In-feed emamectin benzoate abuse affects the biological responses and erythrocytes of Nile tilapia Oreochromis niloticus

References

• MSD Animal Health. SLICE technical monograph; Merck Animal Health: Whitehouse Station, New Jersey, 2012 (accessed Jun 1, 2021).
   Google Scholar
• Batiha, G. E. S.; Beshbishy, A. M.; Wasef, L. G.; Elewa, Y. H. A.; Al-Sagan, A. A.; El-Hack, M. E. A.; Taha, A. E.; Abd-Elhakim, Y. M.; Devkota, H. P. Chemical Constituents and Pharmacological Activities of Garlic (Allium Sativum L.): A Review. Nutrients. 2020, 12, 872. DOI: 10.3390/nu12030872.
   Google Scholar
• Anon. Major Uses of Pesticides: Insecticides; Department of Agriculture, Cooperation and Farmers Welfare, Ministry of Agriculture and Farmers Welfare, Government of India: New Delhi, 2021. https://www.epestodisha.nic.in/public/documents/Major%20Use%20as%20on%201.01.2021.pdf. (accessed 10 May 2022).
   Google Scholar
• Raja, R. A.; Patil, P. K.; Avunje, S.; Kumaran, M.; Solanki, H. G.; Jithendran, K. P.; Alavandi, S. V.; Vijayan, K. K. Efficacy of Emamectin Benzoate in Controlling Natural Infestations of Ectoparasites in Economically Important Fish Species of India. Aquaculture. 2022, 551, 737940. 2022.737940 DOI: 10.1016/j.aquaculture.
   Web of Science ®Google Scholar
• Westcott, J. D.; Revie, C. W.; Giffin, B. L.; Hammell, K. L. Evidence of Sea Lice Lepeophtheirus salmonis Tolerance to Emamectin Benzoate in New Brunswick, Canada. In Proceedings of the 8th International Sea Lice Conference, 2010; Elsevier: Amsterdam, Netherlands, Victoria, BC, Canada; p 85.
   Google Scholar
• Jones, P. G.; Hammell, K. L.; Gettinby, G.; Revie, C. W. Detection of Emamectin Benzoate Tolerance Emergence in Different Life Stages of Sea Lice, Lepeophtheirus salmonis, on Farmed Atlantic Salmon, Salmo Salar L. J. Fish Dis. 2013, 36, 209–220. DOI: 10.1111/jfd.12022.
   PubMed Web of Science ®Google Scholar
• Bravo, S.; Sevatdal, S.; Horsberg, T. E. Sensitivity Assessment of Caligus Rogercresseyi to Emamectin Benzoate in Chile. Aquaculture. 2008, 282, 7–12. DOI: 10.1016/j.aquaculture.2008.06.011.
   Web of Science ®Google Scholar
• Horsberg, T. E. Avermectin Use in Aquaculture. Curr. Pharm. Biotechnol. 2012, 13, 1095–1102. DOI: 10.2174/138920112800399158.
   PubMed Web of Science ®Google Scholar
• Igboeli, O. O.; Burka, J. F.; Fast, M. D. Lepeophtheirus Salmonis: A Persisting Challenge for Salmon Aquaculture. Anim. Front. 2014, 4, 22–32. DOI: 10.1002/ps.3620.
   Web of Science ®Google Scholar
• Lees, F.; Baillie, M.; Gettinby, G.; Revie, C. W. The Efficacy of Emamectin Benzoate against Infestations of Lepeophtheirus salmonis on Farmed Atlantic Salmon (Salmo Salar L.) in Scotland, 2002–2006. PLoS One 2008, 3, e1549. DOI: 10.1371/journal.pone.0001549.
   PubMed Web of Science ®Google Scholar
• Collymore, C.; Watral, V.; White, J. R.; Colvin, M. E.; Rasmussen, S.; Tolwani, R. J.; Kent, M. L. Tolerance and Efficacy of Emamectin Benzoate and Ivermectin for the Treatment of Pseudocapillaria Tomentosa in Laboratory Zebrafish (Danio rerio). Zebrafish. 2014, 11, 490–497. DOI: 10.1089/zeb.2014.1021.
