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Bull Vet Inst Pulawy 59, 357-360, 2015 DOI:10.1515/bvip-2015-0053

Mercury concentration in bivalve molluscs

Józef Szkoda1, Maciej Durkalec1, Agnieszka Nawrocka1, Mirosław Michalski2

1Department of Pharmacology and Toxicology, 2Department of Hygiene of Origin, National Veterinary Research Institute, 24-100 Pulawy, Poland [email protected]

Received: April 23, 2015 Accepted: September 4, 2015

Abstract

A total of 85 samples of eight were examined. Analysis of mercury in the freeze-dried samples was carried out by atomic absorption spectrometry method using direct mercury analyser 254. The analytical procedure for determination of mercury was covered by the quality assurance programme of research and participation in national and international proficiency tests. Concentrations of total mercury in all investigated samples were found to be generally low, in the range of 0.033-0.577 mg/kg of dry weight and of 0.003-0.045 mg/kg of wet weight. The results indicate that obtained levels of mercury in bivalve molluscs are not likely to pose a risk to the health of consumers.

Keywords: mercury, bivalve molluscs, bioaccumulation, food safety.

Introduction which may pose a threat to the health of consumers (7, 13). In Poland, the interest in marine food, or , The rules for the marketing of live bivalve has increased in the recent years. , mostly molluscs for direct consumption and also for shrimps, , and lobsters, are frequently chosen processing are strictly defined in EU law regulating by consumers, but less popular , cockles, all aspects of production, including environmental , and which belong to bivalve molluscs conditions, farming, cleaning, transport, sale, are also purchased. These organisms, living mainly in microbiological and virological limits, as well as the aquatic environment, are found in almost all maximum levels of contaminants and residues of geographical areas. Most of the species inhabit marine biotoxins (6, 14, 18, 19). It has been reported intertidal zone of marine waters as benthic fauna. The that and other aquatic organisms can accumulate minority of bivalve species live in the depths of the toxic metals, including mercury (2, 10, 12, 17, 24, sea, in freshwater, or brackish water. Bivalves adopt 25). Several studies have investigated the toxic effects a sedentary or sessile lifestyle, living on underwater of mercury in living organisms. Mercury and rocks, stones, gravel, woods, or buried in sand, silt, especially its organic forms may disturb enzymatic and mud. Most of the species are filter feeders and use reactions and cause destruction of cells which phytoplankton as an important source of food (4). accumulate this element in large quantities (1, 3, 8, 9). Bivalves play an important role in aquatic ecosystems Various mechanisms of mercury action can lead to in clarifying water (13). It should be mentioned that dysfunction of the central nervous system and bivalve farming is one of economically important numerous developmental disorders (1, 5, 7, 8, 26). branches for such countries as , The aim of the study was to assess mercury , Denmark and Italy, where seafood concentrations in bivalve molluscs available on the consumption is considerable. Given the fact that most Polish market. The material was collected within the of bivalve species are filter feeders, they can multi-annual monitoring programme "Protection of accumulate in their tissues such environmental animal and public health”. contaminants as pesticides, dioxins, and toxic metals,

© 2015 J. Szkoda et al. This is an open access article distributed under the Creative Commons Attribution- NonCommercial-NoDerivs license (http://creativecommons.org/licenses/by-nc-nd/3.0/) 358 J. Szkoda et al./Bull Vet Inst Pulawy/59 (2015) 357-360

Material and Methods performed using the following certified reference materials: SRM-2976 (National Institute of Science and A total of 85 tissue samples of eight species of Technology, USA) and TORT-2 (National Research bivalve molluscs (Table 1) were obtained from local Council, Canada). The chosen method was regularly market in Poland. evaluated by participation in proficiency programmes organised by Food Analyses Performance Assessment Table 1. Bivalve molluscs - the species studied Scheme (FAPAS) and European Union Reference Laboratories comparisons (20). Our laboratory also Number Species of samples organises proficiency testing for regional veterinary laboratories involved in the analysis of mercury Dog (Glycymeris glycymeris) 7 concentration in foods of animal origin and feed. Manila (Ruditapes philippinarum) 17

