Iranian Veterinary Journal

Iranian Veterinary Journal

Investigating the effect of levamisole on some oxidative stress factors in Caspian tortoises

Document Type : Research Paper

Authors
Mohammad Reza Yousefi 1
ُSara Zabihi 2
1 Associate Professor, Department of Veterinary Parasitology, Babol-Branch, Islamic Azad University, Babol, Iran
2 DVSc Student of Clinical Pathology, Faculty of Veterinary Medicine, Shahid Chamran University, Ahvaz, Iran
10.22055/ivj.2025.505137.2771
Abstract
    Veterinary science has so far focused mostly on the study of domestic animals, while reptiles, especially turtles, have received less attention. This is despite the fact that nowadays the use of reptiles, especially turtles, as pets and laboratory animals is increasing. Considering the proof of pathogenicity and the presence of parasites in these animals, it seems necessary to adopt appropriate treatment approaches for them. Due to the toxicity of avermectin and the resistance of nematodes to fenbendazole in turtles, levamisole is the chosen anti-parasitic drug in these animals. This study was conducted with the aim of evaluating the effect of levamisole at a dose of 10 mg/kg body weight as intravenous and subcutaneous injection on some oxidative stress factors in Caspian tortoises. The present study was conducted on 27 Caspian turtles with an average weight of 1.09 kg in 3 groups. The first group received Levamisole intravenously, but the second group received subcutaneously, in the same line the third group was the control group. Blood sampling was done at 7 different times during 24 hours at 0.5, 1, 2, 4, 8, 12 and 24 hours after drug administration. The results showed that the amount of malondialdehyde factor and catalase and superoxide dismutase enzymes in the serum of turtles treated with intravenous and subcutaneous levamisole have significant differences compared to the control group. While the total antioxidant capacity of the groups receiving the drug compared to the control group did not show a significant difference, which indicates the overall balance of the oxidant and antioxidant status so, it can be considered as one of the positive effects of the use of this drug in Caspian turtles. The results of the present study showed the efficient effect of levamisole as an antiparasitic drug with antioxidant properties that helps reduce oxidative stress.
Keywords
Levamisole
Oxidative Stress
Turtle
Parasite