   PubMed Web of Science ®Google Scholar
• Julinta, R. B.; Abraham, T. J.; Roy, A.; Singha, J.; Dash, G.; Sar, T. K.; Patil, P. K. Effects of Oral-Dosing of an Antiparasitic Drug Emamectin Benzoate on the Growth and Serum Biomarkers of Oreochromis niloticus (L.) Juveniles. J. Environ. Biol. 2020, 41, 973–979. DOI: 10.22438/jeb/41/5/MRN-1222.
   Web of Science ®Google Scholar
• Julinta, R. B.; Abraham, T. J.; Roy, A.; Singha, J.; Bardhan, A.; Sar, T. K.; Patil, P. K.; Kumar, K. A. Safety of Emamectin Benzoate Administered in Feed to Nile Tilapia Oreochromis Niloticus (L.). Environ. Toxicol. Pharmacol. 2020, 75, 103348. DOI: 10.1016/j.etap.2020.103348.
   PubMed Web of Science ®Google Scholar
• Singha, J.; Abraham, T. J.; Roy, A.; Bardhan, A.; Sar, T. K.; Rajisha, R.; Krishna, E. K. N.; Kumar, K. A.; Patil, P. K. Influence of Dietary Emamectin Benzoate on the Biological Responses of Monosex (All-Male) Oreochromis niloticus (L.) Fries. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2022, 252, 109223. DOI: 10.1016/j.cbpc.2021.109223.
   PubMed Web of Science ®Google Scholar
• Bowker, J. D.; Carty, D.; Bowman, M. P. The Safety of SLICE (0.2% Emamectin Benzoate) Administered in Feed to Fingerling Rainbow Trout. N. Am. J. Aquac. 2013, 75, 455–462. DOI: 10.1080/15222055.2013.806383.
   Web of Science ®Google Scholar
• Atli, G.; Canli, M. Enzymatic Responses to Metal Exposures in a Freshwater Fish Oreochromis niloticus. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2007, 145, 282–287. DOI: 10.1016/j.cbpc.2006.12.012.
   PubMed Web of Science ®Google Scholar
• Sinha, R.; Jindal, R. Augmenting Fish Health Using Emblica Officinalis against Triarylmethane Dye Induced Blood Toxicity in Cyprinus Carpio. Aquac. Res. 2019, 50, 1644–1650. DOI: 10.1111/are.14044.
   Web of Science ®Google Scholar
• Witeska, M.; Lugowska, K. The Effect of Copper Exposure during Embryonic Development on Deformations of Newly Hatched Common Carp Larvae, and Further Consequences. Electron. J. Pol. Agric. Univ. Ser. Fisheries 2004, 7, 01.
   Google Scholar
• Tahir, R.; Ghaffar, A.; Abbas, G.; Turabi, T. H.; Kausar, S.; Du, X.; Naz, S.; Jamil, H.; Samra.; Riaz, S.; Abdelgayed, S. S. Pesticide Induced Hematological, Biochemical and Genotoxic Changes in Fish: A Review. Agrobiol. Rec. 2021, 3, 41–57. DOI: 10.47278/journal.abr/2021.005.
   Google Scholar
• Das, R.; Abraham, T. J.; Singha, J.; Bardhan, A.; Patil, P. K. Dietary Emamectin Benzoate Induces Dose-Dependent Variations in Haemato-Biochemical and Erythrocyte-Metric Parameters of Oreochromis niloticus (L.). Aquaculture. 2022, 561, 738680. DOI: 10.1016/j.aquaculture.2022.738680.
   Web of Science ®Google Scholar
• Kilercioglu, S.; Ay, O.; Oksuz, H.; Yilmaz, M. B. The Effects of the Neurotoxic Agent Emamectin Benzoate on the Expression of Immune and Stress-Related Genes and Blood Serum Profiles in the Rainbow Trout. Mol. Biol. Rep. 2020, 47, 5243–5251. DOI: 10.1007/s11033-020-05599-w.
