The Effects of Diflubenzuron on Acetylcholinesterase (EC 3.1.1.7) Activity and Liver Ultrastructure in Wistar Rats

Year 2023, , 68 - 78, 01.03.2023

Nursel Gül , Nuri Yiğit , Fulya Saygılı Yiğit , Eda Yazıcı Özçelik , Hakan Eskizengin

https://doi.org/10.35378/gujs.868668

Abstract

Diflubenzuron is a commonly used larvicide/biocidal substance. The present study aimed to reveal the effects of diflubenzuron on Acetylcholinesterase (AChE) enzymatic activity and liver histopathology of a mammalian species (rats). The animals fed with various doses of diflubenzuron and the liver tissues of rats were taken on the 10th, 20th, 25th, 45th days and sixth month. AChE activity of liver was measured by spectrophotometer. Tissues were embedded in Araldite 502 (Sigma), took ultrathin sections, and examined under a 100 CX II Transmission Electron Microscope. AChE activity in the chronic dose of diflubenzuron group was like that in the control group. The enzymatic activity in the subacute dose was found to be significantly different from the control group. After subacute dose exposure was terminated, the AChE activity was still lower on the 45th day compared with the control group. Chronic and subacute doses caused adverse effects to liver tissues, such as numerous mitochondria, abnormally structured nuclei in the hepatocytes and many lipid droplets in the sinusoids of the liver ultrastructure. After the subacute dose was terminated, liver damage was still observed on the 20th and 25th days, but the liver tissue was partly regenerated on the 45th day. Cellular damage might recover after 45 days, but AChE activity probably takes more time to reach a normal level. 

Keywords

Diflubenzuron, Rat, Liver ultrastructure, Acetylcholinesterase enzymatic activity