Subjects

Abdollahi, M., & Jebelli Javan, A. (2020). The effect of adding Levamisole to colostrum on plasma oxidant-antioxidant balance in newborn kids. Iranian Veterinary Journal, 15(4), 93-99.
 Alvela-Suárez, L., Velasco-Tirado, V., Belhassen-Garcia, M., Novo-Veleiro, I., Pardo-Lledías, J., Romero-Alegría, A., . . . Cordero-Sánchez, M. (2014). Safety of the combined use of praziquantel and albendazole in the treatment of human hydatid disease. The American journal of tropical medicine and hygiene, 90(5), 819.
 Arabkhazaeli, F., Rostami, A., Gilvari, A., Nabian, S., & Madani, S. A. (2018). Frequently observed parasites in pet reptiles’ feces in Tehran. Iran. J. Vet. Med, 12(1), 19-25.
 Arifin, W. N., & Zahiruddin, W. M. (2017). Sample size calculation in animal studies using resource equation approach. The Malaysian journal of medical sciences: MJMS, 24(5), 101.
 Bays, T. B., Lightfoot, T., & Mayer, J. (2006). Exotic pet behavior: birds, reptiles, and small mammals: Elsevier Health Sciences.
 Becker, K., Tilley, L., Vennerstrom, J. L., Roberts, D., Rogerson, S., & Ginsburg, H. (2004). Oxidative stress in malaria parasite-infected erythrocytes: host–parasite interactions. International journal for parasitology, 34(2), 163-189.
 Bower, D. S., Brannelly, L. A., McDonald, C. A., Webb, R. J., Greenspan, S. E., Vickers, M., . . . Greenlees, M. J. (2019). A review of the role of parasites in the ecology of reptiles and amphibians. Austral Ecology, 44(3), 433-448.
 Cavanagh, K. (2012). Plumb’s Veterinary Drug Handbook. Pocket—7th edition. The Canadian Veterinary Journal, 53(12), 1284.
 Chakrapani, B., Ramesh, V., Pourna Chander Rao, G., Ramachandran, D., Madhukar Reddy, T., Kalyan Chakravarthy, A., & Sridhar, G. (2018). Synthesis and anticancer evaluation of 1, 2, 4-oxadiazole linked imidazothiadiazole derivatives. Russian Journal of General Chemistry, 88, 1020-1024.
 Corrente, M., Sangiorgio, G., Grandolfo, E., Bodnar, L., Catella, C., Trotta, A., . . . Buonavoglia, D. (2017). Risk for zoonotic Salmonella transmission from pet reptiles: A survey on knowledge, attitudes and practices of reptile-owners related to reptile husbandry. Preventive veterinary medicine, 146, 73-78.
Dalvi, S. M., Patil, V. W., Ramraje, N. N., & Phadtare, J. M. (2012). Lipid peroxidation, superoxide dismutase and catalase co-relation in pulmonary and extra pulmonary tuberculosis. Free Radicals and Antioxidants, 2(4), 1-5.
 Demkowska-Kutrzepa, M., Studzińska, M., Roczeń-Karczmarz, M., Tomczuk, K., Abbas, Z., & Różański, P. (2018). A review of the helminths co-introduced with Trachemys scripta elegans–a threat to European native turtle health. Amphibia-Reptilia, 39(2), 177-189.
 Farhat, Z., Browne, R. W., Bonner, M. R., Tian, L., Deng, F., Swanson, M., & Mu, L. (2018). How do glutathione antioxidant enzymes and total antioxidant status respond to air pollution exposure? Environment international, 112, 287-293.
 Gholami, M. H., Rassouli, A., Mirzaei, S., & Hashemi, F. (2023). The potential immunomodulatory effect of levamisole in humans and farm animals. Journal of Advanced Veterinary and Animal Research, 10(4), 620.
 Gupta, S., Finelli, R., Agarwal, A., & Henkel, R. (2021). Total antioxidant capacity—Relevance, methods and clinical implications. Andrologia, 53(2), e13624.
 Hallinger, M. J., Taubert, A., Hermosilla, C., & Mutschmann, F. (2018). Occurrence of health-compromising protozoan and helminth infections in tortoises kept as pet animals in Germany. Parasites & vectors, 11(1), 352.
 Hidalgo-Vila, J., Díaz-Paniagua, C., Ribas, A., Florencio, M., Pérez-Santigosa, N., & Casanova, J. (2009). Helminth communities of the exotic introduced turtle, Trachemys scripta elegans in southwestern Spain: Transmission from native turtles. Research in veterinary science, 86(3), 463-465.
 Hulbert, A., Pamplona, R., Buffenstein, R., & Buttemer, W. (2007). Life and death: metabolic rate, membrane composition, and life span of animals. Physiological reviews, 87(4), 1175-1213.
Huo, J., Dong, A., Niu, X., Dong, A., Lee, S., Ma, C., & Wang, L. (2018). Effects of cadmium on oxidative stress activities in plasma of freshwater turtle Chinemys reevesii. Environmental Science and Pollution Research, 25, 8027-8034.
 Ince, S., Kozan, E., Kucukkurt, I., & Bacak, E. (2010). The effect of levamisole and levamisole+ vitamin C on oxidative damage in rats naturally infected with Syphacia muris. Experimental parasitology, 124(4), 448-452.
 Jing, M., Han, G., Wan, J., Zhang, S., Yang, J., Zong, W., . . . Liu, R. (2020). Catalase and superoxide dismutase response and the underlying molecular mechanism for naphthalene. Science of the Total Environment, 736, 139567.
 Kami, H. G., & Kalbassi, M. R. (2012). Biological study of the Caspian pond turtle (Mauremys caspica caspica). Animal Environment Journal, 4 (3).
 Machin, R. A. (2015). Common gastrointestinal parasites in reptiles. In Practice, 37(9), 469-475.
