As a result of the Belgian crisis in 1999, during which food contaminated by polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzofurans (PCDFs) and dioxin-like polychlorinated biphenyls (DL-PCBs) was found in that country and almost all over Europe, the European Union adopted a strategy to reduce the levels of these toxic compounds in the environment and food and to reduce consumer exposure to them (3). Thus, in 2001–2002 a level representing the safe weekly human dose of PCDDs, PCDFs, and DL-PCBs, designated the tolerable weekly intake (TWI), was established at 14 pg WHO-(TEQ) kg−1 b.w., as was the provisional tolerable monthly intake (PTMI) at 70 pg WHO-TEQ kg−1 b.w. Since that time, new evidence of dioxins’ toxicity has come to light and therefore in November 2018 the European Food Safety Authority decided to reduce the TWI by a factor of seven (7). Studies show that food, including fish, is a major source (>90%) of dioxins and PCBs for humans (7). Dietary recommendations include eating fish at least twice a week because of the valuable nutrients it contains (11). The most important are long-chain polyunsaturated fatty acids, macro- and trace elements, fat-soluble vitamins (mainly D3), amino acids, and easily absorbed proteins. Unfortunately, fish living in a polluted environment or sustained by contaminated feeds may accumulate toxic compounds, which include PCDD/Fs and PCBs. The aim of the study was to assess the actual state of farmed fish contamination by PCDD/F/DL-PCBs and the related risk for fish consumers in relation to the newly established TWI.
Sampling points
Species | Sampling point (province, country) | Number of samples |
---|---|---|
eel | Warmian-Masuria, Greater Poland, Kuyavia-Pomerania, Pomerania, West Pomerania | 15 |
rainbow trout | Lower Silesia, Lublin, Lubuskie, Lesser Poland, Masovia, Opole, Podlasie, Silesia, Warmia-Masuria | 40 |
bream | West Pomerania, Lesser Poland, Warmia-Masuria, Greater Poland | 18 |
sturgeon | Lower Silesia, Lublin, Lubuskie, Lesser Poland, Masovia, Opole, Podlasie, Silesian, Warmia-Masuria | 15 |
carp | Lower Silesia, Lublin, Lubuskie, Lesser Poland, Masovia, Opole, Podlasie, Silesian, Warmia-Masuria | 42 |
zander | Subcarpathia, Lublin, Warmia-Masuria | 10 |
panga | Vietnam | 10 |
A DB-5 MS fused silica capillary column (60 m × 0.25 mm × 0.1 mm) was used with the splitless injection mode of 2 μL and helium as a carrier gas. The TEQ values were calculated using the WHO toxic equivalency factors established by Van den Berg (22). WHO-TEQs were expressed as upper-bound concentrations (all values of the specific PCDD/F and DL-PCB congeners below the limit of quantitation (LOQ) were equal to their respective LOQ). The LOQs for PCDD/F and DL-PCB were isomer-dependent and varied from 0.002 to 2.71 pg g−1 w.w. and for NDL-PCBs their spread was from 0.0004 to 0.022 ng g−1 w.w. The recoveries of the internal standards ranged between 60% and 120%. Positive electron ionisation (EI) operating in SIM mode at a resolution of 10,000 was employed.
Eels accumulated statistically significantly more dioxins and PCBs than the other species (Table 2). Nevertheless, eel muscles contained low levels in relation to the maximum limits (about 30% for the sum of dioxins and DL-PCBs and 13% for NDL-PCBs) (Table 2). Average concentrations of PCDD/F/DL-PCB in the less-polluted carp, trout, sturgeon, and bream were between 5% and 11% and NDL-PCB between 1% and 3% of the maximum levels. The least-polluted panga and zander accumulated PCDD/F/DL-PCB at the level of the LOQ and the mean concentration ranged from 0.6% to 0.8%; NDL-PCB concentration ranged from 0.08% to 0.6% of the maximum limits. Concentrations of PCDD/F/DL-PCB were higher in species of which the muscles contained more fat (Table 2). The exception was bream, which was on average half as fatty as sturgeon, but accumulated over 50% more PCDD/F/DL-PCBs.
