Therapeutic role of Thymol, Propolis and Balanites aegyptiaca against experimental Toxocara vitulorum infection https://doi.org/10.12982/VIS.2025.028
Main Article Content
Abstract
Toxocara vitulorum (T. vitulorum) is a significant intestinal nematode that has led to a large global economic loss for farm animals. While there is a paucity of safe and effective anthelmintic drug development against it. Thus, this work aimed to estimate the antiparasitic effect of Thymol, Balanites aegyptiaca (B. aegyptiaca), and propolis as an alternative treatments against T. vitulorum larvae in vivo. To achieve this purpose, the embryonation of T. vitulorum eggs were done in vitro. Then, a total of thirty female wester rats were divided into six groups (5 each). Infected rats were orally inoculated by 2500 eggs containing third stage larvae. These groups were (control negative), (control positive), treated with (piperazine citrate 300 mg/kg), (thymol 40 mg/kg), (B. aegyptiaca 250 mg/kg), and (propolis 100 mg/kg). Parasitological and histopathological responses of all treated groups were evaluated at 7 and 14 days post infection (dpi). Microscopical examination of lung, liver (pepsin digested organs) and brain (squashed method) were used for counting of larvae. The numbers of larvae reduced at 14 dpi and accomplished the highest reduction in Thymol group (75%) followed by Propolis group (55.8%) and B. aegyptiaca group (53.8%) than in control positive group. Histopathological examination proved that thymol followed by propolis and B. aegyptiaca extracts were effective in improving the pathological changes and had a good effect on organ damage protection that was caused by T. vitulorum larvae. So, they can be used as an alternative, safe, and effective treatment of T. vitulorum infection.
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
Publishing an article with open access in Veterinary Integrative Sciences leaves the copyright with the author. The article is published under the Creative Commons Attribution License 4.0 (CC-BY 4.0), which allows users to read, copy, distribute and make derivative works from the material, as long as the author of the original work is cited.
References
Abou-El-Naga, I.F., 2018. Developmental stages and viability of Toxocara canis eggs outside the host. Biomédica. 38,189-197.
Amin, M.M., El-Kabany, H., 2013. Evaluation of protective and treatment of Thyme (Thymus vulgaris) oil on Toxocara vitulorum infected rats. J. Radiat. Res. Appl. Sci. 6(1), 209-232.
Amin, M.M., Hafez, E.N., Abd Raboo, M.A., 2016. Assesment of radiation-attenuated vaccine or thyme oil treatment on controlling DNA damage and nitric oxide synthesis in brain of rat infected with Toxocara canis. Arab. J. Nucl. Sci. Appl. 49(2), 199-210.
Arafa, W.M., Abolhadid, S.M., Moawad, A., Abdelaty, A.S., Moawad, U.K., Shokier, K.A., Shehata, O., Gadelhaq, S.M., 2020. Thymol efficacy against coccidiosis in pigeon (Columba livia domestica). Prev. Vet. Med. 176, 104914.
Auliyah, R., Kusnoto, Hamid, I.S., 2021. Histopathology Description of Chicken Liver Infected by L2 Toxocara vitulorum. J. World. Poult. Res. 11(1), 123-128.
Avcioğlu, H., Balkaya, İ., 2011. Prevalence of Toxocara vitulorum in Calves in Erzurum, Turkey. Kafkas Univ. Vet. Fak. Derg. 17(3), 345-347.
Aydin, A., Goz, Y., Yuksek, N., Ayaz, E., 2006. Prevalence of Toxocara vitulorum in Hakkari eastern region of Turkey. Bull. Vet. Inst. Pulawy. 50(1), 51-54.
Azizi, S., Oryan, A., Sadjjadi, S.M., Zibaei, M., 2007. Histopathologic changes and larval recovery of Toxocara cati in experimentally infected chickens. Parasitol. Res. 102(1), 47-52.
Bancroft, J.D., Gambl, M., 2008. Theory and practice of histological techniques, 6th edition. Churchill Livingstone, New York, London, Philadelphia, pp. 126-134.
Bisseru, B., 1969. Studies on the liver, lung, brain and blood of experimental animals infected with Toxocara canis. J. Helminthol. 43(3), 267-272.
Borgsteede, F.H., Holzhauer, M., Herder, F.L., Veldhuis-Wolterbeek, E.G., Hegeman, C., 2012. Toxocara vitulorum in suckling calves in The Netherlands. Res. Vet. Sci. 92(2), 254-256.
Bowman, D.D., Mika-Grieve, M., Grieve, R.B., 1987. Circulating excretory-secretory antigen levels and specific antibody responses in mice infected with Toxocara canis. Am. J. Trop. Med. Hyg. 36(1), 75-82.
