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Metals bioaccumulation in two edible bivalves and health risk assessment

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Abstract

Our aim was to quantify the bioaccumulation of 13 metals in two edible bivalves (Ruditapes decussatus and Paphia undulata) in Lake Timsah, Egypt. A potential human health risk assessment was conducted to evaluate the hazards from bivalve consumption. Fe, Al, Zn, and Sr had the highest concentrations in the bivalve samples. The levels of Cd were much lower than the maximum permissible level, while Pb concentrations in the two bivalves were nearly two times the permissible level. The extent of bioaccumulation factor was site- and species-specific. For low and high bivalve-consuming groups, the estimated daily intake of Pb and Cd ranged from 0.01 to 0.76 μg/kg/day. For low and high bivalve-consuming groups, hazard quotients (HQs) for metals were found to be less than 1 for both bivalve species, except for Co in the high-consuming group. In conclusion, even though there was no apparent risk to bivalve consumers from being exposed to single metals, there is a risk from being exposed to the 13 studied metals together, especially for high bivalve-consuming groups such as fishermen.

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References

  • Alfonso, J. A., Handt, H., Mora, A., Vásquez, Y., Azocar, J., & Marcano, E. (2013). Temporal distribution of heavy metal concentrations in oysters Crassostrea rhizophorae from the central Venezuelan coast. Marine Pollution Bulletin, 73, 394–398.

    Article  CAS  Google Scholar 

  • Birch, G. F., Melwani, A., Lee, J.-H., & Apostolatos, C. (2014). The discrepancy in concentration of metals (Cu, Pb and Zn) in oyster tissue (Saccostrea glomerata) and ambient bottom sediment (Sydney estuary, Australia). Marine Pollution Bulletin, 80, 263–274.

    Article  CAS  Google Scholar 

  • Callén, E., Di Virgilio, M., Kruhlak, M. J., Nieto Soler, M., Wong, N., Chen, H. T., Faryabi, R. B., Polato, F. Santos, M. Starnes, L. M. et al. (2013). 53BP1 mediates productive and mutagenic DNA repair through distinct phosphoprotein interactions. Cell, 153, 1266–1280.

  • Campbell, A., Becaria, A., Lahiri, D. K., Sharmanand, K., & Bondy, S. C. (2004). Chronic exposure to aluminum in drinking water increases inflammatory parameters selectively in the brain. Journal of Neuroscience Research, 75, 565–572.

    Article  CAS  Google Scholar 

  • Casas, S., Gonzalez, J. L., Andral, B., & Cossa, D. (2008). Relation between metal concentration in water and metal content of marine mussels (Mytilus galloprovincialis): impact of physiology. Environmental Toxicology & Chemistry, 27(7), 1543–1552.

    Article  CAS  Google Scholar 

  • Chary, N. S., Kamala C. T. & Raj, D. S. S. (2008). Assessing risk of heavy metals from consuming food grown on sewage irrigated soils and food chain transfer. Ecotoxicology Environmental Safty, 69, 513–524.

  • Chevereuil, M., Blanchard, M., Teil, M. J., Carru, A. M., Testard, P., & Chesterikoff, A. (1996). Evaluation of the pollution by organochlorine compound (polychlorobiphenyles and pesticides) and metals (Cd, Cr, Cu and Pb) in the water and in the zebra mussel (Dreissena polymorpha pallas) of the river Seine. Water, Air, & Soil Pollution, 88, 371–381.

    Article  Google Scholar 

  • Damek-Proprawa, M., & Sawicka-Kapusta, K. (2003). Damage to the liver; kidney and testis with reference to burden of heavy metals in yellow-necked mice from areas around steelworks and zinc smelters in Poland. Toxicology, 186, 1–10.

    Article  Google Scholar 

  • Davies, O. A., Allison, M. E., & Uyi, H. S. (2006). Bioaccumulation of heavy metals in water, sediment and periwinkle (Tympanotonus fuscatus var radula) from the Elechi Creek, Niger Delta. African Journal of Biotechnology, 5(10), 68–73.

    Google Scholar 

  • El Nemr, A., Khaled, A., Moneer, A. A., & El Sikaily, A. (2012). Risk probability due to heavy metals in bivalve from Egyptian Mediterranean coast. The Egyptian Journal of Aquatic Research, 38, 67–75.

    Article  Google Scholar 

  • El-Shenawy, N. S. (2002). The effects of metal bioaccumulation on glutathione and lipid peroxidation as biomarkers of aquatic ecosystem pollution of Ruditapes decussatus and Venerupis pullastra feom lake Timsah, Ismailia. Egyptian Journal of Zoology, 39, 475–492.

