PCDFs and PCBs in fish and seafood from the Catalan (Spain) market: Estimated human intake

Environment International 33 (2007) 170 – 175 www.elsevier.com/locate/envint

Concentrations of PCDD/PCDFs and PCBs in fish and seafood from the Catalan (Spain) market: Estimated human intake Ana Bocio a , José L. Domingo a,⁎, Gemma Falcó b , Juan M. Llobet b a

Laboratory of Toxicology and Environmental Health, School of Medicine, “Rovira i Virgili” University, San Lorenzo 21, 43201 Reus, Spain b Toxicology Unit, School of Pharmacy, University of Barcelona, Avda. Juan XXIII s/n, 08028 Barcelona, Spain Received 28 July 2006; accepted 8 September 2006 Available online 16 October 2006

Abstract The concentrations of polychlorinated dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs) and biphenyls (PCBs) in samples from 14 fish and seafood species widely consumed by the population of Catalonia, Spain, were measured. These samples were randomly purchased independently of their geographical origin. The intake of PCDD/Fs and PCBs through consumption of these species was also estimated for various age and sex groups of this population. The highest and lowest levels of PCDD/Fs and dioxin-like PCBs (DL-PCBs) were found in red mullet and shrimp, respectively. For a standard adult man (70 kg body weight), the intake of PCDD/Fs plus DL-PCBs through consumption of fish and other seafood was estimated to be 38.0 pg WHO-TEQ/day. Tuna, hake, and sardine were the species with the highest contribution to this intake. The results of this study indicate that, in general terms, the dietary habits of the population of Catalonia (Spain) regarding fish and seafood consumption do not contribute remarkably to increase PCDD/F and DL-PCB intake. © 2006 Elsevier Ltd. All rights reserved. Keywords: Polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs); Polychlorinated biphenyls (PCBs); Fish and seafood; Estimated intake; Catalonia, Spain

1. Introduction Human exposure to polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs) and polychlorinated biphenyls (PCBs) occurs mainly from eating food that contains these chemicals (Schecter et al., 2001; Juan et al., 2002; Kiviranta et al., 2002, 2004; Erdogrul et al., 2005; Coelhan et al., 2006). It has been reported that meat, dairy products, and fish, makes up more than 90% of the intake of PCDD/Fs and PCBs for the general population (Schecter et al., 1997; Llobet et al., 2003a,b; Bocio and Domingo, 2005; Charnley and Doull, 2005; Huwe and Larsen, 2005). Recently, we measured the levels of a number of chemical contaminants in 11 groups of foodstuffs. Dietary intake of pollutants was also estimated for various age and sex groups of the population of Catalonia (Spain) (Domingo et al., 2003; Bocio et al., 2003, 2004; Falcó et al., 2003, 2004; Llobet et al., ⁎ Corresponding author. Tel.: +34 977 759380; fax: +34 977 759322. E-mail address: [email protected] (J.L. Domingo). 0160-4120/$ - see front matter © 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.envint.2006.09.005

2003a,b,c). PCDD/Fs and PCBs were included among these contaminants. The highest levels of most inorganic and organic pollutants were mainly detected in fish and other seafood. This group showed the highest contribution to the intake of As, Hg and Pb (Llobet et al., 2003c), PCDD/Fs (Llobet et al., 2003a), PCBs (Llobet et al., 2003b), polybrominated diphenyl ethers (Bocio et al., 2003) and polychlorinated diphenyl ethers (Bocio et al., 2004). However, due to technical and economical reasons, the number of total analyzed composite samples for the 11 groups of foodstuffs was 108. Moreover, the levels of the contaminants were only determined in three species of fresh fish and in two species of canned fish. There is no doubt that these are limiting factors for the purpose of establishing recommendations regarding fish consumption. Therefore, the main purpose of the present study was to obtain new data that should allow making more specific recommendations regarding human consumption (kind of species, and frequency and size of meals) of fish and other seafood. Daily intakes of PCDD/Fs and PCBs through fish and seafood consumption by various age/sex groups of the

