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Food and Chemical Toxicology 46 (2008) 1591–1595 www.elsevier.com/locate/foodchemtox
Contribution of fish consumption to heavy metals exposure in women of childbearing age from a Mediterranean country (Spain) M.A. Herreros a,*, S. In˜igo-Nun˜ez a, E. Sanchez-Perez a, T. Encinas b, A. Gonzalez-Bulnes b,c b
a Direccio´n General de Salud Pu´blica y Alimentacio´n, Comunidad de Madrid, 28220 Majadahonda, Madrid, Spain Dpto. Toxicologı´a y Farmacologı´a, Facultad de Veterinaria, Universidad Complutense de Madrid, 28040 Madrid, Spain c Dpto. Reproduccio´n Animal INIA, 28040 Madrid, Spain
Received 22 June 2007; accepted 30 December 2007
Abstract The concentrations of cadmium (Cd), lead (Pb) and mercury (Hg) were determined in samples from sword-fish (Xiphias gladius, n = 37) and louvar (Luvarus imperialis, n = 17) taken in an official surveillance programme in Madrid (Spain). The levels of heavy metals were measured by atomic absorption spectrophotometry (hydride generator for Hg and flame atomic absorption for Cd and Pb) after digestion of the samples (microwave digestion for Hg and drying chamber for Cd and Pb). Pb contamination was negligible in both species. Cd was detected in 89.19% of the samples from sword-fish and 52.94% from louver; 17.65% of louvar and none from sword-fish being higher than maximum residue limits (MRL). However, around 90% of louvar samples and around 35% of sword-fish portions exceeded MRL for Hg; around 30% of louvar samples having levels even higher than 1 lg/g. The consumption of one serving of 150 g either of louvar or sword-fish would not be relevant for Cd and Pb provisional tolerable weekly intake (PTWI) of these elements for women in childbearing age, but it would largely exceed the tolerable values for Hg. Ó 2008 Elsevier Ltd. All rights reserved. Keywords: Cadmium; Lead; Mercury; Fish; Dietary intake; Spain
1. Introduction Heavy metals like cadmium (Cd), lead (Pb), and mercury (Hg) in its organic form (methylmercury, MeHg), are environmental contaminant of special concern due to its wide distribution and profound implications in human health (Clarkson and Magos, 2006; Islam et al., 2007; Mergler et al., 2007). These compounds are emitted to the environment by industrial activities, accumulating in water sediments of lakes and oceans and, thereafter, in aquatic organisms. Thus, human populations with consumption habits based on fish, seafood and sea mammals are specially exposed. Therefore, the Joint FAO/WHO Expert
*
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[email protected] (M.A. Herreros).
0278-6915/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.fct.2007.12.024
Committee on Food Additives (JECFA) established provisional tolerable weekly intakes (PTWI) for these elements; the limits being 7 lg/kg body weight for Cd (JECFA, 2004a), 25 lg/kg for Pb (JECFA, 2000), and 1.6 lg/kg for MeHg (JECFA, 2004b). Evidences for health effects – mainly neurological, cardiovascular and reproductive disorders – associated with exposure to these contaminants are increasing world-wide, as reported by European Food Safety Authority (EFSA) in 2004 (http://www.efsa.europa.eu/EFSA/News_PR/pr_risk_ mercury%20_fish.pdf). In adults, data from EFSA have related exposure to Cd and Pb to effects like neurotoxicity, nephrotoxicity, carcinogenicity and endocrine and reproductive failures (http://www.efsa.europa.eu/EFSA/ Scientific_Opinion/opinion_contam_01_en1,2.pdf). In these reports, Pb and MeHg have been also related to cardiovascular effects, and MeHg is also a neurological poison. However, effects from prenatal exposure in children are