 Mathews, S., & Selvam, R. (1991). Effect of radical treatment on erythrocyte lipid peroxidation in Plasmodium vivax-infected malaria patients. Biochemistry international, 25(2), 211-220.
 Maurya, R., & Namdeo, M. (2021). Superoxide dismutase: A key enzyme for the survival of intracellular pathogens in host. Reactive Oxygen Species, 14.
 Mushtaq, M., Agrawal, R., Singh, R., & Pande, N. (2019). Immunomodulatory effect of levamisole therapy in pre-parturient dairy cows. Intas Polivet, 20(1), 1-3.
 Olaniyan, M., Ojediran, T., & Olayinka, G. (2020). Evidence of systemic responses to viral pathogens using malondialdehyde, tumor necrosis factor alpha and superoxide dismutase. Int J Clin Exp Physiol, 7(1), 18-21.
 Pane, R. S., Lubis, S. R., & Darmi, M. (2018). Analysis of Malondialdehyde Level in Leprosy Patients. International Journal of Innovative Research in Medical Science, 3 (10).
 Parks, D. (1989). Oxygen radicals: mediators of gastrointestinal pathophysiology. Gut, 30(3), 293.
 Pawłowska, M., Mila-Kierzenkowska, C., Szczegielniak, J., & Woźniak, A. (2023). Oxidative stress in parasitic diseases—Reactive oxygen species as mediators of interactions between the host and the parasites. Antioxidants, 13(1), 38.
 Pekmezci, D., & Cakiroglu, D. (2009). Investigation of immunmodulatory effects of levamisole and vitamin E on immunity and some blood parameters in newborn Jersey calves. Veterinary research communications, 33, 711-721.
 Plumb, D. C. (2018). Plumb's veterinary drug handbook: Desk: John Wiley & Sons.
 Sajid, M., Iqbal, Z., Muhammad, G., & Iqbal, M. (2006). Immunomodulatory effect of various anti-parasitics: a review. Parasitology, 132(3), 301-313.
 Sarkar, P., & Rautaray, S. (2009). A study of serum malondialdehyde levels and paraoxanase activity in ischemic stroke patients. Biomedical research, 20(1), 64-64.
 Schatzman, S. S., & Culotta, V. C. (2018). Chemical warfare at the microorganismal level: a closer look at the superoxide dismutase enzymes of pathogens. ACS infectious diseases, 4(6), 893-903.
 Silvestrini, A., Meucci, E., Ricerca, B. M., & Mancini, A. (2023). Total antioxidant capacity: biochemical aspects and clinical significance. International journal of molecular sciences, 24 (13) 10978.
 Simmons, T. W., & Jamall, I. S. (1988). Significance of alterations in hepatic antioxidant enzymes. Primacy of glutathione peroxidase. Biochemical Journal, 251(3), 913-917.
 Symoens, J., & Rosenthal, M. (1977). Levamisole in the modulation of the immune response: the current experimental and clinical state.
 Tibbetts, L. (2019). 17 Exotic Animal Medicine. Mosby's Comprehensive Review for Veterinary Technicians E-Book, 370.
 Tiedge, M., Lortz, S., Drinkgern, J., & Lenzen, S. (1997). Relation between antioxidant enzyme gene expression and antioxidative defense status of insulin-producing cells. Diabetes, 46(11), 1733-1742.
 Torabi Asl, M., Yasini, S. P., & Shirazi Beheshtiha, S. H. (2022). Evaluation of antioxidant enzymes and lipid peroxidation before and after ovariohysterectomy in queen. Iranian Veterinary Journal, 18(1), 71-76.
 Trimarchi, H., Mongitore, M., Baglioni, P., Forrester, M., Freixas, E., Schropp, M., . . . Alonso, M. (2003). N-acetylcysteine reduces malondialdehyde levels in chronic hemodialysis patients--a pilot study. Clinical Nephrology, 59(6), 441-446.
 Valdivia, P. A., Zenteno-Savín, T., Gardner, S. C., & Aguirre, A. A. (2007). Basic oxidative stress metabolites in eastern Pacific green turtles (Chelonia mydas agassizii). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 146(1-2), 111-117.
 Vamberger, M., Stuckas, H., Ayaz, D., Graciá, E., Aloufi, A. A., Els, J., . . . Fritz, U. (2013). Conservation genetics and phylogeography of the poorly known Middle Eastern terrapin Mauremys caspica (Testudines: Geoemydidae). Organisms Diversity & Evolution, 13, 77-85.
 Vasquez, M., Zuniga, M., & Rodriguez, A. (2021). Oxidative stress and pathogenesis in malaria. Frontiers in cellular and infection microbiology, 11, 768182.
 Vergles Rataj, A., Lindtner-Knific, R., Vlahović, K., Mavri, U., & Dovč, A. (2011). Parasites in pet reptiles. Acta veterinaria scandinavica, 53(33), 1-20.
 Yigit, A., Cinar, M., & Yildirim, E. (2012). The effects of levamisole on oxidative stress induced by copper intoxication in broilers. New Zealand Veterinary Journal, 60(5), 273-277.
 Youssefi, M. R., Mousapour, A., Nikzad, R., Gonzalez-Solis, D., Halajian, A., & Rahimi, M. T. (2016). Gastrointestinal helminths of the Caspian turtle, Mauremys caspica (Testudines), from Northern Iran. Journal of Parasitic Diseases, 40, 65-68.
Yuslianti, E. R., Ratwita, W., Koswara, T., & Afra, A. (2024). Potential of Rambutan-Honey Antioxidants in Reducing Malondialdehyde Levels and Regenerating Hepatocyte Cells in Isoniazid-Rats Induced. Jurnal Profesi Medika: Jurnal Kedokteran dan Kesehatan, 18(1), 76-83.