Atlantic jackknife clam ( directus) 8 Results (Mytilus edulis) 21 Mercury concentrations in the tissues of selected Pacific ( gigas) 17 species of bivalve molluscs (expressed in dry weight) Great () 3 are summarised in Table 2. Mean total mercury concentration was 0.132 mg/kg and median (Cardium edule) 7 0.120 mg/kg (dry wt.). The maximum concentration of (Mercenaria mercenaria) 5 mercury (0.577 mg/kg dry wt.) and the highest mean level (0.170 mg/kg dry wt.) were found in (Crassostrea gigas), but the differences in Bivalves were cleaned and rinsed with deionised concentration of mercury among species were not water. Afterwards, fresh tissues were separated from statistically significant. the shell and homogenised. Moisture content in tissue Mercury concentrations in tissues of selected samples was determined using HR83 moisture analyser bivalve species (expressed in wet wt) are presented in (Mettler-Toledo International Inc., Switzerland). Fig. 1. They ranged from 0.014 to 0.024 mg/kg in Hard Mercury analysis was performed in fresh samples clam (Mercenaria mercenaria) and by atomic absorption spectrometry using AMA254 (Glycymeris glycymeris) respectively. direct mercury analyser (Altec, Czech Republic). The Mercury recoveries in certified reference materials procedure of mercury content determination in (CRMs) and results of selected proficiency tests are biological samples was previously described by presented in Table 3. Szkoda et al. (24). Statistical calculations were The given Z-scores in proficiency tests indicate performed using Statistica 10 PL software (StatSoft, that the obtained values are not statistically different Poland). from the assigned values. Quality control of analytical measurements was

Table 2. Concentrations of mercury in bivalve molluscs, depending on the species (mg/kg dry matter)

Species Number Mean Std. dev. Median Min. Max. Moisture of samples

Dog cockle 7 0.09 0.199 82.8 0.138 0.035 0.133 Manila clam 17 0.035 0.397 87.1 0.118 0.082 0.102 Atlantic jacknife clam 8 0.099 0.135 83.0 0.119 0.012 0.118 Blue mussel 21 0.045 0.250 84.3 0.135 0.063 0.126 Pacific oyster 17 0.052 0.577 86.6 0.170 0.121 0.145 Great scallop 3 0.036 0.096 73.8 0.072 0.032 0.086 Common cockle 7 0.045 0.194 85.2 0.118 0.055 0.125 Hard clam 5 0.102 0.045 0.122 0.033 0.147 87.1

J. Szkoda et al./Bull Vet Inst Pulawy/59 (2015) 357-360 359

Fig. 1. Mean mercury concentrations (with range) in selected species of bivalve molluscs (expressed in wet-weight)

Table 3. Concentration of mercury detected in certified reference material and materials from international and national proficiency tests (mg/kg of dry wt.) Material Assigned value Measured value Recovery (%) Z-score

Certified reference material SRM-2976 (Mussel tissue) 0.061 0.060 98 - Certified reference material TORT-2 (Lobster hepatopancreas) 0.270 0.286 106 - 14th Proficiency test, EURL (Frozen fish) 0.222 0.211 95 -0.5 21th Proficiency test, EURL (Freeze-dried mussels) 0.0328 0.0385 117 0.8 Proficiency test, PIWet-PT2012/ZFT/32 (Frozen fish) 0.116 0.116 100 0.0

Discussion Toxicity of mercury is well known. The main sources of this toxic metal in human diet are fish and Bivalve molluscs are widely used as biomonitors seafood (1, 7, 8). The safety of consumers is provided of environmental metal concentrations. Beiras et al. (2) by legislation setting the maximum levels of mercury in found that mercury concentrations in tissues of Mytilus food. According to Commission Regulation (EC) No. galloprovincialis in , Spain, ranged from 0.100 1881/2006 setting the maximum level for certain to 1.109 mg/kg dry weight. Other authors monitored contaminants in foodstuffs, the maximum concentration heavy metal content in mussels from Apulian in of mercury in fish (with exception of some predatory Italy (22). The level of mercury was similar to the species) and in seafood is 0.5 mg/kg of wet weight (6). value determined by Beiras et al. (2) and ranged from The obtained concentrations of total mercury in fresh 0.10 to 0.81 mg/kg dry wt. Comparable results of tissue of bivalve molluscs were below the maximum mercury concentrations in tissues of Manila clam level (Fig. 1). Our finding corresponds with the results (Ruditapes phillipinarum) from Lagoon of Venice of other authors (10, 23). (0.130-0.830 mg/kg dry wt.) were reported by The European Food Safety Authority (EFSA) Moschino et al (15). Slightly lower content of mercury Panel on Contaminants in the Food Chain (CONTAM) (0.033-0.336 mg/kg dry wt.) was observed by Lepom in the line with Joint FAO/WHO Expert Committee on et al. (12) in tissues of freshwater mussels (Dreissena Food Additives (JECFA) established the following polymorpha) sampled in German surface waters, and tolerable weekly intake (TWI) of 4 μg/kg for inorganic by Rutzke et al. (21) in Lakes Ontario and Erie in the mercury and 1.3 μg/kg of body weight for United States. The ability of bivalve molluscs to methylmercury (8). accumulate toxic metals from water and sediments was To assess the risk associated with the consumption used in numerous studies in the assessment of of mercury presented in bivalve tissues, the tolerable environmental pollution by these elements (2, 11, 15, TWI for inorganic mercury was adopted. Assuming the 17, 22). Our results were slightly lower compared to consumption of 100 g of bivalves per week and the the findings of other authors. highest level of mercury in Manila Clam (0.045 mg/kg

