with other researches indicated that the levels of these compounds in fish might be influenced by complicated factors. 3.3. Health risk assessment and consuming advice Owing to the bioaccumulation characteristics of PCDD/Fs and dioxin-like PCBs, the Joint FAO/WHO Expert Committee on Food Additives (JECFA) proposed a provisional tolerable monthly intake (PTMI) of 70 pg TEQ/kg body weight (bw) as being protective of human health (JECFA, 2002). In the present study, the possible maximum monthly intake from each fish species was estimated and the results have been depicted in Table 4. The levels of dietary intake by fish consuming showed interspecies difference due to various levels of PCDD/Fs and dl-PCBs in these fish species. The current PCDD/Fs
168
X. Wang et al. / Chemosphere 118 (2015) 163–169 Table 4 Estimated dietary intake of PCDD/Fs and dl-PCBs for population in Zhoushan city. Species
Monthly intake (pg WHO-TEQ/kg bw,/month)
Species
Navodon septentrionalis Pneumatophorus japonicus Engraulis japonicus Lateolabrax japonicus Nimbochromis livingstonii Trichiurus lepturus Cephalopholis boenak Pseudosciaena polyactis Bombay duck Collichthys lucidus Goniistius quadricornis Ablennes anastomella Llisha elongata Bullet mackerel Scomberomorus niphonius
0.26 13.22
Rachycentron canadum Oplegnathus fasciatus
3.91 9.01
6.72 4.48 5.68 1.83 10.83 3.75 0.82 0.28 6.09 1.29 2.73 65.61 5.39
8.38 18.45 2.52 4.48 8.97 9.24 1.52 12.96 7.75 1.77 1.32 15.08 1.77
Mugil cephalus Tenualosa reevesii
11.94 12.60
Pangio kuhlii Astroconger myriaster Miichthys miiuy Percocypris pingi Anguilli formes Pampus chinensis Paralichthys olivaceus Pagrosomus major Anchoa lucida Sebastiscus marmoratus Zebrias zebra Setipinna taty Lepidotrigla micropterus Mean –
and dl-PCBs intake through different fish species range from 0.26 to 65.61 pg TEQ kg 1 bw month 1. The mean dietary intake of total PCDD/Fs and dl-PCBs was 10.39 pg TEQ kg 1 bw month 1, only accounting for 14.8% of the PTMI. Compared with other studies, the mean level of dietary intake in this study was lower than the value (18.5 pg TEQ kg 1 bw month 1) acquired in south China (Zhang et al. 2008). However, it should be noted that the highest monthly intake level (65.61 pg TEQ kg 1 bw month 1) from B. mackerel was much more than that from other species and was very close to the PMTI of 70 pg TEQ kg 1 bw month 1 accounting for 93.7% of PMTI. Although the possible maximum monthly intake of dioxin-like compounds from B. mackerel was based on the assumption that only this species was consumed, the present study suggested the potential health risk should be concerned seriously. Except B. mackerel, the dioxin-like compounds intakes from most consumed fish were far from the PTMI. However, as a country with rapid industrialization, health risk associated with various contaminants released from industries to environment would continue to increase in the future years in China. In some previous studies, increasing trend for dioxin-like compounds in environment and human in China were estimated (Zheng et al., 2008; Li et al., 2009). From China total dietary study, increasing trend on dietary intake of dioxin-like compounds was also found for most of residents in China between 2000 and 2007 (Zhang et al., 2013). Therefore, to protect health, we should select the fish species which accumulate less dioxin-like compounds. The present study provides essential information for the selection. Additionally, the monitoring of these contaminants in fish should be conducted continuously to assess the intake levels and to provide risk-based consumption advice in time. Acknowledgements This study was financially supported by the National Nature Science of Foundation of China (No. 81172675), the Special Foundation for Young Scientists of Department of Health of Hubei Province (QJX2010-33) and the Welfare Technology Applied Research Program of Zhejiang Province, China (2011C33001, 2012C23034). Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.chemosphere. 2014.07.057.