   PubMed Web of Science ®Google Scholar
• Choudhary, P.; Swain, P.; Das, R.; Sahoo, S. N.; Das, K. C.; Patil, P. K.; Mishra, S. S. Effect of Graded Levels of Dietary Emamectin Benzoate on Immunity, Enzyme Activity, and Withdrawal Period in Labeo Rohita Juveniles (Hamilton, 1822). Aquac. Nutr. 2022, 2022, 1–11. DOI: 10.1155/2022/4688312.
   Web of Science ®Google Scholar
• Roberts, R. J. Fish Pathology, 4th ed.; Wiley-Blackwell: Chichester, 2012.
   Google Scholar
• Hesser, E. F. Methods for Routine Fish Hematology. Prog. Fish Cult. 1960, 22, 164–171. DOI: 10.1577/1548-8659(1960)22[164:MFRFH].2.0.CO;2.2.0.CO;2
   Google Scholar
• da Silva Souza, T.; Fontanetti, C. S. Micronucleus Test and Observation of Nuclear Alterations in Erythrocytes of Nile Tilapia Exposed to Waters Affected by Refinery Effluent. Mutat. Res. 2006, 605, 87–93. DOI: 10.1016/j.mrgento×.2006.02.010.
   PubMed Web of Science ®Google Scholar
• Bojarski, B.; Lutnicka, H.; Swadźba-Karbowy, M.; Makulska, J.; Jakubiak, M.; Pawlak, K.; Tombarkiewicz, B.; Witeska, M. Effects of Herbicides Pendimethalin and Ethofumesate on Common Carp (Cyprinus Carpio) Erythrocyte Morphology. Folia Biol. 018, 66, 143–149. DOI: 10.3409/fb_66-3.15.
   Web of Science ®Google Scholar
• Dal’Bó, G. A.; Sampaio, F. G.; Losekann, M. E.; Queiroz, J. F. D.; Luiz, A. J. B.; Wolf, V. H. G.; Gonçalves, V. T.; Carra, M. L. Hematological and Morphometric Blood Value of Four Cultured Species of Economically Important Tropical Food Fish. Neotrop. Ichthyol. 2015, 13, 439–446. DOI: 10.1590/1982-0224-20140115.
   Web of Science ®Google Scholar
• Hrubec, T. C.; Cardinale, J. L.; Smith, S. A. Hematology and Plasma Chemistry Reference Intervals for Cultured Tilapia (Oreochromis Hybrid). Vet. Clin. Pathol. 2000, 29, 7–12. DOI: 10.1111/j.1939-165x.2000.tb00389.x.
   PubMed Web of Science ®Google Scholar
• Amaeze, N. H.; Komolafe, B. O.; Salako, A. F.; Akagha, K. K.; Briggs, T. M. D.; Olatinwo, O. O.; Femi, M. A. Comparative Assessment of the Acute Toxicity, Haematological and Genotoxic Effects of Ten Commonly Used Pesticides on the African Catfish, Clarias Gariepinus (Burchell, 1822). Heliyon 2020, 6, e04768. DOI: 10.1016/j.heliyon.2020.e04768.
   PubMedGoogle Scholar
• Ghayyur, S.; Tabassum, S.; Ahmad, M. S.; Akhtar, N.; Khan, M. F. Effect of Chlorpyrifos on Hematological and Seral Biochemical Components of Fish Oreochromis Mossambicus. Pak. J. Zool. 2019, 51, 1047–1052. DOI: 10.17582/journal.pjz/2019.51.3.1047.1052.
   Web of Science ®Google Scholar
• El-Sayed, Y. S.; Saad, T. T.; El-Bahr, S. M. Acute Intoxication of Deltamethrin in Monosex Nile Tilapia, Oreochromis niloticus with Special Reference to the Clinical, Biochemical, and Haematological Effects. Environ. Toxicol. Pharmacol. 2007, 24, 212–217. DOI: 10.1016/j.etap.2007.05.006.
