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Journal of Food Protection, Vol. 77, No. 6, 2014, Pages 1022-1030 doi: 10.4315/0362-028X.JFP-13-485 Copyright © , International Association for Food Protection
Research Note
Contents and Risk Assessment of Heavy Metals in Marine Invertebrates from Korean Coastal Fish Markets JO N G SOO M O K ,1 JI YOUNG KWON,2 KWANG TAE SON,2 WOO SEOK CHOI,2 SUNG RIM KANG,2 NA YOUNG HA,2 MI RA JO ,2 AND JI HOE K IM 2* 1Southeast Sea Fisheries Research Institute, National Fisheries Research and Development Institute, 361 Youngun-ri, Sanyang-up, Tongyoung 650-943, Korea; and '‘■Food Safety Research Division, National Fisheries Research and Development Institute, 408-1 Sirang-ri, Gijang-up, Gijang-gun, Busan 619-705, Korea MS 13-485: Received 29 October 2013/Accepted 24 January 2014
ABSTRACT The concentrations of the heavy metals cadmium (Cd), mercury (Hg), lead (Pb), chromium, silver, nickel, copper, and zinc in the edible portions of 105 marine invertebrates representing 16 mollusk and crustacean species were accurately determined to evaluate their hazard for human consumption. The samples were collected in 2011 from major fish markets on the coast of Korea and analyzed for Hg using a direct Hg analyzer and for other metals using inductively coupled plasma mass spectrometry. Estimated dietary exposure (EDE) was determined, and a risk assessment was made of the heavy metals to provide information concerning consumer safety. The Cd concentrations, which were the highest for the three hazardous metals (Cd, Hg, and Pb), were significantly higher (P < 0.05) in the bivalves and crabs than in the gastropods and cephalopods. However, the concentrations of these metals in all samples were within the regulatory limits set by Korea and other countries. The EDE was compared with the provisional tolerable daily intake (PTDI) adopted by the Joint FAO/WHO Expert Committee on Food Additives or the U.S. Environmental Protection Agency. The EDE of Cd, Hg, and Pb for each class of marine invertebrate were 0.07 to 2.64, 0.01 to 0.43, and 0.001 to 0.16% of the PTDI, respectively. The total EDE of Cd, Hg, and Pb for marine invertebrates accounted for 4.03, 0.96, and 0.21%, respectively, of the PTDI. The EDE of other metals in each class of marine invertebrate was less than 2% of the PTDI. The hazard index is a reasonable parameter for assessing the risk of heavy metal consumption associated with contaminated food. In the present study, the hazard index for all of the species was less than 1.0, which indicates that the intake of heavy metals from consumption of these marine invertebrates does not represent an appreciable hazard to humans.
Fisheries products are an important food resource worldwide. According to the Food and Agriculture Organization of the United Nations (FAO) (11), Korea produced 3,261,120 tons of fisheries products in 2011: 1,354,469 tons of fishes, 1,007,070 tons of aquatic plants, 737,855 tons of mollusks, 135,830 tons of crustaceans, and 25,895 tons of other species. Korea was the world’s 13th largest producer of fisheries products, accounting for almost 1.83% of the global production. Korea ranked 4th and 13th in the world for the production of mollusks and crustaceans, respectively, or about 3.5 and 1.1% of global production, respectively. Heavy metals found naturally in the environment differ widely in their hazard to humans. The metals iron (Fe), copper (Cu), zinc (Zn), and manganese (Mn) are essential to the human body because they play important roles in biological systems, whereas other metals such as mercury (Hg), lead (Pb), and cadmium (Cd) can harm the body, even in trace amounts (1, 8). Generally, heavy metals accumulate in marine organisms, including various species of marine * Author for correspondence. Tel: (+82)-51-720-2610; Fax: (+82)-51720-2619; E-mail: [email protected].