Monthly intake(pg WHO-TEQ/kg bw,/month)
8.14 –
References
Baars, A.J., Bakker, M.I., Baumann, R.A., Boon, P.E., Freijer, J.I., Hoogenboom, L.A.P., Hoogerbrugge, R., Klaveren van, J.D., Liem, A.K.D., Traag, W.A., Vries de, J., 2004. Dioxins, dioxin-like PCBs and non-dioxin-like PCBs in foodstuffs: occurrence and dietary intake in The Netherlands. Toxicol. Lett. 151, 51–61. Bergkvist, C., Öberg, M., Appelgren, M., Becker, W., Aune, M., Ankarberg, H.E., Berglund, M., Håkansson, H., 2008. Exposure to dioxin-like pollutants via different food commodities in Swedish children and young adults. Food Chem. Toxicol. 46, 3360–3367. Clapp, R., Ozonoff, D., 2000. Where the boys aren’t: dioxin and the sex ratio. Lancet 335, 1838–1839. Chinese Nutrition Society, 2007. The guide to Chinese diet. . Dannenberger, D., Andersson, R., Rappe, C., 1997. Levels and patterns of polychlorinated dibenzo-p-dioxins, dibenzofurans and biphenyls in surface sediments from the western Baltic Sea (Arkona Basin) and the Oder River estuarine system. Mar. Pollut. Bull. 34, 1016–1024. Fernandes, A., Mortimer, D., Rose, M., Gem, M., 2010. Dioxins (PCDD/Fs) and PCBs in offal: occurrence and dietary exposure. Chemosphere 81, 536–540. Grassi, P., Fattore, E., Generoso, C., Fanelli, R., Arvati, M., Zuccato, E., 2010. Polychlorobiphenyls (PCBs), polychlorinated dibenzo-p-dioxins (PCDDs) and dibenzofurans (PCDFs) in fruit and vegetables from an industrial area in northern Italy. Chemosphere 79, 292–298. Isosaari, P., Vartiainen, T., Hallikainen, A., Ruohonen, K., 2002. Feeding trial on rainbow trout: comparison of dry fish feed and Baltic herring as a source of PCDD/Fs and PCBs. Chemosphere 48, 795–804. Joint FAO/WHO Expert Committee on Food Additives (JECFA), 2002. Evaluation of Certain Food Additives and Contaminants 57th Report of the Joint FAO/WHO Expert Committee on Foods Additives. WHO Technical Report Series, No. 909. . Kim, B.H., Ikonomou, M.G., Lee, S.J., Kim, H.S., Chang, Y.S., 2005. Concentrations of polybrominated diphenylethers, polychlorinated dibenzo-p-dioxins and dibenzofurans, and polychlorinated biphenyls in human blood samples from Korea. Sci. Total Environ. 336, 45–56. Kim, M., Kim, S., Yun, S.J., Kim, D.G., Chung, G.S., 2007. Background levels and dietary intake of PCDD/Fs in domestic and imported meat in South Korea. Chemosphere 69, 479–484. Kiviranta, H., Ovaskainen, L.M., Vartiainen, T., 2004. Market basket study on dietary intake of PCDD/Fs, PCBs, and PBDEs in Finland. Environ. Int. 30, 923–932. Li, J.G., Wu, Y.N., Zhang, L., Zhao, Y.F., 2007. Dietary intake of polychlorinated dioxins, furans and dioxin-like polychlorinated biphenyls from foods of animal origin in China. Food Addit. Contam. 24, 186–193. Li, J.G., Zhang, L., Wu, Y.N., LiuY, P., Zhou, P.P., Wen, S., Liu, J.Y., Zhao, Y.F., Li, X.W., 2009. A national survey of polychlorinated dioxins, furans (PCDD/Fs) and dioxin-like polychlorinated biphenyls (dl-PCBs) in human milk in China. Chemosphere 75, 1236–1242. Liu, Y.P., Li, J.G., Zhao, Y.F., Wen, S., Huang, F.F., Wu, Y.N., 2011. Polybrominated diphenyl ethers (PBDEs) and indicator polychlorinated biphenyls (PCBs) in marine fish from four areas of China. Chemosphere 83, 168–174. Lorber, M., Patterson, D., Huwe, J., Kahn, H., 2009. Evaluation of background exposures of Americans to dioxin-like compounds in the 1990s and the 2000s. Chemosphere 77, 640–651. Moon, H.B., Ok, G., 2006. Dietary intake of PCDDs, PCDFs and dioxin-like PCBs, due to the consumption of various marine organisms from Korea. Chemosphere 62, 1142–1152.
