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The in vitro anthelmintic activity of the ethanol leaf extracts of Terminalia catappa L. on Fasciola gigantica

Published online by Cambridge University Press:  14 August 2017

PANAT ANURACPREEDA ,
RUNGLAWAN CHAWENGKIRTTIKUL ,
ARIN NGAMNIYOM ,
BUSABA PANYARACHUN ,
PANUPONG PUTTARAK ,
PREEYAPORN KOEDRITH  and
NOPPADOL INTARATAT
PANAT ANURACPREEDA*
Affiliation:
Institute of Molecular Biosciences, Mahidol University, Salaya, Nakhon Pathom 73170, Thailand
RUNGLAWAN CHAWENGKIRTTIKUL
Affiliation:
Department of Microbiology, Faculty of Science, Mahidol University, Rama VI Rd., Bangkok 10400, Thailand
ARIN NGAMNIYOM
Affiliation:
Faculty of Environmental Culture and Ecotourism, Srinakharinwirot University, Sukhumvit 23, Klongtoey Wattana, Bangkok 10110, Thailand
BUSABA PANYARACHUN
Affiliation:
Department of Anatomy, Faculty of Medicine, Srinakharinwirot University, Sukhumvit 23, Klongtoey Wattana, Bangkok 10110, 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, Nakhon Pathom 73170, Thailand
NOPPADOL INTARATAT
Affiliation:
Department of Anatomy, Faculty of Medicine, Srinakharinwirot University, Sukhumvit 23, Klongtoey Wattana, Bangkok 10110, Thailand
*
*Corresponding author: Institute of Molecular Biosciences, Mahidol University, 25/25 Phuttamonthon 4 Road, Salaya, Nakhon Pathom 73170, Thailand. E-mail: Panat1@yahoo.com, panat.anu@mahidol.ac.th
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Summary

At present, there are no medicinal plant extracts currently available for treatment and control of fasciolosis. The present work could provide, for the first study, conclusions on the in vitro fasciolicidal properties of the ethanol extract of Terminalia catappa L. (TcCE) leaves against adult Fasciola gigantica after incubation with RPMI-1640 medium containing the TcCE at various concentrations and times when compared with triclabendazole (TCZ). The relative motility and survival index values of the TcCE-treated flukes decreased at a more rapid rate than the TCZ-treated flukes. The death of the parasites was observed after exposed to TcCE at 3 h incubation with 400, 800 and 1000 µg mL−1, and at 6 h incubation in 100 and 200 µg mL−1. Vacuolization, blebbings and partial disruption on the parasites’ tegument were observed by light microscopy. When examined by scanning electron microscopy, TcCE caused similar tegumental alterations in the parasites as those observed in TCZ treatment but with larger damage at comparative incubation periods, consisting of swelling, blebbing, disrupted blebs, loss of spines, leading to the erosion, lesion and eventual disruption of the total tegument. Therefore, the TcCE may exert its fasciolicidal effect against F. gigantica by initially causing the tegumental alteration.