invertebrates (3 , 4 , 6 , 19, 20 , 22 , 27 , 30). Certain hazardous metals that accumulate in aquatic organisms can pose a health risk to humans via consumption of the organisms ( 13, 35 , 37). To protect public health, Korean authorities have established regulatory limits and monitoring programs for three hazardous metals, Cd, Pb, and Hg, to determine whether fisheries products containing mollusks and crusta ceans are safe to consume (24). Heavy metal pollution can be hazardous to humans; therefore, heavy metal concentrations in foods from the aquatic environment must be determined regularly to advise consumers of the risk. Previously, we reported the heavy metal concentrations in seaweed harvested in 2001 and 2002 (18, 28) and of fishes and marine invertebrates caught in 2003 and 2004 (27 , 29) from the Korean coast. In the present study, we determined the heavy metal concentra tions in the edible portions of marine invertebrates (mollusks and crustaceans) collected from fish markets on the coast of Korea in 2011. Dietary exposure to heavy metals via consumption of marine invertebrates depends on both the metal concentrations in the animals and the amount of these animals consumed. The estimated dietary exposure (EDE) was compared with the provisional tolerable daily
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CONTENTS AND RISK ASSESSMENT OF HEAVY METALS IN MARINE INVERTEBRATES
TABLE 1. Types and average daily intake o f marine invertebrates collected from three fish markets on the Korean coast Scientific name
Common name
Korean name
No. of samples
Sample size (cm)"
Gastropoda Nordotis discus Batillus cornutus Rapana venosa
Abalone Spiny top shell Veined rapa whelk
Jeonbok Sora Pippulgodung
30 12 9 9
Bivalvia Crassostrea gigas Ruditapes philippinarum Mytilus galloprovincialis Argopecten irradians Atrina pectinata Scapharca broughtonii
Oyster Short neck clam Mussel Bay scallop Comb pen shell Ark shell
Gul Bajirak Jinjudamchi Haemangaribi Kijogae Pijogae
38 11 7 8 3 6 3
Japanese flying squid North Pacific giant octopus Small octopus Webfoot octopus
Salojingeo Muneo
22 7 8
5.1 + 0.6 9.6 ± 1.5
X
Nakji Jukkumi
4 3
4.7 ± 0.7 4.2 ± 0.8
X
Snow crab Red snow crab Blue crab
Daege Hongge Kkotge
15 5 6 4
10.4 ± 0.8 10.1 + 1.0 15.7 + 1.3
Cephalopoda Todarodes pacificus Enteroctopus dofleini Octopus minor O. ocellatus Crustacea (crabs) Chionoecetes opilio C. japonicus Portunus trituberculatus
5.7 ± 0.8 6.7 ± 1.7 6.5 ± 1.3 5.4 4.9 3.5 9.1 12.0 5.8
± ± ± ± ± +
0.7 0.3 0.4 0.6 1.3 0.8
X X X
X X X X X X
X
X
X X X
Avg daily intake (pg/kg/day)*
8.5 + 1.1 8.8 ± 1.7 9.0 + 1.8
0.0115 0.0044 0.0020 0.00381'
10.3 ± 1.2 3.2 ± 0.3 6.6 + 0.5 8.8 ± 1.1 23.5 ± 2.2 4.8 ± 0.6
0.0586 0.0198 0.0197 0.0066 0.0027 0.0002 0.0002
38.8 ± 3.3 54.1 + 6.8
0.1232 0.0950 0.0050
71.9 ± 9.9 20.8 ± 3.2
0.0184 0.0044
9.7 + 0.6 9.7 + 0.9 8.0 ± 0.7
0.0232 0.0027 0.0001 0.0203
a Means + standard deviations of total width x length for mollusks or of body only (without legs) width x length for crabs. h Based on Korea health statistics 2010 (23). c Average daily intake of the veined rapa whelk include that of the moon snail (Glossaulax didyma).