X. Wang et al. / Chemosphere 118 (2015) 163–169 Oh, J.R., Ikonomou, M.G., Fernandez, M.P., Hong, S.H., 2003. PCB and PCDD/F totals, TEQs and congener patterns in Korean coastal marine environments, 1987, 1988, 1990, and 1996–1999. Arch. Environ. Contam. Toxicol. 44, 224– 236. Pandelova, M., Henkelmann, B., Roots, O., Simm, M., Jarv, L., Benfenati, E., Schramm, K.-W., 2008. Levels of PCDD/F and dioxin-like PCB in Baltic fish of different age and gender. Chemosphere 71, 369–378. Rawn, F.K.D., Forsyth, S.D., Ryan, J.J., Breakell, K., Verigin, V., Nicolidakis, H., Hayward, S., Laffey, P., Conacher, B.S.H., 2006. PCB, PCDD and PCDF residues in fin and non-fin fish products from the Canadian retail market 2002. Sci. Total Environ. 359, 101–110. Ruus, A., Ugland, K.I., Espeland, O., Skaare, J.U., 1999. Organochlorine contaminants in a local marine food chain from Jarfjord, Northern Norway. Mar. Environ. Res. 48, 131–146. Safe, S., 1990. Polychlorinated biphenyls (PCBs) dibenzo-p-dioxins (PCDDs) dibenzofurans (PCDFs) and related compounds: environmental and mechanistic considerations which support the development of toxic equivalency factors (TEFs). Crit. Rev. Toxicol. 21, 51–88. Sasamoto, T., Ushio, F., Kikutani, N., Saitoh, Y., Yamaki, Y., Hashimoto, T., Horii, S., Nakagawa, J., Ibe, A., 2006. Estimation of 1999–2004 dietary daily intake of PCDDs, PCDFs and dioxin-like PCBs by a total diet study in metropolitan Tokyo, Japan. Chemosphere 64, 634–641. Shen, H.T., Han, J.L., Tie, X.W., Xu, W., Ren, Y.P., Ye, C.S., 2009a. Polychlorinated dibenzo-p-dioxins/furans and polychlorinated biphenyls in human adipose tissue from Zhejiang province, China. Chemosphere 74, 384–388. Shen, H.T., Yu, C., Ying, Y., Zhao, Y.F., Wu, Y.N., Han, J.L., Xu, Q.Y., 2009b. Levels and congener profiles of PCDD/Fs, PCBs and PBDEs in seafood from China. Chemosphere 77, 1206–1211. Song, Y., Wu, N.X., Han, J.L., Shen, H.T., Tan, Y.F., Ding, G.Q., Xiang, J.X., Tao, H., Jin, S.L., 2011. Levels of PCDD/Fs and DL-PCBs in selected foods and estimated dietary intake for the local residents of Luqiao and Yuhang in Zhejiag, China. Chemosphere 85, 329–334.
169
Szlinder-Richert, J., Barska, I., Usydus, Z., Ruczynska, W., Grabic, R., 2009. Investigation of PCDD/Fs and dl-PCBs in fish from the southern Baltic Sea during the 2002–2006 period. Chemosphere 74, 1509–1515. The Codex Alimentarius Commission, 2012. Prevention and Reduction of Food and Feed Contamination, first ed. World Health Organization, Food and Agriculture Organization of the United nations, Rome. USEPA Method1613, 1994. Tetra- through octa-chlorinated dioxins and furans by isotope dilution HRGC/HRMS. Washington, D.C. USEPA Method1668A, 1999. Interlaboratory Validation Study Report. Washington, D.C. United States Environment Protection Agency (USEPA), 2010. Persistent Organic Pollutants: A Global Issue, A Global Response. van Leeuwen, F.X.R., Feeley, M., Schrenk, D., Larsen, C.J., Farland, W., Younes, M., 2000. Dioxins WHOs tolerable daily intake (TDI) revisited. Chemosphere 40, 1095–1101. Wang, I.C., Wu, Y.L., Lin, L.F., Chang-Chien, G.P., 2009. Human dietary exposure to polychlorinated dibenzo-p-dioxins and polychlorinated dibenzofurans in Taiwan. J. Hazard. Mater. 164, 621–626. Zhang, J.Q., Jiang, Y.S., Zhou, J., Fang, D.K., Jiang, J., Liu, G.H., Zhang, H.Y., Xie, J.B., Huang, W., Zhang, J.Z., Li, H., Wang, Z., Pan, L.B., 2008. Concentrations of PCDD/ PCDFs and PCBs in retail foods and an assessment of dietary intake for local population of Shenzhen in China. Environ. Int. 34, 799–803. Zhang, L., Li, J.G., Liu, X., Zhao, Y.F., Li, X.W., Wen, S., Wu, Y.N., 2013a. Dietary intake of PCDD/Fs and dioxin-like PCBs from the Chinese total diet study in 2007. Chemosphere 90, 1625–1630. Zhang, L., Li, J.G., Zhao, Y.F., Li, X.W., Wen, S., Shen, H.T., Wu, Y.N., 2013b. Polybrominated diphenyl ethers (PBDEs) and indicator polychlorinated biphenyls (PCBS) in foods from China: levels, dietary intake, and risk assessment. Agric. Food Chem. 61, 6544–6551. Zheng, J.G., Leung, O.W.A., Jiao, P.L., Wong, H.M., 2008. Polychlorinated dibenzo-pdioxins and dibenzofurans pollution in China: sources, environmental levels and potential human health impacts. Environ. Int. 34, 1050–1061.
