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PCDFs and PCBs in edible marine species and human intake: A literature review
Environment International 33 (2007) 397 – 405 www.elsevier.com/locate/envint
Review article
Levels of PCDD/PCDFs and PCBs in edible marine species and human intake: A literature review José L. Domingo ⁎, Ana Bocio Laboratory of Toxicology and Environmental Health, School of Medicine, “Rovira i Virgili” University, San Lorenzo 21, 43201 Reus, Spain Received 8 August 2006; accepted 18 December 2006 Available online 30 January 2007
Abstract Polychlorinated dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs) and biphenyls (PCBs) are lipophilic organic compounds whose origin comes from many different sources. PCDD/Fs and PCBs are ubiquitous and persistent environmental pollutants with a well known potential toxicity, which were included at the 1998 UN-EC POP protocol. Although human exposure to PCDD/Fs and PCBs can occur by various routes, food is the primary source. A number of studies have shown that the major food sources of these organic pollutants are fat-containing animal products, including fish and other seafood. Because of the frequent health recommendations concerning fish consumption, to determine the contribution to the dietary intake of chemical contaminants such as PCDD/Fs and PCBs through fish and other seafood consumption is an issue of special interest. This paper reviews the state of the science regarding recent literature on PCDD/F and PCB levels in marine species and human intake through fish and seafood consumption. The concentrations of these pollutants depend basically on the environment in which the respective species are caught. It is concluded that some groups of population frequently consuming high quantities of certain species could be significantly increasing health risks due to PCDD/F and PCB exposure. © 2007 Elsevier Ltd. All rights reserved. Keywords: Polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs); Polychlorinated biphenyls (PCBs); Fish and other seafood; Human intake; Recent reports
Contents 1. Introduction . . . . . . . 2. European studies . . . . 3. North American studies. 4. Asian studies . . . . . . 5. African studies . . . . . 6. Conclusions. . . . . . . Acknowledgment. . . . . . . References . . . . . . . . . .
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1. Introduction Polychlorinated dibenzo-p-dioxins (PCDDs) and dibenzofurans (PCDFs), and polychlorinated biphenyls (PCBs) are ⁎ Corresponding author. Tel.: +34 977 759380; fax: +34 977 759322. E-mail address: [email protected] (J.L. Domingo). 0160-4120/$ - see front matter © 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.envint.2006.12.004
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ubiquitous environmental contaminants, which persist and bioaccumulate through the food chain. Human exposure to these pollutants occurs mainly from eating foodstuffs that contain these chemicals (Schecter et al., 2001; Juan et al., 2002; Kiviranta et al., 2004; Bocio and Domingo, 2005). It has been reported that the contribution of meat and meat products, dairy products, and fish and other seafood may surpass the 90% of the
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total exposure to PCDD/Fs and PCBs (Schecter et al., 1997; Llobet et al., 2003a,b; Bocio and Domingo, 2005; Charnley and Doull, 2005; Huwe and Larsen, 2005). Recently, we determined the concentrations of PCDD/Fs and PCBs in a number of foodstuffs purchased from various cities of Catalonia (Spain). The dietary intake of these compounds by the population of Catalonia was also estimated (Llobet et al., 2003a,b). The most important contribution to the dietary intake of PCDD/Fs and PCBs corresponded to fish and other seafood: 31% for PCDD/Fs and 55% for PCBs. These results corroborate 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. The nutritional benefits of fish consumption are well known: an important content of high-quality proteins, vitamins and other essential nutrients, low levels of saturated fats, as well as high amounts of omega3 polyunsaturated fatty acids, which seem to have protective effects in preventing coronary heart disease among other health benefits (Kris-Etherton et al., 2002; Engler and Engler, 2006). In recent years, the number of studies focused on determining the levels of PCDD/Fs, PCBs and other persistent organic pollutants (POPs) in foodstuffs has been notable. This paper presents an overview on the current available scientific information concerning concentrations of PCDD/Fs and PCBs in edible marine species, and the intake of PCDD/Fs and PCBs through consumption of these species. It can be of special interest to those particularly interested in the balance between potential benefits and risks of fish consumption. The reports here reviewed have been discussed according to their respective geographical origins, being divided into European, North American, Asian and African surveys. Only studies published after 2001 have been reviewed. It is important to note that data are reported just as the respective PCDD/F and PCB concentrations were expressed in the corresponding studies: ITEQ, WHO-TEQ and CALUX-TEQ. An important issue that makes difficult, in certain cases, the comparison of the results of the studies here reviewed is how, for TEQ calculations, the different authors considered the non-detected (ND) values of PCDD/F or PCB congeners. We found that depending on the specific study, non-detected concentrations were assumed to be equal to the limit of detection (ND = LOD), equal to zero (ND = 0), or equal to one-half of the respective limit of detection (ND = 1/2 LOD). 2. European studies A summary of the European studies reviewed in this paper is shown in Table 1. Edible marine species (anchovy, squid, mussel, lobster, mackerel, red mullet and clam) from several areas of the Adriatic sea were analyzed for their content in PCDD/Fs and PCBs. In general, I-TEQs were greater for those species at higher levels in the trophic web (mackerel N red mullet N anchovy). The levels of PCDD/Fs and PCBs were between 0.23 and 1.07 pg I-TEQ/g of wet weight (ww) in these species, and within 0.07–0.25 for the remaining species. The
greatest PCB concentrations were found in mackerel (94– 177 ng/g ww) (Bayarri et al., 2001). Marcotrigiano and Storelli (2003) determined the levels of 17 PCB congeners in a considerable number of marine organisms caught in the Adriatic and Ionian seas. Mean values in fish muscles, cephalopods (flesh), bivalves and crustacean (flesh) were: 4.54, 0.33, 4.31 and 4.69 ng/g ww, respectively. No information concerning human exposure to PCBs was reported. Binelli and Provini (2003) measured the concentrations of PCBs in 16 pools of edible clams purchased from different Italian and European markets. The mean PCB concentration was 4.8 (range between 1.6 and 15.4) ng/g of ww. Perugini et al. (2004) analyzed the concentrations of 7 PCB congeners in mussel, lobster, red mullet, cuttlefish, squid, anchovy, sardine and mackerel from two sites of the Italian coast of the Adriatic Sea. The maximum ∑PCB (mean values for the two sites, ng/g ww) corresponded to mackerel (20.8), followed by red mullet (18.0) and anchovy (17.5), while the lowest ∑PCB (mean values for the two sites, ng/g ww) were detected in cuttlefish (0.73) and squid (2.4). In contrast to the results concerning red mullet, Licata et al. (2003) did not find residues of PCBs (Aroclor 1232 series) in tissues of the mullet Liza aurata from the Straits of Messina (Sicily, Italy). Recently, Naso and co-workers (2005) measured the levels of 20 PCBs in edible tissues from 10 marine species collected from the Gulf of Naples (Italy). The sum of all determined PCB congeners ranged between 407 and 22287 ng/g of lipid weight (lw), for octopus and bass, respectively. In another recent Italian study, Taioli et al. (2005) measured the content of PCDD/Fs in 269 samples of food of animal origin, including fish (eel, herring, mullet, mackerel, bass and trout). The highest and lowest mean PCDD/F values corresponded to eel and trout: 1.11 and 0.18 pg WHO-TEQ/g, respectively. Mean PCDD/F concentration in mackerel was also relatively low, 0.22 pg WHO-TEQ/g. According to these results, the estimated daily intake (median value) of PCDD/Fs through fish consumption was 2.34–2.38 pg WHO-TEQ/kg body weight. Karl et al. (2002) analyzed the contents of PCDD/Fs of 184 pooled samples of 20 marine fish and fishery products (canned fish) from the German market (1995–1998). The highest dioxin content in the edible parts was found in herring of the Baltic Sea and halibut of the North Sea: 1.91 and 1.49 ng/kg ww, respectively. The lowest PCDD/F levels were found in hake and Alaska pollack (0.005–0.006 and 0.007 ng/kg ww, respectively). Based on a daily fish consumption of 20 g, the average daily intake of PCDD/Fs via fish was 6.2 pg WHO-TEQ per person. Knutzen et al. (2003) determined the levels of PCDD/Fs and PCBs in marine organisms from the Grenland fjords, in Norway. Composite samples of Atlantic cod, sea trout, flounder, eel, edible crab and blue mussel were analyzed. In edible fillets, or muscle of mollusks, WHO-TEQ for PCDD/Fs ranged between 0.85 (cod) and 28.0 ng/kg ww (flounder). The highest value was found in cod liver (587 ng WHO-TEQ/kg ww). When dioxin-like PCBs (congeners 77, 105, 118, 126, 156 and 169) were also included, the highest and lowest WHO-TEQ values corresponded to flounder (33.5 ng/kg ww) and mussels (1.6 ng/ kg ww). In Baltic Sea fish (salmon, cod, flounder and herring) from the Polish coast, the highest and lowest PCDD/F
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Table 1 A summary of recent literature data concerning levels of PCDD/Fs and PCBs in edible marine species and human dietary intake Sampling site
Species analyzed
Adriatic Sea
Anchovy, squid, mussel, lobster, PCDD/Fs and PCBs: 0.23–1.07 pg mackerel, red mullet, clam I-TEQ/g ww for mackerel, red mullet and anchovy; 0.07–0.25 pg I-TEQ/g ww for the remaining species A number of fish, cephalopods, PCBs (17 congeners); mean values: bivalves and crustacean species 4.54, 0.33, 4.31 and 4.69 ng/g ww, respectively for the indicated groups Edible clams (pools) PCBs; mean value: 4.8 (1.6–15.4) ng/g ww
Adriatic and Ionan Seas
Various European markets Italian coast of the Mussel, lobster, red mullet, Adriatic Sea cuttlefish, squid, anchovy, sardine, mackerel Gulf of Naples, 10 marine species Italy
Levels of PCDD/Fs and/or PCBs
PCBs (7 congeners); highest value: 20.8 ng/g ww (mackerel); lowest value: 0.73 ng/g ww (cuttlefish) PCBs (20 congeners); range between 407 (octopus) and 22287 (bass) ng/g l w PCDD/Fs; highest and lowest mean values: 1.11 and 0.18 pg WHO-TEQ/g for eel and trout, respectively PCDD/Fs; highest and lowest levels: 1.91 and 0.006 ng/kg ww for herring and hake, respectively
Italy
Eel, herring, mullet, mackerel, bass, trout
Germany
Marine fish and fishery products (canned fish) from the German market
Grenland fjords, Norway
Atlantic cod, sea trout, flounder, PCDD/Fs; levels from 0.85 (cod) to eel, edible crab, blue mussel 28.0 ng/kg ww (flounder). When PCBs (6 congeners) were also included, the highest and lowest WHO-TEQ values corresponded to flounder and mussels, respectively Salmon, cod, flounder, herring PCDD/Fs; from 1.6 (cod) to 3.2 pg WHO-TEQ/g ww (salmon)