   PubMed Web of Science ®Google Scholar
• Ghaffar, A.; Hussain, R.; Abbas, G.; Kalim, M.; Khan, A.; Ferrando, S.; Gallus, L.; Ahmed, Z. Fipronil (Phenylpyrazole) Induces Hemato-Biochemical, Histological, and Genetic Damage at Low Doses in Common Carp, Cyprinus Carpio (Linnaeus, 1758). Ecotoxicology. 2018, 27, 1261–1271. DOI: 10.1007/s10646-018-1979-4.
   PubMed Web of Science ®Google Scholar
• Soliman, H. A.; Hamed, M.; Sayed, A. E. D. H. Investigating the Effects of Copper Sulfate and Copper Oxide Nanoparticles in Nile Tilapia (Oreochromis niloticus) Using Multiple Biomarkers: The Prophylactic Role of Spirulina. Environ. Sci. Pollut. Res. Int. 2021, 28, 30046–30057. DOI: 10.1007/s11356-021-12859-0.
   PubMed Web of Science ®Google Scholar
• Mohammadalikhani, M.; Lameeihassankiadeh, S.; Najjar Lashgari, S.; Abbasian, F. Acute Toxicity of Captan on Blood Factors Total Immunoglobulin, Liver, and Gill Tissues of Fingerling Grass Carps: Ctenopharyngodon Idella. J. Chem. Health Risks. 2017, 7, 77–84. DOI: 10.22034/jchr.2017.544167.
   Google Scholar
• de Arcaute, C. R.; Soloneski, S.; Larramendy, M. L. Toxic and Genotoxic Effects of the 2, 4-Dichloropheno × Yacetic Acid (2, 4-D)-Based Herbicide on the Neotropical Fish Cnesterodon Decemmaculatus. Ecotoxicol. Environ. Saf. 2016, 128, 222–229. DOI: 10.1016/j.ecoenv.2016.02.027.
   PubMed Web of Science ®Google Scholar
• Fırat, Ö.; Cogun, H. Y.; Yüzereroğlu, T. A.; Gök, G.; Fırat, Ö.; Kargin, F.; Kötemen, Y. A Comparative Study on the Effects of a Pesticide (Cypermethrin) and Two Metals (Copper, Lead) to Serum Biochemistry of Nile Tilapia, Oreochromis Niloticus. Fish Physiol. Biochem. 2011, 37, 657–666. DOI: 10.1007/s10695-011-9466-3.
   PubMed Web of Science ®Google Scholar
• Chen, C. Y.; Wooster, G. A.; Bowser, P. R. Comparative Blood Chemistry and Histopathology of Tilapia Infected with Vibrio vulnificus or Streptococcus iniae or Exposed to Carbon Tetrachloride, Gentamicin, or Copper Sulphate. Aquaculture 2004, 239, 421–443. DOI: 10.1016/j.aquaculture.2004.05.033.
   Web of Science ®Google Scholar
• Mahboob, S.; Ahmad, L.; Sultana, S.; Alghanim, K.; Al-Misned, F.; Ahmad, Z.; Ghazala  . Fish Cholinesterase as Biomarkers of Sublethal Effects of Organophosphorus and Carbamates in Tissues of Labeo Rohita. J. Biochem. Mol. Toxicol. 2014, 28(3), 137–142. DOI: 10.1002/jbt.21545.
   PubMed Web of Science ®Google Scholar
• Amin, K. A.; Hameid, II, H. A.; Abd Elsttar, A. H. Effect of Food Azo Dyes Tartrazine and Carmoisine on Biochemical Parameters Related to Renal, Hepatic Function and Oxidative Stress Biomarkers in Young Male Rats. Food Chem. Toxicol. 2010, 48, 2994–2999. DOI: 10.1016/j.fct.2010.07.039.
   PubMed Web of Science ®Google Scholar
• Pala, E. M.; Dey, S. Microscopy and Microanalysis of Blood in a Snakehead Fish, Channa Gachua Exposed to Environmental Pollution. Microsc. Microanal. 2016, 22, 39–47. DOI: 10.1017/S1431927616000519.
