Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-23T08:10:24.991Z Has data issue: false hasContentIssue false

The anthelmintic effects of the ethanol extract of Terminalia catappa L. leaves against the ruminant gut parasite, Fischoederius cobboldi

Published online by Cambridge University Press:  01 February 2016

PANAT ANURACPREEDA*
Affiliation:
Division of Agricultural Science, Mahidol University, Kanchanaburi Campus, Saiyok, Kanchanaburi 71150, Thailand Department of Anatomy, Faculty of Science, Mahidol University, Rama VI Road, Bangkok 10400, Thailand
KANOKWAN CHANKAEW
Affiliation:
Division of Agricultural Science, Mahidol University, Kanchanaburi Campus, Saiyok, Kanchanaburi 71150, Thailand
PANUPONG PUTTARAK
Affiliation:
Department of Pharmacognosy and Pharmaceutical Botany, Faculty of Pharmaceutical Sciences, Prince of Songkla University, Hat-Yai, Songkhla 90112, Thailand
PREEYAPORN KOEDRITH
Affiliation:
Faculty of Environment and Resource Studies, Mahidol University, Phuttamonthon District, NakhonPathom 73170, Thailand
RUNGLAWAN CHAWENGKIRTTIKUL
Affiliation:
Department of Microbiology, Faculty of Science, Mahidol University, Rama VI Road, Bangkok 10400, Thailand
BUSABA PANYARACHUN
Affiliation:
Department of Anatomy, Faculty of Medicine, Srinakharinwirot University, Sukhumvit 23, Klongtoey Wattana, Bangkok 10110, Thailand
ARIN NGAMNIYOM
Affiliation:
Faculty of Environmental Culture and Ecotourism, Srinakharinwirot University, Sukhumvit 23, Klongtoey Wattana, Bangkok 10110, Thailand
SUMALEE CHANCHAI
Affiliation:
Department of Anatomy, Faculty of Science, Mahidol University, Rama VI Road, Bangkok 10400, Thailand
PRASERT SOBHON
Affiliation:
Department of Anatomy, Faculty of Science, Mahidol University, Rama VI Road, Bangkok 10400, Thailand
*
* Corresponding author: Division of Agricultural Science, Mahidol University, Kanchanaburi Campus, Saiyok, Kanchanaburi 71150, Thailand. E-mail: [email protected], [email protected]

Summary

Presently, no effective anthelmintic drugs have been used to treat and control paramphistomosis, a severe disease of ruminants. In this study, we have investigated the in vitro anthelmintic effect of the leaves of Terminalia catappa L. crude extract (TcCE) and albendazole (ABZ) on adult Fischoederius cobboldi after incubating the flukes in RPMI-1640 medium containing the TcCE at various doses and times. The TcCE-treated flukes at all dosages exhibited rapid decrease of motility, and the relative motility (RM) values were decreased sharply from start to 3 h. Worms were killed after 6 and 12 h of treatment with 1000, 1500 and 2000 µg mL−1 as well as 500 µg mL−1 of TcCE, respectively. By light microscopy examination, the flukes exhibited the earliest alteration in a limited area of the tegument. At scanning electron microscopy level, the flukes’ tegument showed similar sequence of morphological alterations after treatment with ABZ and TcCE that consisted of swelling of ridges and folds, followed by blebbing and rupturing of the blebs, leading to the erosion, lesion and disruption of the tegument. Hence, in vivo studies should be performed to examine whether the TcCE may serve as a powerful anthelmintic drug for treatment of paramphistomosis.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ahluwalia, S. S. (1960). Gastrodiscoides hominis (Lewis and McConnell, 1876) Leiper, 1913-the amphistome parasite of man and pig. The Indian Journal of Medical Research 48, 315325.Google Scholar
