Original Article
Exposure to Dioxins and Dibenzofurans through the Consumption of Fish
N Engl J Med 1991; 324:8-12January 3, 1991
- Abstract
- Abstract
Background.
In some regions, including the Baltic Sea, fatty fish such as salmon and herring contain high levels of polychlorinated dibenzodioxins and dibenzofurans. We investigated human exposure to these potentially toxic substances in relation to the consumption of fish from the Baltic Sea.
Methods.
Plasma levels of 10 different dibenzofurans and 7 dioxins were analyzed in three groups of Swedish men: one group with a high intake of fish (fish eaten almost daily; n = 11), one with a moderate intake of fish (about once per week; n = 9), and one with no consumption of fish (usually because of allergy; n = 9).
Results.
Plasma levels of several of the compounds we measured were higher in the men with a high intake of fish than in those who consumed moderate amounts, and the levels were higher in those who ate moderate amounts of fish than in those who ate none. The median amounts of the most toxic dioxin (2,3,7,8-tetrachlorodibenzo-p-dioxin) were 8.0 pg per gram of plasma lipid (range, 2.0 to 13) in the high-intake group, 2.6 pg per gram (range, 1.2 to 4.2) in the moderate-intake group, and 1.8 pg per gram (range, 1.0 to 2.5) in the nonconsumers (P = 0.001 and 0.02, respectively). There were consistent and statistically significant associations between the reported amount of fish eaten and the plasma levels of several of the dibenzofurans and dioxins.
Conclusions.
Contaminated fish such as those from the Baltic Sea are an important source of exposure to polychlorinated dibenzofurans and dibenzodioxins in persons who eat fish regularly. However, the clinical consequences of such exposure remain uncertain. (N Engl J Med 1991;324:8–12.)
Media in This Article
Figure 1
Mean Levels (and Ranges) of PCDFs and PCDDs in Plasma of Subjects Consuming Various Amounts of Fish.Figure 2
Plasma Lipid Levels of 2,3,7,8-TCDD, According to Intake of Fish in 29 Subjects.Article Activity
- Article
HUMAN exposure to polychlorinated dibenzo-p-dioxins (PCDDs) and polychlorinated dibenzofurans (PCDFs) is a matter of great concern in many parts of the world. Some of these compounds are the most toxic manufactured chemicals known, at least in some species.1 , 2 Exposure may occur in occupational settings,3 particularly in industrial accidents such as fires in electrical transformers and capacitors containing polychlorinated biphenyls and accidental emissions, like the fire in Seveso, Italy, in 1976.1 Moreover, the defoliant Agent Orange, used during the Vietnamese War, caused exposure to one of the dioxins in particular: 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD), which was present as a contaminant.4
Available data indicate that some exposure occurs in the general population.2 Fatty fish such as herring and salmon from the Baltic Sea have been found to contain high levels of some PCDDs and PCDFs.5 Similar concentrations of TCDD have been detected in fish from the Great Lakes.6 Consumption of fish has previously been shown to be a major source of other organochlorine compounds.7 , 8
We report here data on PCDD and PCDF levels in plasma from subjects with various patterns of fish consumption.
Methods
Study Groups
Twenty-nine men from southeastern Sweden were studied. Nine of them (the nonconsumers) never ate fish. Nine subjects (the moderate-intake group) ate the amount average for Sweden, with about one meal of fish per week. Eleven subjects (the high-intake group) were fishermen or workers in the fish industry and consumed a great deal of fish, mainly salmon and herring caught in the Baltic Sea. They ate fish almost every day. The men in the moderate- and high-intake groups generally obtained their fish from the same sources and cooked and prepared them in similar ways.
The nonconsumers and the men in the high-intake group were recruited nonrandomly through the publication of general information about the study in local newspapers and other sources. The moderate-intake group was drawn from a previously described population9 for which we had information on fish consumption.
All the subjects were healthy according to history, physical examination, and laboratory screening, except that some of the nonconsumers were allergic to fish. None of the subjects had handled herbicides or pesticides. They were interviewed thoroughly about their intake of foodstuffs and about other relevant features of their lifestyles (Table 1Table 1
Characteristics of the Three Study Groups.*). The amount of fish consumed per week was calculated for each man from the reported number and size of the portions eaten. Informed consent was obtained from all the subjects, and the design of the study was approved by the ethics committee of the medical faculty of Lund University.Analysis of Blood Samples
Blood samples were drawn after the subjects had followed a 24-hour diet that was restricted in fat. For the determination of PCDD and PCDF levels, 420 ml of venous blood from each subject was drawn into standard hospital blood bags (Travenol). Plasma was separated with use of the standard procedure for the citrate—phosphate—dextrose Sagman system. The plasma bags were coded and immediately frozen and stored at -20°C. In addition, venous blood was drawn into tubes, centrifuged, and frozen for analysis of levels of fatty acids. All samples were coded before they were shipped to the analyzing laboratory, and the code was broken only after the results had been reported.
