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Occurrence and Bioaccumulation of Semicarbazide in Shellfish from Three Aquaculture Bays, Northern Shandong, China, Using UPLC–MS/MS Method

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Abstract

To assess the correlation of semicarbazide contents between shellfish and the environment, semicarbazide was determined in samples from 11 sites in Jincheng Bay, Sishili Bay, and Laizhou Bay in northern Shandong Province, China. In total, 69 shellfish, 37 seawater, and 37 sediment samples were analyzed using ultra performance liquid chromatography tandem mass spectrometry (UPLC–MS/MS). Semicarbazide contents in the shellfish were lower than 1.00 μg/kg, with bioaccumulation factors (BAFs) ranging within 4.47–18.9 L/kg. The semicarbazide contents in seawater were 0.021 ± 0.002 to 0.085 ± 0.003 μg/L, with BAFs ranging from 6.15 ± 1.31 to 12.5 ± 1.79. Semicarbazide was not detected in sediment. The amount of semicarbazide accumulated from the marine environment of the three bays and the BAF values showed a positive correlation; the semicarbazide content increased with increases in shell length. Additionally, the potential pathways of semicarbazide intake were assessed. Semicarbazide in microalgae (the main food source of filter feeding shellfish) could potentially affect its accumulation in shellfish and increase the BAFs determined using actual environmental samples relative to those obtained in laboratory studies. Semicarbazide BAF values in shellfish were much lower than those for fat-soluble compounds such as amantadine. Enrichment via microalgae was a possible pathway for semicarbazide to accumulate in shellfish. Long-term monitoring will help evaluate the behaviour of semicarbazide in the environment. This research will be useful for further assessments of semicarbazide and as the reference data for determining the effects of semicarbazide on marine organisms.

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REFERENCES

  1. Raja, R., Seshadri, S., Santhanam, V., et al., Growth and characterization of nonlinear optical crystal – Semicarbazide picrate, J. Mol. Struct., 2017, vol. 1147, pp. 515–519.

    Article  CAS  Google Scholar 

  2. Tarek, M., Zaki, M., Fawzy, M.H., et al., Application of rhodanine, fluorene and semicarbazide hydrochloride as new spectrophotometric reagents for quinones, Microchim. Acta, 1986, vol. 90, pp. 321–328.

    Article  Google Scholar 

  3. Nardelli, M., Fava, G., and Giraldi, G., The crystal and molecular structure of semicarbazide hydrochloride, Acta Crystallogr., 1965, vol. 19, no. 6, pp. 1038–1042.

    Article  CAS  Google Scholar 

  4. Becalski, A., Lau, B.P.Y., Lewis, D., et al., Semicarbazide in Canadian bakery products, Food Addit. Contam. A, 2006, vol. 23, no. 2, pp. 107–109.

    Article  CAS  Google Scholar 

  5. Becalski, A., Lau, B.P.Y., Lewis, D., et al., Semicarbazide formation in azodicarbonamide-treated flour: A model study, J. Agric. Food Chem., 2004, vol. 52, pp. 5730–5734.

    Article  CAS  PubMed  Google Scholar 

  6. Commission Decision no. 2003/181/EC, Publication Office of the European Union, 2003.

  7. A Rule by the Food and Drug Administration on 02/06/2002 (Topical nitrofurans; extralabel animal drug use; order of prohibition), Federal Register, 2002, 67 FR 5470.

  8. The Ministry of Agriculture Bulletin of PRC, Beijing: Ministry of Agriculture of the People’s Republic of China, 2002.

  9. Yu, M., Zhang, X., Guo, L., et al., Anti-estrogenic effect of semicarbazide in female zebrafish (Danio rerio) and its potential mechanisms, Aquat. Toxicol., 2016, vol. 170, pp. 262–270.

    Article  CAS  PubMed  Google Scholar 

  10. Hirakawa, K., Midorikawa, K., Oikawa, S., et al., Carcinogenic semicarbazide induces sequence-specific DNA damage through the generation of reactive oxygen species and the derived organic radicals, Mutat. Res., 2003, vol. 536, nos. 1–2, pp. 91–101.

    Article  CAS  PubMed  Google Scholar 

  11. Wang, Y., Chan, H.W., and Chan, W., Facile formation of a DNA adduct of Semicarbazide on reaction with apurinic/apyrimidinic Sites in DNA, Chem. Res. Toxicol., 2016, vol. 29, no. 5, pp. 834–840.