Anuracpreeda, P., Wanichanon, C. and Sobhon, P. (2008). Paramphistomum cervi: antigenic profile of adults as recognized by infected cattle sera. Experimental Parasitology 118, 203207.Google Scholar
Anuracpreeda, P., Panyarachun, B., Ngamniyom, A., Tinikul, Y., Chotwiwatthanakun, C., Poljaroen, J. and Sobhon, P. (2012). Fischoederius cobboldi: a scanning electron microscopy investigation of surface morphology of adult rumen fluke. Experimental Parasitology 130, 400407.Google Scholar
Anuracpreeda, P., Chawengkirtikul, R., Tinikul, Y., Poljaroen, J., Chotwiwatthanakun, C. and Sobhon, P. (2013 a). Diagnosis of Fasciola gigantica infection using a monoclonal antibody-based sandwich ELISA for detection of circulating cathepsin B3 protease. Acta Tropica 127, 3845.Google Scholar
Anuracpreeda, P., Poljaroen, J., Chotwiwatthanakun, C., Tinikul, Y. and Sobhon, P. (2013 b). Antigenic components, isolation and partial characterization of excretion–secretion fraction of Paramphistomum cervi . Experimental Parasitology 133, 327333.Google Scholar
Anuracpreeda, P., Srirakam, T., Pandonlan, S., Changklungmoa, N., Chotwiwatthanakun, C., Tinikul, Y., Poljaroen, J., Meemon, K. and Sobhon, P. (2014). Production and characterization of a monoclonal antibody against recombinant cathepsin L1 of Fasciola gigantica . Acta Tropica 135, 19.CrossRefGoogle Scholar
Anuracpreeda, P., Phutong, S., Ngamniyom, A., Panyarachun, B. and Sobhon, P. (2015). Surface topography and ultrastructural architecture of the tegument of adult Carmyerius spatiosus Brandes, 1898. Acta Tropica 143, 1828.CrossRefGoogle ScholarPubMed
Athanasiadou, S., Githiori, J. and Kyriazakis, I. (2007). Medicinal plants for helminth parasite control: facts and fiction. Animal 1, 13921400.Google Scholar
Atjanasuppat, K., Wongkham, W., Meepowpan, P., Kittakoop, P., Sobhon, P., Bartlett, A. and Whitfield, P. J. (2009). In vitro screening for anthelmintic and antitumour activity of ethnomedicinal plants from Thailand. Journal of Ethnopharmacology 123, 475482.Google Scholar
Bennett, C. E. (1975 a). Surface features, sensory structures and movement of the newly excysted juvenile Fasciola hepatica . Journal of Parasitology 61, 886891.Google Scholar
Bennett, C. E. (1975 b). Scanning electron microscopy of Fasciola hepatica during growth and maturation in the mouse. Journal of Parasitology 61, 892898.CrossRefGoogle ScholarPubMed
Chen, P. S., Li, J. H., Liu, T. Y. and Lin, T. C. (2000). Folk medicine Terminalia catappa and its major tannin component, punicalagin, are effective against bleomycin-induced genotoxicity in Chinese hamster ovary cells. Cancer Letters 152, 115122.Google Scholar
Chethanon, U., Ausavamatha, P. and Piriyayon, S. (1985). Parasitological survey of cattle in the south of Thailand. Proceedings of the 4th Annual Livestock Conference, 3–5 July 1985. Department Livestock Development, pp. 281290.Google Scholar
Chu, S. C., Yang, S. F., Liu, S. J., Kuo, W. H., Chang, Y. Z. and Hsieh, Y. S. (2007). In vitro and in vivo antimetastatic effects of Terminalia catappa L. Leaves on lung cancer cells. Food and Chemical Toxicology 45, 11941201.Google Scholar
Dangprasert, T., Khawsuk, W., Meepol, A., Wanichanon, C., Viyanant, V., Upatham, E. S., Wongratanacheevin, S. and Sobhon, P. (2001). Fasciola gigantica: surface topography of the adult tegument. Journal of Helminthology 75, 4350.Google Scholar
Dutt, S. C. and Srivastava, H. D. (1972). The life history of Gastrodiscoides hominis (Lewis and McConnel, 1876) Leiper, 1913, the amphistome parasite of man and pig. Journal of Helminthology 46, 3546.Google Scholar