intake (PTDI) established by the Joint FAO/WHO Expert Committee on Food Additives (JECFA) (15- 17) or the U.S. Environmental Protection Agency (EPA) (36). A risk assessment of the heavy metals in marine invertebrates also was carried out using the target hazard quotient (THQ). This assessment provides valuable information about the safety of consuming marine invertebrates. MATERIALS AND METHODS Reagents and standard solutions. Suprapur nitric acid (Merck, Darmstadt, Germany) was used for sample preparation. Deionized water (DIW) was passed through a Milli-Q water purification system (Millipore, Billerica, MA). Working standard solutions of Cd, Pb, chromium (Cr), silver (Ag), nickel (Ni), Cu, and Zn were prepared by diluting stock 1,000 mg/liter standard solutions (Merck) in DIW. MESS-3, a marine sediment certified reference material (CRM), was purchased from the National Research Council of Canada (Ottawa, Ontario) and used as a calibration standard for Hg. The SRM-1566b (oyster tissue) CRM was obtained from the National Institute of Standards and Technology (NIST, Gaithersburg, MD) and used for the heavy metal recovery test. Sample collection. Fresh samples of 105 individuals representing 16 species of marine invertebrates (mollusks and cmstaceans) were collected quarterly from three major fish markets located on the eastern (Pohang), western (Gunsan), and southern (Tongyeong) coasts of Korea in 2011: nine species of molluscan shellfish (gastropods and bivalves), four species of cephalopods, and three species of cmstaceans (Table 1). All of the animals were for sale in the markets and were harvested from the respective
coasts of Korea. Most of the selected species are very popular with consumers in Korea. The samples were transported to the laboratory in coolers. Sample preparation. The collected samples were immedi ately separated according to species upon reception and washed with tap water and DIW. The shells of bivalves, gastropods, and crustaceans were shucked. The edible tissues to be used for metal analysis were prepared by removing the inedible parts. For bivalves, whole tissues were prepared, except for the bay scallop and comb pen shell, which were prepared using only their adductor muscles. Gastropods, cephalopods, and cmstaceans were prepared by removing the internal organs (or digestive gland), except for the blue crab, for which whole tissues were used. The tissue samples were cleaned with DIW, homogenized, and weighed. The homogenized tissues were freeze-dried with a vacuum freeze dryer (FDU-2100, EYELA, Tokyo, Japan) and then ground into powder for analysis. About 1.0 g of powdered sample was placed in a 60ml digestion vessel (Savillex, Eden Prairie, MN), and 20 ml of nitric acid was added. The container was covered and left overnight at room temperature. The samples were digested with a heating digester (DigiPREP HP, SCP Science, Champlain, NY), and more nitric acid was added to those samples that were not completely digested. The completely digested samples were allowed to cool to room temperature, dissolved in 2% nitric acid, filtered (glass wool), and made up to 100 ml of 2% nitric acid to analyze all heavy metals except Hg. Approximately 0.1 g of homogenized sample was used for the Hg analysis. Analysis of heavy metals. All digested samples were analyzed in triplicate for Ag, Cd, Cr, Cu, Ni, Pb, and Zn with an inductively coupled plasma mass spectrometer (ELAN DRC II,
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TABLE 2. Recovery ratio o f heavy metals from certified reference materiala Heavy metal*
Certified value (gg/g)
Cd Hg Pb Ag Ni Cu Zn
2.48 0.0371 0.308 0.666 1.04 71.6 1,424
± ± ± ± + ± ±
0.08 0.0013 0.009 0.009 0.09 1.6 46
Measured value (jag/g) 2.384 0.034 0.319 0.531 0.980 70.047 1,362.04
± ± + ± ± ± +
0.172 0.001 0.028 0.218 0.404 6.270 49.81
Recovery (%) 96.1 91.2 103.6 91.1 107.7 97.8 95.6
a Values are means + standard deviations (n = 7). Oyster certified reference material (SRM-1566b) was purchased from the NIST for the recovery test.
h Cd, cadmium; Hg, mercury; Pb, lead; Ag, silver; Ni, nickel; Cu, copper; Zn, zinc. PerkinElmer, Waltham, MA). The total Hg concentration in the homogenized samples was measured directly in triplicate using a combustion gold amalgamation method with a direct Hg analyzer (DMA-80, Milestone, Milano, Italy). The blanks, calibration standards, and CRMs were also analyzed in the same way as the samples. The concentrations of heavy metals are expressed in micrograms per gram of wet weight.
Statistical analysis. The data were analyzed using an analysis of variance with the general linear model procedure (SAS version 9.2, SAS Institute, Cary, NC). D uncan’s multiple range test was applied to determine the significance o f differences between the mean concentrations of heavy metals in marine invertebrates. RESULTS AND DISCUSSION Quality assurance of heavy metal analysis. The quality of the analysis was monitored using oyster CRM (Table 2). The quantitative recoveries of heavy metals ranged from 91.1 to 107.7%. The recoveries were within the acceptable values recommended by AOAC International (2), which are 70 to 125, 75 to 120, and 80 to 115% for concentrations of 0.01, 1.0, and 10 pg/g, respectively. Concentrations of heavy metals in molluscan shellfish. The mean, standard deviation, and range of concentrations of the heavy metals analyzed in the edible portions of each species of molluscan shellfish (gastropods and bivalves) are shown in Table 3. The mean concentra tions in the samples taken from the edible portion of gastropods decreased in the order Zn (35.06 pg/g) > Cu (6.658 pg/g) > Ni (0.746 pg/g) > Ag (0.122 pg/g) > Cr (0.076 pg/g) > Cd (0.050 pg/g) > Hg (0.007 pg/g) > Pb (0.003 pg/g); however, the differences among Ag, Cr, Cd, Hg, and Pb were not significant. The mean concentrations in bivalves decreased in the order Zn (89.56 pg/g) > Cu (11.297 pg/g) > Cd (0.375 pg/g) > Ni (0.251 pg/g) > Cr (0.227 pg/g) > Ag (0.100 pg/g) > Pb (0.097 pg/g) > Hg (0.009 pg/g); however, the differences between Ni and Cr and between Ag and Pb were not significant. The concentrations of harmful heavy metals (Cd, Hg, Pb, and Cr) in the edible portions of molluscan shellfish were significantly higher (P < 0.05) in bivalves than in gastropods. We previously reported that the concentrations of harmful heavy metals (Cd, Pb, and Cr) in bivalves were higher than those in gastropods in 2003 and 2004 (27).