A previously described method of measuring PCDFs and PCDDs was used.10 The procedure involved extraction with organic solvents, multiple cleanup with various absorbents, and finally, detection and quantification by multiple-ion-mode high-resolution gas chromatography and high-resolution mass spectrometry. This method has been found to have a limit of detection of 0.003 to 0.02 ppt (whole-blood weight), depending on the isomer studied, and has been evaluated in a quality-control study measuring levels of polychlorinated biphenyls, PCDDs, and PCDFs in human milk and blood organized by the World Health Organization11 and involving 19 laboratories in all parts of the world. For PCDDs and PCDFs in blood, our laboratory had an average coefficient of variation for reproducibility and repeatability of 6.7 percent. (Laboratories with a mean coefficient of variation of more than 45 percent were not regarded as qualified.)
For the PCDDs and PCDFs analyzed, TCDD equivalents were calculated according to a model proposed by a Nordic expert group,12 which is one of several existing models for risk assessment in persons exposed to complex mixtures of PCDDs and PCDFs. In the model, the toxicity of different congeners is related to that of TCDD, the most studied toxin. The scientific basis for the Nordic model is "best available data" from studies on long-term effects in animals (carcinogenic effects and adverse effects on reproduction). Because of a lack of reliable data on toxicity, it is not possible to use this or any other model to predict health effects in humans more precisely, but it is still useful in evaluating potential risk to human health.
The fatty-acid composition of serum phosphatidylcholine was determined by capillary gas chromatography, as described elsewhere.13
Results
There was a pronounced difference in the levels of many PCDFs and PCDDs in the three study groups (Fig. 1Figure 1
Mean Levels (and Ranges) of PCDFs and PCDDs in Plasma of Subjects Consuming Various Amounts of Fish.). This was particularly apparent for one of the pentachlorodibenzofurans (2,3,4,7,8-pentachlorodibenzofuran), for TCDD, and consequently for TCDD equivalents. There were also differences in 1,2,3,7,8 - pentachlorodibenzofuran values, although this congener was found at very low levels. For the two pentachlorodibenzofurans, the levels in the high-intake group (1.3 and 79 pg per gram of fat) were no less than nine and six times higher, respectively, than in the nonconsumers (0.15 and 12 pg per gram of fat), and for TCDD equivalents there was an approximately threefold difference. For most of the higher chlorinated congeners there were no differences between the groups (Table 2Table 2
Mean Levels of PCDFs and PCDDs in Plasma and of Polyunsaturated Fatty Acids in Serum Phosphatidylcholine in the Study Subjects.). 1,2,3,7,8,9-Hexachlorodibenzofuran and 1,2,3,4,7,8,9-heptachlorodibenzofuran were both below the limits of detection (<1 pg per gram of fat).There were significant associations between the total amount of fish consumed and the levels of several PCDFs and PCDDs (especially 1,2,3,7,8-pentachlorodibenzofuran, 2,3,4,7,8-pentachlorodibenzofuran, TCDD, 1,2,3,7,8-pentachlorodibenzodioxin, and TCDD equivalents) (Fig. 2Figure 2
Plasma Lipid Levels of 2,3,7,8-TCDD, According to Intake of Fish in 29 Subjects.), and the explained variances (R2 by simple regression analysis) were above 60 percent for these congeners. Similar associations were found when the intake of fatty fish was used as the independent variable. The study groups had significant differences in levels of several of the n—3 polyunsaturated fatty acids (Table 2). The n —3 polyunsaturated fatty acids in serum phosphatidylcholine had a strong association with fish intake. Consequently, the levels of n—3 polyunsaturated fatty acids correlated closely with those of several of the PCDFs (Fig. 3Figure 3
Plasma Lipid Levels of 2,3,4,7,8-Pentachlorodibenzofuran (PeCDF), According to Serum Levels of n-3 Polyunsaturated Fatty Acids in 29 Subjects.) and PCDDs and with TCDD equivalents (r = 0.81, P = 0.0001).In the subjects as a whole, the intake of milk fat correlated positively with some of the higher chlorinated congeners, although these congeners were present at levels close to the threshold of detection. There were associations between age and serum levels of some of the tetra, penta, and hexa congeners of PCDFs and PCDDs. A multivariate model, including age and the intake of fish and milk fat, explained much of the variance (R2, 55 to 74 percent) for the tetra and penta congeners of PCDFs and PCDDs.
Discussion
Our data show a clear association between the intake of fish and plasma levels of several PCDFs and PCDDs. The association is underlined by the close relation between levels of n—3 polyunsaturated fatty acids, which have their main dietary origin in fish, and several of the PCDFs and PCDDs. The fish consumed was mainly caught in the Baltic Sea, where some species have high levels of PCDFs and PCDDs. Thus, composite samples of Baltic herring have about 8 to 18 pg of TCDD equivalents per gram of whole fish, as compared with 2 to 3 pg per gram in herring from the less polluted west coast of Sweden.14 Wild salmon from the Baltic Sea have 30 to 90 pg of TCDD equivalents per gram, whereas hatchery salmon from the same area have 3 to 4 pg per gram.5 A survey measuring the contamination of fish with TCDD in major watersheds in the United States has been conducted by the U.S. Environmental Protection Agency. In 10 percent of the samples the level of this single congener was higher than 5 pg per gram; 85 pg per gram was the highest level recorded.6
Among the different congeners, 2,3,4,7,8-pentachlorodibenzofuran is the most prevalent in Baltic herring and salmon samples.5 The differences between study groups were particularly marked with respect to this compound. Dairy products also contain PCDFs and PCDDs. Levels corresponding to 1.5 pg of TCDD equivalents per gram of fat have been estimated in Swedish milk products.15 The exposure to PCDFs and PCDDs from fish, even in the moderate-intake group, was considerably higher than from milk fat, however. Accordingly, the influence of the intake of milk fat on serum levels of PCDFs and PCDDs was obscured in the study groups that ate fish, but it was seen among the subjects who never ate fish.