Fyhrquist, P., Mwasumbi, L., Haeggström, C. A., Vuorela, H., Hiltunen, R. and Vuorela, P. (2002). Ethnobotanical and antimicrobial investigation on some species of Terminalia and Combretum (Combretaceae) growing in Tanzania. Journal of Ethnopharmacology 79, 169177.Google Scholar
Geary, T. G., Chibale, K., Abegaz, B., Andrae-Marobela, K. and Ubalijoro, E. (2012). A new approach for anthelminthic discovery for human. Trends in Parasitology 28, 176181.Google Scholar
Geurden, T., Somers, R., Thanh, N. T., Vien, L. V., Nga, V. T., Giang, H. H., Dorny, P., Giao, H. K. and Vercruysse, J. (2008). Parasitic infections in dairy cattle around Hanoi, northern Vietnam. Veterinary Parasitology 153, 384388.Google Scholar
Germosén-Robineau, L. (2014). Farmacopea Vegetal Carbeña. CICY editorial, Yucatán, Mexico p. 360.Google Scholar
Gupta, P. P., Singh, B. and Dutt, S. C. (1978). A note on amphistomiasis in an adult buffalo. The Indian Veterinary Journal 55, 491492.Google Scholar
Hanna, R. E. B., Williamson, D. S., Mattison, R. G. and Nizami, W. A. (1988). Seasonal reproduction in Paramphistomum epiclitum and Gastrothylax crumenifer, rumen paramphistomes of the Indian water buffalo, and comparison with the biliary paramphistome Gigantocotyle explanatum . International Journal for Parasitology 18, 513521.Google Scholar
Harinasuta, T., Bunnag, D. and Radomyos, P. (1987). Intestinal fluke infections. Baillieres Clinical Tropical Medicine and Communicable Diseases 2, 695721.Google Scholar
Horak, I. G. (1971). Paramphistomiasis of domestic ruminants. Advances in Parasitology 9, 3371.Google Scholar
Halton, D. W. (2004). Review: microscopy and the helminth parasite. Micron 35, 361390.Google Scholar
Hossain, E., Chandra, G., Nandy, A. P., Mandal, S. C. and Gupta, J. K. (2012). Anthelmintic effect of a methanol extract of Bombax malabaricum leaves on Paramphistomum explanatum . Parasitology Research 110, 10971102.Google Scholar
Ilha, M. R., Loretti, A. P. and Reis, A. C. (2005). Wasting and mortality in beef cattle parasitized by Eurytrema coelamaticum in the state of Parana, southern Brazil. Veterinary Parasitology 133, 4960.Google Scholar
Keiser, J. and Morson, G. (2008). Fasciola hepatica: tegumental alterations in adult flukes following in vitro and in vivo administration of artesunate and artemether. Experimental Parasitology 118, 228237.CrossRefGoogle ScholarPubMed
Khan, U. J., Tanveer, A., Maqbool, A. and Masood, S. (2008). Epidemiological studies of paramphistomosis in cattle. Veterinarski Arhiv 78, 243251.Google Scholar
Kiuchi, F., Miyashita, N., Tsuda, Y., Kondo, K. and Yoshimura, H. (1987). Studies on crude drugs effective on visceral larva migrans. I. Identification of larvicidal principles in betel nuts. Chemical and Pharmaceutical Bulletin 35, 28802886.Google Scholar
Kumar, V. (1980). The digenetic trematodes, Fasciolopsis buski, Gastrodiscoides hominis and Artyfechinostomum malayanum, aszoonotic infections in South Asian countries. Annales de la Société belge de médecine tropicale 60, 331339.Google ScholarPubMed
Kumar, B. G., Kumari, D., RAjeshwar, G., Umadevi, V. and Kotla, N. G. (2014). Antiulcer activity of ethanolic extract of Terminalia catappa leaves against gastric ulcers by pyrolic ligation induced model in rats. International Journal of Pharmaceutical Sciences and Drug Research 6, 3840.Google Scholar
Lin, C. C., Chen, Y. L., Lin, J. M. and Ujiie, T. (1997). Evaluation of the antioxidant and hepatoprotective activity of Terminalia catappa . The American Journal of Chinese Medicine 25, 153161.Google Scholar