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even more disturbing because of the high susceptibility of the developing tissues, higher than in adults. The intoxication with Cd in pregnant women has been related to reduced pregnancy length and newborn weight and, recently, to disorders of the endocrine and/or immune system in children (Schoeters et al., 2006). Pb exposure has been mainly related to retardation of neurobehavioral development (Lidsky and Schneider, 2003); like MeHg, which impairs neurodevelopment and causes effects ranging from fetal death to delayed development and cognitive changes (Castoldi et al., 2003). Currently, the European Union (EU) maximum residue limits (MRL) permitted in fish are 0.3 lg/g for Pb, 0.1–0.3 lg/g for Cd and 0.5– 1 lg/g wet weight for Hg, depending on the fish species (Commission Regulation, 1881/2006). Exposure to these metals depends on the diet habits and geographical location. High intakes of fish and seafood are traditional components of the diet in different human populations world-wide. Specifically, in the Mediterranean diet; fish eating being particularly high in Spain. A recent FAO report, released in May 2006 (The international fish trade and world fisheries, http://www.fao.org/newsroom/ common/ecg/1000301/en/enfactsheet2.pdf), estimated that Spanish fish consumption per capita is of about 45 kg per year; in the European Union is around 25.5 kg, and world-wide consumption is estimated at 16.5 kg. Spain is the third country, after Japan and Portugal, in fish consumption. Considering the quantity of fish, the city of Madrid is the second marketplace after Tokyo, and the first one if considering the diversity of species offered; large predatory species, like sword-fish (Xiphias gladius) and louvar (Luvarus imperialis), are traditionally demanded. Therefore, Madrid becomes a good model for evaluation of heavy metals contamination in predatory fishes. The objectives of current study were: (a) the evaluation of Cd, Pb and Hg contamination data in muscle samples of sword-fish and louvar from Madrid markets, and (b) the estimation of the contribution of fish consumption to heavy metals PTWI for women of childbearing age (from 25 to 44 years old). 2. Materials and methods
2.3. Provisional tolerably weekly intake estimation The provisional tolerable weekly intake (PTWI–JECFA) of Cd, Pb and MeHg was expressed in terms of lg per person for two groups of women in childbearing age, considering that women between 25 and 34 years old have a mean body weight of 57.4 kg and women with 35–44 years old have 60.4 kg (from anthropological data obtained from the Comunidad de Madrid).
2.4. Data analysis Mean Cd, Pb and Hg concentrations (mean ± S.E.M. in lg/g wet weight) were firstly considered. Samples were thereafter grouped in three concentration intervals; the first one included samples with values under the detection limit (
3. Results 3.1. Analysis of fish contamination and dietary exposure estimation for cadmium The presence of Cd was found in most of the samples analyzed (Table 1). The mean Cd level was established in 0.08 ± 0.01 lg/g wet weight, ranging from 0.02 to 0.25 lg/g. None of the samples from sword-fish exceeded the maximum residue level (MRL) fixed by the EC (0.3 lg/g). A 17.65% of the louvar samples had Cd levels higher than MRL (0.1 lg/g); however, none of them surpassed the MRL of 0.3 lg/g fixed by the EFSA for other large predatory species like sword-fish. Thereafter, the tolerable Cd intake for women of childbearing age was estimated in a range between 401.80 and 422.80 lg/week, considering the JECFA–PTWI and the regional mean body weights. Overall, one serving of 150 g, either of louvar or sword-fish, would contain a mean Cd concentration of 12 lg; which is around 3% of the PTWI for women in childbearing age.
2.1. Sampling In the framework of an official surveillance programme, 37 samples of edible parts of sword-fish (X. gladius) and 17 of louvar (L. imperialis) were taken in fish retailers from Madrid (Spain).
2.2. Analysis of fish contamination In order to evaluate the bioavailable concentration of heavy metals instead of total levels, the samples were digested (microwave digestion for Hg and drying chamber with temperature ramps up to 450 °C for Cd and Pb). Thereafter, concentrations of Cd, Pb and Hg (assuming that almost all is MeHg; Storelli et al., 2002, 2003a,b) were measured by atomic absorption spectrophotometry (hydride generator for Hg and flame atomic absorption for Cd and Pb). Detection limits were 0.02 lg/g for Cd, 0.1 lg/g for Pb and 0.05 lg/g for Hg.