Cardillo, N., Rosa, A., Ribicich, M., López, C., Sommerfelt, I., 2009. Experimental infection with Toxocara cati in BALB/c mice, migratory behaviour and pathological changes. Zoonoses. Public. Health. 56(4), 198-205.
Carvalho, E.A., Rocha, R.L., 2014. Visceral larva migrans syndromes associated with toxocariasis: epidemiology, clinical and laboratory aspects of human toxocariasis. Curr. Trop. Med. Rep. 1, 74–79.
Chapagain, B.P., Wiesman, Z., 2005. Larvicidal effects of aqueous extracts of Balanites aegyptiaca (desert date) against the larvae of Culex pipiens mosquitoes. Afr. J. Biotechnol. 4(11), 1351–1354.
Chapagain, B.P., Wiesman, Z., 2008. Metabolite profiling of saponins in Balanites aegyptiaca plant tissues using LC (RI)-ESI/MS and MALDI-TOF/MS. Metabolomics. 4, 357–366.
Chelladurai, J.J., Bader, C., Snobl, T., Magstadt, D., Cooper, V., Brewer, M.T., 2015. Toxocara vitulorum infection in a cohort of beef calves in Iowa. Vet. Parasitol. 214(1-2), 96-99.
Chroho, M., Rouphael, Y., Petropoulos, S.A., Bouissane, L., 2024. Carvacrol and thymol content affects the antioxidant and antibacterial activity of origanum compactum and Thymus zygis Essential Oils. Antibiotics. 13, 139.
Courtney, C.H., Roberson, E.L., 1995. Chemotherapy of parasitic diseases, In: Adams, H.R. (Ed.), Veterinary pharmacology and therapeutics, (7th edition). Iowa State University Press, Ames, pp. 886–888.
Cruz, L.M., Allanson, M., Kwa, B., Azizan, A., Izurieta, R., 2012. Morphological changes of Ascaris spp. eggs during their development outside the host. J. Parasitol. 98(1), 63-68.
Dewair, A., Bessat M., 2020. Molecular and microscopic detection of natural and experimental infections of Toxocara vitulorum in bovine milk. PLoS ONE. 15(5), e0233453.
Dunsmore, J.D., Thompson, R.C., Bates, I.A., 1983. The accumulation of Toxocara canis larvae in the brains of mice. Int. J. Parasitol. 13(5), 517-521.
Duru, Ö., Gökpınar, S., Duru, S.Y., Akanbong, E.A., Kara, E., 2023. The therapeutic effectiveness of thyme extract in naturally infected puppies with ascariasis. T.J.V.R. 7(1), 39-45.
El-Nahas, N.S., Abd-Elatty, A.F., Rady, A.A., El-Aswad, B.E., Attallah, A.M., Hemida, A.S., 2020. Anti-Toxocara effects of Cassia nodosa plant extract in experimentally infected mice. Menoufia Med. J. 33, 191-195.
Fan, C., Su, K., 2004. Cross-reactions with Ascaris suum antigens of sera from mice infected with A. suum, Toxocara canis, and Angiostrongylus cantonensis. Parasitol. Int. 53(3), 263-271.
Ferreira, L.E., Benincasa, B.I., Fachin, A.L., França, S.C., Contini, S.S.H.T., Chagas, A.C.S., Beleboni, R.O., 2016. Thymus vulgaris L. essential oil and its main component thymol: Anthelmintic effects against Haemonchus contortus from sheep. Vet. Parasitol. 228, 70-76.
Gasser, R.B., 2013. A perfect time to harness advanced molecular technologies to explore the fundamental biology of Toxocara species. Vet. Parasitol. 193(4), 353-364.
Gibson-Corley, K.N., Olivier, A.K., Meyerholz, D.K., 2013. Principles for valid histopathologic scoring in research. Vet. Pathol. 50(6), 1007-1015.
Glickman, L.T., Magnaval, J.F., Domanski, L.M., Shofer, F.S., Lauria, S.S., Gottstein, B., Brochier, B., 1987. Visceral larva migrans in French adults: a new disease syndrome? Am. J. Epidemiol. 125(6), 1019–1034.
Gnoula, C., Guissou, P., Dubois, J., Frédérich, M., Duez, P., 2006. Nematocidal compounds from the seeds of Balanites aegyptiaca isolation and structure elucidation. Planta. Med. 72, 33.
Hassan, S.E., Abou-El-Dobal, S.K., Hegazi, A.G., 2016. Bioassay of Egyptian Propolis on Toxocara vitulorum adult worms. World. Appl. Sci. J. 34(3), 283-289.
