Skip to main content Accessibility help
Hostname: page-component-559fc8cf4f-67gxp Total loading time: 0.603 Render date: 2021-02-27T22:57:39.522Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": false, "newCiteModal": false, "newCitedByModal": true }

Article contents

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

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
Division of Agricultural Science, Mahidol University, Kanchanaburi Campus, Saiyok, Kanchanaburi 71150, Thailand
Department of Pharmacognosy and Pharmaceutical Botany, Faculty of Pharmaceutical Sciences, Prince of Songkla University, Hat-Yai, Songkhla 90112, Thailand
Faculty of Environment and Resource Studies, Mahidol University, Phuttamonthon District, NakhonPathom 73170, Thailand
Department of Microbiology, Faculty of Science, Mahidol University, Rama VI Road, Bangkok 10400, Thailand
Department of Anatomy, Faculty of Medicine, Srinakharinwirot University, Sukhumvit 23, Klongtoey Wattana, Bangkok 10110, Thailand
Faculty of Environmental Culture and Ecotourism, Srinakharinwirot University, Sukhumvit 23, Klongtoey Wattana, Bangkok 10110, Thailand
Department of Anatomy, Faculty of Science, Mahidol University, Rama VI Road, Bangkok 10400, Thailand
Department of Anatomy, Faculty of Science, Mahidol University, Rama VI Road, Bangkok 10400, Thailand


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.

Research Article
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below.


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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Bennett, C. E. (1975 a). Surface features, sensory structures and movement of the newly excysted juvenile Fasciola hepatica . Journal of Parasitology 61, 886891.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Halton, D. W. (2004). Review: microscopy and the helminth parasite. Micron 35, 361390.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Rolfe, P. F. and Boray, J. C. (1988). Chemotherapy of paramphistomosis in sheep. Australian Veterinary Journal 65, 148150.CrossRefGoogle 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 ScholarPubMed
Sanabria, R. E. F. and Romero, J. R. (2008). Review and update of paramphistomosis. Helminthologia 45, 6468.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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.). 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed

Altmetric attention score

Full text views

Full text views reflects PDF downloads, PDFs sent to Google Drive, Dropbox and Kindle and HTML full text views.

Total number of HTML views: 22
Total number of PDF views: 105 *
View data table for this chart

* Views captured on Cambridge Core between September 2016 - 27th February 2021. This data will be updated every 24 hours.

Send article to Kindle

To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

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

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

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

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

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

Reply to: Submit a response

Your details

Conflicting interests

Do you have any conflicting interests? *