3.2. Analysis of fish contamination and dietary exposure estimation for lead The presence of Pb was lower than DL (0.1 lg/g) in all the samples. Thus, the consumption of one edible portion of 150 g, either of louvar or sword-fish, would be negligible for Pb PTWI. 3.3. Analysis of fish contamination and dietary exposure estimation for methylmercury The presence of Hg was detected in all the samples analyzed (Table 2); mean level was 0.95 ± 0.05 lg/g (range:
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Table 1 Number of samples, frequencies (%) and concentration (lg/g) of cadmium contamination in individuals of louvar and sword-fish in Madrid marketplaces (two first main columns); mean percentages of cadmium JECFA–PTWI supplied to women of childbearing age by the intake of 150 g of these species (third main column) Species
Louvar (Luvarus imperialis) Sword-fish (Xiphias gladius) Total
Number of samples (%)
Concentration (lg/g)
PTWI percentage/150 g fish fillet
DL–MRL
>MRL
Min
Max
Mean
Women 25–34 years old
Women 35–44 years old
5 (29.41) 4 (10.81) 9 (16.66)
9 (52.94) 33 (89.19) 42 (77.77)
3 (17.65) 0 3 (5.55)
0.02 0.02 0.02
0.25 0.24 0.25
0.08 ± 0.01 0.08 ± 0.01 0.08 ± 0.01
3.06 3.15 3.12
2.90 2.99 2.96
Table 2 Number of samples, frequencies (%) and mean concentration (lg/g) of mercury contamination in individuals of louvar and sword-fish in Madrid marketplaces (two first main columns); mean percentages of methylmercury JECFA–PTWI supplied to women of childbearing age by the intake of 150 g of these species (third main column) Species
Number of samples (%)
Concentration (lg/g)
DL–MRL
>MRL
Min
Max
Mean
Women 25–34 years old
Women 35–44 years old
Louvar (Luvarus imperialis) Sword-fish (Xiphias gladius) Total
0 0 0
2 (11.76) 24 (64.86) 26 (48.14)
15 (88.24) 13 (35.14) 28 (51.85)
0.40 0.20 0.20
1.50 1.90 1.90
0.99 ± 0.06 0.93 ± 0.07 0.96 ± 0.05
163.33 152.69 155.71
155.19 145.08 147.95
0.20–1.90 lg/g); there were no differences when comparing mean Hg concentrations between species. The Hg levels were higher than fixed by the EFSA in 88.24% of the louvar samples (limit: 0.5 lg/g) and in 35.14% of the sword-fish fillets (limit: 1 lg/g). Thus, 29.41% of louvar samples had Hg levels higher than 1 lg/g. The PTWI for MeHg in women of childbearing age was estimated in a range between 91.8 and 96.7 lg/week. Thus, one serving of 150 g either of louvar or sword-fish would contain a mean MeHg concentration of 143.25 lg, which largely exceeds the tolerable values. 4. Discussion Current results indicate that Pb contamination in edible portions of sword-fish and louvar is negligible. Conversely, most of the samples showed residues of Cd and Hg, being lower than MRL in a majority of the samples analyzed for Cd levels. However, most (around 90%) of louvar samples and a third part (around 35%) of sword-fish portions exceeded MRL for Hg (0.5 and 1 lg/g, respectively). The most striking finding was that around 30% of louvar samples had Hg levels higher than 1 lg/g. Current study, although based in the estimation of intake instead of assessment of household data and food frequency questionnaires, showed a majority of samples with low concentration of Cd and Pb; which is coincidental with the very low pollution levels reported in many other previous studies, either in the Mediterranean countries or other areas (Storelli et al., 2003b; Cogun et al., 2006; Falco et al., 2006; Hinck et al., 2006). We need to have in mind that contamination levels are related to bioavailability and/or bioaccumulation of the pollutants; parameters which are depending in differences both in the degree of contamination of the sampling area (Meador et al., 2005) and/or the features of the marine and freshwater species
PTWI percentage/150 g fish fillet
analyzed (Barwick and Maher, 2003). It is commonly assumed that heavy metals may accumulate throughout the trophic chain; however, both earlier (Taylor, 1983) and recent studies (Barwick and Maher, 2003) showed no evidence of biomagnification of cadmium or lead, whilst bioconcentration is only found in some molluscs and crustacean. This is confirmed, in the Spanish market, by the study of Falco et al. (2006), reporting a higher presence of both compounds in seafood, specifically mussels, rather than in large predatory fish. The scenario is different for Hg, since it is a compound with significant interspecific differences reflecting trophic levels (Burger et al., 2001a), caused by biomagnification (Monteiro and Lopes, 1990; Nakagawa et al., 1997; Storelli and Marcotrigiano, 