Skip to main content
SpringerLink
Log in

Histopathological and Biochemical Changes in the Gills of Anabas testudineus on Exposure to Polycyclic Aromatic Hydrocarbon Naphthalene

  • Original Article
  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Naphthalene, a polycyclic aromatic hydrocarbon, is generated by various distillation, petroleum, and coal-tar production units and is used worldwide as mothballs, soil fumigants, and toilet deodorants. Considering the susceptibility of aquatic animals to different types of stressors in several water bodies, this study was carried out to evaluate the impact of naphthalene on the architecture of gill tissue including response of various enzymes like cholinesterase (ChE) activity, lactate dehydrogenase (LDH) activity, and lipid peroxidation (LPX) level of the freshwater fish Anabas testudineus. Activities of antioxidants like catalase (CAT), glutathione peroxidase (GPx), and glutathione (GSH) were also evaluated. Constant loss of gill structure and secondary lamellar fusion was observed in fishes exposed to various concentrations of naphthalene. ChE, LDH, LPx, CAT, Gpx and GSH activities indicated significant variation (p < 0.05) between the control and experimental groups. ChE activity was lowered in experimental fishes; however, LDH activity, LPx levels, and CAT activity were elevated in response to various concentrations of naphthalene as compared to control group. Both GPx and GSH activities decreased in the gill tissue of the experimental fishes. Thus, a conclusion was drawn that naphthalene is a potent toxicant capable of inflicting tissue damage leading to physiological changes in the exposed fishes.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

Data Availability

Not applicable.

References

  1. Ahmed, M. K., Al-Mamun, M. H., Parvin, E., Akter, M. S., & Khan, M. S. (2013). Arsenic induced toxicity and histopathological changes in gill and liver tissue of freshwater fish, Tilapia (Oreochromis mossambicus). Experimental and Toxicologic Pathology, 65(6), 903–909.

    Article  CAS  PubMed  Google Scholar 

  2. Ahmed, O., & Mastan, S. A. (2015). RabiabanuS, Indira P, Sub lethal effect of cypermethrin on acetylcholinesterase (AChE) activity and acetylcholine (Ach) content in selected tissues of Channa striatus (Bloch.). Journal of Toxicology and Environmental Health Sciences, 7(4), 31–37.

    Article  Google Scholar 

  3. Aly, S. T., Kanaan, D. M., El-Dieb, A. S., Abu-Eishah, S. I. (2018) Properties of ceramic waste powder-based geopolymer concrete, In International Congress on Polymers in Concrete (pp. 429–435), Springer, Cham

  4. APHA (2005) Standard methods for the examination of water and wastewater. American Public Health Association (16th ed.). New York, USA

  5. Badreddine, S., Abdelhafidh, K., Dellali, M., Mahmoudi, E., Sheehan, D., & Hamouda, B. (2017). The effects of anthracene on biochemical responses of Mediterranean mussels Mytilus galloprovincialis. Chemical Ecology, 33(4), 309–324.

    Article  CAS  Google Scholar 

  6. Balakumaran, M., Cyril, X., Ponmathan, K. P., Praveen, K. J., & Ganesh, K. M. (2015). Comparative studies on floor tiles using geopolymer concrete and cement concrete. International Journal of Engineering Research, 3(11), 1–4.

    Google Scholar 

  7. Bassey, B. O. (2019). Histopathological and biochemical response of Chrysichthys nigrodigitatus to environmental stressors from two polluted lagoons, Southwest Nigeria. Journal of Toxicology and Risk Assessment, 5, 5–25.

    Google Scholar 

  8. Baussant, T., Sanni, S., Skadsheim, A., Jonsson, G., Børseth, J. F., & Gaudebert, B. (2001). Bioaccumulation of polycyclic aromatic compounds: 2. Modeling bioaccumulation in marine organisms chronically exposed to dispersed oil. Environmental Toxicology Chemistry: An International Journal, 20(6), 1185–1195.