According to Alina et al. (1), bivalve mollusks have a high capacity for and propensity to concentrate pollutants. In this study (2011), the mean concentration of Cd in molluscan shellfish was 0.227 pg/g, which is less than the 0.325 pg/g reported in our previous study for 2003 and 2004 (27). The Cd concentration was also lower than the 0.510 and 0.288 pg/g reported by Sho et al. (31) and Ham (14), respectively, in Korea. Our result is similar to the means of 0.22 and 0.224 pg/g for shellfish in India (32) and China (26), respectively. The Cd concentrations of molluscan shellfish ranged from 0.012 to 0.951 pg/g; the highest concentration was found in oysters. All samples had Cd concentrations lower than the regulatory limits (1.0 to 2.0 pg/g) set by the Codex Alimentarius Commission (2.0 pg/g) (7) and other countries such as Korea (2.0 pg/g) (24), Australia and New Zealand (2.0 pg/g) (12), the European Union (EU) (1.0 pg/g, only bivalves) (9), and China (1.0 pg/g) (26). The mean concentration of Hg in molluscan shellfish was 0.008 pg/g, which is three- to fourfold lower than the concentrations found in other Korean studies (14, 31) and similar to the 0.008 pg/g reported for Chinese shellfish (26). The Hg concentrations of the samples ranged from 0.002 to 0.021 pg/g; the highest concentration was found in oysters but is far below the regulatory limits (0.5 pg/g) in Korea (24), the EU (10), and Australia and New Zealand (12). The mean concentration of Pb in molluscan shellfish was 0.055 pg/g, which is fourfold lower than the concentration we reported previously (27). This mean Pb concentration was about two- to sevenfold lower than that for molluscan shellfish reported in Korea (5, 31) and threeto sixfold lower than that reported for shellfish in China (26) and India (32). The highest Pb concentration (0.201 pg/g) was found in oysters, but this value is 5- to 10-fold lower than the regulatory limits (1.0 to 2.0 pg/g) set by various countries, e.g., 2.0 pg/g in Korea (24) and Australia and New Zealand (12) and 1.0 pg/g in both the EU (only bivalves) (9) and China (26). The concentrations of Cr in molluscan shellfish were 0.014 to 0.445 pg/g; the highest concentration was detected in the short necked clam. The mean Cr concentration (0.178 pg/g) in molluscan shellfish is similar to that reported in previous studies in Korea (21, 27) and approximately 10fold lower than the Cr concentrations reported for shellfish in China (26) and India (32).
J. Food Plot., Vol. 77, No. 6
CONTENTS AND RISK ASSESSMENT OF HEAVY METALS IN MARINE INVERTEBRATES
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cephalopods > crustaceans > gastropods (Fig. 2). The mean HI ranged from 4.8 x 10-3 to 6.2 x 10-2 ; the highest (2.2 x 10 l) was for bivalves and is substantially below 1.0. An HI exceeding 1.0 indicates that the contaminant is toxic and represents a hazard to human health (25 , 26). In conclusion, the concentrations of hazardous metal in all samples were lower than the standards set by many governments. The sums of the EDEs of hazardous heavy metals (Cd, Hg, and Pb) for these marine invertebrates were 4.03, 0.96, and 0.21 of the PTDI suggested by the JECFA or the EPA. The HI for all of these invertebrates was less than 1.0, which indicates that the intake of heavy metals via
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MOK ET AL.
consumption of these animals does not pose an appreciable hazard to humans. ACKNOWLEDGMENT This work was supported by a grant from the National Fisheries Research and Development Institute of Korea (RP-2013-FS-043).
