Abstract
Bioaccessibility study is of great significance to the health risk assessment of trace elements in the seafood. In this work, the most consumed crab (Portunus trituberculatus) in coastal area of Shandong, China was analyzed to study the distribution and the bioaccessibility of cadmium (Cd) in the edible tissues of crab, and the dietary risk from consumption of crab was also evaluated. Results showed that the content of Cd in the whole edible tissues of 109 crab specimens ranged from 0.052 to 8.89 mg/kg ww (wet weight) with mean of 2.26 mg/kg ww. The Cd content in 85% of the crab samples was higher than the national food safety limits (0.5 mg/kg ww) of China. The gender study indicated that there was no significant difference in Cd content in total edible tissues between the males and females (p > 0.05). Cadmium was highly concentrated in the brown meat with mean value of 4.13 mg/kg ww, which was about 5 times higher than that in the white meat (0.75 mg/kg ww). The bioaccessibility of Cd ranged from 48.1 to 71.0% in the white and brown meat. The risk assessment based on the bioaccessibility of Cd revealed that the consumption of the edible crab brown and white meat for adults should be limited in 0.13 kg and 1.56 kg per week respectively.
References
Sioen I, Henauw SD, Verdonck F, Thuyne NV, Camp JV (2007) Development of a nutrient database and distributions for use in a probabilistic risk-benefit analysis of human seafood consumption. J Food Compos Anal 20(8):662–670. https://doi.org/10.1016/j.jfca.2006.11.001
Maulvault AL, Machado R, Afonso C, Lourenço HM, Nunes ML, Coelho I, Langerholc T, Marques A (2011) Bioaccessibility of Hg, Cd and As in cooked black scabbard fish and edible crab. Food Chem Toxicol 49:2808–2815. https://doi.org/10.1016/j.fct.2011.07.059
Jiang KJ, Zhang FY, Pi Y, Jiang LL, Yu ZL, Zhang D, Sun MM, Gao LJ, Qiao ZG, Ma LB (2014) Amino acid, fatty acid, and metal compositions in edible parts of three cultured economic crabs: Scylla paramamosain, Portunus trituberculatus, and Eriocheir sinensis. J Aquat Food Prod Technol 23:73–86. https://doi.org/10.1080/10498850.2012.695761
He M, Wang WX (2013) Bioaccessibility of 12 trace elements in marine molluscs. Food Chem Toxicol 55:627–636. https://doi.org/10.1016/j.fct.2013.01.046
Goyer RA, Klaassen CD, Waalkes MP (1995) Metal toxicology. Academic Press, San Diego
Nawrot T, Plusquin M, Hogervorst J, Roels HA, Celis H, Thijs L, Vangronsveld J, Hecke EV, Staessen JA (2006) Environmental exposure to cadmium and risk cancer: a prospective population-based study. Lancet Oncol 7:119–126. https://doi.org/10.1016/S1470-2045(06)70545-9
EU (2006) Commission Regulation (EC) No 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. Off J Eur Union 49(L364):5–24
EU (2011) Commission Regulation (EU) No 420/2011 of 29 April 2011 amending Regulation (EC) No 1881/2006 setting maximum levels for certain contaminants in foodstuffs. Off J Eur Union 49(L111):3–6
GB 2762-2017 (2017) National food safety standard: maximum levels of contaminants in food. Ministry Health People’s Repub. China 5
Mok JS, Yoo HD, Kim PH, Yoon HD, Park YC, Lee TS, Kwon JY, Son KT, Lee HJ, Ha KS, Shim KB, Kim JH (2015) Bioaccumulation of heavy metals in oysters from the southern coast of Korea: assessment of potential risk to human health. Bull Environ Contam Toxicol 94:749–755. https://doi.org/10.1007/s00128-015-1534-4
Brandon EFA, Oomen AG, Rompelberg CJM, Versantvoort CHM, van Engelen JGM, Sips AJAM (2006) Consumer product in vitro digestion model: bioaccessibility of contaminants and its application in risk assessment. Regul Toxicol Pharmacol 44:161–171. https://doi.org/10.1016/j.yrtph.2005.10.002
Amiard JC, Amiard TC, Charbonnier L, Mesnil A, Rainbow PS, Wang WX (2008) Bioaccessibility of essential and non-essential metals in commercial shellfish from Western Europe and Asia. Food Chem Toxicol 46:2010–2022. https://doi.org/10.1016/j.fct.2008.01.041