    Article  CAS  PubMed  Google Scholar 

  12. Takahashi, M., Yoshida, M., Inoue, K., et al., Chronic toxicity and carcinogenicity of semicarbazide hydrochloride in Wistar Hannover GALAS rats, Food Chem. Toxicol., 2014, vol. 73, pp. 84–94.

    Article  CAS  PubMed  Google Scholar 

  13. Opinion of the Scientific Panel on food additives, flavourings, processing aids and materials in contact with food (AFC) related to Treatment of poultry carcasses with chlorine dioxide, acidified sodium chlorite, trisodium phosphate and peroxyacids, EFSA, 2005, vol. 297, pp. 1–27. https://doi.org/10.2903/j.efsa.2006.297

  14. Opinion of the scientific panel on food additives, flavourings, processing aids and materials in contact with food (AFC) related to semicarbazide in food, EFSA, 2005, vol. 219, pp. 1–36. https://doi.org/10.2903/j.efsa.2005.219

  15. Weisburger, E.K., Ulland, B.M., Nam, J., et al., Carcinogenicity tests of certain environmental and industrial chemicals, J. Natl. Cancer Inst.,1981, vol. 67, no. 1, pp. 75–88.

    CAS  PubMed  Google Scholar 

  16. Parodi, S., De Flora, S., Cavanna, M., et al., DNA-damaging activity in vivo and bacterial mutagenicity of sixteen hydrazine derivatives as related quantitatively to their carcinogenicity, Cancer Res., 1981, vol. 41, no. 4, pp. 1469–1482.

    CAS  PubMed  Google Scholar 

  17. Toth, B., A review of the natural occurrence, synthetic production and use of carcinogenic hydrazines and related chemicals, In Vivo, 2000, vol. 14, no. 2, pp. 299–319.

    CAS  PubMed  Google Scholar 

  18. Tian, X., Xu, Y., Gong, X., et al., Environmental status and early warning value of the pollutant Semicarbazide in Jincheng and Sishili Bays, Shandong Peninsula, China, Sci. Total Environ., 2017, vol. 576, pp. 868–878.

    Article  CAS  PubMed  Google Scholar 

  19. Tian, X., Xu, Y., Song, X., et al., Temporal and spatial distribution of semicarbazide in western Laizhou Bay, Mar. Pollut. Bull., 2016, vol. 112, nos. 1–2, pp. 393–398.

    Article  CAS  PubMed  Google Scholar 

  20. Gao, S., Wang, W., Tian, H., et al., An emerging water contaminant, Semicarbazide, exerts an anti-estrogenic effect in zebrafish (Danio rerio), Bull. Environ. Contam. Toxicol., 2014, vol. 93, pp. 280–288.

    Article  CAS  PubMed  Google Scholar 

  21. Zhang, L.M., Safety assessment and monitoring system of shellfish culture of Yellow Sea and Bohai Sea, J. Ocean Press (China), 2014, pp.1–5.

    Google Scholar 

  22. Partelow, S., von-Wehrden, H., and Horn, O., Pollution exposure on marine protected areas: A global assessment, Mar. Pollut. Bull., 2015, vol. 100, no. 1, pp. 352–358.

    Article  CAS  PubMed  Google Scholar 

  23. Fleming, L.E., Broad, K., Clement, A., et al., Oceans and human health: Emerging public health risks in the marine environment, Mar. Pollut. Bull., 2006, vol. 53, nos. 10–12, pp. 545–560.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Lee, J.H., Birch, G.F., Cresswell, T., et al., Dietary ingestion of fine sediments and microalgae represent the dominant route of exposure and metal accumulation for Sydney rock oyster (Saccostrea glomerata): A biokinetic model for zinc, Aquat. Toxicol., 2015, vol. 167, pp. 46–54.

    Article  CAS  PubMed  Google Scholar 

  25. Burkhard, L.P., Endicott, D.D., Cook, P.M., et al., Evaluation of two methods for prediction of bioaccumulation factors, Environ. Sci. Technol., 2003, vol. 37, no. 20, pp. 4626–4634.

    Article  CAS  PubMed  Google Scholar 

  26. Wong, C.S., Capel, P.D., and Nowell, L.H., National-scale, field-based evaluation of the biota-sediment accumulation factor model, Environ. Sci. Technol., 2001, vol. 35, no. 9, pp. 1709–1715.

    Article  CAS  PubMed  Google Scholar 

  27. Zhang, X., Chen, S., Xu, H., et al., Identification and occurrence of endogenous semicarbazide in prawns and crabs from Zhejiang Province, China, Food Addit. Contam., Part A, 2016, vol. 33, pp. 252–258.