A. Bocio et al. / Environment International 33 (2007) 170–175

population of Catalonia were also estimated. The results of the present study are discussed and compared to relevant recent literature concerning PCDD/F and PCB levels in fish species and human daily intake. The objectives of this study were: a) to determine the levels of PCDD/Fs and PCBs in a number of fish and seafood species purchased from the Catalan market, and b) to estimate the intake of PCDD/Fs and PCBs through consumption of fish and other seafood by the population of Catalonia. 2. Materials and methods 2.1. Sampling During the months of March and April 2005, fish and seafood species were acquired in local fish markets, big supermarkets and grocery stores from six main cities of Catalonia, Spain. The following species were represented: sardine, tuna, anchovy, mackerel, swordfish and salmon corresponding to blue fish; hake, red mullet and sole as white fish; cuttlefish and squid as cephalopods; and clam, mussel and shrimp corresponding to shellfish. Fish and seafood species were not necessarily caught from the Catalonian coastal waters. They were randomly purchased independently on their geographical origins. According to recent studies, all these species are included into the most consumed by the population of Catalonia (Serra-Majem et al., 2003; MAPA, 2004). The levels of PCDD/Fs and PCBs were determined in a total of 42 composite samples (3 samples for each species). Each composite sample was made up of 20 samples of the respective species. For small species (i.e., sardine, anchovy, clam, etc.), the entire edible part of each individual was included to prepare the composite sample. However, for bigger species (i.e., hake, swordfish, or tuna) only fillets of edible parts of each individual were collected and included in the respective composite samples. For all species, only edible parts were included in the composites.

2.2. Analytical procedures The 17 most toxic congeners of PCDD/Fs were analyzed. The seven PCB markers (IUPAC No. 28, 52, 101, 118, 138, 153 and 180), the coplanar PCB congeners No. 77, 126 and 169, and the mono-ortho PCB congener No. 105 were also determined. The choice of these PCB congeners was based on our previous PCB survey (Llobet et al., 2003b). Among them, PCB 126 and 169, that possess the highest toxic equivalency factors (TEFs) for PCBs, are included. PCDD/Fs and PCBs were determined by HRGC/HRMS according to

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the US EPA 1613 and 8290 methods, and the US EPA method 1625, respectively. Analytical procedures used in this study are described in detail previously (Llobet et al., 2003a,b). Toxic equivalents (TEQ) of the analyzed PCDD/Fs and dioxin-like PCBs (DL-PCBs) were calculated using the WHOTEF values.

2.3. PCDD/F and DL-PCB intake Average daily consumption data by the general population of Catalonia of the analyzed fish and seafood species were obtained from Serra-Majem et al. (2003). The population was divided into four age groups: children (4–9 years), adolescents (10–19 years), adults (20–65 years), and seniors (N65 years). These were in turn subdivided according to sex. For estimating the daily intake of PCDD/Fs and PCBs from each fish and seafood species, when the concentrations of a PCDD/F or PCB congener were lower than the corresponding detection limit, that value was assumed to be one-half of the respective limit of detection (LOD).

3. Results 3.1. PCDD/F and PCB concentrations Table 1 summarizes the concentrations of PCDD/Fs and PCBs in the fish and seafood species analyzed in this study. The highest levels for both PCDD/Fs and PCBs were found in red mullet, followed by salmon and mackerel for PCDD/Fs, and by sardine and anchovy for PCBs. In contrast, the lowest PCDD/F and PCB concentrations were detected in cuttlefish and shrimp, respectively. The highest total TEQ values corresponded to red mullet followed by anchovy and sardine, while the lowest values were found in cuttlefish, and shrimp and clam. The profiles of the 17 PCDD/F congeners and the 11 PCB congeners analyzed in marine species are depicted in Figs. 1 and 2, respectively. They are shown according to three groups: blue fish, white fish, and cephalopods and shellfish. It can be seen that, in general terms, blue fish showed higher concentrations of PCDD/Fs and PCBs than white fish, and cephalopods and shellfish. TCDF was the predominant congener for both blue and white fish, while in cephalopods and shellfish this role corresponded to OCDD. With respect to PCB congeners, the highest concentration in blue fish, and cephalopods and shellfish, corresponded to PCB 153, while in white fish the most