Barrento S, Marques A, Teixeira B, Mendes R, Bandarra N, Vaz-Pires P, Nunes ML (2010) Chemical composition, cholesterol, fatty acid and amino acid in two populations of brown crab Cancer pagurus: Ecological and human health implications. J Food Compos Anal 23:716–725. https://doi.org/10.1016/j.jfca.2010.03.019
Afonso C, Costa S, Cardoso C, Coelho I, Castanheira I, Lourenço H, Gonçalves S, Oliveira R, Carvalho ML, Martins MF, Bandarra NM, Nunes ML (2018) Bioaccessibility in risk-benefit analysis of raw and cooked seabream consumption. J Food Compos Anal 68:118–127. https://doi.org/10.1016/j.jfca.2016.10.003
Oomen AG, Rompelberg CJM, Bruil MA, Dobbe CJG, Pereboom DPKH, Sips AJAM (2003) Development of an in vitro digestion model for estimating the bioaccessibility of soil contaminants. Arch Environ Contam Toxicol 44:281–287. https://doi.org/10.1007/s00244-002-1278-0
Versantvoort CHM, Oomen AG, Vandekamp E, Rompelberg CJM, Sips AJAM (2005) Applicability of an in vitro digestion model in assessing the bioaccessibility of mycotoxins from food. Food Chem Toxicol 43:31–40. https://doi.org/10.1016/j.fct.2004.08.007
Intawongse M, Dean JR (2006) In-vitro testing for assessing oral bioaccessibility of trace metals in soil and food samples. TrAC Trends Anal Chem 25:876–886. https://doi.org/10.1016/j.trac.2006.03.010
Cardoso C, Afonso C, Lourenço H, Costa S, Nunes ML (2015) Bioaccessibility assessment methodologies and their consequences for the risk-benefit evaluation of food. Trends Food Sci Technol 41:5–23. https://doi.org/10.1016/j.tifs.2014.08.008
He M, Ke CH, Tian L, Li HB (2016) Bioaccessibility and health risk assessment of Cu, Cd, and Zn in “colored” oysters. Arch Environ Contam Toxicol 70(3):595–606. https://doi.org/10.1007/s00244-015-0194-z
Simoneau C, Geiss H, Roncari A, Zocchi P, Hannaert P (2001) Validation of methodologies for the release of di-isononyl phthalate (DINP) in saliva simulant from toys, European Commission, DG-Joint Research Centre, Food Products Unit, Institute for Health and Consumer Protection. Ispra, Italy
Cabañero AI, Madrid Y, Camara C (2004) Selenium and mercury bioaccessibility in fish samples: an in vitro digestion method. Anal Chim Acta 526:51–61. https://doi.org/10.1016/j.aca.2004.09.039
Almela C, Laparra JM, Velez D, Barbera R, Farre R, Montoro R (2005) Arsenosugars in raw and cooked edible seaweed: characterization and bioaccessibility. J Agric Food Chem 53:7344–7351. https://doi.org/10.1021/jf050503u
Metian M, Charbonnier L, Oberhaensli F, Bustamante P, Jeffree R, Amiard JC, Warnau M (2009) Assessment of metal, metalloid, and radionuclide bioaccessibility from mussels to human consumers using centrifugation and simulated digestion methods coupled with radiotracer techniques. Ecotoxicol Environ Saf 72:1499–1502. https://doi.org/10.1016/j.ecoenv.2008.10.009
He M, Ke CH, Wang WX (2010) Effects of cooking and subcellular distribution on the bioaccessibility of trace elements in two marine fish species. J Agric Food Chem 58:3517–3523. https://doi.org/10.1021/jf100227n
Houlbreque F, Herve-Fernandez P, Teyssie JL, Oberhaensli F, Boisson F, Jeffree R (2011) Cooking makes cadmium contained in Chilean mussels less bioaccessible to humans. Food Chem 126:917–921. https://doi.org/10.1016/j.foodchem.2010.11.078
He M, Wang WX (2011) Factors affecting the bioaccessibility of methylmercury in several marine fish species. J Agric Food Chem 59:7155–7162. https://doi.org/10.1021/jf201424g
Gu YG, Ning JJ, Ke CL, Huang HH (2018) Bioaccessibility and human health implications of heavy metals in different trophic level marine organisms: a case study of the South China Sea. Ecotoxicol Environ Saf 163:551–557. https://doi.org/10.1016/j.ecoenv.2018.07.114