  9. Beliaeff, B., & Burgeot, T. (2002). Integrated biomarker response: a useful tool for ecological risk assessment. Environmental Toxicology and Chemistry: An International Journal, 21(6), 1316–1322.

  10. Bhagat, J., Ingole, B. S., & Shyama, S. K. (2017). Effects of benzo (k) fluoranthene, a polycyclic aromatic hydrocarbon on DNA damage, lipid peroxidation and oxidative stress in marine gastropod Morula granulate. Chemical Ecology, 33(9), 869–882.

    Article  CAS  Google Scholar 

  11. Bhagat, J., Sarkar, A., & Ingole, B. S. (2016). DNA damage and oxidative stress in marine gastropod Morula granulata exposed to phenanthrene. Water, Air, and Soil pollution, 227(4), 114.

    Article  Google Scholar 

  12. Brandão, F. P., Pereira, J. L., Gonçalves, F., & Nunes, B. (2011). The impact of paracetamol on selected biomarkers of the mollusc species Corbicula fluminea. Environmental Toxicology, 29, 74–83.

    Article  PubMed  Google Scholar 

  13. Broeg, K., & Lehtonen, K. K. (2006). Indices for the assessment of environmental pollution of the Baltic Sea coasts: Integrated assessment of a multi-biomarker approach. Marine Pollution Bulletin, 53(8–9), 508–522.

    Article  CAS  PubMed  Google Scholar 

  14. Dange, A. D., & Masurekar, V. B. (1980). Toluene toxicity: Effects of sublethal levels on enzyme activities in seawater adapted tilapia (Sarotherodon mossambicus Peters). Journal of Biosciences, 3(2), 129–134.

    Article  Google Scholar 

  15. Deb, S. C., Araki, T., & Fukushima, T. (2000). Polycyclic aromatic hydrocarbons in fish organs. Marine Pollution Bulletin, 40(10), 882–885.

    Article  CAS  Google Scholar 

  16. Dey, R., Biswas, C., & Chaudhuri, M. G. (2017). Effect of naphthalene on reduction characteristics of iron ore nuggets using boiler grade cola. MGMI Transactions, 113, 33–49.

    Google Scholar 

  17. Dey, S., Ballav, P., Manda, A., Samanta, P., Patra, A., Das, S., & Ghosh, A. R. (2020). Blood biochemical and erythrocytic morpho-pathological consequences of naphthalene intoxication in Indian teleost, Anabas testudineus (Bloch). Environmental Toxicology and Pharmacology, 80, 103490.

    Article  CAS  PubMed  Google Scholar 

  18. Dey, S., Samanta, P., Pal, S., Mukherjee, A. K., Kole, D., & Ghosh, A. R. (2016). Integrative assessment of biomarker responses in teleostean fishes exposed to glyphosate-based herbicide (Excel Mera 71). Emerg Contam, 2(4), 191–203.

    Article  Google Scholar 

  19. Ellman, G. L. (1959). Tissue sulphydryl groups. Archives of Biochemistry and Biophysics, 82, 70–77.

    Article  CAS  PubMed  Google Scholar 

  20. Ellman, G. L., Courtney, K. D., Andres, V., & Feather, S. (1961). A new and rapid calorimetric determination of acetyl cholinesterase activity. Biochemical Pharmacology, 7, 88–95.

    Article  CAS  PubMed  Google Scholar 

  21. Filfilan, W. M., & Aljahdali, M. O. (2019). Histological Changes in the Gills of Marine Cultured Tilapia (Oreochromis spilurus) at Larvae Stage Treated by Phenanthrene. Journal of Aquatic Pollution and Toxicology, 3(1), 24.

    Google Scholar 

  22. Haque, M. N., Eom, H. J., & Rhee, J. S. (2018). Waterborne phenanthrene modulates immune, biochemical, and antioxidant parameters in the bloods of juvenile olive flounder. Toxicology and Environmental Health Sciences, 10(3), 194–202.

    Article  Google Scholar 

  23. Has-Schön, E., Bogut, I., & Strelec, I. (2006). Heavy metal profile in five fish species included in human diet, domiciled in the end flow of River Neretva (Croatia). Archives of Environmental Contamination and Toxicology, 50(4), 545–551.