Polish coast of Baltic Sea Finland
The Netherlands
10 market baskets; salmon, rainbow trout, tuna, saithe, Baltic herring and vendace Various fish species among selected food products
Belgium
Fishery products from the Belgian market
Five areas of the Baltic Sea
Fish composite samples
Greece
Fish samples from the Greek market
Basque Country, Spain
Total Diet Study (including fish)
Huelva, SW Spain
Fish and seafood from the Huelva market
Spain
Fish and seafood from Spanish markets
Comments and remarks
References
No information on human exposure
Bayarri et al. (2001)
No information on human exposure
Marcotrigiano and Storelli (2003)
No information on human exposure No information on human exposure
Binelli and Provini (2003) Perugini et al. (2004)
No information on human exposure
Naso et al. (2005)
Estimated daily intake of PCDD/Fs through fish consumption: 2.34–2.38 pg WHO-TEQ Based on a fish consumption of 20 g/day, the average intake of PCDD/Fs via fish was 6.2 pg WHO-TEQ/day No information on human exposure
Taioli et al. (2005)
No information on human exposure
PiskorskaPliszczynska et al. (2004) Kiviranta et al. (2004)
Karl et al. (2002)
Knutzen et al. (2003)
PCDD/Fs; sum: 2.0 pg WHO-TEQ/g Average intakes of PCDD/Fs ww PCBs; sum: 1.5 pg WHO-TEQ/g ww and PCBs: 54 and 41 pg WHO-TEQ/day, respectively Contribution of PCDD/Fs plus dioxin-like PCBs through fish consumption: 16% Dioxin-like compounds; 0.12 No information on (shrimp)–2.53 (herring) human exposure pg CALUX-TEQ/g ww PCDD/Fs; levels from 0.13 (burbot) EU maximum permissible to 17.4 (salmon) pg WHO-TEQ ww levels was exceeded in salmon PCBs; levels from 0.08 (burbot) and Baltic herring to 15.6 (salmon) pg WHO-TEQ ww PCDD/Fs; sums ranging between 0.12 No information on (wild fish) and 0.47 (aquaculture fish) human exposure pg TEQ/g fat Non-ortho PCBs; average sums: from 0.33 to 1.19 pg TEQ/fat for wild and aquaculture fish, respectively Intakes of PCDD/Fs, non-ortho PCBs and ortho-PCBs from fish were 11.6, 52.5 and 17.8 pg WHO-TEQ/day, respectively Total daily intake of PCDD/Fs plus PCDD/Fs plus PCBs; range levels from 0.24 (cuttlefish) PCBs from fish: 0.11 (PCDD/Fs) and 0.18 (PCBs) pg WHO-TEQ(kg to 1.00 (tuna, mackerel and body weight for a 70 kg person sardine) pg WHO-TEQ/g ww PCDD/Fs and PCBs; highest Daily intakes of PCDD/Fs and PCBs from fish and seafood for a 70 kg levels in oysters and clams for person: 0.15 and 0.35 pg WHO-TEQ/kg PCDD/Fs, and white sea bream for PCBs. Lowest levels in prawns, body weight for PCDD/Fs and cuttlefish and sole for dioxin-like PCBs, respectively PCDD/Fs and PCBs
Baars et al. (2004)
Schoeters et al. (2004) Isosaari et al. (2006)
Papadopoulos et al. (2004)
Cuervo et al. (2002)
Bordajandi et al. (2004)
Fernandez et al. (2004)
(continued on next page)
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Table 1 (continued ) Sampling site
Species analyzed
Levels of PCDD/Fs and/or PCBs
Comments and remarks
References
Huelva coast, SW Spain
5 fish species and 4 seafood species
No information on human exposure
Bordajandi et al. (2006)
Catalonia, Spain
Hake, sardine and mussel from Catalan markets
PCDD/F levels; range from 0.2 (angler fish) to 1.8 (shellfish) pg/g ww PCB levels; range from 861 (prawns) to 23787 (sardine) pg/g ww PCDD/Fs; 0.11 (hake), 0.66 (sardine), 0.30 (mussel) pg WHO-TEQ/g ww PCBs; 0.25 (hake), 2.45 (sardine), 0.35 (mussel) pg WHO-TEQ/g ww PCDD/Fs; mean levels (pg/g fat): fish, 3.7; other seafood, 11.6
Contribution to total dietary intake of PCDD/Fs and PCBs: 31% and 55%, respectively
Llobet et al. (2003a,b)
Contribution of fish and seafood to total dietary intake of PCDD/Fs for a 70 kg person: 21.5 pg WHO-TEQ/day PCDD/Fs plus dioxin-like PCBs intake for a 70 kg subject: 38.0 pg WHO-TEQ/day
Bocio and Domingo (2005)
No information on human exposure
Coelhan et al. (2006)
Tarragona, Hake, whiting blue, bass, Catalonia, Spain angler fish, mussel, prawn, sardine, tuna and salmon from Tarragona markets Catalonia, Spain Sardine, tuna, anchovy, mackerel, swordfish, salmon, hake, red mullet, sole, cuttlefish, squid, clam, mussel, shrimp Marmara Sea, 12 edible fish species taken Turkey from the Central Fish Market of Istanbul
PCDD/Fs and PCBs; highest levels found in red mullet (PCDD/Fs and PCBs); lowest levels found in cuttlefish (PCDD/Fs) and shrimp (PCBs) PCBs; average value: 253.08 ng/g fat (range: 63.30–508.71 ng/g fat)
Bocio et al. (2007)
European studies (2001–2006).
concentrations were found in salmon, 3.2 (2.0–4.8) pg WHOTEQ/g ww, followed by herring 1.7 (1.1–2.8) and cod 1.6 (0.8– 2.4) pg WHO-TEQ/g ww, respectively (Piskorska-Pliszczynska et al., 2004). In a market study on the dietary intake of PCDD/Fs and PCBs performed in Finland, Kiviranta et al. (2004) measured the concentrations of these pollutants in 10 market baskets. Fish samples included salmon, rainbow trout, tuna, saithe, Baltic herring and vendace. The sum of PCDD/Fs was 2.0 pg WHOTEQ/g ww, and that of PCBs 1.5 pg WHO-TEQ/g ww. The average intakes of PCDD/Fs and PCBs were 54 and 41 pg WHO-TEQ/day, meaning percentages of 95% and 80% of the total dietary intake of PCDD/Fs and PCBs, respectively. In the Netherlands, Baars et al. (2004) collected (March 1999) a number of selected food products to determine occurrence and dietary intake of PCDD/Fs and PCBs. The contribution of fish to the total intake of PCDD/Fs plus dioxin-like PCBs was 16%, while for non-dioxin-like PCBs it was 26%. In Belgium, Schoeters et al. (2004) analyzed a limited number of different foods for dioxin-like compounds by the CALUX bioassay. Among them, 34 fishery products were purchased from the Belgian market. Median values (expressed as pg CALUX-TEQ/ g ww) oscillated between 0.12 (shrimp) and 2.53 (herring). On the other hand, fish composite samples collected from 5 areas of the Baltic Sea were analyzed for PCDD/F and PCB concentrations (Isosaari et al., 2006). The lowest mean PCDD/F concentrations corresponded to burbot of the Bothnian Bay (0.13 pg WHO-TEQ/g ww), while the highest levels were found in salmon of the Bothnian Sea (17.4 pg WHO-TEQ/g ww). In turn, the lowest PCB levels were also observed in burbot of the Bothnian Bay (0.08 pg WHO-TEQ/g ww), while the highest concentrations were also detected in salmon of the Bothnian Sea (15.6 pg WHO-TEQ/g ww). 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). The EU maximum permissible level for PCDD/Fs was exceeded in salmon and Baltic herring (Isosaari et al., 2006). Papadopoulos et al. (2004) determined the levels of PCDD/ Fs and dioxin-like PCBs in 77 food samples from the Greek market, including fish (wild, 4 samples; aquaculture, 7 samples). The average concentrations of PCDD/Fs were 0.12 and 0.47 pg WHO-TEQ/g fat, for wild and aquaculture fish, respectively. For non-ortho PCBs, average sums were 0.33 and 1.19 pg WHO-TEQ/g fat, for wild and aquaculture fish, respectively. On the other hand, samples of 12 edible fish species from the Marmara Sea, Turkey, were recently analyzed for PCBs and other organochlorinated compounds (Coelhan et al., 2006). Total PCB concentrations (sum of 7 congeners) ranged from 63.30 to 508.71 ng/g fat, with an average value of 253.08 ng/g fat. In Spain, Cuervo et al. (2002) determined the levels of PCDD/Fs and PCBs in 5 food groups of the total diet study of the Basque Country. Fish was one of these groups. Total PCDD/ F and non-ortho and ortho PCB concentrations were between 15 and 58 ng WHO-TEQ/g fat. Concentrations of these pollutants in fish were notably higher (at least a factor of 6) than those found in the remaining food groups. Intakes of PCDD/Fs, non-ortho PCBs and ortho-PCBs from fish were 11.6, 52.5 and 17.8 pg WHO-TEQ/day, respectively. Bordajandi et al. (2004) analyzed a great variety of food purchased across the city of Huelva (SW Spain) for the content of a number of pollutants including PCDD/Fs and PCBs. In fish and other seafood samples, total TEQs ranged between 0.24 pg WHO-TEQ/g ww for cuttlefish and 1.00 pg WHO-TEQ/g ww for fatty sea fish (tuna, mackerel, and sardine). For a 70 kg person, total daily intake of PCDD/Fs and PCBs was estimated to be 2.63 pg WHO-TEQ/kg body weight. From this intake, the
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contributions of fish and other seafood were 4% and 7% for PCDD/Fs and PCBs (mono and non-ortho), respectively. The same research group calculated the average daily intake of PCDD/Fs and dioxin-like PCBs for the general Spanish population, by measuring 258 Spanish foodstuffs collected between 2000 and 2003 (Fernandez et al., 2004). In edible marine species, the highest concentrations of PCDD/Fs, nonortho PCBs and mono-ortho PCBs were found in oysters, followed by clams for PCDD/Fs, and by white sea bream for PCBs. By contrast, the lowest levels corresponded to prawn, cuttlefish and sole for both PCDD/Fs and PCBs. The daily dietary intakes for a person of 70 kg were 1.35 and 3.22 pg WHO-TEQ/kg, for PCDD/Fs and dioxin-like PCBs, respectively. The contribution of fish and other seafood to global TEQ intake was 11%. Recently, the same research group determined the levels of PCDD/Fs and PCBs in 5 fish species and 4 seafood species in the Coast of Huelva (Spanish SW Atlantic coast). These species, collected in 2002, are frequently found and consumed in the area where analyzed. PCDD/F concentrations ranged from 0.2 (angler fish) to 1.18 pg/g ww (shellfish sample), while those of total PCBs ranged between 861 (prawns) and 23787 pg/g ww (sardine). In most species, dioxin-like PCBs contributed with the highest percentage to total TEQ content (Bordajandi et al., 2006). In studies performed in our laboratory, we analyzed the levels of PCDD/Fs and PCBs in 16 composite samples of hake, sardine and mussel purchased from markets across Catalonia (Spain) during 2000. PCDD/F concentrations for these species were 0.11, 0.66 and 0.30 pg WHO-TEQ/g ww, respectively (Llobet et al., 2003a), while PCB levels were 0.25, 2.45 and 0.35 pg WHO-TEQ/g ww (Llobet et al., 2003b). The contributions of these marine species to total daily dietary intake of PCDD/Fs and PCBs were 31% and 55%, respectively. Recently, we reported the levels of PCDD/Fs in 36 composite samples of foodstuffs randomly acquired in 2002 in Tarragona County (Catalonia). Edible marine species included hake, whiting blue, bass, angler fish, mussel, prawn, sardine, tuna and salmon (Bocio and Domingo, 2005). The mean PCDD/F concentrations were 3.7 and 11.6 pg/g lipid weight in fish and other seafood, respectively. Marine species was the food group showing the highest contribution to total dietary intake of PCDD/Fs (63.8 pg WHO-TEQ/day for a person of 70 kg body weight), 33.7%. In a recent study, we determined the levels of PCDD/Fs and PCBs in 14 edible marine species randomly purchased in various cities of Catalonia. Fish and seafood consisted of the following species: sardine, tuna, anchovy, mackerel, swordfish, salmon, hake, red mullet, sole, cuttlefish, squid, clam, mussel, and shrimp. The highest PCDD/F and PCB (11 congeners) levels were found in red mullet (10.28 pg/g ww and 88.10 ng/g ww, respectively), whereas the lowest levels of these pollutants were noted in cuttlefish (PCDD/Fs, 0.64 pg/g ww) and shrimp (PCBs, 0.46 pg/g ww). For an adult man (70 kg body weight), the intake of PCDD/Fs plus dioxin-like PCBs through fish and other seafood was estimated to be 38.0 pg WHO-TEQ/day (Bocio et al., 2007).