2000). The large predatory fishes reach the highest Hg concentrations. Within these species, larger animals usually have higher concentrations than smaller individuals; as a result of the age and, thus, time of exposure to pollutants (Burger and Gochfeld, 2006; Kojadinovic et al., 2006). Moreover, in predators, Hg levels have been found to be linearly related to Hg concentration in preys (Burger et al., 2001a). Then, Hg contamination is higher in edible portions from sword-fish and other predators than in species in lower levels of the trophic chain (Storelli and Marcotrigiano, 2001; Storelli et al., 2002; Dabeka et al., 2004; Falco et al., 2006; Cabanero et al., 2005). The concentration of Hg reported for sword-fish in these studies was higher (around 1.8 lg/g) than reported in our survey (0.93 lg/g); although other studies reflected lower values (0.47 lg/g, 24; 0.20 lg/g, 9). We have to note that, to our knowledge, our study is the first one testing presence of Hg (and also Cd and Pb) in louvar. This is valuable for increasing information on presence of pollutants in marine species and for determining any possible differences with described elsewhere in other species. But we have an arising question. In Spain, as in
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most of the countries, retailers and consumers do not make a clear differentiation between louver and sword-fish. However, such species are different not only at a taxonomic level, but also at an ecological level. All life stages of louvar are pelagic, living below 600–2000 feet from the sea surface. Their habitual preys are small fish, jellyfish, ctenophores, and freeswimming tunicates (www.dfg.ca.gov/mrd/status/ louvar.pdf). Sword-fishes are pelagic, but inhabiting the surface waters; usually, they feed small tuna, dorado, barracuda, flying fish, mackerel, hake rockfish and squid (www.dfg.ca.gov/mrd/status/swordfish.pdf). Usually, louvar is incidentally captured during sword-fish fisheries and, thereafter, sold and eaten like sword-fish. Most of people even believe that the words louvar and sword-fish are synonymous for the same animal. We are wondering if the picture may be the same in those studies determining Hg in fish samples obtained from market; which could explain differences between authors. Thus, the frequency of samples having Hg contamination higher than 1 lg/g in our study was similar in louvar (30%) and sword-fish (35%). Hg levels may be expected to be higher in sword-fish than in louvar due to its higher position in the trophic chain, as discussed above. In fact the MRL is twice higher than in louvar. Possible hypothesis explaining our finding may be related to the location of the catches and/ or in the eating habits of louvar. Several authors reported that fishes searching for food on the deepness, close to the sediment, may thus potentially accumulate higher amounts of mercury (Collings et al., 1996; Storelli et al., 1998; Storelli and Marcotrigiano, 2000), which led to concentrations higher than predicted by their trophic position (Burger et al., 2001b). Whatever the cause, current results support the necessity of revision of the MRL in louvar. In conclusion, in our study, we have found that a high percentage of samples from both species would exceed the Hg JECFA–PTWI for women in childbearing age. We agree with Falco et al. (2006) that intake of these species is not daily, which minimizes risk of exposure to MeHg. However, the exposure may be not the same in adult and fetus; some authors have suggested negative effects derived from a single-meal exposure in critical periods of pregnancy (Ginsberg and Toal, 2000), especially when embryo is developing (Burger et al., 2001a). However, we also have to keep in mind that the half-life of MeHg in human body is 70–80 days, so consumption of MeHg contaminated fish before or at the onset of pregnancy will lead to early fetal exposure (Bjo¨rnberg et al., 2005). Thus, first, it is important to establish periodical monitoring studies to assess Hg intake due to fish and seafood consumption and MRLs for different species. Second, consumers should be informed about risk of fish-based diet, avoiding either masking or magnification of data or conflicting messages. Specifically in order that at risk consumers like women of childbearing age should continue consuming fish with lowest pollutants and receiving the beneficial health effects of omega-3 fatty acids and others compounds provided by diet based in fish.
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