Hafez, E.N., Hafez, M.N., Amin, M.M., 2019. Effect of vaccination with irradiated Toxocara canis larvae or thyme oil treatment on testicular histochemical and immunohistochemical changes of rats. Trop. Biomed. 36(2), 430-442.
Hegazi, A.G., Abd El Hady, F.K., Shalaby, H.A., 2007. An in vitro effect of propolis on adult worms of Fasciola gigantica. Vet. Parasitol. 144 (3-4), 279-286.
Holland, C.V., 2017. Knowledge gaps in the epidemiology of Toxocara: the enigma remains. Parasitology. 144(1), 81-94.
Hossain, R., Quispe, C., Khan, R.A., Saikat, A.M., Ray, P., Ongalbek, D., Yeskaliyeva, B., Jain, D., Smeriglio, A., Trombetta, D., Kiani, R., Kobarfard, F., Mojgani, N., Saffarian, P., Ayatollahi, S.A., Sarkar, C., Islam, M.T., Keriman, D., Ucar, A., Martorell, M., Sureda, A., Pintus, G., Butnariu, M., Sharifi‑Rad, J., Cho, W.C., 2022. Propolis: an update on its chemistry and pharmacological applications. Chinese. Med. 17, 100.
Iqbal, Z., Akhtar, M.S., Sindhu, Z., Khan, M.N., Jabbar, A., 2003. Herbal dewormers in livestock - a traditional therapy. Int. J. Agri. Biol. 5(2), 199-206.
Islam, M.K., Miyoshi, T., Yamada, M., Alim, M.A., Huang, X., Motobu, M., Tsuji, N., 2006. Effect of piperazine (diethylenediamine) on the moulting, proteome expression and pyrophosphatase activity of Ascaris suum lung-stage larvae. Acta Trop. 99(2-3), 208-217.
Janecek, E., Beineke, A., Schnieder, T., Strube, C., 2014. Neurotoxocarosis: marked preference of Toxocara canis for the cerebrum and T. cati for the cerebellum in the paratenic model host mouse. Parasit. Vectors. 7(1), 194.
Jones, J.R., Mitchell, E.S., Redman, E., Gilleard, J.S. 2009. Toxocara vitulorum infection in a cattle herd in the UK. Vet. Rec. 164(6), 171-172.
Kowalczyk, A., Przychodna, M., Sopata, S., Bodalska, A., Fecka, I., 2020. Thymol and Thyme essential oil—new insights into selected therapeutic applications. Molecules. 25(18), 4125.
Llanes, K.K., Besana, C.M., Paller, V.G., 2019. Larval distribution, migratory pattern and histological effects of Toxocara canis in Rattus norvegicus. J. Parasit. Dis. 43(4), 679–685.
Ma, G., Holland, C.V., Wang, T., Hofmann, A., Fan, C., Maizels, R.M., Hotez, P.J., Gasser, R.B., 2018. Human toxocariasis. Lancet Infect. Dis. 18(1), e14-e24.
Macpherson, C.N., 2013. Dog zoonoses and human health: a global perspective - mini review. CABI Reviews. 8(002), 1-2.
Mehlhorn, H., 2015. Toxocara (syn. Neoascaris) vitulorum. In: Mehlhorn, H. (Ed.), Encyclopedia of parasitology. Springer, Berlin, Heidelberg.
Moyo, D.Z., 2002. The Migratory behaviour of Toxocara canis and Toxocara vitulorum in Balb/c Mice. Zimb. Vet. J. 33(1), 7-13.
Murthy, H.N., Yadav, G.G., Dewir, Y.H., Ibrahim, A., 2020. Phytochemicals and biological activity of desert date (Balanites aegyptiaca (L.) Delile). Plants (Basel). 10(1), 32.
Musa, D., Senocak, G., Borazan, G., Altas, M., Ozgonul, A., Sogut, O., Güldür, M.E., 2011. Effects of Nigella sativa and albendazole alone and in combination in Toxocara canis infected mice. J. Pak. Med. Assoc. 61(9), 866-870.
Naderbandi, M., Zibaei, M., Haniloo, A., Firoozeh, F., Hatami, Z., Shokri, E., Taira K., 2022. Larva migrans in BALB/c mice experimentally infected with Toxocara cati ensured by PCR assay. BMC Vet. Res. 18, 257.
Rajkhowa, S., Bujarbaruah, K.M., Rajkhowa, C., 2004. Haematobiochemical changes in ascarosis of Mithun calves. Indian. Vet. J. 81, 571–572.