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Journal of Food Protection, Vol. 77, No. 6, 2014, Pages 1022-1030 doi: 10.4315/0362-028X.JFP-13-485 Copyright © , International Association for Food Protection
Research Note
Contents and Risk Assessment of Heavy Metals in Marine Invertebrates from Korean Coastal Fish Markets JO N G SOO M O K ,1 JI YOUNG KWON,2 KWANG TAE SON,2 WOO SEOK CHOI,2 SUNG RIM KANG,2 NA YOUNG HA,2 MI RA JO ,2 AND JI HOE K IM 2* 1Southeast Sea Fisheries Research Institute, National Fisheries Research and Development Institute, 361 Youngun-ri, Sanyang-up, Tongyoung 650-943, Korea; and '‘■Food Safety Research Division, National Fisheries Research and Development Institute, 408-1 Sirang-ri, Gijang-up, Gijang-gun, Busan 619-705, Korea MS 13-485: Received 29 October 2013/Accepted 24 January 2014
ABSTRACT The concentrations of the heavy metals cadmium (Cd), mercury (Hg), lead (Pb), chromium, silver, nickel, copper, and zinc in the edible portions of 105 marine invertebrates representing 16 mollusk and crustacean species were accurately determined to evaluate their hazard for human consumption. The samples were collected in 2011 from major fish markets on the coast of Korea and analyzed for Hg using a direct Hg analyzer and for other metals using inductively coupled plasma mass spectrometry. Estimated dietary exposure (EDE) was determined, and a risk assessment was made of the heavy metals to provide information concerning consumer safety. The Cd concentrations, which were the highest for the three hazardous metals (Cd, Hg, and Pb), were significantly higher (P < 0.05) in the bivalves and crabs than in the gastropods and cephalopods. However, the concentrations of these metals in all samples were within the regulatory limits set by Korea and other countries. The EDE was compared with the provisional tolerable daily intake (PTDI) adopted by the Joint FAO/WHO Expert Committee on Food Additives or the U.S. Environmental Protection Agency. The EDE of Cd, Hg, and Pb for each class of marine invertebrate were 0.07 to 2.64, 0.01 to 0.43, and 0.001 to 0.16% of the PTDI, respectively. The total EDE of Cd, Hg, and Pb for marine invertebrates accounted for 4.03, 0.96, and 0.21%, respectively, of the PTDI. The EDE of other metals in each class of marine invertebrate was less than 2% of the PTDI. The hazard index is a reasonable parameter for assessing the risk of heavy metal consumption associated with contaminated food. In the present study, the hazard index for all of the species was less than 1.0, which indicates that the intake of heavy metals from consumption of these marine invertebrates does not represent an appreciable hazard to humans.
Fisheries products are an important food resource worldwide. According to the Food and Agriculture Organization of the United Nations (FAO) (11), Korea produced 3,261,120 tons of fisheries products in 2011: 1,354,469 tons of fishes, 1,007,070 tons of aquatic plants, 737,855 tons of mollusks, 135,830 tons of crustaceans, and 25,895 tons of other species. Korea was the world’s 13th largest producer of fisheries products, accounting for almost 1.83% of the global production. Korea ranked 4th and 13th in the world for the production of mollusks and crustaceans, respectively, or about 3.5 and 1.1% of global production, respectively. Heavy metals found naturally in the environment differ widely in their hazard to humans. The metals iron (Fe), copper (Cu), zinc (Zn), and manganese (Mn) are essential to the human body because they play important roles in biological systems, whereas other metals such as mercury (Hg), lead (Pb), and cadmium (Cd) can harm the body, even in trace amounts (1, 8). Generally, heavy metals accumulate in marine organisms, including various species of marine * Author for correspondence. Tel: (+82)-51-720-2610; Fax: (+82)-51720-2619; E-mail: [email protected].