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3. North American studies The most relevant results concerning the North American studies here reviewed, as well those of the Asian and African reports are summarized in Table 2. Jensen and Bolger (2001) conducted a survey of commercial fish and shellfish to obtain data on PCDD/F intake in the USA. Shrimp, cod, blue crab and oysters were included as marine species consumed in the greatest amounts, while catfish was also sampled because it was the dominant aquaculture species. Samples were collected in 1995–1996. Mean concentrations for fish (not catfish), molusks, crustacean, shrimp and catfish were 4.51 × 10− 4, 0.44, 0.35, 0.003 and 2.08 pg WHO-TEQ/g ww, respectively, when ND was assumed to be zero (ND = 0), while when ND was assumed to be equal to the LOD (ND = LOD) the mean levels corresponding to the same species were, respectively, 0.29, 0.46, 0.37, 0.15 and 2.10 pg WHO-TEQ. The bounds of mean PCDD/F intakes (pg WHO-TEQ/person/day) ranged from 0.09 (ND = 0)–4.5(ND = LOD) for shrimp to 148(ND = 0)–150 (ND = LOD) for catfish. In 1998, the FDA annual collection of food samples included, among other food groups, samples of various fish (aquacultured salmon, wild caught salmon, stripped bass, pollack) and shellfish (scallops, lobster, blue crab, crawfish). The levels of PCDD/Fs in the samples were simultaneously analyzed by high resolution mass spectrometry (HRMS) and by quadrupole ion storage tandem mass spectrometry (QISTMS) (Hayward et al., 2001). Using HRMS, I-TEQ values for s. bass, salmon and crab were respectively, 1.9, 0.73 and 1.05 ng/kg ww, whereas the levels of s. bass, salmon and lobster were 1.8, 1.02 and 0.61 ng I-TEQ ww, respectively, when QISTMS was used. The I-TEQ for mean PCDD/F levels in the 40 fish and shellfish samples measured by HRMS were 1.4 ng I-TEQ/kg ww. Recently, Hayward et al. (in press) reported the levels of PCDD/ Fs and PCBs in commercially wild caught and farm-raised fish (bluefish, “rockfish”, wild caught Alaska King, Sockeye and Coho salmon, and farm-raised salmon) fillets purchased from markets in Maryland, Washington, DC, and North Carolina during April–August 2004. The highest and lowest PCB concentrations were found in a wild bluefish fillet (800 ng/g ww) and in a wild Coho salmon fillet (0.35 ng/g ww), respectively. The levels of PCDD/Fs ranged from 0.07(rockfish) to 27 (bluefish) pg WHO-TEQ/g ww. The concentrations of 14 organochlorine contaminants including PCDD/Fs and PCBs and those of 14 polybrominated diphenyl ether flame retardant congeners were determined in farmed salmon obtained from farms in eight major salmon farming regions of the world, samples of five species of wild Pacific salmon, and retail market samples of farmed salmon obtained in 16 cities in Europe and North America (Hites et al., 2004a,b). PCDD/F and PCB levels in salmon showed notable differences depending on the respective origin. Thus, farmed salmon had significantly higher contaminant burdens than wild salmon, whereas farmed salmons from Europe were significantly more contaminated than those from South and North America (Hites et al., 2004a). When a benefit-risk analysis was conducted to compare quantitatively the cancer and noncancer
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Table 2 A summary of recent literature data concerning levels of PCDD/Fs and PCBs in edible marine species and human dietary intake Sampling site
Species analyzed
Levels of PCDD/Fs and/or PCBs
Comments and remarks
References
USA
Shrimp, cod, blue crab, oysters, catfish
PCDD/F levels only
Jensen and Bolger (2001)
USA
Atlantic and Pacific salmon
California coast, USA
Samples of a variety of fish
Dioxin and PCB levels were higher in European farm-raised salmon than in that from North and South America PCDD/Fs; mean I-TEQ for all species: 33.1 pg/g lipid PCBs (3 coplanar congeners); mean I-TEQ for all species: 109 pg/g lipid PCBs; highest value in a wild bluefish fillet, 800 ng/g ww; lowest level in wild Coho salmon fillet, 0.35 ng/g ww PCDD/Fs and PCBs; geometric means WHO-TEQ (pg/g whole weight) ranged from 0.06 (shrimp) to 0.92 (salmon) PCBs; range: from 0.20 (shrimp and mussel) to 2.5 (mackerel) ng/g ww PCDD/Fs and PCBs (pg WHO-TEQ/g lipid weight); bivalves (0.016–27 and 0.07–7.71), gastropods (0.05–44 and 0.53–7.9) PCBs; average concentration: 3.60 ng/g ww; highest and lowest values (ng/g ww): 8.04 (flounder) and 0.83 (cuttlefish) PCDD/Fs and dioxin-like PCBs; total concentration: 0.91 pg WHO-TEQ/g PCBs (22 congeners); mean concentrations (ng/g ww): sport fish, 23.0; market fish, 8.91 PCDD/Fs; 0.02–4.39 pg WHOTEQ/g ww Dioxin-like PCBs; 0.008–0.6 pg WHO-TEQ/g ww Concentrations, not reported
PCDD/F intake: 0.09–4.5 and 140–150 pg/person/day for shrimp and catfish, respectively Most farmed salmon should be consumed at rates of b10 meals/month No information on human exposure
Brown et al. (2006)
No information on human exposure
Hayward et al. (in press)
No information on human exposure
Rawn et al. (2006)
No information on human exposure No information on human exposure
Nakata et al. (2002) Zhao et al. (2005)
Estimated intake of PCBs through fish and shellfish: 1.83 ng/kg body weight
Yang et al. (2006)
Intakes (pg WHO-TEQ/day): PCDDs, 5.13, PCDFs, 8.45, dioxin-like PCBs, 50.20 Intake of sport and marked fish exceeded the risk-based screening value based on US EPA method Intakes (pg WHO-TEQ/kg body weight/day): PCDDs, 0.10, PCDFs, 0.18, dioxin-like PCBs, 0.40 A significant positive multivariateadjusted association was identified between serum PCDD/F levels and marine fish intake for persons N45 years No information on human exposure
Sasamoto et al. (2006)
Maryland, Washington, Wild caught and farm-raised DC; North fish fillets Carolina (USA) Canada Fish products from the Canadian retail market
China
Various fish and seafood
Bohai Sea coastline, China
Bivalves and gastropods
China
Fish and shellfish purchased from supermarkets in 3 cities
Tokyo, Japan
Fish and shellfish; total diet study
Korean coastal waters
Sport and market fish
Korean coastal waters
40 species of marine organisms (fish, crustaceans, cephalopods, bivalves, gastropods) Various fish species and fish viscera, shellfish, octopus, shrimp
Taiwan
Ismailia city, Egypt
Mullet fish, bolti fish, bivalves and crab
PCDD/Fs: 0.12–0.40 pg WHOTEQ/g ww Dioxin-like PCBs: 0.14–0.76 pg WHO-TEQ/ww Upper bound levels
Hites et al. (2004a), Foran et al. (2005)
Yim et al. (2005)
Moon and Ok (2006) Chen et al. (2007)
Loufty et al. (2007)
North American, Asian and African studies (2001–2006).