References

• [1] Silva, A. X., Jander, G., Samaniego, H., Ramsey, J.S., Figueroa, C.C., “ Insecticide resistance mechanisms in the green peach aphid Myzus persicae (Hemiptera: Aphididae) I: a transcriptomic survey”, PloS One, 7(6): p.e36366, (2012). DOI:10.1371/journal.pone.0036366
• [2] Casida, J.E., Durkin, K.A., “Pesticide chemical research in toxicology:lessons from nature”, Chemical Research in Toxicology, 30: 94-104, (2017). DOI: 10.1021/acs.chemrestox.6b00303
• [3] Saleh, T.A., Ahmed, K.S., El-Bermawy, S.M., Ismail, E.H., Abdel-Gawad, M., “Histological and ultrastructural aspects of larval corpus allatum of Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae) treated with diflubenzuron and chromafenozide”, Journal of Entomology and Zoology Studies, 6: 864-872, (2018).
• [4] Hoffman, D.J., Rattner, B.A., Burton, Jr G.A., Cairns, Jr J., Handbook of Ecotoxicology, CRC Press LLC Lewis Publishers, Boca Raton, FL, (2003).
• [5] Meissle, M., Mouron, P., Musa, T., Bigler, F., Pons, X., Vasileiadis, V.P., Otto, S., Antichi, D., Kiss, J., Pálinkás, Z., Dorner, Z., “Pests, pesticide use and alternative options in European maize production: current status and future prospects”, Journal of Applied Entomolology, 134: 357-375, (2010). https://doi.org/10.1111/j.1439-0418.2009.01491.x
• [6] Clasen, B., Loro, V.L., Murussi, C.R., Tiecher, T.L, Moraes, B., Zanella, R., “Bioaccumulation and oxidative stress caused by pesticides in Cyprinus carpio reared in a rice-fish system”, The Science of the Total Environment, 626: 737-743, (2018). DOI: 10.1016/j.scitotenv.2018.01.154
• [7] Bloomquist, J.R., “Ion channels as targets for insecticides”, Annual Review of Entomology, 41: 163-190, (1996). DOI:10.1146/annurev.en.41.010196.001115
• [8] Grosicka-Maciąg, E.,”Biological consequences of oxidative stress induced by pesticides”, Postepy Higieny i Medycyny Doswiadczalnej(Online), 65: 57-366, (2011). DOI: 10.5604/17322693.948816
• [9] Banaee, M., Sureda, A., Mirvaghefi, A.R., Ahmadi, K.J.F., ”Biochemical and histological changes in the liver tissue of rainbow trout (Oncorhynchus mykiss) exposed to sub-lethal concentrations of diazinon”, Fish Physiology and Biochemistry, 39: 489-501, (2013). DOI: 10.1007/s10695-012-9714-1
• [10] Casida, J.E., Durkin, K.A., “Neuroactive insecticides: targets, selectivity, resistance, and secondary effects”, Annual Review of Entomology, 58: 99-117, (2013). DOI: 10.1146/annurev-ento-120811-153645
• [11] Beydilli, H., Yılmaz, N., Çetin, E.S., Topal, Y., Çelik, O.İ., Şahin, C., Topal, H., Ciğerci, I.H., Sözen, H.,”Evaluation of the protective effect of silibinin against diazinon induced hepatotoxicity and free-radical damage in rat liver”, Iranian Red Crescent medical journal, 17: e25310, (2015). DOI: 10.5812/ircmj.17(4)2015.25310
• [12] Nesterov, A., Spalthoff, C., Kandasamy, R., Katana, R., Rankl, N.B., Andrés, M., Jähde, P., Dorsch, J.A., Stam, L.F., Braun, F.J., Warren, B., “TRP channels in insect stretch receptors as insecticide targets”, Neuron, 86: 665-671, (2015). DOI: 10.1016/j.neuron.2015.04.001
• [13] Dantzger, D.D., Jonsson, C.M., Aoyama, H., “Mixtures of diflubenzuron and p-chloroaniline changes the activities of enzymes biomarkers on tilapia fish (Oreochromis niloticus) in the presence and absence of soil”, Ecotoxicology and Environmental Safety, 148: 367-376, (2018), DOI: 10.1016/j.ecoenv.2017.10.054
• [14] World Health Organization (WHO): Diflubenzuron in drinking-water: use for vector control in drinking-water sources and containers. World Health Organization, WHO Press, Geneva, (2008).
• [15] Muzinic, V., Zeljezic, D., “Non-target toxicity of novel insecticides”, Arhiv za Higijenu Rada i Toksikologiju, 69: 86-102, (2018). DOI: 10.2478/aiht-2018-69-3111.