Noël L, Chafey C, Testu C, Pinte J, Velge P, Guérin T (2011) Contamination levels of lead, cadmium and mercury in imported and domestic lobsters and large crab species consumed in France: differences between white and brown meat. J Food Compos Anal 24(3):368–375. https://doi.org/10.1016/j.jfca.2010.08.011
Wu X, Zhou B, Cheng Y, Zeng C, Wang C, Feng L (2010) Comparison of gender differences in biochemical composition and nutritional value of various edible parts of the blue swimmer crab. J Food Compos Anal 23:154–159. https://doi.org/10.1016/j.jfca.2009.08.007
Maulvault AL, Anacleto P, Lourenço HM, Carvalho ML, Nunes ML, Marques A (2012) Nutritional quality and safety of cooked edible crab (Cancer pagurus). Food Chem 133(2):277–283. https://doi.org/10.1016/j.foodchem.2012.01.023
Barrento S, Marques A, Teixeira B, Carvalho ML, Vaz-Pires P, Nunes ML (2009) Accumulation of elements (S, As, Br, Sr, Cd, Hg, Pb) in two populations of Cancer pagurus: ecological implications to human consumption. Food Chem Toxicol 47(1):150–156. https://doi.org/10.1016/j.fct.2008.10.021
Barrento S, Marques A, Teixeira B, Carvalho ML, Vaz-Pires P, Nunes ML (2009) Influence of season and sex on the contents of minerals and trace elements in brown crab (Cancer pagurus, Linnaeus, 1758). J Agric Food Chem 57:3253–3260. https://doi.org/10.1021/jf8039022
Fu J, Cui Y (2013) In vitro digestion/Caco-2 cell model to estimate cadmium and lead bioaccessibility/bioavailability in two vegetables: the influence of cooking and additives. Food Chem Toxicol 59:215–221. https://doi.org/10.1016/j.fct.2013.06.014
Vinceti M, Venturelli M, Sighinolfi C, Trerotoli P, Bonvicini F, Ferrari A, Bianchi G, Serio G, Bergomi M, Vivoli G (2007) Case-control study of toenail cadmium and prostate cancer risk in Italy. Sci Total Environ 373:77–81. https://doi.org/10.1016/j.scitotenv.2006.11.005
Chavez-Crooker P, Pozo P, Castro H, Dice MS, Boutet I, Tanguy A, Moraga D, Ahearn GA (2003) Cellular localization of calcium, heavy metals, and metallothionein in lobster (Homarus americanus) hepatopancreas. Com Biochem Physiol C Comp Pharmacol 136(3):213–224. https://doi.org/10.1016/S1532-0456(03)00213-8
Rouleau C, Gobeil C, Tjälve H (2001) Cadmium accumulation in the snow crab Chionoecetes opilio. Mar Ecol Prog Ser 224:207–217. https://doi.org/10.3354/meps224207
Wu YL, Cui KD, Zhao HR, Hou LY, Lou QX (1986) Studies of trace metal concentrations in invertebrate from Bohai Sea. Oceanol Limnol Sin 17(6):539–547
Falconer CR, Davies IM, Topping G (1986) Cadmium in edible crabs (Cancer pagurus L.) from Scottish coastal waters. Sci Total Environ 54:173–183. https://doi.org/10.1016/0048-9697(86)90263-9
Wiech M, Vik E, Duinker A, Frantzen S, Bakke S, Maage A (2017) Effects of cooking and freezing practices on the distribution of cadmium in different tissues of the brown crab (Cancer pagurus). Food Control 75:14–20. https://doi.org/10.1016/j.foodcont.2016.12.011
Knutsen H, Wiech M, Duinker A, Maage A (2018) Cadmium in the shore crab Carcinus maenas along the Norwegian coast: geographical and seasonal variation and correlation to physiological parameters. Environ Monit Assess 190:253. https://doi.org/10.1007/s10661-018-6606-6
Nędzarek A, Czerniejewski P, Drost A, Harasimiuk F, Machula S, Tórz A, Masalski P (2017) The distribution of elements in the body of invasive Chinese mitten crabs (Eriocheir sinensis H. Milne-Edwards, 1853) from Lake Dąbie, Poland. J Food Compos Anal 60:1–9. https://doi.org/10.1016/j.jfca.2017.03.003
Nędzarek A, Czerniejewski P, Tórz A (2019) Macro- and trace elements in Chinese mitten crabs (Eriocheir sinensis) from Szczecin Lagoon, Poland-implications for human health. Aquaculture 506:229–237. https://doi.org/10.1016/j.aquaculture.2019.03.042