PCDD/F, DL-PCB and NDL-PCB (x ± SD, range)
Species | Fat % | pg WHO-TEQg−1 w.w. | ng g−1 w.w. | ||||
---|---|---|---|---|---|---|---|
PCDD | PCDF | PCDD/F | DL–PCB | PCDD/F/DL-PCB | NDL-PCB | ||
eel | 18.63 ± 6.81 | 0.30 ± 0.14 | 0.18 ± 0.07 | 0.48 ± 0.21 | 1.52 ± 0.68 | 2.00 ± 0.85 | 9.98 ± 6.43 |
0.17–0.64 | 0.10–0.38 | 0.27–1.02 | 0.71–2.97 | 1.03–3.98 | 2.83–24.94 | ||
0.15 ± 0.07 | 0.19 ± 0.1 | 0.33 ± 0.14 | 0.37 ± 0.18 | 0.70 ± 0.23 | 1.53 ± 0.49 | ||
bream | 4.12 ± 0.8 | 0.09–0.26 | 0.06–0.34 | 0.20–0.58 | 0.20–0.67 | 0.45–1.01 | 0.60–1.96 |
0.10 ± 0.03 | 0.08 ± 0.03 | 0.18 ± 0.03 | 0.27 ± 0.22 | 0.45 ± 0.24 | 1.93 ± 0.55 | ||
sturgeon | 8.01 ± 4.16 | 0.09–0.14 | 0.05–0.13 | 0.13–0.21 | 0.17–0.67 | 0.31–0.88 | 1.16–2.4 |
0.09 ± 0.02 | 0.05 ± 0.03 | 0.14 ± 0.3 | 0.19 ± 0.4 | 0.33 ± 0.72 | 0.50 ± 1.67 | ||
carp | 6.01 ± 8.36 | 0.02–0.15 | 0.03–0.15 | 0.02–1.75 | 0.01–2.6 | 0.03–4.35 | 0.11–12.97 |
rainbow | 0.09 ± 0.0 | 0.05 ± 0.01 | 0.14 ± 0.01 | 0.20 ± 0.08 | 0.32 ± 0.08 | 1.80 ± 1.34 | |
trout | 5.51 ± 1.71 | 0.09–0.09 | 0.04–0.07 | 0.03–0.32 | 0.02–0.33 | 0.05–0.47 | 0.05–8.39 |
panga | 0.01 ± 0.0 | 0.01 ± 0.0 | 0.01 ± 0.0 | 0.01 ± 0.0 | 0.02 ± 0.0 | 0.06 ± 0.01 | |
0.93 ± 0.41 | 0.01–0.01 | 0.01–0.01 | 0.01–0.02 | 0.01–0.01 | 0.02–0.02 | 0.05–0.08 | |
zander | 0.01 ± 0.0 | 0.01 ± 0.0 | 0.01 ± 0.0 | 0.01 ± 0.0 | 0.03 ± 0.01 | 0.50 ± 0.67 | |
0.34 ± 0.05 | 0.01–0.01 | 0.01–0.01 | 0.01–0.01 | 0.01–0.02 | 0.02–0.04 | 0.11–2.97 | |
Maximum | levels (reference 4) | – | – | 3.5 | – | 6.5 | 75 |
Fig. 1 compares the percentage share of PCDD, PCDF, and DL-PCB congeners to the total toxicity (expressed in WHO-TEQ) of freshwater fish muscle. Bioaccumulations were species-dependent. DL-PCBs contributed the most to the total toxicity, from 52% in bream to over 76% in eel muscles. Dioxins contributed less than DL-PCBs but more than furans (from 15% in eels to 26% in trout) (Fig. 1). An exception to this trend was bream, because in their muscles furans accounted for 27% and dioxins for 21%. These differences may result from species specificity and environmental pollution or diet. As only one congener from the group of furans was detected in zander and panga muscles, this muscle tissue was not presented in Fig. 1.
Percentage share of PCDD, PCDF and DL–PCB in the total toxicity
The estimated dioxin and DL-PCB intake ranges from 9% to 866% TWI for children and from 4% to 286% TWI for adults (Table 3). Levels of dioxins and DL-PCBs found in panga and zander are low, not exceeding the LOQ level.
