Skip to main content

Advertisement

Springer Nature Link
Log in

Immunotoxicological effects of dioxin-like polychlorinated biphenyls extracted from Zhanjiang Bay sediments in zebrafish

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

Dioxin-like polychlorinated biphenyls (DLPCBs) are ubiquitous environmental contaminants spread all over the world. They can cause disorders in the reproductive, nervous, gut, and immune systems. We investigated the effects of DL-PCB extracted from Zhanjiang (Guangdong Province, China) offshore area on the immune functions of adult zebrafish. Zebrafish were exposed to different levels of DL-PCBs, i.e., control, positive control (PCB77 at 16.0 μg/L), low (LD; PCB81 + PCB118 at 0.32 μg/L), and high-dose (HD; PCB81 + PCB118 at 16.0 μg/L) groups for 28 days. Compared with the control group, positive control and HD group showed a significant decrease (P < 0.05) in the number of red blood cells (RBC) on day 7 and the same decrease was observed in the LD group (P < 0.05) on day 21. The results of white blood cell (WBC) profiles were opposite to that of RBCs. Moreover, the serum lysozyme activity was significantly lower in positive control and HD group (P < 0.05) on day 21 but no significant effect was observed in the LD group. The mucus lysozyme activity and immunoglobulin concentration in positive control and HD group decreased significantly (P < 0.05) from day 14. A similar effect was observed in the LD group but was significant (P < 0.05) only on day 28. Additionally, histopathological examination showed accumulation of hemosiderin in the spleen of experimental animals, which was significant in positive control and HD group. Further, renal tubular epithelial cells of head kidney were swollen in the positive control and HD group while the expansion of lumen and renal interstitial edema was observed in the LD group on day 21 and with significant presence on 28 days. Therefore, these findings suggest that the exposure of zebrafish to DL-PCBs at > 16.0 μg/L can impair their immune functions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Abrha, Y., & Raghavan, D. (2000). Polychlorinated biphenyl (PCB) recovery from spiked organic matrix using accelerated solvent extraction (ASE) and Soxhlet extraction. Journal of Hazardous Materials, 80(1–3), 147–157.

    Article  CAS  Google Scholar 

  • Belair, C. D., Peterson, R. E., & Heideman, W. (2001). Disruption of erythropoiesis by dioxin in the zebrafish. Developmental Dynamics, 594, 581–594.

    Article  Google Scholar 

  • Berg, V., Lyche, J. L., Karlsson, C., Stavik, B., Nourizadeh-Lillabadi, R., Hårdnes, N., Skaare, J. U., Alestrøm, P., Lie, E., & Ropstad, E. (2011). Accumulation and effects of natural mixtures of persistent organic pollutants (POP) in zebrafish after two generations of exposure. Journal of Environmental Science and Health, Part A, 74, 407–423.

    CAS  Google Scholar 

  • Boucher, M. P., Lefebvre, C., & Chapados, N. A. (2015). The effects of PCB126 on intra-hepatic mechanisms associated with non alcoholic fatty liver disease. Journal of Diabetes & Metabolic Disorders, 14, 88.

    Article  Google Scholar 

  • Chang, K. J., Lu, F. J., Tung, T. C., & Lee, T. P. (1980). Studies on patients with polychlorinated biphenyl poisoning. 2. Determination of urinary coproporphyrin, uroporphyrin, delta-aminolevulinic acid and porphobilinogen. Research Communications in Chemical Pathology and Pharmacology, 30(3), 547–554.

    CAS  Google Scholar 

  • Chen, L., Zhang, W., Hua, J., Hu, C., Lok-Shun, L. N., Qian, P. Y., Lam, P. K. S., Lam, J. C. W., & Zhou, B. (2018). Dysregulation of intestinal health by environmental pollutants: involvement of the estrogen receptor and Aryl Hydrocarbon receptor. Environmental Science Technology, 52(4), 2323–2330.

    Article  CAS  Google Scholar 

  • Chun-Feng, L., Wang, Y. M., Peng, S. Q., Zou, L. B., Tan, D. H., Liu, G., Fu, Z., & Wang, Q. X. (2009). Combined effects of repeated administration of 2,3,7,8-tetrachlorodibenzo-p-dioxin and polychlorinated biphenyls on kidneys of male rats. Archives of Environmental Contamination and Toxicology, 57(4), 767–776.

    Article  Google Scholar 

  • Corte, A. (2006). Ontogeny of the immune system of fish. Fish Shellfish Immunology, 20, 126–136.

    Article  Google Scholar 

  • Desforges, J. P. W., Sonne, C., Levin, M., Siebert, U., De-Guise, S., & Dietz, R. (2016). Immunotoxic effects of environmental pollutants in marine mammals. Environment International, 86, 126–139.

    Article  CAS  Google Scholar 

  • Ellis, A. E. (2001). Innate host defense mechanisms of fish against viruses and bacteria. Developmental and Comparative Immunology, 25(8–9), 827–839.