invertebrates (3 , 4 , 6 , 19, 20 , 22 , 27 , 30). Certain hazardous metals that accumulate in aquatic organisms can pose a health risk to humans via consumption of the organisms ( 13, 35 , 37). To protect public health, Korean authorities have established regulatory limits and monitoring programs for three hazardous metals, Cd, Pb, and Hg, to determine whether fisheries products containing mollusks and crusta ceans are safe to consume (24). Heavy metal pollution can be hazardous to humans; therefore, heavy metal concentrations in foods from the aquatic environment must be determined regularly to advise consumers of the risk. Previously, we reported the heavy metal concentrations in seaweed harvested in 2001 and 2002 (18, 28) and of fishes and marine invertebrates caught in 2003 and 2004 (27 , 29) from the Korean coast. In the present study, we determined the heavy metal concentra tions in the edible portions of marine invertebrates (mollusks and crustaceans) collected from fish markets on the coast of Korea in 2011. Dietary exposure to heavy metals via consumption of marine invertebrates depends on both the metal concentrations in the animals and the amount of these animals consumed. The estimated dietary exposure (EDE) was compared with the provisional tolerable daily
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TABLE 1. Types and average daily intake o f marine invertebrates collected from three fish markets on the Korean coast Scientific name
Common name
Korean name
No. of samples
Sample size (cm)"
Gastropoda Nordotis discus Batillus cornutus Rapana venosa
Abalone Spiny top shell Veined rapa whelk
Jeonbok Sora Pippulgodung
30 12 9 9
Bivalvia Crassostrea gigas Ruditapes philippinarum Mytilus galloprovincialis Argopecten irradians Atrina pectinata Scapharca broughtonii
Oyster Short neck clam Mussel Bay scallop Comb pen shell Ark shell
Gul Bajirak Jinjudamchi Haemangaribi Kijogae Pijogae
38 11 7 8 3 6 3
Japanese flying squid North Pacific giant octopus Small octopus Webfoot octopus
Salojingeo Muneo
22 7 8
5.1 + 0.6 9.6 ± 1.5
X
Nakji Jukkumi
4 3
4.7 ± 0.7 4.2 ± 0.8
X
Snow crab Red snow crab Blue crab
Daege Hongge Kkotge
15 5 6 4
10.4 ± 0.8 10.1 + 1.0 15.7 + 1.3
Cephalopoda Todarodes pacificus Enteroctopus dofleini Octopus minor O. ocellatus Crustacea (crabs) Chionoecetes opilio C. japonicus Portunus trituberculatus
5.7 ± 0.8 6.7 ± 1.7 6.5 ± 1.3 5.4 4.9 3.5 9.1 12.0 5.8
± ± ± ± ± +
0.7 0.3 0.4 0.6 1.3 0.8
X X X
X X X X X X
X
X
X X X
Avg daily intake (pg/kg/day)*
8.5 + 1.1 8.8 ± 1.7 9.0 + 1.8
0.0115 0.0044 0.0020 0.00381'
10.3 ± 1.2 3.2 ± 0.3 6.6 + 0.5 8.8 ± 1.1 23.5 ± 2.2 4.8 ± 0.6
0.0586 0.0198 0.0197 0.0066 0.0027 0.0002 0.0002
38.8 ± 3.3 54.1 + 6.8
0.1232 0.0950 0.0050
71.9 ± 9.9 20.8 ± 3.2
0.0184 0.0044
9.7 + 0.6 9.7 + 0.9 8.0 ± 0.7
0.0232 0.0027 0.0001 0.0203
a Means + standard deviations of total width x length for mollusks or of body only (without legs) width x length for crabs. h Based on Korea health statistics 2010 (23). c Average daily intake of the veined rapa whelk include that of the moon snail (Glossaulax didyma).