risks of exposure to organic contaminants in salmon with the omega-3 fatty acid-associated health benefits of salmon consumption, it was suggested that the risk of exposure to contaminants in farmed and wild salmon would be partially offset by the associated health benefits (Foran et al., 2005). However, for the specific case of farmed salmon from northern Europe, the advice was not consuming more than three meals per month (Huang et al., 2006). Recently, Brown et al. (2006) measured the levels of PCDD/ Fs and coplanar PCBs in 65 samples of a variety of fish collected from California coastal waters in 2000–2001. For all species from all sampling areas, the mean I-TEQ was 33.1 pg/g lipid for PCDD/Fs and 109 pg/g lipid for the 3 coplanar PCBs (77, 126, 169). In turn, Rawn et al. (2006) also analyzed the
levels of PCDD/Fs and PCBs in fish products available on the Canadian retail market in 2002. The geometric means WHOTEQ (pg/g whole weight) ranged from 0.06 (shrimp) and 0.08 (tilapia), to 0.92 (salmon). 4. Asian studies Nakata et al. (2002) investigated the residue levels of various pollutants in foodstuffs (including fish and seafood) collected in China in 2000–2001. PCBs were also determined. Relatively high PCB concentrations were found in fish and other seafood, in the range of 0.20 (shrimp and mussel) to 2.5 (mackerel) ng/g ww. Also in China, the levels of PCDD/Fs and PCBs were recently determined in various species of bivalves and
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gastropods (which are routine seafood for most Chinese people) collected in eight sampling sites along Bohai Sea coastline (NE China) (Zhao et al., 2005). For dioxin-like PCBs, WHO-TEQs ranged between 0.87 and 7.71 pg/g lipid weight for bivalves, and between 0.53 and 7.9 pg/g lw for gastropods, while for PCDD/Fs, WHO-TEQs oscillated between 0.016–27 and 0.05– 44 pg/g lw, for bivalves and gastropods, respectively. In a recent survey, Yang and co-workers (2006) analyzed the concentrations of PCBs and organochlorine pesticides in a wide variety of fish and shellfish collected from local supermarkets from three Chinese cities (Dalian, Tianjin and Shangai). In most samples, PCBs 138 and 153 were dominant, followed by PCBs 101 and 180. The average PCB concentration was 3.60 ng/g ww, with the highest values corresponding to flathead flounder (8.04 ng/g ww) and white sardine from Shangai (5.60 ng/g ww), and the lowest to Pacific cuttlefish (0.83 ng/g ww) and white sardine from Dalian (1.11 ng/g ww). The estimated daily intake of PCBs through fish and shellfish, considering a body weight of 60 kg and an average consumption of 30.5 g/person/day, was 1.83 ng/kg body weight. Recently, Sasamoto et al. (2006) estimated the dietary daily intake of PCDD/Fs and dioxin-like PCBs by a total diet study in metropolitan Tokyo, Japan, between 1999 and 2004. Fourteen food groups (including fish and shellfish) were analyzed. Total WHO-TEQ concentrations of PCDD/Fs and dioxin-like PCBs in fish and shellfish ranged from 0.98 to 0.91 pg WHO-TEQ/g in 1999 and 2004, respectively. PCB 126, followed by PCB 118, was the highest contributing congener, and accounted for over 40% of the daily intake of PCDD/Fs and PCBs from fish and shellfish. In 2004, intake of PCDDs, PCDFs, and dioxinlike PCBs from fish and shellfish were found to be 5.13, 8.45 and 50.20 pg WHO-TEQ/day, respectively. In relation to the total dietary intake of all food groups, these amounts mean percentages of 59%, 66% and 90%. In a recent study, Tsukino et al. (2006) determined background serum levels of PCDD/Fs and PCBs in Japanese infertile women in order to estimate the effect of lifestyle factors, especially dietary factors, on serum levels of these pollutants. The authors found that fish consumption was positively associated with serum levels of total TEQ (PCDD/Fs and PCBs) in Japanese infertile women. Yim et al. (2005) determined the levels of 22 PCB congeners in the muscles of sport and market fish to assess the potential risks to humans consuming fish originating in Korea's coastal waters. Mean (and range) concentrations of sport and market fish were 23.0 (4.48–95.6) and 8.91 (2.96–68.2) ng/g ww, respectively. Total PCB concentrations in all sport and marked fish exceeded the risk-based screening value (SV) based on US EPA method (5.04 ng/g based on total PCBs). Moon and Ok (2006) reported the concentrations of PCDD/Fs and dioxin-like PCBs in 40 species of marine organisms from Korean coastal waters. PCDD/F levels varied from 0.02 to 4.39 pg WHO-TEQ/ g ww and the dioxin-like PCB concentrations varied from 0.008 to 0.6 pg WHO-TEQ/g ww. Comparing organism groups, the highest pollutant concentrations were recorded in crustaceans, followed by fish, cephalopods, bivalves and gastropods. The estimated intakes of PCDDs, PCDFs and dioxin-like PCBs were 0.10, 0.18 and 0.40 pg WHO-TEQ/kg body weight/day,
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respectively. These values include the five fish and seafood groups evaluated. The contribution of dioxin-like PCBs to total intake from all organisms (0.68 pg WHO-TEQ/kg body weight/ day) averaged 60%, being the relative contribution of each organism group in descending order: fish, crustaceans, cephalopods, bivalves and gastropods. In a recent study, Chen et al. (2007) examined whether different dietary patterns and body fat content were associated with serum PCDD/F concentrations for different age groups of Taiwanese subjects. For the group of N 45 years, a significant positive multivariate-adjusted association was identified between serum PCDD/F levels and fish intake. Although various marine fish species (including viscera), shellfish, octopus and shrimp were included in the study, the levels of PCDD/Fs were not reported. 5. African studies Recently, Loufty et al. (2007) determined the concentrations of PCDD/Fs and dioxin-like PCBs in samples of fish and seafood (mullet fish, bolti fish, bivalves and crab) randomly acquired in local markets from Ismailia city, Egypt. The upper bound levels for PCDD/Fs and dioxin-like PCBs ranged from 0.12 (crab) to 0.40 (mullet) pg WHO-TEQ/g ww, and from 0.14 (bivalves) to 0.76 (mullet) pg WHO-TEQ/g ww, respectively. For PCDD/Fs, these values are lower than the current EU limit. In a another study of the same research group, it was observed that in Egypt, fish and seafood play a less important role than cereals and vegetables/fruits (Loufty et al., 2006). 6. Conclusions The review of a considerable number of international surveys shows that the comparison among results is rather complicated. While PCDD/Fs and PCBs bioaccumulate in marine species, depending basically on the environment in which the respective species are caught, their levels increase with the age of the fish. For PCBs, an additional difficulty for comparison of results is the great variety of congeners that have been analyzed in the different surveys. Other differences concern the expression of the results: wet weight, dry weight, or lipid weight. Finally, some investigators report their results concerning only some parts of the fish samples: muscle, liver, skin, etc., while other researchers have even evaluated the effects of cooking on the loss of POPs (Bayen et al., 2005). All these circumstances, together with the different units used to report the concentrations of PCDD/Fs and PCBs in the reviewed studies (I-TEQ, WHO-TEQ, CALUX-TEQ), make still more complicated the comparison of the different data. The studies here reviewed shows that some groups of population frequently consuming high quantities of certain fish species could be significantly increasing their health risks due to PCCD/F and PCB intake. Exposure to toxic pollutants through the diet depends on two main factors: 1) the levels of the respective pollutant in the food items consumed, fish and seafood in the present case, and 2) the average amount of the item (fish and seafood) daily/weekly/monthly consumed
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specifically by each subject, or the average consumption for a specific group of population. To give an easy response to this rather complicated issue, we recently determined the levels of a number of metals and organic pollutants (including PCDD/Fs and dioxin-like compounds) in 14 widely consumed fish species (Bocio et al., 2007; Domingo et al., in pressa). To balance the health risks derived from this fish consumption with the potential benefits derived from polyunsaturated omega-3 fatty acid (PUFA) intake, the levels of 2 PUFAs were also determined (Domingo et al., in pressa). All these results were used as the basis to prepare a program, RIBEPEIX, that can be freely consulted in Internet at http://www.fmcs.urv.cat/portada/ribepeix/ (Domingo et al., in pressb). The fish species, the frequency of consumption, and the meal size are essential issues for an adequate balance of the health benefits and risks of a regular fish intake. In relation to it, RIBEPEIX allows, according to the specific consumption habits, to optimize individually the balance between health benefits (omega-3) and risks (chemical contaminants) of fish consumption. However, general recommendations about fish consumption should be done taking into account the data concerning levels of environmental pollutants in the most consumed marine species in each specific region or country. Acknowledgment This study was supported by the Catalan Food Safety Agency, Generalitat de Catalunya, Spain. References Baars AJ, Bakker MI, Baumann RA, Boon PE, Freijer JI, Hoogenboom LAP, et al. Dioxins, dioxin-like PCBs and non-dioxin-like PCBs in foodstuffs: occurrence and dietary intake in the Netherlands. Toxicol Lett 2004;151:51–61. Bayarri S, Baldassarri LT, Iacovella N, Ferrara F, Di Domenico A. PCDDs, PCDFs, PCBs and DDE in edible marine species from the Adriatic Sea. Chemosphere 2001;43:601–10. Bayen S, Barlow P, Lee HK, Obbard JP. Effect of cooking on the loss of persistent organic pollutants from salmon. J Toxicol Environ Health, Part A 2005;68:253–65. Binelli A, Provini A. POPs in edible clams from different Italian and European markets and possible human health risk. Mar Pollut Bull 2003;46:879–86. 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. Bocio A, Domingo JL, Falcó G, Llobet JM. Concentrations of PCDD/PCDFs and PCBs in fish and seafood from the Catalan (Spain) market. Environ Int 2007;33:170–5. Bordajandi LR, Gómez G, Abad E, Rivera J, Fernandez-Baston MM, Blasco J, et al. Survey of persistent organochlorine contaminants (PCBs, PCDD/Fs, and PAHs), heavy metals (Cu, Cd, Zn, Pb, and Hg), and arsenic in food samples from Huelva (Spain): levels and health implications. J Agric Food Chem 2004;52:992–1001. Bordajandi LR, Martín I, Abad E, Rivera J, González MJ. Organochlorine compounds (PCBs, PCDDS and PCDFs) in seafish and seafood from the Spanish Atlantic Southwest coast. Chemosphere 2006;64:1450–7. Brown FR, Winkler J, Visita P, Dhaliwal J, Petreas M. Levels of PBDEs, PCDDs, PCDFs, and coplanar PCBs in edible fish from California coastal waters. Chemosphere 2006;64:276–86.