Table 1 PCDD/F concentrations in fish and other seafood samples Sardine

Tuna

Anchovy

Mackerel

Swordfish

Salmon

Hake

Red mullet

Sole

Cuttlefish

Squid

Clam

Mussel

Shrimp

pg/g of wet weight PCDD PCDF PCDD/PCDF

0.53 2.36 2.89

1.14 4.36 5.44

0.59 3.69 4.28

0.66 6.66 7.31

0.20 1.65 1.85

0.45 6.88 7.33

0.27 0.98 1.25

0.75 9.54 10.28

0.40 2.12 2.52

0.22 0.42 0.64

0.53 3.09 3.62

0.48 1.15 1.63

2.15 3.56 5.70

0.70 0.73 1.42

24.33

14.64

20.87

14.67

13.27

12.16

7.79

88.10

5.66

0.93

9.92

1.22

4.31

0.46

0.09 0.11 0.19 0.19 1.24 1.43

0.06 0.17 0.23 0.23 0.89 1.12

0.03 0.03 0.06 0.05 0.42 0.48

0.08 0.16 0.24 0.24 0.87 1.11

0.02 0.02 0.04 0.01 0.34 0.38

0.25 0.25 0.50 0.50 4.15 4.65

0.05 0.07 0.13 0.11 0.24 0.37

0.02 0.01 0.03 0.001 0.02 0.05

0.04 0.05 0.10 0.09 0.61 0.71

0.02 0.02 0.04 0.02 0.05 0.09

0.05 0.08 0.14 0.13 0.24 0.38

0.02 0.04 0.06 0.03 0.03 0.09

ng/g of wet weight PCB

pg WHO-TEQ/g of wet weight PCDD PCDF PCDD/PCDF PCDD/PCDF⁎ PCB Total TEQ

0.10 0.12 0.22 0.22 1.19 1.41

0.06 0.13 0.19 0.18 1.17 1.36

TEQ values include PCBs No. 77, 105, 118, 126 and 169. ⁎Lowerbound values (ND = 0) and middlebound (ND = ½ LOD) values in the remaining rows concerning TEQ data.

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Fig. 2. PCB congener concentration in fish and seafood samples.

Fig. 1. PCDD/F congener concentrations in fish and seafood samples.

When the intake of PCDD/Fs plus DL-PCBs was expressed in absolute values, the highest value corresponded to adult men (Fig. 3). On average, for a standard adult man (70 kg body weight) living in Catalonia, daily intake of PCDD/Fs and DL-PCBs through fish and seafood consumption was estimated to be 6.02 pg WHO-TEQ for PCDD/Fs, 31.98 pg WHO-TEQ for DL-PCBs, and 38.0 pg WHO-TEQ for the sum of both PCDD/Fs and DL-PCBs (Table 3). Tuna, followed

important contributor to total PCB concentration was PCB 138. PCB 169, followed by PCBs 126 and 77, were the congeners with the lowest concentrations in the three groups of analyzed species. 3.2. Estimated intake of PCDD/Fs and DL-PCBs through consumption of fish and seafood The estimated intakes (pg WHO-TEQ/day) of PCDD/Fs and DLPCBs through fish and other seafood consumption in eight age and sex groups of the population of Catalonia are depicted in Fig. 3. Adult men, followed by adult women and senior men had the highest PCDD/F plus DL-PCB intake: 36.5, 33.3 and 33.1 pg WHO-TEQ/day, respectively. In contrast, the lowest daily intakes corresponded to children: 20.4 and 16.2 pg WHO-TEQ for boys and girls, respectively. However, when the daily intakes of PCDD/Fs plus DL-PCBs were estimated according to the respective average body weight for each age/sex group, children (0.85 and 0.71 pg WHO-TEQ/kg body weight/day for boys and girls, respectively) showed the highest values, whereas seniors (males and females) had the lowest intakes of PCDD/Fs plus DL-PCBs (Table 2).