Keywords

FasciolosisFasciola giganticaTerminalia catappa L.anthelmintic activitymotilitysurvivaltegumentlight microscopyscanning electron microscopy
Type
Research Article
Information
Parasitology , Volume 144 , Issue 14 , December 2017 , pp. 1931 - 1942
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Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Akhtar, M. S. and Riffat, S. (1991). Field trial of Saussurea lappa roots against nematodes and Nigella sativa seeds against cestodes in children. Journal of the Pakistan Medical Association 41, 185–187.Google Scholar
Anuracpreeda, P., Wanichanon, C., Chaithirayanon, K., Preyavichyapugdee, N. and Sobhon, P. (2006). Distribution of 28·5 kDa antigen in tegument of adult Fasciola gigantica . Acta Tropica 100, 31–40.Google Scholar
Anuracpreeda, P., Wanichanon, C., Chawengkirtikul, R., Chaithirayanon, K. and Sobhon, P. (2009 a). Fasciola gigantica: immunodiagnosis of fasciolosis by detection of circulating 28·5 kDa tegumental antigen. Experimental Parasitology 123, 334–340.Google Scholar
Anuracpreeda, P., Wanichanon, C. and Sobhon, P. (2009 b). Fasciola gigantica: immunolocalization of 28·5 kDa antigen in the tegument of metacercaria and juvenile fluke. Experimental Parasitology 122, 75–83.Google Scholar
Anuracpreeda, P., Songkoomkrong, S., Sethadavit, M., Chotwiwatthanakun, C., Tinikul, Y. and Sobhon, P. (2011). Fasciola gigantica: production and characterization of a monoclonal antibody against recombinant cathepsin B3. Experimental Parasitology 127, 340–345.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, 1–9.Google 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, 18–28.Google Scholar
Anuracpreeda, P., Chawengkirttikul, R. and Sobhon, P. (2016 a). Immunodiagnosis of Fasciola gigantica infection using monoclonal antibody-based sandwich ELISA and immunochromatographic assay for detection of circulating cathepsin L1 protease. PLoS ONE 11, 1–22. e0145650.Google Scholar
Anuracpreeda, P., Chawengkirttikul, R. and Sobhon, P. (2016 b). Immunodiagnostic monoclonal antibody-based sandwich ELISA of fasciolosis by detection of Fasciola gigantica circulating fatty acid binding protein. Parasitology 143, 1369–1381.Google Scholar
Anuracpreeda, P., Chankaew, K., Puttarak, P., Koedrith, P., Chawengkirttikul, R., Panyarachun, B., Ngamniyom, A., Chanchai, S. and Sobhon, P. (2016 c). The anthelmintic effects of the ethanol extract of Terminalia catappa L. leaves against the ruminant gut parasite. Fischoederius cobboldi . Parasitology 143, 421–433.Google Scholar
Anuracpreeda, P., Tepsupornkul, K. and Chawengkirttikul, R. (2017 a). Immunodiagnosis of paramphistomosis using monoclonal antibody-based sandwich ELISA for detection of Paramphistomum gracile circulating 16 kDa antigen. Parasitology 144, 899–903.Google Scholar
Anuracpreeda, P., Watthanadirek, A., Chawengkirttikul, R. and Sobhon, P. (2017 b). Production and characterization of a monoclonal antibody against 16 kDa antigen of Paramphistomum gracile . Parasitology Research 116, 167–175.Google Scholar
Aswar, M., Aswar, U., Watkar, B., Vyas, M., Wagh, A. and Gujar, K. N. (2008). Anthelmintic activity of Ficus benghalensis. International Journal of Green Pharmacy 2, 170–172.CrossRefGoogle Scholar
Athanasiadou, S., Githiori, J. and Kyriazakis, I. (2007). Medicinal plants for helminth parasite control: facts and fiction. Animal 1, 1392–1400.Google Scholar
Bennett, C. E., Hughes, D. L. and Harness, E. (1980). Fasciola hepatica: changes in tegument during killing of adult flukes surgically transferred to sensitized rats. Parasite Immunology 2, 39–55.Google Scholar
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, 115–122.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, 1194–1201.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, 43–50.Google Scholar
Fairweather, I. (2005). Triclabendazole: new skills to unravel an old(ish) enigma. Journal of Helminthology 79, 227–234.Google Scholar
Fairweather, I. and Boray, J. C. (1999). Fasciolicides: efficacy, actions, resistance and its management. Veterinary Journal 158, 81–112.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, 169–177.Google Scholar
Gao, J., Dou, H., Tang, X. H., Xu, L. Z., Fan, Y. M. and Zhao, X. N. (2004). Inhibitory effect of TCCE on CCl4-induced overexpression of IL-6 in acute liver injury. Acta Biochimica et Biophysica Sinica (Shanghai) 36, 767–772.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, 176–181.CrossRefGoogle Scholar