Charnley G, Doull J. Human exposure to dioxins from food, 1999–2002. Food Chem Toxicol 2005;43:671–9. Chen HL, Su HJ, Lee CC. Association between tofu intake and serum polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs) in the elderly Taiwanese. Environ Int 2007;33:265–71. Coelhan M, Stroheimer J, Barlas H. Organochlorine levels in edible fish from the Marmara Sea, Turkey. Environ Int 2006;32:775–80. Cuervo L, Jalon M, Rose M, Fernandes A, White S, Gonzalez L. Dietary intakes of PCDDs, PCDFs and PCBs in total diet samples from the Basque Country (Spain). Organohalog Compd 2002;55:219–22. Domingo JL, Bocio A, Falcó G, Llobet JM. Benefits and risks of fish consumption. Part I. A quantitative analysis of the intake of omega-3 fatty acids and chemical contaminants. Toxicology in press, doi:10.1016/j.tox.2006.11.054. _________________________ Domingo JL, Bocio A, Martí-Cid R, Llobet JM. Benefits and risks of fish consumption. Part II. RIBEPEIX, A computer program to optimize the balance between the intake of omega-3 fatty acids and chemical contaminants. Toxicology in press, doi:10.1016/j.tox.2006.11.059. _________________________ EC Commission Regulation. No. 199/2006 of 3 February amending Regulation No. 466/2001 setting maximum levels for certain contaminants in foodstuffs as regard to dioxins and dioxin-like PCBs. Off J Eur Union, L 2006;32/34. Engler MM, Engler MB. Omega-3 fatty acids. Role in the cardiovascular health and disease. J Cardiovasc Nurs 2006;21:17–24. Fernandez MA, Gómara B, Bordajandi LR, Herrero L, Abad E, Abalos M, et al. Dietary intakes of polychlorinated dibenzo-p-dioxins, dibenzofurans and dioxin-like polychlorinated biphenyls in Spain. Food Addit Contam 2004;21:983–91. Foran JA, Carpenter DO, Hamilton MC, Knuth BA, Schwager SJ. Risk-based consumption advice for farmed Atlantic and wild Pacific salmon contaminated with dioxins and dioxin-like compounds. Environ Health Perspect 2005;113:552–6. Hayward DG, Holcomb J, Glidden R, Wilson P, Harris M, Spencer W. Quadrupole ion storage tandem mass spectrometry and high-resolution mass spectrometry: complementary application in the measurement of 2,3,7,8chlorine substituted dibenzo-p-dioxins and dibenzofurans in US foods. Chemosphere 2001:407–15. Hayward D, Wong J, Krynitsky AJ. Polybrominated diphenyl ethers and polychlorinated biphenyls in commercially wild caught and farm-raised fish fillets in the United States. Environ Res in press. Hites RA, Foran JA, Carpenter DO, Hamilton MC, Knuth BA, Schwager SJ. Global assessment of organic contaminants in farmed salmon. Science 2004a;303:226–9. Hites RA, Foran JA, Schwager SJ, Knuth BA, Hamilton MC, Carpenter DO. Global assessment of polybrominated diphenyl ethers in farmed and wild salmon. Environ Sci Technol 2004b;38:4945–9. Huang X, Hites RA, Foran JA, Hammilton C, Knuth BA, Schwager SJ, et al. Consumption advisories for salmon based on risk of cancer and noncancer health effects. Environ Res 2006;101:263–74. Huwe JK, Larsen GL. Polychlorinated dioxins, furans, and biphenyls, and polybrominated diphenyl ethers in a U.S. meat market basket and estimates of dietary intake. Environ Sci Technol 2005;39:5606–11. Isosaari P, Hallikainen A, Kiviranta H, Vuorinen PJ, Parmanne R, Koistinen J, et al. Polychlorinated dibenzo-p-dioxins, dibenzofurans, biphenyls, naphthalenes and polybrominated diphenyl ethers in the edible fish caught from the Baltic Sea and lakes in Finland. Environ Pollut 2006;141:213–25. Jensen E, Bolger PM. Exposure assessment of dioxins/furans consumed in dairy foods and fish. Food Addit Contam 2001;18:395–403. Juan CY, Thomas GO, Sweetman AJ, Jones KC. An input-output balance study for PCBs in humans. Environ Int 2002;28:303–14. Karl H, Ruoff U, Blüthgen A. Levels of dioxins in fish and fishery products on the German market. Chemosphere 2002;49:765–73. Kiviranta H, Ovaskainen ML, Vartiainen T. Market basket study on dietary intake of PCDD/Fs, PCBs, and PBDEs in Finland. Environ Int 2004;30:923–32. Knutzen J, Bjerkeng B, Næs K, Schlabach M. Polychlorinated dibenzofurans/ dibenzo-p-dioxins (PCDF/PCDDS) and other dioxin-like substances in marine organisms from the Grenland fjords, S. Norway, 1975–2001: present contamination levels, trends and species specific accumulation of PCDF/ PCDD congeners. Chemosphere 2003;52:745–60.
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Review article
Levels of PCDD/PCDFs and PCBs in edible marine species and human intake: A literature review José L. Domingo ⁎, Ana Bocio Laboratory of Toxicology and Environmental Health, School of Medicine, “Rovira i Virgili” University, San Lorenzo 21, 43201 Reus, Spain Received 8 August 2006; accepted 18 December 2006 Available online 30 January 2007
Abstract Polychlorinated dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs) and biphenyls (PCBs) are lipophilic organic compounds whose origin comes from many different sources. PCDD/Fs and PCBs are ubiquitous and persistent environmental pollutants with a well known potential toxicity, which were included at the 1998 UN-EC POP protocol. Although human exposure to PCDD/Fs and PCBs can occur by various routes, food is the primary source. A number of studies have shown that the major food sources of these organic pollutants are fat-containing animal products, including fish and other seafood. Because of the frequent health recommendations concerning fish consumption, to determine the contribution to the dietary intake of chemical contaminants such as PCDD/Fs and PCBs through fish and other seafood consumption is an issue of special interest. This paper reviews the state of the science regarding recent literature on PCDD/F and PCB levels in marine species and human intake through fish and seafood consumption. The concentrations of these pollutants depend basically on the environment in which the respective species are caught. It is concluded that some groups of population frequently consuming high quantities of certain species could be significantly increasing health risks due to PCDD/F and PCB exposure. © 2007 Elsevier Ltd. All rights reserved. Keywords: Polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs); Polychlorinated biphenyls (PCBs); Fish and other seafood; Human intake; Recent reports
Contents 1. Introduction . . . . . . . 2. European studies . . . . 3. North American studies. 4. Asian studies . . . . . . 5. African studies . . . . . 6. Conclusions. . . . . . . Acknowledgment. . . . . . . References . . . . . . . . . .
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1. Introduction Polychlorinated dibenzo-p-dioxins (PCDDs) and dibenzofurans (PCDFs), and polychlorinated biphenyls (PCBs) are ⁎ Corresponding author. Tel.: +34 977 759380; fax: +34 977 759322. E-mail address: [email protected] (J.L. Domingo). 0160-4120/$ - see front matter © 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.envint.2006.12.004
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ubiquitous environmental contaminants, which persist and bioaccumulate through the food chain. Human exposure to these pollutants occurs mainly from eating foodstuffs that contain these chemicals (Schecter et al., 2001; Juan et al., 2002; Kiviranta et al., 2004; Bocio and Domingo, 2005). It has been reported that the contribution of meat and meat products, dairy products, and fish and other seafood may surpass the 90% of the
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total exposure to PCDD/Fs and PCBs (Schecter et al., 1997; Llobet et al., 2003a,b; Bocio and Domingo, 2005; Charnley and Doull, 2005; Huwe and Larsen, 2005). Recently, we determined the concentrations of PCDD/Fs and PCBs in a number of foodstuffs purchased from various cities of Catalonia (Spain). The dietary intake of these compounds by the population of Catalonia was also estimated (Llobet et al., 2003a,b). The most important contribution to the dietary intake of PCDD/Fs and PCBs corresponded to fish and other seafood: 31% for PCDD/Fs and 55% for PCBs. These results corroborate 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. The nutritional benefits of fish consumption are well known: an important content of high-quality proteins, vitamins and other essential nutrients, low levels of saturated fats, as well as high amounts of omega3 polyunsaturated fatty acids, which seem to have protective effects in preventing coronary heart disease among other health benefits (Kris-Etherton et al., 2002; Engler and Engler, 2006). In recent years, the number of studies focused on determining the levels of PCDD/Fs, PCBs and other persistent organic pollutants (POPs) in foodstuffs has been notable. This paper presents an overview on the current available scientific information concerning concentrations of PCDD/Fs and PCBs in edible marine species, and the intake of PCDD/Fs and PCBs through consumption of these species. It can be of special interest to those particularly interested in the balance between potential benefits and risks of fish consumption. The reports here reviewed have been discussed according to their respective geographical origins, being divided into European, North American, Asian and African surveys. Only studies published after 2001 have been reviewed. It is important to note that data are reported just as the respective PCDD/F and PCB concentrations were expressed in the corresponding studies: ITEQ, WHO-TEQ and CALUX-TEQ. An important issue that makes difficult, in certain cases, the comparison of the results of the studies here reviewed is how, for TEQ calculations, the different authors considered the non-detected (ND) values of PCDD/F or PCB congeners. We found that depending on the specific study, non-detected concentrations were assumed to be equal to the limit of detection (ND = LOD), equal to zero (ND = 0), or equal to one-half of the respective limit of detection (ND = 1/2 LOD). 2. European studies A summary of the European studies reviewed in this paper is shown in Table 1. Edible marine species (anchovy, squid, mussel, lobster, mackerel, red mullet and clam) from several areas of the Adriatic sea were analyzed for their content in PCDD/Fs and PCBs. In general, I-TEQs were greater for those species at higher levels in the trophic web (mackerel N red mullet N anchovy). The levels of PCDD/Fs and PCBs were between 0.23 and 1.07 pg I-TEQ/g of wet weight (ww) in these species, and within 0.07–0.25 for the remaining species. The