Fig. 3. Estimated intake of PCDD/Fs and PCBs (pg WHO-TEQ/day) through consumption of fish and seafood by adults, children, adolescents and seniors of Catalonia, Spain.

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Table 2 Daily intake of PCDD/Fs and DL-PCBs (dioxin-like PCBs) through fish and seafood consumption by eight age and sex population groups in Catalonia, Spain Intake (pg WHO-TEQ/kg/day) Group

PCDD/Fs

DL-PCBs

PCDD/Fs + DL-PCBs

Adult men Adult women Boys Girls Adolescents (males) Adolescents (females) Seniors (males) Seniors (females)

0.09 0.11 0.13 0.13 0.09 0.08 0.08 0.08

0.44 0.50 0.72 0.58 0.38 0.46 0.44 0.37

0.53 0.61 0.85 0.71 0.47 0.54 0.52 0.45

by hake and sardine, were the main contributors to total TEQ intake. Considering only DL-PCB intake, a similar sequence could be observed. Taken individually, PCDD/Fs showed a different profile in the contribution of marine species to total TEQ intake. Tuna was also the fish showing the highest contribution, followed by sardine and sole. Although red mullet was the species showing the most important concentrations of PCDD/Fs and PCBs (Table 1), this white fish was not a relevant contributor to total TEQ intake (Table 3). The contribution of fish and other seafood to the intake of PCDD/Fs and DL-PCBs (pg WHO-TEQ/day) is depicted in Fig. 4 according to three different groups of fish and seafood species. The highest contribution to the daily intake of these pollutants corresponded to blue fish, 67% of total TEQ, followed by white fish (25%).

4. Discussion The current mean PCDD/F concentration in edible marine species showed a significant decrease in comparison to that found in our previous PCDD/F survey (0.15 vs. 0.31 pg WHOTEQ/g of ww) (Llobet et al., 2003a). However, an increase was noted in the mean PCB level (15.6 ng/g in the present survey vs. 11.9 ng/g in the previous PCB study) (Llobet et al., 2003b). When only the 3 marine species (sardine, hake and mussel) analyzed in both surveys were considered, a reduction could be

Table 3 Estimated intake of PCDD/PCDFs and DL-PCBs (pg WHO-TEQ/day) through fish and seafood consumption by a standard adult man (70 kg body weight) living in Catalonia Consumption (g/day)

PCDD/PCDFs DL-PCBs PCDD/PCDF/DL-PCB

Sardine Tuna Anchovy Mackerel Swordfish Salmon Hake Red mullet Sole Cuttlefish Squid Clam Mussel Shrimp Total

0.83 1.90 0.39 0.26 0.004 0.43 0.58 0.16 0.69 0.13 0.30 0.01 0.13 0.20 6.02

3.78 10.1 2.05 1.13 0.06 1.80 15.8 0.33 5.48 4.46 3.17 0.27 0.97 3.53 52.94

4.50 11.9 2.54 1.00 0.03 1.56 5.41 1.37 1.31 0.08 1.93 0.01 0.24 0.12 31.98

5.33 13.8 2.93 1.26 0.03 1.99 5.99 1.53 2.00 0.21 2.23 0.02 0.37 0.32 38.0

Fig. 4. Contribution of different kinds of fish and other seafood species to total TEQ intake of PCDD/Fs and DL-PCBs.