    Article  PubMed  Google Scholar 

  24. Hesni, M. A., Savari, A., Sohrab, A. D., & Mortazavi, M. S. (2011). Gill histopathological changes in milkfish (Chanos chanos) exposed to acute toxicity of diesel oil. World Applied Sciences Journal, 14(10), 1487–1492.

    CAS  Google Scholar 

  25. Jee, J. H., & Kang, J. C. (2005). Biochemical changes of enzymatic defense system after phenanthrene exposure in olive flounder, Paralichthys olivaceus. Physiological Research, 54(585), e591.

    Google Scholar 

  26. Jeheshadevi, A. K., Ramya, T. M., Sridhar, S., & Chandra, J. H. (2014). Histological alterations on the muscle and intestinal tissues of Catla catla exposed to lethal concentrations of naphthalene. International Journal of Applied Engineering Research, 9(2), 159–164.

    Google Scholar 

  27. Jonsson, G., Bechmann, R. K., Bamber, S. D., & Baussant, T. (2004). Bioconcentration, biotransformation, and elimination of polycyclic aromatic hydrocarbons in sheepshead minnows (Cyprinodon variegatus) exposed to contaminated seawater. Environmental Toxicology Chemistry: An International Journal, 23(6), 1538–1548.

  28. Jovanović, P., Žorić, L., Stefanović, I., Džunić, B., Djordjević-Jocić. J., Radenković, M., & Jovanović, M. (2010). Lactate dehydrogenase and oxidative stress activity in primary open-angle glaucoma aqueous humour. Bosnian journal of basic medical sciences, 10(1), 83. 

  29. Kaur, R., & Dua, A. (2015). 96 h LC50, behavioural alterations and histopathological effects due to wastewater toxicity in a freshwater fish Channa punctatus. Environmental Science and Pollution Research, 22, 5100–5110.

    Article  CAS  PubMed  Google Scholar 

  30. Kaur, M., & Jindal, R. (2018). Toxicopathic branchial lesions in grass carp (Ctenopharyngodon idellus) exposed to chlorpyrifos. Bulletin of Environmental Contamination and Toxicology, 100(5), 665–671.

    Article  CAS  PubMed  Google Scholar 

  31. King, J. (1965) The dehydrogenases or oxidoreductases. Lactate dehydrogenase. Practical Clinical Enzymology, Van Nostrand, D. Co., Ltd., London, pp. 83–93

  32. Kulkarni, B. G., & Masurekar, V. B. (1984). Effects of naphthalene exposure on blood serum enzyme activities in the crab Scylla serrata (Forskal). Indian Journal of Marine Sciences, 13, 97–98.

    CAS  Google Scholar 

  33. Livingstone, D. R. (2001). Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Marine Pollution Bulletin, 42, 656–666.

    Article  CAS  PubMed  Google Scholar 

  34. Mackay, D., & Fraser, A. (2000). Bioaccumulation of persistent organic chemicals: Mechanisms and models. Environmental Pollution, 110(3), 375–391.

    Article  CAS  PubMed  Google Scholar 

  35. Majewski, H. S., Klaverkamp, J. F., & Scott, D. P. (1978). Acute lethality, and sub-lethal effects of acetone, ethanol, and propylene glycol on the cardiovascular and respiratory systems of rainbow trout Salmo gairdneri. Water Research, 12(4), 217–221.

    Article  CAS  Google Scholar 

  36. Marigoudar, S. R., Ahmed, R. N., & David, M. (2009). Cypermethrin induced: In vivo inhibition of the acetylcholinesterase activity in functionally different tissues of the freshwater teleost, Labeo rohita (Hamilton). Environmental Toxicology and Chemistry, 91(6), 1175–1182.

    Article  CAS  Google Scholar 

  37. Mary, S. C. H., Silvan, S., & Elumalai, E. K. (2014). Toxicology study on lead nitrate induced fresh water fish Cirrhinus mrigala(Hamilton). European Journal of Academic Essays, 1(7), 5–8.