greatest PCB concentrations were found in mackerel (94– 177 ng/g ww) (Bayarri et al., 2001). Marcotrigiano and Storelli (2003) determined the levels of 17 PCB congeners in a considerable number of marine organisms caught in the Adriatic and Ionian seas. Mean values in fish muscles, cephalopods (flesh), bivalves and crustacean (flesh) were: 4.54, 0.33, 4.31 and 4.69 ng/g ww, respectively. No information concerning human exposure to PCBs was reported. Binelli and Provini (2003) measured the concentrations of PCBs in 16 pools of edible clams purchased from different Italian and European markets. The mean PCB concentration was 4.8 (range between 1.6 and 15.4) ng/g of ww. Perugini et al. (2004) analyzed the concentrations of 7 PCB congeners in mussel, lobster, red mullet, cuttlefish, squid, anchovy, sardine and mackerel from two sites of the Italian coast of the Adriatic Sea. The maximum ∑PCB (mean values for the two sites, ng/g ww) corresponded to mackerel (20.8), followed by red mullet (18.0) and anchovy (17.5), while the lowest ∑PCB (mean values for the two sites, ng/g ww) were detected in cuttlefish (0.73) and squid (2.4). In contrast to the results concerning red mullet, Licata et al. (2003) did not find residues of PCBs (Aroclor 1232 series) in tissues of the mullet Liza aurata from the Straits of Messina (Sicily, Italy). Recently, Naso and co-workers (2005) measured the levels of 20 PCBs in edible tissues from 10 marine species collected from the Gulf of Naples (Italy). The sum of all determined PCB congeners ranged between 407 and 22287 ng/g of lipid weight (lw), for octopus and bass, respectively. In another recent Italian study, Taioli et al. (2005) measured the content of PCDD/Fs in 269 samples of food of animal origin, including fish (eel, herring, mullet, mackerel, bass and trout). The highest and lowest mean PCDD/F values corresponded to eel and trout: 1.11 and 0.18 pg WHO-TEQ/g, respectively. Mean PCDD/F concentration in mackerel was also relatively low, 0.22 pg WHO-TEQ/g. According to these results, the estimated daily intake (median value) of PCDD/Fs through fish consumption was 2.34–2.38 pg WHO-TEQ/kg body weight. Karl et al. (2002) analyzed the contents of PCDD/Fs of 184 pooled samples of 20 marine fish and fishery products (canned fish) from the German market (1995–1998). The highest dioxin content in the edible parts was found in herring of the Baltic Sea and halibut of the North Sea: 1.91 and 1.49 ng/kg ww, respectively. The lowest PCDD/F levels were found in hake and Alaska pollack (0.005–0.006 and 0.007 ng/kg ww, respectively). Based on a daily fish consumption of 20 g, the average daily intake of PCDD/Fs via fish was 6.2 pg WHO-TEQ per person. Knutzen et al. (2003) determined the levels of PCDD/Fs and PCBs in marine organisms from the Grenland fjords, in Norway. Composite samples of Atlantic cod, sea trout, flounder, eel, edible crab and blue mussel were analyzed. In edible fillets, or muscle of mollusks, WHO-TEQ for PCDD/Fs ranged between 0.85 (cod) and 28.0 ng/kg ww (flounder). The highest value was found in cod liver (587 ng WHO-TEQ/kg ww). When dioxin-like PCBs (congeners 77, 105, 118, 126, 156 and 169) were also included, the highest and lowest WHO-TEQ values corresponded to flounder (33.5 ng/kg ww) and mussels (1.6 ng/ kg ww). In Baltic Sea fish (salmon, cod, flounder and herring) from the Polish coast, the highest and lowest PCDD/F
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Table 1 A summary of recent literature data concerning levels of PCDD/Fs and PCBs in edible marine species and human dietary intake Sampling site
Species analyzed
Adriatic Sea
Anchovy, squid, mussel, lobster, PCDD/Fs and PCBs: 0.23–1.07 pg mackerel, red mullet, clam I-TEQ/g ww for mackerel, red mullet and anchovy; 0.07–0.25 pg I-TEQ/g ww for the remaining species A number of fish, cephalopods, PCBs (17 congeners); mean values: bivalves and crustacean species 4.54, 0.33, 4.31 and 4.69 ng/g ww, respectively for the indicated groups Edible clams (pools) PCBs; mean value: 4.8 (1.6–15.4) ng/g ww
Adriatic and Ionan Seas
Various European markets Italian coast of the Mussel, lobster, red mullet, Adriatic Sea cuttlefish, squid, anchovy, sardine, mackerel Gulf of Naples, 10 marine species Italy
Levels of PCDD/Fs and/or PCBs
PCBs (7 congeners); highest value: 20.8 ng/g ww (mackerel); lowest value: 0.73 ng/g ww (cuttlefish) PCBs (20 congeners); range between 407 (octopus) and 22287 (bass) ng/g l w PCDD/Fs; highest and lowest mean values: 1.11 and 0.18 pg WHO-TEQ/g for eel and trout, respectively PCDD/Fs; highest and lowest levels: 1.91 and 0.006 ng/kg ww for herring and hake, respectively
Italy
Eel, herring, mullet, mackerel, bass, trout
Germany
Marine fish and fishery products (canned fish) from the German market
Grenland fjords, Norway
Atlantic cod, sea trout, flounder, PCDD/Fs; levels from 0.85 (cod) to eel, edible crab, blue mussel 28.0 ng/kg ww (flounder). When PCBs (6 congeners) were also included, the highest and lowest WHO-TEQ values corresponded to flounder and mussels, respectively Salmon, cod, flounder, herring PCDD/Fs; from 1.6 (cod) to 3.2 pg WHO-TEQ/g ww (salmon)
Polish coast of Baltic Sea Finland
The Netherlands
10 market baskets; salmon, rainbow trout, tuna, saithe, Baltic herring and vendace Various fish species among selected food products
Belgium
Fishery products from the Belgian market
Five areas of the Baltic Sea
Fish composite samples
Greece
Fish samples from the Greek market
Basque Country, Spain
Total Diet Study (including fish)
Huelva, SW Spain
Fish and seafood from the Huelva market
Spain
Fish and seafood from Spanish markets
Comments and remarks
References
No information on human exposure
Bayarri et al. (2001)
No information on human exposure
Marcotrigiano and Storelli (2003)
No information on human exposure No information on human exposure
Binelli and Provini (2003) Perugini et al. (2004)
No information on human exposure
Naso et al. (2005)
Estimated daily intake of PCDD/Fs through fish consumption: 2.34–2.38 pg WHO-TEQ Based on a fish consumption of 20 g/day, the average intake of PCDD/Fs via fish was 6.2 pg WHO-TEQ/day No information on human exposure
Taioli et al. (2005)
No information on human exposure
PiskorskaPliszczynska et al. (2004) Kiviranta et al. (2004)
Karl et al. (2002)
Knutzen et al. (2003)
PCDD/Fs; sum: 2.0 pg WHO-TEQ/g Average intakes of PCDD/Fs ww PCBs; sum: 1.5 pg WHO-TEQ/g ww and PCBs: 54 and 41 pg WHO-TEQ/day, respectively Contribution of PCDD/Fs plus dioxin-like PCBs through fish consumption: 16% Dioxin-like compounds; 0.12 No information on (shrimp)–2.53 (herring) human exposure pg CALUX-TEQ/g ww PCDD/Fs; levels from 0.13 (burbot) EU maximum permissible to 17.4 (salmon) pg WHO-TEQ ww levels was exceeded in salmon PCBs; levels from 0.08 (burbot) and Baltic herring to 15.6 (salmon) pg WHO-TEQ ww PCDD/Fs; sums ranging between 0.12 No information on (wild fish) and 0.47 (aquaculture fish) human exposure pg TEQ/g fat Non-ortho PCBs; average sums: from 0.33 to 1.19 pg TEQ/fat for wild and aquaculture fish, respectively Intakes of PCDD/Fs, non-ortho PCBs and ortho-PCBs from fish were 11.6, 52.5 and 17.8 pg WHO-TEQ/day, respectively Total daily intake of PCDD/Fs plus PCDD/Fs plus PCBs; range levels from 0.24 (cuttlefish) PCBs from fish: 0.11 (PCDD/Fs) and 0.18 (PCBs) pg WHO-TEQ(kg to 1.00 (tuna, mackerel and body weight for a 70 kg person sardine) pg WHO-TEQ/g ww PCDD/Fs and PCBs; highest Daily intakes of PCDD/Fs and PCBs from fish and seafood for a 70 kg levels in oysters and clams for person: 0.15 and 0.35 pg WHO-TEQ/kg PCDD/Fs, and white sea bream for PCBs. Lowest levels in prawns, body weight for PCDD/Fs and cuttlefish and sole for dioxin-like PCBs, respectively PCDD/Fs and PCBs
Baars et al. (2004)
Schoeters et al. (2004) Isosaari et al. (2006)
Papadopoulos et al. (2004)
Cuervo et al. (2002)
Bordajandi et al. (2004)
Fernandez et al. (2004)
(continued on next page)
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Table 1 (continued ) Sampling site
Species analyzed
Levels of PCDD/Fs and/or PCBs
Comments and remarks
References
Huelva coast, SW Spain
5 fish species and 4 seafood species
No information on human exposure
Bordajandi et al. (2006)
Catalonia, Spain
Hake, sardine and mussel from Catalan markets
PCDD/F levels; range from 0.2 (angler fish) to 1.8 (shellfish) pg/g ww PCB levels; range from 861 (prawns) to 23787 (sardine) pg/g ww PCDD/Fs; 0.11 (hake), 0.66 (sardine), 0.30 (mussel) pg WHO-TEQ/g ww PCBs; 0.25 (hake), 2.45 (sardine), 0.35 (mussel) pg WHO-TEQ/g ww PCDD/Fs; mean levels (pg/g fat): fish, 3.7; other seafood, 11.6
Contribution to total dietary intake of PCDD/Fs and PCBs: 31% and 55%, respectively
Llobet et al. (2003a,b)
Contribution of fish and seafood to total dietary intake of PCDD/Fs for a 70 kg person: 21.5 pg WHO-TEQ/day PCDD/Fs plus dioxin-like PCBs intake for a 70 kg subject: 38.0 pg WHO-TEQ/day
Bocio and Domingo (2005)
No information on human exposure
Coelhan et al. (2006)
Tarragona, Hake, whiting blue, bass, Catalonia, Spain angler fish, mussel, prawn, sardine, tuna and salmon from Tarragona markets Catalonia, Spain Sardine, tuna, anchovy, mackerel, swordfish, salmon, hake, red mullet, sole, cuttlefish, squid, clam, mussel, shrimp Marmara Sea, 12 edible fish species taken Turkey from the Central Fish Market of Istanbul
PCDD/Fs and PCBs; highest levels found in red mullet (PCDD/Fs and PCBs); lowest levels found in cuttlefish (PCDD/Fs) and shrimp (PCBs) PCBs; average value: 253.08 ng/g fat (range: 63.30–508.71 ng/g fat)
Bocio et al. (2007)
European studies (2001–2006).
concentrations were found in salmon, 3.2 (2.0–4.8) pg WHOTEQ/g ww, followed by herring 1.7 (1.1–2.8) and cod 1.6 (0.8– 2.4) pg WHO-TEQ/g ww, respectively (Piskorska-Pliszczynska et al., 2004). In a market study on the dietary intake of PCDD/Fs and PCBs performed in Finland, Kiviranta et al. (2004) measured the concentrations of these pollutants in 10 market baskets. Fish samples included salmon, rainbow trout, tuna, saithe, Baltic herring and vendace. The sum of PCDD/Fs was 2.0 pg WHOTEQ/g ww, and that of PCBs 1.5 pg WHO-TEQ/g ww. The average intakes of PCDD/Fs and PCBs were 54 and 41 pg WHO-TEQ/day, meaning percentages of 95% and 80% of the total dietary intake of PCDD/Fs and PCBs, respectively. In the Netherlands, Baars et al. (2004) collected (March 1999) a number of selected food products to determine occurrence and dietary intake of PCDD/Fs and PCBs. The contribution of fish to the total intake of PCDD/Fs plus dioxin-like PCBs was 16%, while for non-dioxin-like PCBs it was 26%. In Belgium, Schoeters et al. (2004) analyzed a limited number of different foods for dioxin-like compounds by the CALUX bioassay. Among them, 34 fishery products were purchased from the Belgian market. Median values (expressed as pg CALUX-TEQ/ g ww) oscillated between 0.12 (shrimp) and 2.53 (herring). On the other hand, fish composite samples collected from 5 areas of the Baltic Sea were analyzed for PCDD/F and PCB concentrations (Isosaari et al., 2006). The lowest mean PCDD/F concentrations corresponded to burbot of the Bothnian Bay (0.13 pg WHO-TEQ/g ww), while the highest levels were found in salmon of the Bothnian Sea (17.4 pg WHO-TEQ/g ww). In turn, the lowest PCB levels were also observed in burbot of the Bothnian Bay (0.08 pg WHO-TEQ/g ww), while the highest concentrations were also detected in salmon of the Bothnian Sea (15.6 pg WHO-TEQ/g ww). 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). The EU maximum permissible level for PCDD/Fs was exceeded in salmon and Baltic herring (Isosaari et al., 2006). Papadopoulos et al. (2004) determined the levels of PCDD/ Fs and dioxin-like PCBs in 77 food samples from the Greek market, including fish (wild, 4 samples; aquaculture, 7 samples). The average concentrations of PCDD/Fs were 0.12 and 0.47 pg WHO-TEQ/g fat, for wild and aquaculture fish, respectively. For non-ortho PCBs, average sums were 0.33 and 1.19 pg WHO-TEQ/g fat, for wild and aquaculture fish, respectively. On the other hand, samples of 12 edible fish species from the Marmara Sea, Turkey, were recently analyzed for PCBs and other organochlorinated compounds (Coelhan et al., 2006). Total PCB concentrations (sum of 7 congeners) ranged from 63.30 to 508.71 ng/g fat, with an average value of 253.08 ng/g fat. In Spain, Cuervo et al. (2002) determined the levels of PCDD/Fs and PCBs in 5 food groups of the total diet study of the Basque Country. Fish was one of these groups. Total PCDD/ F and non-ortho and ortho PCB concentrations were between 15 and 58 ng WHO-TEQ/g fat. Concentrations of these pollutants in fish were notably higher (at least a factor of 6) than those found in the remaining food groups. Intakes of PCDD/Fs, non-ortho PCBs and ortho-PCBs from fish were 11.6, 52.5 and 17.8 pg WHO-TEQ/day, respectively. Bordajandi et al. (2004) analyzed a great variety of food purchased across the city of Huelva (SW Spain) for the content of a number of pollutants including PCDD/Fs and PCBs. In fish and other seafood samples, total TEQs ranged between 0.24 pg WHO-TEQ/g ww for cuttlefish and 1.00 pg WHO-TEQ/g ww for fatty sea fish (tuna, mackerel, and sardine). For a 70 kg person, total daily intake of PCDD/Fs and PCBs was estimated to be 2.63 pg WHO-TEQ/kg body weight. From this intake, the