intake (PTDI) established by the Joint FAO/WHO Expert Committee on Food Additives (JECFA) (15- 17) or the U.S. Environmental Protection Agency (EPA) (36). A risk assessment of the heavy metals in marine invertebrates also was carried out using the target hazard quotient (THQ). This assessment provides valuable information about the safety of consuming marine invertebrates. MATERIALS AND METHODS Reagents and standard solutions. Suprapur nitric acid (Merck, Darmstadt, Germany) was used for sample preparation. Deionized water (DIW) was passed through a Milli-Q water purification system (Millipore, Billerica, MA). Working standard solutions of Cd, Pb, chromium (Cr), silver (Ag), nickel (Ni), Cu, and Zn were prepared by diluting stock 1,000 mg/liter standard solutions (Merck) in DIW. MESS-3, a marine sediment certified reference material (CRM), was purchased from the National Research Council of Canada (Ottawa, Ontario) and used as a calibration standard for Hg. The SRM-1566b (oyster tissue) CRM was obtained from the National Institute of Standards and Technology (NIST, Gaithersburg, MD) and used for the heavy metal recovery test. Sample collection. Fresh samples of 105 individuals representing 16 species of marine invertebrates (mollusks and cmstaceans) were collected quarterly from three major fish markets located on the eastern (Pohang), western (Gunsan), and southern (Tongyeong) coasts of Korea in 2011: nine species of molluscan shellfish (gastropods and bivalves), four species of cephalopods, and three species of cmstaceans (Table 1). All of the animals were for sale in the markets and were harvested from the respective
coasts of Korea. Most of the selected species are very popular with consumers in Korea. The samples were transported to the laboratory in coolers. Sample preparation. The collected samples were immedi ately separated according to species upon reception and washed with tap water and DIW. The shells of bivalves, gastropods, and crustaceans were shucked. The edible tissues to be used for metal analysis were prepared by removing the inedible parts. For bivalves, whole tissues were prepared, except for the bay scallop and comb pen shell, which were prepared using only their adductor muscles. Gastropods, cephalopods, and cmstaceans were prepared by removing the internal organs (or digestive gland), except for the blue crab, for which whole tissues were used. The tissue samples were cleaned with DIW, homogenized, and weighed. The homogenized tissues were freeze-dried with a vacuum freeze dryer (FDU-2100, EYELA, Tokyo, Japan) and then ground into powder for analysis. About 1.0 g of powdered sample was placed in a 60ml digestion vessel (Savillex, Eden Prairie, MN), and 20 ml of nitric acid was added. The container was covered and left overnight at room temperature. The samples were digested with a heating digester (DigiPREP HP, SCP Science, Champlain, NY), and more nitric acid was added to those samples that were not completely digested. The completely digested samples were allowed to cool to room temperature, dissolved in 2% nitric acid, filtered (glass wool), and made up to 100 ml of 2% nitric acid to analyze all heavy metals except Hg. Approximately 0.1 g of homogenized sample was used for the Hg analysis. Analysis of heavy metals. All digested samples were analyzed in triplicate for Ag, Cd, Cr, Cu, Ni, Pb, and Zn with an inductively coupled plasma mass spectrometer (ELAN DRC II,
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TABLE 2. Recovery ratio o f heavy metals from certified reference materiala Heavy metal*
Certified value (gg/g)
Cd Hg Pb Ag Ni Cu Zn
2.48 0.0371 0.308 0.666 1.04 71.6 1,424
± ± ± ± + ± ±
0.08 0.0013 0.009 0.009 0.09 1.6 46
Measured value (jag/g) 2.384 0.034 0.319 0.531 0.980 70.047 1,362.04
± ± + ± ± ± +
0.172 0.001 0.028 0.218 0.404 6.270 49.81
Recovery (%) 96.1 91.2 103.6 91.1 107.7 97.8 95.6
a Values are means + standard deviations (n = 7). Oyster certified reference material (SRM-1566b) was purchased from the NIST for the recovery test.
h Cd, cadmium; Hg, mercury; Pb, lead; Ag, silver; Ni, nickel; Cu, copper; Zn, zinc. PerkinElmer, Waltham, MA). The total Hg concentration in the homogenized samples was measured directly in triplicate using a combustion gold amalgamation method with a direct Hg analyzer (DMA-80, Milestone, Milano, Italy). The blanks, calibration standards, and CRMs were also analyzed in the same way as the samples. The concentrations of heavy metals are expressed in micrograms per gram of wet weight.
Statistical analysis. The data were analyzed using an analysis of variance with the general linear model procedure (SAS version 9.2, SAS Institute, Cary, NC). D uncan’s multiple range test was applied to determine the significance o f differences between the mean concentrations of heavy metals in marine invertebrates. RESULTS AND DISCUSSION Quality assurance of heavy metal analysis. The quality of the analysis was monitored using oyster CRM (Table 2). The quantitative recoveries of heavy metals ranged from 91.1 to 107.7%. The recoveries were within the acceptable values recommended by AOAC International (2), which are 70 to 125, 75 to 120, and 80 to 115% for concentrations of 0.01, 1.0, and 10 pg/g, respectively. Concentrations of heavy metals in molluscan shellfish. The mean, standard deviation, and range of concentrations of the heavy metals analyzed in the edible portions of each species of molluscan shellfish (gastropods and bivalves) are shown in Table 3. The mean concentra tions in the samples taken from the edible portion of gastropods decreased in the order Zn (35.06 pg/g) > Cu (6.658 pg/g) > Ni (0.746 pg/g) > Ag (0.122 pg/g) > Cr (0.076 pg/g) > Cd (0.050 pg/g) > Hg (0.007 pg/g) > Pb (0.003 pg/g); however, the differences among Ag, Cr, Cd, Hg, and Pb were not significant. The mean concentrations in bivalves decreased in the order Zn (89.56 pg/g) > Cu (11.297 pg/g) > Cd (0.375 pg/g) > Ni (0.251 pg/g) > Cr (0.227 pg/g) > Ag (0.100 pg/g) > Pb (0.097 pg/g) > Hg (0.009 pg/g); however, the differences between Ni and Cr and between Ag and Pb were not significant. The concentrations of harmful heavy metals (Cd, Hg, Pb, and Cr) in the edible portions of molluscan shellfish were significantly higher (P < 0.05) in bivalves than in gastropods. We previously reported that the concentrations of harmful heavy metals (Cd, Pb, and Cr) in bivalves were higher than those in gastropods in 2003 and 2004 (27).