    Google Scholar 

  38. Mauryaa, P. K., Malika, D. S., Yadav, K. K., Gupta, N., & Kumar, S. (2018). Haematological and histological changes in fish Heteropneustes fossilis exposed to pesticides from industrial waste water. Human and Ecological Risk Assessment, 25(5), 1251–1278.

    Article  Google Scholar 

  39. Mehra, S., & Chadha, P. (2020). Bioaccumulation and toxicity of 2-naphthalene sulfonate: An intermediate compound used in textile industry. Toxicology Research, 9(2), 127–136.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Murali, M., Athif, P., Suganthi, P., Bukhari, A. S., Mohamed, H. E. S., Basu, H., & Singhal, R. K. (2018). Toxicological effect of Al2O3 nanoparticles on histoarchitecture of the freshwater fish Oreochromis mossambicus. Environmental Toxicology and Pharmacology, 59, 74–81.

    Article  CAS  PubMed  Google Scholar 

  41. Nayak, S., & Patnaik, L. (2021). Role of integrated biomarker response tool for assessment of naphthalene toxicity in Anabas testudineus. Bulletin of Environment Contamination and Toxicology, 106(4), 568–574.

    Article  CAS  Google Scholar 

  42. Nayak, S., Dash, S., Pati, S. S., Priyadarshini, P., & Patnaik, L. (2021). Lipid peroxidation and antioxidant levels in Anabas testudineus (Bloch) under naphthalene (PAH) stress. Aquaculture Research, 52(11), 5739–5749.

    Article  CAS  Google Scholar 

  43. Nayak, S., Raut, D., & Patnaik, L. (2019). Naphthalene induced enzymatic alterations in the liver of climbing perch Anabas testudineus. Journal of Aquatic Biology and Fisheries, 7, 134–141.

    Google Scholar 

  44. Obanya, H. E., Omoarukhe, A., Amaeze, N. H., & Okoroafor, C. U. (2019). Polycyclic aromatic hydrocarbons in Ologe lagoon and effects of Benzo [b] fluoranthene in African Catfish. Journal of Health and Pollution, 9(22).

  45. Ohkawa, H., Ohishi, N., & Yagi, K. (1979). Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry, 95, 351–358.

    Article  CAS  PubMed  Google Scholar 

  46. Palanikumar, L., Kumaraguru, A. K., Ramakritinan, C. M., & Anand, M. (2012). Biochemical response of anthracene and benzo [a] pyrene in milkfish Chanos chanos. Ecotoxicology and Environmental Safety, 75, 187–197.

    Article  CAS  PubMed  Google Scholar 

  47. Palanikumar, L., Kumaraguru, A. L., & Ramakritinan, C. M. (2013). Biochemical and genotoxic response of naphthalene to fingerlings of milkfish Chanos chanos. Ecotoxicology, 22(7), 1111–1122.

    Article  CAS  PubMed  Google Scholar 

  48. Patnaik, L., Raut, D., Panda, D., & Nayak, S. (2016). Naphthalene induced biochemical changes in Anabas testudineus. Journal of Biodiversity and Environmental Sciences, 8(2), 154–158.

    Google Scholar 

  49. Paul, B. N., Chanda, S., Bhowmick, B., Sridhar, N., Saha, G. S., & Giri, S. S. (2017). Nutrient profile of Indian climbing perch, Anabas testudineus. SAARC Journal of Agriculture, 15(1), 99–109.

    Article  Google Scholar 

  50. Rao, J. V., Shilpanjali, D., Kavitha, P., & Madhavendra, S. S. (2003). Toxic effects of profenofos on tissue acetylcholinesterase and gill morphology in a euryhaline fish Oreochromis mossambicus. Archives of Toxicology, 77(4), 227–232.

    Article  CAS  Google Scholar 

  51. Rodrigues, S., Antunes, S. C., Nunes, B., & Correia, A. T. (2017). Histological alterations in gills and liver of rainbow trout (Oncorhynchus mykiss) after exposure to the antibiotic oxytetracycline. Environmental toxicology and pharmacology, 53, 164–176.