J.L. Domingo, A. Bocio / Environment International 33 (2007) 397–405
contributions of fish and other seafood were 4% and 7% for PCDD/Fs and PCBs (mono and non-ortho), respectively. The same research group calculated the average daily intake of PCDD/Fs and dioxin-like PCBs for the general Spanish population, by measuring 258 Spanish foodstuffs collected between 2000 and 2003 (Fernandez et al., 2004). In edible marine species, the highest concentrations of PCDD/Fs, nonortho PCBs and mono-ortho PCBs were found in oysters, followed by clams for PCDD/Fs, and by white sea bream for PCBs. By contrast, the lowest levels corresponded to prawn, cuttlefish and sole for both PCDD/Fs and PCBs. The daily dietary intakes for a person of 70 kg were 1.35 and 3.22 pg WHO-TEQ/kg, for PCDD/Fs and dioxin-like PCBs, respectively. The contribution of fish and other seafood to global TEQ intake was 11%. Recently, the same research group determined the levels of PCDD/Fs and PCBs in 5 fish species and 4 seafood species in the Coast of Huelva (Spanish SW Atlantic coast). These species, collected in 2002, are frequently found and consumed in the area where analyzed. PCDD/F concentrations ranged from 0.2 (angler fish) to 1.18 pg/g ww (shellfish sample), while those of total PCBs ranged between 861 (prawns) and 23787 pg/g ww (sardine). In most species, dioxin-like PCBs contributed with the highest percentage to total TEQ content (Bordajandi et al., 2006). In studies performed in our laboratory, we analyzed the levels of PCDD/Fs and PCBs in 16 composite samples of hake, sardine and mussel purchased from markets across Catalonia (Spain) during 2000. PCDD/F concentrations for these species were 0.11, 0.66 and 0.30 pg WHO-TEQ/g ww, respectively (Llobet et al., 2003a), while PCB levels were 0.25, 2.45 and 0.35 pg WHO-TEQ/g ww (Llobet et al., 2003b). The contributions of these marine species to total daily dietary intake of PCDD/Fs and PCBs were 31% and 55%, respectively. Recently, we reported the levels of PCDD/Fs in 36 composite samples of foodstuffs randomly acquired in 2002 in Tarragona County (Catalonia). Edible marine species included hake, whiting blue, bass, angler fish, mussel, prawn, sardine, tuna and salmon (Bocio and Domingo, 2005). The mean PCDD/F concentrations were 3.7 and 11.6 pg/g lipid weight in fish and other seafood, respectively. Marine species was the food group showing the highest contribution to total dietary intake of PCDD/Fs (63.8 pg WHO-TEQ/day for a person of 70 kg body weight), 33.7%. In a recent study, we determined the levels of PCDD/Fs and PCBs in 14 edible marine species randomly purchased in various cities of Catalonia. Fish and seafood consisted of the following species: sardine, tuna, anchovy, mackerel, swordfish, salmon, hake, red mullet, sole, cuttlefish, squid, clam, mussel, and shrimp. The highest PCDD/F and PCB (11 congeners) levels were found in red mullet (10.28 pg/g ww and 88.10 ng/g ww, respectively), whereas the lowest levels of these pollutants were noted in cuttlefish (PCDD/Fs, 0.64 pg/g ww) and shrimp (PCBs, 0.46 pg/g ww). For an adult man (70 kg body weight), the intake of PCDD/Fs plus dioxin-like PCBs through fish and other seafood was estimated to be 38.0 pg WHO-TEQ/day (Bocio et al., 2007).
401
3. North American studies The most relevant results concerning the North American studies here reviewed, as well those of the Asian and African reports are summarized in Table 2. Jensen and Bolger (2001) conducted a survey of commercial fish and shellfish to obtain data on PCDD/F intake in the USA. Shrimp, cod, blue crab and oysters were included as marine species consumed in the greatest amounts, while catfish was also sampled because it was the dominant aquaculture species. Samples were collected in 1995–1996. Mean concentrations for fish (not catfish), molusks, crustacean, shrimp and catfish were 4.51 × 10− 4, 0.44, 0.35, 0.003 and 2.08 pg WHO-TEQ/g ww, respectively, when ND was assumed to be zero (ND = 0), while when ND was assumed to be equal to the LOD (ND = LOD) the mean levels corresponding to the same species were, respectively, 0.29, 0.46, 0.37, 0.15 and 2.10 pg WHO-TEQ. The bounds of mean PCDD/F intakes (pg WHO-TEQ/person/day) ranged from 0.09 (ND = 0)–4.5(ND = LOD) for shrimp to 148(ND = 0)–150 (ND = LOD) for catfish. In 1998, the FDA annual collection of food samples included, among other food groups, samples of various fish (aquacultured salmon, wild caught salmon, stripped bass, pollack) and shellfish (scallops, lobster, blue crab, crawfish). The levels of PCDD/Fs in the samples were simultaneously analyzed by high resolution mass spectrometry (HRMS) and by quadrupole ion storage tandem mass spectrometry (QISTMS) (Hayward et al., 2001). Using HRMS, I-TEQ values for s. bass, salmon and crab were respectively, 1.9, 0.73 and 1.05 ng/kg ww, whereas the levels of s. bass, salmon and lobster were 1.8, 1.02 and 0.61 ng I-TEQ ww, respectively, when QISTMS was used. The I-TEQ for mean PCDD/F levels in the 40 fish and shellfish samples measured by HRMS were 1.4 ng I-TEQ/kg ww. Recently, Hayward et al. (in press) reported the levels of PCDD/ Fs and PCBs in commercially wild caught and farm-raised fish (bluefish, “rockfish”, wild caught Alaska King, Sockeye and Coho salmon, and farm-raised salmon) fillets purchased from markets in Maryland, Washington, DC, and North Carolina during April–August 2004. The highest and lowest PCB concentrations were found in a wild bluefish fillet (800 ng/g ww) and in a wild Coho salmon fillet (0.35 ng/g ww), respectively. The levels of PCDD/Fs ranged from 0.07(rockfish) to 27 (bluefish) pg WHO-TEQ/g ww. The concentrations of 14 organochlorine contaminants including PCDD/Fs and PCBs and those of 14 polybrominated diphenyl ether flame retardant congeners were determined in farmed salmon obtained from farms in eight major salmon farming regions of the world, samples of five species of wild Pacific salmon, and retail market samples of farmed salmon obtained in 16 cities in Europe and North America (Hites et al., 2004a,b). PCDD/F and PCB levels in salmon showed notable differences depending on the respective origin. Thus, farmed salmon had significantly higher contaminant burdens than wild salmon, whereas farmed salmons from Europe were significantly more contaminated than those from South and North America (Hites et al., 2004a). When a benefit-risk analysis was conducted to compare quantitatively the cancer and noncancer
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Table 2 A summary of recent literature data concerning levels of PCDD/Fs and PCBs in edible marine species and human dietary intake Sampling site
Species analyzed
Levels of PCDD/Fs and/or PCBs
Comments and remarks
References
USA
Shrimp, cod, blue crab, oysters, catfish
PCDD/F levels only
Jensen and Bolger (2001)
USA
Atlantic and Pacific salmon
California coast, USA
Samples of a variety of fish
Dioxin and PCB levels were higher in European farm-raised salmon than in that from North and South America PCDD/Fs; mean I-TEQ for all species: 33.1 pg/g lipid PCBs (3 coplanar congeners); mean I-TEQ for all species: 109 pg/g lipid PCBs; highest value in a wild bluefish fillet, 800 ng/g ww; lowest level in wild Coho salmon fillet, 0.35 ng/g ww PCDD/Fs and PCBs; geometric means WHO-TEQ (pg/g whole weight) ranged from 0.06 (shrimp) to 0.92 (salmon) PCBs; range: from 0.20 (shrimp and mussel) to 2.5 (mackerel) ng/g ww PCDD/Fs and PCBs (pg WHO-TEQ/g lipid weight); bivalves (0.016–27 and 0.07–7.71), gastropods (0.05–44 and 0.53–7.9) PCBs; average concentration: 3.60 ng/g ww; highest and lowest values (ng/g ww): 8.04 (flounder) and 0.83 (cuttlefish) PCDD/Fs and dioxin-like PCBs; total concentration: 0.91 pg WHO-TEQ/g PCBs (22 congeners); mean concentrations (ng/g ww): sport fish, 23.0; market fish, 8.91 PCDD/Fs; 0.02–4.39 pg WHOTEQ/g ww Dioxin-like PCBs; 0.008–0.6 pg WHO-TEQ/g ww Concentrations, not reported
PCDD/F intake: 0.09–4.5 and 140–150 pg/person/day for shrimp and catfish, respectively Most farmed salmon should be consumed at rates of b10 meals/month No information on human exposure
Brown et al. (2006)
No information on human exposure
Hayward et al. (in press)
No information on human exposure
Rawn et al. (2006)
No information on human exposure No information on human exposure
Nakata et al. (2002) Zhao et al. (2005)
Estimated intake of PCBs through fish and shellfish: 1.83 ng/kg body weight
Yang et al. (2006)
Intakes (pg WHO-TEQ/day): PCDDs, 5.13, PCDFs, 8.45, dioxin-like PCBs, 50.20 Intake of sport and marked fish exceeded the risk-based screening value based on US EPA method Intakes (pg WHO-TEQ/kg body weight/day): PCDDs, 0.10, PCDFs, 0.18, dioxin-like PCBs, 0.40 A significant positive multivariateadjusted association was identified between serum PCDD/F levels and marine fish intake for persons N45 years No information on human exposure
Sasamoto et al. (2006)
Maryland, Washington, Wild caught and farm-raised DC; North fish fillets Carolina (USA) Canada Fish products from the Canadian retail market
China
Various fish and seafood
Bohai Sea coastline, China
Bivalves and gastropods
China
Fish and shellfish purchased from supermarkets in 3 cities
Tokyo, Japan
Fish and shellfish; total diet study
Korean coastal waters
Sport and market fish
Korean coastal waters
40 species of marine organisms (fish, crustaceans, cephalopods, bivalves, gastropods) Various fish species and fish viscera, shellfish, octopus, shrimp
Taiwan
Ismailia city, Egypt
Mullet fish, bolti fish, bivalves and crab
PCDD/Fs: 0.12–0.40 pg WHOTEQ/g ww Dioxin-like PCBs: 0.14–0.76 pg WHO-TEQ/ww Upper bound levels
Hites et al. (2004a), Foran et al. (2005)
Yim et al. (2005)
Moon and Ok (2006) Chen et al. (2007)
Loufty et al. (2007)
North American, Asian and African studies (2001–2006).