   PubMed Web of Science ®Google Scholar
• Khatun, M. M.; Mostakim, G. M.; Moniruzzaman, M.; Rahman, U. O.; Islam, M. S. Distortion of Micronuclei and Other Peripheral Erythrocytes Caused by Fenitrothion and Their Recovery Assemblage in Zebrafish. Toxicol. Rep. 2021, 8, 415–421. DOI: 10.1016/j.toxrep.2021.02.019.
   PubMed Web of Science ®Google Scholar
• Islam, S. M.; Rohani, M. F.; Zabed, S. A.; Islam, M. T.; Jannat, R.; Akter, Y.; Shahjahan, M. Acute Effects of Chromium on Hemato-Biochemical Parameters and Morphology of Erythrocytes in Striped Catfish Pangasianodon hypophthalmus. Toxicol. Rep. 2020, 7, 664–670. DOI: 10.1016/j.toxrep.2020.04.016.
   PubMed Web of Science ®Google Scholar
• Ventura, B.; de Angelis, D. D. F.; Marin-Morales, M. A. Mutagenic and Genotoxic Effects of the Atrazine Herbicide in Oreochromis niloticus (Perciformes, Cichlidae) Detected by the Micronuclei Test and the Comet Assay. Pestic. Biochem. Phys. 2008, 90, 42–51. DOI: 10.1016/j.pestbp.2007.07.009.
   Web of Science ®Google Scholar
• Rodilla, V. Origin and Evolution of Binucleated Cells and Binucleated Cells with Micronuclei in Cisplatin-Treated CHO Cultures. Mutat. Res. 1993, 300, 281–291. DOI: 10.1016/0165-1218(93)90062-I.
   PubMed Web of Science ®Google Scholar
• Najiah, M.; Nadirah, M.; Marina, H.; Lee, S. W.; Nazaha, W. H. Quantitative Comparisons of Erythrocyte Morphology in Healthy Freshwater Fish Species from Malaysia. Res. J. Fish Hydrobiol. 2008, 3, 32–35.
   Google Scholar
• Tomova, E. S.; Velcheva, I. G.; Arnaudov, A. D. Influence of Copper and Zinc on the Erythrocyte-Metric Parameters of Carassius Gibelio (Pisces, Cyprinidae). Bulg. J. Agric. Sci. 2009, 15, 183–188.
   Web of Science ®Google Scholar
• Drobot, G. P.; Remizova, O. S. Using the Hematological Parameters of Lacerta Agilis L. for Estimating the Anthropogenetically Disturbed Territories. Proc. Samara. Sci. Center Russian Acad. Sci. 2012, 14, 1887–1890.
   Google Scholar
• Zhelev, Z.; Popgeorgiev, G.; Ivanov, I.; Boyadzhiev, P. Changes of Erythrocyte-Metric Parameters in Pelophylax Ridibundus (Amphibia: Anura: Ranidae) Inhabiting Water Bodies with Different Types of Anthropogenic Pollution in Southern Bulgaria. Environ. Sci. Pollut. Res. Int. 2017, 24, 17920–17934. DOI: 10.1007/s11356-017-9364-z.
   PubMed Web of Science ®Google Scholar
• Vieira, J. E.; de Oliveira Ferreira, R.; dos Reis Sampaio, D. M.; da Costa Araújo, A. P.; Malafaia, G. An Insight on the Mutagenicity and Cytotoxicity of Zinc Oxide Nanoparticles in Gallus gallus Domesticus (Phasianidae). Chemosphere 2019, 231, 10–19. DOI: 10.1016/j.chemosphere.2019.05.111.
   PubMed Web of Science ®Google Scholar
• da Costa Araújo, A. P.; Lima, V. S.; de Andrade Vieira, J. E.; Mesak, C.; Malafaia, G. First Report on the Mutagenicity and Cytotoxicity of ZnO Nanoparticles in Reptiles. Chemosphere. 2019, 235, 556–564. DOI: 10.1016/j.chemosphere.2019.06.164.
   PubMed Web of Science ®Google Scholar