  52. Rotruck, J. T., Pope, A. L., Ganther, H. E., Swanson, A. B., Hafeman, D. G., & Hoekstra, W. (1973). Selenium: Biochemical role as a component of glutathione peroxidase. Science, 179(4073), 588–590.

    Article  CAS  PubMed  Google Scholar 

  53. Rubio-Vargas, D. A., de Oliveira Ribeiro, C. A., Neto, F. F., Cordeiro, A. L., Cestari, M. M., de Souza, A. C., ... & Prodocimo, M. M. (2021). Exposure to pollutants present in Iguaçu River Southern Brazil affect the health of Oreochromis niloticus (Linnaeus, 1758): assessment histological, genotoxic and biochemical. Environmental Toxicology and Pharmacology, 87, 103682.

  54. Sahib, I. K. A., Sailatha, D., & Rao, K. R. (1980). Impact of malathion on acetylcholinesterase in the tissues of the fish Tilapia mossambica (Peters)-a time course study. Journal of Biosciences, 2(1), 37–41.

    Article  Google Scholar 

  55. Saliu, J. K., & Bawa-Allah, K. A. (2012). Toxicological effects of lead and zinc on the antioxidant enzyme activities of post juvenile Clarias gariepinus. Resources and Environment, 2(1), 21–26.

    Article  Google Scholar 

  56. Samanta, P., Mukherjee, A. K., Pal, S., Kole, D., & Ghosh, A. R. (2016). Toxic effects of glyphosate-based herbicide, Excel Mera 71 on gill, liver, and kidney of Heteropneustes fossilis under laboratory and field conditions. Journal of Microscopy and Ultrastructure, 4, 147–155.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Samanta, P., Pal, S., Senapati, T., Mukherjee, A. K., & Ghosh, A. R. (2018). Assessment of adverse outcome of Excel Mera 71 in Anabas testudineus by histological and ultrastructural alterations. Aquatic Toxicology, 205, 19–24.

    Article  CAS  PubMed  Google Scholar 

  58. Shenai, V. A. (2001). Non-ecofriendly textile chemicals and their probable substitutes - An overview. Indian Journal of Fibre & Textile Research, 26, 50–54.

    CAS  Google Scholar 

  59. Silva, C., Oliveira, C., Gravato, C., & Almeida, J. R. (2013). Behaviour and biomarkers as tools to assess the acute toxicity of benzo (a) pyrene in the common prawn Palaemon serratus. Marine Environment Research, 90, 39–46.

    Article  CAS  Google Scholar 

  60. Sinha, A. K. (1972). Colorimetric assay of catalase. Analytical biochemistry, 47(2), 389–394.

  61. Sivaram, N. M., Gopal, P. M., Barik, D. (2019) Toxic waste from textile industries. In Energy from toxic organic waste for heat and power generation, (pp. 43–54). Woodhead Publishing

  62. Sogbanmu, T. O., Osibona, A. O., Oguntunde, O. A., & Otitoloju, A. A. (2018). Biomarkers of toxicity in Clarias gariepinus exposed to sublethal concentrations of polycyclic aromatic hydrocarbons. African Journal of Aquatic Science, 43(3), 281–292.

    Article  CAS  Google Scholar 

  63. Stara, A., Zuskova, E., Velisek, J. (2016) Acute toxicity effect of cypermethrin on common carp (Cyprinus carpio), Neuro Endocrinol Letters, (37)1

  64. Tang, J., Zhang, Z., Miao, J., Tian, Y., & Pan, L. (2022). Effects of benzo [a] pyrene exposure on oxidative stress and apoptosis of gill cells of Chlamys farreri in vitro. Environmental Toxicology and Pharmacology, 93, 103867.

    Article  CAS  PubMed  Google Scholar 

  65. US Environmental Protection Agency (USEPA) (1980). Naphthalene: ambient water quality criteria. Washington DC. 

  66. US Environmental Protection Agency (1982). Naphthalene, health and environmental effects. Profile no. 131. USEPA Office of Solid Waste, Washington DC.

