Document Type : Original Article

Authors

1 Department of Pathobiology, Faculty of Veterinary Medicine, University of Tabriz, Tabriz, Iran

2 Department of Food Hygiene and Aquatic Animals, Faculty of Veterinary Medicine, University of Tabriz, Tabriz, Iran

3 Department of Basic Sciences, Faculty of Veterinary Medicine, University of Tabriz, Tabriz, Iran

4 Department of Aquatic Animal Health, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran

Abstract

Arsenic (As) contamination in natural water resources has become a great disaster throughout the world posing serious health problems. The current study was performed to evaluate the protective effects of Escherichia coli strain Nissle 1917 (EcN) against As exposure in goldfish (Carassius auratus). Fish were fed three times a day with 4.00% of body weight of diet with different doses (0.00, 1.00 × 106, 1.00 × 107 and 1.00 × 108 CFU g-1) of EcN for 80 days and then, challenged with 20.00 mg L-1 As for 96 hr under stagnant flow. Physicochemical characteristics of the inlet water were temperature of 25.10 ± 0.70 ˚C, pH of 7.30 ± 0.20 and dissolved oxygen of 7.30 ± 0.30 mg L-1 and 50.00% of water was exchanged once a week. Afterwards, fish were euthanized with a clove oil solution (50.00 μL L-1) and tissues were dissected from each fish and immediately fixed in 10.00% buffered formalin. The histopathological results indicated that the supplemented EcN did not have any side effects on various organs. It was also observed that the damages to kidney, liver, gill and skin were pronounced in fish exposed to As. However, the histopathological damages induced by As in fish tissues were less pronounced in the EcN-treated groups compared to the fish fed with the basal diet. Lamellar blood congestion in gills and epidermal cells detachment from the skin surface as well as hepatocytes, enterocytes and tubular necrosis were reduced in treated groups. These findings indicate that EcN has the potential to ameliorate the As-induced organ toxicity.