Estimated intake of PCDD/F and DL-PCB with 200 g of fish, expressed as % of TWI
Fish species | Children % TWI | Adult % TWI |
---|---|---|
eel | 866 | 286 |
bream | 303 | 100 |
sturgeon | 195 | 64 |
carp | 143 | 47 |
rainbow trout | 139 | 46 |
panga | 9 | 3 |
zander | 13 | 4 |
Taking into account that the results are expressed according to the upper-bound concept, which requires using the limit of quantification for the contribution of each non-quantified congener, the risk assessment results are clearly overestimated. Therefore, panga and zander muscle tissue can be regarded as practically “PCDD/F/DL-PCBs–free” and its consumption as having no significant impact on human health. However, regular consumption of some species (eel and bream) can pose a health risk and especially for vulnerable groups of consumers who frequently consume these species.
Fish farming can be carried out either in open tanks or in closed buildings with a water recirculation system, without contact with the external environment. The closed water recirculation system and isolation from the external environment is designed to eliminate diseases, but also can minimise dioxin and PCB contamination of fish. The quality of the feeds used in the feeding system is becoming important for the breeding process. Feed in Poland is subjected to annual control under the national feed quality monitoring programme (14). Low levels of dioxins and PCBs determined in farmed fish as well as the conducted feed control studies indicate that feed quality is good, and it does not represent a significant source of these contaminants for fish (14).
In the literature there are many papers devoted to farmed marine fish, mainly salmon. In salmon reared in northern Europe, North America, and Chile, levels of PCDD/F/DL-PCB were higher than those in free-living fish, which could indicate a significant impact of feed materials on fish contamination. Salmon reared in Europe were more contaminated than those from North and South America, with the highest levels having been found in salmon reared in Scotland and the Faroe Islands (10). Fish feed technology is based on the use of fish oil and fishmeal (9), both of which may contain dioxins and PCBs (15). Therefore, measures have been taken to replace fish oil with vegetable oil (12, 17). The result has been a decrease in the levels of dioxins and PCBs in Norwegian Atlantic salmon and those of North America and eastern Canada (12, 17). An alternative method of fishmeal decontamination is extraction of dioxins and PCBs with hexane. This method was positively assessed by the EFSA. The process allows for reduction of about 70% of PCDD/F/DL-PCBs and about 60% of NDL-PCBs and meets the requirements of the Regulation laying down criteria for the acceptability of detoxification processes for products intended for animal feed (5).
In a study conducted in Greece, PCDD/F concentrations in freshwater trout were about 7% lower, while DL-PCB concentrations were 65% higher than in this study (6). Low contamination of carp by NDL-PCBs (1.4 ng/g w.w.) and perch (1.14 ng/g w.w.) from farms in the Lorraine area in France was reported by Thomas
Concentrations of PCDD/F/DL-PCB are generally higher in species of which the muscles contain more fat. In our studies, bream was an exception, because its muscle was on average twice as lean as that of sturgeon, but accumulated over 50% more PCDD/F/DL-PCBs. This may be due to the type of feeding and diet, which consists of sucking of bottom sediments and filtering nutrients from them. Therefore, sediment contamination may have a greater impact on the levels of dioxins, furans and PCBs compared to other species.
The latest data provided by EFSA show that fish consumption results in a dioxin and DL-PCB intake of up to 26.3% and 56% for infants and adults, respectively (7). That is why the TWI value (14 pg WHO-TEQ kg−1 b.w. per week) established in 2001 was exceeded for part of the European population and in particular for children (1, 2). It is, therefore, important from the point of view of food safety to find out how decreasing the TWI to 2 pg WHO-TEQ kg−1 b.w. will influence the risk assessment results. The average, total fish and fish product monthly consumption in Poland is estimated at 0.29 kg per person (19). Such values suggest that the dietary intake of dioxins with fish and fishery products of Polish consumers is expected to be low. Taking into account the low national fish consumption, it seems that the problem does not apply to the general population. Occasionally, elevated dioxin intakes above TWI are not necessarily related to health risk because of uncertainty factors embedded in these toxicological reference values. However, vulnerable sub-populations that frequently consume eel, bream or sturgeon may be at elevated health risk due to potential consequences of chronic exposure to dioxins and DL-PCBs.