According to Alina et al. (1), bivalve mollusks have a high capacity for and propensity to concentrate pollutants. In this study (2011), the mean concentration of Cd in molluscan shellfish was 0.227 pg/g, which is less than the 0.325 pg/g reported in our previous study for 2003 and 2004 (27). The Cd concentration was also lower than the 0.510 and 0.288 pg/g reported by Sho et al. (31) and Ham (14), respectively, in Korea. Our result is similar to the means of 0.22 and 0.224 pg/g for shellfish in India (32) and China (26), respectively. The Cd concentrations of molluscan shellfish ranged from 0.012 to 0.951 pg/g; the highest concentration was found in oysters. All samples had Cd concentrations lower than the regulatory limits (1.0 to 2.0 pg/g) set by the Codex Alimentarius Commission (2.0 pg/g) (7) and other countries such as Korea (2.0 pg/g) (24), Australia and New Zealand (2.0 pg/g) (12), the European Union (EU) (1.0 pg/g, only bivalves) (9), and China (1.0 pg/g) (26). The mean concentration of Hg in molluscan shellfish was 0.008 pg/g, which is three- to fourfold lower than the concentrations found in other Korean studies (14, 31) and similar to the 0.008 pg/g reported for Chinese shellfish (26). The Hg concentrations of the samples ranged from 0.002 to 0.021 pg/g; the highest concentration was found in oysters but is far below the regulatory limits (0.5 pg/g) in Korea (24), the EU (10), and Australia and New Zealand (12). The mean concentration of Pb in molluscan shellfish was 0.055 pg/g, which is fourfold lower than the concentration we reported previously (27). This mean Pb concentration was about two- to sevenfold lower than that for molluscan shellfish reported in Korea (5, 31) and threeto sixfold lower than that reported for shellfish in China (26) and India (32). The highest Pb concentration (0.201 pg/g) was found in oysters, but this value is 5- to 10-fold lower than the regulatory limits (1.0 to 2.0 pg/g) set by various countries, e.g., 2.0 pg/g in Korea (24) and Australia and New Zealand (12) and 1.0 pg/g in both the EU (only bivalves) (9) and China (26). The concentrations of Cr in molluscan shellfish were 0.014 to 0.445 pg/g; the highest concentration was detected in the short necked clam. The mean Cr concentration (0.178 pg/g) in molluscan shellfish is similar to that reported in previous studies in Korea (21, 27) and approximately 10fold lower than the Cr concentrations reported for shellfish in China (26) and India (32).
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CONTENTS AND RISK ASSESSMENT OF HEAVY METALS IN MARINE INVERTEBRATES
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cephalopods > crustaceans > gastropods (Fig. 2). The mean HI ranged from 4.8 x 10-3 to 6.2 x 10-2 ; the highest (2.2 x 10 l) was for bivalves and is substantially below 1.0. An HI exceeding 1.0 indicates that the contaminant is toxic and represents a hazard to human health (25 , 26). In conclusion, the concentrations of hazardous metal in all samples were lower than the standards set by many governments. The sums of the EDEs of hazardous heavy metals (Cd, Hg, and Pb) for these marine invertebrates were 4.03, 0.96, and 0.21 of the PTDI suggested by the JECFA or the EPA. The HI for all of these invertebrates was less than 1.0, which indicates that the intake of heavy metals via
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MOK ET AL.
consumption of these animals does not pose an appreciable hazard to humans. ACKNOWLEDGMENT This work was supported by a grant from the National Fisheries Research and Development Institute of Korea (RP-2013-FS-043).
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