Keywords

Main Subjects

  1. Cui D, Zhang P, Li H, et al. The dynamic effects of different inorganic arsenic species in crucian carp (Carassius auratus) liver during chronic dietborne exposure: bioaccumulation, biotransformation and oxidative stress. Sci Total Environ 2020; 727: 138737. doi: 10.1016/j.scitotenv.2020.138737.
  2. Kumari B, Kumar V, Sinha AK, et al. Toxicology of arsenic in fish and aquatic systems. Environ Chem Lett 2017; doi: 10.1007/s10311-016-0588-9.
  3. Lavanya S, Ramesh M, Kavitha C, et al. Hematological, biochemical, and ionoregulatory responses of Indian major carp Catla during chronic sublethal exposure to inorganic arsenic. Chemosphere 2011; 82(7): 977-985.
  4. Pedlar RM, Ptashynski MD, Evans R, et al. Toxicological effects of dietary arsenic exposure in Lake Whitefish (Coregonus clupeaformis). Aquat Toxicol 2002; 57(3): 167-189.
  5. Barth S, Dunker S, Hempe J, et al. Escherichia coli Nissle 1917 for probiotic use in piglets: evidence for intestinal colonization. J Appl Microbiol 2009; 107(5): 1697-1710.
  6. Helmy YA, Kassem II, Kumar A, et al. In vitro evaluation of the impact of the probiotic E. coli Nissle 1917 on Campylobacter jejuni's invasion and intracellular survival in human colonic cells. Front Microbiol 2017; 8: 1588. doi: 10.3389/fmicb.2017.01588.
  7. Zyrek AA, Cichon C, Helms S, et al. Molecular mechanisms underlying the probiotic effects of Escherichia coli Nissle 1917 involve ZO-2 and PKCzeta redistribution resulting in tight junction and epithelial barrier repair. Cell Microbiol 2007; 9(3): 804-816.
  8. ZeinEddine R, Nasser N, Kassem I, et al. Effect of the human probiotic bacterium Escherichia coli Nissle (1917) on performance and immune response of Nile tilapia Oreochromis niloticus. J Appl Aquac 2022; 34(3): 527-541.
  9. Mandal P. An insight of environmental contamination of arsenic on animal health. Emerg Contam 2017; 3(1): 17-22.
  10. Ahmadifar E, Heydari Sadegh T, Dawood MAO, et al. The effects of dietary Pediococcus pentosaceus on growth performance, hemato-immunological para-meters and digestive enzyme activities of common carp (Cyprinus carpio). Aquaculture 2020; 516: 734656. doi: 10.1016/j.aquaculture.2019.734656.
  11. Hayati A, Pramudya M, Soepriandono H. The ability of probiotics to ameliorate blood and gonad damage caused by copper toxicity in Nile tilapia (Oreochromis niloticus). Vet World 2021; 14(11): 2964-2970.
  12. Mousavi S, Sheikhzadeh N, Hamidian G, et al. Changes in rainbow trout (Oncorhynchus mykiss) growth and mucosal immune parameters after dietary administration of grape (Vitis vinifera) seed extract. Fish Physiol Biochem 2021; 47(2): 547-563.
  13. Correia AM, Pedrazzani AS, Mendonça RC, et al. Basil, tea tree and clove essential oils as analgesics and anaesthetics in Amphiprion clarkii (Bennett, 1830). Braz J Biol 2017; doi: 10.1590/1519-6984.166695.
  14. Kim RK, Fitzgerald SD, Kiupel M, et al. Tissue distribution of the piscine novirhabdovirus genotype IVb in Muskellunge (Esox masquinongy). Animals (Basel) 2022; 12(13): 1624. doi: 10.3390/ani12131624.
  15. Hamidian GH, Zirak K, Sheikhzadeh N, et al. Intestinal histology and stereology in rainbow trout (Oncorhynchus mykiss) administrated with nano-chitosan/zeolite and chitosan/zeolite composites. Aquac Res 2018; 49(5): 1803-1815.
  16. Kreutz A, Barger N. Maximizing explanatory power in stereological data collection: A protocol for reliably integrating optical fractionator and multiple immunofluorescence techniques. Front Neuroanat 2018; 12: 73. doi: 10.3389/fnana.2018.00073.
  17. Heidarieh M, Mirvaghefi AR, Sepahi A, et al. Effects of dietary Aloe vera on growth performance, skin and gastrointestine morphology in rainbow trout (Oncorhynchus mykiss). Turkish J Fish Aquat Sci 2013; 13: 367-373.
  18. Liao CM, Tsai JW, Ling MP, et al. Organ-specific toxicokinetics and dose-response of arsenic in tilapia Oreochromis mossambicus. Arch Environ Contam Toxicol 2004; 47(4): 502-510.
  19. Pichhode M, Gaherwal S. Histopathology of liver and kidney of telost, Clarias batrachus of arsenic contaminated Chhilpura Pond water. Uttar Pradesh J Zool 2020; 41(9): 83-92.
  20. Sorensen EMB. Metal poisoning in fish. Florida, USA: CRC press 1991: 367-379.
  21. Laurén JD, McDonald DG. Acclimation to copper by rainbow trout, Salmo gairdneri: physiology. Can J Fish Aquat Sci 1987; 44: 99-104.
  22. Cockell KA, Hilton JW, Bettger WJ. Hepatobiliary and hematological effects of dietary disodium arsenate heptahydrate in juvenile rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol 1992; 103C: 453-458.
  23. Monachese M, Burton JP, Reid G. Bioremediation and tolerance of humans to heavy metal through microbial process: a potential role for probiotics? Appl Environ Microbiol 2012; 78(18): 6397-6404.
  24. Han R, Khan A, Ling Z, et al. Feed-additive Limosilactobacillus fermentum GR-3 reduces arsenic accumulation in Procambarus clarkii. Ecotoxicol Environ Saf 2022; 231: 113216. doi: 10.1016/ j.ecoenv.2022.113216.
  25. Hoseinifar SH, Yousefi S, Doan HV, et al. Oxidative stress and antioxidant defense in fish: the implications of probiotic, prebiotic, and synbiotics. Rev Fish 2020; 29(2): 1-20.
  26. Weifen L, Xiaoping Z, Wenhui S, et al. Effects of Bacillus preparations on immunity and antioxidant activities in grass carp (Ctenopharyngodon idellus). Fish Physiol Biochem 2012; 38(6):1585-1592.
  27. Gobi N, Vaseeharan B, Chen JC, et al. Dietary supplementation of probiotic Bacillus licheniformis Dahb1 improves growth performance, mucus and serum immune parameters, antioxidant enzyme activity as well as resistance against Aeromonas hydrophila in tilapia Oreochromis mossambicus. Fish Shellfish Immunol 2018; 74: 501-508.
  28. Yang G, Shen K, Yu R, et al. Probiotic (Bacillus cereus) enhanced growth of Pengze crucian carp by modulating the antioxidant defense response and exerting beneficial impacts on inflammatory response via Nrf2 activation. Aquaculture 2020; 529: 735691. doi: 10.1016/j.aquaculture.2020.735691.
  29. Bellezza I, Giambanco I, Minelli A, et al. Nrf2-Keap1 signaling in oxidative and reductive stress. Biochim Biophys Acta Mol Cell Res 2018; 1865(5): 721-733.
  30. Hafez M, Hayes K, Goldrick M, et al. The K5 capsule of Escherichia coli Strain Nissle 1917 is important in mediating interactions with intestinal epithelial cells and chemokine induction. Infect Immun 2009; 77(7): 2995-3003.
  31. Lin MY, Yen CL. Antioxidative ability of lactic acid bacteria. J Agric Food Chem 1999; 47(4):1460-1466.
  32. Nimalan N, Sørensen SL, Fečkaninová A, et al. Mucosal barrier status in Atlantic salmon fed marine or plant-based diets supplemented with probiotics. Aquaculture 2022; 547: 737516. doi: 10.1016/j.aquaculture. 2021.737516.
  33. Dash S, Das SK, Samal J, et al. Epidermal mucus, a major determinant in fish health: a review. Iran J Vet Res 2018; 19(2): 72-81.