risks of exposure to organic contaminants in salmon with the omega-3 fatty acid-associated health benefits of salmon consumption, it was suggested that the risk of exposure to contaminants in farmed and wild salmon would be partially offset by the associated health benefits (Foran et al., 2005). However, for the specific case of farmed salmon from northern Europe, the advice was not consuming more than three meals per month (Huang et al., 2006). Recently, Brown et al. (2006) measured the levels of PCDD/ Fs and coplanar PCBs in 65 samples of a variety of fish collected from California coastal waters in 2000–2001. For all species from all sampling areas, the mean I-TEQ was 33.1 pg/g lipid for PCDD/Fs and 109 pg/g lipid for the 3 coplanar PCBs (77, 126, 169). In turn, Rawn et al. (2006) also analyzed the
levels of PCDD/Fs and PCBs in fish products available on the Canadian retail market in 2002. The geometric means WHOTEQ (pg/g whole weight) ranged from 0.06 (shrimp) and 0.08 (tilapia), to 0.92 (salmon). 4. Asian studies Nakata et al. (2002) investigated the residue levels of various pollutants in foodstuffs (including fish and seafood) collected in China in 2000–2001. PCBs were also determined. Relatively high PCB concentrations were found in fish and other seafood, in the range of 0.20 (shrimp and mussel) to 2.5 (mackerel) ng/g ww. Also in China, the levels of PCDD/Fs and PCBs were recently determined in various species of bivalves and
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gastropods (which are routine seafood for most Chinese people) collected in eight sampling sites along Bohai Sea coastline (NE China) (Zhao et al., 2005). For dioxin-like PCBs, WHO-TEQs ranged between 0.87 and 7.71 pg/g lipid weight for bivalves, and between 0.53 and 7.9 pg/g lw for gastropods, while for PCDD/Fs, WHO-TEQs oscillated between 0.016–27 and 0.05– 44 pg/g lw, for bivalves and gastropods, respectively. In a recent survey, Yang and co-workers (2006) analyzed the concentrations of PCBs and organochlorine pesticides in a wide variety of fish and shellfish collected from local supermarkets from three Chinese cities (Dalian, Tianjin and Shangai). In most samples, PCBs 138 and 153 were dominant, followed by PCBs 101 and 180. The average PCB concentration was 3.60 ng/g ww, with the highest values corresponding to flathead flounder (8.04 ng/g ww) and white sardine from Shangai (5.60 ng/g ww), and the lowest to Pacific cuttlefish (0.83 ng/g ww) and white sardine from Dalian (1.11 ng/g ww). The estimated daily intake of PCBs through fish and shellfish, considering a body weight of 60 kg and an average consumption of 30.5 g/person/day, was 1.83 ng/kg body weight. Recently, Sasamoto et al. (2006) estimated the dietary daily intake of PCDD/Fs and dioxin-like PCBs by a total diet study in metropolitan Tokyo, Japan, between 1999 and 2004. Fourteen food groups (including fish and shellfish) were analyzed. Total WHO-TEQ concentrations of PCDD/Fs and dioxin-like PCBs in fish and shellfish ranged from 0.98 to 0.91 pg WHO-TEQ/g in 1999 and 2004, respectively. PCB 126, followed by PCB 118, was the highest contributing congener, and accounted for over 40% of the daily intake of PCDD/Fs and PCBs from fish and shellfish. In 2004, intake of PCDDs, PCDFs, and dioxinlike PCBs from fish and shellfish were found to be 5.13, 8.45 and 50.20 pg WHO-TEQ/day, respectively. In relation to the total dietary intake of all food groups, these amounts mean percentages of 59%, 66% and 90%. In a recent study, Tsukino et al. (2006) determined background serum levels of PCDD/Fs and PCBs in Japanese infertile women in order to estimate the effect of lifestyle factors, especially dietary factors, on serum levels of these pollutants. The authors found that fish consumption was positively associated with serum levels of total TEQ (PCDD/Fs and PCBs) in Japanese infertile women. Yim et al. (2005) determined the levels of 22 PCB congeners in the muscles of sport and market fish to assess the potential risks to humans consuming fish originating in Korea's coastal waters. Mean (and range) concentrations of sport and market fish were 23.0 (4.48–95.6) and 8.91 (2.96–68.2) ng/g ww, respectively. Total PCB concentrations in all sport and marked fish exceeded the risk-based screening value (SV) based on US EPA method (5.04 ng/g based on total PCBs). Moon and Ok (2006) reported the concentrations of PCDD/Fs and dioxin-like PCBs in 40 species of marine organisms from Korean coastal waters. PCDD/F levels varied from 0.02 to 4.39 pg WHO-TEQ/ g ww and the dioxin-like PCB concentrations varied from 0.008 to 0.6 pg WHO-TEQ/g ww. Comparing organism groups, the highest pollutant concentrations were recorded in crustaceans, followed by fish, cephalopods, bivalves and gastropods. The estimated intakes of PCDDs, PCDFs and dioxin-like PCBs were 0.10, 0.18 and 0.40 pg WHO-TEQ/kg body weight/day,
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respectively. These values include the five fish and seafood groups evaluated. The contribution of dioxin-like PCBs to total intake from all organisms (0.68 pg WHO-TEQ/kg body weight/ day) averaged 60%, being the relative contribution of each organism group in descending order: fish, crustaceans, cephalopods, bivalves and gastropods. In a recent study, Chen et al. (2007) examined whether different dietary patterns and body fat content were associated with serum PCDD/F concentrations for different age groups of Taiwanese subjects. For the group of N 45 years, a significant positive multivariate-adjusted association was identified between serum PCDD/F levels and fish intake. Although various marine fish species (including viscera), shellfish, octopus and shrimp were included in the study, the levels of PCDD/Fs were not reported. 5. African studies Recently, Loufty et al. (2007) determined the concentrations of PCDD/Fs and dioxin-like PCBs in samples of fish and seafood (mullet fish, bolti fish, bivalves and crab) randomly acquired in local markets from Ismailia city, Egypt. The upper bound levels for PCDD/Fs and dioxin-like PCBs ranged from 0.12 (crab) to 0.40 (mullet) pg WHO-TEQ/g ww, and from 0.14 (bivalves) to 0.76 (mullet) pg WHO-TEQ/g ww, respectively. For PCDD/Fs, these values are lower than the current EU limit. In a another study of the same research group, it was observed that in Egypt, fish and seafood play a less important role than cereals and vegetables/fruits (Loufty et al., 2006). 6. Conclusions The review of a considerable number of international surveys shows that the comparison among results is rather complicated. While PCDD/Fs and PCBs bioaccumulate in marine species, depending basically on the environment in which the respective species are caught, their levels increase with the age of the fish. For PCBs, an additional difficulty for comparison of results is the great variety of congeners that have been analyzed in the different surveys. Other differences concern the expression of the results: wet weight, dry weight, or lipid weight. Finally, some investigators report their results concerning only some parts of the fish samples: muscle, liver, skin, etc., while other researchers have even evaluated the effects of cooking on the loss of POPs (Bayen et al., 2005). All these circumstances, together with the different units used to report the concentrations of PCDD/Fs and PCBs in the reviewed studies (I-TEQ, WHO-TEQ, CALUX-TEQ), make still more complicated the comparison of the different data. The studies here reviewed shows that some groups of population frequently consuming high quantities of certain fish species could be significantly increasing their health risks due to PCCD/F and PCB intake. Exposure to toxic pollutants through the diet depends on two main factors: 1) the levels of the respective pollutant in the food items consumed, fish and seafood in the present case, and 2) the average amount of the item (fish and seafood) daily/weekly/monthly consumed
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specifically by each subject, or the average consumption for a specific group of population. To give an easy response to this rather complicated issue, we recently determined the levels of a number of metals and organic pollutants (including PCDD/Fs and dioxin-like compounds) in 14 widely consumed fish species (Bocio et al., 2007; Domingo et al., in pressa). To balance the health risks derived from this fish consumption with the potential benefits derived from polyunsaturated omega-3 fatty acid (PUFA) intake, the levels of 2 PUFAs were also determined (Domingo et al., in pressa). All these results were used as the basis to prepare a program, RIBEPEIX, that can be freely consulted in Internet at http://www.fmcs.urv.cat/portada/ribepeix/ (Domingo et al., in pressb). The fish species, the frequency of consumption, and the meal size are essential issues for an adequate balance of the health benefits and risks of a regular fish intake. In relation to it, RIBEPEIX allows, according to the specific consumption habits, to optimize individually the balance between health benefits (omega-3) and risks (chemical contaminants) of fish consumption. However, general recommendations about fish consumption should be done taking into account the data concerning levels of environmental pollutants in the most consumed marine species in each specific region or country. Acknowledgment This study was supported by the Catalan Food Safety Agency, Generalitat de Catalunya, Spain. References Baars AJ, Bakker MI, Baumann RA, Boon PE, Freijer JI, Hoogenboom LAP, et al. Dioxins, dioxin-like PCBs and non-dioxin-like PCBs in foodstuffs: occurrence and dietary intake in the Netherlands. Toxicol Lett 2004;151:51–61. Bayarri S, Baldassarri LT, Iacovella N, Ferrara F, Di Domenico A. PCDDs, PCDFs, PCBs and DDE in edible marine species from the Adriatic Sea. Chemosphere 2001;43:601–10. Bayen S, Barlow P, Lee HK, Obbard JP. Effect of cooking on the loss of persistent organic pollutants from salmon. J Toxicol Environ Health, Part A 2005;68:253–65. Binelli A, Provini A. POPs in edible clams from different Italian and European markets and possible human health risk. Mar Pollut Bull 2003;46:879–86. 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. Bocio A, Domingo JL, Falcó G, Llobet JM. Concentrations of PCDD/PCDFs and PCBs in fish and seafood from the Catalan (Spain) market. Environ Int 2007;33:170–5. Bordajandi LR, Gómez G, Abad E, Rivera J, Fernandez-Baston MM, Blasco J, et al. Survey of persistent organochlorine contaminants (PCBs, PCDD/Fs, and PAHs), heavy metals (Cu, Cd, Zn, Pb, and Hg), and arsenic in food samples from Huelva (Spain): levels and health implications. J Agric Food Chem 2004;52:992–1001. Bordajandi LR, Martín I, Abad E, Rivera J, González MJ. Organochlorine compounds (PCBs, PCDDS and PCDFs) in seafish and seafood from the Spanish Atlantic Southwest coast. Chemosphere 2006;64:1450–7. Brown FR, Winkler J, Visita P, Dhaliwal J, Petreas M. Levels of PBDEs, PCDDs, PCDFs, and coplanar PCBs in edible fish from California coastal waters. Chemosphere 2006;64:276–86.
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