    Google Scholar 

  • Empire Test Pilots’ School (ETPS). (1995). Environmental testing of pollution status in Lake Temsah. Ismailia: Abu-Attwa water Reuse Center Research and Training.

    Google Scholar 

  • EU. (2006). Setting maximum levels for certain contaminants in food stuffs. Commission Regulation (EC) No 1881/ 2006. Journal of the European Union, 364, 5–24.

    Google Scholar 

  • European Commission Development Group (ECDG) (2002). ENV. E3 Project ENV. E.3/ETU/0058. Heavy metals in waste, final report.

  • FAO. (1983). Compilation of legal limits for hazardous substances in fish and fishery products. Rome: FAO Fishery Circular. 464 pp.

    Google Scholar 

  • FAO/WHO. (2000). Evaluation of certain food additives and contaminants: fifty-third report of the Joint FAO/WHO Expert Committee on Food Additives. Geneva: WHO. WHO Technical Report Series, No. 896 128 pp.

    Google Scholar 

  • FAO/WHO. (2004). Summary of evaluations performed by the Joint FAO/WHO Expert Committee on Food Additives (JECFA 1956–2003). Washington,DC: ILSI Press International Life Sciences Institute.

    Google Scholar 

  • FAO/WHO. (2013). Codex alimentarius commission. Procedural manual. 21th ed.

  • Food and Nutrition Board. (2004). Dietary reference intakes [DRIs]: recommended intakes for individuals. Washington, DC, USA: National Academy of Sciences.

    Google Scholar 

  • Förstner, U., & Wittmann, G. T. W. (1981). Metal pollution in the aquatic environment. Berlin Heidelberg: Springer.

    Book  Google Scholar 

  • Freije, A. M. (2015). Heavy metal, trace element and petroleum hydrocarbon pollution in the Arabian Gulf: review. The Journal of the Association of Arab Universities for Basic and Applied Sciences, 17, 90–100.

    Google Scholar 

  • Furumai, H., Balmer, H., & Boller, M. (2002). Dynamic behavior of suspended pollutants and particle size distribution in highway runoff. Water Science Technology, 46(11–12), 413–418.

    CAS  Google Scholar 

  • Gabr, H. R., & Gab-Alla, A. (2008). Effect of transplantation on heavy metal concentrations in commercial clams of Lake Timsah, Suez Canal, Egypt. Oceanology, 50(1), 83–93.

    Google Scholar 

  • Guerra, K., Konz, J., Lisi, K., & Neebrem, C. (2010). Exposure factors handbook. Washington DC: USEPA.

    Google Scholar 

  • Hamza-Chaffai, A., Amiard, J. C., & Cosson, R. P. (1999). Relationship between metallothionein and metals in a natural population of clam Ruditapes decussatus from Sfax coast, a non-linear model using Box–Cox transformation. Comparative Biochemistry and Physiology, 123, 153–163.

    CAS  Google Scholar 

  • Hogstrand, C., & Haux, C. (2001). Binding and detoxification of heavy metals in lower vertebrates with reference to metallothionein. Comparative Biochemistry and Physiology, 100, 137–214.

    Google Scholar 

  • Huang, X., Hites, R. A., Foran, J. A., Hamilton, C., Knuth, B. A., Schwager, S. J., & Carpenter, D. O. (2006). Consumption advisories for salmon based on risk of cancer and noncancer health effects. Environmental Research, 101, 263–274.

    Article  CAS  Google Scholar 

  • Ibrahim, N. K., & Abu El-Regal, M. (2014). Heavy metals accumulation in marine edible molluscs, Timsah Lake, Suez Canal, Egypt. ARPN Journal of Science and Technology-International, 4(4), 282–288.

    Google Scholar 

  • Jebalia, J., Choubab, L., Bannia, M., & Boussettaa, H. (2014). Comparative study of the bioaccumulation and elimination of trace metals (Cd, Pb, Zn, Mn and Fe) in the digestive gland, gills and muscle of bivalve Pinna nobilis during a field transplant experiment. Journal of Trace Elements in Medicine & Biology, 28(2), 212–217.

    Article  Google Scholar 

  • JEFCA. (2001). Expert Committee on Food Additives (JECFA) 57th session held on Rome. Rome: JEFCA.

    Google Scholar 

  • Jovic, M., Onjia, A., & Stankovic, S. (2011). Toxic metal health risk by mussels consumption. Environmental Chemistry Letters, 10, 69–77.

    Article  Google Scholar 

  • Kamel, K. A. (2013). Phytoremediation potentiality of aquatic macrophytes in heavy metal contaminated water of El-Temsah Lake, Ismailia, Egypt. Middle-East Journal of Science and Research, 14(12), 1555–1568.