• [16] World Health Organization (WHO) Guidelines for Drinking-Water Quality, 3rd Edition including 1st and 2nd addenda, 2008.
• [17] Castro, A.A., Lacerda, M.C., Zanuncio, M.C., Ramalho, F.S., Polanczyk, R., Serrão, J.E., Zanuncio, J.C., “Effect of the insect growth regulator diflubenzuron on the predator Podisus nigrispinus (Heteroptera: Pentatomidae)”, Ecotoxicology, 21: 96-103, (2011). DOI: 10.1007/s10646-011-0769-z
• [18] Chang, J., Wang, H., Xu, P., Guo, B., Li, J., Wang, Y., Li, W., “Oral and dermal diflubenzuron exposure causes a hypothalamic–pituitary–thyroid (HPT) axis disturbance in the Mongolian racerunner (Eremias argus)”, Environmental Pollution, 232: 338-346, (2018). DOI: 10.1016/j.envpol.2017.08.115
• [19] World Health Organization (WHO): WHO Specifications and Evaluations for Public Health Pesticides: Diflubenzuron 1-(-4 chlorophenyl)-3-(2,4-difluorobenzoyl) urea. FAO/WHO Evaluation Report on Diflubenzuron, (2006).
• [20] Mason, H.J., Sams, C., Stevenson, A.J., Rawbone, R., “Rates of spontaneous reactivation and aging of acetyicholinesterase in human erythrocytes after inhibition by organophosphorus pesticides”, Human & Experimental Toxicology, 19: 511-516, (2000). DOI: 10.1191/096032700667340089
• [21] Habes, D., Morakchi, S., Aribi, N., Farine, J.P., Soltani, N., “Boric acid toxicity to the German cockroach, Blattella germanica: Alterations in midgut structure, and acetylcholinesterase and glutathione S-transferase activity”, Pesticide Biochemistry and Physiology, 84: 17-24, (2006). https://doi.org/10.1016/j.pestbp.2005.05.002
• [22] Kim, Y.B., Hur, G.H., Shin, S., Sok, D.E., Kang, J.K., Lee, Y.S., “Organophosphate-induced brain injuries: delayed apoptosis mediated by nitric oxide”, Environmental Toxicology and Pharmacology, 7: 147-152, (1999). DOI: 10.1016/s1382-6689(99)00006-x
• [23] Maduenho, L.P., Martinez, C.B., “Acute effects of diflubenzuron on the freshwater fish Prochilodus lineatus”, Comparative Biochemistry and Physiology. Toxicology & Pharmacology, 148: 265-272, (2008). DOI: 10.1016/j.cbpc.2008.06.010
• [24] Zaidi, N., Soltani, N., “Laboratory evaluation of environmental risk assessment of pesticides for mosquito control: toxicity of dimilin on a larvivorous fish, Gambusia affinis”, Advances in Environmental Biology, 7(4): 605-613, (2013).
• [25] Young, M.F., Trombetta, L.D., Carson, S., “Effects of diflubenzuron on the mouse liver”, Journal of Applied Toxicology, 6: 343-348, (1986). DOI: 10.1002/jat.2550060508
• [26] El‐Sebae, A.H., Salem, M.H., El‐Assar, M.R.S., Enan, E.E., “In vitro effect of profenofos, fenvalerate and dimilin on protein and RNA biosynthesis by rabbit liver and muscle tissues”, Journal of environmental science and health. Part. B, Pesticides, food contaminants, and agricultural wastes, 23: 439-451, (1988). DOI: 10.1080/03601238809372618
• [27] Hadler, M.R., Buckle, A.P., “Forty-five years of anticoagulant rodenticides – past, present and future trends”. In: Borrecco JE, Marsh RE, editors. Proceedings of the Fifteenth Vertebrate Pest Conference; 3-5 March 1992, University of California p. 149–155, Newport Beach, California, Davis, (1992).
• [28] Ellman, G.L., Courtney, K.D., Andres, Jr V., Featherstone, R.M., “A new and rapid colorimetric determination of acetylcholinesterase activity”, Biochemical Pharmacology, 7: 88-95, (1961). DOI: 10.1016/0006-2952(61)90145-9
• [29] Hayat, M.A., Principles and techniques of electron microscopy, Biological applications, 2nd Ed., Vol 1., University Park Press, Baltimore, MD, (1981).
• [30] Wilson, B. Cholinesterases. In: Krieger, R., Editor, Hayes Handbook Of Pesticide Toxicology, 3rd Edition. Ch. 68, 1457–1478, London, (2010).