Meaney, M., Fairweather, I., Bernnan, G. P., Ramasamy, P. and Subramanian, P. B. (2002). Fasciola gigantica: tegumental surface alterations following treatment in vitro with the sulphoxide metabolite of triclabendazole. Parasitology Research 88, 315325.Google Scholar
Meaney, M., Fairweather, I., Bernnan, G. P., McDowell, L. S. L. and Forbes, A. B. (2003). Fasciola hepatica: effects of the fasciolicide clorsulon in vitro and in vivo on the tegument surface, and a comparison of the effects on young- and old-mature flukes. Parasitology Research 91, 238250.Google Scholar
Meaney, M., Fairweather, I., Bernnan, G. P. and Forbes, A. B. (2004). Transmission electron microscopy study of the ultrastructural changes induced in the tegument and gut of Fasciola hepatica following in vivo drug treatment with closulon. Parasitology Research 92, 232241.Google Scholar
Magalhães, L. G., Kapadia, G. J., da Silva Tonuci, L. R., Caixeta, S. C., Parreira, N. A., Rodrigues, V. and Da Silva Filho, A. A. (2010). In vitro schistosomicidal effects of some phloroglucinol derivatives from Dryopteris species against Schistosoma mansoni adult worms. Parasitology Research 56, 395401.Google Scholar
Nagappa, A. N., Thakurdesai, P. A., Venkat Rao, N. and Singh, J. (2003). Antidiabetic activity of Terminalia catappa Linn fruits. Journal of Ethnopharmacology 88, 4550.Google Scholar
Nikitin, V. F. (1979). The course of acute enzootic amphistomiasis in claves in the lower Volga region. Helminthological Abstract Series A 48, 463.Google Scholar
Nunes, A. F., Viana, V. S. L., Brito Junior, E. C., Rabelo, R. S., Nunes Filho, D. M., Nunes, P. H. M. and Martins, M. C. C. (2012). Antiulcerogenic activity of ethanol extract of the bark from Terminalia catappa in gastric ulcer model induced by ethanol in Rattus norgegicus . Pharmacologyonline 9, 98101.Google Scholar
Panyarachun, B., Sobhon, P., Yotsawan, T., Chotwiwatthanakun, C., Anupunpisit, V. and Anuracpreeda, P. (2010). Paramphistomum cervi: surface topography of the tegument of adult fluke. Experimental Parasitology 125, 9599.Google Scholar
Panyarachun, B., Ngamniyom, A., Sobhon, P. and Anuracpreeda, P. (2013). Morphology and histology of the adult Paramphistomum gracile Fischoeder, 1901. Journal of Veterinary Science 14, 425432.Google Scholar
Prasitirat, P., Chompoochan, T., Nithiuthai, S., Wongkasemjit, S., Punmamoamg, T., Pongrut, P., Chinone, S. and Itagaki, H. (1997 a). Prevalence of amphistomes of cattle in Thailand. Parasitology (Hungary) 29–30, 2732.Google Scholar
Prasitirat, P., Nithiuthai, S., Ruengsuk, K., Kitwan, P., Bunmatid, C., Roopan, S. and Itagaki, H. (1997 b). Efficacy of bithionol sulfoxide, niclosamide and fenbendazole against natural rumen fluke infection in cattle. Helminthologia 34, 155157.Google Scholar
Robinson, R. D., Williams, L. A. D., Linda, J. F., Terzy, S. I. and Mansingh, A. (1990). Inactivation of Strongyloides stercoralis larvae in vitro by six Jamaican plant extracts and three commercial anthelmintics. The West Indian Medical Journal 39, 213217.Google Scholar
Rolfe, P. F. and Boray, J. C. (1988). Chemotherapy of paramphistomosis in sheep. Australian Veterinary Journal 65, 148150.Google Scholar
Rolfe, P. E., Boray, J. C., Nichols, P. and Collins, G. H. (1991). Epidemiology of paramphistomosis in cattle. Australian Veterinary Journal 21, 813819.Google Scholar
Sanabria, R. E. F. and Romero, J. R. (2008). Review and update of paramphistomosis. Helminthologia 45, 6468.Google Scholar