Germosén-Robineau, L. (2014). Farmacopea Vegetal Carbeña. CICY editorial, Yucatán, Mexico, p. 360.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, 1097–1102.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, 228–237.Google Scholar
Keiser, J., Engels, D., Büscher, G. and Utzinger, J. (2005). Triclabendazole for the treatment of fascioliasis and paragonimiasis. Expert Opinion on Investigational Drugs 14, 1513–1526.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 & Pharmaceutical Bulletin 35, 2880–2886.Google Scholar
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, 38–40.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. American Journal of Chinese Medicine 25, 153–161.Google Scholar
Magalhaes, 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, 395–401.Google Scholar
Mas-Coma, S., Valero, M. A. and Bargues, M. D. (2009). Chapter 2. Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Advances in Parasitology 69, 41–146.Google Scholar
Mas-Coma, S., Bargues, M. D. and Valero, M. A. (2014 a). Diagnosis of human fascioliasis by stool and blood techniques: update for the present global scenario. Parasitology 141, 1918–1946.Google Scholar
Mas-Coma, S., Bargues, M. D. and Valero, M. A. (2014 b). Fascioliasis. In Helminth Infections and Their Impact on Global Public Health (ed. Bruschi, F.), pp. 93–122. Springer-Verlag, Wien, London.Google Scholar
McKinstry, B., Fairweather, I., Brennan, G. P. and Forbes, A. B. (2003). Fasciola hepatica: tegumental surface alterations following treatment in vivo and in vitro with nitroxynil (Trodax). Parasitology Research 91, 251–263.Google Scholar
McManus, D. P. and Dalton, J. P. (2006). Vaccines against the zoonotic trematodes Schistosoma japonicum, Fasciola hepatica and Fasciola gigantica . Parasitology 133(Suppl.), S43–S61.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, 315–325.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, 238–250.Google Scholar
Mehlhorn, H., Quraishy, S. A., Rasheid, K. A. S. A., Jatzlau, A. and Ghaffar, F. A. (2011). Addition of a combination of onion (Allium cepa) and coconut (Cocos nucifera) to food of sheep stops gastrointestinal helminthic infections. Parasitology Research 108, 1041–1046.Google Scholar
Moll, L., Gaasenbeek, C. P. H., Vellema, P. and Borgsteede, F. H. M. (2000). Resistance of Fasciola hepatica against triclabendazole in cattle and sheep in the Netherlands. Veterinary Parasitology 91, 153–158.CrossRefGoogle ScholarPubMed
Nagappa, A. N., Thakurdesai, P. A., Venkat Rao, N. and Singh, J. (2003). Antidiabetic activity of Terminalia catappa Linn fruits. Journal of Ethnopharmacology 88, 45–50.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, 98–101.Google Scholar
Overend, D. J. and Bowen, F. L. (1995). Resistance of Fasciola hepatica to triclabendazole. Australian of Veterinary Journal 72, 275.Google Scholar
Phalee, A. and Wongsawad, C. (2014). Prevalence of infection and molecular confirmation by using ITS-2 region of Fasciola gigantica found in domestic cattle from Chiang Mai province, Thailand. Asian Pacific Journal of Tropical Medicine 7, 207–211.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, 289–298.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, 161–167.Google Scholar
Srihakim, S. and Pholpark, M. (1991). Problem of fasciolosis in animal husbandry in Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 22, 352–355.Google Scholar
Sukhapesna, V., Tantasuvan, D., Sarataphan, N. and Imsup, K. (1994). Eco-nomic impact of fasciolosis in buffalo production. Thai Journal of Veterinary Medicine 45, 45–52.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 & Pharmaceutical Bulletin (Tokyo) 49, 486–487.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, 492–498.CrossRefGoogle 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, 1170–1174.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, 8–19.Google Scholar
Threadgold, L. T. and Brennan, G. P. (1978). Fasciola hepatica: basal infolds and associated vacuoles of the tegument. Experimental Parasitology 118, 228–237.Google Scholar
Torgerson, P. and Claxton, J. (1999). Epidemiology and control. In In Fasciolosis (ed. Dalton, J. P.). CABI Publishing, Oxon, pp. 113–149.Google Scholar
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 doi:10.1155/2012/595292.Google Scholar