• [31] Smulders, C. J., Bueters, T. J., Vailati, S., van Kleef, R. G., Vijverberg, H. P., “Block of Neuronal Nicotinic Acetylcholine Receptors by Organophosphate Insecticides”, Toxicological Sciences : an official journal of the Society of Toxicology, 82, 545– 554, (2004). https://doi.org/10.1093/toxsci/kfh269
• [32] Karami-Mohajeri, S., Abdollahi, M., “Toxic influence of organophosphate, carbamate, and organochlorine pesticides on cellular metabolism of lipids, proteins, and carbohydrates: a systematic review”, Human & Experimental Toxicology, 30: 1119-1140, (2011). DOI: 10.1177/0960327110388959
• [33] Lee, S., Barron, M.G., “ A mechanism-based 3D-QSAR approach for classification and prediction of acetylcholinesterase inhibitory potency of organophosphate and carbamate analogs”, Journal Of Computer-Aided Molecular Design, 30: 347-363, (2016). DOI: 10.1007/s10822-016-9910-7
• [34] Lu, J., Zhang, M., Lu, L., “Tissue metabolism, hematotoxicity, and hepatotoxicity of trichlorfon in Carassius auratus gibelio after a single oral administration”, Frontiers in Physiology, 9: 551, (2018). DOI: 10.3389/fphys.2018.00551
• [35] Begum, S., Reddy, M.M., Indira, K., Swami, K.S., “Effect of dieldrin on catalytic potential of field mouse Mus booduga brain acetylcholinesterase”, Archives internationales de physiologie et de biochimie, 95: 101-104, (1987). https://doi.org/10.3109/13813458709104521
• [36] Afify, A.E.M.R., El-Beltagi, H.S., “Effect of the insecticide cyanophos on liver function in adult male rats”, Fresenius Environmental Bulletin, 20: 1084-1088, (2011).
• [37] Ulusoy, Y., Toprak, B., Uzunhisarcıklı, M., Öğütçü, A., “Diazinonun Sıçan Hepatositleri Üzerine Etkisinin Elektron Mikroskobu İle İncelenmesi”, Etlik Veteriner Mikrobiyoloji Dergisi, 15 (1–2), 29–36, Ankara, (2004).
• [38] Roma, G.C., De Oliveira, P.R., Bechara, G.H., Camargo Mathias M.I., “Cytotoxic Effects of Permethrin on Mouse Liver and Spleen Cells”, Microscopy Research and Technique, 75, 229–238, Roma, (2012). DOI: 10.1002/jemt.21047
• [39] Olsvik, P.A., Samuelsen, O.B., Erdal, A., Holmelid, B., Lunestad, B.T., “Toxicological assessment of the anti-salmon lice drug diflubenzuron on Atlantic cod Gadus morhua”, Diseases of Aquatic Organisms, 105: 27-43, (2013). DOI: 10.3354/dao02613
• [40] De Barros, A.L., Cavalheiro, G.F., De Souza, A.V., Traesel, G.K., Anselmo‐Franci, J.A., Kassuya, C.A., Arena, A.C., “Subacute toxicity assessment of diflubenzuron, an insect growth regulator, in adult male rats”, Environmental Toxicology, 31: 407-414, (2016). DOI: 10.1002/tox.22054
• [41] Sharma, D., Sangha, G.K., “Triazophos induced oxidative stress and histomorphological changes in liver and kidney of female albino rats”, Pesticide Biochemistry and Physiology, 110: 71-80, (2014). DOI: 10.1016/j.pestbp.2014.03.003
• [42] Zhuang, X.M., Wei, X., Tan, Y., Xiao, W.B., Yang, H.Y., Xie, J.W., Lu, C., Li, H., “Contribution of carboxylesterase and cytochrome P450 to the bioactivation and detoxification of isocarbophos and its enantiomers in human liver microsomes”, Toxicological Sciences : an Official Journal of the Society of Toxicology, 140: 40-8, (2014). DOI: 10.1093/toxsci/kfu067
• [43] Sayım, F., “Dimethoate-induced biochemical and histopathological changes in the liver of rats”, Experimental and Toxicologic Pathology, 59: 237-43, (2007). DOI: 10.1016/j.etp.2007.05.008
• [44] Karami-Mohajeri, S., Ahmadipour, A., Rahimi, H.R., Abdollahi, M., “Adverse effects of organophosphorus pesticides on the liver: a brief summary of four decades of research”, Arhiv za higijenu rada i toksikologiju, 68: 261-275, (2017). DOI: 10.1515/aiht-2017-68-2989