Raza, M.A., Murtaza, S., Ayaz, M.M., Akhtar, S., Arshad, H.M., Basit, A., Bachaya, H.A., Ali, M., Khan M.I., 2013. Toxocara vitulorum infestation and associated risk factors in cattle and buffalo at Multan district. Pakistan. Sci. Int (Lahore). 25(2), 291-294.
Resende, N.M., Gazzinelli-Guimarães, P.H., Barbosa, F.S., Oliveira, L.M., Nogueira, D.S., Gazzinelli-Guimarães, A.C., Gonçalves, M.T., Amorim, C.C., Oliveira, F.M., Caliari, M.V., Rachid, M.A., Volpato, G.T., Bueno, L.L., Geiger, S.M., Fujiwara, R.T., 2015. New insights into the immunopathology of early Toxocara canis infection in mice. Parasit. Vectors. 8, 354.
Rizk, M.A., Osman, S.A., AL-Gaabary, M.H., EL-Khodery, S.A., 2018. Comparative clinical and parasitological efficacy of moxidectin pour-on, ivermectin, and piperazine citrate on Toxocara vitulorum infection in buffalo calves (Bubalus bubalis): a randomized clinical trial. Turk. J. Vet. Anim. Sci. 42(1), 29-33.
Roberts, J.A., 1990. The life cycle of Toxocara vitulorum in Asian buffalo (Bubalus bubalis). Int. J. Parasitol. 20(7), 833-840.
Roberts, J.A., Fernando, S.T., Sivanathan, S., 1990. Toxocara vitulorum in the milk of buffalo (Bubalus bubalis) cows. Res. Vet. Sci. 49(3), 289-291.
Sahoo, C.R., Paidesetty, S.K., Padhy, R.N., 2021. The recent development of thymol derivative as a promising pharmacological scaffold. Drug. Dev. Res. 82, 1079–1095.
Samanta, S., Ansari, M., 1990. Embryonation of ova of Toxocara canis (Werner, 1782) and migration of the larvae in mice. Indian J. Anim. Sci. 60, 1391–1393.
Santos, S.V., Lescano, S.Z., Castro, J.M., Chieffi, P.P., 2009. Larval recovery of Toxocara cati in experimentally infected Rattus norvegicus and analysis of the rat as potential reservoir for this ascarid. Mem. Inst. Oswaldo Cruz. 104(6), 933-934.
Shalaby, M.A., Moghazy, F.M., Shalaby, H.A., Nasr, S.M., 2010. Effect of methanolic extract of Balanites aegyptiaca fruits on enteral and parenteral stages of Trichinella spiralis in rats. Parasitol. Res. 107(1), 17-25.
Shalaby, H.A., El Namaky, A.H., Khalil, F.A., Kandil, O.M., 2012. Efficacy of methanolic extract of Balanites aegyptiaca fruits on Toxocara vitulorum. Vet. Parasitol. (183), 386–392.
Shehata, O., Aboelhadid, S.M., Arafa, W.M., Moawad, U.K., Hussien, K.H., Ali, M.I., El-Ashram, S., Abdel Gawad, S.S., Abdel-Aziz, S.A., 2022. Assessment of the efficacy of thymol against Toxocara vitulorum in experimentally infected rats. J. Parasit. Dis. 46(2), 454-465.
Singh, K., Mishra, S.K., Pruthi, A.K., 2008. Pathology of parasitic infestations in gastrointestinal tract in buffalo calves. J. Vet. Parasitol. 22(1), 17-20.
Soares, M.J., 2006. Endocytic portals in Trypanosoma cruzi epimastigote forms. Parasitol. Res. 99, 321–322.
Soulsby, E.J.L., Mönnig, H.O., 1968. Helminths, arthropods & protozoa of domesticated animals, 6th edition. Williams and Wilkins, Baltimore, pp. 824.
Srivastava, A.K., Sharma, D.N., 1981. Studies on the occurrence, clinical features and pathomorphological aspects of ascariasis in buffalo calves. Vet. Res. J. 4, 160–162.
Sultan, K., Omar, M., Desouky, A.Y., El-Seify, M.A., 2015. Molecular and phylogenetic study on Toxocara vitulorum from cattle in the mid-Delta of Egypt. J. Parasit. Dis. 39(3), 584-587.
Venjakob, P.L., Thiele, G., Clausen, P.H., Nijhof, A.M., 2017. Toxocara vitulorum infection in German beef cattle. Parasitol. Res. 116(3), 1085-1088.
Zibaei, M., Sadjjadi, S.M., Uga, S., 2010. Experimental Toxocara cati Infection in Gerbils and Rats. Korean. J. Parasitol. 48(4), 331-333.