    Article  CAS  Google Scholar 

  • Forsatkar, M. N., Sarfari, O., & Boiti, C. (2017). Effects of social isolation on growth, stress response, and immunity of zebrafish. Acta Ethologica, 20(3), 255–261.

    Article  Google Scholar 

  • Haddad, S., Poulin, P., & Krishnan, K. (2000). Relative lipid content as the sole mechanistic determinant of the adipose tissue: blood partition coefficients of highly lipophilic organic chemicals. Chemosphere, 40(8), 839–843.

    Article  CAS  Google Scholar 

  • Han, X. B., Yuen, K. W., & Wu, R. S. (2013). Polybrominated diphenyl ethers affect the reproduction and development, and alter the sex ratio of zebrafish (Danio rerio). Environmental Pollution, 182, 120–126.

    Article  CAS  Google Scholar 

  • Hartung, T., & Corsini, E. (2013). Immunotoxicology: challenges in the 21st century and in vitro opportunities. Altex, 30, 411–426.

    Article  Google Scholar 

  • Jin, Y. X., Wu, S., Zeng, Z., & Fu, Z. (2017). Effects of environmental pollutants on gut microbiota. Environmental Pollution, 222, 1–9.

    Article  CAS  Google Scholar 

  • Khong, H. K., Kuah, M. K., Jaya-Ram, A., & Shu-Chien, A. C. (2009). Prolactin receptor mRNA is upregulated in discus fish (Symphysodon aequifasciata) skin during parental phase. Comparative Biochemistry and Physiology, 153(1), 18–28.

    Article  Google Scholar 

  • Li, M., Wang, X., Zhu, J., Zhu, S., Hu, X., Guo, X., Yu, Z., & Han, S. (2014). Toxic effects of polychlorinated biphenyls on cardiac development in zebrafish. Molecular Biology Reports, 41(12), 7973–7983.

    Article  CAS  Google Scholar 

  • Liu, X., & Haiyan, G. Z. (2009). Study on the tissue and tissue structure of the head and kidney of the yellow catfish. Journal of Water Ecology, 30(3), 108–110.

    CAS  Google Scholar 

  • Luster, M. I., & Gerberick, G. F. (2010). Immunotoxicology testing: past and future. Methods in Molecular Biology, 598, 3–13.

    Article  CAS  Google Scholar 

  • Mazon, A. F., Monteiro, E. A. S., Pinheiro, G. H. D., & Fernadez, M. N. (2002). Hematological and physiological changes induced by short-term exposure to copper in the freshwater fish, Prochilodus scrofa. Brazilian Journal of Medical and Biological Research, 62(4A), 621–631.

    Article  CAS  Google Scholar 

  • Péan, S., Daouk, T., Vignet, C., Lyphout, L., Leguay, D., Loizeau, V., Bégout, M. L., & Cousin, X. (2013). Long-term dietary-exposure to non-coplanar PCBs induces behavioral disruptions in adult zebrafish and their offspring. Neurotoxicology and Teratology, 39, 45–56.

    Article  Google Scholar 

  • Safari, R., Hoseinifar, S. H., Nejadmoghadam, S., & Jafar, A. (2016). Transciptomic study of mucosal immune, antioxidant and growth related genes and non-specific immune response of common carp(Cyprinus carpio) fed dietary Ferula (Ferula assafoetida). Fish & Shellfish Immunology, 55, 242–248.

    Article  CAS  Google Scholar 

  • Scinicariello, F., & Buser, M. C. (2015). Polychlorinated biphenyls and leukocyte telomere length: an analysis of NHANES 1999–2002. Ebiomedicine, 2(12), 1974–1979.

    Article  Google Scholar 

  • Shen, Y., Wang, D., & Zhao, J. X. (2018). Fish red blood cells express immune genes and responses. Aquaculture and Fisheries, 3(1), 14–21.

    Article  Google Scholar 

  • Shigematsu, N., Shuzo Ishimaru, S., Saito, R., Ikeda, T., Matsuba, K., Sugiyama, K., & Masuda, Y. (1978). Respiratory involvement in polychlorinated biphenyls poisoning. Environmental Research, 16(1–3), 92–100.

    Article  CAS  Google Scholar 

  • Singh, N. N., & Srivastava, A. K. (2010). Haematological parameters as bioindicators of insecticide exposure in teleosts. Ecotoxicology, 19(5), 838–854.

    Article  CAS  Google Scholar 

  • Terzaghi, E., Zanardini, E., Morosini, C., Raspa, G., Borin, S., Mapelli, F., Vergani, L. D., & Guardo, A. (2018). Rhizoremediation half-lives of PCBs: role of congener composition, organic carbon forms, bioavailability, microbial activity, plant species and soil conditions, on the prediction of fate and persistence in soil. Science of the Total Environment, 612, 544–560.