observed among samples collected in 2000 and 2005: 0.11 vs. 0.04 pg WHO-TEQ/g of ww in sardine, 0.66 vs. 0.22 pg WHOTEQ/g of ww in hake, and 0.30 vs. 0.14 pg WHO-TEQ/g of ww in mussel. However, for PCBs only sardine showed lower levels in 2005 than those observed in 2000. Recently, the EU established maximum permissible levels for human consumption of 4 and 8 ng/kg of ww of toxic equivalents (WHO-TEQ), for PCDD/Fs and for PCDD/Fs plus dioxin-like compounds, respectively, in the muscle meat of fish and fishery products (EC, 2006). All fish and seafood species analyzed in the current survey showed PCDD/F plus DL-PCB concentrations under the EU maximum permissible level. Similar results were also recently reported by Bordajandi et al. (2004) in fish and other seafood samples from Huelva (SW Spain). By contrast, and only taken as an example, in a recent survey performed with fish samples collected in the Baltic Sea, the EU limit was exceeded by salmon and herring (Isosaari et al., 2006). It is well known that fish and other seafood from the Baltic Sea show habitually higher concentrations of environmental pollutants than species collected in other less contaminated places. In relation to the pattern of PCDD/Fs, Ruus et al. (2006) found that concentrations of PCDD/F declined with increasing trophic level. Principal Component Analysis (PCA) also showed differences between species in the pattern of PCDD/ Fs. Results indicated lower accumulation of higher chlorinated congeners in species at higher trophic levels (fish). A similar trend could be also observed in the present survey (Fig. 1). In cephalopods and shellfish, OCDD and OCDF showed higher contributions to total PCDD/Fs than the lowest substituted congeners, while in fish, the most important contributor was TCDF. In fish samples from Korea, Moon and Ok (2006) found that 2,3,4,7,8-PeCDD was the most important contributor to total TEQ concentration in all analyzed species. However, in a study carried out in Canada in 2002, Rawn et al. (2006) found that 1,2,3,7,8-PeCDD and TCDF were the major contributors to PCDD and PCDF concentrations, respectively. In relation to current PCB concentrations, and similar to the findings of Rawn et al. (2006), PCBs 138 and 153 were also the dominant congeners observed in fish and other seafood. In our previous studies (Llobet et al., 2003a,b), in which 11 food groups were included, a dietary intake of 95.4 pg WHOTEQ/day was estimated (for an adult man of 70 kg body weight)

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for PCDD/Fs, or 245.5 pg WHO-TEQ/day when DL-PCBs were also included. Fish and other seafood contributed with 30.1% to TEQ intake of PCDD/Fs, while for DL-PCBs the contribution of marine species to TEQ intake reached a higher percentage, approximately 55%. In another recent study performed in our laboratory, dietary PCDD/F intake was assessed for the general population of Tarragona (southern Catalonia) (Bocio and Domingo, 2005). The contribution of fish and other seafood was estimated to be 34% of total TEQ intake (21.7 of the total 63.8 pg WHO-TEQ/day). In the current survey, intake of PCDD/Fs and DL-PCBs through edible fish species was estimated to be 38.0 pg WHO-TEQ/day (6.0 and 32.0 pg WHOTEQ/day for PCDD/Fs and DL-PCBs, respectively). In both cases, DL-PCBs were the most important contributors to total TEQ (60% and 84%, respectively). A notable reduction between the 2000 studies (Llobet et al., 2003a,b) and the current survey has been found. However, it is important to note that fish consumption has decreased from the previous study to the current one (92 g/day vs. 53 g/day). Moreover, in our previous survey only 3 fresh and 2 canned marine species were analyzed in comparison to the current 14 species. Probably, these circumstances together with the notable decreases in the atmospheric PCDD/F and PCB levels observed in recent years in most industrialized countries would explain the differences between the results of both studies. However, recently Charnley and Doull (2005) reported an absence of a downward trend in estimated human exposure to dioxin intake in USA between 1999 and 2002. These authors suggested that PCDD/F levels in foodstuffs might now be most highly impacted by reservoir sources or unusual occurrences rather than the low level of ongoing emissions from controlled sources, which would be now small compared to uncontrolled natural and anthropogenic sources. Notwithstanding, this has not been the case of the current survey. The comparison of the results of the present study with data from other surveys is rather complicated, as the levels of pollutants depend mainly on the concentrations of these contaminants in the marine waters where fish and other seafood are caught. A specific difficulty for comparison of PCB levels is the great variety (specific congener and number of congeners) of congeners that are analyzed. Other differences concern the expression of the results: wet weight, dry weight or lipid weight. Finally, some investigators report results concerning only some parts of the fish samples: muscle, liver, skin, etc., which makes still more complicated a comparison of the data (Domingo and Bocio, submitted for publication). The current PCDD/Fs plus DL-PCBs intake through consumption of fish and other seafood by a standard adult male (the age/sex group showing the highest intake in absolute values) of 70 kg body weight was between 13.6% and 54.2% of the tolerable daily intake (TDI) for these compounds, which has been established by the WHO in 1–4 pg WHO-TEQ/kg body weight/ day for non-carcinogenic effects. Although no remarkable differences were found among age and sex groups of the Catalonian population, children showed a lower intake of PCDD/Fs and DLPCBs (Fig. 3), which was due to a lower consumption of fish and other seafood. When TEQ intake was expressed in relation to the