Our results thus indicate that fish is a major source of exposure to PCDFs and PCDDs in the general population consuming fish from the Baltic Sea. The situation could be quite different in other countries, however, where the consumption of fish is lower but the level of contamination in milk is higher.16 There are only limited reports on levels of PCDFs and PCDDs in human blood,4 , 17 and these mostly concern TCDD, the most toxic of the congeners. The levels of this compound in the high-intake group in our study were higher than those reported earlier in Swedes,10 , 18 Americans,4 and Germans19 with no occupational or accidental exposure, whereas the levels in our groups that consumed less fish were comparable or lower. In addition, our high-intake group had higher levels than Swedes with potential occupational exposure.18 , 20 Workers from Missouri engaged in the production of 2,4,5-trichlorophenol, in which TCDD was generated as an unintended contaminant, had an average serum level more than 25 times higher than the highest level (13 pg per gram) observed in our study.17 Vietnam veterans in the United States who had been engaged in the handling and spraying of Agent Orange about 20 years before being studied had 46 pg per gram of fat (mean value in nine subjects studied).4 PCDFs and PCDDs have usually been measured in adipose tissue. Expressed per unit of lipid, levels in adipose tissue are similar to those in plasma.4 , 17
In addition to high levels of TCDD, the consumers of fish in our study had even higher levels of several other congeners. Of particular interest is 2,3,4,7,8-pentachlorodibenzofuran, which was associated with food poisoning in Japan (yusho)21 and Taiwan (yuchen).22 Thus, the total amounts of PCDFs and PCDDs in blood, expressed as TCDD equivalents, were considerably higher than the amount of TCDD alone, and were similar to those found in nine Vietnam veterans exposed to Agent Orange.10 It should be stressed that the toxicologic importance of the equivalent levels in blood is not clear. The levels reported in occupationally or accidentally exposed subjects reflect exposures of limited duration, however, often a very short time. Exposure through food, as in the present study, is often lifelong and, because of the long half-lives of some of the congeners, results in accumulation for decades. This is probably the reason for the positive correlation between age and the levels of some congeners. A corresponding age effect has been noted for TCDD23 and polychlorinated biphenyls.8
PCDFs and PCDDs, although potent, are but a few of the members of a family of related halogenated compounds. Others have similar but less potent toxicologic effects. Several of these compounds (polychlorinated biphenyls and polychlorinated naphthalenes) have been found as pollutants in fish from the Baltic Sea at higher concentrations than PCDFs and PCDDs.24 The compounds we studied may thus represent only a small part of the problem. A complete evaluation of the health risks involved in the consumption of contaminated fish must take into account the whole group of chlorinated compounds.
Since the polychlorinated compounds are excreted in breast milk,25 it is likely that infants breast-fed by mothers who have consumed contaminated fish constitute the most heavily exposed population.
What is the importance to health of the exposure? TCDD is the most extensively studied PCDD. In animals it is an immunosuppressant, a carcinogen, and a teratogen.2 Data from epidemiologic studies in humans are not conclusive. Very little is known about the health effects in humans of the degree of exposure studied here. It is noteworthy, however, that the consumption of fish contaminated with polychlorinated biphenyls (and presumably other related compounds as well) has been claimed to be associated with teratogenic effects in humans.26 On the other hand, the beneficial effects of fish consumption in the prevention of cardiovascular disease have been widely accepted.27 , 28 On balance, the present findings probably do not warrant restrictions on the consumption of fish. However, the fact that persistent, toxic substances can be found in humans as the result of food contamination underscores the need to identify all sources of PCDFs, PCDDs, and other halogenated aromatic hydrocarbons in the environment and limit exposure to them if possible.
Supported by a grant from the Swedish Environmental Protection Agency.
We are indebted to Dr. Åke Björnham of the Blekinge County council and the staffs of the blood-donation centers at the hospitals of Visby, Karlshamn, Simrishamn, Lund, and Helsingborg, Sweden.
Source Information
From the Department of Occupational and Environmental Medicine, University Hospital, Lund (B.-G.S., A.N., S.S.), the Institute of Environmental Chemistry, University of Umeå, Umeå (M.H., C.R.), and the Department of Medical and Physiological Chemistry, University of Lund, Lund (B.Å.), all in Sweden. Address reprint requests to Dr. Svensson at the Department of Occupational and Environmental Medicine, University Hospital, S-221 85 Lund, Sweden.
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