    Article  CAS  Google Scholar 

  • Vos, J. G., & Roij, T. D. (1972). Immunosuppressive activity of a polychlorinated biphenyl preparation on the humoral immune response in guinea pigs. Toxicology and Applied Pharmacology, 21(4), 549–555.

    Article  CAS  Google Scholar 

  • Weber, R., Gaus, C., Tysklind, M., Johnston, P., Forter, M., Hollert, H., Heinisch, E., Holoubek, I., Lloyd-Smith, M., Masunaga, S., Moccarelli, P., Santillo, D., Seike, N., Symons, R., Torres, J. P., Verta, M., Varbelow, G., Vijgen, J., Watson, A., & Costner, P. (2008). Dioxin- and POP-contaminated sites-contemporary and future relevance and challenges: overview on background, aims and scope of the series. Environmental Science and Pollution Research Int, 15(5), 363–393.

    Article  CAS  Google Scholar 

  • Xie, Y., & Zhang, L. (2013). Progress in immunology of zebrafish. Journal of Laboratory Animal Science, 30(3), 50–53.

    Google Scholar 

  • Xu, H., Dong, X., Zhang, Z., Yang, M., Wu, X., Liu, H., Lao, Q., & Li, C. (2015). Assessment of immunotoxicity of dibutyl phthalate using live zebrafish embryos. Fish Shellfish Immunology, 45, 286–292.

    Article  CAS  Google Scholar 

  • Xu, H., Zhang, X., Li, H., Li, C., Huo, X. J., Hou, L. P., & Gong, Z. (2018a). Immune response induced by major environmental pollutants through altering neutrophils in zebrafish larvae. Aquatic Toxicology, 201, 99–108.

    Article  CAS  Google Scholar 

  • Xu, H., Li, C., Suklai, P., Zeng, Q., Chong, R., & Gong, Z. (2018b). Chemosphere differential sensitivities to dioxin-like compounds PCB 126 and PeCDF between Tg ( cyp1a : gfp ) transgenic medaka and zebra fish larvae. Chemosphere, 192, 24–30.

    Article  CAS  Google Scholar 

  • Yu, Y., Nie, F., Hay, A., Lin, H., Ma, Y., Ju, X., Gong, D., Chen, J., & Gooneratne, R. (2017). Histopathological changes in zebrafish embryos exposed to DLPCBs extract from Zhanjiang coastal sediment. Environmental Monitoring and Assessment, 189(6), 289.

    Article  Google Scholar 

  • Zhang, C., & Qiao, H. (2004). Effect of polychlorinated biphenyls on spermatogenesis and testosterone secretion in adult cocks. Journal of Zhejiang University Science B, 5(2), 193–197.

    Article  CAS  Google Scholar 

  • Zodrow, J. M., Stegeman, J. J., & Tanguay, R. L. (2004). Histological analysis of acute toxicity of 2 , 3 , 7 , 8-tetrachlorodibenzo- p -dioxin ( TCDD ) in zebrafish. Aquatic Toxicology, 66, 25–38.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

I acknowledge the cooperative spirit of all my colleagues who helped me in this project.

Funding

This study was financially supported by the Marine Economy Development Project of Guangdong Province for High-Quality Economic Development (GDOE2019A52).

Author information

Authors and Affiliations

  1. Department of Veterinary Medicine, College of Coastal Agricultural Sciences, Guangdong Ocean University, Zhanjiang, 524088, Guangdong, China

    Aftab Qamar, QiaoHua Zhang, Zhao Namula, Zhibao Chen & Jin-Jun Chen

  2. Department of Pathobiology, Faculty of Veterinary Sciences, University of Agriculture Faisalabad, Faisalabad, Punjab, Pakistan

    Javaria Waheed

Authors
  1. Aftab Qamar
    View author publications

    Search author on:PubMed Google Scholar

  2. Javaria Waheed
    View author publications

    Search author on:PubMed Google Scholar

  3. QiaoHua Zhang
    View author publications

    Search author on:PubMed Google Scholar

  4. Zhao Namula
    View author publications

    Search author on:PubMed Google Scholar

  5. Zhibao Chen
    View author publications

    Search author on:PubMed Google Scholar

  6. Jin-Jun Chen
    View author publications

    Search author on:PubMed Google Scholar

Contributions

Jinjun Chen conceived the idea and planned the project. Zhao Namula and Zhibao Chen participated in its design and coordination. QiaoHui Zhang collected the data. Aftab Qamar performed the experiment and wrote the first draft of the manuscript. Jinjun Chen and Javaria Waheed edited the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Jin-Jun Chen.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethics approval and consent to participate

According to rules and regulation of Animal Care Committee of Guangdong Ocean University (Zhanjiang Guangdong, People’s Republic of China).

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Qamar, A., Waheed, J., Zhang, Q. et al. Immunotoxicological effects of dioxin-like polychlorinated biphenyls extracted from Zhanjiang Bay sediments in zebrafish. Environ Monit Assess 192, 479 (2020). https://doi.org/10.1007/s10661-020-08427-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-020-08427-7

Keywords