  67. van der Oost, R., Beyer, J., & Vermeulen, N. P. E. (2003). Fish bioaccumulation and biomarkers in environmental risk assessment: A review. Environmental Toxicology and Pharmacology, 13, 57–149.

    Article  PubMed  Google Scholar 

  68. Velmurugan, B., Selvanayagam, M., Cengiz, E. I., & Ugurlu, P. (2015). Scanning electron microscopy study of the gills, scales and erythrocytes of Anabas testudineus upon exposure to chlorpyrifos. Toxicological and Environmental Chemistry, 97(2), 208–220.

    Article  CAS  Google Scholar 

  69. Vijayavel, K., Gomathi, R. D., Durgabhavani, K., & Balasubramanian, M. P. (2004). Sublethal effect of naphthalene on lipid peroxidation and antioxidant status in the edible marine crab Scylla serrata. Marine Pollution Bulletin, 48(5–6), 429–433.

    Article  CAS  PubMed  Google Scholar 

  70. Yazdani, M. (2020). Comparative toxicity of selected PAHs in rainbow trout hepatocytes: Genotoxicity, oxidative stress and cytotoxicity. Drug and Chemical Toxicology, 43(1), 71–78.

    Article  CAS  PubMed  Google Scholar 

  71. Zhang, Y. M. , Guo, G. Z., La Zhang, L., Song, J. H. (2019) Synthesis, analysis and application of naphthalene sulfonic acid formaldehyde condensate, In IOP Conference Series: Earth and Environmental Science,237(2), IOP Publishing

  72. Zhu, L., Tang, X., Wang, Y., Sui, Y., & Xiao, H. (2016). Use of antioxidant enzymes of clam Ruditapes philippinarum as biomarker to polycyclic aromatic hydrocarbon pollution. Chinese Journal of Oceanology and Limnology, 34(2), 416–442.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are thankful to the Head of the Department, Zoology, for providing infrastructural support for carrying out the research work. We are thankful to Dr. Dhananjay Soren and Ms. Amrita Swain for helping us in taking the photographs of our histological slides.

Funding

The authors gratefully acknowledge the financial support in the form of a project grant (F. No. 33/2012/UGC, dated 14th June 2012) by the University Grants Commission, New Delhi. The authors also acknowledge the financial support in the form of a fellowship grant (S-SCST-MISC-0054-2018-1152) by the Department of Science and Technology, Government of Odisha, under Biju Patnaik Research Fellowship. Financial assistance to the Center of Excellence in Environment and Public Health by Higher Education Department, Government of Odisha under OHEPEE is grateful acknowledged (HE-PTC-WB02017).

Author information

Authors and Affiliations

  1. Environmental Science Laboratory, Department of Zoology, Centre of Excellence in Environment and Public Health, Ravenshaw University, Cuttack, 753008, Odisha, India

    Susri Nayak & Lipika Patnaik

Authors
  1. Susri Nayak
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lipika Patnaik
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Susri Nayak carried out the experimental work (biochemical, HPLC, histology), finalization of results, and preparation of the manuscript. Lipika Patnaik designed the experiment, preparation, and editing of the manuscript, and marked zones in histological sections for photography showing significant variations.

Corresponding author

Correspondence to Lipika Patnaik.

Ethics declarations

Ethical Approval

All procedures performed in studies involving animals were in accordance with the practice at which the studies were conducted.

Informed Consent

Informed consent was obtained from all individual participants included in this study.

Consent for Publication

Not applicable.

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher’s Note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nayak, S., Patnaik, L. Histopathological and Biochemical Changes in the Gills of Anabas testudineus on Exposure to Polycyclic Aromatic Hydrocarbon Naphthalene. Appl Biochem Biotechnol 195, 2414–2431 (2023). https://doi.org/10.1007/s12010-022-04214-x

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-022-04214-x

Keywords

Search

Navigation