Saowakon, N., Tansatit, T., Wanichanon, C., Chanakul, W., Reutrakul, V. and Sobhon, P. (2009). Fasciola gigantica: anthelmintic effect of the aqueous extract of Artocarpus lakoocha . Experimental Parasitology 122, 289298.Google Scholar
Skuce, P. J., Anderson, H. R. and Fairweather, I. (1987). The interaction between the deacetylated (amine) metabolite of diamphenethide (DAMD) and cytochemically demonstrable Na+/K+-ATPase activity in the tegument of Fasciola hepatica . Parasitology Research 74, 161167.Google Scholar
Sobhon, P. and Upatham, E. S. (1990). Snail hosts, life-cycle, and tegumental structure of oriental schistosomes. UNDP/World Bank/WHO Special Programme for Research and Training in Tropical Diseases, pp. 57–88.Google Scholar
Sobhon, P. and Apinhasamit, W. (1996). Opisthorchis viverrini: the effect of colchicines and cytochalasin B on the adult tegument. The Southeast Asian Journal of Tropical Medicine and Public Health 27, 312317.Google Scholar
Tanaka, T., Nonaka, G. I., Ishimatsu, M., Nishioka, I. and Kouno, I. (2001). Revised structure of cercidinin A, a novel ellagitannin having (R)-hexahydroxydiphenoyl esters at the 3, 4-positions of glucopyranose. Chemical and Pharmaceutical Bulletin (Tokyo) 49, 486487.Google Scholar
Tandon, V., Pal, P., Roy, B., Rao, H. S. P. and Reddy, K. S. (1997). In vitro anthelmintic activity of root-tuber extract of Flemingia vestita, an indigenous plant in Shillong, India. Parasitology Research 83, 492498.Google Scholar
Tang, X. H., Gao, J., Wang, Y. P., Xu, L. Z., Zhao, X. N. and Xu, Q. (2003). Hepatoprotective effects of chloroform extract from leaf of Terminalia catappa in relation to the inhibition of liver IL-6 expression. Zhongguo Zhong Yao Za Zhi 28, 11701174.Google Scholar
Tansatit, T., Sahaphong, S., Riengrojpitak, S., Viyanant, V. and Sobhon, P. (2012). Fasciola gigantica: the in vitro effects of artesunate as compared to triclabendazole on the 3-weeks-old juvenile. Experimental Parasitology 131, 819.Google Scholar
Tariq, K. A., Chishti, M. Z., Ahmad, F. and Shawl, A. S. (2008). The epidemiology of paramphistomosis of sheep (Ovis aries L.) in the north west temperate Himalayan region of India. Veterinary Research Communications 32, 383391.Google Scholar
Thomson, L. A. J. and Evans, B. (2006). Terminalia catappa (tropical almond), 2·2. In Species Profiles for Pacific Island Agroflorestry: Permanent Agriculture Resources (PAR) (ed. Elevitch, C. R.). http://www.traditionaltree.org Google Scholar
Veesommai, U. and Janjittikul, T. (2001). Plant Materials in Thailand, 2nd Edn. Amarin Book Center Co., Ltd., Bangkok, Thailand, p. 637.Google Scholar
Wang, C. R., Qiu, J. H., Zhu, X. Q., Han, X. H., Ni, H. B., Zhao, J. P., Zhou, Q. M., Zhang, H. W. and Lun, Z. R. (2006). Survey of helminths in adult sheep in Heilongjiang Province, People's Republic of China. Veterinary Parasitology 140, 378382.Google Scholar
Wongsawad, C., Wongsawad, P., Luangphai, P. and Kumchoo, K. (2005). In vitro effects of aqueous extract from Artocarpus takoocha Roxb on tegumental surface of Haplorchis taichui . The Southeast Asian Journal of Tropical Medicine and Public Health 36(Suppl. 4), 112116.Google ScholarPubMed
Yeh, C. B., Hsieh, M. J., Hsieh, Y. S., Chien, M. H., Lin, P. Y., Chiou, H. L. and Yang, S. F. (2012). Terminalia catappa exerts antimetastatic effects on hepatocellular carcinoma through transcriptional inhibition of matrix metalloproteinase-9 by modulating NF-κB and AP-1 Activity. Evidence-based Complementary and Alternative Medicine 2012, Article ID 595292. doi:10.1155/2012/595292.Google Scholar