He J, Wu XG, Long XW, Ma MJ, Huang Q, Zhao HL, Cheng YX (2015) Comparative studies of morphology and biochemical composition between wild-caught and pond-reared juvenile Chinese mitten crab for Yangtze population. J Fish China 39(11):1665–1678 (in Chinese with English abstract)
Rainbow PS (2002) Trace metal concentrations in aquatic invertebrates: why and so what? Environ Pollut 120:497–507. https://doi.org/10.1016/S0269-7491(02)00238-5
Wang CY, Wang XL (2007) Spatial distribution of dissolved Pb, Hg, Cd, Cu and As in the Bohai Sea. J Environ Sci 19:1061–1066. https://doi.org/10.1016/S1001-0742(07)60173-9
Gao XL, Zhou FX, Chen CTA (2014) Pollution status of the Bohai Sea: an overview of the environmental quality assessment related trace metals. Environ Int 62:12–30. https://doi.org/10.1016/j.envint.2013.09.019
Peng ST (2015) The nutrient, total petroleum hydrocarbon and heavy metal contents in the seawater of Bohai Bay, China: temporal-spatial variations, sources, pollution statues and ecological risks. Mar Pollut Bull 95:445–451. https://doi.org/10.1016/j.marpolbul.2015.03.032
Xu XD, Cao ZM, Zhang ZX, Li RH, Hu BQ (2016) Spatial distribution and pollution assessment of heavy metals in the surface sediments of the Bohai and Yellow Seas. Mar Pollut Bull 110:596–602. https://doi.org/10.1016/j.marpolbul.2016.05.079
Laird BD, Shade C, Gantner N, Chan HM, Siciliano SD (2009) Bioaccessibility of mercury from traditional northern country foods measured using an in vitro gastrointestinal model is independent of mercury concentration. Sci Total Environ 407:6003–6008. https://doi.org/10.1016/j.scitotenv.2009.08.014
Cabañero AI, Madrid Y, Camara C (2007) Mercury-selenium species ratio in representative fish samples and their bioaccessibility by an in vitro digestion method. Biol Trace Elem Res 119:195–211. https://doi.org/10.1007/s12011-007-8007-5
Calatayud M, Devesa V, Virseda JR, Barberá R, Montoro R, Vélez D (2012) Mercury and selenium in fish and shellfish: occurrence, bioaccessibility and uptake by Caco-2 cells. Food Chem Toxicol 50:2696–2702. https://doi.org/10.1016/j.fct.2012.05.028
Bragigand V, Berthet B, Amiard JC, Rainbow PS (2004) Estimates of trace metal bioavailability to humans ingesting contaminated oysters. Food Chem Toxicol 42:1893–1902. https://doi.org/10.1016/j.fct.2004.07.011
Dang F, Wang WX (2010) Subcellular controls of mercury trophic transfer to a marine fish. Aquat Toxicol 99:500–506. https://doi.org/10.1016/j.aquatox.2010.06.010
Cano-Sancho G, Perelló G, Maulvault AL, Marques A, Nadal M, Domingo JL (2015) Oral bioaccessibility of arsenic, mercury and methylmercury in marine species commercialized in Catalonia (Spain) and health risks for the consumers. Food Chem Toxicol 86:34–40. https://doi.org/10.1016/j.fct.2015.09.012
JECFA, 2010. Joint FAO/WHO Expert committee on Food Additives. Summary and conclusions of the 73nd meeting of the Joint FAO/WHO Expert Committee on Food Additives (JECFA). JECFA/73/SC. JECFA, Geneva.
Acknowledgments
We thank the two anonymous reviewers for the constructive comments.
Funding
This study was supported by the National Key Research and development Program of China (Grant No. 2017YFC1600702), the Special Scientific Research Funds for Central Non-profit Institutes, Yellow Sea Fisheries Research Institutes (Grant No. 20603022018010), and the Project supported by the Funds for International Cooperation and Exchange of the National Science Foundation of China (No. NSFC-FCT41761134052).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Ethical Approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Zhao, Y., Kang, X., Shang, D. et al. Study of Cd Content Distribution and Its Bioaccessibility in Edible Tissues of Crab Portunus trituberculatus from the Coastal Area of Shandong, China. Biol Trace Elem Res 197, 294–303 (2020). https://doi.org/10.1007/s12011-019-01968-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12011-019-01968-0