    Google Scholar 

  • Kim, J.-Y., & Sansalone, J. J. (2008). Event-based size distributions of particulate matter transported during urban rainfall-runoff events. Water Research, 42(10–11), 2756–2768.

    Article  CAS  Google Scholar 

  • Krewski, D., Yokel, R. A., Nieboer, E., Borchelt, D., Cohen, J., Harry, J., et al. (2007). Human health risk assessment for aluminium, aluminium oxide, and aluminium hydroxide. Journal of Toxicology and Environmental Health, Part B: Critical Reviews, 1, 1–269.

    Article  Google Scholar 

  • Labrot, F., Narbonne, J. F., Ville, P., Saint Denis, M., & Ribera, D. (1999). Acute toxicity, toxicokinetics, and tissue target of lead and uranium in the clam Corbicula fluminea and the worm Eisenia fetida: comparison with the fish Brachydanio rerio. Archives of Environmental Contamination and Toxicology, 36, 167–178.

    Article  CAS  Google Scholar 

  • Loutfy, N., Mentler, A., Shoeab, M., Ahmed, M. T., & Fuerhacker, M. (2012). Analysis and exposure assessment of some heavy metals in foodstuffs from Ismailia city, Egypt. Environmental Toxicology & Chemistry, 94, 78–90.

    Article  CAS  Google Scholar 

  • Mcgeer, J. C., Brix, K. V., Skeaff, J. M., DeForest, D. K., Brigham, S. I., Adams, W. J., & Green, A. (2003). Inverse relationship between bioconcentration factor and exposure concentration for metals: implications for hazard assessment of metals in the aquatic environment. Environmental Toxicology & Chemistry, 22(5), 1017–1037.

    Article  CAS  Google Scholar 

  • National Academy of Sciences. (1980). The international mussel watch. Washington, DC: National Academy of Sciences (NAS). 213 pp.

    Google Scholar 

  • NRC (National Research Council). (1995). Wetlands: characteristics and boundaries. Washington, DC: National Academy Press.

    Google Scholar 

  • Oliveira, R. C. A., Schatzmann, M., Silva de Assis, H. C., Silva, P. H., & Pelletier, E. (2002). Evaluation of tributyltin subchronic effects in tropical freshwater fish (Astyanax bimaculatus, Linnaeus, 1758). Ecotoxicology and Environmental Safety, 51, 161–167.

    Article  Google Scholar 

  • Otchere, F. A. (2003). Heavy metals concentrations and burden in the bivalves (Anadara (Senilia) senilis, Grassostrea tulipa and Perna perna) from lagoons in Ghana: model to describe mechanism of accumulation/excretion. African Journal of Biotechnology, 2(9), 280–287.

    Article  CAS  Google Scholar 

  • Ponnusamy, K., Sivaperumal, P., Suresh, M., Arularasan, S., Munilkumar, S., & Pal, A. K. (2014). Heavy metal concentration from biologically important edible species of bivalves (Perna viridis and Modiolus metcalfei) from Vellar Estuary, South East Coast of India. Journal of Aquaculture Research and Development, 5, 258. doi:10.4172/2155-9546.1000258.

    Google Scholar 

  • Rainbow, P. S. (2007). Trace metal bioaccumulation: models, metabolic availability and toxicity. Environment International, 33, 576–582.

    Article  CAS  Google Scholar 

  • Rainbow, P. S., & Luoma, S. N. (2011). Metal toxicity, uptake and bioaccumulation in aquatic invertebrates modelling zinc in crustaceans. Aquatic Toxicology, 105(3), 455–465.

    Article  CAS  Google Scholar 

  • Raposo, J. C., Bartolome, E. L., Cortazar, E. E., Arana, E. J., Zabaljauregui, E. M., de Diego, E. M., Zuloaga, E. O., Madariaga, E. J. M., & Etxebarria, E. M. (2009). Trace metals in oysters, Crassotrea sps. From UNESCO protected natural reserve of Urdaibai: space-time observations and source identification. Bulletin of Environmental Contamination and Toxicology, 83, 223–229.

    Article  CAS  Google Scholar 

  • ShibiniMol, P. A., Raveendrana, R., & Sujathaa, C. H. (2015). Elucidation of contaminant-induced toxic responses in the biota of Lake Vembanad, Kerala, India. Human and Ecological Risk Assessment: An International Journal, 21, 1576–1592.

    Article  CAS  Google Scholar 

  • Singh, A., Sharm, R. K., Agrawal, M., & Marshall, F. M. (2010). Health risk assessment of heavy metals via dietary intake of foodstuffs from the wastewater irrigated site of a dry tropical area of India. Food and Chemical Toxicology, 48, 611–619.