average body weight of each group, the highest exposure to these pollutants corresponded to children (Table 2). However, because TDI is based on a lifetime exposure (Charnley and Doull, 2005), a higher risk would not be expected for this specific group of population. For carcinogenic effects, the risk is expressed as the probability of contracting cancer over a lifetime. In the present investigation, a value of 1 × 10− 3 pg I-TEQ/kg/day was used as an estimator of upper bound cancer risk. In an adult population of 1 million, the risk level due to PCDD/F and DL-PCB exposure through the intake of fish and other seafood would be a 540 excess cancer over a lifetime of 70 years. Notwithstanding, it must be noted that the carcinogenic potency used is referred to ITEQ (Larsen et al., 2000). The health benefits, primarily in terms of prevention of sudden cardiac death of eating fish have been widely documented (Kris-Etherton et al., 2002). However, various edible fish and seafood species have shown to accumulate a variety of toxic pollutants, some of which may counteract the beneficial effects of the omega-3 fatty acids present in fish and other seafood by increasing the risk of other diseases (Hites et al., 2004a,b). Among these pollutants PCDD/Fs and DL-PCBs have been associated with numerous adverse health effects. For many individuals, fish and other seafood are the main contributors to total TEQ intake from PCDD/Fs and DL-PCBs. In general terms, the results of the present study indicate that the dietary habits of the population of Catalonia (Spain) regarding fish and seafood do not contribute remarkably to PCDD/F and DL-PCB intake. However, those individuals in some groups of population, which frequently consume high quantities of certain species (i.e., red mullet), could significantly increase their PCDD/F and/or DL-PCB intakes. Moreover, WHO and EU intake recommendations include only PCDD/Fs and dioxin-like compounds, while other organohalogenated substances such as PCNs or PCDEs, whose environmental persistency, bioaccumulation and toxicological effects could be potentially similar to those of PCDD/Fs, are not usually monitored and their health risks assessed (Domingo, 2004, 2006). This is an important gap that should be taken into consideration. As a final conclusion, we suggest that recommendations about consumption of fish and other seafood are done according to the data concerning levels of environmental pollutants in the most consumed fish and seafood species in each specific region or country. Acknowledgements This study was supported by the Catalan Food Safety Agency, Generalitat de Catalunya, Spain. We are grateful to Dr. L. Serra-Majem and co-workers for providing recent data about fish and seafood consumption by the general population of Catalonia. References Bocio A, Domingo JL. Daily intake of polychlorinated dibenzo-p-dioxins/ polychlorinated dibenzofurans (PCDD/PCDFs) in foodstuffs consumed in Tarragona, Spain: a review of recent studies (2001–2003) on human PCDD/ PCDF exposure through the diet. Environ Res 2005;97:1–9.

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