360 J. Szkoda et al./Bull Vet Inst Pulawy/59 (2015) 357-360 wet wt), the weekly intake of mercury was estimated at 12. Lepom P., Irmer U., Wellmitz J.: Mercury levels and trends 4.5 μg/person/week, thus accounting 1.6% of TWI. (1993–2009) in bream (Abramis brama L.) and zebra mussels Taking together our findings and low consumption of (Dreissena polymorpha) from German surface waters. Chemosphere 2012, 86, 202–211. seafood in Poland, there is no risk to consumer's health 13. Michalski M.: General information on bivalves of the bivalve related to the intake of mercury from bivalve molluscs. molluscs intended for human consumption. In: Bivalve molluscs However, taking into account mercury concentrations as a source of biological hazards. Monograph. PIWet-PIB, found by other authors, especially in wild bivalves, the Pulawy, 2013, pp. 8–27. concentration of this element in seafood must be 14. Michalski M.: Marine biotoxins – occurrence and method of analysis. Żywn NaukaTechnol Jakość 2006, 48, 16–22. periodically monitored. 15. Moschino V., Delaney E., Da Ros L.: Assessing the significance of Ruditapes philippinarum as a sentinel for sediment pollution: Conflict of Interests Statement: The authors declare Bioaccumulation and biomarker responses. Environ Pollut 2012, no conflict of interests regarding the publication of this 171, 52–60. article. 16. Peña-Rodríguez S., Fernández-Calviño D., Nóvoa-Muñoz J.C., Arias-Estévez M., Núñez-Delgado A., Fernández-Sanjurjo M.J., Álvarez-Rodríguez E.: Kinetics of Hg(II) adsorption and desorption in calcined mussel shells. J Hazard Mater 2010, 180, References 622–627. 17. Raftopoulou E.K., Dimitriadis V.K.: Comparative study of the 1. ATSDR. Toxicological profile for mercury. Agency for Toxic accumulation and detoxification of Cu (essential metal) and Hg (nonessential metal) in the digestive gland and gills of mussels Substances and Disease Registry. Atlanta, 1999, pp. 1-676. http://www.atsdr.cdc.gov/toxprofiles/tp.asp?id=115&tid=24 Mytilus galloprovincialis, using analytical and histochemical 2. Beiras R., Fernandez N., Gonzalez J.J., Besada V., Schultze F.: techniques. Chemosphere 2011, 83, 1155–1165. 18. Regulation (EC) No 853/2004 of the European Parliament and of Mercury concentrations in seawater sediments and wild mussels from the of Galicia (NW Spain). Mar Pollut Bull 2002, 44, the Council of 29 April 2004 laying down specific hygiene rules 345–349. for food of animal origin. OJ L 226/22. 19. Regulation (EC) No 854/2004 of the European Parliament and of 3. Bełdowski J., Miotk M., Bełdowska M., Pempkowiak J.: Total, methyl and organic mercury in sediments of the Southern Baltic the Council of 29 April 2004 laying down specific rules for the Sea. Mar Pollut Bull 2014, 87, 388–395. organisation of official controls on products of animal origin intended for human consumption. OJ L 226/83. 4. . In: Polish fauna - the characteristics and the list of species. Vol III. edited by Bogdanowicz W., Chudzicka E., 20. Regulation of the Polish Minister of Agriculture and Rural Pilipiuk I., Skibińska E., Museum and Institute of Zoology, Development of 18 April 2012 on the National Reference Laboratories. OJ RP No. 480, 2012. Warsaw, 2008, pp. 366–368.

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