    Google Scholar 

  28. Xu, Y., Ren, C., Han, D., et al., Analysis of amantadine in Laminaria Japonica and seawater of Daqin Island by ultra high performance liquid chromatography with positive electrospray ionization tandem mass spectrometry, J. Chromatogr. B: Anal. Technol. Biomed. Life Sci., 2019, vols. 1126–1127, 121697.

    Article  Google Scholar 

  29. DeForest, D.K., Brix, K.V., and Adams, W.J., Assessing metal bioaccumulation in aquatic environments: The inverse relationship between bioaccumulation factors, trophic transfer factors and exposure concentration, Aquat. Toxicol., 2007, vol. 84, pp. 236–246.

    Article  CAS  PubMed  Google Scholar 

  30. Arnot, J.A. and Gobas, F.A.P.C., A review of bioconcentration factor (BCF) and bioaccumulation factor (BAF) assessments for organic chemicals in aquatic organisms, Environ. Rev., 2006, vol. 14, pp. 257–297.

    Article  CAS  Google Scholar 

  31. Xu, Y.J., Sun, Y.Z., Song, X.K., et al., Survey of semicarbazide contamination in coastal waters adjacent to the Chaohe River estuary, Oceanol. Limnol. Sin., 2010, vol. 41, no. 4, pp. 538–545.

    CAS  Google Scholar 

  32. Xiu-Hui, T., Wei-Yun, Z., Ying-Jiang, X., et al., Rules of accumulation and elimination of semicarbazide residue from different sources in Apostichopus japonicus, J. Food Saf. Food Qual., 2020, vol. 11, pp. 29–37.

    Google Scholar 

  33. Franke, C., Studinger, G., Berger, G., et al., The assessment of bioaccumulation, Chemosphere, 1994, vol. 29, no. 7, pp. 1501–1514.

    Article  CAS  Google Scholar 

  34. Lerche, D., van de Plassche, E., Schwegler, A., et al., Selecting chemical substances for the UN-ECE POP protocol, Chemosphere, 2002, vol. 47, no. 6, pp. 617–630.

    Article  CAS  PubMed  Google Scholar 

  35. Zhang, Y., Lu, X., Wang, N., et al., Heavy metals in aquatic organisms of different trophic levels and their potential human health risk in Bohai Bay, China, Environ. Sci. Pollut. Res. Int., 2016, vol. 23, pp. 17801–17810.

    Article  CAS  PubMed  Google Scholar 

  36. Berry, J. P., Jaja-Chimedza, A., Davalos-Lind, L., et al., Apparent bioaccumulation of cylindrospermopsin and paralytic shellfish toxins by finfish in Lake Catemaco (Veracruz, Mexico), Food Addit. Contam., Part A, 2012, vol. 29, pp. 314–321.

    Article  CAS  Google Scholar 

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ACKNOWLEDGMENTS

We thank Gareth Thomas, PhD, and Kara Bogus, PhD, from Liwen Bianji, Edanz Group China (www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript.

Funding

The work was supported by the Science Foundation of Shandong Province (grant no. ZR2021MD046), the Guangdong Foundation for Program of Science and Technology Research (grant no. 2020B1212060053), and the Modern Agri-industry Technology Research System in Shandong Province (grant no. SDAIT-14-08 and no. SDAIT-26-05).

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Authors and Affiliations

  1. Shandong Marine Resource and Environment Research Institute, 264006, Yantai, China

    Xiuhui Tian, Xiuzhen Zhang, Xiukai Song, Xianghong Gong, Dianfeng Han, Huawei Zhang, Ling Cheng, Yuting Zhao, Xin Liu, Yingjiang Xu & Huanjun Li

  2. State Key Laboratory of Organic Geochemistry and Guangdong Key Laboratory of Environmental Protection and Resources Utilization, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, 510640, Guangzhou, China

    Xiaojun Luo

  3. Shandong Freshwater Fisheries Research Institute, 250014, Jinan, China

    Mengmeng Wu

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  1. Xiuhui Tian
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Correspondence to Yingjiang Xu or Huanjun Li.

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Tian, X., Wu, M., Zhang, X. et al. Occurrence and Bioaccumulation of Semicarbazide in Shellfish from Three Aquaculture Bays, Northern Shandong, China, Using UPLC–MS/MS Method. Russ J Mar Biol 48, 342–352 (2022). https://doi.org/10.1134/S1063074022050200

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  • DOI: https://doi.org/10.1134/S1063074022050200

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