    Article  CAS  Google Scholar 

  • Soliman, M. F. M., El-Shenawy, N. S., Tadros, M. M., & Abd El-Azeez, A. A. (2015). Impaired behavior and changes in some biochemical markers of bivalve (Ruditapes decussatus) due to zinc toxicity. Toxicological & Environmental Chemistry. doi:10.1080/02772248.2015.1058381.

    Google Scholar 

  • Spada, M., Jorba, O., García-Pando, P. C., Janjic, Z., & Baldasano, J. M. (2013). Modeling and evaluation of the global sea-salt aerosol distribution: sensitivity to size-resolved and sea-surface temperature dependent emission schemes. Atmospheric Chemistry and Physics, 13, 11735–11755.

    Article  CAS  Google Scholar 

  • Stankovic, S., Jovic, M., Stankovic, A. R., & Katsikas, L. (2012). Heavy metals in seafood mussels. Risk for human health. In E. Lichtfouse, J. Schwarzbauer, & D. Robert (Eds.), Environmental chemistry for a sustainable world. Volume 1: nanotechnology and health risk (pp. 311–373). Netherlands: Springer.

    Chapter  Google Scholar 

  • Szefer, P., Ali, A. A., Ba-Haroon, A. A., Rajeh, A. A., Gełdon, J., & Nabrzyski, M. (1999). Distribution and relationships of selected trace metals in molluscs and associated sediments from the Gulf of Aden, Yemen. Environmental Pollution, 106, 299–314.

    Article  CAS  Google Scholar 

  • Tao, Y., Yuan, Z., Xiaona, H., & Wei, M. (2012). Distribution and bioaccumulation of heavy metals in aquatic organisms of different trophic levels and potential health risk assessment from Taihu Lake, China. Ecotoxicology and Environmental Safety, 81, 55–64.

    Article  CAS  Google Scholar 

  • USEPA. (1997). Health effects assessment summary tables (HEAST). United States Environmental Protection Agency, Washington DC.

  • USEPA. (2000). Risk-based concentration table. Philadelphia: United States Environmental Protection Agency, Washington DC.

    Google Scholar 

  • USEPA. (2002). Region 9, Preliminary Remediation Goals. http://www.epa.Gov/region09/waste/sfund/prg

  • USEPA. (2008). Cosden Oil & Chemical Co. ecological risk assessment. http://www.epa.gov/region5superfund/ecology/html/casestudies/cosdenoil.htm

  • US EPA. (2009). Final report: integrated science assessment for particulate matter. United States Environmental Protection Agency, Washington DC.

  • USEPA. (2010). Risk-based concentration table. Washington, DC: United State Environmental Protection Agency.

    Google Scholar 

  • USEPA. (2012). Human health risk assessment. Available: http://www.epa.gov/risk/health-risk.htm [Accessed 22 July 2013].

  • USEPA. (2013). Reference dose (RfD): description and use in health risk assessments, Background Document 1A, Integrated risk information system (IRIS). United States Environmental Protection Agency: Washington, DC http://www.epa.gov/iris/rfd.htm.

  • Wang, W. X., & Rainbow, P. S. (2000). Dietary uptake of Cd, Cr, and Zn in the barnacle Balanus trigonus: influence of diet composition. Marine Ecology Progress Series, 204, 159–168.

    Article  CAS  Google Scholar 

  • WHO. (1989). Heavy metals-environmental aspects. Environment health criteria No. 85. Geneva: World Health Organization.

    Google Scholar 

  • WHO. (2006). Evaluation of certain contaminants in food: sixty-fourth report of the Joint FAO/WHO Expert Committee on Food Additives. Geneva: WHO. WHO Technical Report Series, No. 930 100 pp.

    Google Scholar 

  • Yujun, Y., Zhifeng, Y., & Shanghong, Z. (2011). Ecological risk assessment of heavy metals in sediment, and Basin. Journal of Environmental Pollution, 159, 2575–2585.

    Article  Google Scholar 

  • Zhao, L., Yang, F., Yan, X., Huo, Z., & Zhang, G. (2012). Heavy metal concentrations in surface sediments and manila clams (Ruditapes philippinarum) from the Dalian coast, China after the Dalian Port oil spill. Biological Trace Element Research, 149, 241–247.

    Article  CAS  Google Scholar 

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Correspondence to Nahla S. EL-Shenawy.

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EL-Shenawy, N.S., Loutfy, N., Soliman, M.F.M. et al. Metals bioaccumulation in two edible bivalves and health risk assessment. Environ Monit Assess 188, 139 (2016). https://doi.org/10.1007/s10661-016-5145-2

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